Chemosphere 286 (2022) 131721

Contents lists available at ScienceDirect

Chemosphere
journal homepage: www.elsevier.com/locate/chemosphere

Application of microbial immobilization technology for remediation of Cr

(VI) contamination: A review
Yating Jiang a, b, Fei Yang b, Min Dai a, Imran Ali c, ***, Xing Shen b, Xiaoting Hou b, d,
Saleh S. Alhewairini e, Changsheng Peng a, b, *, Iffat Naz f, **
a
Guangdong Provincial Key Laboratory of Environmental Health and Land Resource, Zhaoqing University, Zhaoqing, 526061, China
b
The Key Lab of Marine Environmental Science and Ecology, Ministry of Education, Ocean University of China, Qingdao,266100, China
c
College of Chemistry and Environmental Engineering, Shenzhen University, Shenzhen, 518060, China
d
Sunwater Environmental Science & Technology Co. Ltd., Rizhao, 262300, China
e
Department of Plant Production and Protection, College of Agriculture and Veterinary Medicine, Qassim University, Buraidah 51452, Qassim, Saudi Arabia
f
Department of Biology, Deanship of Educational Services, Qassim University, Buraidah, 51452, Saudi Arabia

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Remediation of Cr(VI)-contamination
via microbial immobilization technique
(MIT) have been critically examined.
• Applications of composite carrier and
modified carrier have been discussed.
• Methods of immobilization of microor­
ganisms have been analyzed and
elucidated.
• Mechanism of Cr removal by immobi­
lized microorganism has been explored
from the selection of immobilized
microorganism.

A R T I C L E I N F O A B S T R A C T

Handling Editor: Y Yeomin Yoon The discharge of chromium (Cr) contaminated wastewater is creating a serious threat to aquatic environment
due to the rapid pace in agricultural and industrial activities. Particularly, the long-term exposure of Cr(VI)
Keywords: polluted wastewater to the environment is causing serious harm to human health. Therefore, the treatment of Cr
Cr(VI) contamination (VI) contaminated wastewater is demanding widespread attention. Regarding this, the bioremediation is being
Bioremediation
considered as a reliable and feasible option to handle Cr(VI) contaminated wastewater because of having low
Microbial immobilization technology
technical investment and operating costs. However, certain factors such as loss of microorganisms, toxicity to
Microbial immobilizing methods
Mechanisms microorganisms and uneven microbial growth cycle in the presence of high concentrations of Cr(VI) are hin­
Microorganism immobilization devices dering its commercial applications. Regarding this, microbial immobilization technology (MIT) is getting great
research interest because it could overcome the shortcomings of bioremediation technology’s poor tolerance
against Cr. Therefore, this review is the first attempt to emphases recent research developments in the reme­
diation of Cr(VI) contamination via MIT. Starting from the selection of immobilized carrier, the present review is
designed to critically discuss the various microbial immobilizing methods i.e., adsorption, embedding, covalent

* Corresponding author. The Key Lab of Marine Environmental Science and Ecology, Ministry of Education, College of Environmental Science and Engineering,
Ocean University of China, Qingdao, 266100, China.
** Corresponding author.
*** Corresponding author.
E-mail addresses: engrimran56@gmail.com (I. Ali), pcs005@sohu.com, cspeng@sohu.com (C. Peng), iffatkhattak@yahoo.com, I.Majid@qu.edu.sa (I. Naz).

https://doi.org/10.1016/j.chemosphere.2021.131721
Received 22 May 2021; Received in revised form 26 July 2021; Accepted 28 July 2021
Available online 31 July 2021
0045-6535/© 2021 Elsevier Ltd. All rights reserved.
Y. Jiang et al. Chemosphere 286 (2022) 131721

binding and medium interception. Further, the mechanism of Cr(VI) removal by immobilized microorganism has
also been explored, precisely. In addition, three kinds of microorganism immobilization devices have been
critically examined. Finally, knowledge gaps/key challenges and future perspectives are also discussed that
would be helpful for the experts in improving MIT for the remediation of Cr(VI) contamination.

