Microbial Assisted Multifaceted Amelioration Processes of Heavy-Metal Remediation: A Clean Perspective Toward Sustainable and Greener Future

Critical Reviews in Biotechnology
ISSN: (Print) (Online) Journal homepage: www.tandfonline.com/journals/ibty20
Microbial assisted multifaceted amelioration

processes of heavy-metal remediation: a clean
perspective toward sustainable and greener future
Komal Agrawal, Tannu Ruhil, Vijai Kumar Gupta & Pradeep Verma
To cite this article: Komal Agrawal, Tannu Ruhil, Vijai Kumar Gupta & Pradeep Verma (2024)
Microbial assisted multifaceted amelioration processes of heavy-metal remediation: a clean
perspective toward sustainable and greener future, Critical Reviews in Biotechnology, 44:3,
429-447, DOI: 10.1080/07388551.2023.2170862
To link to this article: https://doi.org/10.1080/07388551.2023.2170862
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CRITICAL REVIEWS IN BIOTECHNOLOGY
2024, VOL. 44, NO. 3, 429–447
https://doi.org/10.1080/07388551.2023.2170862
REVIEW ARTICLE
Microbial assisted multifaceted amelioration processes of heavy-metal

remediation: a clean perspective toward sustainable and greener future
Komal Agrawala,b, Tannu Ruhila, Vijai Kumar Guptac,d, and Pradeep Vermaa
a
Bioprocess and Bioenergy Laboratory, Department of Microbiology, Central University of Rajasthan, Ajmer, India; bDepartment of
Microbiology, School of Bio Engineering and Biosciences, Lovely Professional University, Phagwara, India; cCenter for Safe and
Improved Food, SRUC, Edinburgh, UK; dBiorefining and Advanced Materials Research Center, SRUC, Edinburgh, UK
ABSTRACT ARTICLE HISTORY

Rapidly increasing heavy metal waste has adversely affected the environment and the Earth’s Received 13 October 2021
health. The lack of appropriate remediation technologies has worsened the issue globally, espe- Revised 18 December 2022
cially in developing countries. Heavy-metals contaminants have severely impacted the environ- Accepted 3 January 2023
ment and led to devastating conditions owing to their abundance and reactivity. As they are
KEYWORDS
nondegradable, the potential risk increases even at a low concentration. However, heavy-metal Heavy metals; pollution;
remediation has increased with the up-gradation of technologies and integration of new microbial remediation;
approaches. Also, of all the treatment methodologies, microbial-assisted multifaceted approach sustainability; nanotechnol-
for ameliorating heavy metals is a promising strategy for propagating the idea of a green and ogy; LCA; TEA
sustainable environment with minimal waste aggregation. Microbial remediation combined with
different biotechniques could aid in unraveling new methods for eradicating heavy metals. Thus,
the present review focuses on various microbial remediation approaches and their affecting fac-
tors, enabling recapitulation of the interplay between heavy-metals ions and microorganisms.
Additionally, heavy-metals remediation mechanisms adapted by microorganisms, the role of gen-
etically modified (GM) microorganisms, life cycle assessment (LCA), techno-economic assessment
(TEA) limitations, and prospects of microbial-assisted amelioration of heavy-metals have been ela-
borated in the current review with focus toward “sustainable and greener future.”
GRAPHICAL ABSTRACT
Introduction mismanagement has resulted in huge garbage

