Rev Environ Sci Biotechnol DOI 10.

1007/s11157-007-9126-3

REVIEW PAPER

Applications of microorganisms to geotechnical engineering for bioclogging and biocementation of soil in situ
Volodymyr Ivanov 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-lling materials 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 microaerophilic 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 applications 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 Engineering 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 inltration into slopes. Biogeotechnology have advantages of low investment and maintenance costs. It also offers benets to environment and aesthetics (Karol 2003). Microbial geotechnology is an emerging branch of Geotechnical Engineering. Although there are various potential applications of microorganisms to geotechnical engineering, at the present, promising applications 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 conductivity 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

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 treatment 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 identication of suitable microorganisms 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 biomodication. Among all the factors, cost effectiveness is the most important factor for large-scale application. As an emerging discipline, microbial geotechnology 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 biocementation. 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 rst before a method for the screening of the suitable physiological groups of prokaryotes is suggested.

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, landll, or dike. One of the bioclogging processes is the microbial production of water-insoluble polysaccharides 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 polysaccharides are produced in industry (Sutherland 1990), these materials cannot be used for soil grouting because of the high cost involved. Only growth of microorganisms, 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 microorganisms that produce insoluble extracellular polysaccharides to bind the soil particles and ll 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, Arcobacter, 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 Cellulomonas avigena (Kenyon et al. 2005) and many

2 Bioclogging: microbial grouting in situ for water ow control Chemical grouting is a process to ll the soil voids with uid grouts. It is often used to control water ow (Karol 2003). Common grouts are solution or suspension of sodium silicate, acrylates, acrylamides, and polyurethanes. Industrially produced water-insoluble 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 bioremediation zone, and mitigating soil liquefaction (Momemi et al. 1999; Yang et al. 1993; Yen et al.

123

Rev Environ Sci Biotechnol

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 avigena 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 horticultural 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 extracellular 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 biolm 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 xed biolm 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 selective zonal bioremediation, harbor and dam control, erosion potential minimization, earthquake liquefaction 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 exopolysaccharideproducing 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 polysaccharideproducing 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 bioclogging. 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 conductivity 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 polysaccharides 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 inltration from the ponds and leakage in construction sites or landlls, 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

123

Rev Environ Sci Biotechnol

biomass and the soil hydraulic conductivity (Wu et al. 1997). Field bioclogging tests to reduce soil permeability 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 exopolysaccharides from the decomposed organic material. However, soil gleization does not provide satisfactory long-term seepage control for ooded channels (McConkey et al. 1990). This supports further the above mentioned conclusion that stable bioclogging is feasible only under soil conditions favorable for exopolysaccharideproducing microorganisms, but not favorable for exopolysaccharide-degrading microorganisms. Bouwer (2002) reported that during articial recharge of groundwater using surface water, clogging 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 organicpoor soil. Articial recharge of groundwater by surface water or efuent of wastewater 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 signicant geotechnical problem due to negative effect of bioclogging on soil bioremediation, sand ltration, 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 microbesmediated 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

ow 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 produce enzyme urease that hydrolyzes urea by the following reaction:
(NH2 )2 CO 3H2 O ! 2NH 4 HCO3 OH

1 Due to this enzymatic reaction, pH is increased and hydrocarbonate is produced. It is initiating precipitation 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 uid ow, enhance the recovery of oil from reservoirs (cited from Kucharski et al. 2005), and repair cracks in concrete (Ramachandran et al. 2001). For the formation 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) bacteriamediated transformation of sand to sandstone using soil bacteria, urea, and calcium ions. Bacteria hydrolyse urea to ammonium increasing pH, producing carbonate, and precipitating calcium as calcium carbonate under high pH (http://www.geodelft.com/les/ bacteriabuildbiodikes.pdf and http://www.smartsoils. nl). A pilot scale test of bioclogging using bioproducton 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 ve. 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 inow 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 injection of nutrients into the groundwater ensures that it ows towards the problem area. If needed group of soil microorganisms is absent in the porous medium, these

