Recent Developments for Remediating Acidic Mine...

18
Review Article Recent Developments for Remediating Acidic Mine Waters Using Sulfidogenic Bacteria Ivan Nancucheo, 1 José A. P. Bitencourt, 2 Prafulla K. Sahoo, 2 Joner Oliveira Alves, 3 José O. Siqueira, 2 and Guilherme Oliveira 2 1 Facultad de Ingenier´ ıa y Tecnolog´ ıa, Universidad San Sebasti´ an, Lientur 1457, 4080871 Concepci´ on, Chile 2 Instituto Tecnol´ ogico Vale, Rua Boaventura da Silva 955, 66055-090 Bel´ em, PA, Brazil 3 SENAI Innovation Institute for Mineral Technologies, Av. Com. Br´ as de Aguiar 548, 66035-405 Bel´ em, PA, Brazil Correspondence should be addressed to Ivan Nancucheo; [email protected] and Guilherme Oliveira; [email protected] Received 27 March 2017; Revised 31 July 2017; Accepted 23 August 2017; Published 3 October 2017 Academic Editor: Raluca M. Hlihor Copyright © 2017 Ivan Nancucheo et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Acidic mine drainage (AMD) is regarded as a pollutant and considered as potential source of valuable metals. With diminishing metal resources and ever-increasing demand on industry, recovering AMD metals is a sustainable initiative, despite facing major challenges. AMD refers to effluents draining from abandoned mines and mine wastes usually highly acidic that contain a variety of dissolved metals (Fe, Mn, Cu, Ni, and Zn) in much greater concentration than what is found in natural water bodies. ere are numerous remediation treatments including chemical (lime treatment) or biological methods (aerobic wetlands and compost bioreactors) used for metal precipitation and removal from AMD. However, controlled biomineralization and selective recovering of metals using sulfidogenic bacteria are advantageous, reducing costs and environmental risks of sludge disposal. e increased understanding of the microbiology of acid-tolerant sulfidogenic bacteria will lead to the development of novel approaches to AMD treatment. We present and discuss several important recent approaches using low sulfidogenic bioreactors to both remediate and selectively recover metal sulfides from AMD. is work also highlights the efficiency and drawbacks of these types of treatments for metal recovery and points to future research for enhancing the use of novel acidophilic and acid-tolerant sulfidogenic microorganisms in AMD treatment. 1. Introduction Metal mining provides everyday goods and services essential to society. However, this activity has at times caused extensive and sometimes severe pollution of air, vegetation, and water bodies [1]. Streams draining active or abandoned mines and mine spoils are widely considered as hazardous to human health and the environment, but on the other hand, they may also be alternative potential sources of valuable metals [2, 3]. Currently, millions of tons of ores are processed every year by the mining industry and are disposed in the form of waste rocks and mine tailings. As higher-grade ores are diminishing, the primary ores that are processed by mining companies are of increasingly lower grade (metal content) and the growing amount of waste material produced by mining operations is consequently significant. e use of lower grade ore was made possible by the development of the flotation technique in the late 19th century, which allowed the separation of metal sulfide minerals from gangue minerals that have no commercial value [4]. As a result of selective flotation, about 95 to 99% of the ground primary ores end up as fine-grain tailings, in the case of copper ores. e composition of tailings is directly dependent on that of the ore, and therefore they are highly variable, though pyrite (FeS 2 ) is frequently the most reactive and dominant sulfide mineral present in tailings wastes [4–6]. Pyritic mine tailings therefore have the potential to become extremely acidic when in contact with surface water. Under oxidizing conditions, pyrite-bearing wastes produce sulfuric acid. e acidic water further dissolves other metals contained in mine waste, resulting in low pH water enriched with soluble sulfate, Fe, Al, and other transition metals, known as acid mine drainage (AMD) (Figure 1) [7, 8]. Hindawi BioMed Research International Volume 2017, Article ID 7256582, 17 pages https://doi.org/10.1155/2017/7256582

Transcript of Recent Developments for Remediating Acidic Mine...

Review ArticleRecent Developments for Remediating Acidic Mine WatersUsing Sulfidogenic Bacteria

Ivan Nancucheo1 Joseacute A P Bitencourt2 Prafulla K Sahoo2 Joner Oliveira Alves3

Joseacute O Siqueira2 and Guilherme Oliveira2

1Facultad de Ingenierıa y Tecnologıa Universidad San Sebastian Lientur 1457 4080871 Concepcion Chile2Instituto Tecnologico Vale Rua Boaventura da Silva 955 66055-090 Belem PA Brazil3SENAI Innovation Institute for Mineral Technologies Av Com Bras de Aguiar 548 66035-405 Belem PA Brazil

Correspondence should be addressed to Ivan Nancucheo inancucheogmailcomand Guilherme Oliveira guilhermeoliveiraitvorg

Received 27 March 2017 Revised 31 July 2017 Accepted 23 August 2017 Published 3 October 2017

Academic Editor Raluca M Hlihor

Copyright copy 2017 Ivan Nancucheo et alThis is an open access article distributed under theCreativeCommonsAttribution Licensewhich permits unrestricted use distribution and reproduction in any medium provided the original work is properly cited

Acidic mine drainage (AMD) is regarded as a pollutant and considered as potential source of valuable metals With diminishingmetal resources and ever-increasing demand on industry recovering AMD metals is a sustainable initiative despite facing majorchallenges AMD refers to effluents draining from abandoned mines and mine wastes usually highly acidic that contain a varietyof dissolved metals (Fe Mn Cu Ni and Zn) in much greater concentration than what is found in natural water bodies Thereare numerous remediation treatments including chemical (lime treatment) or biological methods (aerobic wetlands and compostbioreactors) used for metal precipitation and removal from AMD However controlled biomineralization and selective recoveringof metals using sulfidogenic bacteria are advantageous reducing costs and environmental risks of sludge disposal The increasedunderstanding of the microbiology of acid-tolerant sulfidogenic bacteria will lead to the development of novel approaches to AMDtreatment We present and discuss several important recent approaches using low sulfidogenic bioreactors to both remediateand selectively recover metal sulfides from AMD This work also highlights the efficiency and drawbacks of these types oftreatments formetal recovery and points to future research for enhancing the use of novel acidophilic and acid-tolerant sulfidogenicmicroorganisms in AMD treatment

1 Introduction

Metal mining provides everyday goods and services essentialto society However this activity has at times caused extensiveand sometimes severe pollution of air vegetation and waterbodies [1] Streams draining active or abandoned mines andmine spoils are widely considered as hazardous to humanhealth and the environment but on the other hand they mayalso be alternative potential sources of valuable metals [2 3]

Currently millions of tons of ores are processed everyyear by the mining industry and are disposed in the formof waste rocks and mine tailings As higher-grade ores arediminishing the primary ores that are processed by miningcompanies are of increasingly lower grade (metal content)and the growing amount of waste material produced bymining operations is consequently significant The use oflower grade ore was made possible by the development of the

flotation technique in the late 19th century which allowed theseparation of metal sulfide minerals from gangue mineralsthat have no commercial value [4] As a result of selectiveflotation about 95 to 99 of the ground primary ores endup as fine-grain tailings in the case of copper ores Thecomposition of tailings is directly dependent on that of theore and therefore they are highly variable though pyrite(FeS2) is frequently the most reactive and dominant sulfide

mineral present in tailings wastes [4ndash6]Pyritic mine tailings therefore have the potential to

become extremely acidic when in contact with surface waterUnder oxidizing conditions pyrite-bearing wastes producesulfuric acid The acidic water further dissolves other metalscontained in mine waste resulting in low pH water enrichedwith soluble sulfate Fe Al and other transition metalsknown as acid mine drainage (AMD) (Figure 1) [7 8]

HindawiBioMed Research InternationalVolume 2017 Article ID 7256582 17 pageshttpsdoiorg10115520177256582

2 BioMed Research International

(a) (b)

(c) (d)

(e) (f)

Figure 1 Illustration of streams of acidicwaters draining fromactive or abandonedmines andmine spoils (a)AMD froma coppermine in theState of Para Brazil that has been remediated with limestone treatment (b) acidic water released from abandoned undergroundmetalliferousmine in the Republic of South Africa (reproduced fromAkcil and Koldas [9]) (c) acidic mine water draining from an abandoned sulfurminenorthern Chile (d) AMD discharge in the Lomero-Poyatos mine Spain (reproduced from Espana et al [10]) (e) acidic water draining fromCoal mines Jaintia Hills and (f) AMD originated from mine tailings Canada (reproduced from Burtnyski [11])

BioMed Research International 3

2 Remediation of Acidic Mine Water

Waters draining from abandoned metal mines and minewastes are often acidic (pH lt 4) and contain elevated concen-trations of dissolved metals and metalloids and high osmoticpotential associated with concentration of sulfate salts [14] Inmost cases active chemical treatment and passive biologicaltreatment can provide effective remediation of AMD [15](details and literature of the advantages and disadvantagesof these treatment and others are presented in Table 1) Amajor drawback to both approaches is that the immobilizedmetals are contained in ldquosludgerdquo (chemical treatment) orwithin spent compost (biological treatment) and need to bedisposed in specially designated landfill sites precluding theirrecovery and recycling Changes in redox conditions duringstorage can lead to remobilization of metals (and metalloidssuch as arsenic) in both sludge and spent composts Inaddition potentially useful and valuable metal resources arenot recovered using conventional approaches for remediatingmine waters [3 16]

A radically different approach for remediating AMDwhich like compost bioreactors derives from the abilities ofsome microorganisms to generate alkalinity and to immo-bilize metals is referred to generally as ldquoactive biologicaltreatmentrdquoMicrobiological processes that generate alkalinityare mostly reductive processes and include denitrificationmethanogenesis and dissimilatory reduction of sulfate ferriciron and manganese (IV) which tend to be limited inAMD Considering that AMD usually contains elevatedconcentrations of both ferric iron and sulfate the ability ofsome bacteria to use these compounds as terminal electronacceptors suggests that these reactions can be highly usefulfor mine water remediation Acidic environments in whichsulfur or sulfide minerals are subjected to biologically-accelerated oxidative dissolution characteristically containlarge concentrations of soluble sulfate [17] Therefore micro-bial sulfate reduction might be anticipated to occur withinanaerobic zones in both acidic and nonacidic environmentsBiological sulfidogenesis generates hydrogen sulfide as aresult of a reductive metabolic process using sulfate reducingbacteria (SRB) Biological sulfidogenesis has the additionalbenefits of being a proton-consuming reaction allowing theincrease in pHof theminewater treated contributing towardsmitigation and remediation The hydrogen sulfide generatedcan be used in controlled situations to selectively precipitatemany potentially toxic metals (such as copper and zinc) oftenpresent in AMD at elevated concentrations [3 18] Activebiological treatment has many advantages over alternativestrategies for treatingmine waters one of the most importantbeing its potential for recovering metals that are commonlypresent in AMD

There have been few successful applications of SRB-mediated active AMD treatment systems even though thispossibility has long been appreciated One major reason forthis is that SRB happens preferentially between pH 6 and8 [19] whereas AMD generally has a pH between 2 and 4and commonly pH lt 3 [20] Under these circumstances aneutralization step is necessary beforeAMDeffluents are sub-jected to bacterial sulfate reduction or alternatively ldquooff-linerdquo

systems need to be used The latter is necessary by the factthat current systems use neutrophilic SRB or sulfur reducingbacteria and direct exposure to the inflowing acidic solutionbeing treated would be lethal to these microorganismsTherefore a separate vessel in which sulfide generated bythe bacteria is contacted with the acidic metal-laden wastewater is required [16 21] Examples of this technology arethe Biosulfide and Thiopaq processes (Figure 2) operatedunder the auspices of two biotechnology companies BioTeq(Canada) and Paques B V (The Netherlands) which arecurrently in operation in various parts of the world

The Biosulfide process has two stages one chemicaland the other biological Metals are removed from AMDin the chemical stage by precipitation with biogenic sulfideproduced in the biological stage by SRB under anaerobiccondition In this system hydrogen sulfide is generated bythe reduction of elemental sulfur or other sulfur source inthe presence of an electron donor such as acetic acid Thegas is passed to an anaerobic agitated contactor in whichcopper can be precipitated as a sulfide usually without pHadjustment and without significant precipitation of otherheavy metals present in the water The end result is a highvalue copper product usually containing more than 50 ofthe metal Other metals such as nickel zinc and cobalt canalso be recovered as separate high-grade sulfide productsalthough pH control using an alkali source is usually requiredto selectively precipitate the metal as a sulfide phase Thehigh-grade metal sulfide precipitate is then recovered byconventional clarification and filtration to produce a filtercake which can be shipped to a smelter [12]

TheThiopaqprocess uses another system that involves theuse of two biological continuous reactors connected in series(I) to an anaerobic upflow sludge blanket (UASB) reactorfor the reduction of oxidized sulfur species In this reactorethanol or hydrogen is utilized by the SRB as electron donorproducing sulfide (mostly HSminus) for the precipitation of metalsulfides (which can proceed in the same reactor depending onthe toxicity of the wastewater) and (II) an aerobic submergedfixed film (SFF) reactor where the excess sulfide is oxidizedto elemental sulfur using sulfide-oxidizing bacteria In thisprocess metals such as Zn and Cd can be precipitated downto very low concentrations [22]

The Paques B V process has been successfully imple-mented at an industrial scale at the gold mine Pueblo Viejolocated in the Dominican Republic A copper recovery plantinstalled in 2014 based on sulfide precipitation is used torecover the copper liberated from the gold extraction processThe sulfidogenic bioreactor generates H

2S to recover up to

12000 ton of copper per year generating value and reducingthe amount of copper sent to the tailing dam [23] Applicationof this process has also been demonstrated on a pilot-scaleat the Kennecott Bingham Canyon copper mine in Utahwhere gt99 of copper present in a pH 26 waste stream wasrecovered [22 24 25]

Sulfate reduction activity has been reported in low pHecosystems for example in acidic lakes wetlands and acidmine drainage [19 26 27] However few acidophilictolerantSRB have been cultured [16 26 28ndash30] A major potentialadvantage of using acidophilic sulfidogens would be to allow

4 BioMed Research International

Table1Summaryof

thevario

ustypeso

ftreatmentfor

AMD

(com

piledfro

mSaho

oet

al[15]Gazea

etal[36]Trum

m[37]T

aylore

tal[38]R

oyCh

owdh

uryet

al[39]John

sonand

Hallberg[22]Skousen

[40]Skousen

etal[41]andSeervietal[42])

Syste

mtype

Applicability

Supp

ortm

aterials

Mechanism

sLimitatio

nBiologica

l

Aerobicw

etland

(AeW

)Mod

eratea

ciditynetalkalin

emined

rainage

Organicmattersoillim

estone

gravel

Oxidatio

nhydrolysis

precipitatio

nRe

quire

dlonger

detentiontim

eandhu

gesurfa

cearea

Anaerob

icwetland

(AnW

)Net-acidicw

ater

with

high

AlFe

andDO

Organicmattersuch

ascompo

stsawdu

sthayandlim

estone

gravel

Sulfateredu

ction

metal

precipitateas

sulfidesmicrobial

generatedalkalin

ityRe

quire

dlong

resid

ence

time

Verticalflo

wwetland

(VFW

)Net-acidicw

ater

with

high

AlFe

andDO

Limestoneorganicmatter

SulfateandFe

redu

ction

acid

neutralization

Highcapitalcostpo

tentialfor

armoringandplug

ging

with

hydroxides

Sulfateredu

cing

bioreactor

(SRB

)Sm

allfl

owso

rtosituatio

nsvery

acidicandmetalric

hwater

Organicsubstrates

uchas

hay

alfalfasaw

dust

paper

woo

dchipscrushed

limestone

andcompo

stor

manure

Microbialsulfateredu

ction

Highcapitalcostextre

mely

low

pHseverelyim

pactthee

fficiency

ofSredu

cing

bacteria

Pyrolusitelim

estone

beds

Mod

eratep

Handwhere

majority

ofacidity

isrelated

toMn

Limestoneorganicsubstrate

aerobicm

icroorganism

Hydrolysis

ofMn

Not

suitablefor

drainage

which

contains

high

Fehigh

maintenance

Perm

eabler

eactiveb

arrie

rs(PRB

)Groun

dwaterlow

DO

Organicmatterlim

estonezero

valent

iron

Sulfateredu

ction

sulfide

precipitates

neutralization

Iron

-oxidizing

bioreactor

Acidicwater

Fe-oxidizing

bacteriaand

archaea

Feoxidation

Phytorem

ediatio

nAny

AMD-im

pacted

sites

Metaltolerant

plantspecies

Phytoextractionand

phytostabilization

Successd

epends

onthep

roper

selectionof

the

metal-hyperaccumulator

plant

BioMed Research International 5

Table1Con

tinued

Syste

mtype

Applicability

Supp

ortm

aterials

Mechanism

sLimitatio

nGeochem

ical

Ano

xiclim

estone

drain(A

LD)

Acidicwater

with

lowAlFeD

OLimestone

gravel

compacted

soil

Limestone

dissolution

raise

pH

precipitatio

n

Fe-oxide

armoringlim

estone

limitperm

eabilityandcause

plug

ging

Alkalinity

prod

ucingsyste

m(A

PS)

Acidicwater

Organicmatterlim

estone

Ano

xicc

onditio

nneutralization

precipitatio

n

Openlim

estone

channel(OLC

)Re

quire

dste

epslo

pesnet-a

cidic

water

with

high

AlFe

andDO

Limestone

Limestone

dissolution

neutralization

Arm

oringor

thec

oatin

gof

the

limestonelarge

amou

ntis

neededdecreases

the

neutralizingcapacity

Limestone

leachbed(LLB

)Lo

wpH

andmetal-fr

eewater

Limestone

Limestone

dissolution

neutralization

Arm

oringwith

Fehydroxides

Steel-slagleachbed(SLB

)Highlyacidicandmetal-fr

eewater

Steelslag

Raise

alkalin

ityneutralization

Not

suitablefor

metal-la

den

water

Limestone

diversionwe

lls(LDW)

Sitesthato

ffera

suitable

topo

graphicalfall

Crushedlim

estone

aggregate

Hydraulicforcehydrolysis

and

neutralization

Requ

iredrefillin

gwith

limestone

every2ndash4weeks

Limestone

sand

Stream

flowwater

Sand

-sized

limestone

neutralizingacid

Coatin

gof

limestone

Low-pHFe

oxidationchannels

Shallowchannels

Limestone

orsand

stone

aggregate

Feoxidation

adsorptio

nand

coprecipitatio

n

Itremoves

someF

ebu

trem

oval

efficiency

hasn

otbeen

determ

ined

Sulfide

passivationmicroencapsulation

Pitw

allfacessulfid

ebearin

gwastesrocks

piles

Inorganicc

oatin

gph

osph

ate

silicafly

ashlim

estoneorganic

coatinghu

micacidlipids

polyethylene

polyam

ine

alkoxysilanesfattyacidoxalic

acidcatecho

l

Preventsulfid

eoxidatio

nby

inorganica

ndorganicc

oatin

g

Long

-term

effectiv

enessisstillin

questio

norganicc

oatin

gexpensive

Electro

chem

icalcover

Tailing

wasterock

Con

ductives

teelmeshcathod

emetalanod

eRe

ducing

DOby

electrochem

ical

process

Highcapitalcosto

fano

desno

inform

ationavailableo

nlarge

scalea

pplication

6 BioMed Research International

Table1Con

tinued

Syste

mtype

Applicability

Supp

ortm

aterials

Mechanism

sLimitatio

nPh

ysica

l

Dry

cover

Sulfide

bearingwastesrockpiles

Fine-grained

soilorganic

materials

synthetic

material

(plasticliners)vegetation

Minim

izeo

xidatio

nby

physical

barrierneutralization

precipitates

Shortterm

effectiv

eness

Wetcover

Sulfide

wastes

Und

erwater

Disp

osingwasteun

derw

ater

anoxiccond

ition

sRe

quire

rigorou

seng

ineerin

gdesig

nhigh

maintenance

Gas

redo

xanddisplacement

syste

m(G

aRDS)

Und

ergrou

ndmines

CO2andCH4gas

Gas

mixturesp

hysic

allydisplace

O2

Itson

lyfeasiblewhere

partialor

completefl

ooding

isno

tfeasib

le

BioMed Research International 7

MetalSuldes(ZnS)

Air

Excess

Sulfur

Puriedeuent

Recycle

Neu

troph

ilic

SRB

Bior

eact

or o

ne

Bior

eact

or tw

oSu

lde

oxid

ising

bac

teriaWaste water or

process water(34

2minus and metalssuch as H

2+)

(2-rich gas

2

(3minus

(3I)

34

2minus+ 4(2 + (

+rarr (3

minus+ 4(2

H2+

+ (3minusrarr H3 + (

+

2(3minus+ 2 + 2(

+rarr 23

I+ 2(2

(a)

Bior

eact

orsta

ge I

Stag

e II

Ana

erob

ic ag

itate

dco

ntac

tor

SulfurReagents

Feed water(AMD)

sulfu

r red

ucin

g ba

cter

ia

ClarierTreated water

Filter

Metal sulde (ZnS)to smelter

(23

Gen

erat

ion

by

(23

(b)

Figure 2 Schematic overview of the Thiopaq (a) and Biosulfide (b) processes (adapted from Adams et al [12] Muyzer and Stams [13])

simpler engineering designs and reduce operational costs byusing single on-line reactor vessels that could be used to bothgenerate sulfide and selectively precipitate target metal(s)Precipitation and removal of many soluble transition metalsoften present in AMD emanating from metal mines maybe achieved by ready biomineralization as their sulfides Theproduced metal sulfides have different solubilities thereforemetals can be precipitated together or selectively by con-trolling concentrations of the key reactant S2minus which maybe achieved by controlling pH (S2minus + H+ harr HSminus) Coppersulfide for example is far less soluble than ferrous sulfide(respective log Ksp values of minus359 and minus188) and thereforeCuS precipitates at pH 2 whereas FeS needs much higher pHto precipitate Diez-Ercilla et al [31] have also demonstratedthat selective precipitation of metal sulfides occurs naturallyin Cueva de la Mora pit lake (SW Spain) and the geochemicalcalculations match perfectly with the results of chemicaland mineralogical composition Nancucheo and Johnson[3] showed that it was possible to selectively precipitate

stable metal sulfides in inline reactor vessel testing twosynthetic AMDs in acidic conditions (pH 22ndash48) In the firstbioreactor with a composition of feeding similar to AMD atthe abandoned Cwm Rheidol lead-zinc mine in mid-Waleszinc was efficiently precipitated (gt99) as sulfide inside thereactor while both aluminum and ferrous iron remain insolution (gt99) and were washed out of the reactor vesselThe second sulfidogenic bioreactor was challenged with asynthetic AMD based on that from Mynydd Parys NorthWales Throughout the test period all the copper presentin the feed liquor was precipitated (confirmed as coppersulfide) within the bioreactor but none of the ferrous ironwas present in the solids Although the initial pH at whichthe bioreactor was operated (from pH 36 to 25) causedsome coprecipitation of zinc with the copper by progressivelylowering the bioreactor pH and the concentration of theelectron donor in the influent liquor it was possible toprecipitate gt99 of the copper within the bioreactor as CuSand to maintain gt99 of the zinc iron and aluminum in

8 BioMed Research International

solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]

4C3H8O3+ 10H+ + 7SO

4

2minus+ Cu2+ + Zn2+ + Fe2+

997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H

2O

(1)

This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD

Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H

2S) by the SRB and orpiment

(As2S3) generated within the bioreactor In addition this

process was also observed to occur naturally in an acidic pitlake [31]

Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for

the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes

3 Microbiology in Remediating AcidicMine Waters

Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]

Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents

BioMed Research International 9

Table2Isolated

sulfido

genicm

icroorganism

sand

theirm

aincharacteris

tics

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermocladium

modestiu

s45ndash82

(75)

26ndash

59(40)

Glycogen

starch

proteins

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

mud

)Japan

[43ndash45]

Caldivirg

amaquilin

gensis

70ndash9

023ndash64(37ndash4

2)

Glycogen

beefextract

pepton

etryptoneyeast

extract

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

solfataric

soilmud

)Mt

Maquilin

gPh

ilipp

ines

[46]

Archaeoglobu

slithotro

phicu

snd

60

Acetate

SulfateL-cysteine

nd[4748]

Archaeoglobu

sveneficus

nd69

H2acetateformate

pyruvateyeastextract

citratelactatesta

rch

pepton

e

Sulfitethiosulfate

Wallsof

activ

eblack

smoker

atmiddle

AtlanticRidge

[44]

Archaeoglobu

sprofund

usnd

45ndash75

H2acetatepyruvate

yeastextractlactate

meatextractpeptone

crud

eoilwith

acetate

Sulfatethiosulfate

sulfite

Deepseah

ydrothermal

syste

moff

Guaym

as

Mexico

[4950]

Archaeoglobu

sfulgidu

s60ndash75

(70)

55ndash75

(60)

H2C

O2formate

form

amideD(minus)-and

L(+)-lactateglucose

starchcalam

inea

cids

pepton

egelatincasein

meatextractyeast

extract

Sulfatethiosulfate

sulfite

Marineh

ydrothermal

syste

mN

eron

eIta

ly[4951]

Thermodesulfatatorind

icus

55ndash80

(70)

60ndash

67(625)

H2C

O2stim

ulated

bymethano

lmon

omethylamine

glutam

atepepton

efumaratetryptone

isobu

tyrate3-C

H3

butyrateethanol

prop

anolandlow

amou

ntso

facetate

Sulfate

Marineh

ydrothermal

syste

mC

entralIndian

Ridge

[52]

Thermodesulfobacterium

hydrogeniphilum

50ndash80

(75)

