REVIEW PAPER

Applications of microorganisms to geotechnical engineeringfor bioclogging and biocementation of soil in situ

Volodymyr Ivanov Æ Jian Chu

� Springer Science+Business Media B.V. 2008

Abstract Microbial Geotechnology is a new branch

of geotechnical engineering that deals with the

applications of microbiological methods to geological

materials used in engineering. The aim of these

applications is to improve the mechanical properties

of soil so that it will be more suitable for construction

or environmental purposes. Two notable applications,

bioclogging and biocementation, have been explored.

Bioclogging is the production of pore-filling materi-

als through microbial means so that the porosity and

hydraulic conductivity of soil can be reduced.

Biocementation is the generation of particle-binding

materials through microbial processes in situ so that

the shear strength of soil can be increased. The most

suitable microorganisms for soil bioclogging or

biocementation are facultative anaerobic and micro-

aerophilic bacteria, although anaerobic fermenting

bacteria, anaerobic respiring bacteria, and obligate

aerobic bacteria may also be suitable to be used in

geotechnical engineering. The majority of the studies

on Microbial Geotechnology at present are at the

laboratory stage. Due to the complexity, the applica-

tions of Microbial Geotechnology would require an

integration of microbiology, ecology, geochemistry,

and geotechnical engineering knowledge.

Keywords Bacteria � Biocementation �Bioclogging � Geotechnical engineering

1 Introduction

Biogeotechnology is a branch of Geotechnical Engi-

neering that deals with the applications of biological

methods to geotechnical engineering problems. At the

present, biogeotechnologies are related mainly to the

applications of plants or vegetative soil cover for soil

erosion control and slope protection, prevention of

slope failure, and reduction of water infiltration into

slopes. Biogeotechnology have advantages of low

investment and maintenance costs. It also offers

benefits to environment and aesthetics (Karol 2003).

Microbial geotechnology is an emerging branch of

Geotechnical Engineering. Although there are various

potential applications of microorganisms to geotech-

nical engineering, at the present, promising appli-

cations are only concentrated in the bioclogging and

biocementation. Therefore, this review is covering

mainly the recent developments in these two areas.

Bioclogging is to reduce the hydraulic conductiv-

ity of soil and porous rocks due to microbial activity

or products. It could be used to reduce drain channel

erosion, form grout curtains to reduce the migration

of heavy metals and organic pollutants, and prevent

piping of earth dams and dikes.

Biocementation is to enhance the strength and

stiffness properties of soil and rocks though microbial

V. Ivanov (&) � J. Chu

Block N1, School of Civil and Environmental

Engineering, Nanyang Technological University,

50 Nanyang Avenue, Singapore 639798, Singapore

e-mail: cvivanov@ntu.edu.sg

123

Rev Environ Sci Biotechnol

DOI 10.1007/s11157-007-9126-3

activity or products. It could be used to prevent soil

avalanching, reduce the swelling potential of clayey

soil, mitigate the liquefaction potential of sand, and

compact soil on reclaimed land sites.

As the scale of geotechnical construction such as

land reclamation is usually large, a microbial treat-

ment could be one of the most cost effective methods.

The major factors that affect the applications of

microorganisms to geotechnical engineering include

the screening and identification of suitable microor-

ganisms for different applications and different

environments, the optimization of microbial activity

in situ, biosafety of the application, cost effectiveness,

and stability of soil properties after biomodification.

Among all the factors, cost effectiveness is the most

important factor for large-scale application.

As an emerging discipline, microbial geotechnol-

ogy has been developing rapidly in recent years. Some

of the developments have already been summarized

by Baveye et al. (1998), Castainer et al. (1999) and

Mitchell and Santamarina (2005). This review paper

intends to offer an update of the most recent

developments related to bioclogging and biocemen-

tation. The aims are to summarize the existing or

potential applications in these two areas, to compare

advantages and disadvantages of different methods,

and to identify some of the physiological groups of

prokaryotes that could be potentially used effectively

for biocogging and biocementations. This paper is

organized in such a way that the applications related

to bioclogging and biocementation are summarized

first before a method for the screening of the suitable

physiological groups of prokaryotes is suggested.

2 Bioclogging: microbial grouting in situ

for water flow control

Chemical grouting is a process to fill the soil voids

with fluid grouts. It is often used to control water flow

(Karol 2003). Common grouts are solution or

suspension of sodium silicate, acrylates, acrylamides,

and polyurethanes. Industrially produced water-insol-

uble gel-forming biopolymers of microbial origin

such as xantan, chitosan, polyglutamic acid, sodium

alginate, and polyhydroxybutyrate can also be used as

grouts for soil erosion control, enclosing of bioreme-

diation zone, and mitigating soil liquefaction

(Momemi et al. 1999; Yang et al. 1993; Yen et al.

1996; Etemadi et al. 2003; Gioia and Ciriello 2006).

Suitable microorganisms could be applied to soil to

serve the same purpose through microbial growth and

biosynthesis of extracellular biopolymers.

2.1 Microbial products and processes

It has been observed by Vandevivere and Baveye

(1992) and Bonala and Reddi (1998) that accumulation

of bacterial biomass, insoluble bacterial slime, and

poorly soluble biogenic gas bubbles in soil will make

the soil more impermeable for water. Therefore,

bioclogging can be used to seal a leaking construction

pit, landfill, or dike. One of the bioclogging processes

is the microbial production of water-insoluble poly-

saccharides in situ. This can be performed by addition

of carbon source and enriched or pure culture of

microorganisms to soil if necessary. Role of microbial

polysaccharides in soil particles aggregation and

clogging of soil pores is well known. Although a lot

of gel-forming water-insoluble microbial polysaccha-

rides are produced in industry (Sutherland 1990), these

materials cannot be used for soil grouting because of

the high cost involved. Only growth of microorgan-

isms, which were added to soil, and accumulation of

water-insoluble microbial slime from cheap raw

materials in situ can be considered as economically

reasonable option for bioclogging. An addition of

microorganisms must be accompanied with medium

that initiates bioclogging. However, this process could

be complicated by transport of microbial cells into soil,

which depends on cell size, cell surface properties, and

cell physiological state (Murphy and Ginn 2000).

