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Biogeochemical cycling of metals impacting by microbial mobilization and

immobilization

Article  in  Journal of Environmental Sciences · May 2017

DOI: 10.1016/j.jes.2017.04.035

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J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 7 ) XX X–XXX

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Biogeochemical cycling of metals impacting by microbial

mobilization and immobilization

Ran Jing, Birthe V. Kjellerup⁎

University of Maryland at College Park, Department of Civil and Environmental Engineering, 1147 Glenn L. Martin Hall, College Park,
MD 20742, USA. E-mail: rjingraymond88@gmail.com

AR TIC LE I N FO ABS TR ACT

Article history: Microbial mobilization and immobilization processes can affect the bioavailability and
Received 5 December 2016 mobility of metals thereby influencing their toxicity and can therefore be utilized to treat
Revised 9 February 2017 solid and liquid wastes contaminated by metals. However, the microbial mobilization
Accepted 19 April 2017 and immobilization of metals depends on the microbial metabolism, the environment
Available online xxxx conditions. In this review, mobilization and immobilization of metals are discussed with regard
to the presence and function of involved microorganisms and in relation to applications such
Keywords: as bioleaching. Furthermore, the biosorption process is evaluated as a possible approach for
Bioleaching microbial immobilization of metal on the basis of four mechanisms: (1) physical adsorption,
Biosorption (2) ion exchange, (3) complexation, and (4) microprecipitation. In addition, sulfide precipitation
Microbial immobilization by sulfate reducing bacteria was included as an example of an application of microbial
Microbial mobilization immobilization. Based on the evaluation and recommendations in this paper, bioremediation
Metals strategies for metals can be improved thus increasing the opportunity for field applications.
Toxicity © 2017 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences.
Published by Elsevier B.V.

Introduction
Human activities such as mining, metallurgy, industrial manu-
facturing and production, and domestic and agricultural use of
metal containing compounds have affected the distribution of
metals in the environment (Mohammed et al., 2011). As a result,
a large amount of metals have been redistributed on the surface
of the earth since the industrial revolution in the 18th century
(Thevenon et al., 2011; Wuana and Okieimen, 2011). Therefore,
there is a growing concern about the adverse effects of metals in
the environment. The metals in terrestrial and aquatic envi-
ronments have been shown to have toxicological effects on
the environmental and human health due to toxicological
effects and the ability to bioaccumulation in the food chain (Yi
et al., 2011). There are 13 trace metals and metalloids in the
environment: silver (Ag), arsenic (As), beryllium (Be), cadmium
(Cd), chromium (Cr), copper (Cu), mercury (Hg), nickel (Ni), lead
(Pb), antimony (Sb), selenium (Se), thallium (Tl), and zinc (Zn),
which are considered as the priority pollutants (Blais et al.,
2008). These inorganic pollutants mainly originate from metal-
lurgical processes, microelectronics manufacturing, energy
production, mining, industrial waste discharge and natural
sources such as metal liferous minerals (Voulvoulis et al., 2013).
Sediments are the major contaminated phase for metals in
aquatic systems. The concentration of metal contamination is
controlled by atmospheric transport, precipitation and the
weathering processes in addition to contamination from
urban water systems such as storm water and wastewater
(Harrison, 2012; Nagajyoti et al., 2010). Municipal and industrial
wastewater as well as sewage overflows are the main contrib-
utors of toxic metal pollution to the aquatic systems (Stumm
and Morgan, 2012).

⁎ Corresponding author. E-mail: bvk@umd.edu (Birthe V. Kjellerup).

http://dx.doi.org/10.1016/j.jes.2017.04.035
1001-0742/© 2017 The Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences. Published by Elsevier B.V.