63ndash68(65)

H2C

O2stim

ulated

byacetatefumarate

3-methylbutyrate

glutam

ateyeastextract

pepton

eortrypton

e

Sulfate

Marineh

ydrothermal

syste

mG

uaym

asBa

sin[53]

10 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermodesulfobacterium

commun

e41ndash83

60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA[5455]

Thermodesulfobacterium

thermophilum

nd60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

nd[55]

Thermodesulfobacterium

hveragerdense

7545ndash70

(70)

H2pyruvatelactate

Sulfatesulfite

Hot

sprin

gs(m

icrobial

mats)Iceland

[56]

Thermodesulfobium

narugense

6940ndash

60(55ndash6

0)

H2C

O2

Sulfaten

itrate

thiosulfate

Hot

sprin

gs(m

icrobial

mats)Japan

[57]

Desulfotomaculum

spp(30

species)

nd23ndash55

H2C

O2formatesome

(organicacidslip

idsor

mon

oaromatic

hydrocarbo

ns)

Sulfidesulfur

thiosulfateA

cetate

some(Fe

(III)Mn(IV)

U(V

I)or

Cr(V

I))

Subsurface

environm

ents

rice

fieldsminesoilspills

[58ndash62]

Desulfosporosinus

meridiei

10ndash37

61ndash75

H2C

O2acetatesom

e(la

ctatepyruvate

ethano

l)Sulfatesom

e(nitrate)

Groun

dwater

contam

inated

with

polycyclica

romatic

hydrocarbo

nsinSw

anCoastalPlain

Australia

[63]

Desulfosporosinus

youn

gii

8ndash39

(32ndash35)

57ndash82(70ndash

73)

Beefextractyeast

extractform

ate

succinatelactate

pyruvateethanoland

toluene

Fumaratesulfatesulfite

thiosulfate

Artificialwetland

(sedim

ent)

[64]

BioMed Research International 11

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfosporosinus

orien

tis37ndash4

860ndash

65

H2C

O2formate

lactatepyruvatem

alate

fumaratesuccinate

methano

lethano

lprop

anolbutanol

butyratevalerate

palm

itate

Sulfatesulfite

thiosulfatesulfur

nd[65]

Desulfosporom

usapolytro

pa4ndash

3761ndash80

H2C

O2formate

lactatebu

tyrateseveral

alcoho

lsorganica

cids

carboh

ydratessome

aminoacidscholine

betaine

SulfateFe(OH) 3

Oligotroph

iclake

(sedim

ent)

German

[66]

Thermodesulfovibrio

yellowstonii

41ndash83

60ndash

80(70)

H2C

O2acetate

form

atelactate

pyruvate

Sulfatethiosulfate

sulfite

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA

[67]

Thermodesulfovibrio

islandicus

5545ndash70

(70)

H2pyruvatelactate

form

ate

Sulfaten

itrate

Bioreactor

inoculated

with

hotsprings

(microbialmats)sample

Iceland

[56]

Desulfohalobium

spp(6

species)

nd55ndash80(65ndash70)

H2lactateethanol

acetate

Sulfite

hypersaline

environm

ents

[6869]

Desulfocaldus

terraneus

58nd

H2C

O2aminoacids

proteinaceou

ssub

strates

andorganica

cids

prod

ucingethano

lacetateprop

ionate

isovalerate2-

methylbutyrate

Cystinesulfu

rsulfate

Seao

ilfacilitiesAlaksa

[70]

12 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfomicrobium

spp(4

species)

25ndash30

ndH2lactatepyruvate

Ethano

lform

ate

Sulfatesulfoxyanions

Anaerob

icsediments

(Freshwaterbrackish

marine)anaerob

icstrata

oroverlyingwaterand

insaturatedmineralor

organicd

eposits

[5469]

Desulfonatro

novibrio

hydrogenovoran

s37ndash4

090

ndash102(90ndash97)

H2formate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[71]

Desulfonatro

num

spp(3

species)

20ndash4

5(37ndash45)

80ndash

100(90)

H2form

ateYeast

extractethano

llactate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[72]

Desulfovibriospp(47

species)

25ndash4

4(25ndash35)

ndH2C

O2acetatelactate

carboh

ydrates

Sulfaten

itrate

nd[73]

Desulfomonile

spp(2

species)

30ndash30

(37)

65ndash78

(68ndash70)

H2C

O2benzoate

pyruvateorganic

carbon

halogens

Sulfatesulfite

thiosulfatesulfurFe

(III)NitrateU(V

I)Slud

ge[74]

Syntroph

obacteraceae

(8genera)

31ndash6

070

ndash75

H2C

O2acetate

form

atelactate

pyruvate

Sulfatesulfite

thiosulfate

Sewages

ludge

freshwaterbrackish

marines

edim

ent

marineh

ydrothermal

ventsho

tspring

sediments

[7375]

Desulfobacterium

anilini

3069ndash

75H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

BioMed Research International 13

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfarculus

baarsii

35ndash39

73H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

Desulfobacteraceae(12

genera)

10ndash4

0nd

H2C

O2L

ong-chain

fatty

acidsAlcoh

ols

Polara

romatic

compo

undsand

insome

casese

venAlip

hatic

arom

atichydrocarbo

ns

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[77]

Desulfosporosinus

acidophilus

25ndash4

036ndash

52(52)

H2lactatepyruvate

glycerolglucose

and

fructose

Sulfate

Sedimentfrom

anacid

effluent

pond

[26]

Desulfosporosinus

acididuran

s15ndash4

038ndash70

(55)

H2formatelactate

butyratefum

arate

malatepyruvate

glycerolm

ethano

lethano

lyeastextract

xyloseglucosefructose

Ferriciro

nnitrate

sulfateelem

entalsulfur

thiosulfate

Whiteriv

erdraining

from

theS

oufriere

hills

inMon

serrat(pH32)

[78]

a Valuesc

losedby

parenthesis

arec

onsid

ered

optim

alpH

ndno

tinformed

byconsultedreference

14 BioMed Research International

such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO

2[33]

In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO

2and H

2[17]

D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]

4 Natural Attenuation for the Design of AMDRemediation Strategies

Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and

chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH

2O)were detected presumably due

to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not

Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]

5 Concluding Remarks

Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools

Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico

BioMed Research International 15

(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)

References

[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013

[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014

[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012

[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008

[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011

[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003

[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000

[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014

[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006

[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005

[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007

[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008

[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008

[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015

[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013

[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006

[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006

[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014

[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008

[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006

[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010

[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005

[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016

[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999

[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001

[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010

[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990

[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016

[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014

[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009

[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

2 BioMed Research International

(a) (b)

(c) (d)

(e) (f)

Figure 1 Illustration of streams of acidicwaters draining fromactive or abandonedmines andmine spoils (a)AMD froma coppermine in theState of Para Brazil that has been remediated with limestone treatment (b) acidic water released from abandoned undergroundmetalliferousmine in the Republic of South Africa (reproduced fromAkcil and Koldas [9]) (c) acidic mine water draining from an abandoned sulfurminenorthern Chile (d) AMD discharge in the Lomero-Poyatos mine Spain (reproduced from Espana et al [10]) (e) acidic water draining fromCoal mines Jaintia Hills and (f) AMD originated from mine tailings Canada (reproduced from Burtnyski [11])

BioMed Research International 3

2 Remediation of Acidic Mine Water

Waters draining from abandoned metal mines and minewastes are often acidic (pH lt 4) and contain elevated concen-trations of dissolved metals and metalloids and high osmoticpotential associated with concentration of sulfate salts [14] Inmost cases active chemical treatment and passive biologicaltreatment can provide effective remediation of AMD [15](details and literature of the advantages and disadvantagesof these treatment and others are presented in Table 1) Amajor drawback to both approaches is that the immobilizedmetals are contained in ldquosludgerdquo (chemical treatment) orwithin spent compost (biological treatment) and need to bedisposed in specially designated landfill sites precluding theirrecovery and recycling Changes in redox conditions duringstorage can lead to remobilization of metals (and metalloidssuch as arsenic) in both sludge and spent composts Inaddition potentially useful and valuable metal resources arenot recovered using conventional approaches for remediatingmine waters [3 16]

A radically different approach for remediating AMDwhich like compost bioreactors derives from the abilities ofsome microorganisms to generate alkalinity and to immo-bilize metals is referred to generally as ldquoactive biologicaltreatmentrdquoMicrobiological processes that generate alkalinityare mostly reductive processes and include denitrificationmethanogenesis and dissimilatory reduction of sulfate ferriciron and manganese (IV) which tend to be limited inAMD Considering that AMD usually contains elevatedconcentrations of both ferric iron and sulfate the ability ofsome bacteria to use these compounds as terminal electronacceptors suggests that these reactions can be highly usefulfor mine water remediation Acidic environments in whichsulfur or sulfide minerals are subjected to biologically-accelerated oxidative dissolution characteristically containlarge concentrations of soluble sulfate [17] Therefore micro-bial sulfate reduction might be anticipated to occur withinanaerobic zones in both acidic and nonacidic environmentsBiological sulfidogenesis generates hydrogen sulfide as aresult of a reductive metabolic process using sulfate reducingbacteria (SRB) Biological sulfidogenesis has the additionalbenefits of being a proton-consuming reaction allowing theincrease in pHof theminewater treated contributing towardsmitigation and remediation The hydrogen sulfide generatedcan be used in controlled situations to selectively precipitatemany potentially toxic metals (such as copper and zinc) oftenpresent in AMD at elevated concentrations [3 18] Activebiological treatment has many advantages over alternativestrategies for treatingmine waters one of the most importantbeing its potential for recovering metals that are commonlypresent in AMD

There have been few successful applications of SRB-mediated active AMD treatment systems even though thispossibility has long been appreciated One major reason forthis is that SRB happens preferentially between pH 6 and8 [19] whereas AMD generally has a pH between 2 and 4and commonly pH lt 3 [20] Under these circumstances aneutralization step is necessary beforeAMDeffluents are sub-jected to bacterial sulfate reduction or alternatively ldquooff-linerdquo

systems need to be used The latter is necessary by the factthat current systems use neutrophilic SRB or sulfur reducingbacteria and direct exposure to the inflowing acidic solutionbeing treated would be lethal to these microorganismsTherefore a separate vessel in which sulfide generated bythe bacteria is contacted with the acidic metal-laden wastewater is required [16 21] Examples of this technology arethe Biosulfide and Thiopaq processes (Figure 2) operatedunder the auspices of two biotechnology companies BioTeq(Canada) and Paques B V (The Netherlands) which arecurrently in operation in various parts of the world

The Biosulfide process has two stages one chemicaland the other biological Metals are removed from AMDin the chemical stage by precipitation with biogenic sulfideproduced in the biological stage by SRB under anaerobiccondition In this system hydrogen sulfide is generated bythe reduction of elemental sulfur or other sulfur source inthe presence of an electron donor such as acetic acid Thegas is passed to an anaerobic agitated contactor in whichcopper can be precipitated as a sulfide usually without pHadjustment and without significant precipitation of otherheavy metals present in the water The end result is a highvalue copper product usually containing more than 50 ofthe metal Other metals such as nickel zinc and cobalt canalso be recovered as separate high-grade sulfide productsalthough pH control using an alkali source is usually requiredto selectively precipitate the metal as a sulfide phase Thehigh-grade metal sulfide precipitate is then recovered byconventional clarification and filtration to produce a filtercake which can be shipped to a smelter [12]

TheThiopaqprocess uses another system that involves theuse of two biological continuous reactors connected in series(I) to an anaerobic upflow sludge blanket (UASB) reactorfor the reduction of oxidized sulfur species In this reactorethanol or hydrogen is utilized by the SRB as electron donorproducing sulfide (mostly HSminus) for the precipitation of metalsulfides (which can proceed in the same reactor depending onthe toxicity of the wastewater) and (II) an aerobic submergedfixed film (SFF) reactor where the excess sulfide is oxidizedto elemental sulfur using sulfide-oxidizing bacteria In thisprocess metals such as Zn and Cd can be precipitated downto very low concentrations [22]

The Paques B V process has been successfully imple-mented at an industrial scale at the gold mine Pueblo Viejolocated in the Dominican Republic A copper recovery plantinstalled in 2014 based on sulfide precipitation is used torecover the copper liberated from the gold extraction processThe sulfidogenic bioreactor generates H

2S to recover up to

12000 ton of copper per year generating value and reducingthe amount of copper sent to the tailing dam [23] Applicationof this process has also been demonstrated on a pilot-scaleat the Kennecott Bingham Canyon copper mine in Utahwhere gt99 of copper present in a pH 26 waste stream wasrecovered [22 24 25]

Sulfate reduction activity has been reported in low pHecosystems for example in acidic lakes wetlands and acidmine drainage [19 26 27] However few acidophilictolerantSRB have been cultured [16 26 28ndash30] A major potentialadvantage of using acidophilic sulfidogens would be to allow

4 BioMed Research International

Table1Summaryof

thevario

ustypeso

ftreatmentfor

AMD

(com

piledfro

mSaho

oet

al[15]Gazea

etal[36]Trum

m[37]T

aylore

tal[38]R

oyCh

owdh

uryet

al[39]John

sonand

Hallberg[22]Skousen

[40]Skousen

etal[41]andSeervietal[42])

Syste

mtype

Applicability

Supp

ortm

aterials

Mechanism

sLimitatio

nBiologica

l

Aerobicw

etland

(AeW

)Mod

eratea

ciditynetalkalin

emined

rainage

Organicmattersoillim

estone

gravel

Oxidatio

nhydrolysis

precipitatio

nRe

quire

dlonger

detentiontim

eandhu

gesurfa

cearea

Anaerob

icwetland

(AnW

)Net-acidicw

ater

with

high

AlFe

andDO

Organicmattersuch

ascompo

stsawdu

sthayandlim

estone

gravel

Sulfateredu

ction

metal

precipitateas

sulfidesmicrobial

generatedalkalin

ityRe

quire

dlong

resid

ence

time

Verticalflo

wwetland

(VFW

)Net-acidicw

ater

with

high

AlFe

andDO

Limestoneorganicmatter

SulfateandFe

redu

ction

acid

neutralization

Highcapitalcostpo

tentialfor

armoringandplug

ging

with

hydroxides

Sulfateredu

cing

bioreactor

(SRB

)Sm

allfl

owso

rtosituatio

nsvery

acidicandmetalric

hwater

Organicsubstrates

uchas

hay

alfalfasaw

dust

paper

woo

dchipscrushed

limestone

andcompo

stor

manure

Microbialsulfateredu

ction

Highcapitalcostextre

mely

low

pHseverelyim

pactthee

fficiency

ofSredu

cing

bacteria

Pyrolusitelim

estone

beds

Mod

eratep

Handwhere

majority

ofacidity

isrelated

toMn

Limestoneorganicsubstrate

aerobicm

icroorganism

Hydrolysis

ofMn

Not

suitablefor

drainage

which

contains

high

Fehigh

maintenance

Perm

eabler

eactiveb

arrie

rs(PRB

)Groun

dwaterlow

DO

Organicmatterlim

estonezero

valent

iron

Sulfateredu

ction

sulfide

precipitates

neutralization

Iron

-oxidizing

bioreactor

Acidicwater

Fe-oxidizing

bacteriaand

archaea

Feoxidation

Phytorem

ediatio

nAny

AMD-im

pacted

sites

Metaltolerant

plantspecies

Phytoextractionand

phytostabilization

Successd

epends

onthep

roper

selectionof

the

metal-hyperaccumulator

plant

BioMed Research International 5

Table1Con

tinued

Syste

mtype

Applicability

Supp

ortm

aterials

Mechanism

sLimitatio

nGeochem

ical

Ano

xiclim

estone

drain(A

LD)

Acidicwater

with

lowAlFeD

OLimestone

gravel

compacted

soil

Limestone

dissolution

raise

pH

precipitatio

n

Fe-oxide

armoringlim

estone

limitperm

eabilityandcause

plug

ging

Alkalinity

prod

ucingsyste

m(A

PS)

Acidicwater

Organicmatterlim

estone

Ano

xicc

onditio

nneutralization

precipitatio

n

Openlim

estone

channel(OLC

)Re

quire

dste

epslo

pesnet-a

cidic

water

with

high

AlFe

andDO

Limestone

Limestone

dissolution

neutralization

Arm

oringor

thec

oatin

gof

the

limestonelarge

amou

ntis

neededdecreases

the

neutralizingcapacity

Limestone

leachbed(LLB

)Lo

wpH

andmetal-fr

eewater

Limestone

Limestone

dissolution

neutralization

Arm

oringwith

Fehydroxides

Steel-slagleachbed(SLB

)Highlyacidicandmetal-fr

eewater

Steelslag

Raise

alkalin

ityneutralization

Not

suitablefor

metal-la

den

water

Limestone

diversionwe

lls(LDW)

Sitesthato

ffera

suitable

topo

graphicalfall

Crushedlim

estone

aggregate

Hydraulicforcehydrolysis

and

neutralization

Requ

iredrefillin

gwith

limestone

every2ndash4weeks

Limestone

sand

Stream

flowwater

Sand

-sized

limestone

neutralizingacid

Coatin

gof

limestone

Low-pHFe

oxidationchannels

Shallowchannels

Limestone

orsand

stone

aggregate

Feoxidation

adsorptio

nand

coprecipitatio

n

Itremoves

someF

ebu

trem

oval

efficiency

hasn

otbeen

determ

ined

Sulfide

passivationmicroencapsulation

Pitw

allfacessulfid

ebearin

gwastesrocks

piles

Inorganicc

oatin

gph

osph

ate

silicafly

ashlim

estoneorganic

coatinghu

micacidlipids

polyethylene

polyam

ine

alkoxysilanesfattyacidoxalic

acidcatecho

l

Preventsulfid

eoxidatio

nby

inorganica

ndorganicc

oatin

g

Long

-term

effectiv

enessisstillin

questio

norganicc

oatin

gexpensive

Electro

chem

icalcover

Tailing

wasterock

Con

ductives

teelmeshcathod

emetalanod

eRe

ducing

DOby

electrochem

ical

process

Highcapitalcosto

fano

desno

inform

ationavailableo

nlarge

scalea

pplication

6 BioMed Research International

Table1Con

tinued

Syste

mtype

Applicability

Supp

ortm

aterials

Mechanism

sLimitatio

nPh

ysica

l

Dry

cover

Sulfide

bearingwastesrockpiles

Fine-grained

soilorganic

materials

synthetic

material

(plasticliners)vegetation

Minim

izeo

xidatio

nby

physical

barrierneutralization

precipitates

Shortterm

effectiv

eness

Wetcover

Sulfide

wastes

Und

erwater

Disp

osingwasteun

derw

ater

anoxiccond

ition

sRe

quire

rigorou

seng

ineerin

gdesig

nhigh

maintenance

Gas

redo

xanddisplacement

syste

m(G

aRDS)

Und

ergrou

ndmines

CO2andCH4gas

Gas

mixturesp

hysic

allydisplace

O2

Itson

lyfeasiblewhere

partialor

completefl

ooding

isno

tfeasib

le

BioMed Research International 7

MetalSuldes(ZnS)

Air

Excess

Sulfur

Puriedeuent

Recycle

Neu

troph

ilic

SRB

Bior

eact

or o

ne

Bior

eact

or tw

oSu

lde

oxid

ising

bac

teriaWaste water or

process water(34

2minus and metalssuch as H

2+)

(2-rich gas

2

(3minus

(3I)

34

2minus+ 4(2 + (

+rarr (3

minus+ 4(2

H2+

+ (3minusrarr H3 + (

+

2(3minus+ 2 + 2(

+rarr 23

I+ 2(2

(a)

Bior

eact

orsta

ge I

Stag

e II

Ana

erob

ic ag

itate

dco

ntac

tor

SulfurReagents

Feed water(AMD)

sulfu

r red

ucin

g ba

cter

ia

ClarierTreated water

Filter

Metal sulde (ZnS)to smelter

(23

Gen

erat

ion

by

(23

(b)

Figure 2 Schematic overview of the Thiopaq (a) and Biosulfide (b) processes (adapted from Adams et al [12] Muyzer and Stams [13])

simpler engineering designs and reduce operational costs byusing single on-line reactor vessels that could be used to bothgenerate sulfide and selectively precipitate target metal(s)Precipitation and removal of many soluble transition metalsoften present in AMD emanating from metal mines maybe achieved by ready biomineralization as their sulfides Theproduced metal sulfides have different solubilities thereforemetals can be precipitated together or selectively by con-trolling concentrations of the key reactant S2minus which maybe achieved by controlling pH (S2minus + H+ harr HSminus) Coppersulfide for example is far less soluble than ferrous sulfide(respective log Ksp values of minus359 and minus188) and thereforeCuS precipitates at pH 2 whereas FeS needs much higher pHto precipitate Diez-Ercilla et al [31] have also demonstratedthat selective precipitation of metal sulfides occurs naturallyin Cueva de la Mora pit lake (SW Spain) and the geochemicalcalculations match perfectly with the results of chemicaland mineralogical composition Nancucheo and Johnson[3] showed that it was possible to selectively precipitate

stable metal sulfides in inline reactor vessel testing twosynthetic AMDs in acidic conditions (pH 22ndash48) In the firstbioreactor with a composition of feeding similar to AMD atthe abandoned Cwm Rheidol lead-zinc mine in mid-Waleszinc was efficiently precipitated (gt99) as sulfide inside thereactor while both aluminum and ferrous iron remain insolution (gt99) and were washed out of the reactor vesselThe second sulfidogenic bioreactor was challenged with asynthetic AMD based on that from Mynydd Parys NorthWales Throughout the test period all the copper presentin the feed liquor was precipitated (confirmed as coppersulfide) within the bioreactor but none of the ferrous ironwas present in the solids Although the initial pH at whichthe bioreactor was operated (from pH 36 to 25) causedsome coprecipitation of zinc with the copper by progressivelylowering the bioreactor pH and the concentration of theelectron donor in the influent liquor it was possible toprecipitate gt99 of the copper within the bioreactor as CuSand to maintain gt99 of the zinc iron and aluminum in

8 BioMed Research International

solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]

4C3H8O3+ 10H+ + 7SO

4

2minus+ Cu2+ + Zn2+ + Fe2+

997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H

2O

(1)

This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD

Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H

2S) by the SRB and orpiment

(As2S3) generated within the bioreactor In addition this

process was also observed to occur naturally in an acidic pitlake [31]

Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for

the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes

3 Microbiology in Remediating AcidicMine Waters

Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]

Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents

BioMed Research International 9

Table2Isolated

sulfido

genicm

icroorganism

sand

theirm

aincharacteris

tics

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermocladium

modestiu

s45ndash82

(75)

26ndash

59(40)

Glycogen

starch

proteins

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

mud

)Japan

[43ndash45]

Caldivirg

amaquilin

gensis

70ndash9

023ndash64(37ndash4

2)

Glycogen

beefextract

pepton

etryptoneyeast

extract

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

solfataric

soilmud

)Mt

Maquilin

gPh

ilipp

ines

[46]

Archaeoglobu

slithotro

phicu

snd

60

Acetate

SulfateL-cysteine

nd[4748]

Archaeoglobu

sveneficus

nd69

H2acetateformate

pyruvateyeastextract

citratelactatesta

rch

pepton

e

Sulfitethiosulfate

Wallsof

activ

eblack

smoker

atmiddle

AtlanticRidge

[44]

Archaeoglobu

sprofund

usnd

45ndash75

H2acetatepyruvate

yeastextractlactate

meatextractpeptone

crud

eoilwith

acetate

Sulfatethiosulfate

sulfite

Deepseah

ydrothermal

syste

moff

Guaym

as

Mexico

[4950]

Archaeoglobu

sfulgidu

s60ndash75

(70)

55ndash75

(60)

H2C

O2formate

form

amideD(minus)-and

L(+)-lactateglucose

starchcalam

inea

cids

pepton

egelatincasein

meatextractyeast

extract

Sulfatethiosulfate

sulfite

Marineh

ydrothermal

syste

mN

eron

eIta

ly[4951]

Thermodesulfatatorind

icus

55ndash80

(70)

60ndash

67(625)

H2C

O2stim

ulated

bymethano

lmon

omethylamine

glutam

atepepton

efumaratetryptone

isobu

tyrate3-C

H3

butyrateethanol

prop

anolandlow

amou

ntso

facetate

Sulfate

Marineh

ydrothermal

syste

mC

entralIndian

Ridge

[52]

Thermodesulfobacterium

hydrogeniphilum

50ndash80

(75)

63ndash68(65)

H2C

O2stim

ulated

byacetatefumarate

3-methylbutyrate

glutam

ateyeastextract

pepton

eortrypton

e

Sulfate

Marineh

ydrothermal

syste

mG

uaym

asBa

sin[53]

10 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermodesulfobacterium

commun

e41ndash83

60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA[5455]

Thermodesulfobacterium

thermophilum

nd60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

nd[55]

Thermodesulfobacterium

hveragerdense

7545ndash70

(70)

H2pyruvatelactate

Sulfatesulfite

Hot

sprin

gs(m

icrobial

mats)Iceland

[56]

Thermodesulfobium

narugense

6940ndash

60(55ndash6

0)

H2C

O2

Sulfaten

itrate

thiosulfate

Hot

sprin

gs(m

icrobial

mats)Japan

[57]

Desulfotomaculum

spp(30

species)

nd23ndash55

H2C

O2formatesome

(organicacidslip

idsor

mon

oaromatic

hydrocarbo

ns)

Sulfidesulfur

thiosulfateA

cetate

some(Fe

(III)Mn(IV)

U(V

I)or

Cr(V

I))

Subsurface

environm

ents

rice

fieldsminesoilspills

[58ndash62]