Production of bacterial exopolymers in situ can be

used to modify soil properties. This has been adopted

for enhancing oil recovery or soil bioremediation

(Stewart and Fogler 2001). The groups of microor-

ganisms that produce insoluble extracellular

polysaccharides to bind the soil particles and fill in

the soil pores are oligotrophic bacteria from genus

Caulobacter (Ravenscroft et al. 1991; Tsang et al.

2006), aerobic Gram-negative bacteria from genera

Acinetobacter, Agrobacterium, Alcaligenes, Arcob-

acter, Cytophaga, Flavobacterium, Pseudomonas,

and Rhizobium (Harada 1983; Portilho et al. 2006;

Ross et al. 2001). Other groups of microorganisms

are cellulose-degrading bacteria from species Cellu-

lomonas flavigena (Kenyon et al. 2005) and many

Rev Environ Sci Biotechnol

123

species of Gram-positive facultative anaerobic and

aerobic bacteria, such as Leuconostoc mesenteroides

that is used for the production of a water-insoluble

exopolymer dextran (Stewart and Fogler 2001). The

strains of Cellulomonas flavigena may be suitable for

large scale soil clogging or soil grouting because

these bacteria are Gram-positive (i.e. resistant to the

changes of osmotic pressure) and can utilize cellulose

for the production of a curdlan-type (beta-1,3-glucan)

exopolysaccharide. In this case, such sources of

carbon as cellulose-containing agricultural and hor-

ticultural wastes, and saw dust can be hypothetically

used for the propagation of bacteria in soil and

formation of the pore-clogging polysaccharide.

It is well known that almost all bacteria produce

exopolysaccharides under excess of carbohydrates or

other water soluble sources of carbon over source of

nitrogen (Wingender et al. 1999). Therefore, such

food-processing wastes or sub-products as corn

glucose syrup, cassava glucose syrup and molasses

with C: N ratio [ 20 are used for industrial production

of bacterial water-insoluble polysaccharides (Portilho

et al. 2006).

Probably, nitrifying bacteria that produce extra-

cellular polysaccharides from CO2 of air during

oxidation of ammonium (Stehr et al. 1995) can also

be used for the soil clogging. Almost every natural

nitrifying biofilm contains nitrifying bacteria, which

are embedded into a layer of microbial slime (Ivanov

et al. 2006a). Accumulation of aggregating bacterial

cells in soil pores could also contribute to soil

clogging. Such bacterial strains with fast and strong

cell aggregation are used in wastewater treatment in

fixed biofilm reactors and for the fast formation of

microbial granules (Ivanov et al. 2005; Ivanov 2006;

Ivanov and Tay 2006b).

Exopolysaccharide-producing bacteria may be

used to modify the soil matrix in situ. After growth

of these bacteria in soil, its permeability for water

will be greatly reduced. This approach could be used

for different geotechnical applications such as selec-

tive zonal bioremediation, harbor and dam control,

erosion potential minimization, earthquake liquefac-

tion mitigation, construction of reactive barrier, and

long-term stabilization of contaminated soils (Yang

et al. 1993). Organic wastes can be used as a source

of organic matter for fermenting and exopolysaccha-

ride—producing microorganisms in large-scale

applications to diminish the cost of soil clogging.

For example, municipal solid wastes, sewage

sludge, uncomposted or composted poultry manure

has been added to soil to diminish soil erosion. In

these experiments, a positive correlation between the

stability of soil aggregates and the produced microbial

biomass in soil has been found (Mataix-Solera et al.

2005). It was shown in other experiments that the

introduction of polysaccharide—producing algae and

bacteria in irrigation channel could provide a low cost

technique for seepage control in irrigation channel.

The reduction of hydraulic conductivity by 22% of its

original value within a month of inoculating soil

columns with algae correlated with the amount of

produced polysaccharides (Ragusa et al. 1994).

Laboratory tests have been carried out to identify

the microbial groups that could be used for bioclog-

ging. The study has demonstrated that enrichment

cultures of nitrifying and oligotrophic bacteria can be

used for bioclogging. Enrichment culture of nitrifying

bacteria, grown in sand with dissolved ammonium,

produced microbial polysaccharides from solution of

ammonium and CO2 of air. The application of

ammonium solution decreased the hydraulic conduc-

tivity of sand from 10-4 m/s to 10-6 m/s. Enrichment

culture of oligotrophic bacteria, grown in sand with

low concentration of glucose, produced polysaccha-

rides from solution of glucose and reduced the

hydraulic conductivity of the sand from 10-4 m/s to

10-6 m/s (Ivanov and Chu, unpublished data).

2.2 Field tests and applications

Attempts to use bioclogging to diminish the hydraulic

conductivity of the dams and dykes, to reduce infiltra-

tion from the ponds and leakage in construction sites or

landfills, to prevent soil erosion, and to make a barrier

on soil pollution site have been made (James et al.

2000; Seki et al. 1998, 2005). Microbial plugging

in situ is also used to increase the extent and rate of

heavy oil production by the selective reduction of the

permeability of zones in an oil-bearing underground

formation after injection of exopolymer-producing

microorganisms and carbon source into the oil-bearing

formation (Thompson and Thomas 1984, 1985).

Experimental studies on the reduction of soil

hydraulic conductivity by enhanced biomass growth in

soil with dextrose-nutrient solution have demonstrated

a positive correlation between attached microbial

Rev Environ Sci Biotechnol

123

biomass and the soil hydraulic conductivity (Wu et al.

1997). Field bioclogging tests to reduce soil permeabil-

ity for water and diminish soil erosion have been also

reported (McConkey et al. 1990). If soil has poor

drainage, addition of waste organic matter such as straw

and manure in soil will lead to their microbial aerobic

decomposition and creation of anaerobic conditions in

soil. This soil gleization is accompanied with microbial

reduction of Fe(III) and reduction in soil permeability. It

is considered that the clogging of the soil pores during

gleization is due to the production of exopolysaccha-

rides from the decomposed organic material. However,

soil gleization does not provide satisfactory long-term

seepage control for flooded channels (McConkey et al.

1990). This supports further the above mentioned

conclusion that stable bioclogging is feasible only

under soil conditions favorable for exopolysaccharide-

producing microorganisms, but not favorable for exo-

polysaccharide-degrading microorganisms.

Bouwer (2002) reported that during artificial

recharge of groundwater using surface water, clog-

ging layer of silt on basin bottom was formed. This

type of clogging may also be possible due to the

production of exopolysaccharides by oligotrophic

bacteria in organic–poor soil. Artificial recharge of

groundwater by surface water or effluent of waste-

water treatment plant through permeable soil or sand

could promote growth of oligotrophic bacteria and

formation of clogging layer of their slime.

