Microbial Bioremediation of Heavy Metals: Emerging Trends and Recent Advances

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Microbial Bioremediation of Heavy Metals: Emerging Trends and Recent

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Article in Research Journal of Biotechnology · January 2020
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Research Journal of Biotechnology Vol. 15 (1) January (2020)
Res. J. Biotech
Review Paper:
Microbial Bioremediation of Heavy Metals:
Emerging Trends and Recent Advances
Zango Usman U.1, Yadav Mukesh2, Sharma Vandana3, Sharma J.K.3, Panwar Sanjay4, Dan Sidhartha2
and Sharma Anil K.2*
1. Department of Biotechnology, Sa'adatu Rimi College of Education, Kumbotso, (SRCOE), NIGERIA
2. Department of Biotechnology, Maharishi Markandeshwar (Deemed to be University), Mullana-Ambala (Haryana), 133207, INDIA
3. Department of Physics, Maharishi Markandeshwar (Deemed to be University), Mullana-Ambala (Haryana), 133207, INDIA
4. School of Basic and Applied Sciences, Maharaja Agrasen University, Atal Shiksha Kunj, Kalujhanda, Barotiwala, Solan - 174103,
Himachal Pradesh, INDIA
*anibiotech18@gmail.com; sharma.biotech18@gmail.com
Abstract Nickel (Ni) etc. leading to noxious wastewater.2 Majority of

Significant amounts of heavy metals are being added countries from the developing world are adversely affected
into the soil and effluents each and every day due to due to heavy metals contamination resulting into gross
enhanced industrialization and other anthropocentric environmental, health, economic and planning concerns in
such countries.3 Effluents with heavy metals are discharged
activities. Many heavy metals are even non-degradable
directly into water streams as industries have a strong
in nature and hence once released into the environment perception that these will miraculously disappear as rapidly
remain in circulation. Upon increased concentrations as they are produced.4
beyond the threshold limit, these heavy metals may not
only result in chronic and lethal diseases in humans but Effluents from industries are discharged through mine
also affect the animal and plant metabolism. Many of trailing, sludge dumping or indirectly through runoffs.
the physico-chemical methods employed as of today During this process what we see is a metal-microbe
such as electrochemical treatment, ion exchange, interaction, which recently researchers and industrialists are
precipitation and reverse osmosis for heavy metal looking for to remove, recover or stabilize heavy metals in
removal from waste streams have not been proved cost the soils and effluents.3 Microbial bioremediation therefore
is of paramount importance in the removal of heavy metal
effective, therefore a biological approach could prove
contaminants from the soil and wastewater. Heavy metals
as an alternative remediation technology for heavy are also reported to be leached into the adjacent locations in
metals contamination. the vicinity and likely to contaminate the underground water
affecting negatively on health of living beings.4,5
Microbes have evolved mechanisms such as active
efflux or sequestration with proteins or insoluble The physico-chemical methods such as precipitation, ion
compounds through which they may resist, detoxify or exchange, electrolytic technologies, chemical extraction,
metabolize these heavy metals. Current review leaching, hydrolysis, polymer micro-encapsulation, land
highlights the recent advancements made in filling etc. have not proved effective enough for the heavy
understanding the heavy metals-microbes interaction metal removal.6,7 Many technologies including vapor
and applications thereof in heavy metal remediation. extraction, stabilization, solidification, soil washing and
flushing, vitrification, incineration and thermal desorption
have been tried in the past to remove these pollutants.8 Again
Keywords: Heavy metals, effluents, mechanism, microbes,
bioremediation. at large scale these are quite expensive and require constant
monitoring and control, at times even not completely
removing the contaminants.9
Introduction
There is a strong need to understand the tri-partite Other methods like use of chemicals for treating effluents
relationship between pollution, public health and were also reported to be non-feasible economically,
environment in today's scenario considering the increased especially when dealing with low metal concentrations with
pace of industrialization and urbanization. Industries are high impact of contaminants. However, the biological
discharging effluents (generated during processing of raw treatment or bioremediation technique has been thought of a
materials) at enormous amounts to the water reservoirs better alternative method for the treatment of contaminated
contaminating them profusely. Effluents if left untreated and waters and soils.10
released as such to the environment, have been attributed to
cause pollution in both water bodies and the soil.1
Why Bioremediation?
These effluents are vulnerable to human health and to the life Microbial bioremediation procedures have been rated as
of aquatic animals as they harbor many toxic and hazardous economically feasible displaying promising results in the
substances including heavy metals such as Chromium (Cr), removal of organic compounds like petroleum hydrocarbons
Cadmium (Cd), Lead (Pb), Mercury (Hg), Arsenic (As), as well as heavy metal ions from contaminated water and soil
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[Fig. 1]. As such the techniques were found to be better Biostimulation on the other hand employs nutrients or
option for removing heavy metal ions and hydrocarbons substrates to stimulate the ubiquitous organisms to perform
from polluted sites.9 Biological treatment of toxic chemicals bioremediation. Oxygenation, addition of nutrients such as
accompanied with efficient management of microbial fertilizers, growth supplements are common stimulants.
processes, initially under controlled laboratory conditions, Bioventing is another process which involves the venting of
coupled with effective manipulation of indigenous microbial oxygen through the soil to enhance the bioremediation
communities to ensure successful in situ bioremediation process.18
activity. It requires a basic knowledge of the toxic effect of
various heavy metals on the bacterial and fungal Bioaugmentation is the process of introduction of
populations.3 microorganisms in the area of contamination and optimize
the conditions of the environment to speed up the
Sherma et al11 noted that some microbes were tolerant of biotransformation of the hazardous substances into either
heavy metals with the ability to either remove them from the metabolites or less toxic substances. These substances are
environment or break them down to less toxic or completely further utilized by other microbes in association with
benign forms. Microbial resistance to pollutants particularly plants.19 This process is effectively used in the area where
heavy metals is absolutely vital for the process of intrinsic bioremediation or biostimulation did not show
bioremediation of contaminated soils as the process requires satisfactory results; may be due to the insufficient or
bacteria and other microorganisms to come into close unacclimated microbial populations.