Desulfosporosinus

meridiei

10ndash37

61ndash75

H2C

O2acetatesom

e(la

ctatepyruvate

ethano

l)Sulfatesom

e(nitrate)

Groun

dwater

contam

inated

with

polycyclica

romatic

hydrocarbo

nsinSw

anCoastalPlain

Australia

[63]

Desulfosporosinus

youn

gii

8ndash39

(32ndash35)

57ndash82(70ndash

73)

Beefextractyeast

extractform

ate

succinatelactate

pyruvateethanoland

toluene

Fumaratesulfatesulfite

thiosulfate

Artificialwetland

(sedim

ent)

[64]

BioMed Research International 11

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfosporosinus

orien

tis37ndash4

860ndash

65

H2C

O2formate

lactatepyruvatem

alate

fumaratesuccinate

methano

lethano

lprop

anolbutanol

butyratevalerate

palm

itate

Sulfatesulfite

thiosulfatesulfur

nd[65]

Desulfosporom

usapolytro

pa4ndash

3761ndash80

H2C

O2formate

lactatebu

tyrateseveral

alcoho

lsorganica

cids

carboh

ydratessome

aminoacidscholine

betaine

SulfateFe(OH) 3

Oligotroph

iclake

(sedim

ent)

German

[66]

Thermodesulfovibrio

yellowstonii

41ndash83

60ndash

80(70)

H2C

O2acetate

form

atelactate

pyruvate

Sulfatethiosulfate

sulfite

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA

[67]

Thermodesulfovibrio

islandicus

5545ndash70

(70)

H2pyruvatelactate

form

ate

Sulfaten

itrate

Bioreactor

inoculated

with

hotsprings

(microbialmats)sample

Iceland

[56]

Desulfohalobium

spp(6

species)

nd55ndash80(65ndash70)

H2lactateethanol

acetate

Sulfite

hypersaline

environm

ents

[6869]

Desulfocaldus

terraneus

58nd

H2C

O2aminoacids

proteinaceou

ssub

strates

andorganica

cids

prod

ucingethano

lacetateprop

ionate

isovalerate2-

methylbutyrate

Cystinesulfu

rsulfate

Seao

ilfacilitiesAlaksa

[70]

12 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfomicrobium

spp(4

species)

25ndash30

ndH2lactatepyruvate

Ethano

lform

ate

Sulfatesulfoxyanions

Anaerob

icsediments

(Freshwaterbrackish

marine)anaerob

icstrata

oroverlyingwaterand

insaturatedmineralor

organicd

eposits

[5469]

Desulfonatro

novibrio

hydrogenovoran

s37ndash4

090

ndash102(90ndash97)

H2formate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[71]

Desulfonatro

num

spp(3

species)

20ndash4

5(37ndash45)

80ndash

100(90)

H2form

ateYeast

extractethano

llactate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[72]

Desulfovibriospp(47

species)

25ndash4

4(25ndash35)

ndH2C

O2acetatelactate

carboh

ydrates

Sulfaten

itrate

nd[73]

Desulfomonile

spp(2

species)

30ndash30

(37)

65ndash78

(68ndash70)

H2C

O2benzoate

pyruvateorganic

carbon

halogens

Sulfatesulfite

thiosulfatesulfurFe

(III)NitrateU(V

I)Slud

ge[74]

Syntroph

obacteraceae

(8genera)

31ndash6

070

ndash75

H2C

O2acetate

form

atelactate

pyruvate

Sulfatesulfite

thiosulfate

Sewages

ludge

freshwaterbrackish

marines

edim

ent

marineh

ydrothermal

ventsho

tspring

sediments

[7375]

Desulfobacterium

anilini

3069ndash

75H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

BioMed Research International 13

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfarculus

baarsii

35ndash39

73H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

Desulfobacteraceae(12

genera)

10ndash4

0nd

H2C

O2L

ong-chain

fatty

acidsAlcoh

ols

Polara

romatic

compo

undsand

insome

casese

venAlip

hatic

arom

atichydrocarbo

ns

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[77]

Desulfosporosinus

acidophilus

25ndash4

036ndash

52(52)

H2lactatepyruvate

glycerolglucose

and

fructose

Sulfate

Sedimentfrom

anacid

effluent

pond

[26]

Desulfosporosinus

acididuran

s15ndash4

038ndash70

(55)

H2formatelactate

butyratefum

arate

malatepyruvate

glycerolm

ethano

lethano

lyeastextract

xyloseglucosefructose

Ferriciro

nnitrate

sulfateelem

entalsulfur

thiosulfate

Whiteriv

erdraining

from

theS

oufriere

hills

inMon

serrat(pH32)

[78]

a Valuesc

losedby

parenthesis

arec

onsid

ered

optim

alpH

ndno

tinformed

byconsultedreference

14 BioMed Research International

such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO

2[33]

In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO

2and H

2[17]

D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]

4 Natural Attenuation for the Design of AMDRemediation Strategies

Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and

chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH

2O)were detected presumably due

to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not

Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]

5 Concluding Remarks

Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools

Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico

BioMed Research International 15

(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)

References

[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013

[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014

[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012

[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008

[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011

[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003

[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000

[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014

[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006

[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005

[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007

[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008

[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008

[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015

[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013

[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006

[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006

[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014

[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008

[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006

[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010

[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005

[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016

[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999

[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001

[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010

[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990

[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016

[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014

[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009

[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

BioMed Research International 3

2 Remediation of Acidic Mine Water

Waters draining from abandoned metal mines and minewastes are often acidic (pH lt 4) and contain elevated concen-trations of dissolved metals and metalloids and high osmoticpotential associated with concentration of sulfate salts [14] Inmost cases active chemical treatment and passive biologicaltreatment can provide effective remediation of AMD [15](details and literature of the advantages and disadvantagesof these treatment and others are presented in Table 1) Amajor drawback to both approaches is that the immobilizedmetals are contained in ldquosludgerdquo (chemical treatment) orwithin spent compost (biological treatment) and need to bedisposed in specially designated landfill sites precluding theirrecovery and recycling Changes in redox conditions duringstorage can lead to remobilization of metals (and metalloidssuch as arsenic) in both sludge and spent composts Inaddition potentially useful and valuable metal resources arenot recovered using conventional approaches for remediatingmine waters [3 16]

A radically different approach for remediating AMDwhich like compost bioreactors derives from the abilities ofsome microorganisms to generate alkalinity and to immo-bilize metals is referred to generally as ldquoactive biologicaltreatmentrdquoMicrobiological processes that generate alkalinityare mostly reductive processes and include denitrificationmethanogenesis and dissimilatory reduction of sulfate ferriciron and manganese (IV) which tend to be limited inAMD Considering that AMD usually contains elevatedconcentrations of both ferric iron and sulfate the ability ofsome bacteria to use these compounds as terminal electronacceptors suggests that these reactions can be highly usefulfor mine water remediation Acidic environments in whichsulfur or sulfide minerals are subjected to biologically-accelerated oxidative dissolution characteristically containlarge concentrations of soluble sulfate [17] Therefore micro-bial sulfate reduction might be anticipated to occur withinanaerobic zones in both acidic and nonacidic environmentsBiological sulfidogenesis generates hydrogen sulfide as aresult of a reductive metabolic process using sulfate reducingbacteria (SRB) Biological sulfidogenesis has the additionalbenefits of being a proton-consuming reaction allowing theincrease in pHof theminewater treated contributing towardsmitigation and remediation The hydrogen sulfide generatedcan be used in controlled situations to selectively precipitatemany potentially toxic metals (such as copper and zinc) oftenpresent in AMD at elevated concentrations [3 18] Activebiological treatment has many advantages over alternativestrategies for treatingmine waters one of the most importantbeing its potential for recovering metals that are commonlypresent in AMD

There have been few successful applications of SRB-mediated active AMD treatment systems even though thispossibility has long been appreciated One major reason forthis is that SRB happens preferentially between pH 6 and8 [19] whereas AMD generally has a pH between 2 and 4and commonly pH lt 3 [20] Under these circumstances aneutralization step is necessary beforeAMDeffluents are sub-jected to bacterial sulfate reduction or alternatively ldquooff-linerdquo

systems need to be used The latter is necessary by the factthat current systems use neutrophilic SRB or sulfur reducingbacteria and direct exposure to the inflowing acidic solutionbeing treated would be lethal to these microorganismsTherefore a separate vessel in which sulfide generated bythe bacteria is contacted with the acidic metal-laden wastewater is required [16 21] Examples of this technology arethe Biosulfide and Thiopaq processes (Figure 2) operatedunder the auspices of two biotechnology companies BioTeq(Canada) and Paques B V (The Netherlands) which arecurrently in operation in various parts of the world

The Biosulfide process has two stages one chemicaland the other biological Metals are removed from AMDin the chemical stage by precipitation with biogenic sulfideproduced in the biological stage by SRB under anaerobiccondition In this system hydrogen sulfide is generated bythe reduction of elemental sulfur or other sulfur source inthe presence of an electron donor such as acetic acid Thegas is passed to an anaerobic agitated contactor in whichcopper can be precipitated as a sulfide usually without pHadjustment and without significant precipitation of otherheavy metals present in the water The end result is a highvalue copper product usually containing more than 50 ofthe metal Other metals such as nickel zinc and cobalt canalso be recovered as separate high-grade sulfide productsalthough pH control using an alkali source is usually requiredto selectively precipitate the metal as a sulfide phase Thehigh-grade metal sulfide precipitate is then recovered byconventional clarification and filtration to produce a filtercake which can be shipped to a smelter [12]

TheThiopaqprocess uses another system that involves theuse of two biological continuous reactors connected in series(I) to an anaerobic upflow sludge blanket (UASB) reactorfor the reduction of oxidized sulfur species In this reactorethanol or hydrogen is utilized by the SRB as electron donorproducing sulfide (mostly HSminus) for the precipitation of metalsulfides (which can proceed in the same reactor depending onthe toxicity of the wastewater) and (II) an aerobic submergedfixed film (SFF) reactor where the excess sulfide is oxidizedto elemental sulfur using sulfide-oxidizing bacteria In thisprocess metals such as Zn and Cd can be precipitated downto very low concentrations [22]

The Paques B V process has been successfully imple-mented at an industrial scale at the gold mine Pueblo Viejolocated in the Dominican Republic A copper recovery plantinstalled in 2014 based on sulfide precipitation is used torecover the copper liberated from the gold extraction processThe sulfidogenic bioreactor generates H

2S to recover up to

12000 ton of copper per year generating value and reducingthe amount of copper sent to the tailing dam [23] Applicationof this process has also been demonstrated on a pilot-scaleat the Kennecott Bingham Canyon copper mine in Utahwhere gt99 of copper present in a pH 26 waste stream wasrecovered [22 24 25]

Sulfate reduction activity has been reported in low pHecosystems for example in acidic lakes wetlands and acidmine drainage [19 26 27] However few acidophilictolerantSRB have been cultured [16 26 28ndash30] A major potentialadvantage of using acidophilic sulfidogens would be to allow

4 BioMed Research International

Table1Summaryof

thevario

ustypeso

ftreatmentfor

AMD

(com

piledfro

mSaho

oet

al[15]Gazea

etal[36]Trum

m[37]T

aylore

tal[38]R

oyCh

owdh

uryet

al[39]John

sonand

Hallberg[22]Skousen

[40]Skousen

etal[41]andSeervietal[42])

Syste

mtype

Applicability

Supp

ortm

aterials

Mechanism

sLimitatio

nBiologica

l

Aerobicw

etland

(AeW

)Mod

eratea

ciditynetalkalin

emined

rainage

Organicmattersoillim

estone

gravel

Oxidatio

nhydrolysis

precipitatio

nRe

quire

dlonger

detentiontim

eandhu

gesurfa

cearea

Anaerob

icwetland

(AnW

)Net-acidicw

ater

with

high

AlFe

andDO

Organicmattersuch

ascompo

stsawdu

sthayandlim

estone

gravel

Sulfateredu

ction

metal

precipitateas

sulfidesmicrobial

generatedalkalin

ityRe

quire

dlong

resid

ence

time

Verticalflo

wwetland

(VFW

)Net-acidicw

ater

with

high

AlFe

andDO

Limestoneorganicmatter

SulfateandFe

redu

ction

acid

neutralization

Highcapitalcostpo

tentialfor

armoringandplug

ging

with

hydroxides

Sulfateredu

cing

bioreactor

(SRB

)Sm

allfl

owso

rtosituatio

nsvery

acidicandmetalric

hwater

Organicsubstrates

uchas

hay

alfalfasaw

dust

paper

woo

dchipscrushed

limestone

andcompo

stor

manure

Microbialsulfateredu

ction

Highcapitalcostextre

mely

low

pHseverelyim

pactthee

fficiency

ofSredu

cing

bacteria

Pyrolusitelim

estone

beds

Mod

eratep

Handwhere

majority

ofacidity

isrelated

toMn

Limestoneorganicsubstrate

aerobicm

icroorganism

Hydrolysis

ofMn

Not

suitablefor

drainage

which

contains

high

Fehigh

maintenance

Perm

eabler

eactiveb

arrie

rs(PRB

)Groun

dwaterlow

DO

Organicmatterlim

estonezero

valent

iron

Sulfateredu

ction

sulfide

precipitates

neutralization

Iron

-oxidizing

bioreactor

Acidicwater

Fe-oxidizing

bacteriaand

archaea

Feoxidation

Phytorem

ediatio

nAny

AMD-im

pacted

sites

Metaltolerant

plantspecies

Phytoextractionand

phytostabilization

Successd

epends

onthep

roper

selectionof

the

metal-hyperaccumulator

plant

BioMed Research International 5

Table1Con

tinued

Syste

mtype

Applicability

Supp

ortm

aterials

Mechanism

sLimitatio

nGeochem

ical

Ano

xiclim

estone

drain(A

LD)

Acidicwater

with

lowAlFeD

OLimestone

gravel

compacted

soil

Limestone

dissolution

raise

pH

precipitatio

n

Fe-oxide

armoringlim

estone

limitperm

eabilityandcause

plug

ging

Alkalinity

prod

ucingsyste

m(A

PS)

Acidicwater

Organicmatterlim

estone

Ano

xicc

onditio

nneutralization

precipitatio

n

Openlim

estone

channel(OLC

)Re

quire

dste

epslo

pesnet-a

cidic

water

with

high

AlFe

andDO

Limestone

Limestone

dissolution

neutralization

Arm

oringor

thec

oatin

gof

the

limestonelarge

amou

ntis

neededdecreases

the

neutralizingcapacity

Limestone

leachbed(LLB

)Lo

wpH

andmetal-fr

eewater

Limestone

Limestone

dissolution

neutralization

Arm

oringwith

Fehydroxides

Steel-slagleachbed(SLB

)Highlyacidicandmetal-fr

eewater

Steelslag

Raise

alkalin

ityneutralization

Not

suitablefor

metal-la

den

water

Limestone

diversionwe

lls(LDW)

Sitesthato

ffera

suitable

topo

graphicalfall

Crushedlim

estone

aggregate

Hydraulicforcehydrolysis

and

neutralization

Requ

iredrefillin

gwith

limestone

every2ndash4weeks

Limestone

sand

Stream

flowwater

Sand

-sized

limestone

neutralizingacid

Coatin

gof

limestone

Low-pHFe

oxidationchannels

Shallowchannels

Limestone

orsand

stone

aggregate

Feoxidation

adsorptio

nand

coprecipitatio

n

Itremoves

someF

ebu

trem

oval

efficiency

hasn

otbeen

determ

ined

Sulfide

passivationmicroencapsulation

Pitw

allfacessulfid

ebearin

gwastesrocks

piles

Inorganicc

oatin

gph

osph

ate

silicafly

ashlim

estoneorganic

coatinghu

micacidlipids

polyethylene

polyam

ine

alkoxysilanesfattyacidoxalic

acidcatecho

l

Preventsulfid

eoxidatio

nby

inorganica

ndorganicc

oatin

g

Long

-term

effectiv

enessisstillin

questio

norganicc

oatin

gexpensive

Electro

chem

icalcover

Tailing

wasterock

Con

ductives

teelmeshcathod

emetalanod

eRe

ducing

DOby

electrochem

ical

process

Highcapitalcosto

fano

desno

inform

ationavailableo

nlarge

scalea

pplication

6 BioMed Research International

Table1Con

tinued

Syste

mtype

Applicability

Supp

ortm

aterials

Mechanism

sLimitatio

nPh

ysica

l

Dry

cover

Sulfide

bearingwastesrockpiles

Fine-grained

soilorganic

materials

synthetic

material

(plasticliners)vegetation

Minim

izeo

xidatio

nby

physical

barrierneutralization

precipitates

Shortterm

effectiv

eness

Wetcover

Sulfide

wastes

Und

erwater

Disp

osingwasteun

derw

ater

anoxiccond

ition

sRe

quire

rigorou

seng

ineerin

gdesig

nhigh

maintenance

Gas

redo

xanddisplacement

syste

m(G

aRDS)

Und

ergrou

ndmines

CO2andCH4gas

Gas

mixturesp

hysic

allydisplace

O2

Itson

lyfeasiblewhere

partialor

completefl

ooding

isno

tfeasib

le

BioMed Research International 7

MetalSuldes(ZnS)

Air

Excess

Sulfur

Puriedeuent

Recycle

Neu

troph

ilic

SRB

Bior

eact

or o

ne

Bior

eact

or tw

oSu

lde

oxid

ising

bac

teriaWaste water or

process water(34

2minus and metalssuch as H

2+)

(2-rich gas

2

(3minus

(3I)

34

2minus+ 4(2 + (

+rarr (3

minus+ 4(2

H2+

+ (3minusrarr H3 + (

+

2(3minus+ 2 + 2(

+rarr 23

I+ 2(2

(a)

Bior

eact

orsta

ge I

Stag

e II

Ana

erob

ic ag

itate

dco

ntac

tor

SulfurReagents

Feed water(AMD)

sulfu

r red

ucin

g ba

cter

ia

ClarierTreated water

Filter

Metal sulde (ZnS)to smelter

(23

Gen

erat

ion

by

(23

(b)

Figure 2 Schematic overview of the Thiopaq (a) and Biosulfide (b) processes (adapted from Adams et al [12] Muyzer and Stams [13])

simpler engineering designs and reduce operational costs byusing single on-line reactor vessels that could be used to bothgenerate sulfide and selectively precipitate target metal(s)Precipitation and removal of many soluble transition metalsoften present in AMD emanating from metal mines maybe achieved by ready biomineralization as their sulfides Theproduced metal sulfides have different solubilities thereforemetals can be precipitated together or selectively by con-trolling concentrations of the key reactant S2minus which maybe achieved by controlling pH (S2minus + H+ harr HSminus) Coppersulfide for example is far less soluble than ferrous sulfide(respective log Ksp values of minus359 and minus188) and thereforeCuS precipitates at pH 2 whereas FeS needs much higher pHto precipitate Diez-Ercilla et al [31] have also demonstratedthat selective precipitation of metal sulfides occurs naturallyin Cueva de la Mora pit lake (SW Spain) and the geochemicalcalculations match perfectly with the results of chemicaland mineralogical composition Nancucheo and Johnson[3] showed that it was possible to selectively precipitate

stable metal sulfides in inline reactor vessel testing twosynthetic AMDs in acidic conditions (pH 22ndash48) In the firstbioreactor with a composition of feeding similar to AMD atthe abandoned Cwm Rheidol lead-zinc mine in mid-Waleszinc was efficiently precipitated (gt99) as sulfide inside thereactor while both aluminum and ferrous iron remain insolution (gt99) and were washed out of the reactor vesselThe second sulfidogenic bioreactor was challenged with asynthetic AMD based on that from Mynydd Parys NorthWales Throughout the test period all the copper presentin the feed liquor was precipitated (confirmed as coppersulfide) within the bioreactor but none of the ferrous ironwas present in the solids Although the initial pH at whichthe bioreactor was operated (from pH 36 to 25) causedsome coprecipitation of zinc with the copper by progressivelylowering the bioreactor pH and the concentration of theelectron donor in the influent liquor it was possible toprecipitate gt99 of the copper within the bioreactor as CuSand to maintain gt99 of the zinc iron and aluminum in

8 BioMed Research International

solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]

4C3H8O3+ 10H+ + 7SO

4

2minus+ Cu2+ + Zn2+ + Fe2+

997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H

2O

(1)

This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD

Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H

2S) by the SRB and orpiment

(As2S3) generated within the bioreactor In addition this

process was also observed to occur naturally in an acidic pitlake [31]

Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for

the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes

3 Microbiology in Remediating AcidicMine Waters

Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]

Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents

BioMed Research International 9

Table2Isolated

sulfido

genicm

icroorganism

sand

theirm

aincharacteris

tics

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermocladium

modestiu

s45ndash82

(75)

26ndash

59(40)

Glycogen

starch

proteins

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

mud

)Japan

[43ndash45]

Caldivirg

amaquilin

gensis

70ndash9

023ndash64(37ndash4

2)

Glycogen

beefextract

pepton

etryptoneyeast

extract

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

solfataric

soilmud

)Mt

Maquilin

gPh

ilipp

ines

[46]

Archaeoglobu

slithotro

phicu

snd

60

Acetate

SulfateL-cysteine

nd[4748]

Archaeoglobu

sveneficus

nd69

H2acetateformate

pyruvateyeastextract

citratelactatesta

rch

pepton

e

Sulfitethiosulfate

Wallsof

activ

eblack

smoker

atmiddle

AtlanticRidge

[44]

Archaeoglobu

sprofund

usnd

45ndash75

H2acetatepyruvate

yeastextractlactate

meatextractpeptone

crud

eoilwith

acetate

Sulfatethiosulfate

sulfite

Deepseah

ydrothermal

syste

moff

Guaym

as

Mexico

[4950]

Archaeoglobu

sfulgidu

s60ndash75

(70)

55ndash75

(60)

H2C

O2formate

form

amideD(minus)-and

L(+)-lactateglucose

starchcalam

inea

cids

pepton

egelatincasein

meatextractyeast

extract

Sulfatethiosulfate

sulfite

Marineh

ydrothermal

syste

mN

eron

eIta

ly[4951]

Thermodesulfatatorind

icus

55ndash80

(70)

60ndash

67(625)

H2C

O2stim

ulated

bymethano

lmon

omethylamine

glutam

atepepton

efumaratetryptone

isobu

tyrate3-C

H3

butyrateethanol

prop

anolandlow

amou

ntso

facetate

Sulfate

Marineh

ydrothermal

syste

mC

entralIndian

Ridge

[52]

Thermodesulfobacterium

hydrogeniphilum

50ndash80

(75)

63ndash68(65)

H2C

O2stim

ulated

byacetatefumarate

3-methylbutyrate

glutam

ateyeastextract

pepton

eortrypton

e

Sulfate

Marineh

ydrothermal

syste

mG

uaym

asBa

sin[53]

10 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermodesulfobacterium

commun

e41ndash83

60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA[5455]

Thermodesulfobacterium

thermophilum

nd60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

nd[55]

Thermodesulfobacterium

hveragerdense

7545ndash70

(70)

H2pyruvatelactate

Sulfatesulfite

Hot

sprin

gs(m

icrobial

mats)Iceland

[56]

Thermodesulfobium

narugense

6940ndash

60(55ndash6

0)

H2C

O2

Sulfaten

itrate

thiosulfate

Hot

sprin

gs(m

icrobial

mats)Japan

[57]

Desulfotomaculum

spp(30

species)

nd23ndash55

H2C

O2formatesome

(organicacidslip

idsor

mon

oaromatic

hydrocarbo

ns)

Sulfidesulfur

thiosulfateA

cetate

some(Fe

(III)Mn(IV)

U(V

I)or

Cr(V

I))

Subsurface

environm

ents

rice

fieldsminesoilspills

[58ndash62]

Desulfosporosinus

meridiei

10ndash37

61ndash75

H2C

O2acetatesom

e(la

ctatepyruvate

ethano

l)Sulfatesom

e(nitrate)

Groun

dwater

contam

inated

with

polycyclica

romatic

hydrocarbo

nsinSw

anCoastalPlain

Australia

[63]

Desulfosporosinus

youn

gii

8ndash39

(32ndash35)

57ndash82(70ndash

73)

Beefextractyeast

extractform

ate

succinatelactate

pyruvateethanoland

toluene

Fumaratesulfatesulfite

thiosulfate

Artificialwetland

(sedim

ent)

[64]

BioMed Research International 11

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfosporosinus

orien

tis37ndash4

860ndash

65

H2C

O2formate

lactatepyruvatem

alate

fumaratesuccinate

methano

lethano

lprop

anolbutanol

butyratevalerate

palm

itate

Sulfatesulfite

thiosulfatesulfur

nd[65]

Desulfosporom

usapolytro

pa4ndash

3761ndash80

H2C

O2formate

lactatebu

tyrateseveral

alcoho

lsorganica

cids

carboh

ydratessome

aminoacidscholine

betaine

SulfateFe(OH) 3

Oligotroph

iclake

(sedim

ent)

German

[66]

Thermodesulfovibrio

yellowstonii

41ndash83

60ndash

80(70)

H2C

O2acetate

form

atelactate

pyruvate

Sulfatethiosulfate

sulfite

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA

[67]

Thermodesulfovibrio

islandicus

5545ndash70

(70)

H2pyruvatelactate

form

ate

Sulfaten

itrate

Bioreactor

inoculated

with

hotsprings

(microbialmats)sample

Iceland

[56]

Desulfohalobium

spp(6

species)

nd55ndash80(65ndash70)

H2lactateethanol

acetate

Sulfite

hypersaline

environm

ents

[6869]

