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Bioremediation of Heavy Metals From Contaminated Sites Using Potential

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IJEP 37 (1) : 65-84 (2017) (Received on August 12, 2016)

Bioremediation of Heavy Metals From Contaminated Sites

Using Potential Species: A Review
Krishna Kumar Yadav, Neha Gupta, Vinit Kumar and Jitendra Kumar Singh
Bundelkhand University, Institute of Environment and Development Studies, Jhansi- 284 128

Heavy metals in wastewater, soil and sediment is a major concern of environmental pollution.
A wide range of organic and inorganic compounds causes contamination. Heavy metals are major
component of inorganic contaminants and cannot be degraded. The cleanup of such type of
contaminants from environment usually requires their removal. Several conventional technologies
have already been used for their removal but most of them are cost effective and not successful
to get optimum results. Currently, a vast array of biological materials, especially bacteria, algae,
yeasts and fungi have received increasing attention for heavy metal removal and recovery due
to their good performance, low cost and large available quantities. In view of this, the paper
reviews deeply about bioremediation technology and mechanism of heavy metal uptake by
microorganisms. It also provides sources and effects of various heavy metals on plants and human
health. Some potential species of microorganisms and plants which are commonly used for heavy
metal removal are also reported.
contamination of our ecosystem. A wide range
KEYWORD of inorganic and organic compounds cause con-
Contamination, Microorganism, Remediation, tamination, these include heavy metals, com-
Removal, Heavy metal. bustible and putriscible substances, hazardous
wastes, explosives and petroleum products.
INTRODUCTION Major component of inorganic contaminants
are heavy metals and pose a different prob-
Environmental pollution with heavy metals is lem than organic contaminants (Ghosh and
increasing day by day due to urbanization and Singh, 2005).
industrialization (Mythili and Kartikeyan, 2011)
and become a major global concern because Heavy metals are considered one of the most
of its toxicity and threat to human life and en- common and hazardous pollutants having a
vironment. Heavy metals are present in soil specific density of more than 5 g/cm 3. Met-
and aqueous streams as both natural compo- als, like copper, iron, manganese, zinc are es-
nents or as a result of human activity (Banik sential for life processes whereas others, like
et al., 2014; Raskin et al., 1994). Human ac- cadmium, nickel and mercury have no physi-
tivities create waste and these wastes are ological function but often results in harmful
handled, stored, collected and disposed of, disorders at a higher concentration (Lenin et
which can pose risks to the environment and al., 2014). Heavy metals may enter the hu-
to public health (Gupta et al., 2015; Saxena man body through inhalation of dust, direct in-
et al., 2010; Zhu et al., 2008). Controlled and gestion of soil and consumption of food plants
uncontrolled disposal of waste, accidental and grown in metal contaminated soil (Bigdeli and
process spillage, mining and smelting of met- Seilsepour, 2008; Dudka and Miller, 1999;
alliferous ores, sewage sludge application to ag- Hawley, 1985) and causes serious health haz-
ricultural soils are responsible for the migration ards. Some of the most studied cases of heavy
of contaminants into non-contaminated sites metal poisoning are, Minamata disease caused
as dust or leachate and contribute towards by mercury toxicity from contaminated fish in

