319

15.1 Introduction 15.2 Microbially Infl uenced Corrosion

15.2.1 Metal Corrosion

15.2.2 Microbially Induced

Concrete Corrosion

15.3 Acid Mine Drainage and Metal Recovery

15.3.1 Acid Mine Drainage

15.3.2 Metal Recovery

15.3.3 Desulfurization of Coal

15.4 Biomethylation of Metals and Metalloids

15.5 Nitrous Oxide and Earth’s Atmosphere

15.6 Nitrate Contamination of Groundwater

15.7 Composting Questions and Problems References and Recommended

Readings

Consequences of Biogeochemical Cycles Gone Wild David C. Herman and Raina M. Maier

15.1 INTRODUCTION

In Chapter 14 the basic biogeochemical cycles for carbon, nitrogen, sulfur, and iron were introduced. Without inter-ference, these cycles have remained stable for thousands to millions of years and the changes that have occurred did so very slowly. The increasing need for food and energy by a growing human population has interfered with these natural

Chapter 15

cycles, in some cases accelerating or in some cases slow-ing part of a cycle. As a result, there have been detrimental impacts on a global scale. For instance, microbial activities can accelerate the formation of “ greenhouse ” gases such as carbon dioxide, methane, and nitrous oxide, which contribute to global warming ( Table 15.1 ). There has been direct impact on such microbial activities through human actions as shown in Table 15.2 . These impacts can be costly both in economic

TABLE 15.1 Global Atmospheric Concentrations of Selected Greenhouse Gases

Microbially mediated/Anthropogenic(parts per million)

Anthropogenic only(parts per trillion)

CO 2 CH 4 N 2 O SF 6 a CFC b

Preindustrial 278 0.700 0.275 0 0

2004 377 1.789 0.319 5.22 c 794

Atmospheric lifetime (years)

50–200 12 114 3200 45–100

Data used in this table are from the Carbon Dioxide Information Analysis Center, which is supported by the U.S. Department of Energy Climate Change Research Division, http://cdiac.ornl.gov/ . a SF 6 � sulfur hexafl uoride. b CFC � CFC-11 (trichlorofl uoromethane) and CFC-12 (dichlorodifl uoromethane). c Value is from 2001.

Environmental MicrobiologyCopyright © 2000, 2009 by Academic Press. Inc. All rights of reproduction in any form reserved.

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PART | IV Microbial Communication, Activities, and Interactions with Environment and Nutrient Cycling320

and societal terms. For example, corrosion of metal and con-crete pipes destroys infrastructure, which is costly in terms of dollars, but these same processes result in the corrosion of historical stone and ceramic statues and artifacts ( Fig. 15.1 ).

Not all impacts of changing these cycles are detrimen-tal. In fact, some activities of the biogeochemical cycles have been used to our benefit. This is illustrated by the use

of sulfur-oxidizing bacteria to aid in the recovery of metals such as gold, copper, and uranium from ore. Yet another illustration is the use of microbial degradation activities in composting or remediation of contaminated sites.

The objective of this chapter is to examine some of the detrimental and beneficial aspects of accelerated com-ponents of biogeochemical cycles that pose, or help us solve, modern pollution problems. The examples examined include: metal and concrete corrosion; acid mine drainage and metal recovery; methylation of metals; nitrous oxide and global warming; nitrate contamination of groundwater; biogenesis of halomethanes; and composting.

15.2 MICROBIALLY INFLUENCED CORROSION

15.2.1 Metal Corrosion

Microbially mediated corrosion damage can occur on metal structures submersed in water or wet soil environments, such as the hulls of ships, pipelines that carry water and oil products, and infrastructure in general (bridges, airports, hazardous waste storage facilities, etc.). The resulting cost of preventing and repairing corrosion in the United States alone is estimated to be $276 billion per year ( Koch et al ., 2002 ). It is not clear what percentage of this figure can be ascribed to microorganisms. However, there are estimates that microbially influenced metal corrosion accounts for 15 to 30% of the corrosion failures in the gas and nuclear industries. It is a major cause of pipeline failures in water

TABLE 15.2 Examples of Human Actions on Biogeochemical Activities and the Consequences

Human action Microbial activity impacted Consequence

Waste disposal in landfi lls Anaerobic biodegradation of organics in the waste

Release of methane to the atmosphere

Fertilizer application Nitrifi cation (NH 4 � → NO 3

� ) Nitrate contamination of groundwater

Denitrifi cation (NO 3 � → N 2 O and N 2 ) Release of nitrous oxide to the atmosphere

Mining Microbial oxidation of iron- and sulfur-bearing minerals

Formation of acid mine drainage

Creation of metal-containing infrastructure (buildings, ships, bridges, pipelines, etc.)

Microbial oxidation of iron in combination with sulfate-reducing bacteria

Corrosion of metal infrastructure components

Creation of concrete sewer pipes Microbial oxidation of sulfur combined with sulfate-reducing bacteria

Corrosion of concrete

Manufacturing processes (chemicals, semiconductors, etc.) that produce metal waste

Microbial methylation Changes in metal toxicity and bioaccumulation

Fossil fuel burning None—fossil fuel reservoirs were created by photosynthetic activity on early Earth and until mined are relatively inert

Release of CO 2 to the atmosphere

FIGURE 15.1 Microbially influenced deterioration of an angel statue above the “ Peters ” Portal on the cathedral of Cologne (Germany), documented by the original object in 1880 (photo by Anselm Schmitz, Cologne) and the respective weathered statue in 1993 (Photo by Dombaumeister Prof., Dr. A. Wolff, Cologne). Used with permission from Warscheid and Krumbein, 1996 .

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321Chapter | 15 Consequences of Biogeochemical Cycles Gone Wild

treatment and chemical industries and is also associated with corrosion failures that cause leaking underground gas-oline storage tanks, oil pipelines, and oil storage containers ( Dowling and Guezennec, 1997 ).

Although the mechanisms and scale of microbially influ-enced corrosion are still not fully understood, a common mechanism by which sulfate-reducing bacteria (SRB) are thought to influence corrosion has been described ( Dowling and Guezennec, 1997 ). SRB are active under strictly anaer-obic conditions, utilizing sulfate instead of oxygen in the respiration of organic compounds (Section 14.4.4). SRB-mediated corrosion requires anaerobic conditions, but oxy-gen is often present in the environment surrounding a metal surface. However, when biofilms (Section 6.2.4) form on the metal surface, anaerobic microsites can develop within the biofilm. These sites occur as a result of rapid oxygen utili-zation by bacteria in the outer layers of the biofilm coupled with a slow rate of oxygen diffusion through the exopoly-mer matrix. These anaerobic biofilm microsites support the growth and activity of SRB, which ultimately cause the metal surface to corrode. Because SRB are common con-stituents of natural environments, the use of natural water sources in cooling towers or the pumping of oil from under-ground reservoirs serves to inoculate metal pipeline surfaces with SRB.