physical contact with the pollutants in order to accomplish
the activity of decontamination.12 Selected strains of bacteria or fungi with desired catalytic
capabilities and other essential characteristics are injected
Bioremediation of heavy metals by microorganisms is much directly into the contaminated area along with the necessary
dependent on the nature of the site and the chemicals in the nutrients and conditions were optimized accordingly i.e.
environment.13 But it remains the most cost-effective temperature, pH etc. Bioaugmentation may also be used in
process that reduces pollutants to non-hazardous materials. area where indigenous microbial population does have the
In the past decade or so, the use of microbes in treating capability to break down the pollutants, but may be achieved
wastewaters polluted with heavy metals has become an through molecular breeding or genetic engineering of
attractive bioremediation alternative with a promising microorganisms by removing the adhesives qualities of
potential.14 microbes which in turn would allow them to penetrate
through soils and rock matrices.20,21
Microbes in the soil play either directly or indirectly in
maintaining the biogeochemical cycles within the soil Biosorption is another concept of bioremediation where
ecosystem. They help in the recycling mineral nutrients such heavy metal ions are absorbed in the polluted sites by the
as nitrogen, phosphorus, sulphur and numerous metallic ions microorganisms. The main chemical functional groups are
like Cu, Fe and Al which contribute to the sustainability of removed by the process in the heavy metal compounds that
life, particularly plant life.4 The processes of bioremediation have a strong electronegative group such as carboxyl,
involved the metal-microbe interaction which includes: phosphate groups as well as nitrogen containing groups.
adsorption, complexation, precipitation, oxidation, These groups play vital roles in binding with the toxic metals
reduction, methylation and methylation.15 In addition, the in the specific or non-specific binding sites on the cell
chemical reaction between microbes and metal ions has been membrane of the microbes which in turn absorb these toxic
broadly categorized into six different processes namely: metals into their cellular structure.22 The advantage of this
intracellular accumulation, cell wall associated metals, process is that after their physical removal from the
metal-siderpohore interaction, extracellular mobilization or environment, the metal ions may be recovered, stabilized or
immobilization of metals by bacterial metabolites, buried whatever is deemed as most suitable. The biological
extracellular polymer metal interaction and transformation components in this process may be either living or dead cells
and volatilization of the metals.16 as the process does not require active cell metabolisms.23-25
Bioremediation has now become a field of science that Due to the abundance nature of microbes and low cost, many
involves intrinsic bioremediation, biostimulation and researchers have described the technique as most useful in
bioaugmentation [Fig. 1]. Other technologies are biofilters, the removal of heavy metal ions from polluted area, be it
bioreactors and bioventing.17 Intrinsic bioremediation is the through biosorption, biotransformation or
process whereby the natural indigenous microflora and bioaccumulation.26 Fungi have been reported to be good
environmental conditions interact to bring about the natural biosorption agents in removing heavy metal ions by these
attenuation to the pollutants to safer levels within acceptable processes. In liquid media fungi and yeast removed the
time frame. This process is generally a first choice for heavy metals by chemical transformation through redox
biotreatment, as it requires no intervention with the reactions.18,27 Fungi can also remove the heavy metals by
occasional monitoring of the natural process of process of bioaccumulation in which it uptakes the
biodegradation.17 contaminants through metabolic-dependent processes which
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result in the transportation of the contaminants into cell wall content of Cd in the soil is less than 1ppm with the normal
and its partitioning intracellular components.28 It has now range 0.005–0.02 ppm.36 The production of this metal has
become evident that through bioremediation microbes such increased rapidly in the last few decades from 11000–19000
as bacteria, fungi and algae can coax into accumulating tonnes in 1985.30 This heavy metal is used in making
heavy metals from polluted areas rendering them harmless.29 semiconductors, Nickel–Cadmium batteries, electroplating,
PVC manufacturing, different alloys, pigment and control
Heavy metals and their toxicity: Heavy metals require a rods for nuclear reactors. Water and soil contamination with
great environmental concern because of their distribution, Cd originate from mining and smelting industries, fuel pump
widespread use and toxicity to human beings. However, site, atmospheric pollution and sewage sludge application.39
there are some elements that are essential for living
organisms at low concentrations while some of them are Cadmium has no essential biological function and is highly
toxic to human even at very low concentrations.30 These toxic to the body of living organism. Chronic exposure to
heavy metal elements are usually known as transition metals, cadmium in humans has several toxic effects such as high
among the heavy metals there are essential elements such as blood pressure, kidney, lungs, liver and testes damage.