123

Rev Environ Sci Biotechnol

microorganisms must be injected or inltrated 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 exopolysaccharides. Therefore, a successful and stable bioclogging process is possible only under soil conditions that are favorable for exopolysaccharide-producing microorganisms, but not favorable for exopolysaccharidedegrading microorganisms. One example is the addition of ammonium to organic-poor soil or sand, stimulating growth of nitrifying bacteria, which synthesize polysaccharides 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 concentration of energy and carbon source for bacterial growth and synthesis of polysaccharides (Ivanov and Chu, unpublished data). The cases of clogging of sand-lled and gravel-lled agricultural drains are well known (Baveye et al. 1998). This is probably due to the production of exopolysaccharides 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 oligotrophic bacteria in situ is ranging from 0.1 d-1 to 0.01 d-1. Any temporarily shortage of ammonia or oxygen will signicantly 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 exopolysaccharides 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 biolm in soil pores affects the concentrations and mass transfer rates of nutrients and microbial metabolites between biolm and ow 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, nitrogen, and phosphorous sources, and metabolites such as hydrocarbonate and organic acids will also affect signicantly 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 nitrication. 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 heterotrophic 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 eld.

3 Biocementation: structural microbial grouting in situ Chemical cementation (or chemical grouting) is to ll the sand voids with uid chemical grouts to produce sandstone like masses to carry loads. This method is widely used in geotechnical engineering (Indraratna

123

Rev Environ Sci Biotechnol Table 1 Microbial processes that can lead potentially to bioclogging Physiological group of microorganisms Algae and cyanobacteria Mechanism of bioclogging Essential conditions for bioclogging Light penetration and presence of nutrients Presence of oxygen and medium with ratio of C:N [ 20 Low concentration oxygen and medium with low concentration of carbon source Presence of ammonium and oxygen in soil Potential geotechnical applications Reduce of water inltration into slopes and control seepage Avoide cover for soil erosion control and slope protection.

Formation of impermeable layer of biomass

Aerobic and facultative Production of slime in soil anaerobic heterotrophic slime-producing bacteria Oligotrophic Production of slime in soil microaerophilic bacteria

Reduce drain channel erosion and control seepage

Nitrifying bacteria

Production of slime in soil

Reduce drain channel erosion Form grout curtains to reduce the migration of heavy metals and organic pollutants Prevent piping of earth dams and dikes Prevent piping of earth dams and dikes

Sulphate-reducing bacteria Production of undissolved sulphides of Anaerobic conditions; metals presence of sulphate and carbon source in soil Ammonifying bacteria Formation of undissolved carbonates of Presence of urea and dissolved metal salt metals in soil due to increase of pH and release of CO2 Production of ferrous solution and Anaerobic conditions precipitation of undissolved ferrous changed for aerobic and ferric salts and hydroxides in soil conditions; presence of ferric minerals

Iron-reducing bacteria

and Chu 2005). The chemicals that are used to bind soil particles include sodium silicate, calcium chloride, 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 specic 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 lamentous 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 microorganisms. 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 microorganisms. Example of sand cementation in nature is the formation of ferrihydrite in pores (Ross et al. 1989). Iron hydroxides, depending on its crystallization, 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 nodules. Biological cementation with iron hydroxides can be detected at the roots of all wetland plants

123

Rev Environ Sci Biotechnol

where Fe(II), produced by iron-reducing bacteria, reacts with oxygen released by the roots (JohnsonGreen 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 ironreducing bacteria. Oxidation of ferrous ions and chelates in soil is performed chemically or catalyzed by neutrophlic or acidophilic iron-oxidizing bacteria. Another well known example of natural cementation is the precipitation of silica dioxide, which lls in the pores and glues the soil particles together. It is also known as natural soil calcication due to the deposition of calcium carbonate from upward ow 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 ureaseproducing 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, gypsum, peat, lignite, sand, soil, clay, sediments, and sawdust. The urease-producing microorganisms are from genera Bacillus, Sporosarcina, Sporolactobacillus, Clostridium and Desulfotomaculum.

liquid growth medium with urea and a dissolved calcium 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 particleparticle contacts. This has been conrmed 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, embankments, and dams; Reinforcing or stabilizing soil to facilitate the stability of tunnels or underground constructions; Increasing the bearing capacity of piled or nonpiled 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 lters and bore hole lters; Immobilising bacterial cells into a cemented active biolter.