Please cite this article as: Jing, R., Kjellerup, B.V., Biogeochemical cycling of metals impacting by microbial mobilization and
immobilization, J. Environ. Sci. (2017), http://dx.doi.org/10.1016/j.jes.2017.04.035
2 J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 7 ) XXX –XXX
Metals can be classified into two categories (A and B) on
the basis of their chemical properties. Class A metal cations
easily react with oxygen, while class B metal cations prefer
nitrogen or sulfur as reactants (Ho, 2012). Class A metals can
form stable products with hard acids or hard bases based on
ionic bonds. The most common class A metal cations such as
K+, Na+, and Mg2+ are important components of biological
cells. They exist in essential molecules for biological process-
es such as phospholipids and nucleic acids (Mao et al., 2013).
For example, Mg2+ is important to the living organisms
because it can stabilize the soft structure of macromolecules
such as Ribonucleic acid (RNA) and Deoxyribonucleic acid
(DNA) (Stumm and Morgan, 2012). Class B metals can react
with soft acids to form stable products with covalent bonds.
Some of these metals can also bind with methyl- and alkyl-
to form metal complexes in biological systems (Fallah and
Cundari, 2015). The “class B metals” discussed above was
referred to as “metals” in the following chapter of this
paper.
Many of the class B metals (e.g., Pb2+, Hg2+, Cr2+) are toxic
and can accumulate into biological systems due to adverse
effects on proteins and enzymes. For example, copper is an
essential nutrient at low concentrations, however, excess
copper is toxic to fish and is highly toxic to many invertebrate
species such as crab, shrimp and oysters (Ezeonyejiaku et al.,
2011). Studies indicated that chronic copper in aquatic
environment can cause gill, kidneys and spleens damages
(Yanong, 2010). In addition, excess copper can be a powerful
reactive toxin to human's body causing many symptoms
including immune diseases, fatigue, adrenal burnout, depres-
sion, and Alzheimer's (Govind and Madhuri, 2014). The toxic
copper species include Cu(OH)+, Cu2(OH)2+ 2 and CuCO3 (Okocha
and Adedeji, 2012). On the other hand, Cu2+ as an ion is widely
present in aquatic environment and it is considered as the
most toxic of dissolved copper species. Some class B metals
(e.g., Hg, Ag, and Cd) can cause organ dysfunction such as
disturbance of vision, brain damage, lung and kidney failure
and fragile bones, affects calcium regulation in biological
systems (Gulati et al., 2010). Lead (Pb) can cause short-term
memory loss and enhance the risk of cardiovascular diseases
(Padmavathiamma and Li, 2007). Other class B metals such
as As can impair natural cells activity and affect essential
cellular processes such as oxidative phosphorylation and ATP
synthesis (Tripathi et al., 2007). In addition, studies indicated
that some of the class B metals can also lead to psychiatric
disorders. For instance, Hg exposure can result in insomnia,
loss of memory, and restlessness.
Microorganisms have been applied for the recovery of
metals in polluted water and lands as an appropriate technol-
ogy for soil bioremediation (Akpor and Muchie, 2010; Wuana
and Okieimen, 2011). Two detoxifying mechanisms: microbial
mobilization and immobilization have been exploited for in-situ
or ex-situ bioremediation purpose. Microorganisms are capable
of interacting with metals and change their oxidation state
or organic complex thereby affecting the speciation and
mobility of the metal elements (Olaniran et al., 2013).
However, the mechanisms associated with metal bioreme-
diation by microorganisms are still not well understood.
Thus, this review focused on the role of microorganisms in
the biogeochemical cycling of metals. In addition, the
Please cite this article as: Jing, R., Kjellerup, B.V., Biogeochemical cycling of metals impacting by microbial mobilization and
immobilization, J. Environ. Sci. (2017), http://dx.doi.org/10.1016/j.jes.2017.04.035
processes of mobilization and immobilization by the micro-
organisms under physic-chemical conditions of the envi-
ronment were discussed.
1. Microbial mobilization
In natural environments, metals can exist in soil and
sediments in different physical forms such as dissolved,
colloidal, or as precipitates. They cannot be destroyed or
biodegraded by microorganisms unlike biodegradation of
organic pollutants such as polychlorinated biphenyls (PCBs),
polycyclic aromatic hydrocarbons (PAHs) and organochloride
pesticides (Marco-Urrea et al., 2015). Microorganisms can
increase the bioavailability of metals by bioleaching, rock and
mineral bioweathering and biodeterioration, and methyla-
tion (Gadd et al., 2012). These microbial processes play a
significant role in the mobility of metals. Bioleaching is a
process of using bacteria to dissolve metals and it is widely