Metal corrosion is initiated by two spontaneous elec-trochemical reactions. In the first reaction (Eqs. 15.1 and 15.2), a differential aeration cell is set up in which the metal surface acts as the anode to produce metal ions, and in the corresponding cathodic reaction oxygen accepts the elec-trons produced from the oxidation of elemental iron:

Anodic reaction: Fe Fe e0 2 2� � �� (Eq. 15.1)

Cathodic reaction: O H O e OH12 2 2 2 2� � � ��

(Eq. 15.2)

In the second reaction (Eqs. 15.3 and 15.4) a concentra-tion cell is created under anaerobic conditions in which the

anodic reaction remains the same but the cathodic reaction produces H 2 :

Anodic reaction: Fe Fe e0 2 2� � �� (Eq. 15.3)

Cadthodic reaction: H e H H2 2 2 2� �� � � (Eq. 15.4)

Microbially influenced corrosion refers to the involvement of biofilms in stimulating these electrochemical reactions ( Hamilton, 1995 ). How do microorganisms, specifically SRB, participate in this process? First of all, as already mentioned, a biofilm is formed on the metal surface that facilitates the establishment of these separate electrochemical reactions by establishing an anaerobic environment at the metal sur-face ( Lappin-Scott and Costerton, 1989 ; Hamilton, 1995 ) ( Fig. 15.2 ). Second, SRB utilize H 2 as an electron donor (see Section 14.4.4), thereby removing it from the environment and providing a driving force for the anodic reaction. Finally, the end product of sulfate reduction is sulfide (S 2 � ), which reacts with Fe 2 � to form metal sulfide precipitate:

Step 1 Fe 2 � � 2H 2 O → Fe(OH) 2 ↓ � H 2 (spontaneous)

Step 2 4H 2 � SO 4 2 � → H 2 S � 2OH � � 2H 2 O

(SRB, e.g., Desulfovibrio desulfuricans )

Step 3 H 2 S � Fe 2 � → FeS↓ � H 2 (spontaneous)

Overall 2Fe 2 � � SO 4 2 � � 2H 2 →

FeS↓ � Fe(OH) 2↓ � 2OH �

Other mechanisms also contribute to microbially influ-enced corrosion. For example, the biofilm matrix is thought to contribute to corrosion by trapping corrosion products including organic acids and metal species at the metal–biofilm interface. As a result of all of these corrosion pro-cesses, pits and cracks appear on the metal surface that eventually compromise the integrity of the metal structure.

How can microbially influenced corrosion be controlled? There are basically two strategies. The first is to coat the metal surface with bactericidal chemicals. These include quaternary ammonia compounds, phenolic compounds, surface-active substances, and metals such as copper.

Sulfate reducing bacteria-2 -24H + SO 4H O + S2 4 2

2+ 2-Fe + S FeS

Anodic reaction0 2+ -Fe Fe � 2e

Cathodic reaction--O + 2H O + 4e 4OH2 2

Cathodic reaction- -O + 2H O + 4e 4OH2 2

Iron oxidizing bacteria2+ +Fe � 1/2O � 5 H O 2Fe(OH) � 4H2 2 3

O2

O2

O2

2-SO4

2-SO4

2+Fe2+Fe

-e-e

Iron oxidizersSulfate reducers

Biofilm

Metal surface

FIGURE 15.2 General representation of microbially influenced corrosion of a metal surface. Adapted from Hamilton, 1995 .

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PART | IV Microbial Communication, Activities, and Interactions with Environment and Nutrient Cycling322

However, these compounds can leach into the surrounding environment, raising concern about their use. The sec-ond strategy is to disrupt the organization of surface bio-films, thus removing the microenvironment that supports the activity of SRB. Disinfectant chemicals, such as chlo-rine (see Chapter 26), and addition of cationic surfactants are used to control microbial growth in pipelines, but these chemicals are more effective in killing planktonic cells than in destroying biofilms. Further, the high chlorine concen-trations required to destroy biofilms may have undesirable side effects. The oil industry uses an additional step besides chemical biofilm disruption, namely, mechanical scraping (pigging) of the inside surface of pipes. Regular treatment is required because of biofilm regrowth.

15.2.2 Microbially Induced Concrete Corrosion

Microbially induced concrete corrosion (MICC) occurs through the biogenic production of acid that reacts with binders that hold concrete together ( Roberts et al ., 2002 ). The binding components of concrete are acid sensitive, and therefore microbes that produce acidic metabolites contribute to this type of corrosion as well as to corrosion of other acid-sensitive ceramic and natural stone objects ( Fig. 15.1 ). Different forms of acidic metabolites are pro-duced by microorganisms, but evidence seems to implicate the sulfur-oxidizers and production of sulfuric acid as the major culprit in MICC (Section 14.4.3.1).

A well-documented consequence of MICC is the failure of concrete sanitary sewer pipes. There are thousands of miles of sewer pipes in any major city, and corrosion of these pipes has cost hundreds of millions of dollars in damage and replacement costs ( Sydney et al ., 1996 ). Sewer pipes are corroded from the inside out by a two-step process involving both sulfate-reduc-ing (SRB) and sulfur-oxidizing bacterial populations that cycle sulfur as described in Section 14.4 ( Fig. 15.3 ). Pipes carrying sewage can contain two distinct environments, namely, the liq-uid sewage and the headspace area. In the liquid environment, anaerobic conditions are created by the high rate of microbial activity in the organic-rich sewage. Under anaerobic conditions, the SRB generate sulfide, which is converted to the volatile H 2 S form and exchanged across the liquid–headspace interface. In the aerobic and moist environment of the headspace, sulfide-oxidizing bacteria colonizing the concrete wall surface oxidize H 2 S to sulfuric acid. Moisture condensation along the inside of the sewer pipe walls improves the habitat for microbial activity.

One study investigated the microbial community dynam-ics of MICC ( Okabe et al ., 2007 ). This group placed con-crete coupons (small samples of concrete), for a period of one year, into a sewer pipe in Hachinohe, Japan, that exhib-ited severe corrosion ( Fig. 15.4 ). During this time, they measured the pH of the coupon surfaces and followed development of the microbial community. Their work indi-cates that MICC occurs in three stages. There was an initial

decrease in pH from 12 to 8.2 that took place over a period of 56 days. This was followed, on days 56–102, by a continued decrease in pH from 8.2 to 1.6 and the appearance and suc-cession of neutrophilic sulfur-oxidizers including Thiothrix (grows at neutral pH), Thiobacillus plumbophilus (pH 4–6.5), Thiomonas (pH 5–7.5), and Halothiobacillus (pH 4.5–8.5). The third stage, during which the pH remained at 2, was characterized by the visible corrosion of the concrete and the appearance and dominance of the acidophilic sulfur-oxidizer Acidithiobacillus thiooxidans (grows at pH 2).