3.2 Laboratory tests and applications Some laboratory tests on dike reinforcement using biocementation were carried out in Netherlands (http: //www.geodelft.com/les/bacteriabuildbiodikes.pdf). Biomass of aerobic bacteria has been introduced into soil to achieve cementation due to the bacteria-mediated 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 microbialinduced calcite precipitation due to amendment of the biomass of aerobic bacteria Bacillus pasteurii and a

However, successful eld applications of biocementation have not been reported so far. The study on the biocementation of sand with enrichment culture of iron-reducing bacteria, ne 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 signicant cementation effect for sand after oxidation of Fe2+ by air. The unconned shear strength of the sand has increased from zero to 140 kPa (Ivanov and Chu, unpublished data).

123

Rev Environ Sci Biotechnol

3.3 Comparison of soil biocementation with mechanical compaction and chemical grouting of soil Modication 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 landlls. 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 uids comprise of typically cement, bentonite, silicate (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 polymerizing 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 uids are most effective in sandy soils and cracked rocks with ltration 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 0.31 m (depending on ltration rate) is formed around the injector or injection well. Injectors or injecting wells are arranged by the chess cells order to ensure full xation of soil on dened area. Distance between the injectors must be approximately 1.5 times smaller than radius of the xed 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 lls the voids without the changes of soil volume. In jet grouting, the grouting injects at high pressure and ow 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 specic 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 overlapping 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 ow (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 microorganisms. The typical size of unicellular bacteria is from 1 to 3 lm, but the length of microbial cellular laments can be up to 100 lm, which can be an obstacle in penetration of lamentous microorganisms into soil. The specicity of microbial grouting is that such optimal for microbial activity conditions as optimal pH, salinity, oxidation-reduction potential, concentrations 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

123

Rev Environ Sci Biotechnol Table 2 Approximate cost of raw materials for chemical grouting Material Price ($/kg) Amount of additives required (kg/m3) 2060 1040 510 510 510 15 Cost of additives ($/m3)

LignosulphitesLignosulphonates Sodium silicate formulations Phenoplasts Acrylates Acrylamides Polyurethanes

0.10.3 0.61.8 0.51.5 1.03.0 1.03.0 5.010.0

218 672 2.515 530 530 550

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 grouting, then the cost comparisons shown in the Tables 2 and 3 are relevant.

microbial process is usually slower. Another disadvantage 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 acceptors 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 specic enzymatic activities), chemical reactions accompanied with formation of insoluble compounds, and physico-chemical processes such as precipitation, crystallization, and adhesion. Specic 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 sulphatereducing 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.

3.4 Limitation of soil biocementation A disadvantage of soil bioclogging and biocementation in comparison with chemical grouting is that the

Table 3 Approximate cost of raw materials for microbial grouting Materials Price ($/kg) Amount of additives required (kg/m3) 520 1020 1020 1020 2030 Cost of additives (m3 of soil) 0.54.0 0.52.0 1.04.0 0.52.0 4.09.0

Molasses + microorganisms Homogenized food-processing wastes + microorganisms Iron ore + organic wastes + microorganisms Organic wastes (agricultural, horticultural, food-processing wastes) Calcium chloride + urea + microorganisms

0.10.2 0.050.1 0.10.2 0.050.1 0.20.3

123

Rev Environ Sci Biotechnol Table 4 Possible microbial processes that can lead potentially to biocementation Physiological group of microorganisms Sulphatereducing bacteria Ammonifying bacteria Mechanism of biocementation Essential conditions for biocementation Potential geotechnical applications