Heavy metal-generated pollution severely hampers mounds and is emerging as a challenge globally [4].
and limits environmental productivity by interfering Rapid industrialization, urbanization, and population
with various biogeochemical cycles at different have led to the generation of waste dumping sites,
levels of the food chain [1]. Over time, an increase which initially was a short-term solution that ultim-
in heavy metal generation has taken a toll on ately made the area unfit for further human use due
environment and human health [2,3]. The waste to severe contamination [5].
CONTACT Pradeep Verma pradeepverma@curaj.ac.in Bioprocess and Bioenergy Laboratory, Department of Microbiology, Central University of
Rajasthan, Ajmer, Rajasthan, 305817, India
Supplemental data for this article is available online at https://doi.org/10.1080/07388551.2023.2170862.
ß 2023 Informa UK Limited, trading as Taylor & Francis Group
430 K. AGRAWAL ET AL.
Metals are essential components for plants and ani- heavy-metals contamination for a greener and more
mals [6], however, at higher concentrations, it is fatal sustainable environment (Figure 1).
and can cause diseases in humans and toxicity in plants Thus, this review highlights how various heavy-metal
[7]. Thus, the public outcry has led the countries to generation sources are a nuisance and a threat to the
address the problem of these dumpsites, thus allowing ecosystem and life forms. It also discusses heavy-metal
scientific communities to explore new and biobased remediation mechanisms and the effect of various fac-
alternatives to bioremediation. Various physical and tors on the microbial-assisted amelioration processes of
chemical methods have been used in metal removal. heavy metals. Additionally, it highlights the roles of
These methods encompass membrane separation, genetically modified (GM) microorganisms, bio-nano-
adsorption, ion exchange, and reverse osmosis. They technology, life cycle assessment (LCA), and techno-
are effective against a wide range of contaminants. Still, economic assessment (TEA) in the removal of heavy
limitations, such as high costs, secondary pollutants for- metals and how they can contribute to future research.
mation, and a huge amount of chemical and energy Later the advantages, current limitations, and prospects
consumption have restricted their utility in diverse of microbial remediation technology have been elabo-
rated for a better understanding of the role of micro-
areas [8,9]. Thus, the drawbacks have led to the hunt
bial-assisted heavy-metals amelioration processes,
for more effective, economical, and greener alternatives
which is a clean perspective toward a sustainable and
for decontaminating heavy-metals-contaminated sites.
greener future.
Bioremediation is gaining attention to entail using: bac-
teria, fungi, algae, and plants for environmental clean-
up [10,11] (Supplementary Figure 2). Source, types, and major components of
Microorganisms employ various mechanisms for heavy-metals
their defense against heavy metals, such as biosorption,
The various sources, types, and major components
bioaccumulation, biovolatization, etc. [12]. They are responsible for heavy-metals contamination are dis-
competent to combat these pollutants and must be cussed as follows (Supplementary Figure 1 and
biotechnologically explored to alleviate heavy-metals Supplementary Table 1).
contamination [13]. Also, genetically modified (GM)
microorganisms can be used for enhanced microbial
remediation approaches. The shift to microbial-assisted Municipal waste (MSW)
remediation is the need of the hour and thus requires The US, China, and India are the top producers of MSW
maximal exploration for heavy-metals remediation. [14], accounting for 11.65, 15.55, and 11.95% of global
However, microbial remediation technology is still in its MSW, respectively [15]. Wang et al. [16] investigated
developmental stages and major lags are required to the properties of biochar and associated environmental
be addressed through associations in scientific com- risks of heavy metals, by comparing the residual con-
munities. Also, laboratory and pilot-scale studies will be tents from the co-pyrolysis of sewage sludge with vari-
promoted to commercialize the method to alleviate ous organic fractions of municipal waste (OFMSW) at
Figure 1. Conventional and novel approaches for heavy metals remediation with underlying mechanisms.
CRITICAL REVIEWS IN BIOTECHNOLOGY 431
550 C and pyrolysis at temperatures ranging from 350 critical role of microplastics in serving as vectors for
to 750 C. It was reported that the OFMSW exhibited: toxic metals. Except for Cd, pollution indices, such as
good synergy in co-pyrolysis with sewage sludge, the potential contamination index (PCI), hazard quo-
improved the bent biochar properties, and reduced the tient (HQ), and modified hazard quotient (mHQ) indi-
bioavailability of the toxic heavy metals in the biochar. cated low severity contamination of beach and lagoon
The temperature range of 350 and 750, 550 C was bet- MPs by heavy metals. However, considering the long-
ter as it consolidated heavy metal well and prevented term accumulation of sorbed metals, their potential tox-
the transformation of Cd to the gaseous phase. icity to marine biota may be considerable
Farzadkia et al. [18] estimated the release of heavy
metals from cigarette butts in different environmental
Industrial waste (ISW) and agricultural
conditions and scenarios. The samples were taken
by-products (AB)
through artificial smoking from ten (10) high-consump-
tion brands available in the Iranian market. Their sam- Metallurgy, non-metallurgy, and food processing indus-
ples were taken from urban areas and analyzed for tries are the major ISWs responsible for heavy-metals
heavy metal pollution. It was observed that the concen- pollution [19]. Heavy metals-bearing industries are the
trations of Pb, Cd, Cr, Zn, Cu, and Ni were: 1.71, 0.36, most dangerous among other chemical industries [20].
1.59, 24.61, 12.83, and 2.66 mg/g. The continuous pres- Depending on public health criteria, As, Pb, and Hg are
ence of cigarette butts in the environment has led to ranked in the top three in the agency’s priority list for
the enhanced release of heavy metals (9.7%) and rain- toxic substances and disease registry [21]. Their source
fall further enhanced its leaching to 17.7%. Also, the tracing limits the release and impact studies of these
total mean concentration of studied metals was 32.67– metals. These pollutants are responsible for causing
51.81 lg/g under rainy and non-rainy conditions. Thus, adverse environmental effects and cause a range of
the littering of cigarette butts leads to the release of human diseases even at low concentrations [22].
heavy metals and thus it becomes even more necessary On the other hand, waste generated from the culti-
to reduce its density in urban areas by improving the vation and processing of agricultural products is termed
urban cleaning system. as agricultural waste. In contrast, aquaculture waste
The pervasive existence of microplastics and toxic results from aquaculture feeds [23] and comprises
metals is raising environmental and health concerns. A metabolic waste from which a proportion may solidify
study aimed to establish baseline data on the elemental and result in waste generation. Agricultural by-products
occurrence and distribution of potentially toxic and (AB) have a major portion of degradable waste like ani-
geochemical metals/metalloids in microplastics 1–5 mm mal and food processing waste, but fertilizers and pesti-
and mesoplastics (>5 mm–1 cm) along designated cides consumed in agriculture account for a toxic
coastlines of the Gulf of Guinea (Nigeria) in addition to proportion that contributes significantly to heavy-met-
enabling more comprehensive ecotoxicological risk als pollution [24]. Soil acts as a reservoir for these and
assessment. The concentrations of twenty-six metals other anthropogenically generated heavy-metals pollu-
associated with beach MPs, pristine, and lagoon plastics tants [25]. Also, as the heavy metals are non-degradable
were determined after extraction in 10% nitric acid and [26], increasing metal concentration is a danger to plant
analysis using inductively coupled plasma-optical emis- growth, soil microflora, humans, leading to danger to
sion spectroscopy (ICPOES). The distribution of MPs was food safety [27].
variable, with 3680 particles identified along the drift In the study by Kachenko and Singh [28], it was
and high waterlines across designated shoreline loca- stated that exposure to cadmium (Cd), lead (Pb), zinc
tions. The beach MPs were dominated by polyethylene (Zn), and copper (Cu) has been a source of risk to
(PE), polypropylene (PP), and polystyrene (PS), whereas humans by the consumption of contaminated vege-
lagoon-sourced plastics were characterized by poly- table crops. The study investigated the contamination
ethylene terephthalate (PET), polystyrene (PS), and poly- in soil and vegetables across various sampling sites in
urethane (PUR). Metal concentration was higher when Australia that were a mix of commercial and residential
associated with foam plastic (PS, PUR, PEVA) than hard vegetable growing areas. It was observed that the level
plastic (PE, PP, PET) samples. The results showed that all of metal contamination was high in areas near smelters
samples had slightly elevated Al, Fe, Mn, and Zn con- (Boolaroo and Port Kembla) but the concentration
centrations, suggesting potential sorption interactions decreased with depth. The Cd, Pb, and Zn vegetable
and plastic additive influences. Notably, foam MPs had contaminated by Cd was high at Boolaroo and Cu at
a stronger affinity for metals. This study emphasizes the Port Kembla. It was also observed that at Boolaroo the
samples analyzed had higher concentration of Cd and Heavy-metals accumulation

