Articulo 5
Articulo 5
Review
a r t i c l e i n f o a b s t r a c t
Article history: The concept of using biological process in soil improvement which is known as bio-mediated soil
Received 3 December 2015 improvement technique has shown greater potential in geotechnical engineering applications in terms of
Received in revised form performance and environmental sustainability. This paper presents a review on the soil microorganisms
9 February 2016
responsible for this process, and factors that affect their metabolic activities and geometric compatibility
Accepted 12 February 2016
Available online xxx
with the soil particle sizes. Two mechanisms of biomineralization, i.e. biologically controlled and bio-
logically induced mineralization, were also discussed. Environmental and other factors that may be
encountered in situ during microbially induced calcite precipitation (MICP) and their inuences on the
Keywords:
Bio-mediated soil improvement
process were identied and presented. Improvements in the engineering properties of soil such as
Microorganisms strength/stiffness and permeability as evaluated in some studies were explored. Potential applications of
Metabolic activities the process in geotechnical engineering and the challenges of eld application of the process were
Biomineralization identied.
Urease activity 2016 Institute of Rock and Soil Mechanics, Chinese Academy of Sciences. Production and hosting by
Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/
licenses/by-nc-nd/4.0/).
http://dx.doi.org/10.1016/j.jrmge.2016.02.004
1674-7755 2016 Institute of Rock and Soil Mechanics, Chinese Academy of Sciences. Production and hosting by Elsevier B.V. This is an open access article under the CC BY-
NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article in press as: Umar M, et al., Biological process of soil improvement in civil engineering: A review, Journal of Rock Mechanics
and Geotechnical Engineering (2016), http://dx.doi.org/10.1016/j.jrmge.2016.02.004
2 M. Umar et al. / Journal of Rock Mechanics and Geotechnical Engineering xxx (2016) 1e8
than on the ground, and studies of many years have proved the Table 1
relevance of biological activities in inuencing soil behavior, less Microorganisms whose urease activity is not repressed by NH
4 (Whifn, 2004).
work has been done in exploring the importance, relevance, use- Microorganisms High activity Not repressed Not pathogenic or
fulness and application of biology in geotechnical engineering. by NH4 genetically modied
Meanwhile, it is expected that a clear understanding of the impact Sporosarcina pasteurii Yes Yes Yes
of microorganisms and biological activity on soil behavior can lead Proteus vulgaris Unknown Yes Moderately
to proper soil characterization and/or classication and even Proteus mirabilis Unknown Yes No
Helicobacter pylori Yes Yes No
alternative geotechnical engineering solutions. This paper reviews
Ureplasmas (Mocllicutes) Yes Yes No
the concept of biomineralization and its applications in improving
the engineering properties of soils.
Please cite this article in press as: Umar M, et al., Biological process of soil improvement in civil engineering: A review, Journal of Rock Mechanics
and Geotechnical Engineering (2016), http://dx.doi.org/10.1016/j.jrmge.2016.02.004
M. Umar et al. / Journal of Rock Mechanics and Geotechnical Engineering xxx (2016) 1e8 3
Fig. 1. Microbial calcite precipitation process by urea hydrolysis (DeJong et al., 2010).
Fig. 2. Comparison of soil particles sizes, geometric limitations and microorganisms extended from Mitchell and Santamarina (2005) by DeJong et al. (2010).
Please cite this article in press as: Umar M, et al., Biological process of soil improvement in civil engineering: A review, Journal of Rock Mechanics
and Geotechnical Engineering (2016), http://dx.doi.org/10.1016/j.jrmge.2016.02.004
4 M. Umar et al. / Journal of Rock Mechanics and Geotechnical Engineering xxx (2016) 1e8
depend substantially on the environmental conditions result in the precipitation and the role of the precipitating organisms in this
formation of the minerals (Dhami et al., 2013). Thus, bacterial process within the microbial ecology remain contentious. Thus, the
precipitation of calcium carbonate is generally regarded as the process seems to be recognized in three different related mecha-
biologically induced process which depends largely on the type of nisms. First, biomineralization takes place as unwanted and acci-
bacteria involved, abiotic factors such as salinity and composition of dental by-product of microbial metabolism (Knorre and Krumbein,
medium, and other environmental conditions (Knorre and 2000). This is the most widely accepted mechanism. The process is
Krumbein, 2000; Rivadeneyra et al., 2004). depicted in Fig. 3. Then carbonate nucleation occurs on the cell wall
Biomineralization processes as documented in many studies of the microorganisms due to ion exchange through the cell
reported by Lian et al. (2006) are found to be active in almost every membrane, though the mechanisms are still poorly known
environment on Earth, with much of the microbial activity result- (Castanier et al., 2000). The third mechanism involves the extra-
ing in the carbonate minerals formation near the surface of the cellular macromolecules which are known to be capable of trapping
Earth. The microbial activity has been considered to play an calcium ions or sometimes serve as growth modiers to control
essential role in the carbonate formations as sediments and soil crystallization (Braissant et al., 2003).