used to extract valuable metals such as copper and gold
(Wang et al., 2009). While the metals of rock aggregates can be
decomposed and redistributed by microorganisms through
bioweathering process (Liu et al., 2011). Like bioleaching and
bioweathering, methylation can also increase bioavailability
and toxicity of metals. Some methylated metals such as
methylmercury are lipophilic. As a result, microorganisms
can facilitate volatilization of metals from the environment
(Hsu-Kim et al., 2013). In addition, the impact of biological
processes on metal is dependent on the metal forms and the
chemical environment of the contaminated sites. For example,
mineral components may contain considerable amounts of
metals that are unavailable to microorganisms. The release and
detainment of insoluble metal species can be controlled as a
result of microbial mobilization processes. On the contrary,
soluble metal species have greater mobility and bioavailability
thus making this form more toxic (Wu et al., 2010).
Previous studies have indicated that the mobility of metals
can be influenced by biofilm formation and the presence of
extracellular polymeric substances (EPS) such as polysaccharides
and proteins (Boult et al., 2006). Laboratory-scale experiments
and subsurface field studies performed by Boult et al. (2006)
indicated that the mobility of copper in waste disposal sites was
decreased due to the microbial activity. Because some bacteria
and fungi such as Suillus bovinus, Paxillus involutus, and
Thelephora terrestris produced more than 30 enzymes and
accumulated into the EPS thus enabling transport of copper
into cells (Boult et al., 2006). In addition, extracellular metabolites
such as aliphatic carboxylic acids and aromatic carboxylic acids
produced by mixed bacterial cultures containing species from the
genera Microbacterium, Acinetobacter, Bacillus and Pseudomonas can
mobilize metals (Cu, Ni, Co, V) from alkaline ores (Włodarczyk et
al., 2015). The research of Jensen-Spaulding et al. (2004) has
shown that naturally produced bacterial extracellular polymers
can bind with the metals copper and lead resulting in mobiliza-
tion and increase in the bioavailability of metals at specific
contamination sites. Microbial mobilization of metals can also be
achieved by altering redox (reduction and oxidation) reaction.
The redox reaction is occurring in the soil and aquatic environ-
ment between metals and microorganisms. Microorganisms are
usually served as oxidizing agents resulting metals to lose
 J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 7 ) XX X–XXX
electrons (Dixit et al., 2015). Then the electrons are accepted by
electron acceptors (e.g., nitrate and sulfate).
2. Bioleaching
Bioleaching or microbial leaching is a process in which metals are
extracted from low-grade ores by microorganisms. Bioleaching is
a simple and cheap method which can be operated 10 to 20 years
(Jadhav and Hocheng, 2012). It needs low capital investment and
operating costs for addition of acid to maintain a low pH
environment. Because bioleaching is often taking place in a low
pH environments ranging from 1.5 to 3.0 which allow most metal
cations to dissolve and thereby oxidize ferrous iron and sulfide
(Pradhan et al., 2008). Therefore, it has become an industrial
technology to recover valuable metals via mining of low-grade
ores containing copper sulfide (CuS), metal-bearing minerals, and
other industrial waste which otherwise cannot be processed
economically by traditional methods (Gadd, 2010). Application of
bioleaching processes in the metal industry is used to extract
valuable metals from their ores such as aluminum from bauxite
or copper from chalcocite and bornite (Gadd, 2010; Kostudis et al.,
2015). Fig. 1 shows an example of bioleaching process for copper
sulfide minerals from low-grade ores (below 0.6% Cu). Copper is
extracted based on two mechanisms: contact leaching (Fig. 1a)
and non-contact leaching (Fig. 1b). Contact leaching elaborates
that bacteria attach on the mineral surfaces and oxidize sulfide
minerals to sulfur and sulfate (Mikkelsen et al., 2007). For the
non-contact leaching, the bacteria oxidizes dissolved Fe(II) to
Fe(III) and the free ferric ions can oxidize the sulfide minerals
(Florian et al., 2011; Mikkelsen et al., 2007). As a result, leaching
liquor from ores contains copper ions and ferrous iron as shown
in Fig. 1a and b. The concentration of dissolved iron for leaching
liquor is usually 35–60 mmol/L which contains 40% to 70% of
ferrous iron and the copper concentration of the out-flowing
liquid is approximately 8 mmol/L. In 2014, approximately 20% of
the world's supply of copper is currently extracted by using
bioleaching (Evans, 2014).
Many microorganisms are involved in bioleaching processes
and bacteria within the genus. Studies indicated that microbial
