International Journal of Environmental Science and Technology

https://doi.org/10.1007/s13762-025-06369-6

REVIEW

New insights into immobilized bacterial systems for removal of heavy

metals from wastewater
U. Jhariya1 · M.‑F. Chien1 · M. Umetsu1 · M. Kamitakahara1

Received: 7 October 2024 / Revised: 26 December 2024 / Accepted: 20 January 2025

© The Author(s) 2025

Abstract
Industrial and anthropogenic activities release heavy metals (HMs) from natural resources, transforming them into toxic
elements. HMs can be extremely toxic, even at very low concentrations; their bioaccumulative nature damages ecosystem
endurance and human health. Bacterial bioremediation of HMs is an effective, sustainable, and reliable method owing to
inherent and adaptive systems of bacteria that facilitate significant HMs removal via adsorption, ion exchange, and bioac-
cumulation. However, the use of free cells in wastewater treatment compromises bioremediation efficiency. Bacterial immo-
bilization emerges as a promising visionary technique for treating HMs-contaminated wastewater. Therefore, the present
review elucidates the potential of various bacterial remediation mechanisms and highlights current research outcomes in the
field of metal ion bioremediation. Furthermore, this review explores the importance and potential applications of bacterial
immobilization in the context of metal ion bioremediation. A comprehensive literature review was conducted to demonstrate
the advantages of immobilized bacterial cells in HM-contaminated wastewater treatment. The groundbreaking relationship
between bacterial HM removal mechanisms and immobilization methods has been conclusively established. Future research
that integrates bacterial HM removal mechanisms and bacterial immobilization methods could play an instrumental role in
the effective treatment strategies and efficient recovery of HMs from wastewater.

Keywords Bioremediation · Heavy metals removal · Immobilization techniques · Support materials · Wastewater ·
Adsorption

Introduction et al. 2019). HMs are potentially toxic elements that act as
mutagenic and carcinogenic agents (Jaishankar et al. 2014).
Several anthropogenic activities release hazardous heavy Their perpetual use in various industries such as electroplat-
metals (HMs) into the environment, posing a severe threat to ing, electrolytic depositing, milling, etching industries, and
living beings. Elements with a specific gravity greater than petroleum refinery has led to increased deposition of HMs
5 g/cm3 are considered as HMs, of which a few are essential in the environment (Siddiquee et al. 2015).
micronutrients and macronutrients for the normal physi- The non-degrading, long biological half-life, and bioac-
ological activities in organisms (Ali et al. 2019). Elements cumulating nature of metal ions are the preeminent reasons
like molybdenum (Mo), iron (Fe), copper (Cu), and zinc for their well-delineated toxicity in organisms. Various
(Zn) have harmful effects at a particularly high concentra- environmental regulatory bodies have stipulated regulatory
tion, whereas metals like mercury (Hg), lead (Pb), and cad- mechanisms to control the utilization and release of HMs in
mium (Cd) show detrimental effects on the survival of living the environment (Khadim et al. 2019; Vareda et al. 2019).
beings at minimal concentrations (Qasem et al. 2021; Yin To conform with rules and legislation, many approaches
and technologies, such as physical adsorption, extraction,
or chemical oxidation, have been studied and employed to
Editorial responsibility: Samareh Mirkia.
reduce the presence of metals in the environment (Kapahi
* M. Kamitakahara and Sachdeva 2019). These processes are effective for treat-
masanobu.kamitakahara.a6@tohoku.ac.jp ing highly concentrated HMs in wastewater. Nevertheless,
their high cost, extensive maintenance requirements, exces-
1
Graduate School of Environmental Studies, Tohoku sive generation of toxic by-products, and limited process
University, Miyagi 980‑8579, Japan

Vol.:(0123456789)
 International Journal of Environmental Science and Technology

stability restrict their use in treating wastewater with low during application and vulnerability to external stressors
concentrations of HMs (Shrestha et al. 2021). Biological (Mehrotra et al. 2021). Employing immobilized or encap-
treatment methods appear to be sustainable and cost-effec- sulated bacterial cells provides distinct advantages over
tive alternatives for treating wastewater contaminated with free cell applications, whether involving a single species
low HM concentrations (Verma and Kuila 2019). Extensive or a consortium. These benefits include efficient segrega-
research has been conducted on the employment of organ- tion of biomass from treated water, greater efficacy in con-
isms such as plants, bacteria, and fungi for bioremediation trolling spatial and temporal distribution of biomass within
of HMs. Microbes, especially bacteria, can grow easily in the contaminated water, and improved viability, stability,
low concentrations of HM and mitigate them via adsorption, and reusability of bacterial cells without loss of activity
precipitation and transformation (Mukherjee et al. 2021). (Bouabidi et al. 2018; Li et al. 2013). Because of their
Previous research has demonstrated the ability of versatility, employing immobilized bacteria to remove
diverse bacterial communities to eliminate HMs from different metal ions under different stress conditions is a
wastewater. Table 1 outlines various investigations on the compelling solution. The usefulness of immobilized bacte-
use of bacteria for the remediation of HMs-contaminated ria was substantiated by a list of publications downloaded
wastewater. Nevertheless, the utilization of free bacterial from the Scopus database using the keywords ‘Bacteria &
cells for bioremediation in this context has certain limi- Heavy metals & Immobilization’. A total of 759 publica-
tations. These include low biomass concentrations at a tions were published between the years 2000 and 2023.
particular location or time, potential washout of microbes Figure 1 illustrates a continuous increase in research on