carbonate deposits. Thus microbes from soils and some aqueous Therefore, recent understanding of the concept of bacterially
media are predominantly responsible for the inducement of cal- mediated carbonate precipitation relies on the fact that the car-
cium carbonate precipitates in both natural and laboratory settings bonate precipitate produced does not have any specic biological
(Peckmann et al., 1999). The most evident minerals resulting from functions which may be genetically related to the microorganisms
biomineralization process are carbonates. Microbially induced involved in the process. This conrms that microbially induced
calcium carbonates are mainly considered for their relative appli- mineralization to produced carbonate is the most prevailing pro-
cations in the elds of biotechnology, geotechnology and civil en- cess (Mann, 2001). However, the existence of different possible
gineering (Dhami et al., 2013). mechanisms with respect to the role of the microorganisms in the
Therefore, four factors are generally considered to mainly carbonate precipitation describes the complexity of the biominer-
govern the chemical process that leads to the precipitation of cal- alization process and the need to explore more into the process.
cium carbonate: calcium concentration, concentration of dissolved
inorganic carbon (DIC), the pH value and availability of nucleation 4. Factors affecting MICP process
sites (Hammes and Verstraete, 2002). Many bacterial species have
earlier been identied and suspected to be connected with natural Microbially induced calcium carbonate precipitation as a natural
carbonate precipitates from different environments. The main process that involves metabolic activities of the microorganisms
function of the bacteria in the precipitation process has conse- and some chemical reactions is generally governed by some envi-
quently been attributed to their capability of creating an alkaline ronmental conditions. Mortensen et al. (2011) assessed the effects
environment through the increase in pH value and dissolved of some factors that may be encountered in eld during MICP
inorganic carbon during their physiological activities (Hammes and treatment and are likely to affect bacterial growth, metabolism and
Verstraete, 2002). the precipitation induced by the bacteria using the bacterium
Microbial carbonate precipitation (MCP) has been extensively Sporosarcina pasteurii. Soil column and batch tests were used to
studied under natural environments and controlled laboratory assess the likely subsurface environmental factors in the treatment
conditions, but the precise mechanisms of the carbonate process. Microbial growth and carbonate precipitation were
Fig. 3. Schematic diagram of bacterial metabolism and subsequent CaCO3 precipitation under high pH and high Ca2 extracellular conditions (Hammes and Verstraete, 2002).
Please cite this article in press as: Umar M, et al., Biological process of soil improvement in civil engineering: A review, Journal of Rock Mechanics
and Geotechnical Engineering (2016), http://dx.doi.org/10.1016/j.jrmge.2016.02.004
M. Umar et al. / Journal of Rock Mechanics and Geotechnical Engineering xxx (2016) 1e8 5
evaluated in fresh and sea water as the possible aqueous environ- 5. Improvement in soil engineering properties
ments in situ. Ammonium concentration, oxygen availability,
mineralogy and soil particle sizes are part of the conditions that Many studies have been conducted to evaluate the strength/
may inuence ureolytic activity of the bacteria that are assessed. stiffness and permeability of different soils using calcite precipita-
The authors revealed that MICP treatment can be achieved over a tion induced by microbes. The changes in strength, stiffness,
wide range of soil types, particle sizes, concentrations of ammo- compressibility and permeability of the treated soil depend on
nium chloride and range of salinities. many environmental and other factors that govern the microbial
Okwadha and Li (2010) used Sporosarcina pasteurii at a constant reaction with the required reagents to induce calcite precipitates.
temperature to evaluate the effects of other environmental condi- Hence, improvement of soil properties is always governed by some
tions such as bacterial cell concentration, urea and calcium ions physical properties of soil. The degree of saturation of the soil has a
concentration. The study revealed that the rate of urea hydrolysis considerable impact on the resulting strength and stiffness of the
increases with the increase in bacterial cell concentrations and a treated soil. It was reported by Cheng et al. (2013) that particle size
tremendous increase in calcium carbonate precipitates of 100% was distribution, mineralogy, shape, density and texture of the mineral
recorded when the calcium ions were increased by ten times. The aggregates affect the cementation process in bio-mediated treat-
authors also reported that urease-catalyzed ureolysis is ment process.