1. Introduction
Chromium (Cr) is a common heavy metal, mainly discharge from
leather preparations, chrome-plated parts of metal parts, textile printing
and dyeing, rubber and ceramic materials (Ukhurebor et al., 2021; Xia
et al., 2019). It exists in several oxidation states, while the most stable
forms are Cr(0), the trivalent Cr(III) and the hexavalent Cr(VI) (Pushkar
et al., 2021). The Cr(0) is a solid metallic specie, which is being created
in industry with high fusion point and mostly employed for making steel
and other alloys. Cr(VI) exists in several forms such as H2CrO4, HCrO4− ,
CrO42− and Cr2O72− in aqueous solution. When the pH of the solution is
greater than 7, then only Cr(VI) exists in the form of CrO42− . While, in
the pH range of 1–6, the HCrO4− is the dominant species (Carlos et al.,
2012; Dhal et al., 2013; Ukhurebor et al., 2021). Further, Cr(VI) could
interact with DNA, protein and other substances through skin contact,
respiratory system and digestive system after being absorbed by the
human body to destroy gene expression (Dong et al., 2018; Karthik et al.,
2017). However, Cr(III) could usually aggregates near the cell without
passing through the cell membrane, and destroys the function of the cell
by changing the cell surface morphology (F. Wang et al., 2017).
Compared with Cr(III), Cr(VI) has a higher degree of mobility and
toxicity (Tang et al., 2021; Jiang et al., 2019). That’s the reason it has
been classified as a major contaminant by the USEPA, and recommended
its maximum limit in drinking water to be 0.05 mg/L (Long et al., 2013;
Pushkar et al., 2021; Thacker et al., 2007). Regarding this, Fig. 1 is
illustrating the increasing number of research investigations on the
remediation of Cr pollution from 1991 till to to-date.
Presently, various methods such as chemical reduction, ion ex­
change, photocatalysis and electrokinetic remediation are being used to
treat Cr(VI) contaminated sewage (Singh et al., 2020; Tang et al., 2021).
However, certain factors like utilization of numerous toxic chemicals,
high operating and maintenance costs are the major limitations to use
them for practical applications (Tian et al., 2016). In contrast, the
bioremediation participates in the removal of Cr(VI) through
bio-sorption, bioaccumulation, and biotransformation with small in­
vestment, low operating cost and without generating secondary
pollutants (Sharma et al., 2021; Liu et al., 2006). Therefore, bioreme­
diation is being widely used for the treatment of Cr(VI) contaminated
sewage. However certain issues such as loss of microorganism (Kiran
et al., 2018), toxic effects due to higher concentrations of Cr(VI), and
uneven microbial growth cycle are affecting the bioremediation of Cr
(VI) (Zhu et al., 2019). While, the microbial immobilization technology
(MIT) can overcome these drawbacks by chemically or physically
retaining or confining the free microbial cells or enzymes and other
biological catalysts to a specific space area and can keep it active for
longer period of time can (Kathiravan et al., 2010). In addition, bacteria,
fungi, algae and other microorganisms can be immobilized using
different carriers and immobilization methods to control Cr pollution. It
is also considered as an effective way to solve the problems of microbial
loss and it can protect microorganisms from the direct toxic effects of Cr
(VI) (Kathiravan et al., 2010; Ma et al., 2019; Shi et al., 2018).
From last few years, various researchers have reviewed different
aspects of chromium pollution and MIT. Regarding chromium pollution,
the reviews about the sources, natural occurrence state, toxicity,
migration in the environment, effects on the environment and health,
and remediation strategies of Cr(VI) can be found in the literature
(Sharma et al., 2021; Jobby et al., 2018; Prevot et al., 2018; Ukhurebor
et al., 2021). A few researchers reviewed the bioremediation strategies
for chromium pollution, emphasizing the types of microorganisms in
addition to Cr(VI), the detoxification mechanism of microorganisms to
chromium, the influencing factors of bioremediation, and methods to
strengthen bioremediation (Tang et al., 2021; Fernández et al., 2018;
Pooja et al., 2020; Pradhan et al., 2017; Pushkar et al., 2021). Regarding
MIT, a few researchers reviewed the potential of MIT for different
environmental remediation, introduced different carrier materials and
different fixation methods for MIT, and discussed the factors affecting
the MIT repair process (Tithi et al., 2021; Bouabidi et al., 2018). How­
ever the applied research of MIT in Cr(VI) pollution treatment has not
been comprehensively reviewed.
Therefore, in order to fill this gap, a rigorous review of the literature
has been carried out to finally complete this comprehensive review. This
review is mainly designed to focus on the latest progress of MIT in the

Fig. 1. The number of publications on the treatment of Cr-contaminated sewage in the literature between the years from 1991 to 2021. The plotted date obtained from
“Web of Science” by entering the keyword “Treatment of chromium pollution” into the search field.

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Y. Jiang et al. Chemosphere 286 (2022) 131721

remediation of Cr(VI) pollution from the aspects of the selection of mi­
crobial immobilization carriers, microbial immobilization methods,
microbial immobilization devices and the selection of immobilized mi­
croorganisms. In addition, the future development directions are also
considered in order to provide a reference to research on MIT for the
remediation of Cr(VI) pollution.
2. Carrier selection for microbial immobilization
The selection of carrier material is one of the important factors that
affect the microbial immobilization. Different raw materials and
different preparation methods and processes produce different material
properties (Zhang et al., 2011). The specific surface area, pore size,
structure and mechanical strength of the carrier are the main charac­
teristics for the selection of carrier materials, as it has significant effect
on the microbial load (Qin et al., 2014; Wang and Li, 2006). At present,
the commonly used carriers mainly include inorganic carriers, organic
carriers, composite carriers, and new-type carriers. Table 1 summarizes
the representative substances employed as carrier materials with their
advantages and disadvantages. The application of MIT for remediation
of Cr(VI) pollution is listed in Table 2. The following subsections provide
a description of each carrier material, with comparison of its advantages
and disadvantages.
2.1. Inorganic carrier
Inorganic carrier materials can use its own porous structure to adsorb
microorganisms on its surface, such as activated charcoal, biochar,
diatomite etc. (Shang et al., 2014). Among them, biochar is an emerging
material, which is decomposed from carbon-rich biomass under
oxygen-limited pyrolysis. It has the characteristics of large specific
surface area, rich pore structure, and rich functional groups (Lehmann
and Joseph, 2009). It is an excellent inorganic carrier and can absorb
microorganisms effectively, provide them a stable environment to
maintain its cell activity for the improvement of its biodegradation ef­
ficiencies (Liu et al., 2012a,b). In addition, the hierarchical porosity and
carboxyl, hydroxyl and phenolic functional groups of biochar can pro­
vide considerable adsorption sites for Cr(VI), and can also reduce Cr(VI)
to Cr(III) with lower toxicity (Zhang et al., 2017).
When using biochar for microbial immobilization, the role of biochar
and microorganisms does not exist alone but combines adsorption and
reduction. Zhu et al. (2021) used wheat straw biochar to fix
sulfate-reducing bacteria (IBXM700) to treat Cr(VI) polluted wastewater
and compared its efficiency with free SRB6-2-1. They found maximum
removal of Cr(VI) by IBXM700 (286.54 mg g− 1), which was 166.3 and
30.86 mg g− 1 higher than that of free SRB6-2-1 and XM700,
respectively. The reason is that IBXM700 has the dual functions of
biochar and SRB6-2-1 to remove Cr(VI) by adsorption and reduction.
Biochar enhances the growth ability of SRB6-2-1 to withstand high
concentrations of Cr(VI). In addition, biochar can provide nutrients and
a good growth environment for microorganisms. Compared with free
bacteria, IBXM70 has a higher reproduction rate. Therefore, IBXM700
has a higher Cr(VI) removal ability. Using biochar as the carrier for
microbial growth can not only meet the basic needs of microbial
immobilization, but also achieve the purpose of resource reuse and
waste treatment, which has excellent practical application value (Zhu
et al., 2021).
2.2. Organic carrier
The organic carrier material can be embedded in microorganisms
using a gel formed by a high polymer (Bai et al., 2010). Organic carriers
involve two subcategories, natural carriers such as alginate and agar,
and synthetic polymers such as polyvinyl alcohol, polypropylene
ammonium etc. (Biaecka-Florjańczyk et al., 2011). Alginate is a
permeable, non-toxic and transparent matrix that provides a mild
environment for microorganisms and protects immobilized cells from
extreme changes in chemical and physical conditions during the
immobilization process (Kadimpati et al., 2013; Ruan et al., 2018).
Further, Samuel et al. (2013) used sodium alginate to immobilize Aci­
netobacter johnsonii, Escherichia coli and Bacillus subtilis for elimination of
Cr(VI) from wastewater. Then the efficiency of these immobilized bac­
terial biomass were compared with the unfixed/free bacteria. It was
observed that the maximum Cr(VI) adsorption capacity (657 mg g− 1)
were shown by bacteria immobilized by sodium alginate in the reactor.
After five adsorption and desorption experiments, the removal rate of Cr
(VI) was 74.22 %. Despite natural polymers are used widely, they have
disadvantages such as poor mechanical properties and chemical stabil­
ity. Hence, synthetic polymers such as polyvinyl alcohol are used to
immobilize microorganisms (Tithi et al., 2021). Synthetic polymers are a
kind of synthetic polymer materials with good mechanical properties,
but compared with natural polymers, their diffusion ability is poor
(Szcze Sna-Antczak et al., 2004; Xue et al., 2010).
2.3. Composite carrier
Single inorganic and organic materials often have great limitations,
and cannot meet the needs of complex environmental conditions in the
actual treatment process. Therefore, researchers are adjust the compo­
sition of a variety of organic or inorganic carriers to form a composite
carrier, so that various carrier materials can complement each other
(Zhang et al., 2011). Thus, polyvinyl alcohol and sodium alginate were