However, biopolymers clogging could be unstable

because of their biodegradability, thermal sensitivity,

and low mechanical resistance to pressure drop across

the plug. In some cases, biological clogging of porous

media and wells is a significant geotechnical problem

due to negative effect of bioclogging on soil bioreme-

diation, sand filtration, and aquifer recharge (Bonala

and Reddi 1998; Dupin and McCarty 2000; Hajra et al.

2000; Ralph and Stevenson 1995).

Stable bioclogging could be due to precipitation of

inorganic substances in the soil pores, for example,

precipitation of calcium carbonate at increased

pH (Bachmeier et al. 2002; Castanier et al. 1999;

Hammes and Verstraete 2002; Stocks-Fischer and

Galinat 1999). This approach is used in the microbes-

mediated process for reducing the porosity and

permeability of a subsurface geological formation.

Bioclogging due to the precipitation of minerals from

an aqueous system has also been proposed to enhance

the recovery of oil from oil reservoirs or to control the

flow of a spilled contaminant in a reservoir (Ferris and

Stehmeier 1992; Ferris et al. 1996; Fujita et al. 2000).

One promising application is the formation of the

soil plugs by Bacillus pasteurii in the medium

containing urea and calcium chloride. Bacteria pro-

duce enzyme urease that hydrolyzes urea by the

following reaction:

(NH2)2COþ 3H2O! 2NHþ4 þ HCO�3 þ OH�

ð1ÞDue to this enzymatic reaction, pH is increased and

hydrocarbonate is produced. It is initiating precipita-

tion of calcium carbonate, which clogging the pores

and binding soil particles (cited from Kucharski et al.

2005). The bioclogging could be used in the industry to

decrease permeability of porous media, reduce fluid

flow, enhance the recovery of oil from reservoirs (cited

from Kucharski et al. 2005), and repair cracks in

concrete (Ramachandran et al. 2001). For the forma-

tion of new bioclogging materials the following

microbial techniques are used: (a) the bioproduction

of bacterial slime due to supply of saccharides into soil

for the soil obstruction in the dike or dune; (b) bacteria-

mediated transformation of sand to sandstone using

soil bacteria, urea, and calcium ions. Bacteria hydro-

lyse urea to ammonium increasing pH, producing

carbonate, and precipitating calcium as calcium car-

bonate under high pH (http://www.geodelft.com/files/

bacteriabuildbiodikes.pdf and http://www.smartsoils.

nl). A pilot scale test of bioclogging using bioproduc-

ton of slime in soil was successfully carried out in 2004.

After 6 weeks, the hydraulic resistance of soil in

experiment was enhanced by a factor five. Afterwards,

the resistance factor increased further to a value of

about thirty. Even more then 3 months after the last

injection of nutrients, the hydraulic resistance

remained stable. In control container, without injection

of the nutrients, the hydraulic resistance around the

inflow was not decreased (Veenbergen et al. 2005).

Another potential application of bioclogging is sealing

of the unforeseen leaks in the sheet piling screens

around the construction wells, which occur at some

10% of all construction pits dug in the Netherlands. It is

estimated that the cost of solving such problems totals

several tens of millions of euros each year. The injec-

tion of nutrients into the groundwater ensures that it

flows towards the problem area. If needed group of soil

microorganisms is absent in the porous medium, these

Rev Environ Sci Biotechnol

123

microorganisms must be injected or infiltrated into

groundwater.

2.3 Limitations and potential problems

A major lmitation or problem in the use of microbial

polysaccharides in situ is the stability of soil properties

after treatment. Many known microorganisms in soil

can degrade water-insoluble microbial exopolysaccha-

rides. Therefore, a successful and stable bioclogging

process is possible only under soil conditions that are

favorable for exopolysaccharide-producing microor-

ganisms, but not favorable for exopolysaccharide-

degrading microorganisms. One example is the addition

of ammonium to organic-poor soil or sand, stimulating

growth of nitrifying bacteria, which synthesize poly-

saccharides from CO2. Another example is the

production of water-insoluble exopolysaccharides in

organic-poor soil or sand by oligotrophic bacteria at

permanent supply into soil a solution with low concen-

tration of energy and carbon source for bacterial growth

and synthesis of polysaccharides (Ivanov and Chu,

unpublished data).

The cases of clogging of sand-filled and gravel-filled

agricultural drains are well known (Baveye et al. 1998).

This is probably due to the production of exopolysac-

charides by nitrifying bacteria, oxidizing ammonium in

agricultural drainage. A problem in the application of

nitrifying and oligotrophic bacteria is that they are slow

growing organisms with low rate of exopolysaccharide

production and their applications will require long-term

treatment of soil for its clogging. For example, duration

of exponential accumulation of biomass in soil by

1,000 times from the initial content is from 69 to

690 days when the growth rate of nitrifying or oligo-

trophic bacteria in situ is ranging from 0.1 d-1 to

0.01 d-1. Any temporarily shortage of ammonia or

oxygen will significantly decrease the growth rate and

content of ammonia-oxidizing bacteria in treated soil

because the decay rate of ammonia-oxidizing bacteria

under ammonia or oxygen depletion is from 0.08 to

0.55 d-1 (Geets et al. 2006), which is comparable with

the growth rate of these bacteria in situ. Therefore,

bioclogging of soil with water-insoluble exopolysac-

charides could be used in cases where the long duration

of bioclogging does not limit the application.

Another potential problem of microbial clogging

in situ is that the penetration of microbial cells in

soil depth is limited by the minimum soil pore size

from 0.5 to 2 lm. Therefore, the method can be

used for limited soil types with suitable hydraulic

conductivity.

One more problem is that the growth of clogging

biofilm in soil pores affects the concentrations and

mass transfer rates of nutrients and microbial metab-

olites between biofilm and flow through the pores

(Baveye et al. 1998; Rodgers et al. 2004; Ross et al.

2001; Sharp et al. 1999). Concentration of dissolved

oxygen is the most sensitive parameter in soil

clogging. Although, concentrations of carbon, nitro-

gen, and phosphorous sources, and metabolites such

as hydrocarbonate and organic acids will also affect

significantly the rate of microbial growth and activity

of clogging microorganisms in soil.