Table 1  Recent research on heavy metal removal using different bacteria

S. no HM contaminants Bacteria Initial conc Removal percentage References

1. Pb Lactobacillus brevis 200 mg/L 95.04% Dai et al. (2019)

Staphylococcus hominis AMB-2 50–57 mg/L 88% Rahman et al. (2019)
Micrococcus sp. NCTC-1716 2.5 mM 97.20% Zakaria Gomaa (2019)
Serratia marcescens 100 mg/L 97.57% Zhu et al. (2019)
2. Cr Pseudomonas aeruginosa 20 mg/L 89.67% Oyewole et al. (2019)
Bacillus subtilis, Pseudomonas aeruginosa 25 mg/L 96% Rizvi et al. (2020)
Cronobacter muytjensii KSCAS2 100 mg/L 72.45% Saranya et al. (2018)
Pseudomonas aeruginosa 1688 10 mg/L 26% Chug et al. (2021)
Bacillus sp. CRB-B1 100 mg/L 68.5% Tan et al. (2020)
3. Cu Pseudomonas aeruginosa 15 mg/L 90.89% Oyewole et al. (2019)
Aureispira sp. CCB-QB1 100 mg/L 82.2% Hasyimah et al. (2021)
Cronobacter muytjensii KSCAS2 100 mg/L 76.51% Saranya et al. (2018)
Serratia marcescens 100 mg/L 93.28% Zhu et al. (2019)
4. Cd Bacillus subtilis, Pseudomonas aeruginosa 400 mg/L 91% Rizvi et al. (2020)
Cronobacter muytjensii KSCAS2 100 mg/L 55.23% Saranya et al. (2018)
Serratia marcescens 100 mg/L 84.27% Zhu et al. (2019)
Pseudomonas taiwanensis 50 mg/L 45.08% Satapute et al. (2019)
5. Ni Pseudomonas aeruginosa 1688 10 mg/L 9% Chug et al. (2021)
Bacillus amyloliquefaciens Bcillus 500 mg/L 89% Khadim et al. (2019)
aryabhattai, Proteus mirabilis, Bacillus
subtilis, & Bacillus atrophaeus
6. As Bacillus thuringiensis WS3, Pseu- 7.5 & 9 mg/L resp. 95% As (III), 98%As (V) Altowayti et al. (2020)
domonas stutzeri WS9 & Micrococcus
yunnanensis WS11
Pseudomonas taiwanensis 50 mg/L 65.48% As (III) Satapute et al. (2019)
Lactobacillus acidophilus 1 mg/L 60% As (III) Singh and Sarma (2010)
7. Se (IV) Lysinibacillus fusiformis NDSe-7 80 mg/L 98% Won et al. (2021)
Bacillus safensis JG-B5T 2.5 mM 70% Fischer et al. (2020)
Shewanella putrefaciens 200 100 μM 93% Jiang et al. (2012)
Pseudomonas aeruginosa ATCC 27853 1.0 mM 85.3% Kora and Rastogi (2016)
Burkholderia fungorum 95 2.0 mM 60% Khoei et al. (2017)
International Journal of Environmental Science and Technology

Fig. 1  Number of publications

using keywords ‘bacteria, heavy
metals, and immobilization’
from year 2000 to 2023

HM bioremediation by bacterial immobilization from 2000 Contamination sources and toxicity of HMs
to 2023. The first study on bacterial immobilization for
HM removal was published in 1980. Thereafter, the num- HMs are part of elements that compose the earth’s crust and
ber of publications rose significantly from the year 2000 are introduced into the environment via natural and anthro-
onwards, indicating the increasing interest of researchers pogenic processes. Numerous studies have reported a rise
in utilizing bacterial cell immobilization to remove HMs in HM contamination in recent years (Kapahi and Sachdeva
from wastewater. Moreover, immobilization methods and 2019; Siddiquee et al. 2015). Concerningly, rapidly grow-
the immobilizing matrix are the two most important fac- ing industries are generating large amounts of wastewater
tors for achieving optimal bacterial growth and activity. containing HMs, which is subsequently discharged into the
Some researchers have discussed the effect of immobiliz- environment (Jin et al. 2018). Extremely toxic HMs, such
ing matrices on the functioning of bacteria; however, stud- as V, Cr, Ni, Cu, Sn, Cd, Zn, and Pb, are generated in waste
ies on the effect of immobilization methods on bacterial from industries that engage in electrolytic deposition, elec-
functions remain limited. Utilizing immobilization meth- troplating, conversion coating, anodizing-cleaning, etching,
ods, such as embedding, encapsulation, and surface attach- and milling (Medfu Tarekegn et al. 2020). Other industries
ment, while considering the bacterial mechanisms of HM that contribute remarkable amounts of Sn, Pb, Ni, and As
removal, may enhance the overall remediation efficiency. include printed circuit board manufacturing and wood pro-
This review provides a comprehensive and informa- cessing. In addition, petroleum refineries generate effluents
tive overview of the primary remediation processes and containing Ni, V, and Cr from catalytic conversions. Pho-
underlying cellular mechanisms employed by bacteria to tographic operations also produce effluents containing high
facilitate the HMs removal from wastewater. It delves into concentrations of Ag and ferrocyanide (Shrestha et al. 2021).
the application of bacterial immobilization for the biore- Several of these HMs, even in trace amounts, play impor-
mediation of HM-contaminated environments, highlights tant roles in the biochemical, physiological, and metabolic
factors that influence the efficiency of immobilized cells. A processes of living organisms. They also serve as micronu-
groundbreaking aspect of this paper is the establishment of trients, enzyme co-factors, and regulate the osmotic pressure
a novel link between bacterial immobilization techniques of the cell. However, the acceptable concentration ranges for
and HM removal mechanisms, offering valuable insights for these HMs are narrow, and uptake in excess of these ranges
optimizing remediation processes. Furthermore, the review can result in severe toxicity. The non-biodegradable nature
consolidates and tabulates previous research and recent of HMs results in bioaccumulation and causes several life-
advancements, presenting a well-rounded understanding of threatening diseases (Ayangbenro and Babalola 2017).
the topic. It concludes by addressing key challenges, recent The toxicity levels of metals vary depending on the types
innovations, and potential future directions, making it a piv- of metal ion and their concentrations. The maximum con-
otal resource for researchers and practitioners in the field. centration limit of As is 10 μg/L in drinking water (WHO
 International Journal of Environmental Science and Technology