Zinc (Zn) and Iron (Fe), while the toxic metal includes: Cadmium is also associated with disease called Itai-Itai
Cadmium (Cd), Lead (Pb), Mercury (Hg) and Nickel (Ni).31 meaning “it hurts” in Japanese.39 It is characterized by bone
pain, pathological fractures and signs of renal impairments.31
Heavy metals have adverse effects on human physiology and
the biological system in general.32,33 They show great Lead: Lead (Pb) is a chemical element in the carbon group
affinity to other elements such as sulphur disrupting enzyme with number 82. It is found to be soft, malleable and heavy
functions in living cells by forming bonds with the post transition metal. Metallic lead (Pb) has bluish–white
functional group. Cadmium (Cd), Lead (Pb) and Mercury colour after being freshly cut, but soon tarnishes to dull
(Hg) ions have ability to bind with the cell membranes, then grayish colour when exposed to air. It has a shiny chrome–
interfering in cell transport processes.34 Heavy metals silver luster when it is melted into liquid. Lead (Pb) as annual
stimulate the formation of free radicals and reactive oxygen production is about 8 million tonnes. It is commonly used in
species which may lead to the cell oxidation stress.35 They batteries, painting, automobile fuel, semiconductors and
are non-biodegradable and tend to accumulate in the tissue electroplating industries.
of living organisms by the process of bioconcentration.32,33
Lead (Pb) is highly poisonous metal (when inhaled or
Metal speciation influences toxicity of a given metal that is swallowed) by affecting almost every organ and system in
related to the chemical form or species of the element i.e. the body. It also affects bone and the nervous system both in
speciation. Speciation depends on physical and chemical adults and children. Long term exposure can cause
characteristics of soil and wastewater36 due to the nephropathy and colic-like abdominal pain. It may cause
interactions such as complexation and adsorption which may weakness in fingers, wrist or ankle. Expose to high Pb levels
remove some ions from biological activity. Simple and can cause infertility in men, severe damage to the brain,
complex cations are more mobile while chelated cations are kidney and ultimately cause death.38
slightly mobile. The heavy metals become mobile after
oxidation or weathering in the soil. Kabata-Pandias37 has Zinc: Zinc (Zn) has atomic number 30, it belongs to group
shown that speciation of zinc and cadmium is organically II–B in the periodic table. It is relative found abundant in the
bounded, exchangeable and water solution in the soil earth crust. Zinc (Zn) is bluish–white lustrous metal, very
complex mixture of mineral e.g. clay and organic substances malleable and moderately reactive that it combines with
which make it dynamic with variation in moisture content, oxygen and other non–metals. It only has one common
pH and redox potential conditions. These properties interfere oxidation state of (+2), Zinc is widely used in corrosion–
with form and availability of metals in the soil.30 resistant steel coatings, brass alloys, painting pigments,
woods preservatives, dry cell batteries, cosmetics and
Heavy metal toxicity can result in damaged or reduced pharmaceuticals.34 The industry also uses a large amount of
mental and central nervous system, lower energy level and Zn to produce die-casting, which contributes to emissions to
damaged blood composition, lungs, kidney and other vital the atmosphere water and soil. 40. The principal source of Zn
organs. Long term exposure may result in slowly contamination in the environment involves industrial wastes,
progressing physical muscular and neurological metal plating and acid drainage. Sewage and animal wastes
degenerative processes that mimic Alzheimer’s disease, constitute a source of Zn in the soil.39
Parkinson’s disease, muscular dystrophy and multiple
sclerosis. Allergies are not uncommon with long term Zinc (Zn) is in contrast to the other two heavy metals
contact with some metals or their compounds.38 discussed above, it is an essential trace element for animals,
plants and bacteria necessary for life. It plays important role
Cadmium: Cadmium (Cd) is a member of group II-B of the in the catalytic activity of proteins. Shortage can cause loss
periodic table and is relatively rare metal which makes it of hair, skin lesion, diarrhea in human, while in plants it can
uncommon in most of natural soil and water.30 The average cause chlorosis, impaired growth and malformation of leaves
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and stems.30 Excess exposure to the Zn can lead to loss of Bioaccumulation is a substrate specific process driven by
weight, impaired immune system and blockage of essential ATP58,59 in which active transport is involved in the process
reaction in the cell.41 of heavy metals uptake. Three mechanisms of metal
transport into the bacterial cells are known: passive
Microbial Interaction with Metal Pollutants: Toxic heavy diffusion, facilitated diffusion and active transport. Some of
metals are among the most problematic wastes released to the active transport systems of heavy metal ions are
the environment through indiscriminate disposal of chemical selective. However, there are some exceptions; Cd can be
pollutants and wastes from industrial, mining and transported by some transporters as Zn .60 A disadvantage of
agricultural activities. This results in surface pollution which bioaccumulation is recovery of the accumulated metal which
subsequently moves downward to the underground water.42 has to be carried out by destructive means leading to damage
The recalcitrant nature of heavy metals makes it responsible of biosorbent structural integrity of the cell.61
for their persistence in the environment and subsequently
leads to the bioaccumulation in the food chain.43 Biosorption refers to other mechanisms that are driven by the
Microbiological activity is primary important in the chemiosmotic gradient across the wall cell, but it does not
bioremediation of metal contaminated ecosystem as require ATP and it is primary controlled by physico–
microbial communities represent substantial biomass and chemical factors. These factors include adsorption, ion–
