Chemosphere 207 (2018) 255e266

Contents lists available at ScienceDirect

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

Review

Biosorption and biotransformation of hexavalent chromium [Cr(VI)]: A

comprehensive review
Renitta Jobby*, Pamela Jha, Anoop Kumar Yadav, Nitin Desai
Amity Institute of Biotechnology, Amity University, Mumbai-Pune Expressway, Bhatan, Panvel, Mumbai, 410206 India

h i g h l i g h t s

Chromium e its natural occurrences, its toxicity and contamination.

Chromium remediation methods and their disadvantages.

Role of biosorption and biotransformation as main mechanisms for Cr(VI).

Detailed molecular mechanism adopted by microbes in chromium detoxification.

Chromium removal methods using bacteria, fungi, algae and plants and absorbents.

Applied technologies for in situ and ex situ chromium bioremediation.

a r t i c l e i n f o a b s t r a c t

Article history: Chromium (VI) is one of the most common environmental contaminant due to its tremendous industrial
Received 13 November 2017 applications. It is non-biodegradable as it is a heavy metal, and hence, of major concern. Therefore, it is
Received in revised form pertinent that the remediation method should be such that brings chromium within permissible limits
2 May 2018
before the effluent is discharged. Several different strategies are adopted by microorganisms for Cr (VI)
Accepted 8 May 2018
Available online 9 May 2018
removal mostly involving biosorption and biotransformation or both. These mechanisms are based on
the surface nature of the biosorbent and the availability of reductants. This review article focuses on
Handling Editor: Patryk Oleszczuk chromium pollution problem, its chemistry, sources, effects, remediation strategies by biological agents
and detailed chromium detoxification mechanism in microbial cell. A summary of applied in situ and ex
Keywords: situ chromium bioremediation technologies is also listed. This can be helpful for developing technologies
Biosorption to be more efficient for Cr (VI) removal thereby bridging the gap between laboratory findings and in-
Biotransformation dustrial application for chromium remediation.
Bioremediation © 2018 Elsevier Ltd. All rights reserved.
Hexavalent chromium
Chromate reductase
Biosorbents
CONTENTS

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256
2. Natural occurrence and chemistry of chromium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256
2.1. The chromium cycle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256
2.2. Speciation of Cr . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 256
3. Toxicity of chromium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257
4. Contamination caused by chromium . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257
5. Remediation of chromium (VI) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257
5.1. Physical methods & chemical methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258
5.1.1. Disadvantages of physical and chemical treatments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258
5.2. Biological methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 258

* Corresponding author.
E-mail addresses: renitta7@gmail.com, rjobby@mum.amity.edu (R. Jobby).

https://doi.org/10.1016/j.chemosphere.2018.05.050
0045-6535/© 2018 Elsevier Ltd. All rights reserved.
256 R. Jobby et al. / Chemosphere 207 (2018) 255e266

5.2.1. Molecular mechanisms of Cr bioremediation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259

5.2.2. Bioremediation using bacteria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 260
5.2.3. Bioremediation using fungi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261
5.2.4. Bioremediation using algae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262
5.2.5. Bioremediation using plants and agro-sorbents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 262
5.2.6. Applied in situ and ex situ chromium bioremediation technologies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . 263
6. Conclusion and research lacunas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263
Acknowledgment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 263
Web references . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 266

1. Introduction Cr3þ þ 1.5MnO2 þ H2O / HCrO

4 þ 1.5Mn
2þ
þ Hþ (1)

Rapid industrialization has led to overexploitation of available C6H6O2 þ CrO24 þ 2H2O /

resources as well as unregulated disposal of industrial wastes in the 0.5Cr2O3 þ 1.5C6H4O2 þ 2.5H2O þ 2OH (2)
environment. Any metallic element with relatively high density as
compared to water and toxic even at low concentrations is termed The chemical and physical characteristic of Cr(III) and Cr(VI)
as “Heavy Metal” (Lenntech, 2004). Heavy metal pollution has found in the soil is relatively opposite, former being less mobile,
become a global issue, with severity and levels of pollution differing quite stable and almost non-toxic while the latter being mobile,
from place to place. Most of the heavy metals like Arsenic (As), reactive and toxic. Cr(VI) naturally exist in the environment due to
Cadmium (Cd), Lead (Pb), Mercury (Hg) and Chromium (Cr) are well the oxidation of Cr(III). But when increased concentration are
known for their toxicity, non-biodegradability, persistence in na- released by various industrial effluents this leads to an excess of
ture and bioaccumulation tendency (Garg et al., 2007). Out of these, Cr(VI) which is taken up in the biosphere and leads to toxicity. Fig. 1
Hexavalent chromium [Cr(VI)] has a wide range of applications in depicts the natural Cr cycle in the environment (Dhal et al., 2013).
the stainless steel industries, electroplating processes, dyes and
leather tanneries, as well as in wood preservation processes. The
2.2. Speciation of Cr
United States Environmental Protection Agency (US EPA) has
identified Cr(VI) as one of the seventeen chemicals posing a threat
Cr(VI) is dominant under oxidizing conditions while Cr(III)
to humans (McCullough et al., 1999). It enters into various envi-
predominates under reducing conditions. In aqueous solution,
ronmental systems (air, water, soil etc.) through some natural
Cr(VI) can form several species, namely, Cr2O2 2 4
7 , CrO4 , H2CrO , and
processes as well as via anthropogenic activities like mining,
HCrO 4 . This distribution depends on pH of the solution, total Cr
smelting operations, metal processing, industrial production, do-
concentration, the presence of oxidizing and reducing compounds,
mestic and agricultural use of metals etc. The effluents from most of
the redox potential and kinetics of the redox reactions. If the pH of
the industries are discharged directly into the water bodies or in
the solution is above 7, CrO2
4 is the only existing ion independent
fields without any kind of treatment, which leads to contamination
of the concentration of Cr(VI). Whereas, HCrO 4 is the predominant
and destruction of the ecosystem. Exposure to Cr(VI) causes severe
species in pH range of 1e6 (Barrera-Díaz et al., 2012; Dhal et al.,
health hazards on flora and fauna. Therefore, several research
2013).
groups throughout the world are trying to develop an efficient
technology for removal or conversion of Cr(VI) into a less toxic
H2CrO4 / Hþ þ HCrO
4 (pH ~ 1e6) (3)
form. In this review, we highlight the chemistry of Cr(VI), its
occurrence, toxicity, contamination, and various remediation
HCrO þ 2
4 / H þ CrO4 (pH > 7) (4)
methods with emphasis on bioremediation measures and use of
different biological entities such as bacteria, fungi, algae, plants as
well as agricultural wastes for bioremediation of Cr(VI).

2. Natural occurrence and chemistry of chromium

Cr is a hard, steel-gray metal found naturally in earth's crust in

form of chromite ore. It is a transition metal and belongs to group VI
in the periodic table as the first element of the group. It exists in
various oxidation states ranging from Cr(II) to Cr(VI). Among these
states, Cr(III) and Cr(VI) are most common and highly stable.
Naturally, Cr is found in all sort of environmental components
including air, water, and soil but in trace amounts.