Table 1
Advantages and disadvantages of different microbial immobilization carriers.
Carrier type Material Advantages Disadvantages References

Inorganic Natural inorganic materials: sand,
carrier zeolite, bentonite, diatomite, kaolin,
alumina, etc.
Synthetic inorganic materials:
activated carbon, biochar, porous
glass, porous silicon, etc.
Organic Natural organic carrier: alginate, agar,
carrier carrageenan, gelatin, chitosan, etc.
Synthetic organic carrier: polyvinyl
alcohol, polyethylene glycol,
polyacrylamide, etc.
Composite It is composed of organic and
carrier inorganic carrier materials
New carrier Modified carrier material, magnetic
carrier material, nanometer materials
etc.
Good mass transfer effect, high mechanical strength, good Limited microbial (Gong et al., 2018; Wang
biological stability, extensive material sources, low cost, adsorption capacity and et al., 2012)
environmentally friendly, non-toxic to cells easy to fall off
(Annadurai et al., 2000;
Patricia et al., 2001; Shang
et al., 2014)
Convenient immobilization and molding, low toxicity to Poor mechanical strength, (Bai et al., 2010;
microorganisms, high immobilization density, and good weak durability Krajewska, 2004)
environmental friendliness
Adjustable softness and hardness, good flexibility, strong Not easy to immobilize, and (Bai et al., 2010; Oh et al.,
adhesion, good anti-microbial decomposition, stable poor mass transfer 2000)
properties, strong durability performance
Water-soluble swell ability, durability, ball formation, High preparation conditions (Cai and Sun, 2010; Zhang
permeability, porosity, etc. have been improved, and the and high cost et al., 2019a, 2019b)
treatment effect has been improved
Large microorganism load, high mass transfer efficiency, High preparation (Jing et al., 2012; Yan
high mechanical strength, not easy to be oxidized and requirements, high et al., 2013)
degraded preparation cost

3
Y. Jiang et al. Chemosphere 286 (2022) 131721

Table 2
Application of microbial immobilization technology (MIT) for remediation of Cr(VI) pollution.
Pollutants Microorganism Carrier material Immobilization References
method