play important roles in biogeochemical pathways.14 exchange and covalent bonding and may occur either in
living or dead biomass; it is considered as an alternative to
The structure and diversity of microbial communities have conventional methods of metal recovery from
been known to change in the presence of elevated levels of solutions.58,62,63 Both gram positive and gram negative
heavy metals as the microbes adapt to the pollutant load.44,45 bacteria have negative charge on their cell walls. This is due
In a polluted environment, the response of microbial to carboxyl, hydroxyl and phosphyl group, thus in the
communities to heavy metals depends on the concentration presence of positive heavy metal cations, these groups are
and availability of metals and is also dependent on the very important in cation sorption.64 Biosorption has a
actions of complex processes controlled by multiple factors possible application as a process for the removal of
such as the type of metal, the nature of the medium and the concentration of heavy metals from wastewater and
microbial species.46,47 contaminated sites.59 However, the cost of the biomass plays
an important role in determining the cost of a biosorption
Many findings have found that heavy metals influence process, thus low–cost biomass is an important factor when
microbes by adversely affecting their growth, morphology considering practical application of biosorption.62
and biochemical activities resulting in decreased biomass
and diversity.48-50 Heavy metals generally exert an inhibitory Various microbes show different response to toxicity to the
action on microbes by blocking essential functional groups. heavy metal ions that confer them with a range of metal
For example Cd, Hg compounds affect metabolism by tolerance.65 Bacteria may achieve this in different ways
binding with SH group portions of protein51 interfering with either through biological, physical or chemical mechanism
membrane transport.52 Also, other inhibitory mechanisms that includes adsorption transport, precipitation,
include: displacement of essential metal ions and complexation and specific metal binding protein.64,66,67 From
modification of active conformations of biological metabolic point of view, groups of metal–chelating protein
molecules.53,54 It was also demonstrated that copper and called metallothioneins are very important in bacterial metal
silver blocked an enzyme system involved in respiration.55 tolerance.64,65 Metallothioneins are small cystein–rich
Conversely, at relatively low concentrations, some heavy polypeptides that can bind essential metals like Zn and other
metal ions like Cu, Co, Zn and Ni are essential for microbes, non-essential metals such as Cd, Pb and Cr.64
they provide vital cofactors for metallo–protein enzymes.56
Roane et al38 analyzed soil microbial communities from one
Bacteria as Bioremediation agent: Bacterial surface uncontaminated and two metal - impacted soils, Cd resistant
structures are very important to understand interactions with isolates were found from each soil. With exposure to 24 and
the surrounding environment, especially with heavy metal 48 µ/mL soluble Cd, the metal contaminated soil
ions. Bacteria can be gram positive or gram negative communities were more resistant than uncontaminated soil
depending on the composition of the cell wall membrane. communities. Arthrobacter, Bacillus and Pseudomonas spp
Gram negative cell walls are multilayered structure with an were isolated from cadmium contaminated soil, having total
outer membrane containing lipopolysaccharide i.e. Cd in the range of 5.0–5.50 µg/g and MRL for Cd was
lipopolysaccharide layer (LPS), phospholipids and a small determined. Bacillus spp H9 resisted Cd up to 275µg/mL
peptidoglycan layer. On the other hand, gram positive cell followed by Pseudomonas spp HI (225µg/mL). In another
walls have as much as 90% of the cell wall consisting of study, four Cd resistant isolates showing resistance up to 275
peptidoglycan in several layers with small amount of µg/mL were evaluated for metal detoxification in solution
teichoic acid usually present.51 These structures are and soils. Bioavailable cadmium reduction by these strains
negatively charged and can interact with metal ions in the was measured in MSM broth containing various
surrounding environment.57 concentrations of soluble Cd ranging from 75–3225 µg/25
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mL at 280C and pH 6.0. The amount of Cd present in the Puranik and Paknikar76 demonstrated that
solution decreased with Cd resistant isolates Pseudomonas Streptoverticillium cinnamoneum biomass was effective as a
spp 11a, Arthrobacter spp D9, Pseudomonas spp H1 and biosorption substrate for Pb and Zn.
Bacillus spp H9, with growth from 104 to 106 CFU/mL.
Most dramatic decrease in the levels of soluble Cd were seen Heavy metal ions in the fungal cell interfere with the
with Bacillus spp H9 and Pseudomonas strain H1, such that individual reactions and metabolic processes in the cell.
an average 36% was lost with growth. Growth of When the heavy metal ions are present in high
Arthrobacter spp D9 and Pseudomonas spp 11a resulted in concentrations, it is toxic to the fungal cell and also growth
22% and 11% decrease in soluble Cd respectively.68 rate decreases and this is often accompanied by changes in
the mycelium. These changes could be in the colour e.g.
Bacteria isolated from environmental samples displaying Tramestes versicolor produces a brown pigment in the
resistance to heavy metals have been studied for their presence of Cd due to the stress; Schizophyllum commune
performance in the bioremediation processes. Cupriavidus normally has a creamy mycelium but in the presence of Pb
metallidurans CH34 has been shown to recover heavy changes to black mycelium.71
metals from polluted soils and water. This strain has the
capacity to accumulate selenium (Se), gold (Au) and to Heavy metals are toxic to fungi, because of their role as
volatize Hg through reactive processes.57,69 Pseudomonas enzyme inhibitors and protein denaturing agents.53 Heavy
stutzeri isolated from foundry soil was shown to be resistant metals like Hg bind to SH groups that are responsible for the
to the toxic effect of chromium up to 1mM.70 The interest in regulation of enzyme sites causing irreversible inactivation.