2.1. The chromium cycle

The simultaneous oxidation and reduction of chromium is the

most remarkable fact of the chromium cycle. Cr(III) is oxidized into
Cr(VI) in soils and sediments spontaneously by manganese oxide
(MnO2) (1), While reduction of Cr(VI) to Cr(III) takes place by
various reduced soil carbon compounds (2). Fig. 1. Chromium cycle.
 R. Jobby et al. / Chemosphere 207 (2018) 255e266
2HCrO 2
4 / Cr2O7 þ H2O (5)
Since Cr(VI) is more soluble than Cr(III), the former has high
mobility in water and soil, making the uptake by prokaryotic and
eukaryotic cells more feasible.
3. Toxicity of chromium
Cr, being necessary for the normal metabolism of sugar, lipid
and proteins in mammals, becomes an essential micronutrient in
the diet of animals and humans. There is no known requirement of
Cr in metabolic pathways of plants and microorganisms. Though
high levels of Cr is always toxic, the toxicity level depends on its
oxidation state. Cr(VI) is considered highly toxic as it causes severe
ill effects on human and animal health like diarrhea, ulcers, eye and
skin irritations, kidney dysfunction and lung carcinoma (Costa,
2003; Mohanty et al., 2005). It is not only highly carcinogenic and
mutagenic but is also known to cause birth defects and decrease in
reproductive health (Kanojia et al., 1998). A Large dosage of Cr(VI)
may cause death in animals and humans. In rats, the LD50 for oral
toxicity was found to be in a range of 50e100 mg kg1 for Cr(VI) and
1900e3000 mg kg1 for Cr(III) (De Flora et al., 1990).
The main mechanism of Cr(VI) toxicity in prokaryotes as well as
eukaryotes is related to its easy diffusion across the cell membrane,
followed by reduction of Cr(VI) in cells giving rise to free radicals
that may directly cause DNA alterations and other toxic effects
(Arslan et al., 1987; Kadiiska et al., 1994; Liu et al., 1995).
Impermeability of cellular membrane to Cr(III) complexes makes
it about 10e100 times less toxic than Cr(VI). However, the intracel-
lular Cr(III) resulting from the reduction of Cr(VI), forms amino acid
nucleotide complexes, mutagenic potential of which is not fully
known (Roundhill and Koch, 2002). Prokaryotes are known to be
more resistant to Cr(VI) than eukaryotes (Kamaludeen et al., 2003).
Bielicka et al. (2005) describe the positive and negative effects of
Cr(III) and Cr(VI) on humans. The positive effects of Cr(III) play a
significant role in maintaining the blood glucose level by facilitating
the binding of insulin to cell surface receptors (Pechova and Pavlata,
2007). Also, Cr(III) play a positive role in decreasing body fat,
cholesterol and triglyceride levels, and increase in muscle mass.
Browning and Wise (2017) discovered the mechanism of carci-
nogenesis in lung carcinoma, that is induced by particulate Cr(VI). A
stable, heritable structural change in chromosome resulted in the
formation of lung carcinoma. Cr(VI) has been found to interrupt the
normal pathway of homologous recombination (HR) repair of DNA
double-strand break by changing the subcellular localization of
protein RAD51, an essential protein for HR repair mechanism. An
organism may encounter Cr(VI) from contaminated food or food
supplements, water, or air. The mean daily dietary intake of Cr is
estimated to be < 0.2e0.4, 2.0, and 60 mg, from the air, water and
food, respectively (ATSDR). Cr inhalation can cause nasal perfora-
tion, thus increasing the risk of respiratory tract diseases. Though
most reports are based on the toxic effects of Cr(VI), Cr(III) though
less toxic is also reported to cause damage to lymphocyte DNA
(Medeiros et al., 2003).
Cr(VI) is also associated with a decrease in nutrient uptake and
photosynthesis, which leads to slow growth of plants. It severely
affects several physiological, morphological, biochemical processes
and induces the generation of reactive oxygen species in plant cells.
The toxicity of Cr is indicated in form of chlorosis and necrosis in
plants (Shahid et al., 2017). Additionally, its tendency to bio-
accumulate in living tissues as it travels through a food chain in-
creases a level of concern for its removal from polluted sites
(Volesky, 1990). Kornhauser et al. (2002) reported adverse effects of
iron metabolism of tannery workers, due to excessive accumulation
of Cr in the body.
257
4. Contamination caused by chromium
Cr has tremendous industrial applications due to its corrosion
resistant quality and hardness. It is used at a large scale in various
industries including metallurgical, electroplating, tanning, wood
preservation, manufacturing of stainless steel, production of paints,
pigments, pulp, and paper (Kamaludeen et al., 2003; Baral et al.,
2006; Lu et al., 2013). Waste from these industries (e.g. sludge, fly
ash, slag, etc.) is a major source of Cr(VI) in the environment. There
has been an increase in the total Cr concentration in surface water
in major countries around the world which is extraordinarily high
from its permissible limits i.e. approximately 0.5e2 mg L1 (Shiller
and Boyle, 1987; Xingzhen and Xiuxia, 1987). The total chromium
content upto 84 mg L1 and 0.2e44 mg L1 have been found in sur-
face water of USA (US EPA, 1987) and Central Canada (Guidelines for
drinking-water quality, World Health Organization,1996) respec-
tively. Industrial wastes are commonly used as a fill material at
numerous locations to reclaim marshlands, for tank dikes, and for
backfill at sites, following demolition. Leaching and seeping of
Cr(VI) from the contaminated soil into the underground water raise
the concentration of Cr(VI), which poses a considerable health
hazard. There have been reports of up to 50 mg L1 Cr in ground-
water in the USA (US EPA, 1987). Significantly high Cr concentration
(2e60 mg L1) has been detected, even in drinking water supplies of
Canada (Meranger et al., 1979) and Netherlands (Fonds et al., 1987),
which certainly causes adverse health effects on human population.
The tanneries are one of the largest industries, which use Cr
compounds to tan hides (animal skins) and hence are the major
contributors to its contamination. The Cr used in the process is not
taken up completely by leather and a large proportion of it escapes
into the effluent. Approximately 40 million tons of waste is
generated per year by tanneries around the world containing Cr, a
chief heavy metal contaminant (Papp, 2004). This waste is largely
disposed of by industries on land and in water bodies without
giving any required treatment. Severe contamination of productive
agricultural land and water bodies due to the disposal of tannery
waste had been observed in Australia (Megharaj et al., 2003),
Bangladesh (Park et al., 2000) and in India (Thacker and Datta,
2006). According to US EPA (2010), the permissible concentration
for all forms of Cr inclusive of Cr(VI) is 0.1 mg L1. The concentration
of Cr(VI) and total Cr prescribed under Indian Standards Specifi-
cation for drinking water is 0.05 mg L1.
In India, high concentrations of Cr(VI) (ranging from 1 to
50 g kg1) has been detected in the groundwater nearby tannery and
tannery waste disposal sites. In India alone approximately.
2000e32,000 tons of elemental Cr are released annually into the
environment by tanning industries. The Cr concentration in these
effluents range between 2 and 5 g L1 higher than the permissible
limit of 2 mg L1 (Chandra et al., 1997). Few sites around these tan-
neries were declared as “Critically Polluted Sites” and an in-situ
bioremediation (biotransformation) option was recommended by
NEERI for treatment of contaminated groundwater (Tamil Nadu
Pollution Control Board: ‘Revised Action Plan for Critically polluted
Area e Ranipet’, Nov 2010). Realizing the seriousness of issues
related to chromium pollution, Blacksmith Institute has identified
some sites as contamination hot spots and recommended them for
immediate remediation. The toxic site identification program has
identified over 300 Cr-contaminated sites around the world. ‘Pure
earth’ has estimated approximately 16 million people at risk to
chromium exposure (Pure Earth, 2018; Jobby and Desai, 2017).
5. Remediation of chromium (VI)
Today, man's greatest challenge is to cope up with metal
pollution problem. Unlike organic compounds which are degraded
258 R. Jobby et al. / Chemosphere 207 (2018) 255e266
Table 1
List of available methods for Chromium remediation.
Physical Methods Chemical Reduction
C Adsorption In-situ addition of electron donors like-
C Ion exchange
C Membrane filtration C Hydrogen sulfide (H2S)
C Reverse osmosis C Sodium dithionite (Na2S2O4)
C Granular activated carbon C Sodium metabisulfite (NaHSO3)
C Electrokinetics C Calcium metabisulfite (CaHSO3)
C In situ soil flushing C Calcium polysulfide (CaS5)
C Soil washing and C Ferrous sulfate (FeSO4)
separation C Photocatalysis
C Electrodialysis
naturally, heavy metals cannot be degraded, hence, it gets accu-
mulated at different sites. Remediation of Cr is possible through
various physical, chemical and biological method. Cr(VI) com-
pounds being strong oxidants are readily reduced to Cr(III) in
presence of organic or inorganic electron donors. A comprehensive
list of available physical, chemical and biological methods for Cr
remediation is given in Table 1.
5.1. Physical methods & chemical methods
Physical method explores physicochemical properties of the
substances for remediation. The techniques like adsorption, elec-
trodialysis method, membrane filtration, capping, granular acti-
vated carbon, photocatalysis, and soil washing etc. is included
among physical methods of remediation (Kang et al., 2004; Kent
et al., 1995; Rana et al., 2004; Wang et al., 2008). The diagram-
matic representation of various physical methods of chromium
removal from wastewater is provided in Fig. 2.
Chemical remediation implements use of chemicals like sulfur
dioxide, sodium metabisulfite, ferrous sulfate, sodium sulfite,
barium sulfite, lime and limestone for reduction of Cr(VI) to Cr(III)
(Jacobs et al., 2001; Kato and Nagai, 1991). Another effective
reduction of Cr(VI) is by photocatalysis. In soil, reduction of Cr(VI)
by organic acids is coupled with apparent adsorption of Cr(III). The
type of soil, its composition, texture, pH, conductivity, and other
physical characteristics highly influence the reduction process.
Moreover, transition metal ions present in soil act as a catalyst in
this reduction process. Mn(II) present in soil particles acts as a key
factor leading to the fast transformation of Cr(VI) to Cr(III). In
contrast, Fe ions in presence of light account for the rapid reduction
of Cr(VI). The role of Fe(II)/Fe(III), which acts as a catalyst by
shuttling electrons from dissolved organic matter (DOM) to Cr(VI),
can be demonstrated through a series of equations as follows:
Fe(III)-Cit þ hʋ / Fe(II) þ Cit
þ hʋ þ CO2(g) / R