What is the actual corrosion process? Corrosion occurs when sulfuric acid reacts with the calcium hydroxide binder in the concrete to form calcium sulfate (gypsum), which is a soft, expansive compound with no binding capa-bility ( Fig. 15.4C ) ( Sydney et al ., 1996 ):

H SO Ca(OH) CaSO H O2 4 2 4 22� �→ (Eq. 15.5)

Mori et al . (1992) found that maximum corrosion occurred just above the sewage liquid level and that corrosion on the crown of the pipe was also evident. Near the surface of corroded concrete (0 to 4 mm depth), the population of Acidithiobacillus thiooxidans was found to reach almost 100,000 cells per gram of concrete, and their activity cre-ated a highly acidic environment. The pH of water mois-ture in corroded concrete was reduced to around 2. In the zones of highest activity, the corrosion rate was estimated to be between 4.3 and 4.7 mm per year. Thus, over a 12-year period of use, the thickness of a sewer pipe can be reduced from 88 mm to between 32 and 36 mm. This rate of corrosion effectively reduces the life expectancy of con-crete sewer pipes to approximately 20 years.

Two approaches have been used to control sewer pipe-line corrosion ( Sydney et al ., 1996 ). One approach is to treat the sewage liquid to prevent the production of H 2 S. This type of treatment may include the use of caustic soda

FIGURE 15.3 Cross section showing microbial involvement in the corrosion of a concrete sewer pipe. Adapted from Sydney et al ., 1996 . Reprinted with permission of the Water Environment Federation.

Corrosion

H S2

H S2

H SO2 4 H SO2 4

Aerobic sulfide oxidation

Anaerobic sulfate reduction

Sewageliquid

Concrete pipe

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323Chapter | 15 Consequences of Biogeochemical Cycles Gone Wild

to inhibit microbial growth or the addition of alternative electron acceptors, such as iron (e.g., ferric chloride) or oxy-gen, to inhibit SRB activity competitively. An alternative approach is to neutralize the surface of the concrete above the sewage liquid level by spraying the concrete with a high-pH solution, such as a magnesium hydroxide slurry ( Sydney et al ., 1996 ).

15.3 ACID MINE DRAINAGE AND METAL RECOVERY

15.3.1 Acid Mine Drainage

As discussed in Section 14.4.1, pyrite (FeS 2 ) is a major source of sulfur in the lithosphere. During strip mining of metal-containing ore deposits and of bituminous coal, pyrite is exposed to oxygen and moisture and becomes the source of an acidic, iron-rich leachate known as acid mine drainage (AMD) ( Fig. 15.5 ). Acid mine drainage can have a pH of less than 2, and at that pH metal solubility is greatly increased. So as AMD moves through a site con-taining ore with high metal content, metal concentrations in the AMD increase considerably. As a result of low pH and in some cases high metal content, AMD seriously impairs the quality of receiving waters, such as surface streams or rivers.

Two mining practices have exacerbated AMD forma-tion. The first is strip mining, an activity that uncovers and exposes large surface areas to the atmosphere. Mining also generates large amounts of waste pyrite-containing rock or mine tailings. Tailings are the less valuable rock that remains after the material of interest, such as metal-bearing minerals, has been removed. Deposition of these tailings in open impoundments where they are exposed to air and

FIGURE 15.5 A stream in central Appalachia affected by AMD as a result of coal mining. AMD directly impacts aquatic life as well as the potability of the water. In this photo, large amounts of iron in the AMD changes the color of the stream to red. From Appalachian Center for the Economy and the Environment, 2008.

FIGURE 15.4 Concrete coupons exposed to a sewer atmosphere that contained gaseous H 2 S con-centrations of 30 ppm for 42 days (A), 102 days (B), and 1 year (C and D), showing the progression of concrete corrosion. From Okabe, S., et al. (2007).

(A) (B)

(D)(C)

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PART | IV Microbial Communication, Activities, and Interactions with Environment and Nutrient Cycling324

rainwater is a second practice that results in the formation of AMD. As a result of past mining activities and millions of tons of tailings remaining from abandoned mining oper-ations, AMD currently affects 10,000 miles of waterways on the East Coast of the United States alone.

The formation of acid from pyrite ore is a complex mechanism that involves the oxidation of both iron and sul-fur. The initial reaction leading to the formation of AMD is the spontaneous chemical oxidation of pyrite:

4 14 44 8 8

2 2 2

3 4

FeS (pyrite) O H OFe (OH) SO H2 2

� �

� �� � � �

→ (Eq. 15.6)

This process is initiated spontaneously, but as the local pH drops, a sulfur- and iron-oxidizing bacterium, Acidithioba-cillus ferrooxidans , also begins to participate in the reaction. A. ferrooxidans is a chemoautotroph that derives energy for carbon fixation and growth from the oxidation of inor-ganic sulfur- and iron-containing compounds, such as pyrite (Section 14.4.3.1). This organism is unusual in that its pH optimum is around 2. A. ferrooxidans is an extensively stud-ied microorganism because it is easily cultured from AMD and because it is used in metal recovery. It has been shown to attach directly to the pyrite crystal lattice and there utilize FeS 2 as an electron donor ( Ehrlich, 1996 ). Other microbes, such as the thermophilic archaea Sulfolobus and Acidianus , are also associated with AMD. These are acidophilic chemo-lithotrophs capable of maximal growth around pH 1.5 to 2.5 ( Ehrlich, 1996 ). Because oxidation of pyrite is an exother-mic reaction, temperatures within tailings impoundments can build until they exceed 60°C ( Brierley and Brierley, 1997 ). Acidithiobacillus ferrooxidans is a mesophile, oxi-dizing inorganic substrates in a temperature range around 10 to 40°C. Temperatures above this range create a selective advantage for the thermophilic archaea, which then begin to predominate in the formation of acid mine drainage.

The ferrous iron (Fe 2 � ) formed by the oxidation of pyrite will, in a neutral aerobic environment, spontane-ously oxidize to the ferric iron form (Fe 3 � ):

2 2 22 12 2

32Fe O H Fe H O� � �� � �→ (Eq. 15.7)

This is the rate-limiting step in the formation of acid leach-ates. The autoxidation of Fe 2 � is a very slow process. Alternatively, A. ferrooxidans can oxidize Fe 2 � . Because its pH optimum is 2, at first the microbial contribution to iron oxidation is small. But as the pH decreases, the microbial contribution grows and the reaction begins to occur more rapidly.