Desulfocaldus

terraneus

58nd

H2C

O2aminoacids

proteinaceou

ssub

strates

andorganica

cids

prod

ucingethano

lacetateprop

ionate

isovalerate2-

methylbutyrate

Cystinesulfu

rsulfate

Seao

ilfacilitiesAlaksa

[70]

12 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfomicrobium

spp(4

species)

25ndash30

ndH2lactatepyruvate

Ethano

lform

ate

Sulfatesulfoxyanions

Anaerob

icsediments

(Freshwaterbrackish

marine)anaerob

icstrata

oroverlyingwaterand

insaturatedmineralor

organicd

eposits

[5469]

Desulfonatro

novibrio

hydrogenovoran

s37ndash4

090

ndash102(90ndash97)

H2formate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[71]

Desulfonatro

num

spp(3

species)

20ndash4

5(37ndash45)

80ndash

100(90)

H2form

ateYeast

extractethano

llactate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[72]

Desulfovibriospp(47

species)

25ndash4

4(25ndash35)

ndH2C

O2acetatelactate

carboh

ydrates

Sulfaten

itrate

nd[73]

Desulfomonile

spp(2

species)

30ndash30

(37)

65ndash78

(68ndash70)

H2C

O2benzoate

pyruvateorganic

carbon

halogens

Sulfatesulfite

thiosulfatesulfurFe

(III)NitrateU(V

I)Slud

ge[74]

Syntroph

obacteraceae

(8genera)

31ndash6

070

ndash75

H2C

O2acetate

form

atelactate

pyruvate

Sulfatesulfite

thiosulfate

Sewages

ludge

freshwaterbrackish

marines

edim

ent

marineh

ydrothermal

ventsho

tspring

sediments

[7375]

Desulfobacterium

anilini

3069ndash

75H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

BioMed Research International 13

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfarculus

baarsii

35ndash39

73H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

Desulfobacteraceae(12

genera)

10ndash4

0nd

H2C

O2L

ong-chain

fatty

acidsAlcoh

ols

Polara

romatic

compo

undsand

insome

casese

venAlip

hatic

arom

atichydrocarbo

ns

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[77]

Desulfosporosinus

acidophilus

25ndash4

036ndash

52(52)

H2lactatepyruvate

glycerolglucose

and

fructose

Sulfate

Sedimentfrom

anacid

effluent

pond

[26]

Desulfosporosinus

acididuran

s15ndash4

038ndash70

(55)

H2formatelactate

butyratefum

arate

malatepyruvate

glycerolm

ethano

lethano

lyeastextract

xyloseglucosefructose

Ferriciro

nnitrate

sulfateelem

entalsulfur

thiosulfate

Whiteriv

erdraining

from

theS

oufriere

hills

inMon

serrat(pH32)

[78]

a Valuesc

losedby

parenthesis

arec

onsid

ered

optim

alpH

ndno

tinformed

byconsultedreference

14 BioMed Research International

such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO

2[33]

In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO

2and H

2[17]

D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]

4 Natural Attenuation for the Design of AMDRemediation Strategies

Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and

chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH

2O)were detected presumably due

to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not

Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]

5 Concluding Remarks

Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools

Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico

BioMed Research International 15

(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)

References

[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013

[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014

[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012

[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008

[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011

[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003

[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000

[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014

[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006

[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005

[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007

[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008

[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008

[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015

[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013

[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006

[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006

[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014

[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008

[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006

[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010

[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005

[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016

[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999

[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001

[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010

[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990

[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016

[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014

[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009

[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

4 BioMed Research International

Table1Summaryof

thevario

ustypeso

ftreatmentfor

AMD

(com

piledfro

mSaho

oet

al[15]Gazea

etal[36]Trum

m[37]T

aylore

tal[38]R

oyCh

owdh

uryet

al[39]John

sonand

Hallberg[22]Skousen

[40]Skousen

etal[41]andSeervietal[42])

Syste

mtype

Applicability

Supp

ortm

aterials

Mechanism

sLimitatio

nBiologica

l

Aerobicw

etland

(AeW

)Mod

eratea

ciditynetalkalin

emined

rainage

Organicmattersoillim

estone

gravel

Oxidatio

nhydrolysis

precipitatio

nRe

quire

dlonger

detentiontim

eandhu

gesurfa

cearea

Anaerob

icwetland

(AnW

)Net-acidicw

ater

with

high

AlFe

andDO

Organicmattersuch

ascompo

stsawdu

sthayandlim

estone

gravel

Sulfateredu

ction

metal

precipitateas

sulfidesmicrobial

generatedalkalin

ityRe

quire

dlong

resid

ence

time

Verticalflo

wwetland

(VFW

)Net-acidicw

ater

with

high

AlFe

andDO

Limestoneorganicmatter

SulfateandFe

redu

ction

acid

neutralization

Highcapitalcostpo

tentialfor

armoringandplug

ging

with

hydroxides

Sulfateredu

cing

bioreactor

(SRB

)Sm

allfl

owso

rtosituatio

nsvery

acidicandmetalric

hwater

Organicsubstrates

uchas

hay

alfalfasaw

dust

paper

woo

dchipscrushed

limestone

andcompo

stor

manure

Microbialsulfateredu

ction

Highcapitalcostextre

mely

low

pHseverelyim

pactthee

fficiency

ofSredu

cing

bacteria

Pyrolusitelim

estone

beds

Mod

eratep

Handwhere

majority

ofacidity

isrelated

toMn

Limestoneorganicsubstrate

aerobicm

icroorganism

Hydrolysis

ofMn

Not

suitablefor

drainage

which

contains

high

Fehigh

maintenance

Perm

eabler

eactiveb

arrie

rs(PRB

)Groun

dwaterlow

DO

Organicmatterlim

estonezero

valent

iron

Sulfateredu

ction

sulfide

precipitates

neutralization

Iron

-oxidizing

bioreactor

Acidicwater

Fe-oxidizing

bacteriaand

archaea

Feoxidation

Phytorem

ediatio

nAny

AMD-im

pacted

sites

Metaltolerant

plantspecies

Phytoextractionand

phytostabilization

Successd

epends

onthep

roper

selectionof

the

metal-hyperaccumulator

plant

BioMed Research International 5

Table1Con

tinued

Syste

mtype

Applicability

Supp

ortm

aterials

Mechanism

sLimitatio

nGeochem

ical

Ano

xiclim

estone

drain(A

LD)

Acidicwater

with

lowAlFeD

OLimestone

gravel

compacted

soil

Limestone

dissolution

raise

pH

precipitatio

n

Fe-oxide

armoringlim

estone

limitperm

eabilityandcause

plug

ging

Alkalinity

prod

ucingsyste

m(A

PS)

Acidicwater

Organicmatterlim

estone

Ano

xicc

onditio

nneutralization

precipitatio

n

Openlim

estone

channel(OLC

)Re

quire

dste

epslo

pesnet-a

cidic

water

with

high

AlFe

andDO

Limestone

Limestone

dissolution

neutralization

Arm

oringor

thec

oatin

gof

the

limestonelarge

amou

ntis

neededdecreases

the

neutralizingcapacity

Limestone

leachbed(LLB

)Lo

wpH

andmetal-fr

eewater

Limestone

Limestone

dissolution

neutralization

Arm

oringwith

Fehydroxides

Steel-slagleachbed(SLB

)Highlyacidicandmetal-fr

eewater

Steelslag

Raise

alkalin

ityneutralization

Not

suitablefor

metal-la

den

water

Limestone

diversionwe

lls(LDW)

Sitesthato

ffera

suitable

topo

graphicalfall

Crushedlim

estone

aggregate

Hydraulicforcehydrolysis

and

neutralization

Requ

iredrefillin

gwith

limestone

every2ndash4weeks

Limestone

sand

Stream

flowwater

Sand

-sized

limestone

neutralizingacid

Coatin

gof

limestone

Low-pHFe

oxidationchannels

Shallowchannels

Limestone

orsand

stone

aggregate

Feoxidation

adsorptio

nand

coprecipitatio

n

Itremoves

someF

ebu

trem

oval

efficiency

hasn

otbeen

determ

ined

Sulfide

passivationmicroencapsulation

Pitw

allfacessulfid

ebearin

gwastesrocks

piles

Inorganicc

oatin

gph

osph

ate

silicafly

ashlim

estoneorganic

coatinghu

micacidlipids

polyethylene

polyam

ine

alkoxysilanesfattyacidoxalic

acidcatecho

l

Preventsulfid

eoxidatio

nby

inorganica

ndorganicc

oatin

g

Long

-term

effectiv

enessisstillin

questio

norganicc

oatin

gexpensive

Electro

chem

icalcover

Tailing

wasterock

Con

ductives

teelmeshcathod

emetalanod

eRe

ducing

DOby

electrochem

ical

process

Highcapitalcosto

fano

desno

inform

ationavailableo

nlarge

scalea

pplication

6 BioMed Research International

Table1Con

tinued

Syste

mtype

Applicability

Supp

ortm

aterials

Mechanism

sLimitatio

nPh

ysica

l

Dry

cover

Sulfide

bearingwastesrockpiles

Fine-grained

soilorganic

materials

synthetic

material

(plasticliners)vegetation

Minim

izeo

xidatio

nby

physical

barrierneutralization

precipitates

Shortterm

effectiv

eness

Wetcover

Sulfide

wastes

Und

erwater

Disp

osingwasteun

derw

ater

anoxiccond

ition

sRe

quire

rigorou

seng

ineerin

gdesig

nhigh

maintenance

Gas

redo

xanddisplacement

syste

m(G

aRDS)

Und

ergrou

ndmines

CO2andCH4gas

Gas

mixturesp

hysic

allydisplace

O2

Itson

lyfeasiblewhere

partialor

completefl

ooding

isno

tfeasib

le

BioMed Research International 7

MetalSuldes(ZnS)

Air

Excess

Sulfur

Puriedeuent

Recycle

Neu

troph

ilic

SRB

Bior

eact

or o

ne

Bior

eact

or tw

oSu

lde

oxid

ising

bac

teriaWaste water or

process water(34

2minus and metalssuch as H

2+)

(2-rich gas

2

(3minus

(3I)

34

2minus+ 4(2 + (

+rarr (3

minus+ 4(2

H2+

+ (3minusrarr H3 + (

+

2(3minus+ 2 + 2(

+rarr 23

I+ 2(2

(a)

Bior

eact

orsta

ge I

Stag

e II

Ana

erob

ic ag

itate

dco

ntac

tor

SulfurReagents

Feed water(AMD)

sulfu

r red

ucin

g ba

cter

ia

ClarierTreated water

Filter

Metal sulde (ZnS)to smelter

(23

Gen

erat

ion

by

(23

(b)

Figure 2 Schematic overview of the Thiopaq (a) and Biosulfide (b) processes (adapted from Adams et al [12] Muyzer and Stams [13])

simpler engineering designs and reduce operational costs byusing single on-line reactor vessels that could be used to bothgenerate sulfide and selectively precipitate target metal(s)Precipitation and removal of many soluble transition metalsoften present in AMD emanating from metal mines maybe achieved by ready biomineralization as their sulfides Theproduced metal sulfides have different solubilities thereforemetals can be precipitated together or selectively by con-trolling concentrations of the key reactant S2minus which maybe achieved by controlling pH (S2minus + H+ harr HSminus) Coppersulfide for example is far less soluble than ferrous sulfide(respective log Ksp values of minus359 and minus188) and thereforeCuS precipitates at pH 2 whereas FeS needs much higher pHto precipitate Diez-Ercilla et al [31] have also demonstratedthat selective precipitation of metal sulfides occurs naturallyin Cueva de la Mora pit lake (SW Spain) and the geochemicalcalculations match perfectly with the results of chemicaland mineralogical composition Nancucheo and Johnson[3] showed that it was possible to selectively precipitate

stable metal sulfides in inline reactor vessel testing twosynthetic AMDs in acidic conditions (pH 22ndash48) In the firstbioreactor with a composition of feeding similar to AMD atthe abandoned Cwm Rheidol lead-zinc mine in mid-Waleszinc was efficiently precipitated (gt99) as sulfide inside thereactor while both aluminum and ferrous iron remain insolution (gt99) and were washed out of the reactor vesselThe second sulfidogenic bioreactor was challenged with asynthetic AMD based on that from Mynydd Parys NorthWales Throughout the test period all the copper presentin the feed liquor was precipitated (confirmed as coppersulfide) within the bioreactor but none of the ferrous ironwas present in the solids Although the initial pH at whichthe bioreactor was operated (from pH 36 to 25) causedsome coprecipitation of zinc with the copper by progressivelylowering the bioreactor pH and the concentration of theelectron donor in the influent liquor it was possible toprecipitate gt99 of the copper within the bioreactor as CuSand to maintain gt99 of the zinc iron and aluminum in

8 BioMed Research International

solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]

4C3H8O3+ 10H+ + 7SO

4

2minus+ Cu2+ + Zn2+ + Fe2+

997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H

2O

(1)

This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD

Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H

2S) by the SRB and orpiment

(As2S3) generated within the bioreactor In addition this

process was also observed to occur naturally in an acidic pitlake [31]

Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for

the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes

3 Microbiology in Remediating AcidicMine Waters

Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]

Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents

BioMed Research International 9

Table2Isolated

sulfido

genicm

icroorganism

sand

theirm

aincharacteris

tics

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermocladium

modestiu

s45ndash82

(75)

26ndash

59(40)

Glycogen

starch

proteins

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

mud

)Japan

[43ndash45]

Caldivirg

amaquilin

gensis

70ndash9

023ndash64(37ndash4

2)

Glycogen

beefextract

pepton

etryptoneyeast

extract

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

solfataric

soilmud

)Mt

Maquilin

gPh

ilipp

ines

[46]

Archaeoglobu

slithotro

phicu

snd

60

Acetate

SulfateL-cysteine

nd[4748]

Archaeoglobu

sveneficus

nd69

H2acetateformate

pyruvateyeastextract

citratelactatesta

rch

pepton

e

Sulfitethiosulfate

Wallsof

activ

eblack

smoker

atmiddle

AtlanticRidge

[44]

Archaeoglobu

sprofund

usnd

45ndash75

H2acetatepyruvate

yeastextractlactate

meatextractpeptone

crud

eoilwith

acetate

Sulfatethiosulfate

sulfite

Deepseah

ydrothermal

syste

moff

Guaym

as

Mexico

[4950]

Archaeoglobu

sfulgidu

s60ndash75

(70)

55ndash75

(60)

H2C

O2formate

form

amideD(minus)-and

L(+)-lactateglucose

starchcalam

inea

cids

pepton

egelatincasein

meatextractyeast

extract

Sulfatethiosulfate

sulfite

Marineh

ydrothermal

syste

mN

eron

eIta

ly[4951]

Thermodesulfatatorind

icus

55ndash80

(70)

60ndash

67(625)

H2C

O2stim

ulated

bymethano

lmon

omethylamine

glutam

atepepton

efumaratetryptone

isobu

tyrate3-C

H3

butyrateethanol

prop

anolandlow

amou

ntso

facetate

Sulfate

Marineh

ydrothermal

syste

mC

entralIndian

Ridge

[52]

Thermodesulfobacterium

hydrogeniphilum

50ndash80

(75)

63ndash68(65)

H2C

O2stim

ulated

byacetatefumarate

3-methylbutyrate

glutam

ateyeastextract

pepton

eortrypton

e

Sulfate

Marineh

ydrothermal

syste

mG

uaym

asBa

sin[53]

10 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermodesulfobacterium

commun

e41ndash83

60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA[5455]

Thermodesulfobacterium

thermophilum

nd60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

nd[55]

Thermodesulfobacterium

hveragerdense

7545ndash70

(70)

H2pyruvatelactate

Sulfatesulfite

Hot

sprin

gs(m

icrobial

mats)Iceland

[56]

Thermodesulfobium

narugense

6940ndash

60(55ndash6

0)

H2C

O2

Sulfaten

itrate

thiosulfate

Hot

sprin

gs(m

icrobial

mats)Japan

[57]

Desulfotomaculum

spp(30

species)

nd23ndash55

H2C

O2formatesome

(organicacidslip

idsor

mon

oaromatic

hydrocarbo

ns)

Sulfidesulfur

thiosulfateA

cetate

some(Fe

(III)Mn(IV)

U(V

I)or

Cr(V

I))

Subsurface

environm

ents

rice

fieldsminesoilspills

[58ndash62]

Desulfosporosinus

meridiei

10ndash37

61ndash75

H2C

O2acetatesom

e(la

ctatepyruvate

ethano

l)Sulfatesom

e(nitrate)

Groun

dwater

contam

inated

with

polycyclica

romatic

hydrocarbo

nsinSw

anCoastalPlain

Australia

[63]

Desulfosporosinus

youn

gii

8ndash39

(32ndash35)

57ndash82(70ndash

73)

Beefextractyeast

extractform

ate

succinatelactate

pyruvateethanoland

toluene

Fumaratesulfatesulfite

thiosulfate

Artificialwetland

(sedim

ent)

[64]

BioMed Research International 11

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfosporosinus

orien

tis37ndash4

860ndash

65

H2C

O2formate

lactatepyruvatem

alate

fumaratesuccinate

methano

lethano

lprop

anolbutanol

butyratevalerate

palm

itate

Sulfatesulfite

thiosulfatesulfur

nd[65]

Desulfosporom

usapolytro

pa4ndash

3761ndash80

H2C

O2formate

lactatebu

tyrateseveral

alcoho

lsorganica

cids

carboh

ydratessome

aminoacidscholine

betaine

SulfateFe(OH) 3

Oligotroph

iclake

(sedim

ent)

German

[66]

Thermodesulfovibrio

yellowstonii

41ndash83

60ndash

80(70)

H2C

O2acetate

form

atelactate

pyruvate

Sulfatethiosulfate

sulfite

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA

[67]

Thermodesulfovibrio

islandicus

5545ndash70

(70)

H2pyruvatelactate

form

ate

Sulfaten

itrate

Bioreactor

inoculated

with

hotsprings

(microbialmats)sample

Iceland

[56]

Desulfohalobium

spp(6

species)

nd55ndash80(65ndash70)

H2lactateethanol

acetate

Sulfite

hypersaline

environm

ents

[6869]

Desulfocaldus

terraneus

58nd

H2C

O2aminoacids

proteinaceou

ssub

strates

andorganica

cids

prod

ucingethano

lacetateprop

ionate

isovalerate2-

methylbutyrate

Cystinesulfu

rsulfate

Seao

ilfacilitiesAlaksa

[70]

12 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfomicrobium

spp(4

species)

25ndash30

ndH2lactatepyruvate

Ethano

lform

ate

Sulfatesulfoxyanions

Anaerob

icsediments

(Freshwaterbrackish

marine)anaerob

icstrata

oroverlyingwaterand

insaturatedmineralor

organicd

eposits

[5469]

Desulfonatro

novibrio

hydrogenovoran

s37ndash4

090

ndash102(90ndash97)

H2formate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[71]

Desulfonatro

num

spp(3

species)

20ndash4

5(37ndash45)

80ndash

100(90)

H2form

ateYeast

extractethano

llactate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[72]

Desulfovibriospp(47

species)

25ndash4

4(25ndash35)

ndH2C

O2acetatelactate

carboh

ydrates

Sulfaten

itrate

nd[73]

Desulfomonile

spp(2

species)

30ndash30

(37)

65ndash78

(68ndash70)

H2C

O2benzoate

pyruvateorganic

carbon

halogens

Sulfatesulfite

thiosulfatesulfurFe

(III)NitrateU(V

I)Slud

ge[74]

Syntroph

obacteraceae

(8genera)

31ndash6

070

ndash75

H2C

O2acetate

form

atelactate

pyruvate

Sulfatesulfite

thiosulfate

Sewages

ludge

freshwaterbrackish

marines

edim

ent

marineh

ydrothermal

ventsho

tspring

sediments

[7375]

Desulfobacterium

anilini

3069ndash

75H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

BioMed Research International 13

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfarculus

baarsii

35ndash39

73H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

Desulfobacteraceae(12

genera)

10ndash4

0nd

H2C

O2L

ong-chain

fatty

acidsAlcoh

ols

Polara

romatic

compo

undsand

insome

casese

venAlip

hatic

arom

atichydrocarbo

ns

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[77]

Desulfosporosinus

acidophilus

25ndash4

036ndash

52(52)

H2lactatepyruvate

glycerolglucose

and

fructose

Sulfate

Sedimentfrom

anacid

effluent

pond

[26]

Desulfosporosinus

acididuran

s15ndash4

038ndash70

(55)

H2formatelactate

butyratefum

arate

malatepyruvate

glycerolm

ethano

lethano

lyeastextract

xyloseglucosefructose

Ferriciro

nnitrate

sulfateelem

entalsulfur

thiosulfate

Whiteriv

erdraining

from

theS

oufriere

hills

inMon

serrat(pH32)

[78]

a Valuesc

losedby

parenthesis

arec

onsid

ered

optim

alpH

ndno

tinformed

byconsultedreference

14 BioMed Research International

such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO

2[33]

In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO

2and H

2[17]

D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]

4 Natural Attenuation for the Design of AMDRemediation Strategies

Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and

chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH

2O)were detected presumably due

to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not

Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]

5 Concluding Remarks

Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools

Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico

BioMed Research International 15

(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)

References

[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013

[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014

[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012

[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008

[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011

[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003

[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000

[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014

[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006

[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005

[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007

[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008

[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008

[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015

[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013

[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006

[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006

[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014

[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008

[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006

[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010

[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005

[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016

[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999

[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001

[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010

[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990

[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016

[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014

[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009

[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

BioMed Research International 5

Table1Con

tinued

Syste

mtype

Applicability

Supp

ortm

aterials

Mechanism

sLimitatio

nGeochem

ical

Ano

xiclim

estone

drain(A

LD)

Acidicwater

with

lowAlFeD

OLimestone

gravel

compacted

soil

Limestone

dissolution

raise

pH

precipitatio

n

Fe-oxide

armoringlim

estone

limitperm

eabilityandcause

plug

ging

Alkalinity

prod

ucingsyste

m(A

PS)

Acidicwater

Organicmatterlim

estone

Ano

xicc

onditio

nneutralization

precipitatio

n

Openlim

estone

channel(OLC

)Re

quire

dste

epslo

pesnet-a

cidic

water

with

high

AlFe

andDO

Limestone

Limestone

dissolution

neutralization

Arm

oringor

thec

oatin

gof

the

limestonelarge

amou

ntis

neededdecreases

the

neutralizingcapacity

Limestone

leachbed(LLB

)Lo

wpH

andmetal-fr

eewater

Limestone

Limestone

dissolution

neutralization

Arm

oringwith

Fehydroxides

Steel-slagleachbed(SLB

)Highlyacidicandmetal-fr

eewater

Steelslag

Raise

alkalin

ityneutralization

Not

suitablefor

metal-la

den

water

Limestone

diversionwe

lls(LDW)

Sitesthato

ffera

suitable

topo

graphicalfall

Crushedlim

estone

aggregate

Hydraulicforcehydrolysis

and

neutralization

Requ

iredrefillin

gwith

limestone

every2ndash4weeks

Limestone

sand

Stream

flowwater

Sand

-sized

limestone

neutralizingacid

Coatin

gof

limestone

Low-pHFe

oxidationchannels

Shallowchannels

Limestone

orsand

stone

aggregate

Feoxidation

adsorptio

nand

coprecipitatio

n

Itremoves

someF

ebu

trem

oval

efficiency

hasn

otbeen

determ

ined

Sulfide

passivationmicroencapsulation

Pitw

allfacessulfid

ebearin

gwastesrocks

piles

Inorganicc

oatin

gph

osph

ate

silicafly

ashlim

estoneorganic

coatinghu

micacidlipids

polyethylene

polyam

ine

alkoxysilanesfattyacidoxalic

acidcatecho

l

Preventsulfid

eoxidatio

nby

inorganica

ndorganicc

oatin

g

Long

-term

effectiv

enessisstillin

questio

norganicc

oatin

gexpensive

Electro

chem

icalcover

Tailing

wasterock

Con

ductives

teelmeshcathod

emetalanod

eRe

ducing

DOby

electrochem

ical

process

Highcapitalcosto

fano

desno

inform

ationavailableo

nlarge

scalea

pplication

6 BioMed Research International

Table1Con

tinued

Syste

mtype

Applicability

Supp

ortm

aterials

Mechanism

sLimitatio

nPh

ysica

l

Dry

cover

Sulfide

bearingwastesrockpiles

Fine-grained

soilorganic

materials

synthetic

material

(plasticliners)vegetation

Minim

izeo

xidatio

nby

physical

barrierneutralization

precipitates

Shortterm

effectiv

eness

Wetcover

Sulfide

wastes

Und

erwater

Disp

osingwasteun

derw

ater

anoxiccond

ition

sRe

quire

rigorou

seng

ineerin

gdesig

nhigh

maintenance

Gas

redo

xanddisplacement

syste

m(G

aRDS)

Und

ergrou

ndmines

CO2andCH4gas

Gas

mixturesp

hysic

allydisplace

O2

Itson

lyfeasiblewhere

partialor

completefl

ooding

isno

tfeasib

le

BioMed Research International 7

MetalSuldes(ZnS)

Air

Excess

Sulfur

Puriedeuent

Recycle

Neu

troph

ilic

SRB

Bior

eact

or o

ne

Bior

eact

or tw

oSu

lde

oxid

ising

bac

teriaWaste water or

process water(34

2minus and metalssuch as H

2+)

(2-rich gas

2

(3minus

(3I)

34

2minus+ 4(2 + (

+rarr (3

minus+ 4(2

H2+

+ (3minusrarr H3 + (

+

2(3minus+ 2 + 2(

+rarr 23

I+ 2(2

(a)