Fe(III)-Tar þ hʋ / Fe(II) þ Tar
þ hʋ þ CO2(g) / R

R
/ ROO
/ O
2 (7)
R
þ Fe(III) / Fe(II)
Hþ þO

2 / HO2
HO
2 þ
HO2 / H2O2
7Hþ þ3Fe(II) þ HCrO
4 / 3Fe(III) þ Cr(III) þ 4H2O
O
þ
2 /HO2 þ Fe(II) þ H / Fe(III) þ H2O2
Bioremediation
By using either bacteria, fungi, algae, plants or their biomass respectively
C Biosorption
C Biotransformation
C Bioaccumulation
C Biomineralization
C Extracellular precipitation
H2O2 þ Fe(II) / Fe(III) þ
OH þ OH (13)
Recent investigations have focused on the photolytic reduction
of Cr(VI) by TiO2 at pH 3 both in presence and absence of organic
compounds. A highly active photocatalyst also being used for
reduction of Cr(VI) ions in water is La2Ti2O7 (Barrera-Díaz et al.,
2012).
5.1.1. Disadvantages of physical and chemical treatments
Although, some of the physical and chemical treatment pro-
cedures are simple, fast and possibly help metal recuperation, many
still have to meet the demand of high operational cost, high energy
consumption, and production of secondary pollutants. In addition,
most of them work well only under high metal concentration and
their efficiency is also subject to the presence of interfering agents
(Zouboulis et al., 2004). All these disadvantages need to be
considered for developing a sustainable and economical process for
metal removal Bioremediation seems to be a good alternative to
conventional cleanup technologies (Rani et al., 2008). Bioremedi-
ation refers to the productive use of living systems to remove or
detoxify pollutants. Use of microbial systems for metal bioreme-
diation has a great potential due to its low cost and low waste
generating techniques. Bioremediation is hence foreseen as a
promising technology for removal of Cr from contaminated envi-
ronment in an effective, economical and eco-friendly manner.
Merits and demerits of conventional remediation methods have
been listed in Table 2.
5.2. Biological methods
Transformation of harmful pollutants into nontoxic compounds
by the involvement of living organisms is termed as bioremediation
(Asha Latha and Sandeep Reddy, 2013). Through bioremediation, a
heavy metal contaminated site can be brought back to its original
state without creating any harmful effect on the environment
(6.a) (Adhikari et al., 2004). Living organisms including bacteria, fungi,
yeast, algae, and plants have shown remediation capabilities, but
(6.b) primarily bacteria and fungi have proven to be more efficient in
remediation. Low energy requirement, low operational cost, no
environmental and health hazards, high efficiency, possibility of
reuse and metal recovery are some of the advantages which are
(8) associated with these methods (Garbisu and Alkorta, 2003). Mi-
croorganisms often use metal as a nutrient or energy source to
(9) fulfill their growth requirement (Tang et al., 2007). They metabolize
these chemicals through a characteristic, enzyme-catalyzed
(10) pathway and convert them into harmless compounds more often
CO2 or CH4, water and biomass (Vidali, 2001).
(11) The important parameters which affect the success of biore-
mediation process are (i) chemical nature of pollutants, (ii) mois-
(12) ture content, structure, nutritional state, hydrogeology and pH of
 R. Jobby et al. / Chemosphere 207 (2018) 255e266 259

Fig. 2. Diagrammatic representation of various methods of physical remediation of chromium from waste water.

soil, (iii) microbial community of contaminated site and (iv) tem-
perature (Asha Latha and Sandeep Reddy, 2013).
Microbes adapt different strategies to survive in a heavy metal
polluted environment such as biosorption, bioaccumulation and
biotransformation for detoxification of pollutant into relatively safe
form (Jobby et al., 2016). Bioremediation includes all these mech-
anisms. It has been recognized as superior technology over con-
ventional strategies for removal of Cr(VI) from contaminated
environmental media. Biosorption is a physicochemical process in
which metal pollutant is positively attached to the surface of dead,
inactive or live biomass. It's a natural ability of certain biomass
where contaminants attach to the cell surface structures by forming
a chemical bond. A similar but slightly different process is “Bio-
accumulation”, a metabolically active process, operated by respi-
ration energy of living organisms and in this Cr(VI) is mounted
within the cell wall. Another potential mechanism for decreasing
the level of Cr(VI) at a contaminated industrial site is “Biotrans-
formation”. It is defined as the conversion of Cr(VI) to Cr(III) by
involving a biological system (Wang et al., 1989).
5.2.1. Molecular mechanisms of Cr bioremediation
The molecular mechanism of Cr biosorption, bioaccumulation
and biotransformation have been discovered up to a certain extent
by different research groups. This section of the review focuses on
all possible ways of Cr(VI) removal by a microbial cell. As shown in
Fig. 3, Cr(VI) adheres on the surface of the microbial cell through a
chemical bond between the metal ion and functional groups pre-
sent on cell surface structures including a variety of proteins, gly-
coproteins, polysaccharides, glycolipids etc. Upon adsorption,
Cr(VI) either precipitates on the surface of the microbial cell or

Table 2
Qualities and drawbacks of conventional methods of Chromium removal from aqueous system (Hawley et al., 2004).

Sl. Name of Method Merits Demerits

No.