The oxidized iron formed in Eq. 15.7 can have three fates. It can be precipitated as iron oxide, a reaction that generates more acid:

Fe H O Fe(OH) H32 33 3� �� �� � (Eq. 15.8)

Alternatively, the ferric iron can aid in the further chemical oxidation of pyrite:

FeS (pyrite) Fe H OFe SO H

23

22

42

14 815 2 16� �

� �

�

� � �

→

(Eq. 15.9)

Note that this reaction produces acid and regenerates reduced or ferrous iron, which can then be reoxidized by A. ferroxidans (Eq. 15.7). Finally, there are heterotrophic acidophilic iron-reducers such as Sulfobacillus thermosul-fidooxidans, S. acidophilus , and Acidimicrobium ferrooxi-dans that can use ferric iron as a terminal electron acceptor in dissimilatory iron reduction ( Baker and Banfield, 2003 ). This process also helps regenerate ferrous iron for use in Eq. 15.7 (Section 14.5.5).

This combination of microbially and chemically medi-ated reactions creates a loop that speeds the oxidation of pyrite. Overall, these reactions can be summarized as

4 15 144 8 16

2 2 2

3 42

FeS (pyrite) O H OFe(OH) SO H

� �

� �� �

→� (Eq. 15.10)

Thus, the leachate produced is highly acidic and contains high levels of a dark brown ferrous hydroxide precipitate. Ferric iron remaining in the leachate can, in the presence of sulfate and a monovalent cation such as potassium, pre-cipitate as a complex sulfate mineral, KFe 3 (SO 4 ) 2 (OH) 6 , which is a yellow-brown product characteristic of AMD ( Brierley and Brierley, 1997 ). In addition, the leachate can contain other acid-soluble elements including aluminum, which can be toxic to aquatic organisms. The leachate is carried by surface water and groundwater flow into receiv-ing stream and river waters.

As already mentioned, acid mine drainage can have a pH of less than 2. The actual pH depends on the rate of growth of the pyrite-oxidizing bacteria, which in turn depends on environmental factors such as the amount of rainfall, nitro-gen availability, temperature, and pH conditions ( Ehrlich, 1996 ). The amount of acid produced is also dependent on the mineral composition of the tailings. Acid-consuming reactions can occur, which neutralize the pH to some extent. These reactions include the dissolution of carbonate miner-als, such as calcite and dolomite; the formation of gypsum; and the bacterial oxidation of certain metal sulfides, such as copper and zinc sulfides ( Brierley and Brierley, 1997 ). The balance between acid-generating and acid-consuming reac-tions influences the final pH of tailings leachate.

Abatement actions to remediate acid mine drainage are best applied as the tailings are being produced to pre-vent the initiation of pyrite oxidation. Prevention meth-ods focus on restricting the exposure of tailings to oxygen and moisture, such as capping or encapsulating tailings with low-permeability material, such as clay. Other meth-ods include mixing tailings with acid-consuming rocks to neutralize acid production and depositing tailings on

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325Chapter | 15 Consequences of Biogeochemical Cycles Gone Wild

impermeable material so that acid leachate can be collected and treated. It may also be possible to treat acid mine drainage using engineered environments such as wetlands that promote the activity of the sulfate-reducing bacteria ( Southam et al ., 1995 ). The SRB can neutralize drainage waters by utilizing sulfate as an electron acceptor during anaerobic respiration of a supplied carbon source, such as acetate. The sulfides produced will also contribute to acid drainage abatement by the precipitation of divalent metal ions as metal sulfides.

15.3.2 Metal Recovery

The reactions just described for formation of AMD that are so environmentally damaging can be harnessed in a controlled way for use in metal recovery from metal sul-fide ores and in the desulfurization of coal. As high-grade ore deposits become increasingly scarce, the recovery of metals from remaining low-grade deposits becomes more important. As it is less economical to smelt low-grade ores, microbially mediated metal recovery has become an attrac-tive alternative to smelting ( Agate, 1996 ). Bioleaching is considered environmentally friendly in that it requires less energy and does not produce sulfur dioxide during the extraction process ( Rawlings, 2002 ).

Metal recovery using acidophilic iron- and sulfur-oxidizers (e.g., Acidithiobacillus, Leptospirillum, Acidi-philium ) has become a well-understood, efficient, and cost-effective process ( Rawlings, 2002 ). As of 1989, more than 30% of U.S. copper and uranium production was microbially mediated. Microorganisms can participate in both direct bioleaching and indirect bioleaching of metals from a variety of ores. Copper is the major metal recov-ered using bioleaching. Example reactions for removal of

copper from ores such as chalcopyrite (CuFeS 2 ), chalcocite (CuS 2 ), and covellite (CuS) are as follows:

Direct leaching MS O MSO� 2 2 4→ (Eq. 15.11)

where M represents the metal being leached. An example of direct leaching is the recovery of copper from chalcocite as shown in Eq. 15.12. Note that energy is provided to the microbe by the oxidation of Cu � to Cu 2 � , and there is no change in the valence of sulfur ( Atlas and Bartha, 1993 ).

2 4 2 2 22 22Cu S O H CuS Cu

chalcocite covellite leached copper

� � � �� �→ HH O2

(Eq. 15.12)

More important overall are the indirect metal leaching reactions:

CuS Fe (SO ) CuSO FeSO S� � �2 2 42 4 3 4 40→

(Eq. 15.13)

2 41

2 2 2 4 2 4 3 2FeSO O H SO Fe (SO ) H O� � �→ (Eq. 15.14)

where copper is spontaneously oxidized by the presence of the ferric ion (Fe 3 � ) and acid (Eq. 15.13), and then the resulting ferrous iron (Fe 2 � ) is reoxidized biologically by A. ferrooxidans (Eq. 15.14). Finally, the copper ions (Cu 2 � ) can be recovered from the solution by spontaneous precipi-tation in the presence of scrap iron:

Cu Fe Fe Cu2 0 2 0� �� �→ (Eq. 15.15)

There are two commercial-scale approaches for bioleaching ( Rawlings, 2002 ). The first is used primarily for copper and involves recycling leach liquor through a copper sulfide ore body. As shown in Figure 15.6 , this can be done in situ or on ore heaps placed on pads on the ground. In situ bioleaching

Crushed ore

Dump or heapleaching

In-place leaching

New ore body Disused mine

Metal recovered byprecipitation electrolysis

Metal-rich leachsolution

Barren leachsolution containing

iron-oxidizers

Recycle acidic leachsolution

Pumpout

Pumpout

ore body

FIGURE 15.6 Various approaches to bioleaching. Metals can be recovered from ores that are in place in the ground if the hydrological conditions permit, or in dumps or heaps on the ground. Some of the heaps can be hundreds of feet high. In each case, an acidic leach solution created and maintained by iron-oxidiz-ers is flushed through the ore, dissolving the metals. The metal-laden leachate is subjected to a precipita-tion or electrolysis process to remove the metal and then the spent leach solution is recycled back onto the ore body.