temperature-dependant like any other enzymatic reaction, as such However, excellent results demonstrated by this technique in
a temperature range of 20 Ce37 C provided efcient MCP sealing leakages in water retaining structures and reducing the
depending on environmental conditions and concentrations of permeability of some soils by means of bioclogging have led to
other reactants in the system. Nemati and Voordouw (2003) and many interesting researches and applications of biosealing in many
Ferris et al. (2004) reported that the rate of ureolysis increases by civil engineering works (Whifn et al., 2007; Ivanov and Chu, 2008;
twice and ve times when the temperature was increased from van Paassen, 2011). The technique of using microorganisms to
10 C to 15 C and 15 C to 20 C, respectively. This clearly indicated improve the strength of granular soil which is referred to as bio-
that the increase in temperature within the optimum range accel- cementation started in 2001 in Australia. As reported by Kucharski
erates the rate of ureolysis depending on the other conditions. It et al. (2006), the technique was widely accepted by civil engineers
was also reported by Whifn (2004) that the urease activity in- after a bag of sand was turned into columns of calcareous sandstone
creases proportionally with the increasing temperature up to 70 C. when treated by Australian research group.
Soon et al. (2014) investigated the effects of some factors on the Biocementation can be dened as the soil improvement process
performance of Bacillus megaterium species in inducing calcium through the production of particle-binding materials via microbial
carbonate precipitates in residual soils. The factors considered in means. It is mainly used in geotechnical engineering applications
the study were concentration of bacteria, concentration of for strengthening, plugging and improving soils (Ferris et al., 1997;
cementation reagent, treatment duration, and ow pressure of the Nemati and Voordouw, 2003; Whifn et al., 2007). Recent studies
cementation reagents. The study revealed that substantial increase by Soon et al. (2013) revealed the effectiveness of microbial induced
in shear strength and reduction in hydraulic conductivity (69% and calcite precipitation in improving the shear strength and reducing
90%, respectively) were recorded after 48 h treatment period of the permeability of tropical residual soil and sand. The results
0.5 M cementation reagents and 1 108 cfu/mL bacteria concen- proved an excellent improvement in shear strength of 96% at 0.5 M
trations. Though many factors inuence the ureolysis of the bac- concentration of the cementation reagents. However, the strength
teria and the subsequent calcium carbonate precipitates such as improvement was retarded at higher concentration of the reagent
temperature, bacterial cell concentrations, type of bacteria, salinity (i.e. 1 M) due to high salinity that resulted in inhibitory effects on
and pH value of the medium, concentration of calcium ions, avail- the microbial activities. The ndings are in agreement with those of
ability of nucleation sites, mineralogy and particles sizes of the soil De Muynck et al. (2010) who found that higher concentration of
and many more, only some of these factors were evaluated in cementation reagents usually increases the salinity of the medium
relation to bacterial carbonate precipitates mostly in coarse- thereby retarding the microbial activity due to inhibitory effects,
grained soil, i.e. sand. Therefore, more studies are needed to though the activity of some microorganisms is not really affected by
assess the effects of these factors particularly in residual soil for the high salinity of the environment (Whifn, 2004). Some of these
eld implementation of the process. organisms are presented in Table 1.
Likewise, studies on the effect of different degrees of saturation Bioclogging can be dened as the reduction of hydraulic con-
on the geotechnical properties of bio-cemented sands were con- ductivity of soils or porous rocks by pore-lling materials generated
ducted by Cheng et al. (2013). Scanning electron microscope (SEM) by microbial processes. The carbonate precipitate generated
was used for the tested sand samples. It was revealed that the microbially is responsible for clogging the soil pore spaces, thereby
distribution of calcite precipitates depends on the degree of satu- restricting ow of water and decreasing the permeability of the soil.
ration of the samples, with fully saturated samples forming scat- Whifn et al. (2007) reported a reduction in permeability from 22%
tered crystals on the grain surface, while samples with lower to 75% of the initial permeability of the treated soil. Yasuhara et al.