1 Adsorption a. Conventional adsorbents a. Effective for Cr(IV) but not for Cr(III);
(e.g. clay, sand and soil containing iron and manganese oxides) b. Affected by the pH of solution;
c. Affected by the chemical nature of adsorbent.
2 Reverse osmosis a. Effluent recycling is possible after treatment. a. Requirement of high pressure;
b. High probability of membranes damage;
c. High costs
3 Ion-exchange a. Effective; a. It is sensible to the presence of particulate materials;
b. Possibility of chromium recovery b. Resins with high cost
4 Electrochemical a. Conversion of Cr(VI) to Cr(III) is easy in presence of common electron donors like a. Probability of reverse reaction i.e. conversion of Cr(III)
2þ 2þ 2
(Oxidation- Fe , Mn , CH4, S , reduced organics such as humic acid, fulvic acid etc. to Cr(VI) is very high under unfavorable conditions.
reduction)
5 Chemical a. Simple procedures; a. Separation of chromium salts from aqueous solution is
precipitation b. Generally presents low costs. difficult due to their high solubility;
b. Precipitation of soluble chromium (VI) is difficult in
presence of organics;
c. Commonly inefficient in low chromium concentration
260 R. Jobby et al. / Chemosphere 207 (2018) 255e266
Fig. 3. Showing possible mechanisms of chromium removal by a microbial cell. 1: Hexavalent chromium is adsorbed on microbial cell by forming chemical bonds with cell surface
molecules having certain functional groups; 2a: The adsorbed Cr(VI) may get reduced into Cr(III) via chromate reductase enzyme; 2b: Spontaneous conversion. 3a: Hexavalent
chromium enter into microbial cell through uptake system (sulfate transporters); 3b: Inside cell it is reduced to Cr(III) via highly unstable intermediates Cr(V/IV). Intracellular
translocation of Cr(VI) occurs with the help of metal binding proteins; 4: Accumulation of Cr(VI) within cell wall; 5: Excess Cr(VI) is removed from the cell through chromium
specific efflux system. The protein transporter is encoded by gene chrA (in Pseusomonas aeruginosa) which is present on a plasmid.
transforms into Cr(III). This conversion is either catalyzed by a
chromate reductase (Singh et al., 2008) or occurs spontaneously
(Thatheyus and Ramya, 2016). In both prokaryotes and eukaryotes,
chromate is actively transported across biological membranes
through sulfate transporters. Inside the cell, it is translocated with
the help of specific metal binding proteins and finally reduced to
Cr(III), via highly unstable oxidative states i.e. Cr(V) and Cr(IV). Both
aerobic, as well as anaerobic microorganisms, have the ability to
reduce Cr(VI) to Cr(III). In presence of oxygen, NADH, NADPH or any
other endogenous reserve serve as electron donor but in absence of
oxygen, Cr(VI) itself serves as a terminal electron acceptor in the
respiratory chain and frequently involves proteins from cyto-
chrome families like cytochrome b and cytochrome c (Singh et al.,
2008; Wielinga et al., 2001). Efflux of excess Cr(VI) from microbi-
al cell occurs through a transmembrane protein (efflux pump)
which is encoded by a plasmid gene Chr A.
Similar mechanisms like the accumulation of Cr ions in vacuoles,
their binding with organic ligands, scavenging of Cr generated
reactive oxygen species (ROS) via antioxidative enzymes have been
discovered in plants to provide them resistance against hexavalent
chromium (Shahid et al., 2017).
5.2.2. Bioremediation using bacteria
The bacterial remediation of Cr is characterized as fast, eco-
nomic, no-chemical, less energy requiring process that could be
achieved by using native, non-hazardous bacterial strains. Bacteria
are primarily used and proven to be most potent to convert Cr(VI)
into Cr(III), its less toxic form (Badar et al., 2000; Kanmani et al.,
2012). Both gram negative and gram positive bacteria have
demonstrated the ability of Cr(VI) removal by biosorption or
biotransformation. Bacillus coagulans, isolated from the waste of
electroplating industry reduced Cr(VI) by using a soluble enzyme
and malate as an external electron donor (Philip et al., 1998). A
remarkable ability of chromium biosorption had been reported in
B. circulans (34.5 mg Cr g1 of dry weight), B. megaterium (32.0 mg
Cr g1 of dry weight) and B. coagulans (39.9 mg Cr g1 of dry
weight) by Srinath et al. (2002). Additionally, the biosorption ability
of living and dead cells of B. coagulans and B. megaterium were
compared and dead cells were found to be more effective for
chromium biosorption. Living cells of B. coagulans adsorbed
23.8 mg Cr g1 dry weight, whereas dead cells adsorbed 39.9 mg Cr
g1 dry weight. Similar results were obtained in case of
B. megaterium (15.7 and 30.7 mg Cr g1 dry weight by living and
dead cells, respectively). The better performance of inactive/dead
biomass as compared to live cells is due to their susceptibility to-
wards toxic effects of metal ions which may lead to cell death
during the metal removal process. In a few experiments performed
with intact cells and cell-free extracts of Arthrobacter sp. and Ba-
cillus sp., Bacillus sp. was found to be inferior as compared to
Arthrobacter sp. in terms of their resistance to Cr(VI) and Cr(VI)
reducing ability (Asatiani et al., 2004; Arvindhan and Madhan,
2004). Reduction of Cr(VI) by implementation of a cell-free
extract of Arthrobacter sp. have proven the involvement of some
soluble proteins in the reduction process. Kapoor et al. (1999) have
also explained the involvement of a soluble protein during con-
version of Cr(VI) to Cr(III) by Pseudomonas putida. This protein was
characterized as an enzyme, chromate reductase and it was found
to use NADH or NADPH as an electron donor.
Removal of carcinogenic Cr(VI) by implementation of mixed
population of Pseudomonas sp. was demonstrated by Aravindhan
and Nair (2006). Cheung and Gu (2003) also reported the reduc-
tion of chromate through a sulfur-reducing bacterium which was
isolated from metal contaminated marine sediments of Tokwawan,
Hong Kong under anaerobic condition. The enrichment bacterial
consortium resulted in the complete reduction of chromate (98.5%)
in 168 h. Microbial consortia constructed by immobilized cells of
P. aeruginosa, B. subtilis and Saccharomyces cerevisiae on a solid
support showed good efficiency in removal of Cr(VI) from tannery
effluent (Fathima Benazir et al., 2010). Joutey et al. (2013) demon-
strated that microbial consortium developed by using indigenous
bacteria from tannery waste contaminated biotopes was able to
reduce Cr(VI) at various concentrations ranging from 100 to 300 mg
Cr L1 in a wide range of pH, using a variety of electron donors.
The resistance towards Cr(VI) was first time reported in Pseu-
domonas sp. (Romanenko and Korenkov, 1977). Later on, analogous
resistance mechanism has been discovered in other bacterial
genera like Cupriavidus metallidurans (Cervantes and Campos-
Garcia, 2007), Ochrobactrum tritici (Morais et al., 2011) etc. Cr
resistant bacteria with high remediation efficiency under both
aerobic and anaerobic conditions have been isolated from highly
 R. Jobby et al. / Chemosphere 207 (2018) 255e266 261

contaminated premises of Tamil Nadu Chromates and Chemicals
Limited (TCCL), Ranipet, Tamil Nadu, India. Maximum chromate
reduction was achieved by using 15 mg of bacterial cells g1 of soil
and molasses (50 mg g1 of soil) as a carbon source.
Divyasree et al. (2016) used a gram-positive bacterium, Cory-
nebacterium paurometabolum to demonstrate that biosorption, as
well as biotransformation, contributes equally to minimize the
toxicity of chromium compounds.
Biosorption experiments require optimization of several pa-
rameters like pH, temperature, biomass, time intervals etc. Mrudula
et al. (2012) used statistical design techniques like Plackett-Burman
design, Central Composite design etc. to optimize physical and
chemical factors for Cr biosorption and biotransformation through
Acinetobacter junii VITSUKMW2. It was observed that maximum
99.95% removal of Cr(VI) was achieved in 12 h through A. junii
VITSUKMW2 under optimized parameters i.e. 14.85 g L1 molasses,
4.72 g L1 yeast extract, and 54 mg L1 initial Cr(VI).
Jeyasingh and Philip (2005) operated a bioreactor under opti-
mized conditions for chromium reduction and achieved complete
reduction of Cr (5.6 mg Cr(VI) g1 of soil) in 20 d. Such findings
paved the way for developing and implementing bioreactors for
removal of hexavalent chromium from contaminated industrial
effluents. Several more works have been reported on bacterial
biosorption and biotransformation of hazardous Cr(VI) to Cr(III). A
few of them have been summarized in Table 3.
5.2.3. Bioremediation using fungi
Fungi have also been recognized and implemented for remedi-
ation of Cr-contaminated sites. Biosorption is found to be a more
effective method in fungi as compared to biotransformation. The
biosorption of Cr had been discovered in several genera of fungi
including Aspergillus oryzae (Igwe and Abia, 2006), A. niger
(Srivastava and Thakur, 2006), Trichoderma sp. (Vankar and Bajpai,
2007) and Fusarium oxysporum (Amatussalam et al., 2011). Meta-
bolism dependent and independent are the two different ap-
proaches used by fungi for Cr biosorption. Cr(VI) is adsorbed on the
fungal cell surface by forming a chemical bond with functional
groups which are present on cell surface proteins. Through FTIR
spectroscopic analysis carbonyl, carboxyl, amino, and hydroxyl
functional groups are depicted to be involved in binding of Cr on
the surface of the fungal cell wall (Amatussalam et al., 2011; Vankar
and Bajpai, 2007).
Biosorptive materials had been developed by using a variety of
fungal strains and analyzed for their chromium removal efficiency.
A biosorbent matrix was constructed by using dry stems of Carica
papaya plant in which cells of F. oxysporum were colonized. The
maximum level of Cr biosorption (90%) was achieved using this
matrix at the end of 5th day of incubation (Amatussalam et al.,
2011). Singh et al. (2016) developed Aspergillus flavus biomaterial,
infused with Fe2þ ions, as it enhances Cr removal as well as the
stickiness of biomaterial. Marine seaweed associated strains of
A. flavus and A. niger were tested for tolerance and accumulation of
Cr(VI). The results revealed that both the isolates accumulated
more than 25% of the supplied Cr. Invariably higher accumulation
potential was exhibited by Aspergillus flavus (Gupta et al., 2000).
Following biosorption, Cr(VI) is reduced to less toxic Cr(III) by some
fungi like Hypocrea tawa (Morales-Barrera et al., 2008) and Tri-
choderma inhamatum (Morales-Barrera et al., 2008).