Pb in vegetables as per the standards set by the
Heavy metals are nondegradable with a high specific
Australian Food Standards maximum level (ML)
gravity of 5 g/cm3 [35,36]. Natural sources, such as vol-
(0.01 mg kg1 fresh weight) and 63% of the samples
canic eruptions, metal-rocks weathering [37], soil ero-
analyzed exceeded the limit set by International Food
sion, and metal evaporation from water resources to
Standard Guidelines set by the Commission of the soil and groundwater [38], along with anthropogenic
European Communities and the Codex Alimentarius activities, geogenic, pharmaceutical, and domestic sour-
Commission. However, in Cowra, the levels of Cd and ces [39], have contributed toward heavy-metals con-
Pb were lower than the Australian and international tamination. The World Health Organization (WHO)
food standards guideline values. report 2020 stated that: As, Cd, Pb, and Hg are among
ten (10) chemicals causing public health concerns.
Clinical waste (CW) Heavy metals and their compounds are a concern
because of their: high persistence, non-degradability,
During the COVID-19 outbreak, a press release of the and easy absorption in air, water, and soil. They com-
State Council’s Joint Prevention and Control Mechanism pete with other essential ions in soil and accumulate in
reported that China decreased MSW generation by 30% plants, becoming toxic to plants, animals, and humans
[29] and consequently increased medical waste by via the food chain [40]. Thus, the various impact of
370% [30]. The waste produced from medical, dental, heavy-metals contamination is discussed as follows:
pharmaceutical, or other medical activity accounts for
CW [21]. Open dumping is preferred in developing
Impacts of heavy metals on environmental health
countries like Yemen, Al-Geria, South Africa, and Egypt.
Insufficient financial investment, lack of trained staff in Heavy metals have severely impaired the environment
WM, absence of suitable guidelines/legislation, lack of through different types of pollution and failed WM
awareness, and suitable disposal and treatment meth- which significantly aids in its rise. Heavy metals linger
ods can be the reasons and challenges behind the pref- in waste dump sites over a long period and eventually
erence for open dumping sites [31]. Additionally, are leeched down in soil, leading to underground water
wastes near beaches are prone to be carried by wind contamination [41]. The soil near these dumps becomes
and tides from where it reaches the vegetation, accu- contaminated, negatively affecting agricultural activities
mulating in aquatic organisms, and producing deleteri- [42]. Heavy metals within soil compete with essential
ous results for humans on consumption. The burning of macro and micronutrients leading to stress in plants
these wastes in public places is the commonly used and showing multiple toxicity symptoms due to heavy-
approach utilized to treat such waste and is reported to metals accumulation or essential nutrient deficiency
[43]. Heavy metals accumulated by plants become a
cause respiratory infections through air transmission
part of their biomass and will subsequently transfer to
[17]. Also, developed countries like the USA rely on
higher-level organisms via the food chain [44], spread-
treating their CW by microwave plasma sterilization and
ing their toxicity at each level. Wastewater discharged
incineration before disposal [32]. Waste generation
from industries, manufacturing activities, and natural
needs to be minimized at each source level and good
sources (Pollution, National Geographic) is a major
management practices like segregation and sorting can
threat to water sources but metals leaching down from
be the possible solution for CW mismanagement [33].
waste sites also significantly contribute to groundwater
Adama et al. [34] studied the concentration of heavy
pollution [45]. Lack of monitoring and control over dif-
metals, such as Hg, Pb, Cd, Cr, and Ag from incinerator ferent sectors and industries has worsened the condi-
bottom ash, soils (100 m) from incinerator bottom ash tion. The contaminated water is deleterious to humans
dump sites, and ash samples along with soil samples at and aquatic life [46].
various depths from the incinerator. It was observed
that: Zn, Pb, Cr, and Cd were present at: 16417.69,
143.80, 99.30, and 7.54 mg/kg which were beyond the Impact of heavy metals on humans
permissible limit for disposal in landfill. Thus, it Heavy-metals contamination in the air near the dump-
becomes crucial that healthcare waste managers are sites poses serious threats to mankind [47] and is evi-
educated and trained regarding the implications of the dent from increased cases of diseases in people
improper management of incinerator bottom ash and residing near waste dumpsites [48]. Heavy metals also
also regulate hospital waste incinerator sites. negatively affect organisms’ molecular makeup, leading
to different forms of cancer and DNA alterations [49]. Remediation potential can vary among bacteria,
Heavy metal’s wide applications in various sectors like Gram-positive are found to be better in terms of accu-
agricultural, domestic, and industrial sectors have also mulation potential [57], and remediation efficiency can
increased their exposure to humans [50]. Heavy-metals also be altered by modification in inorganic nutrients,
toxicity depends on three (3) major factors: dose, route, bulking agents, biosurfactants, and other factors [58].
and duration of exposure [51]. Awasthi et al. [52] Bizily et al. [59] mentioned that mercury-resistant bac-
reported municipal waste-related diseases in humans teria converted toxic methyl mercury to less toxic form
and the major routes of exposure to heavy metals were Hg(II) by organomercurial lyase. Bacillus sp. and
ingestion, inhalation, and absorption. Paenibacillus sp. isolated from Cd and Ni-contaminated
soil showed functional groups, such as –OH, –NH2, and
–COO on bacterial surfaces, resulting in metal immobili-
Microbial-assisted metal remediation of heavy zations and subsequent remediation [60]. Other nega-
metals tively charged functional groups employed by
microorganisms for cationic metal species immobiliza-
Indigenous microflora is sensitive to metals, and those
tion include phosphoryl, carboxyl, thioether, hydroxyl,
microorganisms that can tolerate high concentrations
alcohol, sulfhydryl [61]. Desulfovibrio desulfuricans, a sul-
are potential candidates for remediation [53]. The
fate-reducing bacterium, effectively remediates metal
microorganisms have been successfully exploited for
ions Cd, Ni, and Cr through a precipitation mechanism
remediation applications and are discussed in