degree of saturations forming strong calcite coating on the sand (2012) similarly revealed a decrease in permeability of 60%e70% of
grains which bonds them together. A mathematical model also a soil sample when an extract of urease enzyme was used directly
conrmed the ndings of this study, indicating a positive rela- to calcite precipitations induced. Meanwhile, Soon et al. (2014)
tionship between degree of saturation and particle size of the soil presented a decrease in hydraulic conductivity of 90% in residual
with the crystallization efciency. The ndings from Cheng et al. soil after a species of bacillus, Bacillus megaterium, was used to
(2013) revealed that higher strength can be obtained at lower de- trigger calcite precipitation in the soil.
gree of saturation with less chemicals, which is in compliance with Hence, considerable increase in unconned compressive
the result of Horn and Meike (1995). Meanwhile, it was found that strength and limited reduction in permeability of treated samples
aerobic microbial activity is optimum at 60%e80% degree of satu- are the basic qualities that make biocementation treatment
ration. Thus conducting the MICP treatment at lower degree of attractive (Harkes et al., 2010; Cheng and Cord-Ruwisch, 2012;
saturation would make it more economical by using smaller Soon et al., 2014). Meanwhile, preservation of permeability allows
quantity of cementation reagents, contrary to the other MICP for multiple treatments, use of low injection pressure and possi-
treatments conducted under fully saturated conditions. bility of treating large volume of soil. Therefore, biocementation
Please cite this article in press as: Umar M, et al., Biological process of soil improvement in civil engineering: A review, Journal of Rock Mechanics
and Geotechnical Engineering (2016), http://dx.doi.org/10.1016/j.jrmge.2016.02.004
6 M. Umar et al. / Journal of Rock Mechanics and Geotechnical Engineering xxx (2016) 1e8
can be used for in situ treatment underneath without disturbing unconsolidated porous media. They found that the increase in the
the existing buildings (Karol, 2003). Microbial calcite precipitate concentration of urease enzyme from 0.01 g/L to 0.1 g/L increases
induced in sands was studied and various microscopy techniques the production of CaCO3, while increases in urea and calcium
were used to assess how the pore space volume was altered by chloride beyond 36 g/L and 90 g/L, respectively, do not increase the
calcite precipitation. The calcite precipitate was distributed amount of calcite obtained by MCP. Hence, the temperature range
spatially within the pore spaces of the sand, thereby reducing the of 20 Ce50 C enhanced the production of CaCO3 at low concen-
permeability and increasing the stiffness of the sand samples tration of enzyme. Although the temperature effect has been
(DeJong et al., 2010). evaluated by some authors in relation to microbial carbonate pre-
Table 2 shows some reaction conditions reported in literature cipitation, other environmental factors such as humidity, dissolved
for the production of calcium carbonate via microbial urea hydro- cations, degree of saturation of the soil and many more need to be
lysis for biocementation, bioclogging and other applications. evaluated.
Though different methods of injecting the cementation reagents Yasuhara et al. (2012) reported potentials of using urease
into the soils were used in the treatment processes, substantial enzyme from other sources different from bacteria to catalyze the
improvement in strength and reduction in hydraulic conductivity hydrolysis of urea in the presence of calcium chloride to precipitate
of treated soils were reported. The major concern regarding the calcium carbonate for the improvement of engineering properties
usually adopted methods of injecting the cementation reagent from of sand samples. Findings from this study indicated that unconned
surface downward is the differential distribution of the calcite, with compressive strength of the treated samples increases consider-
many being deposited at the surface compared to that at the bot- ably, with the initial hydraulic conductivity of the treated samples
tom of the specimen, as reported by van Paassen (2009). being decreased by 60%e70%. Hence, since the urease enzyme can
Chu et al. (2012) observed substantial reduction in hydraulic be obtained directly from some plants such as sword beans,
conductivity and shear strength improvement both on the surface exploring into this alternative would be of immense contributions
and within the bulk of soil upon application of ureolytic bacterial particularly in eld applications of this technique. This is because
Sporosarcina pasteurii isolated from tropical beach sand. They also that handling of bacteria in terms of cultivation and storage needs
revealed that the modulus of rupture of the thin layer of calcium some technical expertise, and microbial metabolism which is a key
carbonate formed at the surface of the soil was 35.9 MPa, which is factor in MICP may not be straightforward enough to be controlled.
comparable with that of limestone. Likewise, Filet et al. (2012) Therefore, it may be impossible to constrain the extinction and/or
described MICP as a competitive treatment method for consolida- the generation of living bacteria in natural environments.