Table 3
Remediation Chromium (VI) using bacteria.

Sl. Name of Organism Isolation Site Mechanism of Chromium Initial Cr(VI) Optimum pH & % Time (in Reference
no. Removal Concentra-tion Tempera-ture Remedia- hrs.)
tion

1 B. coagulans Electroplating waste discharge Biotransforma-tion 26 mg L1 7; NA 100 72 Philip et al.

contaminated soil (1998)
2 B. circulans Treated tannery effluent Biosorption, Bioaccumula- 50 mg L1 NA 69 24 Srinath et al.
tion (2002)
3 B. megaterium Treated tannery effluent Biosorption, Bioaccumula- 50 mg L1 NA 64 24 Srinath et al.
tion (2002)
1
4 B. coagulans (live cells) Treated tannery effluent Biosorption 50 mg L NA 47.6 24 Srinath et al.
(2002)
5 B. coagulans (dead cells) Treated tannery effluent Biosorption 50 mg L1 NA 79.8 24 Srinath et al.
(2002)
6 Bravibacterium sp. CrT- Tannery effluent Reduction 100 mg L1 NA 100 72 Faisal and
12 (live cells) Hasnain (2004)
1
7 Arthrobacter oxydans Basalt rock from contaminated Reduction 35 mg L NA 100 10 d Asatiani et al.
site (2004)
1
8 Providencia sp. Chromium contaminated Reduction 400 mg L 7; 37  C 99.3 NA Thacker et al.
chemical industrial site (2006)
9 Acinetobacter sp. Tannery effluent Reduction 100 mg L1 NA 67 24 Srivastava et al.
(2007)
10 Pannonibacter Steel-alloy industry site Reduction 462 mg kg1 NA 97.8 10 d Chai et al. (2009)
phragmitetus
1
11 Enterococcus Tannery effluent Biosorption 800 mg L 7.0 to 7.5; 35 NA NA Saranraj et al.
casseliflavus e45  C (2010)
12 Acinetobacter junii Chromite mine site Reduction 54 mg L1 9; 37.5  C 99.95 12 Mrudula et al.
(2012)
13 Corynebacterium Procured from culture Biosorption, Bioreduction 4 mg L1 2 55 2 Divyasree et al.
paurometabolum collection bank (2016)
1 
14 Cellulosimicro-bium Leather industry effluent Biosorption, Bioaccumula- 250 mg L 7.0; 35 C 80.43 120 Karthik et al.
funkei strain AR6 contaminated soil tion & Reduction (2016)
1
15 Ochrobactrum sp. Soil around electroplating Reduction 300 mg L 7.0; 30  C 96.5 NA Chen et al.
industry (2016)
16 Pseudomonas stutzeri L1 Crude oil samples Biosorption, Bioreduction 100e1000 mg L1 7; 37  C 97 24 Sathishkumar
et al. (2016)
17 Acinetobacter Crude oil samples Biosorption, Bioreduction 1000 mg L1 8; 37  C 99.58 24 Sathishkumar
baumannii L2 et al. (2016)
262 R. Jobby et al. / Chemosphere 207 (2018) 255e266

Table 4
Remediation of Chromium (VI) using fungi.

Sl. Name of Organism Isolation Site Mechanism of Initial Cr(VI) Optimum pH & % Time (in Reference
no. Chromium Removal Concentration Tempera-ture Remedia- hrs.)
tion

1 Aspergillus niger Tannery effluent Biosorption 500 ppm 6; 30  C 70 NA Srivastava and Thakur
contaminated soil (2006)
2 Trichoderma sp. Procured from culture Biosorption 4 ppm 5.5 97.39 2 Vankar and Bajpai (2007)
collection bank
3 Trichoderma inhamatum Industrial effluent Biotransform-ation 2.43 mM NA 100 60 Morales-Barrera and
Cristiani-Urbina (2008)
4 Hypocrea tawa Procured from culture Reduction 0.59e4.13 mM NA 100 NA Morales-Barrera et al.
collection bank (2008)
5 Fusarium oxysporum NCBT- Tannery effluent Biosorption, 100e200 ppm 5.8 90 120 Amatussalam et al. (2011)
156 contaminated soil Bioaccumula-tion

6 Phaneroch-aete chrysospor- Procured from culture Biosorption 100 ppm 7; 40 C 99.7 72 Pal and Vimala (2011)
ium (viable cells) collection bank
7 Paecilomyces lilacinus Tannery effluent Biotransform-ation, 200 mg L1 5.5; 25  C 100 120 Sharma and Adholeya
Bioaccumula-tion (2011)
8 Pichia jadinii M9 (cell free Textile-dye factory Reduction 1.3 mM 6; 60  C 36.2 1 Martorell et al. (2012)
extract) effluent

9 Pichia anomala M10 (cell free Textile-dye factory Reduction 1.7 mM 7; 50 C 52.9 3 Martorell et al. (2012)
extract) effluent
1
10 Pleurotus ostreatus Mushroom farms Biosorption 500 mg L <65  C 80 12 Carol et al. (2012)
11 Acremonium sp. (as fungal- Tannery effluent Biosorption, 100 ppm 5.6 90 10 d Herath et al. (2014)
bacterial biofilm) contaminated soil Biotransform-ation
12 Penicillium griseofulvum Tannery effluent site Biosorption 67.8 mg L1 NA 79.9 37.5 min Abigail et al. (2015)
MSR1
1
13 A. niger Contaminat-ed soil Biosorption 18.125 mg L 3 96.3 7d Sivakumar (2016)
14 Saccharomyces cerevisiae Procured from culture Biosorption 200 ppm 3.5; 25  C 85 24 Mahmoud and Mohamed
(immobilized beads) collection bank (2017)

NA: data not available.