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can occur either in a spent mine or can be applied to a new unmined ore body. However, in situ bioleaching requires suitable hydrologic conditions to allow efficient collection of the leachates and to ensure that leachates do not go off-site. Heap bioleaching or dump bioleaching usually involves mining the ore, crushing it, and then placing it in piles on an irrigation pad. The leach liquor is applied to the top of the heap and percolates through the ore, collecting metals. The metal-laden leach liquor is collected from the bottom of the pile, processed to remove the metals, and then recycled onto the top of the pile again.

The second commercial-scale approach for bioleaching involves the use of a series of continuous-flow bioreactors, a much more costly process. This process is usually used for high value metals such as gold. However, the principle is the same—the bioreactors are filled with ore and leach liquor is cycled through the bioreactors to remove the met-als from the ore ( Rawlings, 2002 ).

15.3.3 Desulfurization of Coal

A second controlled process that utilizes the activity of sulfur-oxidizing bacteria is the microbial desulfurization of coal. The problem here is that coal reserves can con-tain high levels of sulfur-containing compounds. In fact, as cleaner coal reserves are utilized, much of the remaining coal resources contain higher levels of sulfur. As a result, when the coal is burned to generate energy, sulfur com-pounds are released to the atmosphere as sulfur dioxide (SO 2 ). In the atmosphere, SO 2 combines with water to form sulfuric acid (H 2 SO 4 ), which lowers the pH of the water, forming acid rain.

One strategy that is being developed as a solution to this problem is to use natural sulfur-oxidizing microbial activ-ity (Eq. 15.11) to oxidize, solubilize, and remove inorganic sulfur from coal by leaching. The most important inorganic sulfur compound in coal is pyrite so the removal process is much like that discussed for metal recovery ( Bos et al ., 1992 ). Unfortunately, this only addresses part of the prob-lem. Sulfur is actually found in two forms in coal: inor-ganic sulfur as discussed earlier, or in an organic form, most commonly as dibenzothiophene ( Fig. 15.7 ). Both forms of

sulfur contribute to SO 2 emissions during coal burning—their relative importance depends on the coal deposit and the type of sulfur it contains. Although sulfur-oxidizer activ-ity will remove inorganic sulfur, it does not remove organic sulfur forms. So an additional approach to microbial desul-furization is being investigated that uses heterotrophic bac-teria to carry out the degradation of the organic sulfur forms (e.g., dibenzothiophene; Cara et al ., 2007 ).

15.4 BIOMETHYLATION OF METALS AND METALLOIDS

Metals cycle not only between their oxidized and reduced forms but also between inorganic and organic forms. As already discussed for the iron cycle (Section 14.5), microorganisms mediate redox cycling of metals. They also mediate the transformation of metals between their organic and inorganic forms. Methylation is the microbi-ally mediated linking of a methyl group (—CH 3 ) to a metal or metalloid element, thus forming an organometal(loid) compound. Some of the metal(loid)s that are known to be methylated include arsenic, mercury, selenium, lead, nickel, and tin. The problem is that methylation greatly alters the physical and chemical properties as well as the toxicity of a metal(loid). This has a major effect on the fate and biologi-cal impact of metal(loid)s in the environment. For example, the methylated form of metal(loid)s is more volatile and more soluble in lipids. The latter property means that meth-ylated metal(loid)s that enter a cell will partition into cel-lular lipids, resulting in their bioaccumulation through the food chain (Fig. 21.3).

Mercury is an example of a metalloid that increases in toxicity when methylated. Trace levels of mercury are pres-ent in soil and sediments, and higher concentrations are released into the environment through industrial activities. The most common form of mercury released to the envi-ronment is the divalent form, Hg 2 � . In the aquatic environ-ment, the organic-rich sediment becomes a natural sink for Hg 2 � . Biomethylation of mercury occurs in the sedi-ments of lakes, rivers, and estuaries, where organic matter concentrations are high and redox conditions are favor-able for the activity of sulfate-reducing bacteria. In fact, the primary generators of methylmercury in the environ-ment are believed to be the sulfate-reducing bacteria ( Drott et al ., 2007 ). The most important intracellular agent of mercury methylation is believed to be methylcobalamine (CH 3 CoB 12 ), a derivative of vitamin B 12 . Methylation reac-tions can be summarized as follows ( Compeau and Bartha, 1985 ; Gadd, 1993 ):

CH CoB Hg H O CH Hg H OC

methylcobalamine methylmercury

3 122

2 3 2� � �� �→ ooB12�

(Eq. 15.16)

S

Dibenzothiophene

FIGURE 15.7 Dibenzothiophene, the most common organic form of sulfur found in coal.

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327Chapter | 15 Consequences of Biogeochemical Cycles Gone Wild

CH CoB CH Hg H O (CH ) Hg

methylcobalamine dimethylmercur

3 12 3 2 3 2� �� →yy

H OCoB� �2 12

(Eq. 15.17)

The dominant product formed is the salt of the methylmer-curic ion, CH 3 Hg � (methylmercury) because the volatile dimethylmercury, (CH 3 ) 2 Hg, forms at a much slower rate. Microbially mediated reactions affecting the fate of Hg 2 � are shown in Figure 15.8 .

The reason for the methylation of mercury by bacteria is not fully understood, although it has been suggested to be an accidental process ( Drott et al ., 2007 ). It has also been postulated that it is a detoxification mechanism. For example, the methylation of selenium to methylselenides results in compounds that are less toxic, less reactive, and more readily excreted from the cell (see Case Study 21.1). In the case of mercury, methylation increases toxicity but also may facilitate diffusion of both methylmercury and dimethylmercury from the cell more easily than Hg 2 � ( Gadd, 1993 ). Still, the most common mechanism used by microorganisms to resist mercury toxicity is not meth-ylation but the enzymatic reduction of Hg 2 � to elemental mercury (Hg 0 ). Elemental mercury is less toxic than Hg 2 � and is also volatile and thus can be removed from the envi-ronment of the cell.

The environmental significance of mercury methyla-tion is the fate of methylmercury within the aquatic food chain. Methylation converts sediment-associated Hg 2 � into an organometal that has greater lipid solubility. Methylated mercury can partition into lipophilic cell components and can accumulate to high levels in fish and shellfish. Human consumption of contaminated fish and shellfish concentrates

the mercury present in the fish further and, with continued consumption of fish, can gradually accumulate to toxic lev-els. This is undesirable because mercury is a strong neuro-toxin and, if ingested in high enough levels by humans, can be fatal (Case Study 15.1).

One area of concern is the flooding of terrestrial envi-ronments in order to create water reservoirs ( Bodaly et al ., 1997 ). Fish in certain newly created reservoirs, particularly in subarctic environments, have shown unexpectedly high levels of mercury in their tissue. The source of the mercury in fish in these sites is the accumulation of methylmercury in the aquatic food chain. Although mercury occurs naturally in the soil and vegetation that was flooded, this mercury was methylated, and made more bioavailable, by microbial activ-ity in the anoxic sediments created when the vegetation-rich terrain was flooded. Thus, although very low levels of available mercury were present in the environment before flooding, the methylation of mercury and the process of bioaccumulation in the food chain has resulted in mercury levels in fish that exceed accepted concentrations for safe human consumption.