tion of ne-grained soil. The ndings of the study revealed that
volume of soil treated turned like calcareous sandstone in few days 6. Conclusions and suggestion for further studies
without considerable modication of the initial permeability of the
soil. Hence, an upscaling work for site application that led to the MICP can be considered as a practicable technique that can
validation of industrial concept was also presented. A 5 m sand improves soil-supporting new and existing structures and can be
column was treated using MICP under the condition that reects used in many geotechnical engineering applications, such as slope
eld application process. After treatment, the sand column shows stabilization and subgrade reinforcement. The process has shown
considerable improvement in strength, stiffness and load bearing greater potential in many engineering applications, but much work
capacity without making the soil impermeable (Whifn et al., has to be done to bring this convenient technology to eld appli-
2007). cations. Comparative studies need to be conducted to assess the
Biomineralized calcium carbonate has proved its efciency in feasibility of MICP with that of traditional grouting, particularly
both bioclogging and biocementation of soils and could be used in with regard to environmental implications and economy. Though
geotechnical engineering to improve the engineering properties of the technique has been recommended as an alternative method of
soil in situ (Ivanov and Chu, 2008). The authors further emphasized soil improvement, degrading of the calcite precipitate during
that these methods could be used as a replacement of the tradi- loading as reported by DeJong et al. (2010) poses a question on the
tional energy demanding mechanical compaction and chemical durability of strength induced by calcite precipitation. Likewise,
grouting methods that are expensive and sometimes harmful to the using higher concentration of cementation reagents would result in
environment. However, collaborative studies of civil engineering, higher strength but may make the environment more salty and
ecology and micro-biology are very fundamental for effective mi- affect some bacterial growth. Therefore, more studies on the
crobial treatment method. Nemati and Voordouw (2003) consid- feasibility of combining this technique with other methods that
ered the effects of varying concentration of urease enzyme, would provide long-term strength and durability such as lime are
cementation reagents and temperature on the permeability of recommended.
Table 2
Reaction conditions for the production of calcium carbonate using microbial urea hydrolysis.
Application Urea (mM) Ca2 (mM) Urease activity Microorganisms Soil type References
(mM urea/min)
Please cite this article in press as: Umar M, et al., Biological process of soil improvement in civil engineering: A review, Journal of Rock Mechanics
and Geotechnical Engineering (2016), http://dx.doi.org/10.1016/j.jrmge.2016.02.004
M. Umar et al. / Journal of Rock Mechanics and Geotechnical Engineering xxx (2016) 1e8 7
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and Geotechnical Engineering (2016), http://dx.doi.org/10.1016/j.jrmge.2016.02.004
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eralization of carbonates by Halobacillus trueperi in solid and liquid media with Murtala Umar is a lecturer at the Department of Civil
different salinities. FEMS Microbiology Ecology 2004;48(1):39e46. Engineering, Faculty of Engineering, Bayero University
Soon NW, Lee LM, Khun TC, Ling HS. Improvements in engineering properties of Kano, Nigeria. He obtained his rst degree in civil engi-
soils through microbial-induced calcite precipitation. KSCE Journal of Civil neering, master degree in geotechnical engineering from
Engineering 2013;17(4):718e28. Bayero University Kano, Nigeria and currently is under-
Soon NW, Lee LM, Khun TC, Ling HS. Factors affecting improvement in engineering going his PhD program at Universiti Tecknologi Malaysia.
properties of residual soil through microbial-induced calcite precipitation. He is currently a member of the Nigerian Society of En-
Journal of Geotechnical and Geoenvironmental Engineering 2014;140(5). http:// gineers and a registered engineer with the Council for the
dx.doi.org/10.1061/(ASCE)GT.1943-5606.0001089. Regulation of Engineering in Nigeria. He started his career
Stotzky G. Soil as an environment for microbial life. In: van Elsas JD, Trevors JT, as a lecturer in 2005 and taught a number of undergrad-
Wellington EMH, editors. Modern soil microbiology. Taylor & Francis; 1997. uate and postgraduate diploma courses and supervised
p. 1e20. some undergraduate projects. He published about ten
van Paassen LA. Bio-mediated ground improvement: from laboratory experiment to journal articles and attended some international
pilot applications. In: Geo-Frontiers 2011. ASCE; 2011. p. 4099e108. conferences.
Please cite this article in press as: Umar M, et al., Biological process of soil improvement in civil engineering: A review, Journal of Rock Mechanics
and Geotechnical Engineering (2016), http://dx.doi.org/10.1016/j.jrmge.2016.02.004