Martorell et al. (2012) studied the ability of yeast to reduce
Cr(VI). They isolated two yeast strains i.e. Pichia jadinii M9 and
Pichia anomala M10 from the effluent of textile dye industry. Yeasts
also accomplish conversion of Cr(VI) into Cr(III) through chromate
reductase (ChR) enzyme. Mahmoud and Mohamed (2017) investi-
gated the biosorption of Cr(VI) from aqueous solution as well as
from effluent of tannery industry by using Biomass/Polymer
Matrices Beads (BPMB). These beads were developed by immobi-
lizing baker's yeast in alginate extract (3%) and 85% reduction in Cr
concentration was achieved under optimized conditions at
200 ppm of initial Cr concentration.
Herath et al. (2014) implemented fungal-bacterial biofilms as a
novel and promising tool for removal of Cr(VI). Some additional
research attempts of fungal mediated removal of Cr(VI) are sum-
marized in Table 4.
5.2.4. Bioremediation using algae
Biosorption of Cr(VI) from aqueous solutions like contaminated
wastewater, industrial effluent etc. can also be achieved by using
algal biomass. Presence of specific molecules such as metal-
lothioneins, phytochelatins, alginates, guluronic acid, sulfated
polysaccharides with amino, hydroxyl, carboxyl and sulfate as
functional groups impart it the ability of Cr remediation from
aqueous solutions (El-Sikaily et al., 2007; Volesky, 2001; Shanab
et al., 2012). Cr(VI) is adsorbed on the surface of algal cells and
may further be followed by its accumulation inside the cell (Jyoti
and Awasthi, 2014; Sen and Dastidar, 2010). Biosorbents had been
developed and evaluated for their Cr removal efficiency by imple-
menting biomass of Euglena (Fasulo et al., 1983), Cladophora sp.
(Deng et al., 2009; Vymazal, 1990), Scenedesmus (Corradi and Gorbi,
1993), Selenastrum (Brady et al., 1994), Spirogyra sp. (Gupta et al.,
2001), Ceramium virgatum (Sari and Tuzen, 2008), Nostoc linckia
(Mona et al., 2011) Spirulina sp. (Rezaei, 2013), Chlorella vulgaris
(Sibi, 2016). Biosorption studies were performed in batch mode to
optimize various physical and chemical parameters (pH,
temperature, agitation time, adsorbent concentration, adsorbent
dose, initial chromium concentration, contact time) for achieving
maximum adsorption of chromium on algal biosorbents. Highest
accumulation of Cr (72% after 15 min) was obtained with Clado-
phora biomass which is followed by Chlorella vulgaris (34e48%) and
Selenastrum (39%). Up to 82.67% of chromium biosorption was re-
ported with Spirulina biomass under optimized conditions at
10 mg L1 of initial concentration (Rezaei, 2013).
5.2.5. Bioremediation using plants and agro-sorbents
Remediation of metal pollution from environmental media by
green, living plants are defined as Phytoremediation. Some plants
show incredible resistance towards high metal concentration and
grow very well in an environment which is contaminated by
various heavy metals like Al, As, Hg, Pb, Cr etc. (Ali et al., 2013;
Reeves, 2003; Tangahu et al., 2011). They have tremendous ability
to absorb metals from their surroundings and accumulate them in
their tissues. Plants usually accumulate Cr in their root tissues and
very rarely it is translocated up to shoots (Lotfy and Mostafa, 2014).
Such plants with extraordinary metal accumulating ability are
known as “Hyperaccumulators” (Cho-Ruk et al., 2006). Several
studies and field trials have proved phytoremediation as a prom-
ising and cost-effective technology for Cr removal from polluted
sites (Ali et al., 2013; Revathi et al., 2011; Tangahu et al., 2011).
Cr(VI) is taken up by plant cells through sulfate transporters, fol-
lowed by its reduction to Cr(III) (Shewry and Peterson, 1974;
Cervantes et al., 2001). Plants having ability to remove Cr produce
some specific enzymes which are similar to bacterial chromate
reductase and mediate the conversion of Cr(VI) to Cr(III) (Lytle et al.,
1998). Initial attempts for phytoremediation of chromium polluted
soil of Ranipet Tanneries in Tamil Nadu was performed by Revathi
et al. (2011) using Sorghum. They investigated the impact of
Cr(VI) on chlorophyll content and plant biomass. Significant
reduction in plant biomass was observed along with increasing
dosage of Cr. Addition of vermicompost to the contaminated soil
 R. Jobby et al. / Chemosphere 207 (2018) 255e266
proved effective to obtain an increase in plant biomass by creating
room for more bioaccumulation (Revathi et al., 2011). Several other
plants had been investigated for their Cr bioaccumulation ability
including Pterocarpus indicus, Jatropha curcas (Mangkoedihardjo
et al., 2008), Callitriche cophocarpa (Augustynowicz et al., 2010),
Jasminum sambac, Jasminum grandiflorum, Polyanthus tuberosa,
Nerium oleander and Helianthus sp. (Santiago and Santhamani,
2010), Barringtonia acutangula (Kumar et al., 2014). Callitriche
cophocarpa was found to be an excellent Cr accumulator as twenty-
seven times greater concentration of Cr was found in fresh shoots
as compared to that in the medium. Among flowering plants which
were examined, J. sambac and J. grandiflorum showed maximum
tolerance towards a higher concentration of Cr in soil. Pennisetum
purpureum, Brachiaria decumbens, and Phragmites australis were
grown hydroponically in artificial gravel beds containing Cr solu-
tions (10e20 mg dm3) to determine their removal potential.
Although P. purpureum proved to be the best in terms of Cr removal
efficiency, 97e99.6% removal was achieved with all the systems
within 24 h (Mant et al., 2006). Thayaparan et al. (2015) demon-
strated Lemna minor to be a hyperaccumulator of Cr with the ability
to bio-concentrate 3.4 g Cr(VI) kg1 distilled water within 4 d.
Various types of plant-based biosorbents were constructed and
evaluated for their Cr removal efficiency. Maingi et al. (2016) used
ashes of tea leaves and pumpkin seeds as adsorbents for remedi-
ation of Cr(VI) contaminated wastewater whereas Ankitha et al.
(2016) used Areca nut husk as an adsorbent. Up to 98% removal
of hexavalent chromium was achieved within 60 min by imple-
menting a biosorbent material which was constructed by mixing
ashes of tea leaves and pumpkin seeds in equal proportion with
50 mg g1 of maximum adsorption capacity (Maingi et al., 2016).
The adsorbent which was developed from Areca nut husk along
with biofilm had demonstrated a substantial potential for Cr(VI)
bioremediation from polluted effluents. More than 50% of Cr(VI)
was reduced at 50 ppm initial chromium (VI) concentration
(Ankitha et al., 2016). Many other plant wastes like pistachio hull
powder (Moussavi and Barikbin, 2010), green coconut husk
(Tharannum et al., 2015), drumstick oil-free cake, sweet potato
peels (Abdulsalam et al., 2014) had been evaluated as adsorbent
material to provide a low-cost alternative to synthetic adsorbents.
Results pointed out that green coconut shell has high biosorption
capacity as it reduced 50% of initial Cr concentration (100 mg L1) in
a span of 24 h. Increased adsorption of metal on biosorbent could
be achieved by using smaller sized particles (Tharannum et al.,
2015). Ali and Alrafai (2016) designed a low cost, eco-friendly and
effective sorbent for removal of chromium (VI) from aqueous so-
lutions with chemically activated leaves of Ficus nitida. A signifi-