15.5 NITROUS OXIDE AND EARTH’S ATMOSPHERE

The agricultural practice of adding nitrogen, either as chemical or manure fertilizer, to soil is a major contribu-tor to the gradual increase in N 2 O emissions to the atmo-sphere, although other sources of N 2 O in the atmosphere include burning of biomass, combustion of fossil fuels, and

To atmosphere Bioaccumulationin food chain

To atmosphere

volatile

oHg

Spontaneous reactionwith biogenic H2SOxidation

2+Hg +CH Hg3 (CH ) Hg3 2

HgS

Methylation

Demethylation

Methylation

DemethylationChemicalreaction

Reduction

FIGURE 15.8 Microbially mediated reactions with Hg 2 � in the environment. Hg 2 � can be reduced to elemental Hg 0 by chemical reaction with humic acids or by microbially mediated reactions that are believed to be a detoxification mechanism. Hg 2 � can be precipitated by reaction with sulfide (S 2 � ) produced under sulfate-reducing conditions but can also be released by microbial oxidation of HgS. Methylation of Hg 2 � produces organometals, which can accumulate in the tissues of living organisms. The production of organometals may to some extent be balanced by demethylation reac-tions occurring in both aerobic and anaerobic environments. Based on Gadd, 1993 , and Ehrlich, 1996 .

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PART | IV Microbial Communication, Activities, and Interactions with Environment and Nutrient Cycling328

chemical manufacturing of nylon ( Mosier et al ., 1996 ). The source of nitrogen in fertilizers is mainly ammonia or ammonium-producing compounds such as urea. However, normally only about half the total nitrogen as applied to a field as fertilizer or manure is assimilated by the crop ( Delgado and Mosier, 1996 ). The remaining nitrogen is lost through leaching, erosion, gaseous emissions, and microbial activity. Due to microbial activity about 1% of the nitrogen applied is released to the atmosphere ( Lessard et al ., 1996 ). This activity includes two steps, both of which have the potential to produce N 2 O. The first is nitri-fication, a process in which ammonium is chemoautotro-phically oxidized first to nitrite and then to nitrate (Section 14.3.4). It has been suggested that N 2 O production is asso-ciated with low-oxygen conditions, in which nitrifying bacteria utilize nitrite as an electron acceptor in place of oxygen, as a result reducing NO 2

� to N 2 O ( Conrad, 1990 ). The second step is denitrification, which is the utiliza-tion of nitrate (NO 3

� ) as a terminal electron acceptor dur-ing anaerobic respiration of organic compounds (Section 14.3.5). N 2 O is an intermediate in the reduction of NO 3

� to N 2 , but it can be the end point of nitrate reduction espe-cially in environments where initial nitrate concentrations are low. Thus, N 2 O can be produced as an intermediate both in denitrification and in nitrification. There has been intense interest to determine the relative contributions of denitrification and nitrification processes to N 2 O pro-duction and to determine the environmental factors that control each process.

Why is this a problem? Nitrous oxide gas that is released to the atmosphere from industrial and biogenic sources contributes both to global warming as a greenhouse gas and to the destruction of the protective ozone layer in Earth’s stratosphere ( Table 15.1 ). Greenhouse gases are of concern because they absorb long-wave radiation from the sun after it hits Earth and is reflected back into space. This effectively traps heat in the atmosphere. N 2 O is of concern in two respects. It has a long residence time ( � 100 years)

in the atmosphere, and it is highly efficient in absorbing long-wave radiation. One molecule of N 2 O is equivalent in heat-trapping ability to about 200 molecules of CO 2 . Therefore, small increases in atmospheric N 2 O concentra-tion can have a large impact on warming trends.

A second concern with N 2 O is that in the upper atmo-sphere, solar radiation can photolytically convert N 2 O to nitric oxide (NO), which is a contributor to the depletion of the protective ozone layer ( Fig. 15.9 ). The ozone layer acts as a filter to remove biologically harmful ultraviolet (UV) light. Stratospheric ozone depletion occurs through a chemi-cal interaction between sunlight, ozone, and certain reactive chemical species, including nitrogen oxides and organo-halogens such as CFCs (chlorofluorocarbons). Depletion of the protective ozone layer can have serious ecological and human health consequences. Increased levels of UV radia-tion may be inhibitory to certain microorganisms, such as phytoplankton, and may also increase the incidence of skin cancer in humans. Ozone is depleted in the series of reactions shown in Figure 15.9 , where light energy begins the reaction by splitting nitrous oxide into N 2 and singlet oxy-gen, in which one of the electrons is in a high-energy state. This singlet oxygen can react with nitrous oxide to form two molecules of nitric oxide. Nitric oxide in turn reacts with ozone (O 3 ) to produce nitrogen dioxide and oxygen. The nitrogen dioxide then reacts with singlet oxygen (O*) to pro-duce oxygen and regenerate nitric oxide. The fact that nitric oxide is regenerated in this series of reactions means that for every nitrous oxide molecule released to the atmosphere, a large number of ozone molecules can be destroyed.

As already mentioned, agriculture is a major source of N 2 O emissions. As a result, strategies can be implemented to reduce biogenic N 2 O emissions ( Mosier et al ., 1996 ). A primary factor in N 2 O emissions is the low efficiency of utilization of nitrogen fertilizers, which leaves them subject to nitrification/denitrification processes. Several measures can be taken to increase fertilizer utilization efficiency. The most economical approach is simply to manage the amount

Case Study 15.1 Mercury Poisoning in Minamata Bay, Japan

The most infamous example of mercury poisoning due to the consumption of contaminated fish occurred in Minamata, Japan. Minamata is a small town on the Shiranui Sea where the Chisso Company produced a variety of chemicals includ-ing acetaldehyde. Mercury sulfate was used as a catalyst in the production of acetaldehyde from 1932 to 1968. Following pro-duction, wastes were released into Minamata Bay, including both mercury and methylmercury. The first human poisoning case came to light in the mid-1950s. The symptoms of mercury accumulation in the central nervous system include tremors, inability to coordinate body movements, impairment of vision and speech, as well as liver and kidney damage. Subsequently, thousands of people became poisoned by mercury, with an

official count of 1700 deaths. So what happened in Minamata Bay to make this poisoning so extensive? A number of factors exacerbated this tragedy: the residents of Minamata Bay were largely dependent on fishing for their livelihoods and diets; the fish in Minamata Bay were exposed to and bioaccumlated mer-cury and methylmercury; and the company as well as the gov-ernment ignored and even denied the problem for a long time. Although it is known that mercury was released into Minamata Bay in several forms, the extent to which biological methyla-tion of inorganic mercury contributed to the contamination of the food chain remains unclear. However, incidents of mercury poisoning provide compelling reasons to monitor closely the fate of mercury in natural systems (Kudo et al., 1998).