Cr(VI) Bacteria Bacillus sp. Sodium alginate Embedding Kathiravan et al. (2010)
Bacillus sp. CRB-7 Sodium alginate, humic acid, biochar, diatomite, Adsorption - Wu et al. (2019)
vermiculite and bentonite embedding
Intrasporangium sp. Polyvinyl alcohol, sodium alginate, activated Adsorption - Yang et al. (2009)
carbon and diatomite embedding
Enterobacter sp. Sodium alginate Embedding Shi et al. (2020)
Alcaligenes, Myroides and Acinetobacter Sodium alginate and phosphorus mineral Adsorption - (Ma et al., 2019)
embedding
Discarded brewer’s yeast Sodium alginate and gelatin Embedding Yun et al. (2010)
Acinetobacter junii, Escherichia coli and Sodium alginate Embedding Samuel et al. (2013)
Bacillus subtilis
A. haemolyticus Sodium alginate Embedding Amir et al. (2016)
Ochrobactrum sp. Cr–B4 Polyvinyl alcohol and sodium alginate Embedding (Anuradha et al., 2016)
Ochrobactrum intermedium Polyvinyl alcohol and sodium alginate Embedding Yadav et al. (2021)
Streptomyces griseus Polyvinyl alcohol and sodium alginate Embedding Poopal and Laxman
(2009)
Pannonibacter phragmitetus LSSE-09 superparamagnetic Fe3O4 Adsorption Xu et al. (2011)
Shewanella oneidensis MR-1 Carbon nanotubes (CNTs) and sodium alginate Adsorption - Yan et al. (2013)
embedding
Pseudomonas aeruginosa Kaolin and vermiculite Adsorption Kang et al. (2015)
Anacystis nidulans agar Embedding Khattar et al. (1999)
Shewanella xiamenensis Graphene oxide Adsorption Li et al. (2019)
Graphene oxide and polyvinyl alcohol Adsorption – Luo et al. (2019)
embedding
Cr resistant strain QY-1 nano zero valent iron and humic acid Adsorption Hou et al. (2020)
Microbacterium liquefaciens MP30 Polyvinyl alcohol and sodium alginate Embedding Pattanapipitpaisal et al.
(2001)
Pseudomonas cells membranes Medium retention Viktoriya et al. (2003)
Arthrobacter CR47 gravel Medium retention Córdoba et al. (2008)
Enterobacter cloacae, porous media Medium retention Williams et al. (2014)
Flavobacterium sp. and Ralstonia sp.
Sulfate-reducing bacteria Sodium alginate Embedding Chai et al. (2005)
Biochar Adsorption Zhu et al. (2021)
Polyvinyl alcohol and sodium alginate Embedding Zhang et al. (2018)
Polyvinyl alcohol, sodium alginate, medical stone Adsorption - Di et al. (2019)
and corn cob embedding
F− , Cr(VI), Cr(III) Nano ZrO2 - polyacrylamide hybrid material, Adsorption - Zhang et al. (2020)
and SO42- sodium alginate and polyethylene glycol embedding
Pyrene and Cr(VI) Bacillus sp. and Microbacterium sp. Sodium alginate and biochar Adsorption – Wang et al. (2018)
embedding
Cr(VI) and phenol Acinetobacter guillouiae SFC 500-1A Sodium alginate Embedding (Onta On et al., 2017)
and Bacillus sp. SFC 500-1E Polymeric nanofibers Adsorption Pereira et al. (2021)
Cr(VI) and SO42- Extracellular polymeric substances Graphene oxide Adsorption Yan et al. (2020)
Cr(VI), Ni (II) and Bacillus brevis Sodium alginate Embedding Rajender et al. (2008)
Zn (II)
Cr(VI) Fungi Rhizopus sp. LG04 Polyvinyl alcohol and Sodium alginate Embedding Liu et al. (2012a,b)
Coriolus versicolor ceramic beads Adsorption (Rashmi et al., 2010)
Algae Cyanobacteria Sodium alginate Embedding Kamra et al. (2007)
Chlorella minutissima Sodium alginate Embedding Singh et al. (2012)
Pediastrum boryanum Sodium alginate Embedding Ozer et al. (2012)
Chlorella sorokiniana Corn cob Adsorption Athira et al. (2020)

used to make a composite carrier for fixation of sulfate-reducing bacteria
to treat Cr(VI)-polluted wastewater, and it was found that addition of
sodium alginate was beneficial for improvement of the mass transfer
performance, durability and Cr(VI) removal efficiency of the pellets
(Chai et al., 2005). Further, carbon nanotubes and sodium alginate
composite were employed for immobilization of Shewanella oneidensis
MR-1 to treat Cr(VI) contaminated wastewater. It was observed that
compared with free cells and microbeads without carbon nanotubes, the
beads added with carbon nanotubes accelerated the electron transfer
and reduced the rate of Cr(VI) up to 4 times. Moreover, the addition of
carbon nanotubes had greatly improved the stability and reusability of
the microbeads (Yan et al., 2013). Despite the composite carrier com­
bines the advantages of the two carriers, the high requirements for
preparation conditions and the high cost limit its application.
2.4. New carrier
The new carrier for specific performance can be obtained by
modifying the surface group or pore structure of the carrier material
(Huang et al., 2015). The number of oxygen-containing functional
groups, specific surface area and pore structure of the modified carrier
materials can be significantly changed, which greatly improves the
adsorption performance of the materials and become conducive for the
immobilization of microorganisms. Carrier material can be modified via
acid modification or alkali modification (Deng et al., 2016), salt modi­
fication such as ferric chloride modification (Y. F. Wang et al., 2017),
ferrous sulfate and calcium carbonate modification (Qiao et al., 2015).
Acid-modified loofah was employed to immobilize the Phanerochaete
chrysosporium for Cr(VI) elimination and it was noticed that acid
modification has increased the number of surface functional groups,
improved the reduction ability of biomass, provided more active
adsorption sites for Cr(VI), and thereby improved the efficiency of Cr
(VI) removal (Verma et al., 2014).
Recently, biochar carrier materials was usually modified to improve
the electron shuttling capacity and the adsorption capacity of Cr(VI),
thereby increasing the contact probability of microorganisms with Cr