Production of undissolved sulphides of metals

Anaerobic conditions; presence Enhance stability for of sulphate and carbon source slopes and dams in soil Mitigate liquefaction potential of sand Enhance stability for retaining walls, embankments, and dams; Increase bearing capacity of foundations

Formation of undissolved carbonates of metals in Presence of urea and dissolved soil due to increase of pH and release of CO2 metal salt

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

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 inltration 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 biolm, production of a layer of exopolymers, and lithication of sediments by the precipitation of microcrystalline carbonate (Reid et al. 2000; Bufe and van Leeuwen 2002). Selection of the groups of chemotrophic bacteria for bioclogging and biocementation using modern phylogenetic classication of prokaryotes is impossible because it is based mainly on the comparisons of the gene of 16S rRNA (Bergeys Manual of Systematic Bacteriology 2001, 2005). This classication 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 classication of chemotrophic prokaryotes, originally proposed by the authors as shown in Table 5, can be used in ecological design of bioclogging and biocementation. This classication 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 prokaryotes that produce energy by anaerobic oxidation of chemical substances using such electron acceptors 3+ as nitrate (NO3 ), nitrite (NO2 ), ferric (Fe ), sulphate 2(SO4 ), sulphur (S), or carbon dioxide (CO2); (3) microaerophilic and facultative anaerobic prokaryotes; (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 chemotrophic prokaryotes. Archaea could be excluded from the consideration of being used as bioagents for soil bioclogging and

123

Rev Environ Sci Biotechnol Table 5 The periodic table of physiological classication 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 Prokaryotes of aquatic origin Bacteroides Prevotella Ruminobacter Prokaryotes of terrestrial origin Clostridium Peptococcus Eubacterium Prokaryotes originating from extreme Desulfurococcus environments (Archaea) Thermosphaera Pyrodictium Anaerobic respirating prokaryotes Desulfobacter Geobacter Wolinella Desulfotomaculum Desultobacterium Bacillus infernus Methanobacterium Thermococcus Haloarcula Facultative anaerobic and microaerophilic prokaryotes Aerobic respirating prokaryotes Pseudomonas Acinetobacter Nitrosomonas Bacillus Arthrobacter Streptomyces Picrophilus Ferroplasma Sulfolobus

Escherichia Shewanella Beggiatoa Microthrix Nocardia Streptococcus Metallosphaera Acidianus Haloferax

Selected examples of conventional genera are shown in the cells

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 cementation can be due to the increase in pH caused by ammonication (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 precipitating 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 fermentation 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 extracellular polymers because they are not able to produce big quantity of slime (Atmaca et al. 1996) due to

their low efciency 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 biocementation, 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

123

Rev Environ Sci Biotechnol

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 nonweathered mudstone sediments were damaged by microbially induced heaves of foundations (Yamanaka et al. 2002). The mechanisms of this damage were identied 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 sulde was oxidized by sulphide-oxidizing bacteria to sulphuric acid; and (4) acid dissolved calcium carbonate binding the particles of mudstone sediments. Additional negative impact of activity of sulphate-reducing bacteria is the increased corrosion and release of toxic and bad smelling dihydrogen sulphide. Denitrication 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 denitrication 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 Alcaligenes, Enterobacter, Staphylococcus, Streptococcus, Rhodococcus, corynebacteria (Gordonia, Nocardioides), 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 laments (Beccari and Ramadori 1996; Seviour and Blackall

2007) or joined by sheathes (Mulder and Deinema 1992) and these lamentous structures can also bind the soil particles. The lamentous 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 bioclogging, biocementation, and biobinding of soil particles because many species are able to produce big quantity of slime, form chains and laments, increase pH, and oxidize different organic and inorganic substances. Cells of many Actinomycetes, a group of Gram-positive bacteria, typical soil inhabitants, form particles-binding mycelium and produce particlesbinding 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, biocementation, 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 ammonication 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-, sulphur-, and ammoniumoxidizing 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. Alternatively, 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 sufcient, 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