2021); an increase beyond this limit can cause mental disor- environments. Various traditional physicochemical methods
ders, dermatitis, liver cirrhosis, ulcers, bronchitis, and cancer used in industries are well-suited for treating wastewater
(Gogoi et al. 2024). Exposure to Cr can instigate chronic with a high load of metals. Nevertheless, these traditional
proteinuria and lung emphysema. Excess concentrations of chemical methods are unsuitable for addressing low-con-
Cr can lead to hair loss, asthma, diarrhea, and osteomalacia centration HM-contaminated wastewater due to drawbacks
in humans (Chug et al. 2021). The permissible limit of Co is such as high costs owing to the generation of toxic byprod-
5–50 μg/day, which is very important for the functioning of ucts, excessive secondary sludge production, and demand-
vitamin B12. Ingestion of Co beyond the permissible limit is ing maintenance requirements (Jacob et al. 2018). In this
associated with adverse effects on the thyroid, hematopoietic context, the advancement of new technologies has resulted
systems, and heart, frequently implicated in occupational in the evolution of “bioremediation” as a powerful alterna-
lung disease, allergic reactions, and the development of tive tool to remediate low-concentration HM contaminated
tumors (Genchi et al. 2023). Overconsumption of Pb may wastewater at a cheap expense. Microbes, especially bac-
cause detrimental effects such as reduced intelligence in teria, have gained recognition for their remarkable ability
children, lower cognitive function, and encephalopathy. to remove HM via bio-sorption, bio-accumulation, bio-
Copper ion toxicity affects glucose metabolism, fat metabo- precipitation, and bio-transformation. Figure 2 explains the
lism, gastrointestinal, kidney, and liver functions, along with detailed mechanism performed by bacteria to remove HMs
the indirect genesis of oxidative stress (Concórdio-Reis et al. from the surrounding environment. Omnipresence, diversity,
2020; Dixit et al. 2015). extensive range of genes, enzymes, and the ability to adapt
to any harsh conditions govern the environmental resilience
of bacteria to bioremediate HMs-contaminated wastewater
Bacteria‑facilitated HM bioremediation (Rizvi et al. 2020).
Several bacterial species, such as Micrococcus, Pseu-
Health effects associated with HMs include disruption of domonas, Flavobacterium, Enterobacter, and Bacillus, that
vital enzymatic functions, catalysis of reactive oxygen spe- are exposed to HM-polluted habitats have developed and
cies generation, and directly inhibiting protein and DNA adopted various detoxification mechanisms. Bacteria pre-
formation. These effects necessitate an immediate and dominantly perform adsorption by uptake of HMs on the cell
effective solution for the remediation of HM-contaminated surface, intracellular sequestration by accumulation of HM

Fig. 2  Generalized schematic diagram of heavy metal removal mechanisms by bacterial cells
International Journal of Environmental Science and Technology

within the cell, and extracellular sequestration by precipita- imine, amide, imidazole, and carbonyl (ketone), exhibit
tion and interaction with other ions (Sreedevi et al. 2022). remarkable metal-binding capacity (Singh et al. 2020).
These mechanisms are associated with an active defense Wang et al. (2023) showed that COOH, NH, OH and C–H
system in microorganisms. However, the success of these groups were present on the surface of Bacillus subtilis TR1
mechanisms depends on different factors, such as micro- and were responsible for uptake of Cd(II) (Wang et al. 2023).
bial growth conditions, pH, temperature, and nutrient avail- These functional groups are recognized for their role as
ability (Nanda et al. 2019). Furthermore, according to some exceptionally active ligands, facilitating rapid binding pro-
studies, HM absorption from wastewater can be achieved cess with metal ions (Zvinowanda et al. 2010). Fourier trans-
using dead bacterial biomass as well. This process, called form infrared spectroscopy (FTIR) studies have additionally
metabolism-independent biosorption, occurs because of the revealed that carboxyl, hydroxyl, and amine groups present
physicochemical interactions between the metal ions and on the biomass surface of Aeromonas hydrophila contribute
functional groups present on the outer surface of microbial to Pb(II) sorption (Hasan et al. 2009). Dawwam et al. (2023)
cells (García-García et al. 2016). conducted another study to understand the adsorptive and
hydrophilic properties of Paenibacillus dendritiformis 17OS
cells for the removal of Pb(II). FTIR analysis revealed that
HM remediation mechanisms employed functional groups such as P-O, COOH, and C=O, played
by bacteria crucial roles in the adsorption process. Adsorption of metal
ions also occurs through extracellular polymeric substances
Bio‑adsorption (EPS), as demonstrated by various researchers. The role of
EPS in Cr(VI) removal was explained in a study on biosorp-
Adsorption is the non-directional physicochemical interac- tion by Pseudomonas aeruginosa ATHA23. It was also
tion of organic and inorganic substances with cellular com- found that EPS production increased to 0.717 mg/L when
ponents. Adsorption of a few HMs is preferentially medi- Pseudomonas aeruginosa ATHA23 was exposed to Cr(VI)
ated through the interplay of active functional groups on the and significantly decreased by 0.117 mg/L in the absence of
microbial cell surface and metal ions (Stephanie et al. 2020). Cr(VI) (Ataabadi et al. 2022). FTIR analysis revealed the
Electrostatic interactions between charged compounds and role of amide and C=O groups in the attachment of Ni(II)
van der Waals forces between non-charged compounds are with EPS and the involvement of OH, C-O, NH, diketone,
the primary attractive forces for adsorption. Physical adsorp- and ester functional groups of EPS in the binding of Cr(VI)
tion relies primarily on van der Waals forces, whereas acti- (Chug et al. 2021).
vated or chemical adsorption involves interaction between The functional groups present on the bacterial surface
the absorbent and adsorbate. A combination of these mecha- also assist in the transformation of toxic HMs into their non-
nisms and interactions functions either simultaneously or toxic forms via ion exchange mechanisms. Metal cations
independently to support HM adsorption on the surface of adhere to an unoccupied site that was previously occupied
microbes (Pham et al. 2022). by other cations during the ion exchange process (Sag and
The accumulation of metals on the cell surface also Kutsal 2001). The adsorption of divalent metal ions occurs
depends on the cell wall composition of microbes, which can via an exchange mechanism with polysaccharide counter
be affected by surrounding environmental conditions (Dixit ions located on the cell wall and outer membrane of bacte-
et al. 2015). In Gram-positive bacteria, functional groups ria. This intricate process is influenced by multiple factors,
like phosphoryl and carboxyl create negatively charged sites including the types and quantities of sites available on the
for the adsorption of HMs, whereas lipopolysaccharides are cell surface, as well as their ionization behavior, which in
the primary sites for metal interaction in Gram-negative turn is dictated by the pH and pKa values associated with
bacteria (Verma and Kuila 2019). Biogenic precipitates, the respective functional groups (Hasan et al. 2009; Liu
such as iron and sulfide precipitates, have been identified as et al. 2017). For example, Pseudomonas fluorescens 4F39
potentially suitable alternatives to traditional techniques for can remove Ni from wastewater via an ion exchange mech-
treating HM-contaminated wastewater (Jhariya et al. 2024). anism (López et al. 2000). Micrococcus luteus and Pseu-
Moreover, certain heterogeneous compounds located within domonas pseudoalcaligenes adsorbed high concentrations
or exterior to cell walls can also effectively accumulate HM of Pb and Cu at pH 6 (Leung et al. 2000). Streptomyces
ions. This phenomenon contributes to the enhanced survival rimosus performs ion exchange of ­Na+ from the functional
of microorganisms in challenging environmental conditions. group of the cell wall with silver ions (Bakhti et al. 2008).
Extensive research involving spectroscopic and chemical Chergui et al. (2007) performed a series of experiments and
modifications has unveiled that cellular functional groups, discovered that the ion exchange mechanism was involved
including hydroxyl, carboxyl, sulfate, sulfhydryl (thiol), in the removal of Cr(VI), Cu(II), and Zn(II) by Streptomyces
thioether, phosphate, phosphonate, phosphodiester, amino, rimosus.
 International Journal of Environmental Science and Technology