Secondary microbial products can be produced

during bioclogging, for example, organic acids due to

fermentation or nitrate due to nitrification. All

residual products of bioclogging must be removed

from soil or converted to neutral products like water,

carbon dioxide, and nitrogen gas.

2.4 Summary on bioclogging

Different possible microbial processes that can lead

potentially to bioclogging are summarized in Table 1.

These include formation of impermeable layer of

algal and cyanobacterial biomass; production of slime

in soil by aerobic and facultative anaerobic heterotro-

phic bacteria, oligotrophic microaerophilic bacteria

and nitrifying bacteria; production of undissolved

sulphides of metals by sulphate-reducing bacteria;

formation of undissolved carbonates of metals by

ammonifying bacteria; and production of ferrous

solution and precipitation of undissolved ferrous and

ferric salts and hydroxides in soil by iron-reducing

bacteria. Not all of these processes have been tested in

the laboratory and in the field.

3 Biocementation: structural microbial grouting

in situ

Chemical cementation (or chemical grouting) is to fill

the sand voids with fluid chemical grouts to produce

sandstone like masses to carry loads. This method is

widely used in geotechnical engineering (Indraratna

Rev Environ Sci Biotechnol

123

and Chu 2005). The chemicals that are used to bind

soil particles include sodium silicate, calcium chlo-

ride, calcium hydroxide (lime), cement, acrylates,

acrylamides, polyurethanes (Karol 2003).

Microbial cementation (or structural microbial

grouting) is to form soil particle-binding material

after introduction of microbes and specific additives

into soil. It is different from biobinding, which is

formation of the particle-binding cellular chains.

Biobinding can be performed by mycelial fungi,

actynomycetes, and filamentous phototrophic and

heterotrophic bacteria. In some experiments, the

added biomass of some fungal strains binds the sand

grains and increases the shear strength of soil

(Meadows et al. 1994). However, biobinding does

not seem to be suitable for large scale operations such

as enhancing the liquefaction resistance of land

reclamation sites because all biological bindings are

unstable and can be degraded by other microorgan-

isms. Only processes that are mediated by microbial

activity, such as oxidation, reduction, dissolution, and

precipitation of inorganic substances in soil pores can

form stable and strong binding of soil particles.

3.1 Microbial products and processes

Chemical cementation of soil in nature is due to the

precipitation of material in spaces between soil

particles and binding of these particles together into

a hard rock. Microorganisms are often associated

with the cemented sediments containing calcium,

magnesium, iron, manganese, and aluminium, which

are crystallized as carbonates, silicates, phosphates,

sulphides, and hydroxides, especially iron hydroxides

(DeJong et al. 2006). Chemical transformations of

metals and ions in soil are mediated by soil micro-

organisms. Example of sand cementation in nature is

the formation of ferrihydrite in pores (Ross et al.

1989). Iron hydroxides, depending on its crystalliza-

tion, can be also an important cementing agent in

soils (Dniker et al. 2003). Drying of soil samples

containing iron hydroxide can produce irreversible

soil hardening and cementation. In areas of soil with

high pH or redox potential the iron hydroxide is

precipitated forming cemented concretions or nod-

ules. Biological cementation with iron hydroxides

can be detected at the roots of all wetland plants

Table 1 Microbial processes that can lead potentially to bioclogging

Physiological group of

microorganisms

Mechanism of bioclogging Essential conditions for

bioclogging

Potential geotechnical

applications

Algae and cyanobacteria Formation of impermeable layer of

biomass

Light penetration and

presence of nutrients

Reduce of water infiltration

into slopes and control

seepage

Aerobic and facultative

anaerobic heterotrophic

slime-producing

bacteria

Production of slime in soil Presence of oxygen and

medium with ratio of

C:N [ 20

Avoide cover for soil erosion

control and slope protection.

Oligotrophic

microaerophilic bacteria

Production of slime in soil Low concentration oxygen

and medium with low

concentration of carbon

source

Reduce drain channel erosion

and control seepage

Nitrifying bacteria Production of slime in soil Presence of ammonium and

oxygen in soil

Reduce drain channel erosion

Sulphate-reducing bacteria Production of undissolved sulphides of

metals

Anaerobic conditions;

presence of sulphate and

carbon source in soil

Form grout curtains to reduce

the migration of heavy

metals and organic

pollutants

Ammonifying bacteria Formation of undissolved carbonates of

metals in soil due to increase of pH

and release of CO2

Presence of urea and

dissolved metal salt

Prevent piping of earth dams

and dikes

Iron-reducing bacteria Production of ferrous solution and

precipitation of undissolved ferrous

and ferric salts and hydroxides in soil

Anaerobic conditions

changed for aerobic

conditions; presence of

ferric minerals

Prevent piping of earth dams

and dikes

Rev Environ Sci Biotechnol

123

where Fe(II), produced by iron-reducing bacteria,

reacts with oxygen released by the roots (Johnson-

Green and Crowder 1991; Weiss et al. 2005). To

form ferric hydrates by oxidation and hydrolysis of

Fe(II), iron (III) must be preliminary reduced by iron-

reducing bacteria. Oxidation of ferrous ions and

chelates in soil is performed chemically or cata-

lyzed by neutrophlic or acidophilic iron-oxidizing

bacteria.

Another well known example of natural cemen-

tation is the precipitation of silica dioxide, which

fills in the pores and glues the soil particles together.

It is also known as natural soil calcification due to

the deposition of calcium carbonate from upward

flow of groundwater, enhanced evapotranspiration

from soil, or formation of calcium carbonate within

zones of elevated carbonate alkalinity formed by

microbial decay of organic matter (Mozley and

Davis 2005).

Kucharski et al. (2005) applied for a patent on

microbial biocementation for the formation of high

strength cement in a permeable material using the

combination of this material with biomass of urease-

producing microorganism, urea, and soluble calcium

salts. Microorganisms provide fast urea hydrolysis,

increase the pH during hydrolysis of urea to ammonia,

and form calcite in soil or rocks. The cement produced

has a compressive strength up to 5MPa. The materials,

treated by biocementation, may be conglomerate,

breccia, sandstone, siltstone, shale, limestone, gyp-

sum, peat, lignite, sand, soil, clay, sediments, and

sawdust. The urease-producing microorganisms are

from genera Bacillus, Sporosarcina, Sporolactobacil-

lus, Clostridium and Desulfotomaculum.