cantly higher percentage (99%) of Cr(VI) removal from aqueous
solutions was obtained by using 0.80 g of chemically activated
leaves of Ficus nitida at 50.0 mg L1 of initial chromium
concentration.
5.2.6. Applied in situ and ex situ chromium bioremediation
technologies
All the biological processes discussed so far and the various
systems studied for Cr remediations targets either reduction, up-
take or precipitation of carcinogenic, soluble and mobile Cr(VI) to
less toxic and less mobile Cr(III).
Ex situ technologies mostly use chemical reduction of Cr(VI) to
Cr(III) which is then precipitated and the water is filtered. In situ
approaches use chemical reduction and fixation eg: geochemical,
permeable reactive barrier, enhanced extraction, electrokinetics
(Clu-in.org, 2018). Natural attenuation and phytoremediation are
emerging technologies under study for in situ Cr remediation.
Monitored natural attenuation (MNA) has been implemented at
Superfund sites such as the Quality Plating Superfund Site, Missouri
263
(USEPA, 1995). At a chrome electroplating facility in Kansas in 1999
(Ace Services Superfund Site), biostimulation was chosen as part of
final treatment technology (USEPA, 1995). Bioaugmentation is
generally not applied as a technology as Cr(VI) contaminated sites
naturally contain organisms which have acclimatize to the envi-
ronment and hence prove to be better bioremediators. Indigenous
soil microorganisms augmented with organic amendments, fol-
lowed by precipitation and thereafter immobilization of Cr(III) has
been used to decontaminate large volume of Cr(VI) contaminated
water (Losi et al., 1994).
The successful use of bioreactors is limited in case of Cr(VI)
remediation in soil due to its complexity. But anaerobic packed-bed
bioreactors were found to successfully reduce Cr(VI) from tannery
waste. Turick et al. (1997) have developed such bioreactors using
indigenous anaerobic Cr(VI) reducing microorganisms. A novel
remediation of Cr(VI) contaminated soil through ex situ treatment
was evaluated using a bioreactor-biosorption system (Krishna and
Philip, 2005). In this study, initial Cr(VI) concentration of
50 mg L1 was reduced to > 80% in the bioreactor with an HRT of
8 h. An adsorption column was developed using Ganoderm lucidum,
a wood rotting fungus as the adsorbent for the removal of Cr(III)
with the specific adsorption capacity of 576 mg g1.
6. Conclusion and research lacunas
Biosorption and biotransformation have been proven as effi-
cient, eco-friendly and cost-effective strategies for remediation of
Cr(VI) contaminated environment. Biomass of bacteria, fungi, algae,
plants have been implemented and found to be effective for Cr(VI)
transformation. The molecular mechanism suggested in this review
provides an insight into a better understanding of Cr(VI) removal.
This can help in developing the existing technologies of chromium
remediation to be more efficient.
Still, a huge gap exists between laboratory findings and suc-
cessful implementation of bioremediation technology for the
treatment of Cr(VI) contaminated sites. Most of the laboratory ex-
periments are performed by using synthetic Cr solutions to analyze
the efficiency of the developed system for chromium remediation.
Thus, the potential of biological systems for the treatment of Cr(VI)
contaminated soil or industrial effluents needs to be evaluated. In
addition, most of the reported findings are from the batch mode of
treatment with small quantities of effluents. If these concerns are
addressed, a suitable operational strategy, inclusive of integrated
methods known, for the development of a continuous removal of
Cr(VI) from the industrial effluents is not far away to solve this
global menace.
Acknowledgment
The authors are grateful for the editing services rendered by
TEXTiFRAME.
References
Abdulsalam, S., Mohammed, J., Olubiyo, D.E., Tenimu II, 2014. Biosorption of chro-
mium(VI) ion from tannery waste water using two novel agricultural by-
products. Int. J. Innovat. Manag. Technol. 5, 78e82.
Abigail, E.A.M., Samuel, M.S., Chidambaram, R., 2015. Hexavalent chromium bio-
sorption studies using Penicillium griseofulvum MSR1 a novel isolate from tan-
nery effluent site: BoxeBehnken optimization, equilibrium, kinetics and ther-
modynamic studies. J. Taiwan Inst. Chem. Eng. 49, 156e164.
Adhikari, T., Manna, M.C., Singh, M.V., Wanjari, R.H., 2004. Bioremediation measure
to minimize heavy metals accumulation in soils and crops irrigated with city
effluent. J. Food Agric. Environ. 2, 266e270.
Ali, H., Khan, E., Sajad, M.A., 2013. Phytoremediation of heavy metalsdconcepts and
applications. Chemosphere 91, 869e881.
Ali, I.H., Alrafai, H.A., 2016. Kinetic, isotherm and thermodynamic studies on bio-
sorption of chromium(VI) by using activated carbon from leaves of Ficus nitida.
264 R. Jobby et al. / Chemosphere 207 (2018) 255e266
Chem. Cent. J. 10, 1e7.
Amatussalam, A., Abubacker, M.N., Rajendran, R.B., 2011. In situ Carica papaya stem
matrix and Fusarium oxysporum (NCBT-156) mediated bioremediation of
chromium. Indian J. Exp. Biol. 49, 925e931.
Ankitha, R., Prakruthi, S., Sneha, S., Tharannum, S., 2016. Areca nut as a potential
bio-adsorbent for remediation of chromium. Int. J. Sci. Eng. Manag. 1, 7e14.
Aravindhan, R., Nair, B.U., 2006. Biological removal of carcinogenic Cr(VI) using
mixed Pseudomonas strains. Bioresour. Technol. 11, 11e17.
Arslan, P., Beltrame, M., Tomasi, A., 1987. Intracellular chromium reduction. Bio-
chim. Biophys. Acta Mol. Cell Res. 931 (1), 10e15.
Arvindhan, S., Madhan, M., 2004. Bioaccumulation of Cr from tannery wastewater.
J. Am. Leather Chem. Assoc. 1, 197e203.
Asatiani, Z., Abuladze, N., Lejava, H., 2004. Effect of chromium VI action on
Arthrobacter oxydans. J. Current Microbiol. 49, 321e326.
Asha Latha, P., Sandeep Reddy, S., 2013. Review on bioremediation potential tool for
removing environmental pollution. Int. J. Basic Appl. Chem. Sci. 3, 21e33.
Augustynowicz, J., Grosicki, M., Hanus-Fajerska, E., Lekka, M., Waloszek, A.,
Kołoczek, H., 2010. Chromium(VI) bioremediation by aquatic macrophyte Cal-
litriche cophocarpa Sendtn. Chemosphere 79, 1077e1083.
Badar, U., Ahmed, N., Beswick, A.J., Pattanapipitpaisal, P., Macaskie, L.E., 2000.
Reduction of chromate by microorganisms isolated from metal contaminated
sites of Karachi, Pakistan. Biotechnol. Lett. 23, 829.
Baral, A., Engelken, R., Stephens, W., Farris, J., Hannigan, R., 2006. Evaluation of
aquatic toxicities of chromium and chromium containing effluents in reference
to chromium electroplating industries. Arch. Environ. Contam. Toxicol. 50,
496e502.
Barrera-Díaz, C., Lugo-Lugo, V., Bilyeu, B., 2012. A Review of Chemical, Electro-
chemical and Biological Methods for Aqueous Cr(VI) Reduction.
Bielicka, A., Bojanowska, I., Wisniewski, A., 2005. Two faces of chromiumepollutant
and bioelement. Pol. J. Environ. Stud. 14 (1), 5e10.
Brady, D., Letebele, B., Duncan, J.R., Rose, P.D., 1994. Bioaccumulation of metals by
Scenedesmus, Selenastrum and Chlorella algae. Water SA 20, 213e218.
Browning, C.L., Wise, J.P., 2017. Prolonged exposure to particulate chromate inhibits
RAD51 nuclear import mediator proteins. Toxicol. Appl. Pharmacol. 331,
101e107.