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329Chapter | 15 Consequences of Biogeochemical Cycles Gone Wild

and time of fertilizer application to a crop ( Thompson, 1996 ). Enough fertilizer must be added to meet crop needs, but overfertilization will result in increased nitrate forma-tion and leaching. A second way to minimize nitrogen losses in irrigated croplands is through control of the timing and amount of irrigation. Remember, although fertilizers generally add nitrogen as ammonia, plants prefer to take up nitrate. However, once ammonia is oxidized to nitrate, it is easily removed from the plant root area by water leaching. Many states in the United States have studied and adopted Best Management Practices (BMPs) for fertilizer applica-tion and irrigation. These BMPs are region specific since climate and soil types change dramatically from region to region. Finally, two other approaches to minimizing nitrate formation and leaching are the use of slow-release fertil-izers, which allow more controlled release of ammonia into the environment, and the application of nitrification inhibi-tors, for example, N-serve (2-chloro-6-(trichloromethyl)pyridine), which suppress the formation of nitrate. However, application of slow-release fertilizers or nitrification inhibi-tors is costly and so neither approach is widely used.

15.6 NITRATE CONTAMINATION OF GROUNDWATER

As just discussed for nitrous oxide emissions, agricultural systems often result in the addition of excess nitrogen to the environment. This can lead to the accumulation of excess nitrate in the environment. Although nitrate does not normally accumulate, agricultural systems that use ammonia fertilizers, or produce large concentrations of ani-mal waste in dairy or feedlot operations, and domestic use of septic tanks result in increase levels of nitrogen in the soil and groundwater environment. Although this nitrogen is normally added as ammonia or the ammonia-containing compound urea, the conversion of ammonia to nitrate by aerobic, chemoautotrophic nitrifying bacteria results in the accumulation of nitrate in many agricultural systems. Because nitrate is an anion, it is very mobile in soil and, when produced in excess of denitrification needs, is eas-ily transported with water flow into groundwater supplies. In fact, according to a recent survey by the Environmental Protection Agency, most states have nitrate levels that

Alti

tude

(K

m)

Stratosphere

Troposphere

Biogenic emission of N O (denitrification and nitrification) 2

and industrial sources

N O2

150-

140-

130-

120-

110-

100-

90-

80-

70-

60-

50-

40-

30-

20-

10-

Photodissociation of N O2

N O + hυ N + O*22

N O + O* 2NO2

Depletion of O3

NO + O NO + O3 2 2

O + hυ O + O23

NO + O NO + O22

2O + hυ 3O23

Ozone formation

O + hυ O + O2

2O + 2O + Μ 2O + Μ32

3O + hυ O32

O + hυ O + O23

O + O 2O23

2O + hυ 3O23

N O2

N O2

N O2

N O2

N O2

N O2

N O2

N O2

N O2

FIGURE 15.9 Equations summarizing ozone formation and the depletion of ozone by reaction with nitric oxide (NO). (left panel) Solar UV radiation (h � ) photodissociates molecular oxygen (O 2 ) into two oxygen atoms (O), which recombine with undissociated O 2 (in the presence of another chemical species, M) to form ozone (O 3 ). Ozone is then photodissociated back to molecular oxygen (O 2 ). The constant cycling between ozone and oxygen is important because it consumes harmful UV radiation in the stratosphere. (middle panel) Nitrous oxide (N 2 O) emitted to the atmosphere is photodissociated to nitro-gen and an oxygen atom in an electronically excited state, O*, which reacts with N 2 O to produce nitric oxide (NO). (right panel) Nitric oxide can react with ozone and, in a series of reactions, produce O 2 , resulting in a net depletion of ozone.

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PART | IV Microbial Communication, Activities, and Interactions with Environment and Nutrient Cycling330

exceed drinking water standards in 1 to 10% of the ground-water wells tested ( Fig. 15.10 ).

As a result, there is concern about potential health effects on humans and animals that use these water sup-plies. One of these effects is a condition called methemo-globinemia or “ blue baby syndrome ” that affects infants less than six months old as well as young animals. The stomachs of these young are not yet acidic enough to prevent the growth of denitrifying bacteria that convert nitrate to nitrite. The nitrite produced binds to hemoglo-bin and prevents the hemoglobin from carrying oxygen throughout the body. This can result in cyanosis, which causes the infant’s skin to turn a bluish color. At its worst methemoglobinemia can result in brain damage or death, although few such cases have been reported. When high nitrate levels in drinking water are suspected and detected, the problem is easy to solve by substituting bottled water. The allowable level of nitrate-nitrogen (NO 3 -N) in water for children six months or younger is 10 mg/1. A second concern about elevated nitrate levels in groundwater is that in adults denitrification of nitrate to nitrite in the stomach can lead to the formation of nitrosamines, which are highly carcinogenic. Although there is no proven link between nitrate consumption and human cancer, in laboratory stud-ies nitrites have been shown to interact with amino com-pounds in the stomach to form N -nitrosamines. Many of these N -nitrosamine compounds have been shown to be carcinogenic in test animals.

15.7 COMPOSTING

Composting is a solid waste disposal technique that has been practiced since ancient times. It has been used to treat a variety of wastes including biosolids, municipal solid waste, food and agricultural wastes, and even hazard-ous wastes ( Table 15.3 ). Essentially, the composting pro-cess turns waste products into an organic soil amendment by taking advantage of the normal microbes found in soil and optimizing their carbon cycling activities. In fact, the spatial characteristics and physical–chemical gradients found in a compost system are very similar to those found in a soil system. But compost and soil systems are distinct in several respects. For example, compost is primarily organic in composition, and the rate of microbial activ-ity is extremely high during compost formation and after it is added to soil. In contrast, in a soil, both organic mat-ter content and microbial activity levels are much lower. In soils, physical factors including temperature, moisture, and bulk density are imposed externally, but in composting systems these factors are controlled internally (Information Box 24.2). Finally, the soil matrix is a very stable one and undergoes change slowly. The compost matrix is organic substrate that undergoes rapid physical change as a result of degradative activities.

As an ecosystem, a compost pile is characterized by high substrate density and diverse and highly interactive micro-bial populations that go through a succession of populations

Risk of Groundwater NitrateContamination (1970–1995)

Low Risk

Alaska

Hawaii

Puerto Rico

Moderate RiskHigh RiskInsufficient Data

FIGURE 15.10 Risk of groundwater nitrate contamination for shallow aquifers in the United States ( � 100 feet in depth). Image courtesy of U.S. EPA. From Pepper et al., 2006.