123

Rev Environ Sci Biotechnol

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 implemented 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 biocementation 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 selective 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 2+ (NH+ 4 , Fe , S) are used as electron donor; the conditions that are suitable for application of bacteria able for anaerobic respiration with SO2 4 3+ or Fe as electron acceptors; an application of solution with low concentration of carbon source for preferable growth of oligotrophic microorganisms in soil.

(2)

(3)

the mechanical properties of soil in situ. These methods can replace the more energy demanding 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. The most suitable microorganisms for soil bioclogging or biocementation for large scale construction and environmental problems are facultative anaerobic and microaerophilic bacteria. There are several laboratory-scale studies and eld tests on bioclogging and biocementation of soil. However, the industrial-scale applications of microorganisms in geotechnical engineering have yet to be demonstrated.

References
Atmaca S, Elci S, Gul K (1996) Comparison of slime production under aerobic and anaerobic conditions. Cytobios 88:149152 Bachmeier K, Williams AE, Warmington J, Bang SS (2002) Urease activity in microbiologically-induced calcite precipitation. J Biotechnol 93:171181 Baveye P, Vandevivere P, Hoyle BL, DeLeo PC, de Lozada DS (1998) Environmental impact and mechanisms of the biological clogging of saturated soils and aquifer materials. Crit Rev Environ Sci Technol 28:123191 Beccari M, Ramadori R (1996) Filamentous activated sludge bulking. In: Horan N (ed) Environmental waste management: a European perspective. John Wiley & Sons, New York, pp 87114 Bergeys Manual of Systematic Bacteriology (2001) The Archaea and the deeply branching and phototrophic bacteria, 2nd edn, vol 1. Springer-Verlag, New York Bergeys Manual of Systematic Bacteriology (2005) The proteobacteria, 2nd edn, vol 2. Springer-Verlag, New York Bonala MVS, Reddi LN (1998) Physicochemical and biological mechanisms of soil clogging: an overview. ASCE Geotech Spec Publ 78:4368 Bouwer H (2002) Articial recharge of groundwater: hydrogeology and engineering. Hydrogeol J 10:121142 Bufe J, van Leeuwen HP (Ser eds) (2002) Interactions between soil particles and microorganisms. In: Huand M, Bollag JM, Senesi N (Vol eds) IUPAC series on analytical and physical chemistry of environmental systems, vol 8. John Wiley & Sons, Chichester, UK Castanier S, Le Metayer-Levrel G, Perthuisot JP (1999) Cacarbonates precipitation and limestone genesisthe microbiogeologist point of view. Sediment Geol 126:923 DeJong JT, Fritzges MB, Nusstein K (2006) Microbially induced cementation to control sand response to undrained shear. J Geotech Geoenviron Eng 32:13811392