in the presence of FeSO4 [62] (Figure 2(a)). Along with
Supplementary Table 2.
living biomass, dead biomass also has been explored
for the bioaccumulation and biosorption of heavy met-
Bacterial-mediated remediation als. Velasquez and Dussan [63] studied the tolerance of
various Colombian Bacillus sphaericus native strains to
They can be effectively administered as a greener alter- As, Hg, Co, Fe, and Cr. It was reported that both the liv-
native for metal remediation due to associated advan- ing and dead cells of B. sphaericus OT4b31 showed 32
tages, such as small size, fast growth rate, simple and 45% biosorption, respectively. It was stated that, in
cultivation, competitiveness, and high metal concentra- the case of dead cells, the biosorption was due to the
tion tolerance [12,53]. Metals are directly and indirectly lack of active metabolism and adjustment in pH. Also,
involved in various metabolic processes of bacteria [54]. the S-layer protein could be responsible for metal
They eventually develop tolerance toward heavy met- entrapment in the case of both living and dead cells.
als, but higher metal concentrations initially result in Since both living and dead cells have biosorption cap-
molecular alterations inhibiting: a few enzyme activities, acity, the dead can be a better alternative as it can be
modifications in substrate degradation, and chemical stored in powdered form and does not require add-
nutrient cycling [55,56]. itional nutritional requirements as in the case of living
Figure 2. A typical bacterial cell representing the mechanisms utilized by (a) bacteria, (b) fungi, and (c) algae. (d) Represents
phycoremediation of contaminated effluents for metal recovery and algal biomass future utilization for biorefinery approaches
microbe for effective metal remediation.
cells. Thus, alongside living cells, dead bacterial biomass transforming or removing armful contaminants [73].
can also be an effective alternative for the remediation Algae can even grow well on polluted sites, and waste-
of heavy metals. water and can effectively carry out metal remediation
through bioaccumulation and biosorption mechanisms
[74]. Algal biomass extracted from these sites can also
Fungi-mediated remediation
be further consumed in a biorefinery including biofuel
Fungi can easily adapt and thrive under extreme abiotic production [75]. In the study by Mane et al. [76] the
conditions including high metal concentrations [12]. pretreated algal biomass of Spirogyra sp and Nostoc
Stress-tolerant fungi, such as Gliocladium, Penicillium, commune was used for the biosorption of Selenium
Fusarium, and Trichoderma can be effectively exploited (Se). Two methods, i.e., physical (heat and autoclaving)
for metal decontamination for environmental clean-up and chemical (sodium hydroxide and acetic acid) treat-
[64]. The fungi cell wall exhibits remarkable metal-bind- ments were applied to the biomass. It was reported
ing ability [65] and function as an adsorbent for metal that the pretreatment enhanced the biosorption of
ions immobilization exhibiting high remediation poten- Spirogyra biomass as compared to the live biomass. The
tial, consequently leading to its wide applications in maximum biosorption of 50 and 52.4% was attained
remediation [66]. The metal adsorption process is medi- with oven-dried biomass (60 C for 12 h) of Spirogyra sp
ated with the help of chitin-chitosan complex, glucuronic and N. commune, respectively. Under laboratory condi-
acid, phosphate, and polysaccharides present in/on fungi tions, all the pretreated biomass increased biosorption
cells, through ion exchange and coordination [67], and of Se in comparison with live biomass. The maximum
functional groups, such as amine, carboxyl, sulfhydryl, metal removal efficiency for Se was observed with bio-
etc. that are involved in influencing adsorption potential. mass dried at 60 C for 12 h for Spirogyra (50%) and
The strains: Aspergillus, Penicillium, Mucor, Rhizopus, Nostoc (52.4%), respectively.
Saccharomyces, etc., are widely employed in remediation Phycoremediation offers numerous advantages over
owing to their high metal adsorption capacities [68,69]. other conventional methods like easy manipulation,
Metal remediation conciliated by a cell wall and/or extra- cost-efficient, environment friendly, no secondary waste
cellular material can also occur in dead cells. Rozman production, easy recovery of metal contaminants,
et al. [70] investigated the biosorbent potential for waste energy-efficient, and less sludge generation [77–79].
fungal biomass to accumulate and remove PbII and CdII Metal remediation in algae is a two-step process, i.e.,
ions. The waste fungal biomass was dried and pretreated physical adsorption followed by chemisorption [80].
with three (3) different chemical procedures, i.e., using: Microalgae like Chlorella, Chlamydomonas, Spirulina,
NaOH, H2O2, and NaCl, and then directly used for the Scenedesmus, Nostoc, and Oscillatoria have been effect-
accumulation and removal of Pb(II) and Cd(II)ions. The ively utilized in wastewater treatment [81,82]. Algal cells
pretreatment enhanced the removal efficiency from 87 are an ideal and cheap alternative to costly adsorbents
and 84 to 93 and 97% for Pb(II) and Cd(II), respectively. due to their diversity and multi-layered cell walls [83]
Metal-binding proteins may facilitate metal uptake in liv- leading to their wide applications (Figures 2(c,d)).
ing cells [64]. Intracellular accumulation of metals in a
fungal cell is an active process where metal ions are sub-
Mechanisms involved in microbial-assisted
sequently compartmentalized to different subcellular
remediation
places [71]. Dead cells are preferred over live cells due to
their numerous advantages, leading to their wide utiliza- As mentioned earlier, microorganisms’ ability to thrive
tion in remediation. Living cells use is limited owing to even in the most unsuitable habitats, including contami-
their: sensitivity to the environment, set-up conditions nated sites, makes them ideal agents for remediation. In
and concentration of metal ions, more nutrient require- addition, different responses have been shown by microor-
ments, and difficult biosorbent regeneration [64]. These ganisms toward different metal ions [54]. Thus, metal-
live cells’ intricacies and dead cells’ high metal-binding resistant microorganisms can be utilized for metals remedi-
ability have made the latter a preferred choice for ation to reduce their negative impacts on the environ-
remediation [72] (Figure 2(b)). ment, and the various mechanisms employed include:
Micro algae-assisted metal remediation Microbe-assisted biosorption