Biotransformation 2007). Many studies have shown that bacteria can convert
As into gaseous arsine ­(AsH3), selenium into volatile dime-
Biotransformation is the process through which certain thyl selenide ­(C2H6Se), and Pb into decomposable dimethyl
bacterial species can alter the chemical form and toxicity lead ­(C6H16Pb) in polluted aqueous solutions. However, each
of HM contaminants in the environment. Bacteria capable metal conversion via methylation follows unique pathways,
of biotransformation possess unique metabolic capabilities differs between bacterial species, and involves different
that enable them to interact with metals or metalloids and oxidation states of metal ions. Therefore, microorganism-
convert them into less toxic or less bioavailable forms. Bio- mediated ion state transformation is a valuable approach for
transformation of metals occurs primarily after uptake of the mitigating the detrimental effects of HMs in the environment
metal via different metal carriers, such as capsule biogen- (Ramasamy and Kamaludeen Banu 2007).
esis/assembly (CBA) or cation diffusion facilitator (CDF)
transporters (details of metal transporters are explained in
next Section "Bio-accumulation"). Additionally, some bacte- Bio‑accumulation
ria have the potential to catalyze redox reactions and convert
the redox state of free toxic forms into non-toxic forms using Bioaccumulation is the process by which bacterial cells
metalloids or metals as terminal electron acceptors (Ayang- internalize and accumulate metals, including non-metabolic
benro and Babalola 2017). For instance, Cr(VI) reduction to metals, by utilizing the same carrier pathway employed for
Cr(III) through the enzymatic action of microbes has been metabolically essential metals. In this process, metal ions
widely examined in HM bioremediation. A study by Das attached to active groups located on the exterior of the bac-
et al. (2014) found that Bacillus amyloliquefaciens biotrans- terial cell wall, followed by their entry into the cell through
formed Cr(VI) to Cr(III) at a 2.22 mg/L∙h Cr(VI) reduction channels, primary active transporters, and secondary carrier
rate. They explained that transformation to Cr(III) occurs proteins (Arisah et al. 2021). The transport pathway for met-
first, followed by surface immobilization and intracellular abolically crucial ions such as K, Na, and Mg facilitates the
accumulation (Das et al. 2014). In another study, a batch exchange of metals across cell membranes, enabling their
and continuous reactor using sulfate-reducing bacteria intracellular accumulation. Cation transport systems exhibit
(SRB) was utilized for the removal of HMs with a favorable affinity for metal ions with ionic radii and charges identical
metal dosing rate of 2.20 mg/L∙h for Pb(II), Ni(II), Fe(III), to those of essential metal ions (Sharma and Shukla 2021).
Zn(II), and Cd(II) and up to 4.29 mg/L∙h for Cu(II). In this Moreover, α-helical proteins belong to the major intrin-
batch bioreactor, 95% of all metals removal was observed, sic protein’s superfamily, involved in the transportation
whereas 99% of Cu(II) and 95.8% Zn(II) were removed from of As and Hg in a series of bacterial genera like Serratia,
the continuous reactor (Gopi Kiran et al. 2018). It has been Corynebacterium, Lactobacillus acidophilus, Streptomyces
reported that the biofilm formed by SRB can reduce and coelicolor, and Pseudomonas (Chellaiah 2018; Song et al.
precipitate Cr(VI) on the bacterial surface by increasing the 2021). Gram-negative bacteria have been discovered to pos-
sulfide concentration, resulting in a reduction of sulfate. This sess β-barrel proteins and porins that facilitate the transloca-
sulfide after sulfate reduction has the potential to bind toxic tion of metals. Secondary carrier proteins such as uniport-
metals, produce insoluble metal sulfides, and regulate the ers, symporters, and antiporters play crucial roles in HM
metal concentration, serving as a trapping material for HMs accumulation. After entering the cell, metal ions undergo
(Gopi Kiran et al. 2018). translocation, attachment, or embedding within cellular
Methylation is another mechanism of HM transformation. organelles, depending on the specific element and the bac-
Some bacteria are able to methylate metals, metalloids, and terial strain, effectively preventing them from reaching toxic
organometallics and convert them into volatile or degradable levels (Yamaguchi et al. 2007). Different microorganisms
forms. Methylation is a basic biochemical cycle of bacte- sequester HMs through various mechanisms. For example,
rial life that occurs predominantly in aquatic environments some microbes utilize cellular polyphosphates, sulfides,
(Nanda et al. 2019). Major pathways involved in intracellu- and cysteine-rich proteins to transform HM ions, whereas
lar methylation of metals and metalloids are S-adenosylme- others transform metals into insoluble metal precipitates.
thionine, N-methyltetrahydrofolate, and methylcobalamin. Some bacteria sequester metals by utilizing cysteine-rich
Bacteria methylate As via S-adenosylmethionine, whereas proteins like metallothionines, which contain cysteine resi-
mercury is methylated by the methylcobalamin pathway dues and act as a sink for excess metals (Yin et al. 2019).
(Aljerf and AlMasri 2018). Baralkiewicz et al. showed Cao et al. (2020) demonstrated the intracellular deposition
that when sediment containing H ­ g2+ was incubated under of Cd and Fe (as nanoparticles) by the efflux system of Halo-
aerobic conditions, methyl mercury was initially produced, monas sp. from its surrounding. Another study by Arisah
followed by a reduction in the concentration of methyl mer- et al. (2021) reported 1.24 mg/L of Cr deposition inside the
cury and a rapid increase in volatile ­Hg0 (Baralkiewicz et al. cell and extracellular sequestration (6.74 mg/L) by the strain
International Journal of Environmental Science and Technology