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Table 1. Worldwide emissions of trace metals to
the atmosphere (in thousand tonne per year)
(Clark, 2001).
Metal Natural Anthropogenic
source source
Cadmium 1.3 7.6
Copper 28.0 35.0
Nickel 30.0 56.0
Lead 12.0 332.0
Zinc 45.0 132.0
Arsenic 12.0 18.0
Japan, Itai Itai disease due to elevated dietary
cadmium in rice in the Jinzu river basin in
Japan as a result of pollution from the waste
of a zinc ore, most recent case of general ar-
senic toxicity in Bangladesh due to contaminated
groundwater (Bandara, 2011).
Metal-contaminated sites are notoriously hard to
remediate (Lasat, 2000). Remediation methods,
such as excavation and landfill, thermal treatment,
acid leaching and electro reclamation are not suit-
able due to their high cost, low efficiency, large
destruction of soil structure and fertility and high
dependence on the specific conditions of the con-
tamination, soil properties, site condition and so
on. In light of this, the development and applica-
tion of the more broadly-applicable bioremediation
techniques for heavy metal contamination are
necessary (Banik et al., 2014). Bioremediation is
an option that offers the possibility to destroy or
render harmless various contaminants using natural
biological activity (Vidali, 2001). Compared to
other methods, bioremediation is a more promis-
ing and less expensive way for cleaning up con-
taminated soil and water. At present,
bioremediation is the most effective management
tool to manage the polluted environment and re-
cover contaminated environment (Ahemad, 2012).
Bioremediation uses biological agents, mainly
microorganisms, such as yeast, fungi or bacteria
to clean up contaminated soil and water (Kumar
et al., 2011; Strong and Burgess, 2008). In
bioremediation process, microorganisms use the
contaminants as nutrient and energy sources
(Kumar et al., 2011; Tang et al., 2007; Agarwal,
1998; Hess et al., 1997).
66 INDIAN J. ENVIRONMENTAL PROTECTION, VOL. 37, NO. 1, JANUARY 2017
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SOURCES OF HEAVY METAL POLLUTION
Metals are natural elements in the environment
but many anthropogenic sources increase metal
concentration in the atmosphere (Table 1). As a
result over recent decades, an annual worldwide
release of heavy metals reached 22,000 tonne
for cadmium, 9,39,000 tonne for copper,
7,83,000 tonne for lead and 13,50,000 tonne for
zinc (Singh et al., 2003). Heavy metals can be
emitted into the environment by both natural and
anthropogenic sources. The major causes are
anthropogenic sources such as mining (Kpan et
al., 2014; Modoi et al., 2014; Cobbina et al., 2013;
Dhakate and Singh, 2008; Mishra et al., 2008;
Bidone et al., 2001), smelting procedures (Kapusta
and Sobczyk, 2015; Asami, 1988; Whitby and
Hutchinson, 1974), industrial activities, like chemi-
cal and metallurgical industries (Nakayama et al.,
2010; Cortes et al., 2003), cement industry (Al-
Khashman et al., 2006; Isikli et al., 2003;
Schuhmacher et al., 2002), electroplating, plas-
tics manufacturing, transports, pesticides, fertil-
izers (Bolan et al., 2005) and agriculture
(Vaalgamaa and Conley, 2008). Long range trans-
port of atmospheric pollutants also adds the metal
concentration in the natural environment (EEA,
1995).
EFFECT OF HEAVY METAL
Pollution of the natural environment by heavy metal
is a worldwide problem because these metals are
indestructible and most of them have toxic ef-
fects on living organisms, when they exceed a
certain concentration (Ghrefat and Yusuf, 2006).
Concentrations of several toxic metal and metal-
loids have been largely increased as a result of
human activities. They can disturb important bio-
chemical processes, constituting an important
threat for the health of plant and animals. Plants
and animals absorb these elements from soils,
sediments and water by contact with their exter-
nal surfaces, through ingestion and also from in-
halation of airborne particles and vapourized met-
als (Mudgal et al., 2010a; Madaan and Mudgal,
2009).
Heavy metal toxicity in plants has an inhibitory
effect on growth, enzymatic activity, stomata
function, photosynthesis activity, accumulation
of other nutrient elements and root system (Addo
Table 2. Main effect of heavy metal on plant
Heavy Effect Reference
metal
Cadmium Alter the uptake of minerals, reduces microbes Moreno et al., 1999; Haghiri,
population in soil, iron deficiency, phosphorous 1974; Godbold and Hutterman,
deficiency or reduce Mn transport, reduces nit- 1985; Hernandez et al., 1996
trate absorption and transportation from roots
to shoots
Copper Inhibits plant growth, interfere with cellular Yruela, 2005
process, such as photosynthesis and respiration,
reduces biomass and shows chlorotic symptoms
Nickel Inhibits growth and development, induces leaf Chen et al., 2009
chlorosis, necrosis and wilting, disrupted photo-
synthesis and reduces yield
Lead Decreases germination percentage, length and Ghani, 2010
dry mass of root and shoots, disturbed mineral
nutrition, reduction in cell division
Zinc Inhibits metabolic functions results in retarded Fontes and Cox, 1998
growth and senescence, limits the root and
shoot growth, chlorosis
Chromium Reduces germination percentage and bud Shanker et al., 2005
sprouting, decreases root, shoot and leaf
growth, reduces yield and dry matter production
Mercury Interferes the mitochondrial activity and indu- Messer et al., 2005
ces oxidative stress by triggering the genera-
tion of reactive oxidative species
(ROS) resulting disruption of biomembrane
lipids and cellular metabolism
Cobalt Decreases shoot growth and biomass, restricts
concentration of iron, chlorophyll and protein Nagajyoti et al., 2010
Manganese Reduces photosynthetic rate, necrotic brown
spotting on leaves, petioles and stems Wu, 1994