Bior

eact

orsta

ge I

Stag

e II

Ana

erob

ic ag

itate

dco

ntac

tor

SulfurReagents

Feed water(AMD)

sulfu

r red

ucin

g ba

cter

ia

ClarierTreated water

Filter

Metal sulde (ZnS)to smelter

(23

Gen

erat

ion

by

(23

(b)

Figure 2 Schematic overview of the Thiopaq (a) and Biosulfide (b) processes (adapted from Adams et al [12] Muyzer and Stams [13])

simpler engineering designs and reduce operational costs byusing single on-line reactor vessels that could be used to bothgenerate sulfide and selectively precipitate target metal(s)Precipitation and removal of many soluble transition metalsoften present in AMD emanating from metal mines maybe achieved by ready biomineralization as their sulfides Theproduced metal sulfides have different solubilities thereforemetals can be precipitated together or selectively by con-trolling concentrations of the key reactant S2minus which maybe achieved by controlling pH (S2minus + H+ harr HSminus) Coppersulfide for example is far less soluble than ferrous sulfide(respective log Ksp values of minus359 and minus188) and thereforeCuS precipitates at pH 2 whereas FeS needs much higher pHto precipitate Diez-Ercilla et al [31] have also demonstratedthat selective precipitation of metal sulfides occurs naturallyin Cueva de la Mora pit lake (SW Spain) and the geochemicalcalculations match perfectly with the results of chemicaland mineralogical composition Nancucheo and Johnson[3] showed that it was possible to selectively precipitate

stable metal sulfides in inline reactor vessel testing twosynthetic AMDs in acidic conditions (pH 22ndash48) In the firstbioreactor with a composition of feeding similar to AMD atthe abandoned Cwm Rheidol lead-zinc mine in mid-Waleszinc was efficiently precipitated (gt99) as sulfide inside thereactor while both aluminum and ferrous iron remain insolution (gt99) and were washed out of the reactor vesselThe second sulfidogenic bioreactor was challenged with asynthetic AMD based on that from Mynydd Parys NorthWales Throughout the test period all the copper presentin the feed liquor was precipitated (confirmed as coppersulfide) within the bioreactor but none of the ferrous ironwas present in the solids Although the initial pH at whichthe bioreactor was operated (from pH 36 to 25) causedsome coprecipitation of zinc with the copper by progressivelylowering the bioreactor pH and the concentration of theelectron donor in the influent liquor it was possible toprecipitate gt99 of the copper within the bioreactor as CuSand to maintain gt99 of the zinc iron and aluminum in

8 BioMed Research International

solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]

4C3H8O3+ 10H+ + 7SO

4

2minus+ Cu2+ + Zn2+ + Fe2+

997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H

2O

(1)

This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD

Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H

2S) by the SRB and orpiment

(As2S3) generated within the bioreactor In addition this

process was also observed to occur naturally in an acidic pitlake [31]

Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for

the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes

3 Microbiology in Remediating AcidicMine Waters

Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]

Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents

BioMed Research International 9

Table2Isolated

sulfido

genicm

icroorganism

sand

theirm

aincharacteris

tics

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermocladium

modestiu

s45ndash82

(75)

26ndash

59(40)

Glycogen

starch

proteins

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

mud

)Japan

[43ndash45]

Caldivirg

amaquilin

gensis

70ndash9

023ndash64(37ndash4

2)

Glycogen

beefextract

pepton

etryptoneyeast

extract

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

solfataric

soilmud

)Mt

Maquilin

gPh

ilipp

ines

[46]

Archaeoglobu

slithotro

phicu

snd

60

Acetate

SulfateL-cysteine

nd[4748]

Archaeoglobu

sveneficus

nd69

H2acetateformate

pyruvateyeastextract

citratelactatesta

rch

pepton

e

Sulfitethiosulfate

Wallsof

activ

eblack

smoker

atmiddle

AtlanticRidge

[44]

Archaeoglobu

sprofund

usnd

45ndash75

H2acetatepyruvate

yeastextractlactate

meatextractpeptone

crud

eoilwith

acetate

Sulfatethiosulfate

sulfite

Deepseah

ydrothermal

syste

moff

Guaym

as

Mexico

[4950]

Archaeoglobu

sfulgidu

s60ndash75

(70)

55ndash75

(60)

H2C

O2formate

form

amideD(minus)-and

L(+)-lactateglucose

starchcalam

inea

cids

pepton

egelatincasein

meatextractyeast

extract

Sulfatethiosulfate

sulfite

Marineh

ydrothermal

syste

mN

eron

eIta

ly[4951]

Thermodesulfatatorind

icus

55ndash80

(70)

60ndash

67(625)

H2C

O2stim

ulated

bymethano

lmon

omethylamine

glutam

atepepton

efumaratetryptone

isobu

tyrate3-C

H3

butyrateethanol

prop

anolandlow

amou

ntso

facetate

Sulfate

Marineh

ydrothermal

syste

mC

entralIndian

Ridge

[52]

Thermodesulfobacterium

hydrogeniphilum

50ndash80

(75)

63ndash68(65)

H2C

O2stim

ulated

byacetatefumarate

3-methylbutyrate

glutam

ateyeastextract

pepton

eortrypton

e

Sulfate

Marineh

ydrothermal

syste

mG

uaym

asBa

sin[53]

10 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermodesulfobacterium

commun

e41ndash83

60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA[5455]

Thermodesulfobacterium

thermophilum

nd60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

nd[55]

Thermodesulfobacterium

hveragerdense

7545ndash70

(70)

H2pyruvatelactate

Sulfatesulfite

Hot

sprin

gs(m

icrobial

mats)Iceland

[56]

Thermodesulfobium

narugense

6940ndash

60(55ndash6

0)

H2C

O2

Sulfaten

itrate

thiosulfate

Hot

sprin

gs(m

icrobial

mats)Japan

[57]

Desulfotomaculum

spp(30

species)

nd23ndash55

H2C

O2formatesome

(organicacidslip

idsor

mon

oaromatic

hydrocarbo

ns)

Sulfidesulfur

thiosulfateA

cetate

some(Fe

(III)Mn(IV)

U(V

I)or

Cr(V

I))

Subsurface

environm

ents

rice

fieldsminesoilspills

[58ndash62]

Desulfosporosinus

meridiei

10ndash37

61ndash75

H2C

O2acetatesom

e(la

ctatepyruvate

ethano

l)Sulfatesom

e(nitrate)

Groun

dwater

contam

inated

with

polycyclica

romatic

hydrocarbo

nsinSw

anCoastalPlain

Australia

[63]

Desulfosporosinus

youn

gii

8ndash39

(32ndash35)

57ndash82(70ndash

73)

Beefextractyeast

extractform

ate

succinatelactate

pyruvateethanoland

toluene

Fumaratesulfatesulfite

thiosulfate

Artificialwetland

(sedim

ent)

[64]

BioMed Research International 11

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfosporosinus

orien

tis37ndash4

860ndash

65

H2C

O2formate

lactatepyruvatem

alate

fumaratesuccinate

methano

lethano

lprop

anolbutanol

butyratevalerate

palm

itate

Sulfatesulfite

thiosulfatesulfur

nd[65]

Desulfosporom

usapolytro

pa4ndash

3761ndash80

H2C

O2formate

lactatebu

tyrateseveral

alcoho

lsorganica

cids

carboh

ydratessome

aminoacidscholine

betaine

SulfateFe(OH) 3

Oligotroph

iclake

(sedim

ent)

German

[66]

Thermodesulfovibrio

yellowstonii

41ndash83

60ndash

80(70)

H2C

O2acetate

form

atelactate

pyruvate

Sulfatethiosulfate

sulfite

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA

[67]

Thermodesulfovibrio

islandicus

5545ndash70

(70)

H2pyruvatelactate

form

ate

Sulfaten

itrate

Bioreactor

inoculated

with

hotsprings

(microbialmats)sample

Iceland

[56]

Desulfohalobium

spp(6

species)

nd55ndash80(65ndash70)

H2lactateethanol

acetate

Sulfite

hypersaline

environm

ents

[6869]

Desulfocaldus

terraneus

58nd

H2C

O2aminoacids

proteinaceou

ssub

strates

andorganica

cids

prod

ucingethano

lacetateprop

ionate

isovalerate2-

methylbutyrate

Cystinesulfu

rsulfate

Seao

ilfacilitiesAlaksa

[70]

12 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfomicrobium

spp(4

species)

25ndash30

ndH2lactatepyruvate

Ethano

lform

ate

Sulfatesulfoxyanions

Anaerob

icsediments

(Freshwaterbrackish

marine)anaerob

icstrata

oroverlyingwaterand

insaturatedmineralor

organicd

eposits

[5469]

Desulfonatro

novibrio

hydrogenovoran

s37ndash4

090

ndash102(90ndash97)

H2formate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[71]

Desulfonatro

num

spp(3

species)

20ndash4

5(37ndash45)

80ndash

100(90)

H2form

ateYeast

extractethano

llactate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[72]

Desulfovibriospp(47

species)

25ndash4

4(25ndash35)

ndH2C

O2acetatelactate

carboh

ydrates

Sulfaten

itrate

nd[73]

Desulfomonile

spp(2

species)

30ndash30

(37)

65ndash78

(68ndash70)

H2C

O2benzoate

pyruvateorganic

carbon

halogens

Sulfatesulfite

thiosulfatesulfurFe

(III)NitrateU(V

I)Slud

ge[74]

Syntroph

obacteraceae

(8genera)

31ndash6

070

ndash75

H2C

O2acetate

form

atelactate

pyruvate

Sulfatesulfite

thiosulfate

Sewages

ludge

freshwaterbrackish

marines

edim

ent

marineh

ydrothermal

ventsho

tspring

sediments

[7375]

Desulfobacterium

anilini

3069ndash

75H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

BioMed Research International 13

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfarculus

baarsii

35ndash39

73H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

Desulfobacteraceae(12

genera)

10ndash4

0nd

H2C

O2L

ong-chain

fatty

acidsAlcoh

ols

Polara

romatic

compo

undsand

insome

casese

venAlip

hatic

arom

atichydrocarbo

ns

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[77]

Desulfosporosinus

acidophilus

25ndash4

036ndash

52(52)

H2lactatepyruvate

glycerolglucose

and

fructose

Sulfate

Sedimentfrom

anacid

effluent

pond

[26]

Desulfosporosinus

acididuran

s15ndash4

038ndash70

(55)

H2formatelactate

butyratefum

arate

malatepyruvate

glycerolm

ethano

lethano

lyeastextract

xyloseglucosefructose

Ferriciro

nnitrate

sulfateelem

entalsulfur

thiosulfate

Whiteriv

erdraining

from

theS

oufriere

hills

inMon

serrat(pH32)

[78]

a Valuesc

losedby

parenthesis

arec

onsid

ered

optim

alpH

ndno

tinformed

byconsultedreference

14 BioMed Research International

such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO

2[33]

In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO

2and H

2[17]

D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]

4 Natural Attenuation for the Design of AMDRemediation Strategies

Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and

chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH

2O)were detected presumably due

to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not

Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]

5 Concluding Remarks

Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools

Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico

BioMed Research International 15

(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)

References

[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013

[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014

[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012

[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008

[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011

[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003

[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000

[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014

[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006

[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005

[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007

[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008

[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008

[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015

[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013

[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006

[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006

[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014

[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008

[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006

[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010

[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005

[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016

[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999

[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001

[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010

[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990

[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016

[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014

[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009

[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

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BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

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BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Virolog y

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Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

6 BioMed Research International

Table1Con

tinued

Syste

mtype

Applicability

Supp

ortm

aterials

Mechanism

sLimitatio

nPh

ysica

l

Dry

cover

Sulfide

bearingwastesrockpiles

Fine-grained

soilorganic

materials

synthetic

material

(plasticliners)vegetation

Minim

izeo

xidatio

nby

physical

barrierneutralization

precipitates

Shortterm

effectiv

eness

Wetcover

Sulfide

wastes

Und

erwater

Disp

osingwasteun

derw

ater

anoxiccond

ition

sRe

quire

rigorou

seng

ineerin

gdesig

nhigh

maintenance

Gas

redo

xanddisplacement

syste

m(G

aRDS)

Und

ergrou

ndmines

CO2andCH4gas

Gas

mixturesp

hysic

allydisplace

O2

Itson

lyfeasiblewhere

partialor

completefl

ooding

isno

tfeasib

le

BioMed Research International 7

MetalSuldes(ZnS)

Air

Excess

Sulfur

Puriedeuent

Recycle

Neu

troph

ilic

SRB

Bior

eact

or o

ne

Bior

eact

or tw

oSu

lde

oxid

ising

bac

teriaWaste water or

process water(34

2minus and metalssuch as H

2+)

(2-rich gas

2

(3minus

(3I)

34

2minus+ 4(2 + (

+rarr (3

minus+ 4(2

H2+

+ (3minusrarr H3 + (

+

2(3minus+ 2 + 2(

+rarr 23

I+ 2(2

(a)

Bior

eact

orsta

ge I

Stag

e II

Ana

erob

ic ag

itate

dco

ntac

tor

SulfurReagents

Feed water(AMD)

sulfu

r red

ucin

g ba

cter

ia

ClarierTreated water

Filter

Metal sulde (ZnS)to smelter

(23

Gen

erat

ion

by

(23

(b)

Figure 2 Schematic overview of the Thiopaq (a) and Biosulfide (b) processes (adapted from Adams et al [12] Muyzer and Stams [13])

simpler engineering designs and reduce operational costs byusing single on-line reactor vessels that could be used to bothgenerate sulfide and selectively precipitate target metal(s)Precipitation and removal of many soluble transition metalsoften present in AMD emanating from metal mines maybe achieved by ready biomineralization as their sulfides Theproduced metal sulfides have different solubilities thereforemetals can be precipitated together or selectively by con-trolling concentrations of the key reactant S2minus which maybe achieved by controlling pH (S2minus + H+ harr HSminus) Coppersulfide for example is far less soluble than ferrous sulfide(respective log Ksp values of minus359 and minus188) and thereforeCuS precipitates at pH 2 whereas FeS needs much higher pHto precipitate Diez-Ercilla et al [31] have also demonstratedthat selective precipitation of metal sulfides occurs naturallyin Cueva de la Mora pit lake (SW Spain) and the geochemicalcalculations match perfectly with the results of chemicaland mineralogical composition Nancucheo and Johnson[3] showed that it was possible to selectively precipitate

stable metal sulfides in inline reactor vessel testing twosynthetic AMDs in acidic conditions (pH 22ndash48) In the firstbioreactor with a composition of feeding similar to AMD atthe abandoned Cwm Rheidol lead-zinc mine in mid-Waleszinc was efficiently precipitated (gt99) as sulfide inside thereactor while both aluminum and ferrous iron remain insolution (gt99) and were washed out of the reactor vesselThe second sulfidogenic bioreactor was challenged with asynthetic AMD based on that from Mynydd Parys NorthWales Throughout the test period all the copper presentin the feed liquor was precipitated (confirmed as coppersulfide) within the bioreactor but none of the ferrous ironwas present in the solids Although the initial pH at whichthe bioreactor was operated (from pH 36 to 25) causedsome coprecipitation of zinc with the copper by progressivelylowering the bioreactor pH and the concentration of theelectron donor in the influent liquor it was possible toprecipitate gt99 of the copper within the bioreactor as CuSand to maintain gt99 of the zinc iron and aluminum in

8 BioMed Research International

solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]

4C3H8O3+ 10H+ + 7SO

4

2minus+ Cu2+ + Zn2+ + Fe2+

997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H

2O

(1)

This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD

Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H

2S) by the SRB and orpiment

(As2S3) generated within the bioreactor In addition this

process was also observed to occur naturally in an acidic pitlake [31]

Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for

the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes

3 Microbiology in Remediating AcidicMine Waters

Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]

Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents

BioMed Research International 9

Table2Isolated

sulfido

genicm

icroorganism

sand

theirm

aincharacteris

tics

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermocladium

modestiu

s45ndash82

(75)

26ndash

59(40)

Glycogen

starch

proteins

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

mud

)Japan

[43ndash45]

Caldivirg

amaquilin

gensis

70ndash9

023ndash64(37ndash4

2)

Glycogen

beefextract

pepton

etryptoneyeast

extract

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

solfataric

soilmud

)Mt

Maquilin

gPh

ilipp

ines

[46]

Archaeoglobu

slithotro

phicu

snd

60

Acetate

SulfateL-cysteine

nd[4748]

Archaeoglobu

sveneficus

nd69

H2acetateformate

pyruvateyeastextract

citratelactatesta

rch

pepton

e

Sulfitethiosulfate

Wallsof

activ

eblack

smoker

atmiddle

AtlanticRidge

[44]

Archaeoglobu

sprofund

usnd

45ndash75

H2acetatepyruvate

yeastextractlactate

meatextractpeptone

crud

eoilwith

acetate

Sulfatethiosulfate

sulfite

Deepseah

ydrothermal

syste

moff

Guaym

as

Mexico

[4950]

Archaeoglobu

sfulgidu

s60ndash75

(70)

55ndash75

(60)

H2C

O2formate

form

amideD(minus)-and

L(+)-lactateglucose

starchcalam

inea

cids

pepton

egelatincasein

meatextractyeast

extract

Sulfatethiosulfate

sulfite

Marineh

ydrothermal

syste

mN

eron

eIta

ly[4951]

Thermodesulfatatorind

icus

55ndash80

(70)

60ndash

67(625)

H2C

O2stim

ulated

bymethano

lmon

omethylamine

glutam

atepepton

efumaratetryptone

isobu

tyrate3-C

H3

butyrateethanol

prop

anolandlow

amou

ntso

facetate

Sulfate

Marineh

ydrothermal

syste

mC

entralIndian

Ridge

[52]

Thermodesulfobacterium

hydrogeniphilum

50ndash80

(75)

63ndash68(65)

H2C

O2stim

ulated

byacetatefumarate

3-methylbutyrate

glutam

ateyeastextract

pepton

eortrypton

e

Sulfate

Marineh

ydrothermal

syste

mG

uaym

asBa

sin[53]

10 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermodesulfobacterium

commun

e41ndash83

60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA[5455]

Thermodesulfobacterium

thermophilum

nd60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

nd[55]

Thermodesulfobacterium

hveragerdense

7545ndash70

(70)

H2pyruvatelactate

Sulfatesulfite

Hot

sprin

gs(m

icrobial

mats)Iceland

[56]

Thermodesulfobium

narugense

6940ndash

60(55ndash6

0)

H2C

O2

Sulfaten

itrate

thiosulfate

Hot

sprin

gs(m

icrobial

mats)Japan

[57]

Desulfotomaculum

spp(30

species)

nd23ndash55

H2C

O2formatesome

(organicacidslip

idsor

mon

oaromatic

hydrocarbo

ns)

Sulfidesulfur

thiosulfateA

cetate

some(Fe

(III)Mn(IV)

U(V

I)or

Cr(V

I))

Subsurface

environm

ents

rice

fieldsminesoilspills

[58ndash62]

Desulfosporosinus

meridiei

10ndash37

61ndash75

H2C

O2acetatesom

e(la

ctatepyruvate

ethano

l)Sulfatesom

e(nitrate)

Groun

dwater

contam

inated

with

polycyclica

romatic

hydrocarbo

nsinSw

anCoastalPlain

Australia

[63]

Desulfosporosinus

youn

gii

8ndash39

(32ndash35)

57ndash82(70ndash

73)

Beefextractyeast

extractform

ate

succinatelactate

pyruvateethanoland

toluene

Fumaratesulfatesulfite

thiosulfate

Artificialwetland

(sedim

ent)

[64]

BioMed Research International 11

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfosporosinus

orien

tis37ndash4

860ndash

65

H2C

O2formate

lactatepyruvatem

alate

fumaratesuccinate

methano

lethano

lprop

anolbutanol

butyratevalerate

palm

itate

Sulfatesulfite

thiosulfatesulfur

nd[65]

Desulfosporom

usapolytro

pa4ndash

3761ndash80

H2C

O2formate

lactatebu

tyrateseveral

alcoho

lsorganica

cids

carboh

ydratessome

aminoacidscholine

betaine

SulfateFe(OH) 3

Oligotroph

iclake

(sedim

ent)

German

[66]

Thermodesulfovibrio

yellowstonii

41ndash83

60ndash

80(70)

H2C

O2acetate

form

atelactate

pyruvate

Sulfatethiosulfate

sulfite

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA

[67]

Thermodesulfovibrio

islandicus

5545ndash70

(70)

H2pyruvatelactate

form

ate

Sulfaten

itrate

Bioreactor

inoculated

with

hotsprings

(microbialmats)sample

Iceland

[56]

Desulfohalobium

spp(6

species)

nd55ndash80(65ndash70)

H2lactateethanol

acetate

Sulfite

hypersaline

environm

ents

[6869]

Desulfocaldus

terraneus

58nd

H2C

O2aminoacids

proteinaceou

ssub

strates

andorganica

cids

prod

ucingethano

lacetateprop

ionate

isovalerate2-

methylbutyrate

Cystinesulfu

rsulfate

Seao

ilfacilitiesAlaksa

[70]

12 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfomicrobium

spp(4

species)

25ndash30

ndH2lactatepyruvate

Ethano

lform

ate

Sulfatesulfoxyanions

Anaerob

icsediments

(Freshwaterbrackish

marine)anaerob

icstrata

oroverlyingwaterand

insaturatedmineralor

organicd

eposits

[5469]

Desulfonatro

novibrio

hydrogenovoran

s37ndash4

090

ndash102(90ndash97)

H2formate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[71]

Desulfonatro

num

spp(3

species)

20ndash4

5(37ndash45)

80ndash

100(90)

H2form

ateYeast

extractethano

llactate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[72]

Desulfovibriospp(47

species)

25ndash4

4(25ndash35)

ndH2C

O2acetatelactate

carboh

ydrates

Sulfaten

itrate

nd[73]

Desulfomonile

spp(2

species)

30ndash30

(37)

65ndash78

(68ndash70)

H2C

O2benzoate

pyruvateorganic

carbon

halogens

Sulfatesulfite

thiosulfatesulfurFe

(III)NitrateU(V

I)Slud

ge[74]

Syntroph

obacteraceae

(8genera)

31ndash6

070

ndash75

H2C

O2acetate

form

atelactate

pyruvate

Sulfatesulfite

thiosulfate

Sewages

ludge

freshwaterbrackish

marines

edim

ent

marineh

ydrothermal

ventsho

tspring

sediments

[7375]

Desulfobacterium

anilini

3069ndash

75H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

BioMed Research International 13

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfarculus

baarsii

35ndash39

73H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

Desulfobacteraceae(12

genera)

10ndash4

0nd

H2C

O2L

ong-chain

fatty

acidsAlcoh

ols

Polara

romatic

compo

undsand

insome

casese

venAlip

hatic

arom

atichydrocarbo

ns

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[77]

Desulfosporosinus

acidophilus

25ndash4

036ndash

52(52)

H2lactatepyruvate

glycerolglucose

and

fructose

Sulfate

Sedimentfrom

anacid

effluent

pond

[26]

Desulfosporosinus

acididuran

s15ndash4

038ndash70

(55)

H2formatelactate

butyratefum

arate

malatepyruvate

glycerolm

ethano

lethano

lyeastextract

xyloseglucosefructose

Ferriciro

nnitrate

sulfateelem

entalsulfur

thiosulfate

Whiteriv

erdraining

from

theS

oufriere

hills

inMon

serrat(pH32)

[78]

a Valuesc

losedby

parenthesis

arec

onsid

ered

optim

alpH

ndno

tinformed

byconsultedreference

14 BioMed Research International

such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO

2[33]

In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO

2and H

2[17]

D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]

4 Natural Attenuation for the Design of AMDRemediation Strategies

Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and

chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH

2O)were detected presumably due

to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not

Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]

5 Concluding Remarks

Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools

Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico

BioMed Research International 15

(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)

References

[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013

[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014

[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012

[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008

[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011

[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003

[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000

[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014

[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006

[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005

[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007

[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008

[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008

[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015

[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013

[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006

[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006

[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014

[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008

[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006

[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010

[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005

[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016

[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999

[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001

[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010

[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990

[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016

[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014

[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009

[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

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Signal TransductionJournal of

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BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

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Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

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Enzyme Research

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International Journal of

Microbiology

BioMed Research International 7

MetalSuldes(ZnS)

Air

Excess

Sulfur

Puriedeuent

Recycle

Neu

troph

ilic

SRB

Bior

eact

or o

ne

Bior

eact

or tw

oSu

lde

oxid

ising

bac

teriaWaste water or

process water(34

2minus and metalssuch as H

2+)

(2-rich gas

2

(3minus

(3I)

34

2minus+ 4(2 + (

+rarr (3

minus+ 4(2

H2+

+ (3minusrarr H3 + (

+

2(3minus+ 2 + 2(

+rarr 23

I+ 2(2

(a)

Bior

eact

orsta

ge I

Stag

e II

Ana

erob

ic ag

itate

dco

ntac

tor

SulfurReagents

Feed water(AMD)

sulfu

r red

ucin

g ba

cter

ia

ClarierTreated water

Filter

Metal sulde (ZnS)to smelter

(23

Gen

erat

ion

by

(23

(b)