communities of bioleaching process have a complex microbial
interactions and nutrient patterns due to a high microbial
diversity (Pradhan et al., 2008). Table 1 shows the key microbial
genera involved in the bioleaching. In bioleaching industry,
chalcopyrite (CuFeS2) is the most important copper-bearing
mineral as well as the major mineral source for commercial
copper recovery (Romo et al., 2013). Thiobacillus can utilize sulfur
from chalcopyrite as electron donor to obtain energy (Fu et al.,
2008; Kellermann and Griebler, 2009). Most Thiobacillus species are
chemolithoautotrophic bacteria growing at aerobic conditions
and utilizing carbon dioxide as the carbon sources. Microorgan-
isms for metal-sulfide-dissolving are usually extremely acido-
philic bacteria that can oxidize inorganic sulfur compounds and
Fe (II) (Bertoldo et al., 2004; Vera et al., 2013). Leptospirillum is a
genus of chemolithoautotrophic bacterium involved in ferrous
iron oxidizing. They can grow at a low pH (1.5–1.8) and high
concentrations of uranium in the environment (Bertrand et al.,
2015; Lollar, 2005). Thiobacillus is another genus which gains
energy from oxidation of reduced sulfur and thiosulfate (Xin et
al., 2009). Thiobacillus-like bacteria are moderately thermophilic
Please cite this article as: Jing, R., Kjellerup, B.V., Biogeochemical cycling of metals impacting by microbial mobilization and
immobilization, J. Environ. Sci. (2017), http://dx.doi.org/10.1016/j.jes.2017.04.035
3
and generally grow on pyrite and chalcopyrite. Other bacterial
genus like Acidianus and Sulfolobus can grow on ferrous iron and
reduce elemental sulfur and metal sulfur compounds as an
electron acceptor to hydrogen sulfide (H2S) (Jensen et al., 2015;
Vera et al., 2013).
Non-sulfide minerals can also be exposed to bioleaching,
which often takes place by heterotrophic bacteria (e.g., Bacillus sp.)
and by fungi (e.g., Aspergillus and Penicillium) (Panda et al., 2012;
Watling, 2014). During the bioleaching process, the microorgan-
isms need organic supplements as carbon resources for their
growth and energy from metal leaching. A previous study
indicated that Bacillus cereus isolated from the Kupferschiefer
black shale ore can be use to extract metals (Watling, 2014).
Kupferschiefer black shale ore contains rare and precious
metals (e.g., Cu, Ni, Zn, Pb, Ag, Zn, Co, Mo, Re, V, Se, Sn, Bi,
Au, Pt, Pd) of which Europe is the main consumer. The
leaching recoveries after 24–28 days were 2.5% for copper
and 9.3% for nickel. Aspergillus and Penicillium are two of the
most widely used fungi in bioleaching processes (Watling,
2014). Studies have shown that Aspergillus and Penicillium
can be applied for enhancement of bioleaching processes in
a variety of environment such as contaminated soil or waste
materials including fly ash and electrical waste (Qu et al.,
2013; Wu and Ting, 2006).
3. Microbial immobilization
Microbial immobilization of metals can be described as
changing the physical or chemical state of metals to reduce
the mobilization of metals (Dixit et al., 2015). Metals cannot be
biodegraded or destroyed completely but it is possible to
change their oxidation state or form organic complexes,
which can cause precipitation, reducing the bioavailability
thereby making the metals less toxic (Olaniran et al., 2013).
Microbial immobilization of metals is a complicated which is
affected by several factors such as characteristics of metal
concentration and solution, pH and temperature (Fu and
Wang, 2011; Gadd, 2009). pH value affects the functional
groups participating in metal binding groups thereby allowing
varying binding sites on microbial surfaces at different pH
levels. Most bacteria have a net negative surface charge due to
the ionization of their functional groups. Therefore, the
biosorption process is also highly depended on the charges
on the microbial surface and the presence of metallic cation
with positive charge or the extent of the complexation
reactions. Some studies have shown that metal biosorption
by living microorganisms occur in two steps (Abbas et al.,
2014). First, the metal is binding to cell walls. After that, the
metal ions are transported through the membrane (Abbas et
al., 2014). The mechanisms for metals transport across the cell
membrane are similar to the ion transport mechanism for Na+
and K+. On the other hand, dead bacterial cells can also
perform as biosorbents for metal cations except for mobile
alkali metal (e.g., K+) (Sulaymon et al., 2013). Microorganisms
can produce biofilm matrix consisting EPS that can act as a
metal cation sink (Flemming and Wingender, 2010). EPS play
one of the most important roles in biosorption of metals in
biofilms. This is mainly attributed to the fact that EPS is
anionic which can promote the biomineralization of metal
4 J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 7 ) XXX –XXX