4
Y. Jiang et al.
(VI) and enhancing the ability of microorganisms to remove Cr(VI)
(Zheng et al., 2020). The materials used in the study of biochar modi­
fication are mainly metal compounds containing Iron (Fe) (Sun et al.,
2019), Zinc (Zn) (Shi et al., 2020), Magnesium (Mg) (Xiao et al., 2018),
Manganese (Mn) (Zhang et al., 2019a, 2019b) or Aluminum (Al) (Huang
et al., 2018). These metal compounds generally improve the removal Cr
(VI) by biochar via enhancing chemical adsorption (Xiao et al., 2018;
Zhang et al., 2019a, 2019b). Further, FeCl3 was employed to modify
biochar, it was found that FeCl3 formed iron (hydrogen) oxide minerals
with a higher mass ratio of Fe during the high-temperature pyrolysis,
thus increased the surface charge of the biochar (Sun et al., 2019). Thus,
the electrostatic interaction with the surface of the positively charged
biochar have significantly increased the adsorption capacity of the
biochar to oxygen anions such as Cr(VI) (Cho et al., 2017). Further,
Zhang et al. (2020) used sodium alginate as the embedding agent,
montmorillonite and iron-modified biochar as the immobilized carrier
material to fix the fusion strain F14 to treat Cr(VI) contaminated soil,
and found that the modified biochar as an immobilized carrier had
improved the stability and adsorption capacity of the ball (Lu et al.,
2020).
In recent years, new carrier materials such as magnetic carrier ma­
terials and nanomaterials, are often used as additives for composite
carriers. Thus, Wang et al. (2021)used sodium alginate, polyvinyl
alcohol and Fe3O4 nanoparticles immobilized Escherichia coli to treat
tannery wastewater. The results showed that after 5 cycles, the magnetic
properties and high adsorption efficiency could still be maintained.
Further, Zhang et al. (2020) used ZrOCl2 and acrylamide monomer
hybrid polymerization to obtain nano ZrO2-polyacrylamide hybrid ma­
terial, and then it was employed to immobilize SRB to form nano
ZrO2-SRB particles to treat Cr(VI) and F− in groundwater. It was found
that the particles have the dual effects of reducing and adsorbing pol­
lutants in the water, which has effectively removed chromium and
fluorine form groundwater simultaneously, thus overcomes the limita­
tions of a single treatment method.
Through the comparison of different immobilized carriers, the
immobilization of microorganisms based on magnetic nanomaterials
was considered a promising method. It can improve the adsorption site,
physicochemical properties and mechanical strength of the material by
adjusting the morphology and composition of the material, thus pro­
moting the recycling of immobilized microorganisms after adsorption.
Fig. 2. Microbial immobilization methods: (a) Adsorption, (b) Embedding, (c) Covalent bonding, (d) Media retention (adopted and revised from (Bouabidi et al.,
2018) with permission from Springer).
5
Chemosphere 286 (2022) 131721
3. Microbial immobilization methods
Due to the different ability of microorganisms to adapt to the
external environment, appropriate immobilization methods should be
selected. According to the force and form of action between microbial
cells and carrier, the fixed state of microbial cells and the properties of
carrier, microbial immobilization methods can be divided into adsorp­
tion, embedding, medium interception, covalent binding, composite
immobilization and other methods in Fig. 2 (Bouabidi et al., 2018). The
following subsections provide a description of the immobilization
methodologies, their advantages and disadvantages and development
direction.
3.1. Adsorption
The adsorption method employs the physical properties of the carrier
material such as adhesion, surface tension, etc.) or the force between the
microorganism and the carrier (such as van der Waals force, hydrogen
bond and electrostatic attraction) to adsorb the microorganisms on the
carrier, thus achieving the immobilization of the microorganisms
(Huang et al., 2015). The advantages of the adsorption method are
simple preparation, good mass transfer performance, and good micro­
bial activity. However, the contact between the microorganisms and the
carrier is weak, and the ability to resist impact load is also weak. The
microorganisms adsorbed on the surface are not firmly attached and
easy to fall off.
A team of researchers’ have used clay minerals such as kaolinite and
vermiculite to adsorb and immobilize Pseudomonas aeruginosa to reduce
Cr(VI) in a glucose-modified medium, and found that glucose served as
the necessary electron donor. Thus, the growth of Pseudomonas aerugi­
nosa, was stimulated and have significantly improved the microbial
reduction rate of Cr(VI) (Kang et al., 2015).
Another group of researcher have modified superparamagnetic
Fe3O4 nanoparticles (NPs) with sodium citrate and polyethyleneimine,
and immobilized Pantobacter LSSE-09 cells by electrostatic attraction at
an initial pH of 9.0. They observed that as to compare with free cells,
immobilized cells not only have excellent Cr(VI) reduction ability, but
also smoothly separated and recovered from the reaction solution. In
addition, the immobilized cells has retained a high Cr(VI) reduction
ability even after six batch cycles (Xu et al., 2011).
Y. Jiang et al.
3.2. Embedding
The embedding method is to directly encapsulate microbial cells in
an immobilized carrier, which is relatively simple and has little effect on
microbial activity. Common embedding methods include gel embed­
ding, microcapsule and fiber embedding methods (Huang et al., 2015).
However, the entrapment will cause high mass transfer resistance, so it
is suitable for the reaction system where the substrate and product are
small molecules. Further, it is not suitable for the immobilization of
aerobic microorganisms due to its poor permeability (Seo et al., 2001).
The materials commonly used as embedding carriers include alginate,
polyvinyl alcohol, etc. They have porous structure, which makes pol­
lutants and metabolites easy to enter the carrier (Bayat et al., 2015).
Khattar et al. (1999) have used agar-immobilized Ancystis nidulans to
remove Cr(VI) from wastewater. They have compared the efficiency of
Cr(VI) removal from wastewater in the bioreactor at various different
cell densities, pH values and flow rates under the condition of 30 μm Cr
(VI) concentration. It was found that the bioreactor has shown the Cr(VI)
removal rate of 86 %, when operated for 6 h at a cell density of 200 mg
protein/ml, a pH of 7.0, and a flow rate of 0.05 mL/min.
Further, Shailendra et al. (2012) immobilized chlorella with sodium
alginate and were cultured in the designed photo bioreactor having
sewage for 48 h. Then these immobilized algal cells were employed for
Cr(VI) elimination from simulated wastewater. It was observed that at
pH of 2 and when the amount of adsorbent was 20 % (w/v), the
maximum adsorption capacity of Cr(VI) was 57.33 mg/g dry bio­
sorbent/L solution. While, with 0.5 M sodium hydroxide as the
desorption medium, more than 90 % of the total adsorption capacity was
recovered.
3.3. Covalent bonding
The covalent bonding method uses the amino, sulfhydryl, hydro­
carbon, and imidazole groups on microbial cell surfaces to form a co­
valent bond with the groups on the surface of the carrier, so that the
microbial cells and the carrier have strong binding force, not easy to fall
off, and have good stability (Hashem et al., 2015). However, this is more
complicated and the reaction conditions are more difficult to control
(Cao et al., 2003). Thus, presently the covalent bonding method has not
been used for the treatment of Cr-contamination.
3.4. Medium retention
The medium retention method is basically derived from the mem­
brane biological method. It mainly uses the special structure of the
immobilized carrier to trap or limit the targeted microorganisms within
a certain range, restricting the movement of the microorganisms in the
carrier without affecting the material transport. However, this method
has shortcomings such as easy fouling and clogging of the membrane
(Shen et al., 2011).
Viktoriya et al. (2003) used UAM-300 ultrafiltration membrane and
MFA-MA4 microfiltration membrane as carriers, and mixed the cell
suspension and agar solution in equal volumes and smeared it on the
membrane surface. They have observed that as compared to free mi­
crobial cells, immobilized cells were protected from excessive toxicity at
high chromate concentrations, thus immobilization has increased cell
viability. Further, Córdoba et al. (2008) trapped Arthrobacter Cr47 in a
gravel packed bed reactor to form a biofilm for reduction of Cr(VI). They
have noticed that the Arthrobacter Cr47 biofilm packed bed bioreactor