et al., 2012). Some of the metals, like zinc (Zn),
copper (Cu), manganese (Mn), nickel (Ni) and
cobalt (Co) are micronutrients, essential for plant
growth (Marschner, 1995) while others, like cad-
mium (Cd), lead (Pb) and mercury (Hg) have no
known biological function and very toxic even at
lower concentration of 0.001-0.1 mg/L (Alkorta
et al., 2004; Wang, 2002; Volesky, 1990). Food
chain polluted with toxic metals and metalloids is
an important route of human exposure and may
cause several dangerous effects on human
(Mudgal et al., 2010b). Main effects of some
heavy metals on plants and human health are
given in tables 2 and 3, respectively.
REMOVAL TECHNIQUES OF HEAVY METAL
Several heavy metals removal technologies
including chemical precipitation, ion exchange, ad-
sorption, ultrafiltration, reverse osmosis, electrodi-
alysis, coagulation/flocculation and flotation
are commonly used in industries. However,
these technologies are becoming uneconomical
and unfavourable to remove heavy metals from
contaminated sites. Description and disadvantages
of these treatment technologies are presented in
table 4. Use of microorganisms and plants for
remediation purposes is thus a possible solution
for heavy metal pollution since it includes sus-
tainable remediation technologies to rectify and
re-establish the natural condition of soil (Doelman
et al., 1994).
BIOREMEDIATION OF HEAVY METAL

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Table 3. Effect of some heavy metal on human health
Heavy EPA Toxic effect Reference
metal regulatory
limit, ppm
Cadmium 5.0 Carcinogenic, mutagenic, endocrine Salem et al., 2000;
disruptor, lung damage and fragile Degraeve, 1981
bones, affects calcium regulation in
biological systems
Copper 1.3 Brain and kidney damage, elevated le- Wuana and Okieimen,
vels result in liver cirrhosis and chronic, 2011
anemia stomach and intestine irritation
Nickel 0.2 Allergic skin diseases, such as itching, Duda-Chodak and
(WHO cancer of the lungs, nose, sinuses, Blaszczyk, 2008; Khan
permissible throat through continuous inhalation, et al., 2007
limit) immunotoxic, neurotoxic, genotoxic,
affects fertility, hair loss
Lead 15 Excess exposure in children causes Wuana and Okieimen,
impaired development, reduced 2011; Padmavathiamma
intelligence, short-term memory loss, and Li, 2007
disabilities in learning and coordination
problems, risk of cardiovascular disease
Zinc 0.5 Dizziness, fatigue, etc. Hess and Schmid, 2002
chromium 0.1 Nose ulcers, runny nose, breathing Salem et al., 2000
problems, such as asthma, cough,
shortness of breath, or wheezing
and hair loss
Mercury 2.0 Autoimmune diseases, depression, Gulati et al., 2010;
drowsiness, fatigue, hair loss, insomnia, Neustadt and Pieczenik,
loss of memory, restlessness disturbance 2007
of vision, tremors, temper outbursts,
brain damage, lung and kidney failure
Arsenic 0.01 Affects essential cellular processes, Tripathi et al., 2007
such as oxidative phosphorylation and
ATP synthesis
Silver 0.10 Exposure may cause skin and other ATSDR, 1990
body tissues to turn gray or blue-gray,
breathing problems, lung and throat
irritation and stomach pain.
Barium 2.0 Cause cardiac arrhythmias, respiratory Acobs et al., 2002
failure, gastrointestinal dysfunction,
muscle twitching and elevated blood
pressure
Selenium 50 Dietary exposure of around 300 g/day Vinceti et al., 2001
affects endocrine function, impairment
of natural killer cells activity, hepatoto-
xicity and gastrointestinal disturbances