Phycoremediation can be described as treating conta- Biosorbate-like heavy-metals ions bind on biosorbents
minated sites by applying microalgae through through various interactions [84]. In the case of
biosorption, dead biomass is better than living biomass mechanism employed is ligand-mediated metal solubil-
as it is less expensive and unaffected by nutritional sup- ization [97], leading to remediation from the dump site.
ply, metal toxicity, and inimical operating conditions The secretions produced by microorganisms like low
[85]. A Hg-tolerant study of bacterial strains suggested molecular weight organic acids or inorganic acids can dis-
that both live and dead bacteria sequestered mercury solve heavy metals in dumpsites [93,98]. The range of
extracellularly as spherical deposits with a sequestration microorganisms employing bioleaching mechanisms for
capacity of 1–2 mg mercury/g [dry weight] of biomass metal remediation, Acidithiobacilli, Chromobacterium vio-
and 40–120 mg mercury/g [dry weight] of biomass, laceum, and Pseudomonas fluorescens is mentioned in
respectively. The chemical analysis and Fourier trans- Supplementary Table 2.
form-infrared (FTIR) spectroscopy showed the presence Bioleaching has limitations, such as low kinetics,
of EPS on the surface of the strains highlighting Hg-tol- time-taking, toxic chemical production, and the expen-
erant bacteria potential by biosorption on the surface of sive limit of its productivity and utilization [99]. A cul-
biomass or secreted EPS [86]. In the case of bacteria, ture of sulfur-oxidizing bacteria and a consortium of
both live and dead cells have been reported for the bio- biosurfactant-producing bacteria and sulfur-oxidizing
sorption of heavy metals. It has also been observed that bacteria were studied for their bioleaching ability
the pretreated bacterial biomass increased biosorption toward Zn, Cu, Pb, Ni, Cd, and Cr from printed circuit
of heavy metals due to the rupturing of the cell wall boards [100]. Aspergillus niger focused on valuable
and/or the formation of additional binding sites [87,88]. metal leaching from electronic waste printed circuit
In the case of physical treatment, e.g., heating surface boards where metal extraction was mainly attributed to
binding sites increased biomass whereas, chemical the release of organic acids from the fungi, hence, the
(acidic) treatment enhanced surface binding sites, and study proved fungal bioleaching-mediated metal mobil-
alkali treatment enhanced positively charged functional ization from printed circuit boards to recycle electronic
groups to negative and resulted in the enhancement of wastes [101]. Similarly, Penicillium simplicissimum was
biosorption [89]. In the case of fungi, two mechanisms used to recover metals from power plant residual ash
have been proposed, i.e., extracellular (chelation and and the highest extraction of V (100%) and Ni (40%)
cell membrane binding) and intracellular sequestration was achieved by the spent-medium bioleaching
of heavy metal via binding to proteins/other ligands. method. It was also observed that bioleaching was
The intracellular sequestration additionally prevents the more effective than chemical leaching with improve-
fungal cells from harming the metal-sensitive cellular ment in V (19%) and Ni (12%) recovery [102].
targets. The biosorption capacity of Chlorella sp. isolated
from local environments in Malaysia was investigated
Microbe-mediated bioaccumulation
toward Cu and Zn ions where energy-dispersive X-ray
spectroscopy and scanning electron microscopy (SEM) Microbial strains with self-replenishment ability are
revealed ions sorption on the cell surface with biosorp- employed to uptake metals metabolically, after their
tion capacity of 33.4 and 28.5 mg/g for Cu and Zn ions, passive physical adsorption on the microbial surface,
respectively [90]. The rectification of contaminated soil which can be further improved through resistant spe-
employed Absidia cylindrospora against Cd, Cu, and Pb cies and surface modification development [103,104].
was investigated and studies revealed 14, 59, and 68% Bioaccumulation and biotransformation are the key
biosorption of Cu, Pb, and Cd, respectively by fungi [91]. processes in controlling the remediation efficiency of a
microorganism. Microorganisms’ survival in the conta-
minated environment is attributed to their adaption,
Microbe-mediated bioleaching
leading to their accumulation potential evolution [105].
Bioleaching involves metal solubilization and recovery Biomass employed in remediation can adsorb metals,
from insoluble ores/waste mediated by microorganisms actively (bioaccumulation), passively (biosorption), and
[92]. The process is also known as biohydrometallurgy or through a mix of both processes [106]. Within the bio-
microbial leaching [93]. The process has been utilized to accumulation process, metallothioneins and metal-
remove and extract metals, such as Zn, U, Cu, and Ni binding proteins can be exploited and expressed within
through their solubilization [94]. It differs from biomining environmentally vigorous microorganisms to improve
which focuses on metal recovery for industrial applica- their accumulation potential and metal tolerance within
tions [95]. It can be divided into types, direct and indirect, microbial cells [107]. The diverse range of studies focus-
depending on the involvement of metabolic activity or ing on bioaccumulation survival strategy provides
metabolic compounds for metal extraction [96]. The insight into wide applications of microorganisms in
environmental remediation from toxic heavy metals. uptake and transformation with 60% Hg sequestered in
Strategies for arsenic detoxification through bio- bacterial biomass and 5% of sequestered Hg volatilized.
accumulation and biotransformation mechanisms are There was biotransformation of sequestered mercuric
exclusively reported within the microbial system by ions into monovalent mercury (Hg2Cl2), a non-bioavail-
Tripathi et al. [108]. Genetically modified (GM) microor- able form of Hg [118]. The wood-rotting fungal strain
ganisms to treat a combination of radionuclide and isolated from Thailand was shown to transform: zinc
metal contamination can be employed through engin- sulfate into zinc oxalate dihydrate, copper sulfate into
eering of radiation-resistant strains which can effect- copper oxalate hydrate, cadmium sulfate into cadmium
ively treat dump sites contaminated by heavy metals oxalate trihydrate, and lead nitrate into lead oxalate