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

123

Rev Environ Sci Biotechnol Dniker SW, Rhoton FE, Torrent J, Smeck NE, Lal R (2003) Iron (hydr)oxide crystallinity effects on soil aggregation. Soil Sci Soc Am J 67:606611 Dupin HJ, McCarty PL (2000) Impact of colony morphologies and disinfection on biological clogging in porous media. Environ Sci Technol 34:15131520 Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) (2006) The prokaryotes: a handbook on the biology of bacteria, vol 3: Archaea. Bacteria: Firmicutes, Actinomycetes, 3rd edn. Springer-Verlag, New York Etemadi O, Petrisor IG, Kim D, Wan MW, Yen TF (2003) Stabilization of metals in subsurface by biopolymers: laboratory drainage ow studies. Soil Sediment Contam 12:647661 Ferris FG, Stehmeier LG (1992) Bacteriogenic mineral plugging, United States Patent 5143155 Ferris FG, Stehmeier LG, Kantzas A, Mourits FM (1996) Bacteriogenic mineral plugging. Can J Petrol Technol 35:5661 Fredrickson JK, Gorby YA (1996) Environmental processes mediated by iron-reducing bacteria. Curr Opin Biotechnol 7:287294 Fujita Y, Ferris FG, Lawson RD, Colwell FS, Smith RW (2000) Calcium carbonate precipitation by ureolytic subsurface bacteria. Geomicrobiol J 17:305318 Geets J, Boon N, Verstraete W (2006) Strategies of aerobic ammonia-oxidizing bacteria for coping with nutrient and oxygen uctuations. FEMS Microbiol Ecol 58:113 Gioia F, Ciriello PP (2006) The containment of oil spills in porous media using xanthan/aluminium solutions, gelled by gaseous CO2 or by AlCl3 solutions. J Hazard Mater 138:500506 Hajra MG, Reddi LN, Marchin GL, Mutyala J (2000) Biological clogging in porous media. In: Zimme TF (ed) Environ Geotech ASCE geotechnical special publication 105, New York, pp 151165 Hammes F, Verstraete W (2002) Key roles of pH and calcium metabolism in microbial carbonate precipitation. Rev Environ Sci Biotechnol 1:37 Harada T (1983) Special bacterial polysaccharides and polysaccharases. Biochem Soc Symp 48:97116 Indraratna B, Chu J (Eds) (2005) Ground improvement case histories. Elsevier, Oxford, UK Ivanov V (2006) Structure of aerobically grown microbial granules. In: Tay JH, Tay STL, Liu Y, Show KY, Ivanov V (eds) Biogranulation technologies for wastewater treatment. Elsevier, Amsterdam, pp 115134 Ivanov V, Tay STL (2006a) Seeds for aerobic microbial granules. In: Tay JH, Tay STL, Liu Y, Show KY, Ivanov V (eds) Biogranulation technologies for wastewater treatment. Elsevier, Amsterdam, pp 213244 Ivanov V, Tay STL (2006b) Microorganisms of aerobic microbial granules. In: Tay JH, Tay STL, Liu Y, Show KY, Ivanov V (eds) Biogranulation technologies for wastewater treatment. Elsevier, Amsterdam, pp 135162 Ivanov V, Wang JY, Stabnikova O, Krasinko V, Stabnikov V, Tay STL, Tay JH (2004) Iron-mediated removal of ammonia from strong nitrogenous wastewater of food processing. Water Sci Technol 49:421431 Ivanov V, Stabnikov V, Zhuang WQ, Tay ST L, Tay JH (2005) Phosphate