heavy metal uptake by bacteria has increased in recent years, In contrast, Cd has the capacity to bind aromatic amino acids
especially because of the biotechnological potential of residue in enzyme formation and cause oxidation damage to
bacteria in the removal or recovery of metal ions protein.77 Heavy metals interfere with reproduction of many
contaminants.65 fungi where the spore formation and germination are very
sensitive when compared with mycelia growth.71,78
Fungi in Bioremediation: Some heavy metals are essential
for the fungal metabolism, while others do not have any Fungi have developed some resistant mechanisms against
known role in their cell metabolism such as Cd and Pb. toxicity of heavy metals. The first line of defense is
When in excess, essential and non-essential metals become immobilization by means of extracellular and intracellular
toxic and this toxicity could be many times greater than chelating compounds. Heavy metals can be chelated by
required.71 Heavy metal ions present in the environment can small peptide like phytochelatins or metallothioneins.71,73
interact with extracellular enzymes of fungi which can cause Another type of metal binding compound called melanin,
a physiological response to heavy metals and that leads to has been found to be associated with fungi cell wall. Melanin
the uptake of metal by the fungi. and related proteins are able to absorb some metal ions.75,79
The metals uptake systems are usually present in the cell The relationship of heavy metal and fungi is not yet fully
membrane. Heavy metals can be co–transported with understood, but experiments made with some
calcium (Ca). At a subcellular level 50% of the metal is Basidiomycetes have given promising results. The cell wall
bound to the cell wall, 30% stays in the cytoplasm and the of fungi mainly composed of polysaccharide and peptides
remaining 20% is transported to vacuole. Studies with that have good capacity for heavy metal binding.71 Fungi are
Aspergillus niger have shown that Cd uptake involves a good alternative for the removal of toxic heavy metals from
rapid binding to the cell wall and carrier mediated transport the environment; they are more tolerant to heavy metals than
slowly into the cell.72 Fungi can also take a preventive bacteria.80,81
approach to reduce the uptake of heavy metals; this involves
the reduction in the availability of heavy metals through Dead cells of fungi accumulate metal ions to equal or even
various extracellular precipitation and complexation greater extent than living cells. This is because cell surface
strategies, which could also enhance impermeability to is ionic due to the presence of ionized groups in the cell
heavy metals. polymers attracting heavy metals. Ion – exchange is believed
to be the principal mechanism for metal uptake.82 Waste
Fungi cell wall contains basically cellulose, chitin, glucan biomass is readily available from industry (penicillin
and mannan; in addition to this cell wall of fungi is production). The use of dead fungal biomass eliminates any
composed of protein, lipids, pigments and polyphosphates.73 nutrient requirement.
Passive uptake of heavy metal may occur on to the cell wall
components, without any type of metabolic control.74 Metal Tolerance Mechanisms: Resistance mechanisms to
Similarly to what happens in the bacteria, it is supposed that toxic metals are known to exist as metal resistance in
functional groups like phosphoryl, carboxyl and hydroxyl, bacteria and fungi is controlled by resistance genes that are
may be involved in this mechanism known as found on their chromosomes, plasmid and transposons.
biosorption.63,75 Biosorption using fungal biomass seems to Although plasmid mediated resistance is most common, yet
be very promising methods for the removal of metal ions. other system of resistance has also been documented e.g.83
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Res. J. Biotech
mercury resistance in Bacillus spp, cadmium efflux by p– Besides different advantages, physico-chemical techniques
type ATPase also Bacillus spp and arsenic efflux in E. coli have also some major disadvantages due to which they are
and chromosomal metal resistance system.84 still not seen as permanent answers for the treatment of
heavy metals from industries.94
There are considerable evidences that microbes can rapidly
adapt to the toxic metals by altering their chemistry and Biological Techniques: Biological techniques for the
mobility.85,86 The mechanism of resistance includes metal removal of heavy metal wastes are based on microbial
reduction or transformation to more volatile or less toxic biotransformation of the heavy metal compounds. Many
forms. Some bacteria such as Pseudomonas spp, Clostridium researchers have demonstrated partial or complete
spp and E. coli enzymatically reduce Hg2+ to Hg0 which is biodegradation of metal ions by pure and mixed cultures of
highly volatile and diffuses away from the bacteria. Also bacteria, fungi and algae. In the 1950s, there was a strongly
some bacteria like Alcaligens faecalis can reduce the held view amongst microbiologists often called the
oxidation state of AsO2- to AsO43-, which is less toxic; the principles of microbial infallibility that all chemicals were
same is with Pseudomonas florescens which reduces CrO4 susceptible to microbial degradation if the right organisms
to Cr(OH)3. Microbes secrete inorganic metabolic products and conditions could be provided. The growing realization
such as sulphide, carbonate or phosphate ions in their that chemicals like dyes and metal ions, which find their way
respiratory metabolisms and precipitate toxic metal ions as into the environment, were not being degraded and were
form of non- enzymatic detoxification along with these persisting for many years, put an end to such thinking.95
products.
Microorganisms are capable of resisting and surviving in
In nature, microbes immobilize metals through cellular polluted environment and provide the knowledge for
sequestration and accumulation or through extracellular bioremediation. This natural process bioremediation
precipitation.87 Chelating and complexion of metal species includes bioengineering of capabilities of intrinsic micro-
with media components and organisms induced pH changes organisms and to clean up the environment, is an effective
can also contribute to the metal tolerance. Chromate alternative to conventional remediation methods.96
tolerance is also achieved through methylation, reduction
and precipitation at the cell surface.88 In addition to that it Different mechanisms supposed to be involved in the
blocks the cellular uptake by altering the uptake pathway and bioremediation of heavy metal ions, textile dyes and related
removal from cytoplasm by efflux pumps. In many cases xenobiotic chemicals are: biodegradation by direct and
these responses appear to be plasmid mediated.89 indirect extracellular enzymes.97,98 Sometimes, a single
biological mechanism of an organism may work out for the
Cadmium binds to sulfhydryl group on essential proteins, remediation of any chemical or at times a combination of any
thus interfering with important cellular functions.90 It can of the aforementioned mechanisms in different organisms
also cause single – stranded breakage of DNA in E. Coli.91 can go along together in series.99
Two cadmium plasmid mediated resistance efflux system,
that is cad in Staphylococcus aureus and czc in Bacteria have the ability to degrade most naturally occurring
Acinatobacter eutrophus are well characterized and compounds as well as manufacturing new ones. They are
documented.90,92 The system czc system also confers usually involved in the stimulation of indigenous microbes
resistance to zinc and cobalt. Another system confers to reduce or eliminate contaminants, especially heavy metals
resistance to zinc and cobalt that chromosomally encoded is and azo dyes. Researchers have examined soils
known to exist. Cadmium resistance genes located on the contaminated with Cr6+ in which they found bacterial species
transposon have been reported in Listeria monocytogenes.93 capable of catalyzing reduction of Cr6+ to Cr3+, which is less
Mercury resistance is widely distributed among gram toxic and less soluble form of chromium.87
positive and gram-negative bacteria.