Fig. 1 – Bioleaching process for copper sulfide minerals from low-grade ores based on two mechanisms: contact leaching
(a) and non-contact leaching (b).

ions as a good agent for deposition of mineral ions that are
cationic (Srivastava et al., 2013).
Studies indicated that microbial cells covered soil particles
have a higher sorption capacity for metals than other particles
such as clay minerals (Barakat, 2011). Therefore, bioavailability
of metals can influence biosorption and microbial immobiliza-
tion. However, to date, the exact mechanism of biosorption is
not well understood due to multiple possibilities of the metals
to be captured and transported inside the microbial cell (Wang
and Chen, 2006). There are four possible mechanisms for metal
immobilization of microorganisms in all microbe–metal–min-
eral interactions: (1) microprecipitation, (2) physical adsorption,
(3) ion exchange, and (4) complexation. The mobility, bioavail-
ability, and toxicity of metals can be decreased by microorgan-
isms, since they can obtain energy from metals redox reactions
by converting metals to a redox state with relatively low toxicity
through enzymatic (Wall and Krumholz, 2006). For example,
hexavalent chromium Cr(VI) can be reduced to Cr(III), resulting
in less soluble chromium(III), so hexavalent chromium is
removed from contaminated waters or sites by formation of
chromium oxide.
3.1. Microprecipitation
Microprecipitation is another possible mechanism of metal
biosorption that can take place at the cell surface. The process
is constrained by local conditions as a result of chemical
interaction between metal and microorganism cell surface
(Silva et al., 2016). Therefore, change of pH or redox potential
could influence the occurrence of microprecipitation. This
process does not necessarily involve a bond between micro-
organism cell and the metal. Instead, the metal cations and
metabolic products can form insoluble aggregates such as
sulfides, carbonates, and phosphonates. It is worth to mention
that microprecipitation is not dependent on the cellular metab-
olism, which shows that this process may occur with either living
or dead cells.