has proved to be promising technology for Cr(VI) removal from water
with a concentration of up to 30 mg/L in batches and cycles.
3.5. Composite immobilization
The composite immobilization technique employs the combination
of the above two or more immobilization methods to immobilize
6
Chemosphere 286 (2022) 131721
microorganisms. It can select a composite immobilization carrier (often
polyvinyl alcohol or sodium alginate is used as the basic carrier, and
additives with certain functions are added) with excellent performance
and low price according to the actual situation of the sewage, and the
combined immobilization process with reasonable economy and simple
operation. For example, Luo et al. (2019) immobilized Shewanella xia­
menensis on polyvinyl alcohol/graphene oxide biofilm (Fig. 3). It was
found that the assembled film had good biocompatibility and good
recyclability, and graphene oxide can play a role in electron shuttling to
promote the removal of Cr(VI) by microorganisms.
In composite immobilization, the adsorption embedding method is
an important immobilization method. First, the microorganisms and the
carrier material are fully mixed to make the microorganisms adhere to
the carrier material as much as possible, and then the mixed solution is
embedded and fixed with a gel agent such as sodium alginate. The
adsorption embedding method not only achieves high concentration of
microbial immobilization and high immobilization intensity, but also
solves the problem of microbial inactivation due to the microenviron­
ment and nutrients provided by carrier materials in the adsorption
process (Qian et al., 2012).
Ma et al., (2019) comparatively analyzed the restoration of Cr(VI) by
microorganism-phosphate rock immobilized inoculum (FB),
microorganism-alginate immobilized inoculum (MA) and microor­
ganism phosphate rock alginate immobilized inoculum, and found that
the Cr(VI) reduction rate of MPA was the highest with the reduction rate
of 94 %. It was proposed that the reduction of Cr(VI) occurs outside the
immobilized microorganisms which can protect the microorganisms
from the toxic effects of Cr(VI). The composite immobilization method
has a good application prospect in the remediation of Cr(VI) contami­
nated groundwater. While, Wang et al. (2018) studied three microbial
immobilization methods to treat pyrene-chromium(VI) co-contaminated
soil: (1) Biochar adsorbed bacteria (BC), (2) Sodium alginate embedded
bacteria (AC), (3) Sodium alginate and biochar adsorbed embedded
bacteria (BAC). They have concluded from the comparative analysis that
the use of BAC bioremediation has increased the dissipation of pyrene
and has reduced the content of Cr(VI) in the soil.
Further, Di et al. (2019) used polyvinyl alcohol and sodium alginate
as embedding agents, corn cobs and medical stones as carrier materials.
They analyzed the removal rate of SO42− , Cr(VI) and Cr(III) by immo­
bilized particles when comparing with or without medical stone as
carrier. They have observed that medical stone has a certain adsorption
capacity for SO42− , and a strong pH raising capacity for acidic solutions,
which can reduce the inhibition of the acidic environment on SRB ac­
tivity. It provides an excellent growth and metabolism environment for
SRB, which has a positive effect on the biological activity of SRB, and
thus resulted in the improvement of their abilities to treat pollutants. At
the same time, medical stone can strengthen the particle structure and
ensure the stability of the particles.
Through comparative analysis of different microbial immobilization
technologies, it was observed that the adsorption and the embedding
methods are the most common and simple, but the adsorption method
has shortcomings like weak binding force between the microorganisms
and the carrier, ultimately leading to loss of microorganisms during the
treatment process. While the embedding method has limitations like
large mass transfer resistance and poor permeability, which is not suit­
able for immobilizing aerobic microorganisms. Hence, composite
immobilization method covers the inadequacies of single immobiliza­
tion method, thus makes the microbial system more active, higher unit
density, less bacterial loss, stronger tolerance, higher mechanical sta­
bility and biochemical stability (Huang et al., 2015). The composite
immobilization method is a promising technology, which has incom­
parable performance and treatment effects.
Y. Jiang et al.
Fig. 3. Schematic illustration of the preparation of Xiamen Shewanella-grafted graphene oxide/polyvinyl alcohol biofilm. (Adopted and revised from (Luo et al.,
2019) with permission from ACS).
4. Research progresses in the development of microorganism
immobilization devices
In most microbial immobilization research experiments, a syringe is
used to manually drop the viscous polymer solution into immobilized
pellets. Although this technique is simple, but its disadvantage includes
low preparation efficiency of immobilized pellets. In order to overcome
these shortcomings, three kinds of microbial immobilization devices are
described in Fig. 4: (1) An automated equipment was used to prepare the
small amount of immobilized pellets required at a laboratory scale, as
shown in Fig. 4a (De-Bashan and Bashan, 2010). The equipment is
mainly composed of peristaltic pump, infusion tube, syringe and other
accessories. (2) Then same research group have developed a method of
using gravity to prepare a large number of immobilized balls with a large
diameter (2–4 mm), given in Fig. 4b (De-Bashan et al., 2004). The
bottom plate of the container of the device was drilled with a hole array
of 64 special-shaped nozzles. The alginate solution is poured into
container and then dropped into the container having the calcium
chloride solution under the action of gravity to form immobilized beads.
(3) De-Bashan et al. (2002) improved the equipment containing the
multi-nozzle embedding/immobilization system, pressurized to 10–15
psi with a compressor, and continuously produced immobilized pellets
of different diameters (100–200 μm) and regular shapes at a rate of 1–15
mL/min, as illustrated in Fig. 4c. This equipment design was based on
the above laminar jet splitting technology, and can be used to immo­
bilize microorganisms in different types of alginate solutions. Table 3
shows the comparison of immobilized products produced by three mi­
crobial immobilization devices.
5. Selection of microorganisms for immobilization
The selection of microorganism for immobilization is the key factor
to determine the treatment efficiency of Cr(VI) contaminated water by
MIT. The following subsections describe in detail the removal
7
Chemosphere 286 (2022) 131721
mechanism of Cr(VI) pollution by different types of immobilized
microorganisms.
5.1. Sulfate reducing bacteria (SRB)
The mechanism of SRB treating Cr(VI) polluted wastewater mainly
includes: (1) It uses sulfate as electron acceptor to oxidize simple organic
matter (such as lactic acid, acetic acid, etc.) in anaerobic environment to
produce hydrogen sulfide and bicarbonate ions (Eq. (1)), which reduce
Cr(VI) to Cr(III) (Eq. (2)) (Kieu et al., 2011); (2) it reduces Cr(VI) by
reductase enzymes (Smith and Gadd, 2010); (3) under neutral or slightly
alkaline conditions, Cr is absorbed and removes Cr(III) in the form of Cr
(OH)3↓ or Cr(VI) by microorganism (Li et al., 2012).
2CH2O + SO42− → 2HCO3− + H2S (1)
- 6+
3HS + 2Cr → 3S0 + 2Cr 3+
+ 3H +
(2)
Further, the removal mechanism of heavy metals by sodium alginate
entrapped SRB as illustrated in Fig. 5, demonstrated the removal of
metals by sulfide precipitation outside the immobilized spheres. It has
shown different steps such as the first was the diffusion of sulfate, then
the reduction by the anaerobic bacteria in the bead. While the second
was sulfide release, followed by the formation of metal sulfide, which
can effectively overcome the toxic effect of heavy metals on SRB. But the
biomass of SRB will be lost in the long-term operation process, thus it
required further research for improvement of the mechanical and mass
transfer characteristics of the immobilized beads (Kiran et al., 2018).
Moreover, it was observed that the adsorption and immobilization of
SRB by biochar has dual functions of removing Cr(VI) by biochar and
SRB. The mechanism of Cr(VI) removal is mainly adsorption and
reduction such as an ion exchange between Cr(VI) and
oxygen-containing functional groups of biochar based SRB; cation - π
interaction between Cr(VI) and C = C bond of aromatic ring; SRB can
reduce Cr(VI) to Cr(III) by reducing SO42− to S2− or by secreting some
Y. Jiang et al. Chemosphere 286 (2022) 131721