The utilization of organisms, primarily microbes, rapidly changing and expanding area of environ-
to cleanup contaminated soils, aquifers, sludges, mental biotechnology, that offers a potentially
residues and air, known as 'bioremediation', is a more effective and economical clean-up technique

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Table 4. Treatment methods used in removal of heavy metal
Treatment Process detail Disadvantage
Chemical Precipitation of metal ions is achieved by the Sludge generation, extra
precipitation addition of coagulants, such as alum, lime, iron operational cost for sludge
salts and other organic polymers disposal
Ion exchange Metal ions from dilute solutions are exchanged High cost, partial removal of
with ions held by electrostatic forces on the certain ions
exchange
Adsorption Molecular or atomic film is formed by accumu- Chemical regeneration re
lation of gas or liquid solute on surface of an quirement, fouling and cor-
adsorbent rosion of plant, disposal of
exhausted adsorbent
Ultrafiltration Membranes having pore sizes 0.1 to 0.001 Membrane fouling, produc
micros are used for the removal of metal ions tion of polluted water (from
backwashing)
Reverse Metal ions are separated by a semi-permeable High power consumption due
osmosis membrane at a pressure greater than osmotic to pumping pressure, resto-
pressure caused by the dissolved solids ration of membranes
Electrodialysis Metal ions are separated by the use of semi- High operational cost due to
permeable ion selective membranes. An elec- membrane fouling and en-
trical potential between the two electrodes ergy consumption
causes a separation of cations and anions thus
cells of concentrated and dilute salts are formed
Coagulation/ Coagulant is added to the water which encour- High operational cost due to
flocculation ages colloidal material to join together into chemical consumption incre-
small aggregates called ‘flocs’. Suspended ased sludge volume gen-
matter is attracted to these flocs eration
Flotation Bubble attachment is used to separate solids High initial capital cost, high
or dispersed liquid phase maintenance and operation
cost

than conventional physico-chemical methods
(Garbisu and Alkorta, 2003). Bioremediation is an
option that offers the possibility to destroy or ren-
der harmless various contaminants using natural
biological activity (Vidali, 2001). Bioremediation
techniques are more beneficial than traditional
methods because it can be implemented on site,
thus reducing risks for personnel. Effluent volume
generated by bioremediation is much smaller re-
ducing the problem of sludge disposal. Addition-
ally, since the technology is based on natural pro-
cesses, the public considers it more acceptable
and green than others. Bioremediation of heavy
metals can be done using bacteria, fungi, algae
and plants. The remediation of heavy metals us-
ing plants is phytoremediation.
MECHANISM OF HEAVY METAL TOXICITY
Organisms respond to heavy metal stress using
different defense systems, such as exclusion,
compartmentalization, formation of complexes
and synthesis of binding proteins, like
metallothioneins and phytochelatins (Rajen-dran
et al., 2003). Mechanisms of metal toxicity are
generally agreed to be a consequence of metal
ion affinity for cellular components and
biomolecules, or the stability of metal–biomolecule
complexes formed, although the consequences
are varied (Hobman and Crossman, 2014; Silver
and Hobman, 2007; Nies, 1999). At high concen-
trations, metal ions can either completely inhibit
the microbial population by inhibiting their various
metabolic activities (Figure 1) or organisms can
develop resistance or tolerance to the elevated
levels of metals (Ahmed, 2012).
MECHANISM OF METAL TOLERANCE