Pseudomonas aeruginosa RW9, accounting for ~ 85% of the such as carboxyl, amino, and hydroxyl groups (Jacob et al.
removal efficiency. 2018). Conversely, an attachment method is generally used
to immobilize cells on inorganic carrier materials (Das and
Adholeya 2015). Figure 3 shows the pros and cons of differ-
Immobilization of bacterial cells for HM ent bacterial immobilization techniques. Further exploration
remediation of immobilization techniques based on the metal removal
mechanisms of bacteria will forge ahead in conventional
Immobilization is one of the most efficacious bioengineering treatment methods.
technologies used to improve the performance and economy Another advantage of immobilization is that it signifi-
of many bioremediation processes. Bacterial removal of cantly enhances or alter specific biochemical and physiologi-
HMs offers advantages in terms of lower energy require- cal processes in bacteria. This enhancement results from the
ments, superior secondary waste stream quality, compatibil- tailored microenvironment provided by the immobilization
ity with existing systems, and environmental friendliness. matrix, which improves bacterial stability and efficiency.
However, treatment of wastewater using a free-cell system The key processes such as biofilm formation, and EPS pro-
has encountered two major drawbacks: poor functional sta- duction also enhanced, enabling bacteria to form a protec-
bility and difficulties in cell recovery and reuse (Bouabidi tive barrier that improve their survival and functionality in
et al. 2018). These drawbacks can be mitigated by immobi- the presence of toxic HMs (Wu et al. 2022). Immobilized
lizing the bacterial cells in a suitable support matrix. bacteria may exhibit shifts in metabolic pathways to adapt to
Immobilization techniques employ chemical or physical the confined environment, enhancing their ability to process
methods to attach or confine cells in a specific spatial range and detoxify metals effectively. Additionally, immobiliza-
to a suitable matrix, preventing random movement and facil- tion material often provides additional functional groups
itating recovery for reuse. Studies have shown that conven- or increases the availability of bacterial cell surface sites,
tional biological systems augmented with carrier materials thereby improving the capacity for HM adsorption (Mehro-
can enhance the removal of HMs from wastewater (Girijan tra et al. 2021).
and Kumar 2019). However, the efficiency of cell immobi-
lization remains low, owing to the lack of appropriate tech- Techniques for cell immobilization
niques for cell attachment based on bacterial function.
Various organic, inorganic, and composite materials have Entrapment
been used for immobilization of bacteria. Immobilization
on organic materials is primarily achieved through entrap- Entrapment is a popular cell immobilization technique in
ment and benefits from a wide range of reactive groups, which cells are encased in a three-dimensional complex

Fig. 3  Characteristics of dif-

ferent bacterial immobiliza-
tion techniques used in heavy
metal-contaminated wastewater
treatment
 International Journal of Environmental Science and Technology