Figure 2 Schematic overview of the Thiopaq (a) and Biosulfide (b) processes (adapted from Adams et al [12] Muyzer and Stams [13])

simpler engineering designs and reduce operational costs byusing single on-line reactor vessels that could be used to bothgenerate sulfide and selectively precipitate target metal(s)Precipitation and removal of many soluble transition metalsoften present in AMD emanating from metal mines maybe achieved by ready biomineralization as their sulfides Theproduced metal sulfides have different solubilities thereforemetals can be precipitated together or selectively by con-trolling concentrations of the key reactant S2minus which maybe achieved by controlling pH (S2minus + H+ harr HSminus) Coppersulfide for example is far less soluble than ferrous sulfide(respective log Ksp values of minus359 and minus188) and thereforeCuS precipitates at pH 2 whereas FeS needs much higher pHto precipitate Diez-Ercilla et al [31] have also demonstratedthat selective precipitation of metal sulfides occurs naturallyin Cueva de la Mora pit lake (SW Spain) and the geochemicalcalculations match perfectly with the results of chemicaland mineralogical composition Nancucheo and Johnson[3] showed that it was possible to selectively precipitate

stable metal sulfides in inline reactor vessel testing twosynthetic AMDs in acidic conditions (pH 22ndash48) In the firstbioreactor with a composition of feeding similar to AMD atthe abandoned Cwm Rheidol lead-zinc mine in mid-Waleszinc was efficiently precipitated (gt99) as sulfide inside thereactor while both aluminum and ferrous iron remain insolution (gt99) and were washed out of the reactor vesselThe second sulfidogenic bioreactor was challenged with asynthetic AMD based on that from Mynydd Parys NorthWales Throughout the test period all the copper presentin the feed liquor was precipitated (confirmed as coppersulfide) within the bioreactor but none of the ferrous ironwas present in the solids Although the initial pH at whichthe bioreactor was operated (from pH 36 to 25) causedsome coprecipitation of zinc with the copper by progressivelylowering the bioreactor pH and the concentration of theelectron donor in the influent liquor it was possible toprecipitate gt99 of the copper within the bioreactor as CuSand to maintain gt99 of the zinc iron and aluminum in

8 BioMed Research International

solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]

4C3H8O3+ 10H+ + 7SO

4

2minus+ Cu2+ + Zn2+ + Fe2+

997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H

2O

(1)

This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD

Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H

2S) by the SRB and orpiment

(As2S3) generated within the bioreactor In addition this

process was also observed to occur naturally in an acidic pitlake [31]

Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for

the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes

3 Microbiology in Remediating AcidicMine Waters

Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]

Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents

BioMed Research International 9

Table2Isolated

sulfido

genicm

icroorganism

sand

theirm

aincharacteris

tics

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermocladium

modestiu

s45ndash82

(75)

26ndash

59(40)

Glycogen

starch

proteins

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

mud

)Japan

[43ndash45]

Caldivirg

amaquilin

gensis

70ndash9

023ndash64(37ndash4

2)

Glycogen

beefextract

pepton

etryptoneyeast

extract

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

solfataric

soilmud

)Mt

Maquilin

gPh

ilipp

ines

[46]

Archaeoglobu

slithotro

phicu

snd

60

Acetate

SulfateL-cysteine

nd[4748]

Archaeoglobu

sveneficus

nd69

H2acetateformate

pyruvateyeastextract

citratelactatesta

rch

pepton

e

Sulfitethiosulfate

Wallsof

activ

eblack

smoker

atmiddle

AtlanticRidge

[44]

Archaeoglobu

sprofund

usnd

45ndash75

H2acetatepyruvate

yeastextractlactate

meatextractpeptone

crud

eoilwith

acetate

Sulfatethiosulfate

sulfite

Deepseah

ydrothermal

syste

moff

Guaym

as

Mexico

[4950]

Archaeoglobu

sfulgidu

s60ndash75

(70)

55ndash75

(60)

H2C

O2formate

form

amideD(minus)-and

L(+)-lactateglucose

starchcalam

inea

cids

pepton

egelatincasein

meatextractyeast

extract

Sulfatethiosulfate

sulfite

Marineh

ydrothermal

syste

mN

eron

eIta

ly[4951]

Thermodesulfatatorind

icus

55ndash80

(70)

60ndash

67(625)

H2C

O2stim

ulated

bymethano

lmon

omethylamine

glutam

atepepton

efumaratetryptone

isobu

tyrate3-C

H3

butyrateethanol

prop

anolandlow

amou

ntso

facetate

Sulfate

Marineh

ydrothermal

syste

mC

entralIndian

Ridge

[52]

Thermodesulfobacterium

hydrogeniphilum

50ndash80

(75)

63ndash68(65)

H2C

O2stim

ulated

byacetatefumarate

3-methylbutyrate

glutam

ateyeastextract

pepton

eortrypton

e

Sulfate

Marineh

ydrothermal

syste

mG

uaym

asBa

sin[53]

10 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermodesulfobacterium

commun

e41ndash83

60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA[5455]

Thermodesulfobacterium

thermophilum

nd60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

nd[55]

Thermodesulfobacterium

hveragerdense

7545ndash70

(70)

H2pyruvatelactate

Sulfatesulfite

Hot

sprin

gs(m

icrobial

mats)Iceland

[56]

Thermodesulfobium

narugense

6940ndash

60(55ndash6

0)

H2C

O2

Sulfaten

itrate

thiosulfate

Hot

sprin

gs(m

icrobial

mats)Japan

[57]

Desulfotomaculum

spp(30

species)

nd23ndash55

H2C

O2formatesome

(organicacidslip

idsor

mon

oaromatic

hydrocarbo

ns)

Sulfidesulfur

thiosulfateA

cetate

some(Fe

(III)Mn(IV)

U(V

I)or

Cr(V

I))

Subsurface

environm

ents

rice

fieldsminesoilspills

[58ndash62]

Desulfosporosinus

meridiei

10ndash37

61ndash75

H2C

O2acetatesom

e(la

ctatepyruvate

ethano

l)Sulfatesom

e(nitrate)

Groun

dwater

contam

inated

with

polycyclica

romatic

hydrocarbo

nsinSw

anCoastalPlain

Australia

[63]

Desulfosporosinus

youn

gii

8ndash39

(32ndash35)

57ndash82(70ndash

73)

Beefextractyeast

extractform

ate

succinatelactate

pyruvateethanoland

toluene

Fumaratesulfatesulfite

thiosulfate

Artificialwetland

(sedim

ent)

[64]

BioMed Research International 11

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfosporosinus

orien

tis37ndash4

860ndash

65

H2C

O2formate

lactatepyruvatem

alate

fumaratesuccinate

methano

lethano

lprop

anolbutanol

butyratevalerate

palm

itate

Sulfatesulfite

thiosulfatesulfur

nd[65]

Desulfosporom

usapolytro

pa4ndash

3761ndash80

H2C

O2formate

lactatebu

tyrateseveral

alcoho

lsorganica

cids

carboh

ydratessome

aminoacidscholine

betaine

SulfateFe(OH) 3

Oligotroph

iclake

(sedim

ent)

German

[66]

Thermodesulfovibrio

yellowstonii

41ndash83

60ndash

80(70)

H2C

O2acetate

form

atelactate

pyruvate

Sulfatethiosulfate

sulfite

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA

[67]

Thermodesulfovibrio

islandicus

5545ndash70

(70)

H2pyruvatelactate

form

ate

Sulfaten

itrate

Bioreactor

inoculated

with

hotsprings

(microbialmats)sample

Iceland

[56]

Desulfohalobium

spp(6

species)

nd55ndash80(65ndash70)

H2lactateethanol

acetate

Sulfite

hypersaline

environm

ents

[6869]

Desulfocaldus

terraneus

58nd

H2C

O2aminoacids

proteinaceou

ssub

strates

andorganica

cids

prod

ucingethano

lacetateprop

ionate

isovalerate2-

methylbutyrate

Cystinesulfu

rsulfate

Seao

ilfacilitiesAlaksa

[70]

12 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfomicrobium

spp(4

species)

25ndash30

ndH2lactatepyruvate

Ethano

lform

ate

Sulfatesulfoxyanions

Anaerob

icsediments

(Freshwaterbrackish

marine)anaerob

icstrata

oroverlyingwaterand

insaturatedmineralor

organicd

eposits

[5469]

Desulfonatro

novibrio

hydrogenovoran

s37ndash4

090

ndash102(90ndash97)

H2formate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[71]

Desulfonatro

num

spp(3

species)

20ndash4

5(37ndash45)

80ndash

100(90)

H2form

ateYeast

extractethano

llactate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[72]

Desulfovibriospp(47

species)

25ndash4

4(25ndash35)

ndH2C

O2acetatelactate

carboh

ydrates

Sulfaten

itrate

nd[73]

Desulfomonile

spp(2

species)

30ndash30

(37)

65ndash78

(68ndash70)

H2C

O2benzoate

pyruvateorganic

carbon

halogens

Sulfatesulfite

thiosulfatesulfurFe

(III)NitrateU(V

I)Slud

ge[74]

Syntroph

obacteraceae

(8genera)

31ndash6

070

ndash75

H2C

O2acetate

form

atelactate

pyruvate

Sulfatesulfite

thiosulfate

Sewages

ludge

freshwaterbrackish

marines

edim

ent

marineh

ydrothermal

ventsho

tspring

sediments

[7375]

Desulfobacterium

anilini

3069ndash

75H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

BioMed Research International 13

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfarculus

baarsii

35ndash39

73H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

Desulfobacteraceae(12

genera)

10ndash4

0nd

H2C

O2L

ong-chain

fatty

acidsAlcoh

ols

Polara

romatic

compo

undsand

insome

casese

venAlip

hatic

arom

atichydrocarbo

ns

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[77]

Desulfosporosinus

acidophilus

25ndash4

036ndash

52(52)

H2lactatepyruvate

glycerolglucose

and

fructose

Sulfate

Sedimentfrom

anacid

effluent

pond

[26]

Desulfosporosinus

acididuran

s15ndash4

038ndash70

(55)

H2formatelactate

butyratefum

arate

malatepyruvate

glycerolm

ethano

lethano

lyeastextract

xyloseglucosefructose

Ferriciro

nnitrate

sulfateelem

entalsulfur

thiosulfate

Whiteriv

erdraining

from

theS

oufriere

hills

inMon

serrat(pH32)

[78]

a Valuesc

losedby

parenthesis

arec

onsid

ered

optim

alpH

ndno

tinformed

byconsultedreference

14 BioMed Research International

such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO

2[33]

In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO

2and H

2[17]

D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]

4 Natural Attenuation for the Design of AMDRemediation Strategies

Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and

chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH

2O)were detected presumably due

to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not

Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]

5 Concluding Remarks

Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools

Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico

BioMed Research International 15

(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)

References

[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013

[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014

[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012

[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008

[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011

[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003

[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000

[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014

[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006

[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005

[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007

[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008

[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008

[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015

[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013

[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006

[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006

[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014

[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008

[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006

[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010

[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005

[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016

[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999

[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001

[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010

[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990

[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016

[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014

[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009

[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

8 BioMed Research International

solution Glycerol was used as energy and carbon source(electron donor) and the generalized reaction is [1]

4C3H8O3+ 10H+ + 7SO

4

2minus+ Cu2+ + Zn2+ + Fe2+

997888rarr 12CO2+ 5H2S + CuS + ZnS + Fe2+ + 16H

2O

(1)

This low sulfidogenic bioreactor system was also demon-strated to be effective at processing complex acidic waterdraining from the Mauriden mine in Sweden [18] Through-out the test period zincwas removed from the syntheticminewater as ZnS from which the metal could be recovered asin the case at the Budel zinc refinery in The Netherlands[24] Recently Falagan et al [32] have operated this sulfi-dogenic reactor to mediate the precipitation of aluminumin acidic mine waters as hydroxysulfate minerals Besidesthis bioreactor was tested to demonstrate the recovery ofover 99 of the copper present in a synthetic mine waterdrained from a copper mine in Carajas in the State of ParaBrazil [33] The sulfidogenic system was also operated underdifferent temperatures Although there were large variationsin rates of sulfate reduction measured at each temperaturethe bioreactor operated effectively over a wide temperaturerange (30ndash45∘C) which can have major advantages in somesituations where temperatures are relatively high for examplein mine sites located in northern Brazil and in other regionswhere high temperatures are observed Therefore therewould be no requirements to have temperature control (heat-ing or cooling) to preserve the integrity of the acidophilic SRBreactor [33] The perceived advantages of this system are thatthere are simple engineering and relatively low operationalcost The system can be configured to optimize mine waterremediation and metal recovery according to the nature ofthe mine water which are the constraining factors in usingactive biological technologies to mitigate AMD

Metalloids such as arsenic are a common constituent ofmine waters Battaglia-Brunet and colleagues [34] demon-strated that As (III) can be removed by precipitation as asulfideThe results demonstrated the feasibility of continuoustreatment of an acidic solution (pH 275ndash5) containing up to100mgAs (V)Under this approachAs (V)was reduced toAs(III) directly or indirectly (via H

2S) by the SRB and orpiment

(As2S3) generated within the bioreactor In addition this

process was also observed to occur naturally in an acidic pitlake [31]

Recently Florentino and colleagues [35] studied themicrobiological suitability of using acidophilic sulfur reduc-ing bacteria for metal recovery These authors demonstratedthat the Desulfurella strain TR1 was able to perform sulfurreduction to precipitate and recover metals such as copperfrom acidic waste water and mining water without the needto neutralize the water before treatment One drawback onthe of use sulfur reducing microorganisms is that a suitableelectron donor needs to be added for sulfate reduction Eventhough sulfate is present in AMD the additional cost ofelectron donors (such as glycerol) for sulfate reduction ishigher than the cost of the combined addition of elementalsulfur and electron donors Subsequently elemental sulfur asan electron acceptor can be more economically attractive for

the application of biogenic sulfide technologies On the otherhand cheaper electron donor such organic waste materialmay be used but their variable composition makes it lesssuitable for controlled high rate technologies Besides deadalgal biomass can release organic products suitable to sustainthe growth of SRB Therefore Diez-Ercilla et al [31] haveproposed that under controlled eutrophication it could bepossible to decrease the metal concentrations in acidic minepit lakes

3 Microbiology in Remediating AcidicMine Waters

Based on 16S rRNA sequence analysis microorganisms thatcatalyze the dissimilatory reduction of sulfate to sulfideinclude representatives of five phylogenetic lineages ofbacteria (Deltaproteobacteria Clostridia Nitrospirae Ther-modesulfobiaceae and Thermodesulfobacteria) and twomajor subgroups (Crenarchaeota and Euryarchaeota) of theArchaea domain (Table 2 shows a summary of sulfidogenicmicroorganisms used for their main characteristics) SRB arehighly diverse in terms of the range of organic compoundsused as a carbon source and energy though polymericorganic materials generally are not utilized directly by SRB[13] In addition some SRB can grow autotrophically usinghydrogen as electron donor and fixing carbon dioxidethough others have requirement for organic carbon such asacetate when growing on hydrogen Besides many SRB canalso use electron acceptors other than sulfate for growthsuch as sulfur sulfite thiosulfate nitrate arsenate iron orfumarate [78]

Most species of SRB that have been isolated from acidicmine waste such asDesulfosarcinaDesulfococcusDesulfovib-rio and Desulfomonile are neutrophiles and are active atneutral pH [14 25] Besides for a long time the accepted viewwas that sulfate reducing activity was limited to slightly acidicto near neutral pH explained by the existence of micronichesof elevated pH around the bacteria [21 31] Attempts to isolateacidophilic or acid-tolerant strains of SRB (aSRB) havemostlybeen unsuccessful until recently [79] One of the reasons forthe failure to isolate aSRB has been the use of organic acidssuch as lactate (carbon and energy source) which are toxicto many acidophiles In acidic media these compounds existpredominantly as nondissociated lipophilicmolecules and assuch can transverse bacterial membranes where they disso-ciate in the circumneutral internal cell cytoplasm causing adisequilibrium and the influx of further undissociated acidsand acidification of the cytosol [80] In contrast glycerolcan be used as carbon and energy source as it is unchargedat low pH In addition many SRB are incomplete substrateoxidizers producing acetic acid as a product enough to limitthe growth of aSRB even at micromolar concentration Tocircumvent this problem and for isolating aSRB overlay platecan be used to remove acetic acid This technique uses adouble layer where the lower layer is inoculatedwith an activeculture of Acidocella (Ac) aromatica while the upper layer isnot Therefore the heterotrophic acidophiles metabolize thesmall molecular weight compounds (such as acetic acid) thatderive from acid hydrolysis of commonly used gelling agents

BioMed Research International 9

Table2Isolated

sulfido

genicm

icroorganism

sand

theirm

aincharacteris

tics

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermocladium

modestiu

s45ndash82

(75)

26ndash

59(40)

Glycogen

starch

proteins

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

mud

)Japan

[43ndash45]

Caldivirg

amaquilin

gensis

70ndash9

023ndash64(37ndash4

2)

Glycogen

beefextract

pepton

etryptoneyeast

extract

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

solfataric

soilmud

)Mt

Maquilin

gPh

ilipp

ines

[46]

Archaeoglobu

slithotro

phicu

snd

60

Acetate

SulfateL-cysteine

nd[4748]

Archaeoglobu

sveneficus

nd69

H2acetateformate

pyruvateyeastextract

citratelactatesta

rch

pepton

e

Sulfitethiosulfate

Wallsof

activ

eblack

smoker

atmiddle

AtlanticRidge

[44]

Archaeoglobu

sprofund

usnd

45ndash75

H2acetatepyruvate

yeastextractlactate

meatextractpeptone

crud

eoilwith

acetate

Sulfatethiosulfate

sulfite

Deepseah

ydrothermal

syste

moff

Guaym

as

Mexico

[4950]

Archaeoglobu

sfulgidu

s60ndash75

(70)

55ndash75

(60)

H2C

O2formate

form

amideD(minus)-and

L(+)-lactateglucose

starchcalam

inea

cids

pepton

egelatincasein

meatextractyeast

extract

Sulfatethiosulfate

sulfite

Marineh

ydrothermal

syste

mN

eron

eIta

ly[4951]

Thermodesulfatatorind

icus

55ndash80

(70)

60ndash

67(625)

H2C

O2stim

ulated

bymethano

lmon

omethylamine

glutam

atepepton

efumaratetryptone

isobu

tyrate3-C

H3

butyrateethanol

prop

anolandlow

amou

ntso

facetate

Sulfate

Marineh

ydrothermal

syste

mC

entralIndian

Ridge

[52]

Thermodesulfobacterium

hydrogeniphilum

50ndash80

(75)

63ndash68(65)

H2C

O2stim

ulated

byacetatefumarate

3-methylbutyrate

glutam

ateyeastextract

pepton

eortrypton

e

Sulfate

Marineh

ydrothermal

syste

mG

uaym

asBa

sin[53]

10 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermodesulfobacterium

commun

e41ndash83

60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA[5455]

Thermodesulfobacterium

thermophilum

nd60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

nd[55]

Thermodesulfobacterium

hveragerdense

7545ndash70

(70)

H2pyruvatelactate

Sulfatesulfite

Hot

sprin

gs(m

icrobial

mats)Iceland

[56]

Thermodesulfobium

narugense

6940ndash

60(55ndash6

0)

H2C

O2

Sulfaten

itrate

thiosulfate

Hot

sprin

gs(m

icrobial

mats)Japan

[57]

Desulfotomaculum

spp(30

species)

nd23ndash55

H2C

O2formatesome

(organicacidslip

idsor

mon

oaromatic

hydrocarbo

ns)

Sulfidesulfur

thiosulfateA

cetate

some(Fe

(III)Mn(IV)

U(V

I)or

Cr(V

I))

Subsurface

environm

ents

rice

fieldsminesoilspills

[58ndash62]

Desulfosporosinus

meridiei

10ndash37

61ndash75

H2C

O2acetatesom

e(la

ctatepyruvate

ethano

l)Sulfatesom

e(nitrate)

Groun

dwater

contam

inated

with

polycyclica

romatic

hydrocarbo

nsinSw

anCoastalPlain

Australia

[63]

Desulfosporosinus

youn

gii

8ndash39

(32ndash35)

57ndash82(70ndash

73)

Beefextractyeast

extractform

ate

succinatelactate

pyruvateethanoland

toluene

Fumaratesulfatesulfite

thiosulfate

Artificialwetland

(sedim

ent)

[64]

BioMed Research International 11

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfosporosinus

orien

tis37ndash4

860ndash

65

H2C

O2formate

lactatepyruvatem

alate

fumaratesuccinate

methano

lethano

lprop

anolbutanol

butyratevalerate

palm

itate

Sulfatesulfite

thiosulfatesulfur

nd[65]

Desulfosporom

usapolytro

pa4ndash

3761ndash80

H2C

O2formate

lactatebu

tyrateseveral

alcoho

lsorganica

cids

carboh

ydratessome

aminoacidscholine

betaine

SulfateFe(OH) 3

Oligotroph

iclake

(sedim

ent)

German

[66]

Thermodesulfovibrio

yellowstonii

41ndash83

60ndash

80(70)

H2C

O2acetate

form

atelactate

pyruvate

Sulfatethiosulfate

sulfite

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA

[67]

Thermodesulfovibrio

islandicus

5545ndash70

(70)

H2pyruvatelactate

form

ate

Sulfaten

itrate

Bioreactor

inoculated

with

hotsprings

(microbialmats)sample

Iceland

[56]

Desulfohalobium

spp(6

species)

nd55ndash80(65ndash70)

H2lactateethanol

acetate

Sulfite

hypersaline

environm

ents

[6869]

Desulfocaldus

terraneus

58nd

H2C

O2aminoacids

proteinaceou

ssub

strates

andorganica

cids

prod

ucingethano

lacetateprop

ionate

isovalerate2-

methylbutyrate

Cystinesulfu

rsulfate

Seao

ilfacilitiesAlaksa

[70]

12 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfomicrobium

spp(4

species)

25ndash30

ndH2lactatepyruvate

Ethano

lform

ate

Sulfatesulfoxyanions

Anaerob

icsediments

(Freshwaterbrackish

marine)anaerob

icstrata

oroverlyingwaterand

insaturatedmineralor

organicd

eposits

[5469]

Desulfonatro

novibrio

hydrogenovoran

s37ndash4

090

ndash102(90ndash97)

H2formate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[71]

Desulfonatro

num

spp(3

species)

20ndash4

5(37ndash45)

80ndash

100(90)

H2form

ateYeast

extractethano

llactate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[72]

Desulfovibriospp(47

species)

25ndash4

4(25ndash35)

ndH2C

O2acetatelactate

carboh

ydrates

Sulfaten

itrate

nd[73]

Desulfomonile

spp(2

species)

30ndash30

(37)

65ndash78

(68ndash70)

H2C

O2benzoate

pyruvateorganic

carbon

halogens

Sulfatesulfite

thiosulfatesulfurFe

(III)NitrateU(V

I)Slud

ge[74]

Syntroph

obacteraceae

(8genera)

31ndash6

070

ndash75

H2C

O2acetate

form

atelactate

pyruvate

Sulfatesulfite

thiosulfate

Sewages

ludge

freshwaterbrackish

marines

edim

ent

marineh

ydrothermal

ventsho

tspring

sediments

[7375]

Desulfobacterium

anilini

3069ndash

75H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

BioMed Research International 13

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfarculus

baarsii

35ndash39

73H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

Desulfobacteraceae(12

genera)

10ndash4

0nd

H2C

O2L

ong-chain

fatty

acidsAlcoh

ols

Polara

romatic

compo

undsand

insome

casese

venAlip

hatic

arom

atichydrocarbo

ns

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[77]

Desulfosporosinus

acidophilus

25ndash4

036ndash

52(52)

H2lactatepyruvate

glycerolglucose

and

fructose

Sulfate

Sedimentfrom

anacid

effluent

pond

[26]

Desulfosporosinus

acididuran

s15ndash4

038ndash70

(55)

H2formatelactate

butyratefum

arate

malatepyruvate

glycerolm

ethano

lethano

lyeastextract

xyloseglucosefructose

Ferriciro

nnitrate

sulfateelem

entalsulfur

thiosulfate

Whiteriv

erdraining

from

theS

oufriere

hills

inMon

serrat(pH32)

[78]

a Valuesc

losedby

parenthesis

arec

onsid

ered

optim

alpH

ndno

tinformed

byconsultedreference

14 BioMed Research International

such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO

2[33]

In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO

2and H

2[17]

D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]

4 Natural Attenuation for the Design of AMDRemediation Strategies

Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and

chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH

2O)were detected presumably due

to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not

Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]

5 Concluding Remarks

Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools

Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico

BioMed Research International 15

(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)

References

[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013

[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014

[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012

[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008

[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011

[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003

[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000

[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014

[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006

[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005

[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007

[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008

[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008

[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015

[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013

[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006

[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006

[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014

[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008

[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006

[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010

[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005

[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016

[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999

[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001

[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010

[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990

[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016

[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014

[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009

[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

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Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

BioMed Research International 9

Table2Isolated

sulfido

genicm

icroorganism

sand

theirm

aincharacteris

tics

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermocladium

modestiu

s45ndash82

(75)

26ndash

59(40)

Glycogen

starch

proteins

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

mud

)Japan

[43ndash45]

Caldivirg

amaquilin

gensis

70ndash9

023ndash64(37ndash4

2)

Glycogen

beefextract

pepton

etryptoneyeast

extract

Sulfu

rthiosulfate

L-cyste

ine

Hot

sprin

gs(w

ater

solfataric

soilmud

)Mt

Maquilin

gPh

ilipp

ines

[46]

Archaeoglobu

slithotro

phicu

snd

60

Acetate

SulfateL-cysteine

nd[4748]

Archaeoglobu

sveneficus

nd69

H2acetateformate

pyruvateyeastextract

citratelactatesta

rch

pepton

e

Sulfitethiosulfate

Wallsof

activ

eblack

smoker

atmiddle

AtlanticRidge

[44]

Archaeoglobu

sprofund

usnd

45ndash75

H2acetatepyruvate

yeastextractlactate

meatextractpeptone

crud

eoilwith

acetate

Sulfatethiosulfate

sulfite

Deepseah

ydrothermal

syste

moff

Guaym

as

Mexico

[4950]