3.2 Laboratory tests and applications

Some laboratory tests on dike reinforcement using

biocementation were carried out in Netherlands (http:

//www.geodelft.com/files/bacteriabuildbiodikes.pdf).

Biomass of aerobic bacteria has been introduced into

soil to achieve cementation due to the bacteria-med-

iated production of calcium carbonate connecting the

sand grains together with the formation of sandstone.

Similarly, a cemented soil matrix within initially

loose, collapsible sand was formed using microbial-

induced calcite precipitation due to amendment of the

biomass of aerobic bacteria Bacillus pasteurii and a

liquid growth medium with urea and a dissolved cal-

cium salt. Cemented sand, assessed by shear wave

velocity and undrained compression triaxial tests,

exhibits a less brittle shear behavior with a higher

initial shear stiffness and ultimate shear capacity than

untreated loose specimens. Precipitated calcite is

formed through particle–particle contacts. This has

been confirmed by X-ray compositional mapping in

which the observed cement bonds comprise of calcite

(DeJong et al. 2006).

This method of microbial cementation could be

used for the following civil and environmental

engineering applications (Kucharski et al. 2005):

• Enhancing stability for retaining walls, embank-

ments, and dams;

• Reinforcing or stabilizing soil to facilitate the

stability of tunnels or underground constructions;

• Increasing the bearing capacity of piled or non-

piled foundations;

• Reducing the liquefaction potential of soil;

• Treating pavement surface;

• Strengthening tailings dams to prevent erosion

and slope failure;

• Constructing a permeable reactive barriers in

mining and environmental engineering;

• Binding of the dust particles on exposed surfaces

to reduce dust levels;

• Increasing the resistance to petroleum borehole

degradation during drilling and extraction;

• Increasing the resistance of offshore structures to

erosion of sediment within or beneath gravity

foundations and pipelines;

• Stabilising pollutants from soil by the binding;

• Controlling erosion in coastal area and rivers;

• Creating water filters and bore hole filters;

• Immobilising bacterial cells into a cemented

active biofilter.

However, successful field applications of biocemen-

tation have not been reported so far.

The study on the biocementation of sand with

enrichment culture of iron-reducing bacteria, fine

particles of iron ore, and cellulose as electron donor

has demonstrated that solution of Fe2+ (700 mg Fe2+/

L), formed from iron ore particles, can produce

significant cementation effect for sand after oxidation

of Fe2+ by air. The unconfined shear strength of the

sand has increased from zero to 140 kPa (Ivanov and

Chu, unpublished data).

Rev Environ Sci Biotechnol

123

3.3 Comparison of soil biocementation

with mechanical compaction and chemical

grouting of soil

Modification of the physical properties of soil can be

achieved using mechanical compaction, chemical

grouting, or biocementation. Shallow mechanical

compaction of soil is accomplished by rolling or

vibrating. Deep compaction of soil is performed by

vibrocompaction or dynamic compaction which

involves tamping the ground by repeated dropping a

heavy weight. However, most of the compaction

techniques are only effective or economically viable

to a depth less than 10 m (Indraratna and Chu 2005).

Another major disadvantage of dynamic compaction

is that it is not applicable for clayey soils and recent

municipal landfills.

Chemical grouting injects chemical grout into soil

or rock to enhance their mechanical properties by

changing their physical properties. To increase soil

stability and strength, some chemical suspended

substances (particulate grout) or dissolved substances

(chemical grout) must be added. For soil slope

stability and erosion control, only the top layer of

soil is needed to be treated. To diminish soil

permeability and increase its mechanical strength,

an injection of additives into soil is used. Grouting

fluids comprise of typically cement, bentonite, sili-

cate (sodium silicate solution with cement, bentonite,

or chemical additives such as calcium chloride,

sodium aluminate, phosphoric and some other acids),

lignosulfonates (waste by-product of paper mills),

pozzolanic-based materials, thermoplastic polymers,

organic polymers, a solution of monomers polymer-

izing in situ, a mixture of ferrous sulfate combined

with calcium hydroxide (Karol 2003). The market

share of two major commercial products, silicates and

acrylic-based grouts, is from 85% to 90% in the

United States (Karol 2003). The pressure injections

of grouting fluids are most effective in sandy soils

and cracked rocks with filtration rates from 0.5 to

80 m/day. After injection of the suspension into soil,

a cylinder of strengthened soil or rock with a

diameter 0.3–1 m (depending on filtration rate) is

formed around the injector or injection well. Injectors

or injecting wells are arranged by the chess cells

order to ensure full fixation of soil on defined area.

Distance between the injectors must be approxi-

mately 1.5 times smaller than radius of the fixed soil

column formed by one injector. The grout must have

a proper hardening time that matches the method of

injection. This will ensure that the grout does not

harden before it reaches the areas required, or harden

too slowly so the grout will spread too thinly.

There are several ways of injection in chemical

grouting, which can be used also for microbial

grouting. In low pressure grouting, a low-viscosity

grout is injected into soil at low pressure and fills the

voids without the changes of soil volume. In jet

grouting, the grouting injects at high pressure and flow

of high velocity mixes the grout and soil (Karol 2003).

The grout can be performed using stage-down or

stage-up methods, grout port, and vibrating beam. In

the stage-down method, a borehole is drilled to the full

depth and grout is injected as the drill is withdrawn. In

the stage-up method, the grout is injected starting at

the top of the borehole and continuing to the desired

depth. The grout port method uses a slotted injection

pipe and a double packer to inject the grout at specific

intervals. In the vibrating beam method, a beam is

vibrated into the soil to the desired depth, and then

grout is injected as the beam is withdrawn. Horizontal

grout curtains are constructed by horizontal overlap-

ping of the grout injection zones, or using grout holes

installed using horizontal drilling methods. Vertical

microbial grout curtains could also be designed as

barriers to groundwater flow (Karol 2003).

Technologies for the microbial grouting could be

similar to those used in chemical grouting. Depth of

penetration depends on the size of used microorgan-

isms. The typical size of unicellular bacteria is from 1

to 3 lm, but the length of microbial cellular filaments

can be up to 100 lm, which can be an obstacle in

penetration of filamentous microorganisms into soil.

The specificity of microbial grouting is that such

optimal for microbial activity conditions as optimal

pH, salinity, oxidation-reduction potential, concentra-

tions of nutrients, and content of water must be

provided for.