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331Chapter | 15 Consequences of Biogeochemical Cycles Gone Wild

What parameters are important in composting (see Information Box 24.2)? The carbon to nitrogen (C:N) ratio is one parameter critical to the success of compost-ing. If too high, � 80:1, there is too much carbon and not enough nitrogen. In this case the system must recycle the nitrogen through microbial decomposition, which slows the composting process. If too low, � 10:1, there is an excess of ammonium liberated from the system, resulting in nox-ious odors. Temperature is another factor critical for suc-cessful composting. The elevated temperatures reached in composting are fundamental to the high rate of decomposi-tion but are also important from several other aspects. High temperatures in composting sludge wastes help to kill any viruses and coliform bacteria present, especially those that are added as a part of biosolids or municipal solid waste. High temperatures also help to kill weed seeds and patho-gens, which are an undesirable component of the final com-post product that will be used on lawns and gardens. The optimal temperature for composting is around 60°C. Above 60°C, the temperature optimum for thermophilic growth is exceeded. Above 82°C, activity will be totally inhibited until the compost pile cools down. The success of the com-posting process also depends on the construction of the compost pile. If it is too large, the organic matter will be compressed and the system will become anaerobic. If it is too small, a majority of the heat generated will escape and the rate of decomposition will not be maximized. It is also important to maintain sufficient oxygen levels. If oxygen is depleted, the rate of activity and hence heat generation will slow. Also, under anaerobic conditions, undesirable gaseous degradation products are formed, including carbon com-pounds such as methane and volatile organic acids as well as sulfur and nitrogen compounds such as H 2 S and NH 3 .

The overall process of composting is to build a pile of organic matter that can be easily aerated to maintain aero-bic conditions and to provide a way to cool the compost system. Details of different types of compost systems are

TABLE 15.3 Potential Compost Substrates

Type of compost substrate

Examples

Biosolids 5.6 million dry tons produced per year in the United States (NRC, 2002)

Industrial sludge Food, textile, pulp and paper, pharmaceutical, and petroleum industries

Manure Feedlots, dairies, poultry production

Yard waste Second largest component of U.S. solid waste stream, primarily grass clippings, leaves, and brush

Food and agricultural waste

Fruit and vegetable processing wastes, agricultural residues (e.g., rice and nut hulls, corncobs, cotton gin residues)

Municipal solid waste Production is 4.3 lb/day per capita in the United States, includes paper, food, and yard wastes

Special wastes Hazardous wastes such as TNT, petroleum sludge, and pesticide residues that are incorporated into compost materials

Adapted from Haug, 1993 . Reproduced with permission from CRC Press.

TABLE 15.4 Microbial Populations during Aerobic Composting

Microbial type CFU/g compost (wet weight)

Mesophilic, initial temperature � 40°C

Thermophilic, 40–70°C

Mesophilic, 70°C to cooler

Number of species identifi ed

Mesophilic bacteria 10 8 10 6 10 11 6

Thermophilic bacteria 10 4 10 9 10 7 1

Thermophilic actinomycetes

10 4 10 8 10 5 14

Mesophilic fungi 10 6 10 3 10 5 18

Thermophilic fungi 10 3 10 7 10 6 16

From Haug, 1993 . Reproduced with permission from CRC Press.

dominated first by mesophilic organisms and then by ther-mophiles. As shown in Table 15.4 , the microorganisms found in a compost system are a mixed population of bacte-ria, actinomycetes, and fungi. The numbers of actinomycetes and fungi peak during the thermophilic stage of the com-posting process. Bacteria peak in numbers as the compost system starts to cool. All of these microbes are important components of the system in terms of carbon assimilation.

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PART | IV Microbial Communication, Activities, and Interactions with Environment and Nutrient Cycling332

given in Section 24.7.2.1. Once the compost system is con-structed, the organic matter in the compost pile acts as an insulator and allows heat to build up as the degradation proceeds. As the temperature increases and reaches 40°C, usually after two to three days, the initial mesophilic popu-lations die off and are replaced by thermophilic microbes. Once all of the usable organic material is degraded, decom-position activity slows, as does the generation of heat. After composting is complete, which usually takes three to four weeks, the compost pile cools to ambient temperature.

QUESTIONS AND PROBLEMS

1. Think about the activities involved in the carbon, nitrogen, and sulfur cycles and develop your own idea for applying one of these activities in the commercial sector.

2. As city mayor, you are informed that the concrete sewer system is corroded and will need to be replaced within the next three years. You are running for reelection and the cost of replacing the sewer system means that taxes will have to be raised. How would you explain, in lay terms, to your constituents why the concrete pipes have corroded and justify raising taxes to replace the system?

3. A mine that supports much of the local economy is releasing acid leachates into a receiving stream that eventually feeds a fishery important to local tourism. The concern is that a significant decrease in pH of the fishery waters will affect fish survival. What suggestions would you make to the local mine to (1) prevent acid leachate formation and (2) treat acid leachates before their release so that this does not become an insurmountable problem?

4. Methylation of metals increases their volatility. Is it a good idea to use microbial methylation as a basis for removal of metals such as mercury and selenium from contaminated soils? Support your answer.

5. Municipal sludge or biosolids left after wastewater treatment can be landfilled, combusted, or composted. Discuss the advantages and disadvantages of each approach.

6. Groundwater under cattle feedlot operations is often found to have nitrate contamination. Explain the microbial basis for nitrate contamination of groundwater in these areas.

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Koch, G. H., Brongers, M. P. H., Thompson, N. G., Virmani, Y. P., and Payer, J. H. (2002). Corrosion cost and preventive strategies in the United States. Technical Report # FHWA-RD-01-156.

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Mori , T. , Nonaka , T. , Tazaki , K. , Koga , M. , Hikosaka , Y. , and Noda , S. ( 1992 ) Interactions of nutrients, moisture and pH on microbial corro-sion of concrete sewer pipes . Water Res. 26 , 29 – 37 .

Mosier , A. R. , Duxbury , J. M. , Freney , J. R. , Heinemeyer , O. , and Minami , K. ( 1996 ) Nitrous oxide emissions from agricultural fi elds: Assessment, measurement, and mitigation . Plant Soil 181 , 95 – 108 .

Myrold , D. D. ( 1998 ) Transformations of nitrogen . In “ Principles and Applications of Soil Microbiology ” ( D. M. Sylvia , J. J. Fuhrmann , P. G. Hartel , and D. A. Zuberer , eds.) , Prentice-Hall, Upper Saddle River , NJ , pp. 218 – 258 .

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Okabe , S. , Odagiri , M. , Ito , T. , and Satoh , H. ( 2007 ) Succession of sulfur-oxidizing bacteria in the microbial community on corroding concrete in sewer systems . Appl. Environ. Microbiol. 73 , 971 – 980 .

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