Archaeoglobu

sfulgidu

s60ndash75

(70)

55ndash75

(60)

H2C

O2formate

form

amideD(minus)-and

L(+)-lactateglucose

starchcalam

inea

cids

pepton

egelatincasein

meatextractyeast

extract

Sulfatethiosulfate

sulfite

Marineh

ydrothermal

syste

mN

eron

eIta

ly[4951]

Thermodesulfatatorind

icus

55ndash80

(70)

60ndash

67(625)

H2C

O2stim

ulated

bymethano

lmon

omethylamine

glutam

atepepton

efumaratetryptone

isobu

tyrate3-C

H3

butyrateethanol

prop

anolandlow

amou

ntso

facetate

Sulfate

Marineh

ydrothermal

syste

mC

entralIndian

Ridge

[52]

Thermodesulfobacterium

hydrogeniphilum

50ndash80

(75)

63ndash68(65)

H2C

O2stim

ulated

byacetatefumarate

3-methylbutyrate

glutam

ateyeastextract

pepton

eortrypton

e

Sulfate

Marineh

ydrothermal

syste

mG

uaym

asBa

sin[53]

10 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermodesulfobacterium

commun

e41ndash83

60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA[5455]

Thermodesulfobacterium

thermophilum

nd60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

nd[55]

Thermodesulfobacterium

hveragerdense

7545ndash70

(70)

H2pyruvatelactate

Sulfatesulfite

Hot

sprin

gs(m

icrobial

mats)Iceland

[56]

Thermodesulfobium

narugense

6940ndash

60(55ndash6

0)

H2C

O2

Sulfaten

itrate

thiosulfate

Hot

sprin

gs(m

icrobial

mats)Japan

[57]

Desulfotomaculum

spp(30

species)

nd23ndash55

H2C

O2formatesome

(organicacidslip

idsor

mon

oaromatic

hydrocarbo

ns)

Sulfidesulfur

thiosulfateA

cetate

some(Fe

(III)Mn(IV)

U(V

I)or

Cr(V

I))

Subsurface

environm

ents

rice

fieldsminesoilspills

[58ndash62]

Desulfosporosinus

meridiei

10ndash37

61ndash75

H2C

O2acetatesom

e(la

ctatepyruvate

ethano

l)Sulfatesom

e(nitrate)

Groun

dwater

contam

inated

with

polycyclica

romatic

hydrocarbo

nsinSw

anCoastalPlain

Australia

[63]

Desulfosporosinus

youn

gii

8ndash39

(32ndash35)

57ndash82(70ndash

73)

Beefextractyeast

extractform

ate

succinatelactate

pyruvateethanoland

toluene

Fumaratesulfatesulfite

thiosulfate

Artificialwetland

(sedim

ent)

[64]

BioMed Research International 11

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfosporosinus

orien

tis37ndash4

860ndash

65

H2C

O2formate

lactatepyruvatem

alate

fumaratesuccinate

methano

lethano

lprop

anolbutanol

butyratevalerate

palm

itate

Sulfatesulfite

thiosulfatesulfur

nd[65]

Desulfosporom

usapolytro

pa4ndash

3761ndash80

H2C

O2formate

lactatebu

tyrateseveral

alcoho

lsorganica

cids

carboh

ydratessome

aminoacidscholine

betaine

SulfateFe(OH) 3

Oligotroph

iclake

(sedim

ent)

German

[66]

Thermodesulfovibrio

yellowstonii

41ndash83

60ndash

80(70)

H2C

O2acetate

form

atelactate

pyruvate

Sulfatethiosulfate

sulfite

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA

[67]

Thermodesulfovibrio

islandicus

5545ndash70

(70)

H2pyruvatelactate

form

ate

Sulfaten

itrate

Bioreactor

inoculated

with

hotsprings

(microbialmats)sample

Iceland

[56]

Desulfohalobium

spp(6

species)

nd55ndash80(65ndash70)

H2lactateethanol

acetate

Sulfite

hypersaline

environm

ents

[6869]

Desulfocaldus

terraneus

58nd

H2C

O2aminoacids

proteinaceou

ssub

strates

andorganica

cids

prod

ucingethano

lacetateprop

ionate

isovalerate2-

methylbutyrate

Cystinesulfu

rsulfate

Seao

ilfacilitiesAlaksa

[70]

12 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfomicrobium

spp(4

species)

25ndash30

ndH2lactatepyruvate

Ethano

lform

ate

Sulfatesulfoxyanions

Anaerob

icsediments

(Freshwaterbrackish

marine)anaerob

icstrata

oroverlyingwaterand

insaturatedmineralor

organicd

eposits

[5469]

Desulfonatro

novibrio

hydrogenovoran

s37ndash4

090

ndash102(90ndash97)

H2formate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[71]

Desulfonatro

num

spp(3

species)

20ndash4

5(37ndash45)

80ndash

100(90)

H2form

ateYeast

extractethano

llactate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[72]

Desulfovibriospp(47

species)

25ndash4

4(25ndash35)

ndH2C

O2acetatelactate

carboh

ydrates

Sulfaten

itrate

nd[73]

Desulfomonile

spp(2

species)

30ndash30

(37)

65ndash78

(68ndash70)

H2C

O2benzoate

pyruvateorganic

carbon

halogens

Sulfatesulfite

thiosulfatesulfurFe

(III)NitrateU(V

I)Slud

ge[74]

Syntroph

obacteraceae

(8genera)

31ndash6

070

ndash75

H2C

O2acetate

form

atelactate

pyruvate

Sulfatesulfite

thiosulfate

Sewages

ludge

freshwaterbrackish

marines

edim

ent

marineh

ydrothermal

ventsho

tspring

sediments

[7375]

Desulfobacterium

anilini

3069ndash

75H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

BioMed Research International 13

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfarculus

baarsii

35ndash39

73H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

Desulfobacteraceae(12

genera)

10ndash4

0nd

H2C

O2L

ong-chain

fatty

acidsAlcoh

ols

Polara

romatic

compo

undsand

insome

casese

venAlip

hatic

arom

atichydrocarbo

ns

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[77]

Desulfosporosinus

acidophilus

25ndash4

036ndash

52(52)

H2lactatepyruvate

glycerolglucose

and

fructose

Sulfate

Sedimentfrom

anacid

effluent

pond

[26]

Desulfosporosinus

acididuran

s15ndash4

038ndash70

(55)

H2formatelactate

butyratefum

arate

malatepyruvate

glycerolm

ethano

lethano

lyeastextract

xyloseglucosefructose

Ferriciro

nnitrate

sulfateelem

entalsulfur

thiosulfate

Whiteriv

erdraining

from

theS

oufriere

hills

inMon

serrat(pH32)

[78]

a Valuesc

losedby

parenthesis

arec

onsid

ered

optim

alpH

ndno

tinformed

byconsultedreference

14 BioMed Research International

such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO

2[33]

In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO

2and H

2[17]

D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]

4 Natural Attenuation for the Design of AMDRemediation Strategies

Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and

chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH

2O)were detected presumably due

to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not

Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]

5 Concluding Remarks

Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools

Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico

BioMed Research International 15

(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)

References

[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013

[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014

[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012

[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008

[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011

[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003

[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000

[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014

[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006

[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005

[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007

[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008

[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008

[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015

[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013

[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006

[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006

[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014

[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008

[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006

[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010

[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005

[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016

[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999

[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001

[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010

[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990

[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016

[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014

[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009

[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

10 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Thermodesulfobacterium

commun

e41ndash83

60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA[5455]

Thermodesulfobacterium

thermophilum

nd60ndash

80(70)

H2C

O2pyruvate

lactate

Sulfatethiosulfate

nd[55]

Thermodesulfobacterium

hveragerdense

7545ndash70

(70)

H2pyruvatelactate

Sulfatesulfite

Hot

sprin

gs(m

icrobial

mats)Iceland

[56]

Thermodesulfobium

narugense

6940ndash

60(55ndash6

0)

H2C

O2

Sulfaten

itrate

thiosulfate

Hot

sprin

gs(m

icrobial

mats)Japan

[57]

Desulfotomaculum

spp(30

species)

nd23ndash55

H2C

O2formatesome

(organicacidslip

idsor

mon

oaromatic

hydrocarbo

ns)

Sulfidesulfur

thiosulfateA

cetate

some(Fe

(III)Mn(IV)

U(V

I)or

Cr(V

I))

Subsurface

environm

ents

rice

fieldsminesoilspills

[58ndash62]

Desulfosporosinus

meridiei

10ndash37

61ndash75

H2C

O2acetatesom

e(la

ctatepyruvate

ethano

l)Sulfatesom

e(nitrate)

Groun

dwater

contam

inated

with

polycyclica

romatic

hydrocarbo

nsinSw

anCoastalPlain

Australia

[63]

Desulfosporosinus

youn

gii

8ndash39

(32ndash35)

57ndash82(70ndash

73)

Beefextractyeast

extractform

ate

succinatelactate

pyruvateethanoland

toluene

Fumaratesulfatesulfite

thiosulfate

Artificialwetland

(sedim

ent)

[64]

BioMed Research International 11

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfosporosinus

orien

tis37ndash4

860ndash

65

H2C

O2formate

lactatepyruvatem

alate

fumaratesuccinate

methano

lethano

lprop

anolbutanol

butyratevalerate

palm

itate

Sulfatesulfite

thiosulfatesulfur

nd[65]

Desulfosporom

usapolytro

pa4ndash

3761ndash80

H2C

O2formate

lactatebu

tyrateseveral

alcoho

lsorganica

cids

carboh

ydratessome

aminoacidscholine

betaine

SulfateFe(OH) 3

Oligotroph

iclake

(sedim

ent)

German

[66]

Thermodesulfovibrio

yellowstonii

41ndash83

60ndash

80(70)

H2C

O2acetate

form

atelactate

pyruvate

Sulfatethiosulfate

sulfite

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA

[67]

Thermodesulfovibrio

islandicus

5545ndash70

(70)

H2pyruvatelactate

form

ate

Sulfaten

itrate

Bioreactor

inoculated

with

hotsprings

(microbialmats)sample

Iceland

[56]

Desulfohalobium

spp(6

species)

nd55ndash80(65ndash70)

H2lactateethanol

acetate

Sulfite

hypersaline

environm

ents

[6869]

Desulfocaldus

terraneus

58nd

H2C

O2aminoacids

proteinaceou

ssub

strates

andorganica

cids

prod

ucingethano

lacetateprop

ionate

isovalerate2-

methylbutyrate

Cystinesulfu

rsulfate

Seao

ilfacilitiesAlaksa

[70]

12 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfomicrobium

spp(4

species)

25ndash30

ndH2lactatepyruvate

Ethano

lform

ate

Sulfatesulfoxyanions

Anaerob

icsediments

(Freshwaterbrackish

marine)anaerob

icstrata

oroverlyingwaterand

insaturatedmineralor

organicd

eposits

[5469]

Desulfonatro

novibrio

hydrogenovoran

s37ndash4

090

ndash102(90ndash97)

H2formate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[71]

Desulfonatro

num

spp(3

species)

20ndash4

5(37ndash45)

80ndash

100(90)

H2form

ateYeast

extractethano

llactate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[72]

Desulfovibriospp(47

species)

25ndash4

4(25ndash35)

ndH2C

O2acetatelactate

carboh

ydrates

Sulfaten

itrate

nd[73]

Desulfomonile

spp(2

species)

30ndash30

(37)

65ndash78

(68ndash70)

H2C

O2benzoate

pyruvateorganic

carbon

halogens

Sulfatesulfite

thiosulfatesulfurFe

(III)NitrateU(V

I)Slud

ge[74]

Syntroph

obacteraceae

(8genera)

31ndash6

070

ndash75

H2C

O2acetate

form

atelactate

pyruvate

Sulfatesulfite

thiosulfate

Sewages

ludge

freshwaterbrackish

marines

edim

ent

marineh

ydrothermal

ventsho

tspring

sediments

[7375]

Desulfobacterium

anilini

3069ndash

75H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

BioMed Research International 13

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfarculus

baarsii

35ndash39

73H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

Desulfobacteraceae(12

genera)

10ndash4

0nd

H2C

O2L

ong-chain

fatty

acidsAlcoh

ols

Polara

romatic

compo

undsand

insome

casese

venAlip

hatic

arom

atichydrocarbo

ns

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[77]

Desulfosporosinus

acidophilus

25ndash4

036ndash

52(52)

H2lactatepyruvate

glycerolglucose

and

fructose

Sulfate

Sedimentfrom

anacid

effluent

pond

[26]

Desulfosporosinus

acididuran

s15ndash4

038ndash70

(55)

H2formatelactate

butyratefum

arate

malatepyruvate

glycerolm

ethano

lethano

lyeastextract

xyloseglucosefructose

Ferriciro

nnitrate

sulfateelem

entalsulfur

thiosulfate

Whiteriv

erdraining

from

theS

oufriere

hills

inMon

serrat(pH32)

[78]

a Valuesc

losedby

parenthesis

arec

onsid

ered

optim

alpH

ndno

tinformed

byconsultedreference

14 BioMed Research International

such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO

2[33]

In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO

2and H

2[17]

D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]

4 Natural Attenuation for the Design of AMDRemediation Strategies

Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and

chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH

2O)were detected presumably due

to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not

Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]

5 Concluding Remarks

Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools

Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico

BioMed Research International 15

(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)

References

[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013

[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014

[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012

[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008

[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011

[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003

[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000

[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014

[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006

[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005

[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007

[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008

[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008

[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015

[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013

[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006

[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006

[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014

[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008

[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006

[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010

[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005

[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016

[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999

[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001

[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010

[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990

[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016

[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014

[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009

[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

BioMed Research International 11

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfosporosinus

orien

tis37ndash4

860ndash

65

H2C

O2formate

lactatepyruvatem

alate

fumaratesuccinate

methano

lethano

lprop

anolbutanol

butyratevalerate

palm

itate

Sulfatesulfite

thiosulfatesulfur

nd[65]

Desulfosporom

usapolytro

pa4ndash

3761ndash80

H2C

O2formate

lactatebu

tyrateseveral

alcoho

lsorganica

cids

carboh

ydratessome

aminoacidscholine

betaine

SulfateFe(OH) 3

Oligotroph

iclake

(sedim

ent)

German

[66]

Thermodesulfovibrio

yellowstonii

41ndash83

60ndash

80(70)

H2C

O2acetate

form

atelactate

pyruvate

Sulfatethiosulfate

sulfite

Hot

sprin

gs(w

ater

sedimentand

mats)

Yellowsto

neNational

ParkU

SA

[67]

Thermodesulfovibrio

islandicus

5545ndash70

(70)

H2pyruvatelactate

form

ate

Sulfaten

itrate

Bioreactor

inoculated

with

hotsprings

(microbialmats)sample

Iceland

[56]

Desulfohalobium

spp(6

species)

nd55ndash80(65ndash70)

H2lactateethanol

acetate

Sulfite

hypersaline

environm

ents

[6869]

Desulfocaldus

terraneus

58nd

H2C

O2aminoacids

proteinaceou

ssub

strates

andorganica

cids

prod

ucingethano

lacetateprop

ionate

isovalerate2-

methylbutyrate

Cystinesulfu

rsulfate

Seao

ilfacilitiesAlaksa

[70]

12 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfomicrobium

spp(4

species)

25ndash30

ndH2lactatepyruvate

Ethano

lform

ate

Sulfatesulfoxyanions

Anaerob

icsediments

(Freshwaterbrackish

marine)anaerob

icstrata

oroverlyingwaterand

insaturatedmineralor

organicd

eposits

[5469]

Desulfonatro

novibrio

hydrogenovoran

s37ndash4

090

ndash102(90ndash97)

H2formate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[71]

Desulfonatro

num

spp(3

species)

20ndash4

5(37ndash45)

80ndash

100(90)

H2form

ateYeast

extractethano

llactate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[72]

Desulfovibriospp(47

species)

25ndash4

4(25ndash35)

ndH2C

O2acetatelactate

carboh

ydrates

Sulfaten

itrate

nd[73]

Desulfomonile

spp(2

species)

30ndash30

(37)

65ndash78

(68ndash70)

H2C

O2benzoate

pyruvateorganic

carbon

halogens

Sulfatesulfite

thiosulfatesulfurFe

(III)NitrateU(V

I)Slud

ge[74]

Syntroph

obacteraceae

(8genera)

31ndash6

070

ndash75

H2C

O2acetate

form

atelactate

pyruvate

Sulfatesulfite

thiosulfate

Sewages

ludge

freshwaterbrackish

marines

edim

ent

marineh

ydrothermal

ventsho

tspring

sediments

[7375]

Desulfobacterium

anilini

3069ndash

75H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

BioMed Research International 13

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfarculus

baarsii

35ndash39

73H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

Desulfobacteraceae(12

genera)

10ndash4

0nd

H2C

O2L

ong-chain

fatty

acidsAlcoh

ols

Polara

romatic

compo

undsand

insome

casese

venAlip

hatic

arom

atichydrocarbo

ns

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[77]

Desulfosporosinus

acidophilus

25ndash4

036ndash

52(52)

H2lactatepyruvate

glycerolglucose

and

fructose

Sulfate

Sedimentfrom

anacid

effluent

pond

[26]

Desulfosporosinus

acididuran

s15ndash4

038ndash70

(55)

H2formatelactate

butyratefum

arate

malatepyruvate

glycerolm

ethano

lethano

lyeastextract

xyloseglucosefructose

Ferriciro

nnitrate

sulfateelem

entalsulfur

thiosulfate

Whiteriv

erdraining

from

theS

oufriere

hills

inMon

serrat(pH32)

[78]

a Valuesc

losedby

parenthesis

arec

onsid

ered

optim

alpH

ndno

tinformed

byconsultedreference

14 BioMed Research International

such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO

2[33]

In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO

2and H

2[17]

D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]

4 Natural Attenuation for the Design of AMDRemediation Strategies

Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and

chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH

2O)were detected presumably due

to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not

Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]

5 Concluding Remarks

Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools

Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico

BioMed Research International 15

(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)

References

[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013

[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014

[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012

[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008

[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011

[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003

[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000

[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014

[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006

[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005

[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007

[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008

[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008

[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015

[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013

[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006

[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006

[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014

[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008

[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006

[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010

[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005

[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016

[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999

[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001

[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010

[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990

[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016

[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014

[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009

[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

12 BioMed Research International

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfomicrobium

spp(4

species)

25ndash30

ndH2lactatepyruvate

Ethano

lform

ate

Sulfatesulfoxyanions

Anaerob

icsediments

(Freshwaterbrackish

marine)anaerob

icstrata

oroverlyingwaterand

insaturatedmineralor

organicd

eposits

[5469]

Desulfonatro

novibrio

hydrogenovoran

s37ndash4

090

ndash102(90ndash97)

H2formate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[71]

Desulfonatro

num

spp(3

species)

20ndash4

5(37ndash45)

80ndash

100(90)

H2form

ateYeast

extractethano

llactate

Sulfatesulfite

thiosulfate

Alkalines

odalakes

(anaerob

ic)

[72]

Desulfovibriospp(47

species)

25ndash4

4(25ndash35)

ndH2C

O2acetatelactate

carboh

ydrates

Sulfaten

itrate

nd[73]

Desulfomonile

spp(2

species)

30ndash30

(37)

65ndash78

(68ndash70)

H2C

O2benzoate

pyruvateorganic

carbon

halogens

Sulfatesulfite

thiosulfatesulfurFe

(III)NitrateU(V

I)Slud

ge[74]

Syntroph

obacteraceae

(8genera)

31ndash6

070

ndash75

H2C

O2acetate

form

atelactate

pyruvate

Sulfatesulfite

thiosulfate

Sewages

ludge

freshwaterbrackish

marines

edim

ent

marineh

ydrothermal

ventsho

tspring

sediments

[7375]

Desulfobacterium

anilini

3069ndash

75H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

BioMed Research International 13

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfarculus

baarsii

35ndash39

73H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

Desulfobacteraceae(12

genera)

10ndash4

0nd

H2C

O2L

ong-chain

fatty

acidsAlcoh

ols

Polara

romatic

compo

undsand

insome

casese

venAlip

hatic

arom

atichydrocarbo

ns

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[77]

Desulfosporosinus

acidophilus

25ndash4

036ndash

52(52)

H2lactatepyruvate

glycerolglucose

and

fructose

Sulfate

Sedimentfrom

anacid

effluent

pond

[26]

Desulfosporosinus

acididuran

s15ndash4

038ndash70

(55)

H2formatelactate

butyratefum

arate

malatepyruvate

glycerolm

ethano

lethano

lyeastextract

xyloseglucosefructose

Ferriciro

nnitrate

sulfateelem

entalsulfur

thiosulfate

Whiteriv

erdraining

from

theS

oufriere

hills

inMon

serrat(pH32)

[78]

a Valuesc

losedby

parenthesis

arec

onsid

ered

optim

alpH

ndno

tinformed

byconsultedreference

14 BioMed Research International

such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO

2[33]

In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO

2and H

2[17]

D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]

4 Natural Attenuation for the Design of AMDRemediation Strategies

Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and

chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH

2O)were detected presumably due

to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not

Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]

5 Concluding Remarks

Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools

Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico

BioMed Research International 15

(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)

References

[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013

[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014

[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012

[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008

[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011

[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003

[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000

[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014

[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006

[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005

[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007

[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008

[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008

[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015

[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013

[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006

[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006

[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014

[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008

[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006

[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010

[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005

[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016

[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999

[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001

[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010

[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990

[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016

[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014

[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009

[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

BioMed Research International 13

Table2Con

tinued

Microorganism

Temperature

(∘ C)

pHa

Carbon

andele

ctron

source

Electro

nacceptor

Source

Reference

Desulfarculus

baarsii

35ndash39

73H2C

O2butyrate

high

erfatty

acidsother

organica

cidsalcoh

ols

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[76]

Desulfobacteraceae(12

genera)

10ndash4

0nd

H2C

O2L

ong-chain

fatty

acidsAlcoh

ols

Polara

romatic

compo

undsand

insome

casese

venAlip

hatic

arom

atichydrocarbo

ns

Sulfatesulfite

thiosulfate

Freshw

aterB

rackish

waterM

arineand

Haloalkalineh

abitats

[77]

Desulfosporosinus

acidophilus

25ndash4

036ndash

52(52)

H2lactatepyruvate

glycerolglucose

and

fructose

Sulfate

Sedimentfrom

anacid

effluent

pond

[26]

Desulfosporosinus

acididuran

s15ndash4

038ndash70

(55)

H2formatelactate

butyratefum

arate

malatepyruvate

glycerolm

ethano

lethano

lyeastextract

xyloseglucosefructose

Ferriciro

nnitrate

sulfateelem

entalsulfur

thiosulfate

Whiteriv

erdraining

from

theS

oufriere

hills

inMon

serrat(pH32)

[78]

a Valuesc

losedby

parenthesis

arec

onsid

ered

optim

alpH

ndno

tinformed

byconsultedreference

14 BioMed Research International

such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO

2[33]

In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO

2and H

2[17]

D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]

4 Natural Attenuation for the Design of AMDRemediation Strategies

Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and

chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH

2O)were detected presumably due

to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not

Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]

5 Concluding Remarks

Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools

Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico

BioMed Research International 15

(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)

References

[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013

[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014

[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012

[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008

[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011

[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003

[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000

[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014

[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006

[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005

[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007

[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008

[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008

[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015

[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013

[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006

[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006

[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014

[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008

[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006

[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010

[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005

[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016

[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999

[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001

[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010

[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990

[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016

[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014

[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009

[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

14 BioMed Research International

such agarThe advantage ofAc aromatica is its use of a limitedrange of organic donors and that it does not grow on yeastextract glucose glycerol or many other small molecularweight organic compounds that are commonly metabolizedby acidophilic heterotrophic microorganisms Overlay platesare considered to be more versatile and efficient particularlyfor isolating acidophilic sulfidogens from environmentalsamples given that these microorganisms cannot completelymetabolize the substrate [20] Using this technique aSRB andnonsulfidogens have been isolated from acidic sulfidogenicbioreactors Two acidophilic sulfidogens (Desulfosporosinus(D) acididurans and Peptococcaceae strain CEB3) and strainIR2 were all isolated from a low pH sulfidogenic bioreactorat different stages of operation previously inoculated withan undefined microbial mat found at abandoned coppermine in Spain [3] Although not yet fully characterizedPeptococcaceae CEB3 appears to be a more thermotolerantand acidophilic SRB that can oxidize glycerol to CO

2[33]

In addition D acididurans grew successfully togetherwith Ac aromatica in a pH controlled bioreactor showingan example of microbial syntrophy where this heterotrophicbacterium converted acetic acid into CO

2and H

2[17]

D acididurans tolerates relatively high concentrations ofaluminum and ferrous iron and can grow in a pH range of38ndash7 with and optimum pH at 55 The temperature rangefor growth was 15ndash40∘C with (optimum pH at 30∘C) andit can use ferric iron nitrate sulfate elemental sulfur andthiosulfate as electron acceptors [78] D acidophilus thesecond acidophilic SRB validly described [26] isolated froma sediment sample collected in a decantation pond receivingacidmine effluent (pH sim 30) showed high tolerance to NaClSRB belonging to the genus Desulfosporosinus are known tothrive in low pH environments together with members ofthe closely related genus Desulfitobacterium which have alsobeen detected in reactors operating at low pH InterestinglyDesulfitobacterium is a genus with members that can usesulfite as electron acceptor but not sulfate Some bacteriaphylogenetically related to sulfur reducers have been alsodetected in AMD bioreactors as well in natural acidic con-ditions [29]