An advantage of microbial grouting over chemical

one is that the microbial grouts may be non-toxic,

whereas many chemical grouts, especially those based

on acrylamides, lignosulfonates, and polyurethane,

are toxic and environmentally harmful. Another

advantage of microbial grouting over chemical one

is the lower cost of reagents. The evaluated costs of

the raw materials for the chemical soil grouting are in

the range from $2 to $72 per m3 of soil (Table 2). The

Rev Environ Sci Biotechnol

123

chemical grouts, especially those based on acrylates,

acrylamides, and polyurethanes are most expensive.

The costs of the raw materials for the microbial

grouting could be in the range from $0.5 to $9.0 per

m3 of soil in cases when the waste materials are used

as the source of carbon for microbial growth

(Table 3). It should be pointed out that the evaluated

costs given in the Tables 2 and 3 are raw material

costs at the market prices only and the cost of

placement is not included. As pointed out by Karol

(2003), the cost of placement of grouts can be a major

part of the total cost of chemical grouting. However,

assuming that the costs of placement involved in the

chemical grouting is comparable to microbial grout-

ing, then the cost comparisons shown in the Tables 2

and 3 are relevant.

3.4 Limitation of soil biocementation

A disadvantage of soil bioclogging and biocementation

in comparison with chemical grouting is that the

microbial process is usually slower. Another disad-

vantage is that the microbial process is more complex

than the chemical one because the microbial activity

depends on many environmental factors such as

temperature, pH, concentrations of donors and accep-

tors of electrons, concentrations and diffusion rates of

nutrients and metabolites. The design of microbial

applications in bioclogging and biocementation must

take into account not only soil conditions and grouting

medium content but also microbiological, ecological

and geotechnical engineering aspects of the process.

Design of bioclogging and biocementation requires

data of the biological processes (growth, biosynthesis,

biodegradation, bioreduction, biooxidation, and spe-

cific enzymatic activities), chemical reactions

accompanied with formation of insoluble compounds,

and physico-chemical processes such as precipitation,

crystallization, and adhesion. Specific geotechnical

parameters of soil must be used as process optimization

criteria. Design of bioclogging and biocementation

processes is not shown in this review because there are

no related papers yet. Due to the complexity, none of

the bioclogging or biocementation processes have been

tested in large-scale construction or land reclamation

project yet.

3.5 Summary

Different possible microbial processes that can lead

potentially to biocementation are summarized in

Table 4. These include binding of the soil particles

with sulphides of metals produced by sulphate-

reducing bacteria; binding of the particles with

carbonates of metals produced due to hydrolysis of

urea; and binding of the particles with ferrous and

ferric salts and hydroxides, produced due to activity

of iron-reducing bacteria.

Table 2 Approximate cost of raw materials for chemical

grouting

Material Price

($/kg)

Amount of

additives

required

(kg/m3)

Cost of

additives

($/m3)

Lignosulphites-

Lignosulphonates

0.1–0.3 20–60 2–18

Sodium silicate

formulations

0.6–1.8 10–40 6–72

Phenoplasts 0.5–1.5 5–10 2.5–15

Acrylates 1.0–3.0 5–10 5–30

Acrylamides 1.0–3.0 5–10 5–30

Polyurethanes 5.0–10.0 1–5 5–50

Table 3 Approximate cost of raw materials for microbial grouting

Materials Price ($/kg) Amount of additives

required (kg/m3)

Cost of additives

(m3 of soil)

Molasses + microorganisms 0.1–0.2 5–20 0.5–4.0

Homogenized food-processing wastes + microorganisms 0.05–0.1 10–20 0.5–2.0

Iron ore + organic wastes + microorganisms 0.1–0.2 10–20 1.0–4.0

Organic wastes (agricultural, horticultural, food-processing wastes) 0.05–0.1 10–20 0.5–2.0

Calcium chloride + urea + microorganisms 0.2–0.3 20–30 4.0–9.0

Rev Environ Sci Biotechnol

123

4 Screening of microorganisms suitable for soil

bioclogging and biocementation

The group of chemotrophic prokaryotes is most

suitable for the soil bioclogging and biocementation

because of their smallest cell size, typically from 0.5

to 2 lm, ability to grow inside soil, and big

physiological diversity. Phototrophic prokaryotes,

mainly cyanobacteria, grow on soil surface only

because light penetrates only a few millimeters into

soil. These bacteria can produce rigid crust on surface

of soil or sediment, which diminishes soil infiltration

rate and improves slope stability. Cyanobacteria can

also create millimeter-scale laminated carbonate

build-ups called stromatolites, which are formed in

shallow marine environment, due to the sequence of

sedimentation, growth of biofilm, production of a

layer of exopolymers, and lithification of sediments

by the precipitation of microcrystalline carbonate

(Reid et al. 2000; Buffle and van Leeuwen 2002).

Selection of the groups of chemotrophic bacteria

for bioclogging and biocementation using modern

phylogenetic classification of prokaryotes is impossi-

ble because it is based mainly on the comparisons of

the gene of 16S rRNA (Bergey’s Manual of System-

atic Bacteriology 2001, 2005). This classification has

weak connection with physiological grouping of

chemotrophic prokaryotes and cannot be used as a

practical tool in the ecological design of bioclogging

or biocementation. Physiological classification of

chemotrophic prokaryotes, originally proposed by

the authors as shown in Table 5, can be used in

ecological design of bioclogging and biocementation.

This classification is based on two features: (1)

relation to oxygen connected with the type of energy

generation and (2) type of cell wall. The four periods

(columns) as shown in Table 5 are as follows: (1)

fermenting anaerobes; (2) anaerobic respiring pro-

karyotes that produce energy by anaerobic oxidation

of chemical substances using such electron acceptors

as nitrate (NO3-), nitrite (NO2

-), ferric (Fe3+), sulphate

(SO42-), sulphur (S), or carbon dioxide (CO2); (3)

microaerophilic and facultative anaerobic prokary-

otes; (4) aerobes. Three parallel lines in the periodic

table of chemotrophic prokaryotes show evolutionary

origin of microbial group: (1) prokaryotes of aquatic

origin, cells with Gram-negative type of cell wall that

were evolutionary adapted to the environments with

stable osmotic pressure; (2) prokaryotes of terrestrial

origin, cells with Gram-positive type cell wall that

were evolutionary adapted to the environments with

changeable osmotic pressure; (3) Archaea originated

from the environments with extreme temperature,

salinity, pH, or redox potential. There are total 12

physiological groups in the periodic table of chemo-

trophic prokaryotes.