like mercury [109]. Vibrio alginolyticus was isolated from proving the ability of wood-rotting fungi in metal
a metal-contaminated site in El-tebeen, south Helwan, removal from the metal-amended substrate via trans-
bacteria showed a bioaccumulation mechanism for formation leading to precipitation as metal oxalates
mixed metal decontamination with subsequent reduc- (biominerals) which are nontoxic toward fungi [119]. In
tion of 20% for Cd, 31% for Cu, 40% for Pb, and 45% for a study near the smelter emission zone with Cd, Zn, Pb,
Zn in the culture supernatant [110]. For metal-contami- As, and Cu contaminants, a richness of indigenous
nated water treatment, sulfate-reducing bacteria (SRB), microorganisms, such as Proteobacteria, Actinobacteria,
Bacillus cereus (B. cereus), and Camellia oleifera cake Bacteroidetes, and Acidobacteria was found which was
(COC) was employed in a novel technology where bio- attributed to antioxidant response, metal exportation,
sorption, bioaccumulation processes concurrently with and biotransformation mechanisms leading to metal
biosurfactant production by bacteria resulted in waste- removal from such sites [120]. Cyanidioschyzon sp. iso-
water remediation with 97% metal removal [111]. The late 5508 study showed oxidation-mediated biotrans-
bioaccumulation survival strategy can be exploited for formation of arsenic where arsenite [As(III)] was
metal recovery of precious metals like Au where strains converted to arsenate [As(V)]. The same study was ela-
capable of withstanding high metal concentrations can borated with two arsenic methyltransferase genes,
be domesticated and engineered for their retrieval effi- CmarsM7 and CmarsM8 cloned from the alga into an
ciency [112]. A Pb-resistant bacterial strain, arsenite hypersensitive strain of Escherichia coli where
Acinetobacter junii, was isolated from a coal mine dump the bacteria later conferred tolerance to As(III) [121].
which showed antibiotic and multi-metal resistance Similarly, rhizospheric fungi Aspergillus flavus, isolated
with 60% accumulation of Pb(II) after 120 h which from an As-contaminated rice field, could convert sol-
proved the bacterium efficiency in the restoration of uble As into As particles whereas the latter showed less
Pb(II) contaminated repositories [113]. One major lag toxicity effects to soil-dwelling bacteria, fungi, plant,
with bioaccumulation is during the recovery of accumu- and slime mold proving the fungi as an effective metal
lated metal, which is only possible through destructive toxicity reducer within the contaminated sites [122].
means, leading to damage to the structural integrity of
biosorbent [105].
Factors impelling microbial remediation,
mechanisms, and microbial activities
Microbe-assisted biotransformation
Environmental conditions significantly influence the
Biotransformation employs the conversion of com- bioremediation process, directly affecting microorgan-
pounds through enzymatic reactions, such as reduction, isms’ growth and survival in contaminated sites
oxidation, and hydrolysis for reducing the toxicity of through enzymatic and metabolic changes [123,124]. It
metal from soil, water, and sediments [114]. Metal is necessary to provide an appropriate biochemical and
reduction within microorganisms which is not necessar- biophysical environment for any optimum microorgan-
ily coupled to respiration may also impart metal toler- ism’s propagation [124]. Environmental conditions dir-
ance in microorganisms, for instance, removal of Se(VI) ectly affect remediation by altering heavy-metaloxicity
to elemental Se [115]; U(VI) to U(IV); and Hg(II) to Hg(0) and indirectly by regulating microbial activity [125].
[109,116]. Metals are generally soluble in oxidized forms There also exists a gap between their laboratory and
whereas reduced forms are highly insoluble and pre- on-site performances [126]. After the remediation setup,
cipitate from the solution [106]. Microorganisms like the addition of contaminants or disturbances through
bacteria and fungi can secrete extracellular enzymes for anthropogenic sources can significantly alter microbial
heavy-metals transformation [117]. The Alcaligenes fae- activity and generate pressure for continuous on-site
calis strain showed tolerance for Hg through metal monitoring [127]. Environmental variables controlling
microorganisms’ metabolism, such as pH, temperature, pollutants due to temperature changes enhance their
metal concentration, and microbial diversity are briefly bioavailability toward microorganisms. This, in turn,
summarized [128]. upregulates the waste’s microbial uptake potential of
the waste, thus enhancing the metabolism and enzym-
atic activity and eventually increasing bioremediation
Influence of pH in microbial remediation
[52]. Removal efficiency tends to increase proportionally
pH emerged as a primary regulator to influence micro- with the rise in temperature [142]. Different microor-
organisms’ activity [129]. Microorganisms can be acido- ganisms have their own set of optimum temperature
philes (pH < 5), neutrophiles (pH 5–9), and alkaliphiles ranges evident from their environmental distribution
(pH > 9) depending on their optimum pH requirements [143]. Enzymatic machinery within microorganisms is
[97,130]. pH plays a critical role in shaping the compos- controlled by temperature, showing a general trend of
ition and activity of microorganisms [131]. Even minor doubling for every 10 C rise, affecting their remedi-
pH changes brought into the natural environment ation [126]. The 25–35 C range is generally optimum
result in a significant deviation from the normal meta- for microbial activity [144]. Leaching and degradation
bolic activity of microorganisms [132]. Studying pH on within microbial remediation notably depend on tem-
any dumpsite cannot solve the problem as we have perature conditions [145]. It has been reported that the
seen many microorganisms release different organic increase in temperature decreases liquid viscosity,
acids in response to remediation, leading to a change thereby resulting in an increase in the diffusion of
in the site’s pH [133]. In addition, pH plays a key role in adsorbate across the outer periphery layer and the
metal toxicity mitigation, modifying metal dissolution adsorbate particles [146]. Though it has to be consid-
and compound formation under high pH [125]. Ideal ered that an increase in temperature increases biosorp-