4 Natural Attenuation for the Design of AMDRemediation Strategies

Natural remediation of metal pollutants generally involvesthe catalytic action of microbial activities that can acceler-ate the precipitation reaction of soluble toxic compoundsresulting in their accumulation in precipitates [81] Suchinformation fromnatural systems can be useful for the designof engineered systems Natural attenuation of transitionmetals in AMD has been described for example at theCarnoules mine in France [81] and the Iberian Pyrite Belt(IPB) in Spain [10] Rowe and colleagues [82] described indetail such process at a small site at the abandonedCantarerascopper mine which is located in theTharsis mine district inthe IPBThey reported that SRB other thanDesulfosporosinusspp were responsible for precipitating copper (as CuS) ina microbial mat found at the bottom layer and dissolvedorganic carbon (DOC) originated from photosynthetic and

chemosynthetic primary producers serving as substrates forthe aSRB The pH of AMD obtained from this bottomlayer was extremely acidic (pH lt 3) and the dark greycoloration was due to the accumulation of copper sulfidepresumably as a result of biosulfidogenesis No iron sulfides(eg hydrotroilite FeSsdotnH

2O)were detected presumably due

to the low pH of the mine water even at depth Because thesolubility product of CuS (log Ksp at 25∘C is minus359) is muchlower than that of FeS (minus188) this sulfidemineral precipitatesin acidic waters whereas FeS does not

Furthermore Sanchez-Andrea and colleagues [83] describedin detail the importance of sulfidogenic bacteria of the TintoRiver sediments (Spain) and their role in attenuating acidmine drainage as an example of performing natural biore-mediation The results showed that for attenuation in layerswhere sulfate reducing genera such as Desulfosporosinusand Desulfurella were abundant pH was higher and redoxpotential and levels of dissolved metals and iron were lowerThey suggested that sulfate reducers and the consequentprecipitation of metals as sulfides biologically drive theattenuation of acid rock drainage Lastly the isolation andfurther understanding of anaerobic acidophiles in naturalenvironments such as Cantareras and Rio Tinto have ledto the proposal of new approaches to selectively precipitatetoxic metals from AMD turning a pollution problem into apotential source of metals [3 83]

5 Concluding Remarks

Mining companies are increasing the extraction of mineralresources guided by a higher market demand and also sup-ported by productivity improvement resultant from advanceson prospection and extraction technologies Increased pro-duction consequently results in a higher generation ofresidues that is a global concern The mining process hasbeen significantly developed however pollution is still one ofthe main challenges of the mining industry and will requireinnovative management tools

Given the fact that protecting aquatic and terrestrialecosystems from pollutants generated from mine wastes isa major concern new strategies must be employed such asthe application of robust and empirically design bioreactorsas part of an integrated system for remediation of acidicmine water and metal recovery Using novel acidophilic andacid-tolerant sulfidogenic microorganisms that are the keycomponents for bioremediation and knowledge about themicrobial interactions that occur in extremely acidic metal-rich environments will help in the development of newmethods for bioremediation purposes

Conflicts of Interest

The authors declare that there are no conflicts of interestregarding the publication of this paper

Acknowledgments

The authors acknowledge the financial support by Con-selho Nacional de Desenvolvimento Cientıfico e Tecnologico

BioMed Research International 15

(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)

References

[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013

[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014

[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012

[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008

[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011

[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003

[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000

[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014

[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006

[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005

[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007

[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008

[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008

[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015

[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013

[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006

[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006

[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014

[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008

[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006

[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010

[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005

[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016

[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999

[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001

[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010

[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990

[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016

[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014

[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009

[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

BioMed Research International 15

(CNPq) to Jose O Siqueira and Guilherme Oliveira and Valeand the sponsorship of SENAISESI Innovation Call IvanNancucheo is supported by Fondecyt Chile (no 11150170)

References

[1] D B Johnson ldquoDevelopment and application of biotechnolo-gies in the metal mining industryrdquo Environmental Science andPollution Research vol 20 no 11 pp 7768ndash7776 2013

[2] TChen B YanC Lei andXXiao ldquoPollution control andmetalresource recovery for acid mine drainagerdquo Hydrometallurgyvol 147-148 pp 112ndash119 2014

[3] I Nancucheo and D B Johnson ldquoSelective removal of tran-sition metals from acidic mine waters by novel consortia ofacidophilic sulfidogenic bacteriardquoMicrobial Biotechnology vol5 no 1 pp 34ndash44 2012

[4] BDold ldquoSustainability inmetalmining Fromexploration overprocessing to mine waste managementrdquo Reviews in Environ-mental Science and Biotechnology vol 7 no 4 pp 275ndash2852008

[5] I Nancucheo and D B Johnson ldquoSignificance of microbialcommunities and Interactions in Safeguarding reactive minetailings by ecological engineeringrdquo Applied and EnvironmentalMicrobiology vol 77 no 23 pp 8201ndash8208 2011

[6] D B Johnson and K B Hallberg ldquoThe microbiology of acidicmine watersrdquo Research in Microbiology vol 154 no 7 pp 466ndash473 2003

[7] D K Nordstrom ldquoAdvances in the hydrogeochemistry andmicrobiology of acid mine watersrdquo International GeologyReview vol 42 no 6 pp 499ndash515 2000

[8] P K Sahoo S Tripathy M K Panigrahi and S M Equeenud-din ldquoGeochemical characterization of coal and waste rocksfrom a high sulfur bearing coalfield India Implication for acidand metal generationrdquo Journal of Geochemical Exploration vol145 pp 135ndash147 2014

[9] A Akcil and S Koldas ldquoAcid Mine Drainage (AMD) causestreatment and case studiesrdquo Journal of Cleaner Production vol14 no 12-13 pp 1139ndash1145 2006

[10] J S Espana E L Pamo E S Pastor J R Andres and JA M Rubı ldquoThe natural attenuation of two acidic effluentsin Tharsis and La Zarza-Perrunal mines (Iberian Pyrite BeltHuelva Spain)rdquo Environmental Geology vol 49 no 2 pp 253ndash266 2005

[11] E Burtnyski Double Threat of Cyanide Leach Mining and AcidMine Drainage (AMD) Imperils the Futaleufu River Valley-Kinross Gold and Geocom Resources Responsible Mine TailingsSudbury Ontario Canada 2007

[12] M Adams R Lawrence and M Bratty ldquoBiogenic sulphidefor cyanide recycle and copper recovery in gold-copper oreprocessingrdquo Minerals Engineering vol 21 no 6 pp 509ndash5172008

[13] G Muyzer and A J M Stams ldquoThe ecology and biotechnologyof sulphate-reducing bacteriardquo Nature Reviews Microbiologyvol 6 no 6 pp 441ndash454 2008

[14] D K Nordstrom D W Blowes and C J Ptacek ldquoHydro-geochemistry and microbiology of mine drainage An updaterdquoApplied Geochemistry vol 57 pp 3ndash16 2015

[15] P K Sahoo K Kim S M Equeenuddin and M A Pow-ell ldquoCurrent approaches for mitigating acid mine drainagerdquoReviews of environmental contamination and toxicology vol226 pp 1ndash32 2013

[16] D B Johnson A M Sen S Kimura O F Rowe and K BHallberg ldquoNovel biosulfidogenic system for selective recoveryof metals from acidic leach liquors and waste streamsrdquo Trans-actions of the Institutions of Mining and Metallurgy Section CMineral Processing and Extractive Metallurgy vol 115 no 1 pp19ndash24 2006

[17] S Kimura K B Hallberg and D B Johnson ldquoSulfidogenesisin low pH (38-42) media by a mixed population of acidophilicbacteriardquo Biodegradation vol 17 no 2 pp 159ndash167 2006

[18] S Hedrich and D B Johnson ldquoRemediation and selectiverecovery ofmetals fromacidicminewaters using novelmodularbioreactorsrdquo Environmental Science and Technology vol 48 no20 pp 12206ndash12212 2014

[19] M Koschorreck ldquoMicrobial sulphate reduction at a low pHrdquoFEMS Microbiology Ecology vol 64 no 3 pp 329ndash342 2008

[20] T Jong and D L Parry ldquoMicrobial sulfate reduction undersequentially acidic conditions in an upflow anaerobic packedbed bioreactorrdquo Water Research vol 40 no 13 pp 2561ndash25712006

[21] E Jameson O F Rowe K B Hallberg and D B JohnsonldquoSulfidogenesis and selective precipitation of metals at lowpH mediated by Acidithiobacillus spp and acidophilic sulfate-reducing bacteriardquo Hydrometallurgy vol 104 no 3-4 pp 488ndash493 2010

[22] D B Johnson and K B Hallberg ldquoAcid mine drainage remedi-ation options A reviewrdquo Science of the Total Environment vol338 no 1-2 pp 3ndash14 2005

[23] I Sanchez-Andrea A J M Stams J Weijma et al ldquoA case insupport of implementing innovative bio-processes in the metalmining industryrdquo FEMSMicrobiology Letters vol 363 no 11 pp1ndash4 2016

[24] J Boonstra R van Lier G Janssen H Dijkman and C J NBuisman ldquoBiological treatment of acid mine drainagerdquo ProcessMetallurgy vol 9 no C pp 559ndash567 1999

[25] T Pumpel and K M Paknikar ldquoBioremediation technologiesfor metal-containing wastewaters using metabolically activemicroorganismsrdquoAdvances in AppliedMicrobiology vol 48 pp135ndash169 2001

[26] D Alazard M Joseph F Battaglia-Brunet J-L Cayol and BOllivier ldquoDesulfosporosinus acidiphilus sp nov A moderatelyacidophilic sulfate-reducing bacterium isolated from acid min-ing drainage sedimentsrdquo Extremophiles vol 14 no 3 pp 305ndash312 2010

[27] RAGyure AKonopkaA Brooks andWDoemel ldquoMicrobialsulfate reduction in acidic (pH 3) strip-mine lakesrdquo FEMSMicrobiology Letters vol 73 no 3 pp 193ndash201 1990

[28] I Nancucheo O F Rowe S Hedrich and D B Johnson ldquoSolidand liquid media for isolating and cultivating acidophilic andacid-tolerant sulfate-reducing bacteriardquo FEMS MicrobiologyLetters vol 363 no 10 Article ID fnw083 2016

[29] I Sanchez-Andrea J L Sanz M F M Bijmans and A J MStams ldquoSulfate reduction at low pH to remediate acid minedrainagerdquo Journal of Hazardous Materials vol 269 pp 98ndash1092014

[30] J M Senko G Zhang J T McDonough M A Bruns and WD Burgos ldquoMetal reduction at low pH by a Desulfosporosi-nusspecies Implications for the biological treatment of acidicmine drainagerdquo Geomicrobiology Journal vol 26 no 2 pp 71ndash82 2009

[31] M Diez-Ercilla J Sanchez-Espana I Yusta KWendt-Potthoffand M Koschorreck ldquoFormation of biogenic sulphides in the

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

16 BioMed Research International

water column of an acidic pit lake biogeochemical controls andeffects on trace metal dynamicsrdquo Biogeochemistry vol 121 no3 pp 519ndash536 2014

[32] C Falagan I Yusta J Sanchez-Espana and D B JohnsonldquoBiologically-induced precipitation of aluminium in syntheticacidmine waterrdquoMinerals Engineering vol 106 pp 79ndash85 2017

[33] A L Santos and D B Johnson ldquoThe effects of temperature andpH on the kinetics of an acidophilic sulfidogenic bioreactor andindigenous microbial communitiesrdquo Hydrometallurgy vol 168pp 116ndash120 2017

[34] F Battaglia-Brunet C Crouzet A Burnol S Coulon DMorinand C Joulian ldquoPrecipitation of arsenic sulphide from acidicwater in a fixed-film bioreactorrdquoWater Research vol 46 no 12pp 3923ndash3933 2012

[35] A P Florentino J Weijma A J M Stams and I Sanchez-Andrea ldquoSulfur Reduction in Acid Rock Drainage Environ-mentsrdquo Environmental Science and Technology vol 49 no 19pp 11746ndash11755 2015

[36] B Gazea K Adam and A Kontopoulos ldquoA review of passivesystems for the treatment of acid mine drainagerdquo MineralsEngineering vol 9 no 1 pp 23ndash42 1996

[37] D Trumm ldquoSelection of active and passive treatment systemsfor AMD - Flow charts for New Zealand conditionsrdquo NewZealand Journal of Geology and Geophysics vol 53 no 2-3 pp195ndash210 2010

[38] J Taylor S Pape and N Murphy ldquoA summary of passiveand active treatment technologies for acid and metalliferousdrainage (AMDrdquo in Proceedings of the in Fifth Australian work-shop on Acid Mine Drainage Fremantle Werstern Australia2005

[39] A RoyChowdhury D Sarkar and R Datta ldquoRemediationof Acid Mine Drainage-Impacted Waterrdquo Current PollutionReports vol 1 no 3 pp 131ndash141 2015

[40] J Skousen ldquoA brief overview of control and treatment technolo-gies for acid mine drainage with special emphasis on passivesystemsrdquo in Proceedings of theWest VirginiaMine Drainage TaskForce Symposium Morgantown WV USA 2016

[41] J Skousen C E Zipper A Rose et al ldquoReview of PassiveSystems for Acid Mine Drainage Treatmentrdquo Mine Water andthe Environment vol 36 no 1 pp 133ndash153 2017

[42] V Seervi H L Yadav S K Srivastav and A Jamal ldquoOverviewof Active and Passive Systems for TreatingAcidMineDrainagerdquoIARJSET vol 4 no 5 pp 131ndash137 2017

[43] W Zillig K O Stetter and W Schaefer ldquoThermoproteales Anovel type of extremely thermoacidophilic anaerobic archae-bacteria isolated from Icelandic solfatarasrdquo Zentralblatt furBakteriologieAllgemeine Angewandte und Okologische Microbi-ologie Abt1 OrigC Hyg vol 2 no 3 pp 205ndash227 1981

[44] H Huber H Jannasch R Rachel T Fuchs and K OStetter ldquoArchaeoglobus veneficus sp nov a novel facultativechemolithoautotrophic hyperthermophilic sulfite reducer iso-lated from abyssal black smokersrdquo Systematic and AppliedMicrobiology vol 20 no 3 pp 374ndash380 1997

[45] T Itoh K-I Suzuki andTNakase ldquoThermocladiummodestiusgen nov sp nov a new genus of rod-shaped extremelythermophilic crenarchaeoterdquo International Journal of SystematicBacteriology vol 48 no 3 pp 879ndash887 1998

[46] T Itoh K-I Suzuki P C Sanchez and T Nakase ldquoCaldivirgamaquilingensis gen nov sp nov a new genus of rod- shapedcrenarchaeote isolated from a hot spring in the PhilippinesrdquoInternational Journal of Systematic Bacteriology vol 49 no 3pp 1157ndash1163 1999

[47] J Vornolt J Kunow K O Stetter and R K Thauer ldquoEnzymesand coenzymes of the carbon monoxide dehydrogenase path-way for autotrophic CO

2fixation in Archaeoglobus lithotroph-

icus and the lack of carbon monoxide dehydrogenase in theheterotrophic A profundusrdquo Archives of Microbiology vol 163no 2 pp 112ndash118 1995

[48] Y Boucher H Huber S LrsquoHaridon K O Stetter and WF Doolittle ldquoBacterial origin for the isoprenoid biosynthesisenzyme HMG-CoA reductase of the archaeal orders ther-moplasmatales and archaeoglobalesrdquo Molecular Biology andEvolution vol 18 no 7 pp 1378ndash1388 2001

[49] H Huber ldquoHyperthermophilesgeochemical and industrialimplications in Biohydrometallurgical technologies Fossilenergy materials bioremediation microbial physiologyrdquo inProceedings of an International Biohydrometallurgy SymposiumTorma M L Apel C L Brierley and A E Torma Eds pp495ndash505 1996

[50] S Burggraf H W Jannasch B Nicolaus and K O StetterldquoArchaeoglobus profundus sp nov represents a new specieswithin the sulfate-reducing archaebacteriardquo Systematic andApplied Microbiology vol 13 no 1 pp 24ndash28 1990

[51] K O Stetter ldquoArchaeoglobus fulgidus gen nov sp nov a newtaxon of extremely thermophilic archaebacteriardquo Systematicand Applied Microbiology vol 10 no 2 pp 172-173 1988

[52] H Moussard S LrsquoHaridon B J Tindall et al ldquoTher-modesulfatator indicus gen nov sp nov a novel ther-mophilic chemolithoautotrophic sulfate-reducing bacteriumisolated from the Central Indian Ridgerdquo International Journalof Systematic and Evolutionary Microbiology vol 54 no 1 pp227ndash233 2004

[53] C Jeanthon S LrsquoHaridon V Cueff A Banta A-L Reysenbachand D Prieur ldquoThermodesulfobacterium hydrogeniphilum spnov a thermophilic chemolithoautotrophic sulfate-reducingbacterium isolated from a deep-sea hydrothermal vent at Guay-mas Basin and emendation of the genus Thermodesulfobac-teriumrdquo International Journal of Systematic and EvolutionaryMicrobiology vol 52 no 3 pp 765ndash772 2002

[54] E C Hatchikian and J G Zeikus ldquoCharacterization of anew type of dissimilatory sulfite reductase present in theThermodesulfobacterium communerdquo Journal of Bacteriologyvol 153 no 3 pp 1211ndash1220 1983

[55] J G Zeikus M A Dawson and T E Thompson ldquoMicrobialecology of volcanic sulphidogenesis Isolation and characteri-zation of Thermodesulfobacterium commune gen nov and spnovrdquo Journal of General Microbiology vol 129 no 4 pp 1159ndash1169 1983

[56] J Sonne-Hansen and B K Ahring ldquoThermodesulfobacteriumhveragerdense sp nov andThermodesulfovibrio islandicus spnov two thermophilic sulfate reducing bacteria isolated from aIcelandic hot springrdquo Systematic and Applied Microbiology vol22 no 4 pp 559ndash564 1999

[57] K Mori H Kim T Kakegawa and S Hanada ldquoA novellineage of sulfate-reducing microorganisms Thermodesulfo-biaceae fam nov Thermodesulfobium narugense gen novsp nov a new thermophilic isolate from a hot springrdquoExtremophiles vol 7 no 4 pp 283ndash290 2003

[58] T Aullo A Ranchou-Peyruse B Ollivier and M MagotldquoDesulfotomaculum spp and related gram-positive sulfate-reducing bacteria in deep subsurface environmentsrdquo Frontiersin Microbiology vol 4 article 362 2013

[59] A H Kaksonen S Spring P Schumann R M Kroppenstedtand J A Puhakka ldquoDesulfotomaculum thermosubterraneum

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

BioMed Research International 17

sp nov a thermophilic sulfate-reducer isolated from an under-ground mine located in a geothermally active areardquo Interna-tional Journal of Systematic and Evolutionary Microbiology vol56 no 11 pp 2603ndash2608 2006

[60] Y Liu T M Karnauchow K F Jarrell et al ldquoDescription of twonew thermophilic Desulfotomaculum spp Desulfotomaculumputei sp nov from a deep terrestrial subsurface and Desul-fotomaculum luciae sp nov from a hot springrdquo InternationalJournal of Systematic Bacteriology vol 47 no 3 pp 615ndash6211997

[61] D P Moser T M Gihring F J Brockman et al ldquoDesulfo-tomaculum and Methanobacterium spp dominate a 4- to 5-kilometer-deep faultrdquoApplied and Environmental Microbiologyvol 71 no 12 pp 8773ndash8783 2005

[62] C D Ogg and B K Patel ldquoDesulfotomaculum varum sp nova moderately thermophilic sulfate-reducing bacterium isolatedfrom a microbial mat colonizing a Great Artesian Basin borewell runoff channelrdquo 3 Biotech vol 1 no 3 pp 139ndash149 2011

[63] W J Robertson J P Bowman P D Franzmann andB J Mee ldquoDesulfosporosinus meridiei sp nov a spore-forming sulfate-reducing bacterium isolated from gasolene-contaminated groundwaterrdquo International Journal of Systematicand Evolutionary Microbiology vol 51 no 1 pp 133ndash140 2001

[64] Y-J Lee C S Romanek and J Wiegel ldquoDesulfosporosi-nus youngiae sp nov a sporeforming sulfate-reducing bac-terium isolated from a constructed wetland treating acid minedrainagerdquo International Journal of Systematic and EvolutionaryMicrobiology vol 59 no 11 pp 2743ndash2746 2009

[65] R Bartha ldquoSulfate Reducers Revisited The Sulphate-ReducingBacteria J R Postgaterdquo BioScience vol 35 no 5 pp 319-3191985

[66] H Sass J Overmann H Rutters H-D Babenzien andH Cyp-ionka ldquoDesulfosporomusa polytropa gen nov sp nov a novelsulfate-reducing bacterium from sediments of an oligotrophiclakerdquo Archives of Microbiology vol 182 no 2-3 pp 204ndash2112004

[67] E A Henry R Devereux J S Maki et al ldquoCharacterizationof a new thermophilic sulfate-reducing bacterium - Thermod-esulfovibrio yellowstonii gen nov and sp nov its phylogeneticrelationship to Thermodesulfobacterium commune and theirorigins deep within the bacterial domainrdquo Archives of Microbi-ology vol 161 no 1 pp 62ndash69 1994

[68] B Ollivier C E Hatchikian G Prensier J Guezennec andJ-L Garcia ldquoDesulfohalobium retbaense gen nov sp nova halophilic sulfate-reducing bacterium from sediments of ahypersaline lake in Senegalrdquo International Journal of SystematicBacteriology vol 41 no 1 pp 74ndash81 1991

[69] B Ollivier B K C Patel and J-L Garcia ldquoDesulfohalobiumrdquoin Bergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[70] K E Duncan L M Gieg V A Parisi et al ldquoBiocorrosivethermophilic microbial communities in Alaskan North Slopeoil facilitiesrdquo Environmental Science and Technology vol 43 no20 pp 7977ndash7984 2009

[71] T N Zhilina G A Zavarzin F A Rainey E N Pikuta G AOsipov andNA Kostrikina ldquoDesulfonatronovibrio hydrogen-ovorans gen nov sp nov an alkaliphilic sulfate-reducingbacteriumrdquo International Journal of Systematic Bacteriology vol47 no 1 pp 144ndash149 1997

[72] E V Pikuta ldquoDesulfonatronum lacustre gen nov sp nov Anew alkaliphilic sulfate-reducing bacterium utilizing ethanolrdquoMikrobiologiya vol 67 no 1 pp 123ndash131 1998

[73] J Kuever F A Rainey and F Widdel ldquoDesulfovibriordquo inBergeyrsquos Manual of Systematics of Archaea and Bacteria JohnWiley amp Sons Ltd 2015

[74] K A DeWeerd G Todd Townsend and J M Suflita ldquoDesul-fomonilerdquo in Bergeyrsquos Manual of Systematics of Archaea andBacteria John Wiley amp Sons Ltd 2015

[75] J Kuever et al ldquoThe Family Syntrophobacteraceaerdquo in TheProkaryotes Deltaproteobacteria and Epsilonproteobacteria ERosenberg et al Ed pp 289ndash299 Springer Berlin HeidelbergBerlin Heidelberg Germany 2014

[76] K Brysch C Schneider G Fuchs and F Widdel ldquoLithoau-totrophic growth of sulfate-reducing bacteria and descrip-tion of Desulfobacterium autotrophicum gen nov sp novrdquoArchives of Microbiology vol 148 no 4 pp 264ndash274 1987

[77] F Widdel Anaerober Abbau von Fettsauren und Benzoesauredurch neu isolierte Arten sulfat-reduzierender Bakterien Georg-August-Universitat zu Gottingen 1980

[78] I Sanchez-Andrea A J M Stams S Hedrich I Nancucheoand D B Johnson ldquoDesulfosporosinus acididurans sp novan acidophilic sulfate-reducing bacterium isolated from acidicsedimentsrdquo Extremophiles vol 19 no 1 pp 39ndash47 2015

[79] M Dopson and D B Johnson ldquoBiodiversity metabolism andapplications of acidophilic sulfur-metabolizing microorgan-ismsrdquo Environmental Microbiology vol 14 no 10 pp 2620ndash2631 2012

[80] P Norris and W Ingledew ldquoAcidophilic bacteria adaptationsand applicationsrdquo in Molecular biology and biotechnology ofextremophiles R J Herbert RAaS Ed pp 115ndash142 SpringerScience+Business media Glasgow Scotland 1992

[81] O Bruneel A Volant S Gallien et al ldquoCharacterization of theActive Bacterial Community Involved in Natural AttenuationProcesses in Arsenic-Rich Creek SedimentsrdquoMicrobial Ecologyvol 61 no 4 pp 793ndash810 2011

[82] O F Rowe J Sanchez-Espana K B Hallberg and D BJohnson ldquoMicrobial communities and geochemical dynamicsin an extremely acidic metal-rich stream at an abandonedsulfide mine (Huelva Spain) underpinned by two functionalprimary production systemsrdquo Environmental Microbiology vol9 no 7 pp 1761ndash1771 2007

[83] I Sanchez-Andrea K Knittel R Amann R Amils and J LSanz ldquoQuantification of Tinto river sediment microbial com-munities Importance of sulfate-reducing bacteria and their rolein attenuating acid mine drainagerdquo Applied and EnvironmentalMicrobiology vol 78 no 13 pp 4638ndash4645 2012

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Submit your manuscripts athttpswwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 201

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Molecular Biology International

GenomicsInternational Journal of

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The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

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BioinformaticsAdvances in

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Signal TransductionJournal of

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BioMed Research International

Evolutionary BiologyInternational Journal of

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Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

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Genetics Research International

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Advances in

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Nucleic AcidsJournal of

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Stem CellsInternational

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Enzyme Research

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International Journal of

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