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Figure1. Heavy metal toxicity mechanism to mi-
crobes (Ahemad, 2012; Khan et al., 2009)
Generally, there are 2 types of uptake mecha-
nisms for heavy metals (Figure 2); one is indepen-
dent of cell metabolic activity and is referred to
as biosorption or passive uptake. It involves the
surface binding of metal ions to cell wall and ex-
tracellular material. The second mode of metal
uptake into the cell across the cell membrane is
dependent on the cell metabolism and is referred
to as intracellular uptake, active uptake or
bioaccumulation. The first mode is common to
metal adsorption by both living and dead cells;
the second mode, which is metabolism depen-
dent, occurs in living cells (Kapoor and
Viraraghavan, 1997).
REMEDIATION OF HEAVY METAL BY BACTERIA
It is known, that microorganisms accumulate
heavy metals in polluted soil and water systems.
In order to survive in heavy-metal polluted envi-
ronments, many microorganisms have developed
means of resistance to toxic metal ions and most
microorganisms are known to have specific genes
for resistance to toxic ions of heavy metals.
Mostly, the resistant genes are found on plas-
mids or on chromosomes (Nies, 1999). Bacteria
are the most abundant and versatile of microor-
ganisms and constitute a significant fraction of
the entire living terrestrial biomass of ~1018 g
(Mann, 1990). Bacteria were used as biosorbents
because of their small size, their ubiquity, their
ability to grow under controlled conditions and
70 INDIAN J. ENVIRONMENTAL PROTECTION, VOL. 37, NO. 1, JANUARY 2017
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Figure 2. Mechanism of microbial metal tolerance
(Rajendran et al., 2003)
their resilience to a wide range of environmental
situations (Urrutia, 1997). Table 5 lists out the
name of some bacteria which may be used for
bioremediation in heavy metals contaminated en-
vironment. They can remove heavy metals from
contaminated sites either by bioaccumulation, pre-
cipitation or biosorption.
REMEDIATION OF HEAVY METAL BY FUNGI
Microorganisms including fungi have been reported
to exclude heavy metals through bioaccumulation
and biosorption at low cost and in eco-friendly
way. Like bacteria, some fungi could also be a
good alternative for removal of toxic heavy met-
als from the environment even more when it is
suggested that fungi are more tolerant of heavy
metals as a group than bacteria (Rajapaksha et
al., 2004). It has been found that some of the
fungal species are typically associated with heavy
metal rich area and considered as hyper accumu-
lators of heavy metals (Purvis and Halls, 1996).
Alternatively, fungi can be exposed to heavy
metals from the atmosphere and are very well
known for biomonitoring studies focused on heavy
metal pollution (Garty, 2001).
Fungi offer a wide range of chemical groups that
can attract and sequester the metals in biomass.
Cell walls are composed of structural polysaccha-
rides, proteins and lipids that offer metal-binding
functional groups (Veglio and Beolchini, 1997). Many
Table 5. Potential bacteria used for heavy metal remediation
Potential bacteria Heavy metal Reference
Aeromonas caviae Cd, Cr (IV) Loukidou et al., 2004
Alcaligenes eutrophus Cd Mahvi and Diels, 2004
Aphanothece halophytica Zn Incharoensakdi and Kitjaharn, 2002
Bacillus coagulans, Bacillus Cr (IV) Srinath et al., 2002
megaterium
Bacillus firmus Pb, Zn, Cu Salehizadeh and Shojaosadati, 2003
Bacillus licheniformis, Escherichia
coli, Pseudomonas fluorescens, Cd, Pb, Zn Basha and Rajaganesh, 2014
Salmonella typhi
Bacillus licheniformis Cu, Cr, Fe Samarth et al., 2012
Bacillus licheniformis Cr (IV) Zhou et al., 2007
Bacillus subtilis, Micrococcus Cu Nakajima et al., 2001
luteus, Pseudomonas stutzeri
Bacillus thuringiensis Cr (IV) Sahin and Ozturk, 2005
Bacillus thuringiensis Ni Ozturk, 2007
Corynebacterium glutamicum Pb Choi and Yun, 2004
Nostoc muscorum Cr (VI) Gupta and Rastogi, 2008
Ochrobactrum anthropi Cd Ozdemir et al., 2003
Pseudomonas aeruginosa Cu Kazy et al., 2002; Chang and Chen, 1999
Pseudomonas aeruginosa Pb Lin and Lai, 2006; Chang and Chen, 1999
Pseudomonas cepacia Cu Savvaidis et al., 2003
Pseudomonas putida Pb, Cu Uslu and Tanyol, 2006; Pardo et al., 2003
Sphaerotilus natans Cu Beolchini et al., 2006
Sphingomonas paucimobilis Cd Tangaromsuk et al., 2002
Staphylococcus xylosus Cd, Cr (IV) Ziagova et al., 2007
Streptomyces coelicolor Cu Ozturk et al., 2004
Streptomyces pimprina Cd Puranik et al., 1995
Streptomyces rimosus Fe (III) Selatnia et al., 2004
Streptoverticillium cinnamoneum Zn Puranik and Paknikar, 1997
Thiobacillus ferrooxidans Zn Liu et al.,, 2004; Celaya et al., 2000
Zoogloea ramigera Cr (IV) Nourbakhsh et al., 1994