removal from return liquor of municipal wastewater treatment plant using iron-reducing bacteria. J Appl Microbiol 98:11521161 Ivanov V, Stabnikova O, Sihanonth P, Menasveta P (2006a) Aggregation of ammonia-oxidizing bacteria in microbial biolm on oyster shell surface. World J Microbiol Biotechnol 22:807812 Ivanov V, Wang XH, Tay STL, Tay JH (2006b) Bioaugmentation and enhanced formation of microbial granules used in aerobic wastewater treatment. Appl Microbiol Biotechnol 70:374381 James GA, Warwood BK, Hiebert R., Cunningham AB (2000) Microbial barriers to the spread of pollution. In: Bioremediation. Kluwer Academic, Amsterdam, pp 114 Jones AL, Brown JM, Mishra V, Perry JD, Steigerwalt AG, Goodfellow M (2004) Rhodococcus gordoniae sp. nov., an actinomycete isolated from clinical material and phenolcontaminated soil. Int J Syst Evol Microbiol 54:407411 Johnson-Green PC, Crowder AA (1991) Iron oxide deposition on axenic and non-axenic roots of rice seedlings (Oryza sativa L.). J Plant Nutr 14:375386 Karol RH (2003) Chemical grouting and soil stabilization, 3rd edn. M. Dekker, New York Kenyon WJ, Esch SW, Buller CS (2005) The curdlan-type exopolysaccharide produced by cellulomonas avigena KU forms part of an extracellular glycocalyx involved in cellulose degradation. Antonie Van Leeuwenhoek 87: 143148 Kucharski ES, Winchester W, Leeming WA, Cord-Ruwisch R, Muir C, Banjup WA, Whifn VS, Al-Thawadi S, Mutlaq J (2005) Microbial biocementation. Patent Application WO/2006/066326; International Application No.PCT/ AU2005/001927 Lovley DR, Holmes DE, Nevin KP (2004) Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49: 219286 McConkey BG, Reimer CD, Nicholaichuk W (1990) Sealing earthen hydraulic structures with enhanced gleization and sodium carbonate: 2. Application for lining an irrigation canal. C Agr Eng 163170 ndez MT, Garc a-Orenes F, Mataix-Solera J, Guerrero C, Herna mez I, Escalante B (2005) Mataix-Beneyto J, Go Improving soil physical properties related to hydrological behaviour by inducing microbiological changes after organic amendments. Geophys Res Abs 7, 00341 Meadows A, Meadows PS, Wood DM, Murray JMH (1994) Microbiological effects on slope stability: an experimental analysis. Sedimentology 41:423435 Mitchell JK, Santamarina JC (2005) Biological considerations in geotechnical engineering. J Geotech Geoenviron Eng 131:12221233 Momemi D, Kamel R, Martin R, Yen TF (1999) Potential use of biopolymer grouts for liquefaction mitigation. In: Leeson A, Alleman BC (eds) Phytoremediation and innovation strategies for specialized remedial applications. Batelle Press, Columbus, pp 175180 Mozley PS, Davis JM (2005) Internal structure and mode of growth of elongate calcite concretions: evidence for small-scale, microbially induced, chemical heterogeneity in groundwater. Geol Soc Am Bull 117:14001412 Mulder EG, Deinema MH (1992) The sheathed bacteria. In: Balows A (ed) The prokaryotes: a handbook on the biology