pH conditions are different for different microorganisms tion (via enhanced kinetic energy and surface activity of
under other conditions affecting their metabolism and the solute) an increase above optimal temperature will
enzymatic activity [134]. Optimum pH for aerobic and destroy the binding site and decrease biosorption [147].
anaerobic microorganisms may also differ significantly Farhan et al. [148] reported the use of Saccharomyces
[135]. Most bacteria are generally neutrophiles, most cerevisiae as a biosorbent material. It was observed that
algae are alkaliphiles and most fungi are acidophiles temperature influences the biosorption of metals and is
[136]. In the case of biosorption, pH plays a vital role as restricted under a certain temperature range. Also, a
in bacteria as it contains a weak acid and basic func- point to be noted is that biosorption cannot be per-
tional groups that enables the binding of metal ions or formed at high temperatures due to the rise in oper-
its solubility. It was reported that the electrochemical ational cost. Also, as adsorption is generally an
attraction and metal ion adsorption is directly propor- exothermic reaction, the biosorption potential rises
tional to the increase in pH (optimum pH 4–8) which, in with the decrease in temperature.
turn, increases the negative charge on the biomass sur-
face, thereby enhancing metal biosorption [137,138]. Li
Effect of heavy-metals concentration on microbial
et al. [139] reported Zn(II) biosorption by both live and
remediation
dead cells by the Streptomyces ciscaucasicus strain
CCNWHX 72-14. For the role of pH, it was reported that Heavy metal toxicity depends on two (2) major factors:
pH played a significant role in the biosorption potential. exposure and absorption, by microorganisms [145].
In the case of live cells, uptake of Zn2þ increased with Richer genetic diversity is generally seen in contami-
the increase of pH from 3.0 to 5.0, whereas for dead nated environments than in non-contaminated
cells it was restricted to a pH < 4.0 and at pH 5 it rose ones, along with a significant decrease in microbial
to 54.7 mg/g. Though a common feature beyond pH % diversity on raising metal concentrations, making the
the biosorption of both live and dead cells diminished. fight of microorganisms for survival evident [149].
However, it has been noted that the optimal pH will Microorganisms are particularly sensitive to greater con-
vary the organism used and the pollutant [140]. centrations of heavy metals [150]. However, to reduce
the impact of high metal concentrations, microorgan-
isms have many mechanisms in which efflux transport-
Temperature-mediated microbial remediation
ers play a very crucial role. They excrete excess metal
Resembling pH, the ideal temperature conditions also outside the cell thus increasing its tolerance. Lenart-
vary significantly based on microorganisms [141]. The Boron et al. [151] studied the effect of risk elements
alteration in the solubility of heavy metals and other (heavy metals, soil pH, and some mesophilic bacteria,
fungi, actinomycetes, and Azotobacter) on the groups adaptability and high treatment efficiency are two
of microorganisms from the industrial soils of one of important characteristics of typical GM bacteria [153].
the steelworks in Poland. It was reported that in the Little modifications utilizing GM microorganisms can
areas of high contamination, the presence of microor- significantly alter the metal remediation pathways
ganisms was abundant and the direct correlation thereby enhancing the remediation [154]. While deal-
between the microorganism and the concentration of ing with GM microorganisms, the main aim is to
heavy metals was insignificant. Do €nmez et al. [152] broaden their effectiveness and spectrum against a
reported the biosorption of Cu(II), nickel(II), and range of toxic metal combinations. It also involves
chromium(VI) using aqueous solutions on dried algae, enzyme alterations concerning: specificity and affinity,
i.e., Chlorella vulgaris, Scenedesmus obliquus, and gene construction and regulation pathways, process
Synechocystis sp. Among the various parameters tested development, monitoring and controlling bioremedi-
it was reported that the metal ion concentration greatly ation, and sensor-based bio affinity bioreporters appli-
influences the metal uptake potential. The higher the cations. The GM microorganisms can also have an
metal ion concentration the more the uptake, e.g., as enhanced ability to degrade a wide range of pollutants
Cu(II) concentration increased from 25 to 250 mg l1 and can also be employed for bioaugmentation
the loading capacity increased for Chlorella vulgaris [13,155]. The microbial strains altered through the
(31.2–46.8 mg g1), Scenedesmus obliquus (10.3–26.8 mg advancement in the molecular biology field to improve
g1) and Synechocystis sp. (14.2–32.2 mg g1), whereas their remediation potential through carbon flux redir-
for nickel(II) the maximum was 55.6, 24.7, and 30.3 mg ection to prevent: harmful intermediates formation,
g1. For chromium(VI) it was 33.8, 30.2, and 39.0 mg catabolic enzyme modifications, genetic stability
g1, respectively. improvement, increment in pollutants bioavailability,
and enhancing: monitoring, control, and yield with effi-
ciency of processes [155]. GM microorganisms also
Exploration of genetically engineering
exhibit enhanced bioaccumulation with the aid of
approaches for enhancing heavy-metals
enzymes like phytochelatin synthase which further
remediation
improves their tolerance [156]. Genetic engineering
The diverse metal ions in waste dump sites limit the can help avoid the employment of conditionally patho-
optimum activity of native microorganisms [12]. The genic microorganisms and can help utilize their func-
problems linked with toxicity and complexity in waste tional genes to improve remediation efficiency,
dump sites paved the way for GM microorganisms. It thereby broadening its scope in the future [12]. A
involves the modifications of microorganisms through greater remediation efficiency, in the case of GM micro-
human interference by introducing genes to improve organisms, than their indigenous counterparts, as sug-
their inbuilt remediation potential (Figure 3). Strong gested through various research and review articles,
Figure 3. Schematic representation of the role of genetic engineering approach and GM microorganisms in enhancing heavy
metal remediation.
claimed their potential as remediators in the future Potential role of bio-nanotechnology in