researchers have used the fungal species for heavy
metal removal and obtained significant results (Table
6).
REMEDIATION OF HEAVY METAL BY ALGAE
Alike bacteria and fungi, many algae also have
immense capability to sorb metals and there is
considerable potential for using them to remove
heavy metals (Mehta and Gaur, 2005). The mecha-
nisms possible for heavy metal tolerance, stor-
age or up-take are varied depending on different
factors ranging from the anatomy of the algae
species to the environmental conditions or the
growing mediums (Benchraka, 2014). The metal
ions are adsorbed over the cell surface very quickly
just in a few seconds or minutes; this process is
called physical adsorption. Then, these ions are
transported slowly into the cytoplasm in a pro-
cess called chemisorption (Dwivedi, 2012). In
recent year, many researchers have used various
algae for removal of heavy metal from contami-
nated sites (Table 7).
REMEDIATION OF HEAVY METAL BY PLANTS
A very promising eco-friendly, cost-effective and
efficient alternative is plant based bioremediation
or phytoremediation which has already been used
for years (Gleba et al., 1999; Chaney et al., 1997;

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Table 6. Potential fungi used for heavy metal remediation
Potential fungi Heavy metal Reference
Aspergillus brasiliensis, Penicillium Cu, Mn, Zn Pereira et al., 2014
cirtinum
Aspergillus niger Pb, Cd, Cu, Ni Kapoor et al., 1999
Aspergillus niger, Aspergillus flavus Pb, Ni, Cr Dwivedi et al., 2012
Aspergillus niger, Mucor rouxii, Au Kapoor and Viraraghavan, 1997
Rhizopus arrhizus
Aspergillus terreus Ni ,Fe, Cr Dias et al., 2002
Aspergillus terreus Pb, Cd Joshi et al., 2011; Massaccesi
et al., 2002
Glicocladium roseum Cd Massaccesi et al., 2002
Mucor rouxii Pb, Cd, Ni, Zn Yan and Viraraghavan, 2001
Rhizopus arrhizus Zn Zhou, 1999
Rhizopus delemar Cu, Co, Fe Tsekova and Petrov, 2002
Rhizopus oligosporus Cd Aloysius et al., 1999
Saccharomyces cerevisiae Pb, Cd Damodaran et al., 2011
Saprolegnia delica, Trichoderma viride Zn (II), Pb (II), Ali and Hashem, 2007
Cd (II)
Talaromyces helices Cd Massaccesi et al., 2002
Trichoderma longibrachiatum Cr Joshi et al., 2011
Trichoderma viridae Cd Joshi et al., 2011

Cunningham et al., 1997; Raskin et al., 1997;
Baker et al., 1994). Phytoremediation basically
refers to the use of plants and associated micro-
organisms to partially or completely remediate
selected contaminants from soil, sludge, sedi-
ments, wastewater and ground water. It can be
used for removal of heavy metals, radionuclides
as well as organic pollutants (Dixit et al., 2015).
All plants have the ability to accumulate essen-
tial metals (Ca, Co, Cu, Fe, K, Mg, Mn, Mo, Na,
Ni, Se, V and Zn) from the soil. This ability also
allows plants to accumulate other non-essential
metals (Al, As, Au, Cd, Cr, Hg, Pb, Pd, Pt, Sb,
Te, Tl and U) which have no known biological
function (Djingova and Kuleff, 2000). Atleast 45
families have been identified to accumulate heavy
metal; some of the families are Brassicaceae,
Fabaceae, Euphorbiaceae, Asteraceae, Lamiaceae
and Scrophulariaceae. The mangrove plants have
also been reported to accumulate heavy metals
(Lacerda, 1998). Phytoremediation is not only an
aesthetically pleasing mechanism but also has
numerous advantages, like potential to reduce
remedial costs, restore habitat and cleanup con-
tamination in place rather than entombing it in
place or transporting the problem to another site
(Zynda, 2001). Some examples of heavy metal
removal using various plant species are given in
table 8.
NANOBIOREMEDIATION
Various nanoparticles have been found to be very
effective for removal of toxic metals as they
enhance the microbial activity to remove heavy
metals due to the very small size and high reac-
tivity. The fundamental properties of the material
at nano-scale may differ from that of correspond-
ing bulk material (Grover, 2012). Nano-based tech-
nologies reduce the costs of cleaning up contami-
nated sites at a large scale and the process time
as well (Dixit et al., 2015). Nanoparticles can be
synthesized using various plants and microorgan-
isms, such as bacteria, algae and fungi (Table 9).
The use of such particles to clean-up the sites
contaminated with toxic metals is called
nanobioremediation.
SUMMARY
Heavy metal pollution in water, soil and sediment
has become a major concern worldwide today.
The bioremediation process of heavy metals would
not only be economical but also eco-friendly and
sustainable to rid of the problem.
Phytoremediation is a new cleanup concept that