Table 1 – Phylogenetic relationships of microbial genera involved in bioleaching.

Bacteria name Found in environment Optimal Growth temperature (°C) References
growth pH

Thiobacillus Soil, marine sediments, sewage and 6.90 29.5 Fu et al. (2008), Kellermann and
industrial waste-treatment ponds Griebler (2009)
Leptospirillum Acid mine drainage and underground 1.5–2.1 40 Bertrand et al. (2015), Lollar (2005)
in the mines
Acidianus Hot acidic springs 3 60–95 Vera et al. (2013), Bertoldo et al. (2004)
Sulfolobus Sea sediment 2–3 75–80 Jensen et al. (2015), Vera et al. (2013)
Aspergillus Soil and decomposing plant matter 6–6.5 30 Panda et al. (2012), Watling (2014)
Penicillium Soil, fruits and bulbs of plants, –⁎ 34 Watling (2014)
seeds and stored foods

⁎ The pH range of the optimal growth for Penicillium is broad, because there are more than 150 species.

Please cite this article as: Jing, R., Kjellerup, B.V., Biogeochemical cycling of metals impacting by microbial mobilization and
immobilization, J. Environ. Sci. (2017), http://dx.doi.org/10.1016/j.jes.2017.04.035
 J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 7 ) XX X–XXX
Sulfate reducing bacteria (SRB) are capable of producing
hydrogen sulfide (H2S) in anaerobic conditions with the presence
of organic substrate or H2 as electron donor. Hydrogen sulfide is
a strong reducing agent and it is one of the most effective
precipitant to precipitate complex metals in wastewater, soil, and
sediments (Villa Gómez and Denys, 2013). The sulfide produced
from biological sulfate reduction can react with metals thereby
forming metal-sulfide precipitates with low solubility. Many
sulfide precipitates of toxic metals such as lead sulfide (PbS),
cadmium sulfide (CdS) and zinc sulfide (ZnS) have low solubility
products (Ksp), which often are several orders of magnitude lower
than that of their hydroxides (Azabou et al., 2007). The produced
hydrogen sulfide combines with metal dissolved in aqueous
solution to form metal sulfides (Tsuji et al., 2005). Therefore, SRB
can be used to sulfate reduction for metal removal from soil or
sediments (Fig. 2). First, sulfur-oxidizing bacteria produce sulfuric
acid through breakdown of sulfide minerals to leach metals from
contaminated soils. Metals are then released as an acidic sulfate
solution thereby allowing them to be removed by SRB in a
subsequent process. Effluent from industrial waste water usually
riches in sulfates and dissolved metals, such as Cu, Ni, Fe, and Pb
(Kiran et al., 2016). Discharge of such metal containing industrial
still has high sulfate in addition to metals. The sulfate can be
reduced to H2S, which often can lead to pipe corrosion (Al Zuhair
et al., 2008; Kiran et al., 2016). Hence, it should be noted that
the optimal environmental conditions must be achieved to allow
for sulfate reducing activity, when SRB has been applied to
bioremediation of metals (Gómez, 2013). Therefore, it is impor-
tant to reduce the sulfate from wastewater prior to its discharge
into the environment (Kiran et al., 2016). According to Gibert et al.
(2002), effective environmental conditions for SRB include: the
redox potential lower than 200 mV; excess of organic substrate or
existed H2 as electron donor; and pH higher than 5. Recent
studies indicated that microbial sulfate reduction can conduct in
environments with pH lower than 5 (Kieu et al., 2011; Singh et al.,
2011). SRB can form microniches that are small sites in microbial
ecology that have different microbial actions from bulk habitat of
soils or sediments (Bertics and Ziebis, 2010). Sulfate-reducing at a
low pH environment could be explained by the existence of
microniches with elevated pH around the bacteria (Koschorreck,
2008).
3.2. Physical adsorption
Physical adsorption of metals by microorganisms can be
described as a physico-chemical process of particles or mole-
cules adhering to a cell surface attributed by van der Waals'
forces and electrostatic interactions. The major components of
microorganisms' cell walls are polysaccharides, proteins, lipids,
and many functional groups such as hydroxyl, sulfate, and
phosphate contributing to metal binding such as hydroxyl,
sulfate, and phosphate as mentioned above. Therefore, the cell
surface adsorption process between the metal and its function-
al groups is independent of the metabolism. The energy
involved in this process is generally smaller than 1 kcal/g mol
(Kotrba, 2011). As a result, physical adsorption of metals is
usually passive process in natural environment. For example,
zinc, and copper can be adsorbed by biomasses of algae and
fungi through electrostatic interactions between the metal
ions and microbial cell wall (Abbas et al., 2014). In addition,
Please cite this article as: Jing, R., Kjellerup, B.V., Biogeochemical cycling of metals impacting by microbial mobilization and
immobilization, J. Environ. Sci. (2017), http://dx.doi.org/10.1016/j.jes.2017.04.035
5
electrostatic interactions have been demonstrated to be
responsible for biosorption of copper by Zoogloea ramigera
and Chiarella vulgaris (Abbas et al., 2014).
3.3. Ion exchange
Ion exchange is also affecting metal biosorption. Studies
showed that bacterial cell walls contain a mixture of monova-
lent and divalent cations that can be substituted by another
cation (e.g., H+) (Michalak et al., 2013). The major driving force
involved in ion exchange is the attraction of metals to the
bacterial cell surface. Cells have specific binding preferences for
certain cation exchange, which is highly depending on their
structure. For example, the ion exchange properties of natural
polysaccharides can result in bivalent metals exchange with
counter ions of the polysaccharides (Jee, 2007). These bivalent
metals can exchange with the counter ions such as Co2+, Cd2+
and Cu2+.
3.4. Coordination complexes
Metal ions can also combine with ligands to form coordination
complexes. A coordination complex compound can consist of
one or several metal cations as central atoms surrounded by
ligands (Cotton, 2005). If a single ligand binds to the metal ion
through two or more coordinating atoms, this complex com-
pound is called chelate. The most likely groups to be engaged in
this process include carboxyl, amino, thiol, hydroxyl, phosphate,
and hydroxyl–carboxyl. The complexation therefore binds to the
cell surface as a consequence of interaction between metal–
ligand and the active groups on the cell wall.
Although there are many explanations for metal biosorption,
the mechanisms are still not well known. The main reasons are
due to the complexity of the bacterial cell structure indicating
that multiple possibilities of the metals to be captured outside
and at the cell as well as transported inside the cell (Porcheron et
al., 2013). The possible mechanisms to explain the metal
biosorption process include physical adsorption, ion exchange,
surface adsorption and complexation, and microprecipitation
(Fig. 3). On the other hand, the mechanism of metal biosorption
based on the location of metal removed can be explained as
extracellular accumulation/precipitation, cell surface sorption/
precipitation, and intracellular accumulation (Porcheron et al.,
2013).
4. Conclusion and future perspectives
Rapid industrialization and technology development have
changed the concentrations and distribution of metals on the
surface and subsurface of the earth. As a result, metals are
widespread environmental pollutants concerning as they cannot
be biodegraded or destroyed (Förstner and Wittmann, 2012;
Mohammed et al., 2011). Instead microbial mobilization and
immobilization processes play an important role in bioremedia-
tion and biogeochemical cycling of metals. Bioleaching is an
important application of microbial mobilization that can be
utilized to recover valuable metal source from low-grade mining
ores and other industrial waste which otherwise would not be
6 J O U RN A L OF E N V I RO N ME N TA L S CIE N CE S X X (2 0 1 7 ) XXX –XXX