Metal ions adsorption is accomplished by bacterial/surface
Convectional Techniques for Remediation: There are membrane and their subsequent binding due to dissociation
different conventional methods of removing wastes of protons from carboxyl and phosphoryl group which
including membrane filtration, coagulation/flocculation, constitute the cell wall macromolecules. Bacterial cell wall
precipitation, flotation adsorption, ion exchange, ion pair is known to serve as template for nucleation and growth of
extraction, ultrasonic mineralization, electrolysis, advanced metal precipitate.85,100 Metal adsorption tends to reverse the
oxidation (chlorination, bleaching, ozonation and photo negative charge on the bacterial cells and numerous studies
catalytic oxidation). Chemical reduction was previously have reported that the phosphoryl residues on the outer
used in the treatment of different industrial effluents. These membrane of bacterial cells are the most likely binding sites
physico-chemical techniques are of great values specifically for metals for most of gram-negative bacteria.101 The
when effluents from industries contain chemical compounds negative charge groups (carboxyl, hydroxyl and phosphoryl)
hazardous to biological resources like bacteria and fungi of the bacterial cell wall adsorb metal cations which further
which play a vital role in nourishing other biotic resources get mineral nucleated.102 Surfactants such as rhamnolipid
by providing basic nutrient in soil and water. produced by Pseudomonas aeruginosa show specificity for
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Res. J. Biotech
certain metals such as Cd and Pb. Higher molecular weight complexes between ions and extracellular enzymes.116 Also
(~ 106) bioemulsifiers such as emulsan can also aid in metal fungi can absorb heavy metals such as Cr, Ni and Fe in the
removal.103 Studies of Sand et al104 revealed that effluents of steel foundry by using Aspergillus terreus in
Thiobacillus ferroxidans and Leptospirillum ferroxidans are polyurethane foam.
capable of oxidizing iron and sulphur. Also, Joerger et al105
reported that metal accumulating bacterium Pseudomonas Factors affecting biosorption
stulzeri AG 259 is capable of producing silver based single A number of physical and chemical factors are known to
crystal which can reduce the toxicity of metal. affect biosorption of heavy metals by microbes.
However, metal oxyanion such as arsenate, selenate do not Effect of pH: Biosorption is an analogue of ion exchange
bind to the electropositive sites on the bacterial surface or process; pH of aqueous solution influences the binding of
through metal ligands bridging. Bioremediation of these metal to the biomass. Many researchers have studied the
anions is predominantly based on microbial–catalyzed redox effect of pH on heavy metal ion uptake. Biosorption of metal
conversions to insoluble forms. The rate of these reactions is ions and dyes has been observed as a pH dependent process.
largely dependent on the enzyme activity and biomass It seems to be a very important factor in the biosorption
concentration.15 process. It affects the solution chemistry of the metal, the
activity of the functional group in the biomass and
Numerous researchers have identified several bacterial competition of metallic ions.117 The pH strongly influences
species capable of bioremediation such as Acinetobacteria the speciation and biosorption availability of the metal
calcoaceticus, Aureobacterium esteroaromatium, Klebsiella ions.118
oxyloca, Bacillus licheniformis, Pseudomonas stulzeri,
Pseudomonas aeruginosa, Escherichia coli, Aeromonas and The uptake of Zn, Cd and Pb by mycelium of Penicillium
Micrococcus species.106-108 chrysogenum was highly pH-sensitive and inhibited below
pH 3. It was shown that removal of Pb from aqueous solution
Fungi are capable to remove heavy metal ions from by the same organism was strongly affected by pH. Its dried
contaminated sites, especially from industrial effluents in biomass showed maximum uptake of Pb (116 mg/g) within
substantial quantities.109 It is also used in the bioremediation a pH range of 4 to 5.
of heavy metal contaminants from landfills. Fungi are
recognized for their abilities to produce a large variety of Effect of temperature: Temperature seems to affect
extracellular proteins, enzymes and other metabolites and for biosorption only within the range from 20 to 35 °C.120 Due
their capabilities to adapt to severe environmental to the exothermic nature of some adsorption processes, an
conditions.110 Beyond the production of such relevant increase in temperature has been found to reduce the
metabolites, fungi have been attracting in growing interest biosorption capacity of the biomass.121 Temperature changes
for their biotreatment (removal and destruction) of affect a number of factors in heavy metals biosorption, some
wastewater ingredient such as metals, inorganic nutrients of the factors include: (i) stability of the metal ion species
and organic compounds.111,112 initially placed in solution; (ii) microorganism-metal
complex depending on the biosorption sites; (iii) effect of
Fungi are well suited for uptake and removal of metals from temperature on microorganism cell wall configuration and
waste waters, because they often exhibit marked tolerance (iv) ionization of chemical moieties on the cell wall.122
towards metals and other adverse conditions such as low
pH.113 They have high capacities of metal binding to cell Higher temperature usually enhances sorption due to the
walls and may also exhibit high values of intracellular increased surface activity and kinetic energy of the solute.
accumulation. However, filamentous fungi seem to exhibit However, physical damage to the biosorbent can be expected
low rates of intracellular uptake and binding to walls and at higher temperature. It is always desirable to
other materials which is the significant component of conduct/evaluate biosorption at room temperature, as this
uptake.79 condition is easy to replicate. Kacar et al123 reported that Fe
(III), Cr (VI) and Pb (II) biosorption by Zoogloea ramigera
Ibanez and Umetsu114 have demonstrated the ability of and Rhizopus arrhizus was an endothermic process and
protonated alginate beads in removal of Chromium, Copper, increased binding occurred as the temperature was increased
Zinc, Nickel and Cobalt ions from aqueous solutions. in the range 15-35 °C. The maximum removal of Cr by
Biomass immobilized in range of inert materials like silica, powdered biomass of Rhizopus nigricans was observed at
polyacrylamide, polymethane and polysulphone have been 35°C.