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Table 7. Potential algae used for heavy metal remediation
Potential algae Heavy metal Reference
Ascophyllum nodosum Au, Co Kuyucak and Volesky, 1988, 1989
Ascophyllum nodosum Ni, Pb Holan and Volesky, 1994
Chlorella vulgaris Cd, Pb Aung et al., 2013; Edris et al., 2012
Chlorella vulgaris, Spirulina maxima Cu, Zn Chan et al., 2014
Cladophora fascicularis Pb (II) Deng et al., 2007
Cladophora fascicularis Cd (II) Deng et al., 2008
Cladophora glomerata Zn, Cu Vymazal, 1990
Cladophora glomerata, Oedogonium Cu, Pb, Cd, Co Dwivedi, 2012
rivulare
Cymodocea nodosa Cu, Zn Sanchez et al., 1999
Daphnia magna As Irgolic et al.,1977
Euglena gracilis Zn Fukami et al.,1988
Fucus vesiculosus, Laminaria japonica Zn Fourest and Volesky, 1997
Garcinia cambogia As (III) Kamala et al., 2005
Micrasterias denticulata Cd Volland et al., 2012
Oscillatoria quadripunctulata, Cu, Pb Rana et al., 2013; Azizi et al., 2012;
Oscillatoria tenius Ajavan et al., 2011
Phormedium bohner Cr Dwivedi et al., 2010
Platymonas subcordiformis Sr Mei et al., 2006
Sargassum filipendula Cu Davis et al., 2000
Sargassum fluitans Cu, Fe, Zn, Ni Davis et al., 2000; Figueira et al.,1997;
Fourest and Volesky, 1997
Sargassum natans, Sargassum vulgare Pb Holan and Volesky, 1994
Scenedesmus acutus, Scenedesmus Cd, Zn Shanab et al., 2012; Cannizares-
quadricauda Villanueva et al., 2000; Travieso
et al., 1999
Spirogyra hatillensis Ni, Cr, Fe, Mn Dwivedi, 2012
Spirogyra hyalina Cd, Hg, Pb, As, Kumar and Oommen, 2012
Co
Tetraselmis chuil As Irgolic et al.,1977

involves the use of plants to clean or stabilize
contaminated environments. Many bacteria, fungi
and plant species acquired high resistance against
the well-known toxic metals providing them effi-
cient capabilities to remove high load of such
metals from contaminated media. In situ
remediation technologies, due to their easy op-
eration, low costs and fast remediation effect,
are applied widely. However, the immobilized toxic
metal still remains in soil, sediment and may be
released into water again under some special con-
ditions. Therefore, for avoiding a possible pollu-
tion of the sediment remedied, the ex situ
remediation should be advocated in future.
pared to other conventional technologies in terms
of cost and sustainability. Like other technolo-
gies, bioremediation has also its own limitation.
Several microbes cannot break toxic metals that
are biodegradable, such as chlorinated organic or
high aromatic hydrocarbons as the contaminants
are resistant to microbial attack. Future studies
should focus on involvement of interdisciplinary
approach such disciplines as engineering,
nanotechnology, microbiology, geology, ecology
and chemistry so that bioremediation could be
effective in all adverse conditions.
CONFLICT OF INTEREST

FUTURE PROSPECTIVE The authors declare no conflict of interest.