structure of a polymer substrate. The final structure of the agents such as glutaraldehyde (GA) or aminosilane (Ber-
polymer substrate containing microbes shields the cells illo et al. 2021). For the spontaneous attachment of cells,
from leakage and external forces. Entrapping cells achieves a suitable adsorbent exhibits a strong affinity and causes
a higher density in the matrix than surface attachment tech- minimal damage. Van der Waal forces and ionic interactions
niques (Li et al. 2020, 2017). Carriers commonly used for are primarily responsible for the adhesion of cells to organic
entrapment are hydrogels such as alginate, agar, polyacryla- or inorganic materials (Lu et al. 2020). Additionally, attach-
mide, and carboxymethyl cellulose sodium salt. Generally, ment of cells through covalent bonding is another method
highly porous materials are used for entrapment, allowing for improving activity by stabilizing the active conforma-
substrates and products/metabolites to easily diffuse from tion. It allows covalent bonds to form between the active
the matrix. Entrapment of cells in materials, such as cel- face of the functional group of the matrix and the cells (Zur
lulosic compounds and polyvinyl alcohol (PVA), has been et al. 2016). Moreover, many multifunctional cross-linking
reported to be very effective, allowing maximum adsorp- agents are also used to attach cells to surfaces. However, this
tion efficiency, improved mechanical strength enhanced HM process involves the use of chemical agents for cross-linking
removal (Asgher and Bhatti 2010). that are cytotoxic in nature and can affect microbial activity.
The fabrication of cross-linked gels with the use of cross
Encapsulation linkers/chemicals could be a promising approach for effec-
tive cell immobilization with enhanced activity (Partovinia
Encapsulation is an advanced form of entrapment that and Rasekh 2018).
entails the confinement of cells within a semi-permeable
membrane. Unlike entrapment, encapsulated cells can freely Interlink between immobilization methods
move within a defined shell space (Páez-Vélez et al. 2019; and bacterial HM remediation mechanisms
Partovinia and Rasekh 2018). Encapsulation is a physico-
chemical method of entrapment, in which a capsule or shell Immobilization is the physical confinement of viable cells,
is formed around the cell. The capsule membrane is semi- and it offers many advantages over suspended cells, includ-
permeable, which permits the free movement of nutrients ing hydrodynamic properties, easy biomass dewatering, effi-
and metabolites while restricting the cell from passing cient product retrieval, and specific metabolic improvements
through the membrane. This technique offers a significant for contaminant removal (Khashei et al. 2018). Immobiliza-
benefit in that it eliminates the need for any chemical modi- tion of cells increases metabolic activity and reduces the
fication of the core material. Consequently, the activity of non-productive growth phase, resulting in a more efficient
the immobilized microorganisms remained unaltered (Páez- operation. It is well recognized that a high cell density of
Vélez et al. 2019). Factors such as cell selection, support confined cells improves the degradation of contaminants
material, and the process of capsule formation are critical along with the removal efficiencies of bioreactors (Medfu
variables for achieving better results using this technology Tarekegn et al. 2020).
(Sánchez et al. 2013). Table 2 enlists key literature clearly demonstrating the
enhanced bacterial efficiency of HM removal after immo-
Cell attachment bilization on a support matrix. The selection of a proper
support matrix can protect bacteria from shear forces and
The restricted diffusivity within gel beads employed in other external pressures such as pH, temperature, and self-
entrapment methodologies, coupled with their susceptibil- destruction. Additionally, the use of suitable immobilization
ity to shear forces and restricted mass transfer in encapsu- methods can increase the activity, viability, and productivity
lation techniques, impose limitations on their efficacy for of bacteria under harsh conditions (Velkova et al. 2018).
a wide range of applications (Lapponi et al. 2022). Con- Immobilization can be performed through various methods
sequently, physical and chemical adsorption methods for such as entrapment, adhesion, and covalent bonding to sup-
cell immobilization are considered more advantageous than port materials (Lu et al. 2020; Qin et al. 2020). The immo-
entrapment methods. Cell attachment involves the fixation of bilization material provides physical support to bacterial
microbial cells on the surface and within the support mate- cells, whereas the immobilization method determines how
rial, resulting in the formation of a biofilm facilitated by the the bacterial cells are attached to the material.
interplay of surface tension, static electricity, and adhesive For example, entrapment in hydrogel matrices like algi-
forces between the microbial cells and the support substrate nate creates a protective microenvironment that minimizes
(Kamitakahara et al. 2019, 2016). The immobilization of nutrient diffusion barriers while maximizing bacterial per-
cells via adhesion to a support material can be accomplished formance. Adsorption-based methods using activated car-
through natural means or artificially by employing linking bon or biochar improve the system's ability to tolerate and
agents, including metal oxides, as well as covalent bonding remediate high concentrations of toxic metals. The choice
International Journal of Environmental Science and Technology

Table 2  Potential of heavy metal removal using immobilized and non-immobilized bacterial strains in bioremediation of wastewater
S.no Bacteria Immobilizing Immobilizing HM contami- Initial conc Experimental Percentage References
material approach nants conditions removal

1. Escherichia Suspended Cr (III) 70 mg/L 37 °C, 150 rpm 61.4% Wang et al.
coli M-BL21 cells (2021)
Magnetic pel- Attachment Cr (III) 140 mg/L 37 °C, 150 rpm 91.29% Wang et al.
lets (2021)
2. Pseudomonas Suspended Cd (II) ~ 10 mg/L 30.48 °C, 82.30%, Su et al. (2019,
sp. H117 cells Mn (II) ~ 50 mg/L 150 rpm 60.71% 2020)
Modified poly- Attachment Cd (II) 10 mg/L 37 °C, 98.78% Su et al. (2020)
vinyl alco- Mn (II) 50 mg/L 150 rpm, &90.98%
hol (PVA) time is not
sponge with clear
iron oxide
3. Paenibacillus Suspended Pb (II) 200 mg/L 25 °C, 99.1% Dawwam et al.
dendriti- cells 150 rpm, (2023)
formis 17OS 48 h
Polyethersul- Entrapment Pb (II) 200 mg/L 25 °C, 98% Dawwam et al.
fone 150 rpm, 2 h (2023)
4. Acinetobacter Suspended As (III) 50 mg/L 24 h 30.70 by K1 Zhao et al.
gandensis cells & 43.40% (2023)
(K1) & Delf- by K7
tiatsuruhat-
ensis (K7)
Sodium algi- Attachment As (III) 50 mg/L 180 min 61.52% Zhao et al.
nate & PVA (2023)
5. Serratia Suspended Pb (II), Cd (II), 1.64 mg/L, 30 °C, 94.4, 91.5, 85, Moula et al.
rubidaea cells Cu (II), & Zn 1.03 mg/L, 120 rpm, & 66.5% (2021)
NCTC12971 (II) 1.04 mg/L, 48 h
1.12 mg/L
Ca-alginate Entrapment Pb (II), Cd (II), 1.64 mg/L, 30 °C, 92.07, 98.05, Moula et al.
beads Cu (II), & Zn 1.03 mg/L, 120 rpm, 95.57, & (2023)
(II) 1.04 mg/L, 48 h 88.39%
1.12 mg/L
6. Lysinibacillus Suspended Au (III) 60 mg/L 30 °C, 52% Páez-Vélez et al.
sphaericus cells 130 rpm, 2 h (2019)
CBAM5
Alginate Encapsulated Au (III) 60 mg/L 30 °C, 100% Páez-Vélez et al.
spheres 130 rpm, 2 h (2019)
7. Bacillus Suspended Pb (II) 200 mg/L 12 h 38% Wen et al.
licheniformis cells (2018)
Magnetic Entrapment Pb (II) 200 mg/L 12 h 98% Wen et al.
PVA) beads (2018)
with sodium
alginate
8. Leclercia ade- Suspended Pb (II) 200 mg/L 30 °C, 24 h 40% Teng et al.
carboxylata cells (2020)
Biochar nZVI Entrapment Pb (II) 200 mg/L 30 °C, 24 h 93% Teng et al.
bio-beads (2020)

of immobilization material and method are entirely depend- methods enhance bacterial heavy metal remediation mecha-
ent on the specific application and bacterial mechanisms in nisms. Proper alignment of immobilization strategies with
the treatment process (Khashei et al. 2018). These inter- bacterial processes ensures high efficiency, scalability,
linked factors collectively demonstrate how immobilization
 International Journal of Environmental Science and Technology