Archaea could be excluded from the consideration

of being used as bioagents for soil bioclogging and

Table 4 Possible microbial processes that can lead potentially to biocementation

Physiological

group of

microorganisms

Mechanism of biocementation Essential conditions for

biocementation

Potential geotechnical

applications

Sulphate-

reducing

bacteria

Production of undissolved sulphides of metals Anaerobic conditions; presence

of sulphate and carbon source

in soil

Enhance stability for

slopes and dams

Ammonifying

bacteria

Formation of undissolved carbonates of metals in

soil due to increase of pH and release of CO2

Presence of urea and dissolved

metal salt

Mitigate liquefaction

potential of sand

Enhance stability for

retaining walls,

embankments, and dams;

Increase bearing capacity

of foundations

Iron-reducing

bacteria

Production of ferrous solution and precipitation

of undissolved ferrous and ferric salts and

hydroxides in soil

Anaerobic conditions changed

for aerobic conditions;

presence of ferric minerals

Density soil on reclaimed

land sites and prevent

soil avalanching

Reduce liquefaction

potential of soil

Rev Environ Sci Biotechnol

123

biocemenetation, because all of them are living in

extreme environments that are not compatible with

the majority of the construction or land reclamation

site conditions.

Anaerobic fermenting bacteria may be involved in

cementation of soil particles under the presence of

calcium, magnesium, or ferrous ions. This cementa-

tion can be due to the increase in pH caused by

ammonification (release of ammonia) and carbon

dioxide production in soil added with urea or waste

protein (Bachmeier et al. 2002; Castanier et al. 1999;

Hammes and Verstraete 2002; Kucharski et al. 2005;

Stocks-Fischer and Galinat 1999). The insoluble

carbonates and hydroxides of metals will be precip-

itating at high pH thus binding the soil particles and

clogging soil. However, if carbohydrates are added to

soil, fermenting anaerobic bacteria can diminish the

pH due to formation of organic acids during fermen-

tation of carbohydrates. This could be potentially

used in bioclogging and biocementation to precipitate

silicates from colloidal silica suspension. It is known

that stability of colloidal silica suspension is reduced

at acidic pH and inorganic acids are added in this type

of chemical grouting (Karol 2003). From other point

of view, organic acids produced in fermentation can

dissolve carbonates and hydroxides binding soil

particles or plugging soil pores. Anaerobic bacteria

cannot clog soil pores by the synthesis of extracel-

lular polymers because they are not able to produce

big quantity of slime (Atmaca et al. 1996) due to

their low efficiency of biological energy production

in fermentation.

Organic acids, hydrogen, and alcohols, which are

produced by anaerobic fermenting bacteria from

polysaccharides and monosaccharides, can be used

as donors of electrons by anaerobic respiring bacteria.

One example is the group of iron-reducing bacteria,

which are using products of fermentation as electron

donors to produce dissolved Fe(II) ions by reduction

of insoluble Fe(III) compounds (Lovley et al. 2004;

Weber et al. 2006). Microbial reduction of Fe(III) is

used in environmental biotechnology for treatment of

groundwater and wastewater (Fredrickson and Gorby

1996; Ivanov et al. 2004, 2005; Stabnikov and Ivanov

2006) and could be used hypothetically for soil

cementation because iron-reducing bacteria could

produce Fe2+ in situ from cheap sources of Fe(III)

and products of anaerobic fermentation of organic

wastes (Ivanov et al. 2004, 2005; Stabnikov and

Ivanov 2006). Ions of ferrous can be oxidized

chemically or biologically. Products of this oxidation

are insoluble ferric hydroxides and ferric carbonates,

which could clog the soil pores and bind the soil

particles altogether.

Another example of anaerobic respiring bacteria,

which could be used in bioclogging and biocementa-

tion, is sulphate-reducing bacteria. These bacteria

produce dihydrogen sulphide using organic acids,

hydrogen, or alcohols as electron donors and sulphate

as electron acceptor. Sulphide reacts with iron and

Table 5 The periodic table of physiological classification of chemotrophic prokaryotes for the screening of the physiological groups

suitable for soil bioclogging and biocementation

Ecology of origin Relation to oxygen and type of energy generation

Anaerobic

fermenting

prokaryotes

Anaerobic

respirating

prokaryotes

Facultative anaerobic and

microaerophilic prokaryotes

Aerobic

respirating

prokaryotes

Prokaryotes of aquatic origin Bacteroides

Prevotella

Ruminobacter

Desulfobacter

Geobacter

Wolinella

Escherichia

Shewanella

Beggiatoa

Pseudomonas

Acinetobacter

Nitrosomonas

Prokaryotes of terrestrial origin Clostridium

Peptococcus

Eubacterium

Desulfotomaculum

Desulfitobacterium

Bacillus infernus

Microthrix

Nocardia

Streptococcus

Bacillus

Arthrobacter

Streptomyces

Prokaryotes originating from extreme

environments (Archaea)

Desulfurococcus

Thermosphaera

Pyrodictium

Methanobacterium

Thermococcus

Haloarcula

Metallosphaera

Acidianus

Haloferax

Picrophilus

Ferroplasma

Sulfolobus

Selected examples of conventional genera are shown in the cells

Rev Environ Sci Biotechnol

123

other metal cations to form insoluble suphides of

metals, which clogs the soil pores and binds the soil

particles. However, the soil compaction created by the

formation of sulphides is unstable because they can be

chemically or biologically oxidized to sulphuric acid

or sulphates under aerobic conditions. There is a case

where a thousand houses built on excavated non-

weathered mudstone sediments were damaged by

microbially induced heaves of foundations (Yama-

naka et al. 2002). The mechanisms of this damage

were identified as: (1) sulphate-reducing bacteria in

the mudstone reduced sulphate to hydrogen sulphide;

(2) the mudstone sediments under the houses became

permeable to air due to gradual drying; (3) dihydrogen

sulfide was oxidized by sulphide-oxidizing bacteria to

sulphuric acid; and (4) acid dissolved calcium

carbonate binding the particles of mudstone sedi-

ments. Additional negative impact of activity of

sulphate-reducing bacteria is the increased corrosion

and release of toxic and bad smelling dihydrogen

sulphide.