used in a variety of bioreactor configurations including
rotating biological contractors, fixed reactors, trickle filters, At the temperature 30°C, Escherichia coli and Bacillus
fluidized beds and air lift bioreactors. Karna et al115 subtilis removed 63.39 % and 69.90 % Cd of (II), 68.51 %
immobilized Phormidium valderianum BDU 3050 in polyl and 67.36 % of Pb (II) while 60.26 % and 54.56 % of Cr
foam and used it for removal of Co2+, Cu2+ and Ni2+. Besides respectively. Temperature over the range 15-35 °C had no
that, fungi also have the capacity to form chemical significant effect on the biosorption capacity of Ca-alginate
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immobilized Phanerochaete chrysosporium for Hg (II) and higher concentration resulting in a low metal uptake.134 This
Cd (II).18 is because at lower initial metal concentrations, the ratio of
the initial moles of metal to the available surface area is low;
Effect of Inoculum size: The inoculum size of a biosorbent subsequently, the fractional sorption becomes independent
strongly influences the extent of biosorption. In many of the initial concentration. It is always necessary to identify
instances, lower biosorbent dosages yield higher uptakes and the maximum saturation potential of a biosorbent for which
lower percentage removal efficiencies.109,124 An increase in experiments should be conducted at the highest possible
the biomass concentration generally increases the amount of initial metal concentration. Cd (II) biosorption to non-living
solute biosorbed due to the increased surface area of the biomass of fungus Rhizopus arrhizus and green alga
biosorbent which in turn increases the number of binding Schizomeris leiblenii showed that maximum adsorption rate
sites.119 Biomass concentration in solution seems to of Cd (II) ions to microbial biomass was increased with
influence the specific uptake: for lower values of biomass increasing Cd (II) concentration up to 100-150 mg/l.
concentrations, there is an increase in the specific uptake.125
An increase in biomass concentration leads to interference Adsorption by R. arrhizus was much higher than S.
between the binding sites. Leiblenii.124 At an initial lead concentration ranging from 50
to 200 mg/l, the maximum Pb adsorption of Rhizopus
Fourest and Roux126 invalidated this hypothesis attributing olgisporus was 750 mg/g with Pb uptake capacity of 126
the responsibility of the specific uptake decrease to metal mg/g as recorded by Niyogi et al.128
concentration shortage in solution. Hence this factor needs
to be taken into consideration in any application of microbial Effect of co-ions: Industrial effluent usually contains
biomass as biosorbent. Higher uptake of cadmium was various ionic components including metal cations and
observed at lower biomass concentration of Aspergillus anions. Some studies indicated that cations and anions
oryzae, Aspergillus niger, Mucor racemosus, Penicillium additional to the ions of interest have a generally detrimental
chrysogenum and Trichoderma viride.127 The amount of Cr impact on metal accumulation.135 Usually, the biosorption
biosorbed per unit weight of biomass decreased with an capacity of one metal ion is interfered and reduced by co-
increase in concentration of Rhizopus arrhizus, R. nigricans, ions, including other metal ions and anions presenting in
A. oryzae and A. niger .128 solution; however the gross uptake capacity of all heavy
metals in solutions remains almost unchangeable.
Effect of Incubation time: The incubation time has great
importance in adsorption for the assessment of the suitability Tsezos et al136 related this to the Pearson classification of
of microbes to serve as biosorbents in a continuous flow metal ions according to the theory of hard and soft acids and
system. The biosorption consists of two phases: a primary bases (HSAB). The HSAB theory can be condensed into a
rapid phase that accounts for the major part in the total metal simple statement that hard acids prefer to associate with hard
biosorption and a second slow phase that contributes to a bases and soft acids prefer to associate with soft bases. The
relatively small part. Murugesan et al129 suggested that metal Uranium uptake by R. arrhizus was reduced in the presence
uptake increases with an increase in contact time but remains of iron and zinc. Yakubu and Dudeney137 showed that
constant after equilibrium time period. biosorption of Uranium by A. niger was substantially
reduced in the presence of Cu, Zn and Fe and the preferential
Equilibrium time varied with heavy metal ions due to the order for biosorption was Fe > U > Cu > Zn.
difference in initial metal concentration and affinity of
biosorbent for a particular metal ion. It was also noted that Consortia of Microbes in remediation of Heavy metals:
copper uptake by Bacillus circularis occurred very rapidly In bioremediation, different species which can work in
during the initial 15 min of the experiments.130 Dead cells of synergy with each other have been implicated to clean up the
Saccharomyces cerevisiae removed 40 % more uranium or contaminated sites of heavy metals as well as other organic
zinc than live cultures and biosorption rapidly reached 60 % pollutants.138 At times, pure single bacteria which can
of the final uptake value within 15 min of contact and remediate the wastewater or soil heavily polluted by heavy
uranium was deposited as fine needle-like crystals inside the metal is not feasible. Application of judicious consortium of
cells and on the outer cell surface.131 Also, Kapoor et al132 growing metal resistance cells can ensure better removal
used the fungal biomass of Aspergillus niger for removal of through combination of bioprecipitation, biosorption and
Pb, Cd and Ni from aqueous solution. The biosorption continuous metabolic uptake of metals by the combination
equilibrium for Pb and Cd was reached in 5 h and for Ni in of the organisms at contaminated sites. They have been
8 h respectively. The equilibrium time for maximum known to possess excellent capacity of metal scavenging.