and adaptability for real-world wastewater treatment reducing long-term viability (Lapponi et al. 2022). Although
applications. adhesion is the most widely used, simple, and cost-effective
method, it has certain drawbacks. For instance, weak bond-
Factors affecting the HMs removal using ing between bacteria and the support material results in
immobilized bacteria bacterial loss during treatment, thereby reducing the overall
process stability. According to previous reports, adhesion of
While immobilization in material like hydrogels provides some microbes increases in the exponential growth phase
protection against toxic contaminants, it can hinder nutrient owing to heightened cell wall hydrophobicity. Therefore,
and oxygen transfer, slowing bacterial growth. For example, outer layer become the preferred adhesion site for metaboli-
calcium alginate (CA) beads were found to restrict pollutant cally active bacteria (Krasowska et al. 2014; Van Loosdrecht
and nutrient transport, a limitation resolved by incorporat- et al. 1990). However, to address the limitations of adhe-
ing straw to create straw-alginate beads (Xue et al. 2019). sion, covalent bonding has been utilized as an immobili-
Immobilization matrices serve dual roles as carriers and zation technique. This method provides bacteria with high
adsorbents, enhancing heavy metal uptake. For instance, resistance and reusability to withstand harsh environmental
biochar-enhanced CA beads achieved high Cd(II) uptake conditions and maintain their activity, making them effective
(~ 158.77 mg/g) due to combined biosorption and bioaccu- in wastewater treatment (Mehrotra et al. 2021). Although
mulation, tolerating higher metal concentrations compared this method improves the stability of bacteria, it also reduces
to free cells (Huang et al. 2020). bioactivity during operation (Qin et al. 2020). In conclu-
High concentrations of HMs or other co-contaminants sion, selecting immobilization methods based on the specific
can cause toxicity and damage bacterial proteins and nucleic mechanisms used by bacteria for HM remediation, such as
acid, reducing the removal efficiency. Selection of protec- adsorption, bioaccumulation, and transformation, can lead
tive immobilization matrix shields bacteria from such toxic to more effective and efficient immobilization performance
effects. For instance, immobilized Pseudomonas cells in and HM removal capacity.
PVA-sodium alginate (SA) and SA-kaolin matrices sig-
nificantly improved denitrification efficiency under Cr(VI) Studies related to enhanced efficiency
stress, with removal of up to 100%, compared to just 4% for through immobilization techniques
free cells (Yu et al. 2020). Similarly, CA-immobilized bac-
teria tolerated phenol concentration up to 800 mg/L, double It is challenging to determine how immobilization methods
the lethal dose for free cells (Namane et al. 2020). affect bacterial physiology because there are many differ-
pH and temperature critically influence biosorption and ences between bacteria in terms of their taxonomy, genet-
bioaccumulation by altering bacterial surface properties ics, and functions. The use of various carriers, bacterial
and pollutant interactions. Immobilized cells often exhibit species, immobilization techniques, and culture conditions
a broader pH tolerance as the carrier material shields them can all result in different outcomes, making it difficult to
from adverse conditions. For example, maximum Cr(VI) draw definitive conclusions. Additionally, the impact of
uptake by baker's yeast immobilized in CA occurred at cell confinement on the functioning of microbes remains
pH 3.5, when examined from pH 1.5–7.5 (Mahmoud and poorly understood. Ellwood et al. (1982) proposed that
Mohamed 2017). Similarly, pH affects enzyme activity and augmenting the growth rate of surface-associated bacteria
bacterial growth rate, but with immobilization the enzymatic is related to an elevation in the nearby proton concentration
activity at broader pH can be saved (Ruan et al. 2018). between the solid surface and the bacterial cell, thereby
fosters bacterial growth. Al-Garni et al. (2010) reported
Comparison between immobilization methods an increased growth of Pseudomonas aeruginosa attached
to glass. The surface attachment of Pseudomonas aerugi-
General methods employed for immobilization include adhe- nosa helped create an extracellular slime layer around the
sion on surfaces, cross-linking of cells, covalent bonding, surface, resulting in an increased negative charge, which
entrapment, and encapsulation. Each method has unique allowed more HMs to bind (Al-Garni et al. 2010). Pic-
advantages and disadvantages that potentially influence the cirillo et al. (2013) performed immobilization of bacteria
functioning of bacteria (Ismail et al. 2015). Techniques like (Pseudomonas fluorescens (S3X), Microbacterium oxy-
entrapment in gel beads or cellulosic fibers can enhance bac- dans (EC29) and Cupriavidus sp. (1C2)) onto the surface
terial activity. However, retaining cells in the enclosed space of fish-derived hydroxyapatite (HAp) to remove Zn (II)
decreases the exposure time to contaminants, which may and Cd (II) at relatively low and high concentrations. Their
lead to reduced productivity. Methods such as encapsulation results showed that combined systems (HAp + bacteria)
offer protection from environmental stress while limiting were effective and removed three times more Zn and Cd
the diffusion of nutrients and oxygen to bacteria, thereby compared to unmodified HAp. The enhanced efficiency of
International Journal of Environmental Science and Technology