Fig. 4. Microorganism immobilization devices. (a) Laboratory scale (adopted and revised (De-Bashan and Bashan, 2010) with permission from Elsevier) and (b)
Medium scale production (adopted and revised (De-Bashan et al., 2004) with permission from Elsevier) and (c) Mass production (adopted and revised (Bashan et al.,
2002) with permission from Springer).

Table 3
Comparison of immobilized products produced by microbial immobilization devices.
Plant scale Ball diameter The formation of spherules Ball production rate Production quantity of pellets References

Laboratory scale 3–5 mm Peristaltic pump extrusion 0–100 mL/h Less De-Bashan and Bashan (2010)
Medium scale production 2–4 mm Gravity flow action 100 mL/min More De-Bashan et al. (2004)
Mass production 100–200 μm Compressor pressurization 1–15 mL/min Many Bashan et al. (2002)

reductase, so as to achieve the purpose of removal. While, the removal
efficiency of Cr(VI) from biochar immobilized SRB is affected by the
amount of biochar added (Zhu et al., 2021).
5.2. Bacillus sp.
The removal of Cr(VI) by Bacillus sp. is mainly achieved by extra­
cellular and intracellular reduction and by a small amount of biosorption
(Fig. 6). Bacterial cells produce Cr(VI) reductase and export it to culture
medium, which reduces Cr(VI) to Cr(III) in in vitro. In addition, Cr(VI)
mainly exist in the form of CrO42− , its structure is similar to sulfate.
Therefore, Cr(VI) can enter bacterial cells through sulfate transport
channels in the cell membrane, while Cr(III) cannot penetrate the cell
membrane, and the cytoplasmic material reduces Cr(VI) in the inclusion
solution to Cr(III). Wu et al. (2019) used sodium alginate (SA) as the
embedding material and humic acid (HA) as the adsorption material to
fix Bacillus sp. (CRB-7) to remove Cr(VI) pollution. Adsorption material
(HA) and embedding material (SA) have no direct contribution to the
removal of Cr(VI), but these materials are of great significance as a
carrier for fixing CRB-7. HA provides effective surface area for bacterial
growth, and uses abundant functional groups to directly contact the
bacteria and their exudates with Cr, thus promoting bacterial coloni­
zation and biological reactions. SA can be used as a controlled release
material for bacteria and their exudates, and provides better protection