Denitrification process, which is bioreduction of

nitrate (NO3-) and nitrite (NO2

-) to nitrogen gas, is not

applicable to the soil bioclogging or biocementation,

because bacteria produce big volume of dinitrogen

gas during denitrification and the cost of nitrate as

electron acceptor is not affordable for large-scale

construction and land reclamation projects.

Facultative anaerobic bacteria could be considered

as the most suitable bioagents for soil bioclogging and

biocementation because many species are able to

produce big quantity of exopolysaccharides, which

usually promote formation of cell aggregates, and can

grow under either aerobic or anaerobic conditions. Last

property of facultative anaerobic bacteria is most

essential for biotreatment of soil in situ where supply

of oxygen is limited by the soil porosity and both

aerobic and anaerobic microzones co-exist in soil.

There are, for example, bacteria from genera Alcalig-

enes, Enterobacter, Staphylococcus, Streptococcus,

Rhodococcus, corynebacteria (Gordonia, Nocardio-

ides), gliding bacteria (Myxococcus, Flexibacter,

Cytophaga) and oligotrophic bacteria (Caulobacter)

(Wingender et al. 1999; Jones et al. 2004; Ivanov and

Tay 2006b).

Microaerophilic bacteria could be used for the

biobinding of soil particles because many strains of

microaerophilic bacteria are combined in filaments

(Beccari and Ramadori 1996; Seviour and Blackall

2007) or joined by sheathes (Mulder and Deinema

1992) and these filamentous structures can also bind

the soil particles. The filamentous bacteria from the

genera Beggiatoa, Haliscomenobacter, Microthrix,

Nocardia, Sphaerotilus, and Thiothrix are common in

aerobic tanks of wastewater treatment plants (Beccari

and Ramadori 1996; Seviour and Blackall 2007) and

can be probably used for biobinding of soil particles.

Aerobic bacteria could be suitable for soil bioclog-

ging, biocementation, and biobinding of soil particles

because many species are able to produce big quantity

of slime, form chains and filaments, increase pH,

and oxidize different organic and inorganic sub-

stances. Cells of many Actinomycetes, a group of

Gram-positive bacteria, typical soil inhabitants, form

particles-binding mycelium and produce particles-

binding slime in soil (Wu et al. 1997; Jones et al.

2004; Dworkin et al. 2006). These bacteria are most

prospective for the aerobic soil bioclogging, bioce-

mentation, and biobinding. The examples of direct

involvement of both facultative anaerobic and aerobic

bacteria may be the cementation of soil particles under

presence of calcium, magnesium, or ferrous ions due

to increase of pH caused by ammonification and

carbon dioxide production in soil with added urea

(Kucharski et al. 2005). The insoluble carbonates and

hydroxides of metals are precipitating at high pH thus

binding the soil particles and clogging the soil pores.

Such bacterial groups as gliding bacteria, oligotrophic

bacteria, and nitrifying bacteria could be most active

in the formation of polysaccharides, which are

binding the soil particles. Aerobic sulphide-, sul-

phur-, and ammonium—oxidizing bacteria produce

sulphuric or nitric acids could hypothetically compact

the soil particles due to dissolution of minerals,

change of zeta-potential of colloid particles and

precipitation of colloidal silica at low pH.

The use of anaerobic bacteria can be complicated by

the presence of oxygen in the upper layer of soil and

sensitivity of anaerobic bacteria to oxygen. Alterna-

tively, if aerobic bacteria are used for soil clogging or

cementation, a major technological problem is the air

supply into soil. If the rate of oxygen supply into soil by

aeration and diffusion is not sufficient, there will be

formation of anaerobic layer or zones, where aerobic

bacteria will not be active. Therefore, from the

technological and biological points of view, the most

suitable physiological groups for the soil bioclogging

and biocementation in situ are facultative anaerobic

Rev Environ Sci Biotechnol

123

bacteria, which are active under both aerobic and

anaerobic conditions. Depending on the site conditions

of a real soil treatment project, a technique to alter the

anaerobic and aerobic conditions in situ can be imple-

mented to ensure the sequence of anaerobic and

aerobic biogeochemical processes and facilitate soil

bioclogging or biocementation.

Another assumption from the general consideration

of physiological diversity of prokaryotes is that the

most suitable bacteria for soil bioclogging or bioce-

mentation are bacteria with Gram-positive type of cell

wall because these bacteria are most resistant to the

changes of osmotic pressure, which is the typical

condition for soil on construction or reclamation sites.

Another important aspect in the screening of

microorganisms suitable for soil bioclogging and

biocementation is biosafety. To diminish the risk of

pathogenic bacteria accumulation and release during

bioclogging and biocementation, the following selec-

tive conditions can be used:

• an application of carbon sources, which are used

in nature by saprophytic microorganisms, such as

cellulose, cellulose-containing agricultural waste,

vegetable-processing waste, molasses;

• the conditions that are suitable for the growth of

autolithotrophic bacteria. Carbon dioxide is used

as a carbon source and inorganic substances

(NH4+, Fe2+, S) are used as electron donor;

• the conditions that are suitable for application of

bacteria able for anaerobic respiration with SO42-

or Fe3+ as electron acceptors;

• an application of solution with low concentration

of carbon source for preferable growth of oligo-

trophic microorganisms in soil.

The problem of biosafety can be solved also by the

selection of safe bacterial strain. The biomass of this

safe strain can be produced in bioreactor and used as a

starter culture for bioclogging or biocementation.

There are known similar applications of starter cultures

to start up the large-scale non-aseptic environmental

processes for faster start-up and increased biosafety

(Ivanov et al. 2006b; Ivanov and Tay 2006a).

5 Conclusions

(1) Bioclogging and biocementation of soils could

be used in geotechnical engineering to improve

the mechanical properties of soil in situ. These

methods can replace the more energy demand-

ing mechanical compaction methods or the

expensive and environmentally unfriendly

chemical grouting methods. However, to adopt

the microbial method effectively, an integration

of engineering, microbiological, and ecological

studies and design consideration are required.

(2) The most suitable microorganisms for soil

bioclogging or biocementation for large scale

construction and environmental problems are

facultative anaerobic and microaerophilic bacteria.

(3) There are several laboratory-scale studies and

field tests on bioclogging and biocementation of

soil. However, the industrial-scale applications

of microorganisms in geotechnical engineering

have yet to be demonstrated.

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