metal removal observed when bacteria were immobilized Prospects, challenges, and opportunities
on the HAp surface can be attributed to the increased num-
ber of functional sites for metallic ion chelation, thereby Bacteria exhibit remarkable potential in the remediation of
facilitating the sorption of HMs (Piccirillo et al. 2013). heavy metals (HMs) through mechanisms such as adsorp-
Huang et al. (2020) demonstrated that cells immobilized tion, precipitation, and transformation, which convert
on the rice straw-derived biochar adsorbed more Cd(II) toxic HMs into less harmful forms (Das and Adholeya
(158.77 mg/g) than free cell suspension. They immobi- 2015). These natural processes provide an eco-friendly
lized Cd-resistant Bacillus cereus RC-1 on different car- and sustainable alternative to conventional chemical treat-
riers using different techniques under varying conditions ments. However, direct use of bacteria in HM remediation
and observed better removal efficiency (50–80% removal) faces significant challenges. Bacterial performance can be
by bacteria immobilized on biochar when the initial Cd(II) inconsistent under varying environmental conditions, and
concentration was less than 180 mg/L (Huang et al. 2020). high concentrations of metal ions often inhibit bacterial
Li et al. (2017) explained that the embedding method growth, reducing their effectiveness (Berillo et al. 2021).
of immobilizing sulfate reducing bacteria into PVA and To overcome these limitations, immobilization tech-
reticular SA beads increased the surface area for adsorp- niques have emerged as a promising approach. Immo-
tion and achieved 95.6, 100, 76.3, and 91.2% removal effi- bilization enhances the functional stability of bacteria,
ciencies of Zn, Pb, Cu, and Cd, respectively. They also improves their resistance to harsh environmental condi-
stated that this method of immobilization method protects tions, and provides a safe, nourishing environment that
cells from the toxicity of metals and permits the transmis- allows them to thrive and function optimally. Various
sion of matter (Li et al. 2017). The activity of embedded immobilization methods have been developed to enhance
cells also depends on substrate and oxygen diffusion. It bacterial attachment, enabling efficient HM removal.
has also been reported that the ion exchange in Ca-alginate Additionally, immobilization can be paired with geneti-
hydrogels is a pivotal factor in determining nutrient diffu- cally modified bacteria (GMBs), offering an advanced
sion, thus affecting bacterial growth and metabolism (Gol- strategy to further improve bioremediation potential. The
mohamadi and Wilkinson 2013). Furthermore, Xiao et al. greater risk of release of GMBs into natural environment
(2022) demonstrated that embedding viable cells is a very can also mitigate by application of immobilization. Addi-
feasible strategy for supporting the synthesis of cellulose tionally, using immobilization GMBs can be modified to
with unique properties. They embedded Synechococcus withstand extreme conditions, such as high temperatures,
elongatus cells into the biopolymer bacterial cellulose low oxygen levels, and toxic environments, allowing for
and found excellent copper removal efficiency from an more efficient and targeted HM remediation (Saravanan
aqueous solution compared to pure bacterial cellulose or et al. 2022; García-García et al. 2016).
other materials (Xiao et al. 2022). In macroporous cryo- Despite these advancements, several challenges impede
gels, bacteria can either be encapsulated within the pore large-scale implementation. Practical application of immo-
walls, adsorb on the cryogel surfaces, or covalently bind bilized bacterial systems is hindered by limited research,
to the polymer walls. A previous study showed that bac- complex operations, and the need for cost-effective and
teria are immobilized in cryogels via crosslinking using durable materials. Selecting appropriate support materi-
glutaraldehyde (GA). However, the small GA molecule als that enhance bacterial activity while being cost-effec-
enters into the cell and destroys cellular metabolism, thus tive and long-lasting is crucial. Moreover, the intricate
adversely affecting the viability and growth of the bac- relationship between immobilization methods, bacterial
terial cells. However, modifications to the crosslinking stability, and HM removal mechanisms requires further
method and concentration of GA provided satisfactory exploration to optimize these systems. Another critical
mechanical properties and proper growth and metabolism challenge is the environmental implications of immobili-
of the bacteria (Berillo et al. 2021). Moreover, a study on zation matrices. Over time, these materials may degrade,
the immobilization of Bacillus sp. KSB7 on peanut shell leading to secondary pollution through leaching of harm-
biochar prepared at 400 °C improved bacterial coloniza- ful substances or heavy metals. Additionally, the safe dis-
tion and also the growth of other functional bacteria in posal or recycling of immobilized materials saturated with
the soil (Song et al. 2022). Therefore, a proper study of heavy metals remains an unresolved issue.
immobilization techniques on support material according Addressing these challenges presents significant oppor-
to the HM removal mechanism of bacteria could stimulate tunities. The development of biodegradable, non-toxic,
the active site and enhance the removal efficiency. In con- and physically stable immobilization matrices can miti-
clusion, microbial immobilization systems can be made gate secondary pollution risks and ensure safe end-of-
more stable, robust, orderly, and industrious by selecting life management. Integration of genetic engineering with
appropriate immobilization materials and methods.
 International Journal of Environmental Science and Technology

immobilization techniques could further enhance bacte- Acknowledgements This study was supported by the JSPS KAKENHI
rial efficiency while controlling the release of modified Grant Number JP22K19860, JP19K22918.
strains into the environment. This dual approach could Authors contribution Upasana Jhariya: Conceptualization, Writing-
address both safety concerns and bioremediation effective- original draft. Mei-Fang Chien: Writing-review & Editing. Masaki
ness. Furthermore, immobilized bacterial systems offer the Umetsu: Writing-review & Editing. Masanobu Kamitakahara: Super-
potential for resource recovery, enabling the extraction of vision, Conceptualization, Writing- reviewing & editing.
valuable or precious metals from treated materials. This Data availability No primary data were used in this review article,
aligns with sustainability goals while improving the eco- however, all secondary datasets used are publicly available at Scopus.
nomic viability of bioremediation.
Future research must focus on interdisciplinary Declarations
approaches to design innovative carriers that are cost-effec-
Conflict of interest The authors declare that they have no known com-
tive, durable, and biologically compatible. Additionally, peting financial interests or personal relationships that could have ap-
efforts should be directed toward understanding the environ- peared to influence the work reported in this paper.
mental fate of immobilized materials, ensuring their appli-
cations do not inadvertently harm ecosystems. Combining Open Access This article is licensed under a Creative Commons Attri-
bution 4.0 International License, which permits use, sharing, adapta-
genetic engineering with immobilization holds promise for tion, distribution and reproduction in any medium or format, as long
developing scalable, efficient, and environmentally safe HM as you give appropriate credit to the original author(s) and the source,
remediation strategies. By addressing these gaps, the field provide a link to the Creative Commons licence, and indicate if changes
can advance toward sustainable solutions that balance eco- were made. The images or other third party material in this article are
included in the article’s Creative Commons licence, unless indicated
logical preservation with technological innovation. otherwise in a credit line to the material. If material is not included in
the article’s Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
Conclusion need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

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