Fig. 2 – Bioremediation of heavy metal-contaminated soils by utilizing bioleaching and bioprecipitation.

processed by conventional methods. Application of biosorption from contaminated sites. However, there is little research
as a possible technology for microbial immobilization of metal conducted on the mechanism of biosorption and important
can be used to reduce the toxicity and mobilization of metals details are still not well known besides some descriptive studies.

Fig. 3 – Mechanisms of metal biosorption.

Please cite this article as: Jing, R., Kjellerup, B.V., Biogeochemical cycling of metals impacting by microbial mobilization and
immobilization, J. Environ. Sci. (2017), http://dx.doi.org/10.1016/j.jes.2017.04.035
 J O U RN A L OF E N V I RO N ME N TA L S CI EN CE S X X (2 0 1 7 ) XX X–XXX
Recently, many approaches have been proposed and studied
to improve mobilization and immobilization of the metals in
environment to decrease its toxicity effects. Adsorption can be
one of the alternative methods due to their low-cost and metal
binding capacities (Kurniawan et al., 2006). Industrial by-products
and agricultural by-products can be chemically modified to
enhance the removal performance for a hot spot of interest for
metal removal (Barakat, 2011). Different types of membranes
such as nanofiltration membranes and reverse osmosis mem-
branes have been increasingly studied for metal removal from
industrial wastewater effluent on the basis of the pore size and
the metals that needed be retained. Ultrafiltration with 5–
20 nm of pore size has become one of the most effective
approaches to separate metals from industrial wastewater
effluents (Barakat, 2011). Additionally, with the development
of nanoparticle technologies, there has been an increasing
application of magnetic nanoparticles for metal remediation
(Tang and Lo, 2013; Xu et al., 2012). The magnetic nanoparticles
have a nanoscale of particle size with high surface-area-to-
volume ratio which can remove metal faster. More importantly,
the magnetic property allows separation and recovery of
magnetic nanoparticles (Tang and Lo, 2013). Unlike in
microbial immobilization, magnetic nanoparticles treatment
can prove several advantages such as rapid process and
neglect of temperature effects. However, it is important to note
that recovery of magnetic nanoparticles still lacks controllabil-
ity and requires high installation and maintaining costs.
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