Bioremediation technology is a good option as com- FINANCIAL DISCLOSURE

INDIAN J. ENVIRONMENTAL PROTECTION, VOL. 37, NO.1, JANUARY 2017 73

© 2017 - Kalpana Corporation
Table 8. Potential plant species used for heavy metal remediation
Potential plant species Heavy metal Reference
Armeria maritime, Arrhenatherum elatius, Zn Schwartz et al., 2001
Arabidopsis hallerii
Brassica juncea Pb, Cd, Ni, Zn Kumar et al., 1995
Cu
Brassica juncea Se De Souza et al., 1999
Brassica juncea, Astragalus bisulcatus Se Dhankar et al., 2011
Brassica oleracea, Raphanus sativus, Zn, Cd, Ni, Cu, Baker et al., 1991
Thlaspi caerulescens, Alyssum lesbiacum, Pb, Cr
Alyssum murale, Arabidopsis thaliana
Eichhornia crassipes Cd Lytle et al., 1998
Elsholtzia splendens, Salix viminalis Cu Chen et al., 2005
Euphorbia cheiradenia Pb, Zn, Cu, Ni, Chehregani and Malayeri, 2007
Cd
Helianthus annuus, Agrostistenuis, Pteris As Pajuelo et al., 2008; Wu et al.,
vittata 2007; Gonzaga et al., 2006;
Trotta et al., 2006; Al Agely et
al., 2005; Cai et al., 2004
Jatropha curcas Cd, Cu, Ni, Pb Abhilash et al., 2009; Jamil et
al., 2009
Populus canescens Zn Bittsanszkya et al., 2005
Populus deltoides, Populus nigra, Cd, Cu, Pb, Zn Ruttens et al., 2011
Populus trichocarpa
Populus deltoids Hg Che et al., 2003
Potamogeton pectinatus Mn Lytle and Smith, 1995
Pteris vittata As Ma et al., 2001
Ricinus communis Cd Huang et al., 2011
Salix viminalis, Salix fragilis Cd, Cu, P, Zn Ruttens et al., 2011; Volk et
al., 2006; Pulford and Watson,
2003
Sedum alfredii Cd, Zn Yang et al., 2006, 2004; Xiong
et al., 2004
Stipa barbata, Melica jacquemontii, Fe, Zn Nouri et al., 2009
Cousinia bijarensis
Thlaspi caerulescens Cd, Zn Keller et al., 2003; Lombi et al.,
2001
Thlaspi caerulescens, Silene vulgaris Cd, Zn Brown et al., 1995
Thlaspi goesingense, Lycopersicon esculen- Ni Madhaiyan et al., 2007; Zaidi et
tom, Alyssum murale al., 2006 ; Idris et al., 2004;
Abou-Shanab et al., 2003
Trifolium alexandrinum Zn, Pb, Cu, Cd Ali et al., 2012
Verbascum speciosum Fe Nouri et al., 2009
Zea mays Cd, Pb, Zn Meers et al., 2010
Zea mays, Ambrosia artemisiifolia Pb Huang and Cunningham, 1996

The work is not supported by any grant. Abhilash, P.C., S. Jamil and N. Singh. 2009.
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Table 9. Organisms used for biosynthesis of nanoparticle
Name of organism Nanoparticle Size (nm) Reference
produced
(A) Bacteria
Marinobacter pelagius Gold 2-6 Sharma et al., 2012
Pseudomonas aerogenosa Silver 42-94 Shivakrishna et al., 2013
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(C) Plants and extracts
Acalypha indica Gold 20-30 Krishnaraj et al., 2014
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Azhadirachta indica Silver 21 Lalitha et al., 2013
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AUTHOR
1*. Mr. Krishna Kumar Yadav, Research Scholar
, Institute of Environment and Development Stud-
ies, Bundelkhand University, Jhansi-284 128.
2. Ms. Neha Gupta, Research Scholar , Institute
of Environment and Development Studies,
Bundelkhand University, Jhansi- 284 128.
3. Mr. Vinit Kumar, Assistant Professor , Insti-
tute of Environment and Development Studies,
Bundelkhand University, Jhansi- 284 128.
4. Mr. Jitendra Kumar Singh, Research Scholar,
School of Environment and Sustainable Develop-
ment, Central University of Gujarat, Gandhi Nagar-
382 030.
83
84 INDIAN J. ENVIRONMENTAL PROTECTION, VOL. 37, NO. 1, JANUARY 2017
© 2017 - Kalpana Corporation

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