biosorption of Cd (II) by Pseudomonas spp and Some bacteria and fungi strains possess high tolerance to
Staphylococcus xylosus was 30 min and 1.0 h whereas 90 various metals and may have potential applications for
min and 165 min for Cr (VI) respectively.133 removal of wastes.139
Effect of metal ion concentration: The low metal Microbes exhibit positive (commensalism, synergism and
concentration seems to have impact on biosorption with a mutualism) interaction that results in growth, survival and
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metabolism, which are essential for bioremediation. First, in process.146 A number of studies have highlighted the
commensalism contaminants are co-metabolized, in which potential of inexpensive adsorbents prepared from an
microbes transform the contaminants without being able to agricultural by product. In the investigation of capacity of
use the energy derived from the metabolism to support adsorption using different inexpensive materials from
growth.140 Co-metabolizing microbes may interact with agricultural by products which are rice husk, wheat straw
other community members’ through commensalism, to and saw dust to remove Cadmium from aqueous solutions.
produce co-metabolites which can serve as substrates for It was found that the rice husk had the maximum adsorption
other microbes. Co-metabolism is predominant mechanism capacity of Cd.147,148.
for the transformation of many substrates. These approaches
have advantages to reduce the length of time of degradation Also, Agave sisalana (sisal fibre) was used as biosorbent of
for the contaminant.141 Pb and Cd from wastewater.149 In addition, adsorption of Ni
(II) ions from effluent of electroplating industry was studied
Secondly, in consortium there is a synergism in which using Yarrowia lipolytica and rice husk.150
microbes interact with each other, so that they benefit from
one another by supplying nutrients for their needs. Biomass, Rice husk and Wheat straw in Bioremediation:
Syntrophism is common in anaerobic microbial Agricultural wastes such as rice husk, wheat straw and saw
communities, possibly due to the small enthalpy changes dust were used in removing heavy metal from wastewater.
associated with most anaerobic bioconversions.141 The Cost is an important parameter for comparing the sorbent
metabolic end products with high free-energy content create materials, in which the agricultural wastes are very cheap
a niche for other organisms to exploit and this can result in and easily available. In general, an adsorbent can be termed
community succession. Microbial interaction can have a as low-cost adsorbent, if it requires little processing, it is
thermodynamic basis as in anaerobic microbial consortia abundant in nature or as by product or as waste materials
that transfer hydrogen. Interspecific hydrogen transfer form from other industry.146
the basis for syntrophic interaction e.g. metabolism of 3-
chlorobenzoate.90 Also, competitions occur within microbes Rice husk is an agricultural waste material generated in rice
for the available of nutritional and physical resources. producing countries. Dry rice husk contains 70-85% organic
matter (lignin, cellulose, sugar etc.) and silicon. Rice husk
Due to the competition, the expected bioconversion does not has been studied as good adsorbent of pollutants.151 Batch
occur, even though the relevant degradative microbes were studies using tartaric acid modified rice husk have been
found in the environment. The dominance of one species carried out for the removal of Pb and Cu with effects of
over another can be due to its faster growth rate under various parameters such as pH, initial concentration of
imposed selection pressure or its greater affinity for a adsorbent particle size and temperature.152
substance, nutrient or physical resource. An understanding
of the community structure is important for predicting the It was reported that rice husk is a potentially useful material
fate of contaminants in the environment and for remedial for the removal of Cd, Mn, Zn, Hg and Pb from aqueous
attempts.142 solutions.153
Evidently the stage has already been set for the application The wheat straw is an agricultural by product, as it consists
of growing microbial cells for heavy metal ions removal and of the dry stalks of cereal plant after the grain and shaft have
efforts directed towards cell process development to make been removed. Straw makes up about half of the yield of the
this option technically/economically viable for the cereal crops such as barley and wheat. In addition, straw
comprehensive treatment of effluent or soil that is contains alkaloids, flavonoids, lignin, phenol and steroids.
polluted.143 Wheat straw serves as a good adsorbent for Pb, Cd, Cr and
Hg which also depend on the pH and initial concentration.154
Agricultural Biomass as Biosorbent: Agricultural waste High efficiency and biosorption capacity of the wheat straw
materials are usually, composed of lignin and cellulose as have been observed as stated earlier; however, the
the main constituents.144 Other components are biosorption mechanism has been found to be quite complex.
hemicelluloses, lipids, proteins, simple sugars and starch,
water, hydrocarbons, ash etc. There are many more It comprises a number of ion-exchange mechanisms and
compounds that contain variety of functional groups present equilibrium reached at a certain time. Ayub et al155 reported
in the binding process, for example carboxyl, amino, alcohol the use of microbial organisms and certain plant derivatives
and esters.145 biomass such as wheat straw in the removal of heavy metals.
These groups assumed to have the ability to bind with heavy Saccharomyces cerevisiae was used with the wheat straw
metals by replacement of hydrogen ions for metal ion particles to remove 65.23% of Cd.156 More recently, authors
solutions. Many researchers showed the relation between the investigated the use of microbial consortium in the
presence of various functional groups and their bioremoval of heavy metals especially cadmium from
complexation with heavy metals during biosorption wastewater.157
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Res. J. Biotech
Fig. 1: Microbial Bioremediation has been an efficient process for the removal of heavy metal contaminants.
Figure shows various positive aspects and some drawbacks associated with this process over
other physico-chemical techniques.
Conclusion 4. Khan A.G., Relationship between Chromium biomagnifications

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Future work should focus on agriculture biomass along with Congress of the Soil Science Society of Pakistan: Effluent use of
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(2000)
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