8
Y. Jiang et al.
Fig. 5. The mechanism of metal removal by SRB immobilization (adopted and revised from (Kiran et al., 2018) with permission from Elsevier).
Fig. 6. Reduction mechanisms of Cr(VI) by CrB-7: (a) Cr(VI) is reduced outside
the cell and Cr(III) cannot pass through the cell membrane. (b) Cr(VI) through
SO42− transport channel into cells. (c) Cr(VI) is reduced in the cell. (d) Cr(VI) is
adsorbed on the cell surface (adopted and revised from (Wu et al., 2019) with
permission from Elsevier).
for microorganisms. Therefore, the use of HA and SA immobilized
strains combines the advantages of the two materials, it helps to increase
the bacterial density and stability for removing Cr(VI), and reduce the
toxic effect of Cr(VI) on microorganisms, thus successfully carrying out
biological reactions inside the immobilized strains.
5.3. Coriolus versicolor
Long-term reduction of Cr(VI) by the immobilized fungus Coriolus
versicolor was reported by Rashmi and Ashish (2010). It was found that
the sulfhydryl group in fungal protein can reduce Cr(VI) to Cr(III) and
can also interact with Cr(VI) ions. It was further reported that the thiols
in fungal proteins may have important significance for the reduction of
Cr(VI) by generating thioester compounds (Eq. (3)) (Mazurek et al.,
1991).
[Cr2O7]2− + 2RSH → 2[RSCrO3]− + H2O
Where, RSCrO3-
is a relatively stable Cr(VI)-thioester intermediate
(RSH stands for the corresponding mercaptan). The –SH of mercaptans is
an important group for the reaction of Cr(VI) with biological reducing
agents. The reducing agent will react with Cr(VI) only when the
Chemosphere 286 (2022) 131721
protonation or reducing agent protonates the protons with Cr(VI) (Eq.
(4)) (Rashmi and Ashish, 2010). The Cr(III) formed by the reaction is
adsorbed on the surface of the fungus by the amino group.
nH+ + 2Cr(VI) + 6RSH → 2Cr(III) + 3RSSR (4)
5.4. Ochrobactrum sp.
The Ochrobactrum sp. Cr–B4 was embedded in polyvinyl alcohol and
sodium alginate for biological reduction of Cr(VI) in sewage (Anuradha
and Vidya, 2016). It was found that when using PVA-alginate micro
beads with embedded bacteria, the removal effect of Cr(VI) was signif­
icant as compare to using bare PVA-alginate micro beads (without
embedded cells). Thus, illustrating biological reduction of Cr(VI) by the
PVA-alginate micro beads embedded with bacteria instead of adsorption
on the micro beads. The bacteria removal mechanism included bio­
sorption and enzyme-catalyzed chromate reduction. The rate of
removing Cr(VI) from sewage depended on the Cr(VI) concentration and
the rate of bacteria enzymatically reducing Cr(VI), rather than the
diffusion and mass transfer rate in the immobilized cell system.
Despite many advances have been made in the research on the
mechanism of chromium removal by immobilized microorganisms,
many studies are limited to the isolation of single anti-Cr microorgan­
isms and testing their bioremediation efficacy at a laboratory scale.
Hence, future research should further explore the mechanism of Cr
repair under the condition of multiple microbial compound immobili­
zation in order to clearly understand the response of each microbe, so as
to promote more on-site repair research.
6. Desorption and reusability of immobilized microorganisms
MIT has shown excellent potential in removing Cr(VI). However,
considering the economic and technological sustainability, the regen­
eration and reuse of immobilized microorganisms and the recovery of
chromium are very important. Therefore, ideally, the immobilized mi­
croorganisms should be able to be regenerated with eluent, and reused
for multiple consecutive treatment cycles. Studies have shown that
NaOH is an effective desorbent for eluting and adsorbing Cr from bio­
adsorbent materials (Bai and Abraham, 2003; He et al., 2019; Samuel
et al., 2013). Shailendra et al. (2012) used three desorbents (distilled
water, 0.5 M hydrochloric acid and 0.5 M sodium hydroxide) to elute Cr
from the biosorbent. The results have shown that the treatment effect of
(3)
sodium hydroxide was relatively good as compared to distilled water
and hydrochloric acid. It might be due to the adsorption of Cr(VI) by the
biosorbent caused the proton bridge effect on the surface of the bio­
sorbent. The alkaline washing will consume protons and the adsorbed Cr
will be released. However, the recovery rate of Cr(VI) after desorption is
9
Y. Jiang et al.
low. In addition, it is difficult to separate the microorganisms and the
carrier from the material when removing Cr(VI), thus leading to sec­
ondary pollution. In recent years, researchers have tried to use
magnetically modified materials as immobilization carriers. They found
that magnetic biosorbents have excellent stability and reusability, and
are easy to recycle (Wang et al., 2021; He et al., 2020). Therefore, future
research should explore magnetically modified materials to make MIT
more sustainable. However, Wang et al. (2021) found that the adsorp­
tion efficiency of the magnetic biosorbent decreased by 24 % after 5
cycles of adsorption and desorption. Therefore, it is necessary to conduct
more research attempts to increase the continuous treatment cycle of
MIT. In addition, detailed research on the recovery and regeneration of
immobilized microorganisms is needed because of its good economic
benefits.
7. Conclusions and future perspectives
Altogether, the microbial immobilization technology (MIT) could
improve the tolerance and treatment efficiency of microorganisms even
against a high concentrations of Cr-pollution, and also enhance the
stability of microbial cells, but most of the existing work is mainly
limited to laboratory-scale research. The practical application of this
technology is restricted due to the complexity of the operation. Further,
the environment of actual pollution site is complicated, having usually
multiple pollutants, and the application of this technology become
difficult. Therefore, the practical use of immobilized cells is demanding
further researches.
The selection of microorganisms and immobilized carriers plays a
vital role in the practical application of MIT. The main function of mi­
croorganisms is to adsorb and reduce Cr(VI), while the main function of
carrier materials is to protect microorganisms from Cr(VI) poisoning,
but some carriers such as biochar and graphene oxide can transfer
electrons, thereby improving the ability of microorganisms towards Cr-
remediation. Therefore, research should be focused on the development
of a cost-effective, physico-chemically stable, sufficient adsorption sites
and good biocompatibility carriers for immobilization of microorgan­
isms. Another direction of future research is to select suitable microor­
ganisms, the amount of microorganisms, the amount of carrier materials
and the immobilization time to prevent overcrowding of cells. In addi­
tion, we should deeply explore the interaction mechanism between
materials and microorganisms to achieve low operating costs and high
Cr-removal efficiencies.
Moreover, a detailed research on the recovery and regeneration of
immobilized microorganisms is highly needed because of its good eco­
nomic benefits. In recent years, researchers have tried to use modified
magnetic materials as immobilization carriers, and found that magnetic
biosorbents had a good stability and reusability, and are easy to recycle.
Therefore, imminent research should explore magnetically modified
materials to make MIT more sustainable and practically applicable for
industries.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Acknowledgements
This work was supported by the Guangdong College Students’
Innovative Project (pdjh2021b0538, X201910580158), the Guangdong
Provincial Key Laboratory of Environmental Health and Land Resource
(2020B121201014) and the Technology Innovation Project of Zhaoqing
(201904030103).
10
Chemosphere 286 (2022) 131721
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