123

Rev Environ Sci Biotechnol of bacteria: ecophysiology, isolation, identication, applications. Springer-Verlag, New York, pp 26132624 Murphy EM, Ginn TR (2000) Modeling microbial processes in porous media. Hydrogeol J 8:142158 Portilho M, Matioli G, Zanin GM, de Moraes FF, Scamparini AR (2006) Production of insoluble exopolysaccharide Agrobacterium sp. (ATCC 31749 and IFO 13140). Appl Biochem Biotechnol 129132:864869 Ragusa SR, de Zoysa DS, Rengasamy P (1994) The effect of microorganisms, salinity and turbidity on hydraulic conductivity of irrigation channel soil. Irrigation Sci 15: 159166 Ralph DE, Stevenson JM (1995) The role of bacteria in well clogging. Water Res 29:365369 Ramachandran SK, Ramakrishnan V, Bang SS (2001) Remediation of concrete using microorganisms. ACI Mat J 98:39 Ravenscroft N, Walker SG, Dutton GG, Smit J (1991) Identication, isolation, and structural studies of extracellular polysaccharides produced by Caulobacter crescentus. J Bacteriol 173:56775684 Reid RP, Visscher PT, Decho AW, Stolz JF, Bebout BM, Dupraz C, Macintyre IG, Paerl HW, Pinckney JL, PrufertBebout L, Steppe TF, DesMarais DJ (2000) The role of microbes in accretion, lamination and early lithication of modern marine stromatolites. Nature 406:989992 Rodgers M, Mulqueen J, Healy MG (2004) Surface clogging in an intermittent stratied sand lter. Soil Sci Soc Am J 68:18271832 Ross CW, Mew G, Childs CW (1989) Deep cementation in late quaternary sands near Westport, New Zealand. Aust J Soil Res 27:275288 Ross N, Villemur R, Deschenes L, Samson R (2001) Clogging of limestone fracture by stimulating groundwater microbes. Water Res 35:20292037 Seki K, Miyazaki T, Nakano M (1998) Effects of microorganisms on hydraulic conductivity decrease in inltration. Eur J Soil Sci 49:231236 Seki K, Kamiya J, Miyazaki T (2005) Temperature dependence of hydraulic conductivity decrease due to biological clogging under ponded inltration. Trans Jap Soc Irrigation Drain Reclam Eng 237:1319 Seviour R, Blackall L (Eds) (2007) The microbiology of activated sludge, 2nd edn. IWA Publishing Sharp RR, Cunningham AB, Komlos J, Billmayer J (1999) Observation of thick biolm accumulation and structure in porous media and corresponding hydrodynamic and mass transfer effects. Water Sci Technol 39:195201 Stabnikov VP, Ivanov VN (2006) The effect of iron hydroxide concentrations on the anaerobic fermentation of sulfatecontaining model wastewater. Appl Biochem Microbiol 42:284288 Stehr G, Zorner S, Bottcher B, Koops HP (1995) Exopolymers: an ecological characteristic of a oc-attached, ammoniaoxidizing bacterium. Microb Ecol 30:15126 Stewart TL, Fogler HS (2001) Biomass plug development and propagation in porous media. Biotechnol Bioeng 72: 353363 Stocks-Fischer S, Galinat JK, Bang S.S (1999). Microbiological precipitation of CaCO3. Soil Biol Biochem 31: 15631571 Sutherland IW (1990) Biotechnology of microbial exopolysaccharides. Cambridge University Press, Cambridge Thompson BG, Thomas JR (1984) Method of enhancing oil recovery by use of exopolymer producing microorganisms, United States Patent 4460043 Thompson BG, Thomas JR (1985) Method of enhancing oil recovery by use of exopolymer-producing micro-organisms, United States Patent 4561500 Tsang PH, Li G, Brun YV, Freund LB, Tang JX (2006) Adhesion of single bacterial cells in the micronewton range. Proc Natl Acad Sci USA 103:1143511436 Vandevivere P, Baveye P (1992) Relationship between transport of bacteria and their clogging efciency in sand columns. Appl Environ Microbiol 58:25232530 Veenbergen V, Lambert JWM, VanderHoek EE, VanTol AF, Weersma SI (2005) Underground space use, analysis of the past and lessons for the future. In: Proceedings ITAAITES World Tunnel Congress, 712 May 2005, Istanbul Weber KA, Achenbach LA, Coates JD (2006) Microorganisms pumping iron: anaerobic microbial iron oxidation and reduction. Nat Rev Microbiol 4:752764 Weiss JV, Emerson D, Megonigal JP (2005) Rhizosphere iron (III) deposition and reduction in a Juncus effusus L.dominated wetland. Soil Sci Soc Am J 69:18611870 Wingender J, Neu TR, Flemming HC (eds) (1999) Microbial extracellular polymeric substances: characterization, structure and function. Springer-Verlag Berlin and Heidelberg GmbH & Co Wu JG, Stahl P, Zhang R (1997) Experimental study on the reduction of soil hydraulic conductivity by enhanced biomass growth. Soil Sci 162:741748 Yamanaka T, Miyasaka H, Aso I, Tanigawa M, Shoji K (2002) Involvement of sulfur- and iron-transforming bacteria in heaving of house foundations. Geomicrobiol J 19:519528 Yang IC, Li Y, Park JK, Yen TF (1993) Subsurface application of slimeforming bacteria in soil matrices. In: Proceedings of the 2nd international symposium in situ and on site bioreclamation, April 1993, San Diego, CA, Lewis Publishers, Boca Raton, FL Yen TF, Yang ICY, Karimi S, Martin GR (1996) Biopolymers for geotechnical applications. In: Chenchayya TB (ed) North American water and environment congress & destructive water. ASCE, New York, pp 16021607

123