[157,158]. In a study, microalgae were engineered from remediation of heavy-metals
cell-surface to combine surface engineering to self-floc-
Recent work has focused on the role of bio-nanotech-
culating microalga sorbents for selective biosorption of
nology in metal remediation through microbe-synthe-
target metal from multi-metal solution [159]. Another sized nanoparticles which are economically feasible,
study employed transgenic Chlamydomonas reinhardtii and sustainable. It is the integration of bioremediation
(C. reinhardtii), a green alga combined with ultrasound with nanotechnology, i.e., nano bioremediation. It
for Hg remediation where the transgenic C. reinhardtii enhances the remediation of heavy metals and can be
(2AMT-2) expressing a plasma membrane-anchored used with different nanomaterials and microbes.
metallothionein polymer effectively recovered Hg (II) Additionally, they can be used as nanocarriers for
through sonication over a broad pH range which is microbial biosorbents in enhancing heavy metal
effective for Hg contaminated sediments remediation removal [166,167]. In the case of biogenic nanopar-
[160]. Rojas et al. [161] reported that IncP-1b plasmid ticles, two approaches can be accomplished for the syn-
pTP6, providing novel MerB, MerG genes, and other thesis, i.e., extracellular and intercellular. These two
Mer genes, were introduced into a bacterium approaches for the synthesis of nanoparticles can be
Cupriavidus metallidurans, strain MSR33 where organo- conducted via biologically controlled mineralization
mercurial lyase protein MerB and the mercuric reduc- and biologically induced mineralization under aerobic
tase MerA of this strain were synthesized in presence or anaerobic conditions [168]. The major benefit of bio-
of mercury, leading to bio-volatilization mechanisms genic nanoparticles is that the size and shape can be
for effective remediation [162]. Microorganisms cannot engineered as per the requirement via manipulating
escape unscathed during the biotransformation, as in the parameters like pH, temperature, etc. Fe nanopar-
the case of bacteria reducing chromium (VI) to chro- ticles synthesized using Chlorococcum sp. MM11 was
mium (III), so GM bacteria producing trehalose were found effective in Cr6þ restoration, instantly reducing
able to effectively reduce chromium (VI) to chromium 92% of 4 mg/L Cr6þ to Cr3þ [169]. In another study,
(III), compared to that of a wild type where only half of algae-mediated biosynthetic Fe3O4 nanoparticles which
the same amount was reduced. Genetic modifications were wrapped in calcium alginate beads were found
have proved effective in reducing chromate reduction- effective for Pb adsorption with a removal capacity of
related side effects [163]. Overexpression of operons 91% [170]. Conventional approaches employ hazardous
like ars (ars1 and ars2), as in Corynebacterium glutami- resources for nanoparticle assembly which led to the
shift to bioinspired synthesis with the help of bacteria
cum, is effective against As contaminated sites remedi-
which further offers numerous advantages to cost and
ation [164]. Along with gene modifications and
environment along with heavy-metals ions bioreduc-
alterations, surface modifications on microorganisms
tion and bio-recovery. Metallic nanoparticles can also
can effectively ameliorate their metal-binding ability to
be employed as calorimetric sensors for metal ions in
improve their remediation potential, though it
contaminated environments and offer numerous
increases the overall process cost which is another obs-
advantages like simplicity, cost-effectiveness, and high
tacle for the scientific community to address [162]
sensitivity which are critical for efficient remediation
(Supplementary Table 3).
[171]. Additionally, for more advantage, various nano-
It also must be noted that the use of biolumines-
scale structures can be concurrently used with microbes
cent GM Pseudomonas fluorescens HK44 in the field to facilitate enhanced heavy metal removal. Also, the
was conducted for bioremediation and has been immobilization of various microbes in various nanoma-
successfully implemented under moderately large- terials can be used to prepare effective nanocomposi-
scale and controlled field conditions [165]. Despite te/biosorbents. Although there are also certain
the ethical argument of using GM microorganisms, disadvantages, such as nanoparticles, these can
their significance in the removal of heavy metals enhance the toxicity of certain pollutants, e.g., TiO2
should not be overlooked. Also, the major limita- nanoparticles (5 ppm) enhanced the toxicity of phenan-
tion of using GM microorganisms, such as tolerance threne and Cd by 2.0 and 12.2%, respectively for
to hostile field conditions and exploring novel Zooplanktons though it reduced the toxicity by 24.5
microorganisms while considering native environ- and 57.1% at 400 ppm of TiO2 nanoparticles due to the
mental factors under laboratory conditions, should aggregation of nanoparticles, suggesting concentra-
be addressed via a multidimensional and holistic tion-dependent toxicity nanoparticles. Thus, bio-nano-
approach. technology has given a new direction to effective metal
detection and remediation, which can be further Advantages, limitations, and future
explored in the future and can lay the foundation perspective of microbial-assisted remediation
toward sustainable development.
Microbial remediation employs microorganisms’ natural
activity for remediation by speeding up decontamin-
ation under optimized conditions [186]. The pollution
Role of life cycle assessment (LCA) alleviation prompts the biodegradation processes
and techno-economic assessment (TEA) in already occurring in nature with little/no modification
heavy-metals remediation [150]. Ease of handling as well as genetic manipulations
for metal binding and transforming genes of microor-
The LCA approach analyses the overall impact on the ganisms led to their wide-level exploration for remedi-
environment, economy, and social factors of any indus- ation [187]. Their high remediation potential
trial process and technology [172–174]. It has been contributes another remarkable advantage owned by
applied in numerous advanced bio-refineries to funda- microorganisms even at low metal concentrations that
mentally assess their performance toward environmen- too without any secondary pollutants production [188].
tal performance indexes as well as energy output [175]. Bioremediation is a comparatively low-cost, more spe-
The major components of LCA analysis can be applied cific, safe, and uncomplicated in situ remediation
in a range of sectors, such as renewable bioenergy and method [150]. Additionally, long-term stability is
biobased products [176,177], chemical generation [178– another remarkable advantage interlinked with bio-
181], and WM [182]. In a study by Yao et al. [183] the remediation [189]. Thus, the increasing study on bio-
environmental effects of constructed wetlands (CWs), remediation proves its promising future in pollutant
ecological floating beds (EFBs), and combined eco- clean-up in dumpsites.
logical floating beds (CEFBs) were investigated where Despite the advantages, the major limitation is that
the acquisition of raw material, construction, and oper- their effectiveness is only for a limited range of com-
ation of these accounted for 24.1, 35.3, and 40.6%, pounds [190]. Additionally, the need for prior labora-
respectively, to the total environmental effects. In this tory-scale study of contaminated sites to find the
study, raw material acquisition for bioremediation sys- remediation potential of individual strains or consorti-
tem construction contributed to 51.6% of the total ums thriving on contaminated sites makes it time-con-
environmental effects. Thus, the LCA approach provides suming [191]. The designing of set-up also requires
new dimensions to future research by dealing with all expertise in the area and concerned people need to be
the associated limitations throughout the process. LCA trained accordingly making it further laborious [192].
Microorganisms and plant partnerships can be effect-
and its streamlined versions, such as environmental
ively utilized in various remediation events, but a
footprint analysis can be used as supporting tools in
slower plant growth rate is an obstacle for laboratory
decision-making by the scientific community [184]
and field applications [193].
whose results are then analyzed to find the ideal
A newer approach in the bioremediation field is GM
remediation technology.
microorganisms [194], however, more investigation is
On the other hand, the TEA provides an overall
required before large-scale implementations. Another
insight into the market feasibility of the method or pro-
set of limitations with microbial remediation is the lack
cess used. A study was conducted by Abd Elhafez et al.
of inherent ability in every microorganism to degrade
[185] for the analysis of Cu(II) ions removal using rice contaminants thus, bioremediation cannot be regarded
husk through adsorption and discusses the economic as a completely environment-friendly process owing to
aspect of rice husk employment for remediation. The partial degradation of pollutants leading to the produc-
major limitations hindering its use are the transporta- tion of more toxic products, thus harming the environ-
tion cost compared to benefits in uses like animal feed ment severalfold than the parent compound [195,196].
and compost. The revenues exceed the operational The need for monitoring throughout the process makes
costs with a net profit margin of 144,000 e/y and bioremediation a very laborious and expensive task
1200 t/y production of adsorbent material production. [127]. Difficulties are also faced in terms of applying
The revenues of this enterprise are higher than the laboratory studies in field applications. [126]. Likewise,
operational costs, leaving a net profit of 144,000 e/y for on sites at high concentrations of chemicals, microbial
an adsorbent material production of 1200 t/y. This led remediation will not be effective as most microorgan-
to its wide applications owing to environmental, eco- isms will not be able to tolerate higher metal concen-
nomic, and social benefits. trations [150].
Thus, a more detailed study along with focusing the References

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Microbial Assisted Multifaceted Amelioration Processes of Heavy-Metal Remediation: A Clean Perspective Toward Sustainable and Greener Future

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Critical Reviews in Biotechnology

ISSN: (Print) (Online) Journal homepage: www.tandfonline.com/journals/ibty20

Microbial assisted multifaceted amelioration

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Microbial assisted multifaceted amelioration processes of heavy-metal

ABSTRACT ARTICLE HISTORY

Introduction mismanagement has resulted in huge garbage

samples analyzed had higher concentration of Cd and Heavy-metals accumulation

Micro algae-assisted metal remediation Microbe-assisted biosorption

claimed their potential as remediators in the future Potential role of bio-nanotechnology in

Thus, a more detailed study along with focusing the References

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