Carol, D., Kingsley, S.J., Vincent, S., 2012. Hexavalent chromium removal from
aqueous solutions by Pleurotus ostreatus spent biomass. Int. J. Eng. Sci. Technol.
4, 7e22.
Cervantes, C., Campos-Garcia, J., 2007. Reduction and efflux of chromate by bacteria.
In: Nies, D.H., Silver, S. (Eds.), Molecular Microbiology of Heavy Metals.
Springer-Verlag, Berlin, pp. 407e420.
Cervantes, C., Campos-Garc|ia, J., Devars, S., Gutierrez-Corona, F., Loza-Tavera, H.,
Torres-Guzman, J.C., Moreno-Sanchez, R., 2001. Interactions of chromium with
microorganisms and plants. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev. 25,
335e347.
Chai, L., Huang, S., Yang, Z., Peng, B., Huang, Y., Chen, Y., 2009. Cr(VI) remediation by
indigenous bacteria in soils contaminated by chromium-containing sla.
J. Hazard Mater. 167, 516e522.
Chandra, P., Sinha, S., Rai, U.N., 1997. Bioremediation of Cr. from water and soil by
vascular aquatic plants. In: ACS Sympopsium, Series, vol. 664, pp. 274e282.
Washington.
Chen, C.Y., Cheng, C.Y., Chen, C.K., Hsieh, M.C., Lin, S.T., Ho, K.Y., Li, J.W., Lin, C.P.,
Chung, Y.C., 2016. Hexavalent chromium removal and bioelectricity generation
by Ochrobactrum sp. YC211 under different oxygen conditions. J. Environ. Sci.
Health 51, 502e508.
Cheung, K.H., Gu, Ji-Dong, 2003. Reduction of chromate (CrO2) by an enrichment
consortium and an isolate of marine sulfate-reducing bacteria. Chemosphere
52, 1523e1529.
Cho-Ruk, K., Kurukote, J., Supprung, P., Vetayasuporn, S., 2006. Perennial plants in
the phytoremediation of lead contaminated soils. Biotechnology 5, 1e4.
Corradi, M.G., Gorbi, G., 1993. Chromium toxicity on two linked trophic levels. II
morphophysiological effects on Scenedesmus acutus. Ecotoxicol. Environ. Saf.
25, 72e78.
Costa, M., 2003. Potential hazards of hexavalent chromate in our drinking water.
Toxicol. Appl. Pharmacol. 188, 1e5.
Deng, L., Zhang, Y., Qin, J., Wang, X., Zhu, X., 2009. Biosorption of Cr(VI) from
aqueous solutions by nonliving green algae Cladophora albida. Miner. Eng. 22,
372e377.
De Flora, S., Bagnasco, M., Serra, D., Zanacchi, P., 1990. Genotoxicity of chromium
compounds. A review. Mutat. Res. Rev. Genet. Toxicol. 238 (2), 99e172.
Dhal, B., Thatoi, H., Das, N., Pandey, B., 2013. Chemical and Microbial Remediation of
Hexavalent Chromium from Contaminated Soil and Mining/metallurgical Solid
Waste: a Review.
Divyasree, C., Prabhakaran, Subramanian, S., 2016. Studies on the bioremediation of
chromium from aqueous solutions using Corynebacterium paurometabolum.
Trans. Indian Inst. Met. 70, 497e509.
El-Sikaily, A., El Nemr, A., Khaled, A., Abdelwehab, O., 2007. Removal of toxic
chromium from wastewater using green alga Ulva lactuca and its activated
carbon. J. Hazard Mater. 148, 216e228.
Faisal, M., Hasnain, S., 2004. Microbial conversion of Cr(VI) in to Cr(III) in industrial
effluent. Afr. J. Biotechnol. 3, 610e617.
Fasulo, M.P., Bassi, M., Donini, A., 1983. Cytotoxic effects of hexavalent chromium in
Euglena gracilis. II. physiological and ultrastructural studies. Protoplasma 114,
35e43.
Fathima Benazir, J., Suganthi, R., Rajvel, D., Padmini Pooja, M., Mathithumilan, B.,
2010. Bioremediation of chromium in tannery effluent by microbial consortia.
Afr. J. Biotechnol. 9, 3140e3143.
Fonds, A.W., van den Eshof, A.J., Smit, E., 1987. Water Quality in the Netherlands.
National Institute of Public Health and Environmental Protection, Bilthoven,
Netherlands. Report no. 218108004.
Garbisu, C., Alkorta, I., 2003. Basic concepts on heavy metal soil bioremediation. Eur.
J. Miner. Process. Environ. Protect. 3, 58e66.
Garg, U.K., Kaur, M.P., Garg, V.K., Sud, D., 2007. Removal of hexavalent Cr from
aqueous solutions by agricultural waste biomass. J. Hazard Mater. 140, 60e68.
Guidelines for drinking-water quality, 1996. Health Criteria and Other Supporting
Information, second ed., 2. World Health Organization, Geneva.
Gupta, R., Ahuja, P., Khan, S., Saxena, R.K., Mohapata, H., 2000. Microbial bio-
sorbents: meeting challenges of heavy metal pollution in aqueous solutions.
Curr. Sci. 78, 967e973.
Gupta, V.K., Shrivastava, A.K., Jain, N., 2001. Biosorption of chromium(VI) from
aqueous solutions by green algae spirogyra sp. Water Res. 35, 4079e4085.
Hawley, E.L., Deeb, R.A., Kavanaugh, M.C., James Jacobs, R.G., 2004. Treatment
Technologies for Chromium(VI). In: Guertin, Jacques, Jacobs, James A.,
Avakian, Cynthia P. (Eds.), Chromium (VI) Handbook. CRC Press, pp. 273e308.
Chap. 8.
Herath, H.M.L.I., Rajapaksha, A.U., Vithanage, M., Seneviratne, G., 2014. Developed
fungalebacterial biofilms as a novel tool for bioremoval of hexavelant chro-
mium from wastewater. Chem. Ecol. 30, 418e427.
Igwe, J.C., Abia, A.A., 2006. A bioseparation process for removing heavy metals from
waste water using biosorbents. Afr. J. Biotechnol. 5, 1167e1179.
Jacobs, J., Hardison, R.L., Rouse, J.V., 2001. In- situ remediation of heavy metals using
sulfur- based treatment technologies. Hydrovisions 10, 1e4.
Jeyasingh, J., Philip, L., 2005. Bioremediation of chromium contaminated soil:
optimization of operating parameters under laboratory conditions. J. Hazard
Mater. 118, 113e120.
Jobby, R., Desai, N., 2017. Bioremediation of heavy metals. In: Kumar, P., Gurjar, B.R.,
Govil, J.N. (Eds.), Biodegradation and Bioremediation. Environmental Science
and Engineering. Studium Press, New Delhi, pp. 201e220.
Jobby, R., Shah, K., Shah, R., Jha, P., Desai, N., 2016. Differential expression of anti-
oxidant enzymes under arsenic stress in Enterobacter sp. Environ. Prog. Sustain.
Energy 35, 1642e1645.
Joutey, N.T., Bahafid, W., Sayel, H., Abed, S., Ghachtouli, N., 2013. Remediation of
hexavalent chromium by consortia of indigenous bacteria from tannery waste-
contaminated biotopes in Fez, Morocco. Int. J. Environ. Stud. 68, 901e912.
Jyoti, J., Awasthi, M., 2014. Bioremediation of wastewater chromium through
microalgae: a review. Int. J. Eng. Res. Technol. 3, 1210e1215.
Kadiiska, M., Xiang, Q., Mason, R., 1994. In vivo free radical generation by chromium
(VI): an electron spin resonance spin-trapping investigation. Chem. Res. Toxicol.
7 (6), 800e805.
Kamaludeen, S.P., Megharaj, M., Juhasz, A.L., Sethunathan, N., Naidu, R., 2003.
Chromium-microorganism interactions in soils: remediation implications. Rev.
Environ. Contam. Toxicol. 178, 93e164.
Kang, S.Y., Lee, J.U., Moon, S.H., Kim, K.W., 2004. Competitive adsorption charac-
teristics of Coþ2, Niþ2 and Crþ3 by IRN-77 cation exchange resin in synthesised
wastewater. J. Chem. 56, 141e147.
Kanmani, P., Aravind, J., Preston, D., 2012. Remediation of chromium contaminants
using bacteria. Int. J. Environ. Sci. Technol. 9, 183e193.
Kanojia, R., Junaid, M., Murthy, R., 1998. Embryo and fetotoxicity of hexavalent
chromium: a long-term study. Toxicol. Lett. 95 (3), 165e172.
Kapoor, A., Viraraghvan, T., Roy Cullimore, D., 1999. Removal of heavy metals using
Aspergillus Niger. Bioresour. Technol. 70, 95e104.
Karthik, C., Ramkumar, V.S., Pugazhendhi, A., Gopalakrishnan, K., Arulselvi, P.I.,
2016. Biosorption and biotransformation of Cr(VI) by novel Cellulosimicrobium
funkei strain AR6. J. Taiwan Inst. Chem. Eng. 70, 282e290.
Kato, I., Nagai, S., 1991. Treatment of chromium containing wastewater. Japan Kokai
Tokkyo Koho JP03, 224e691.
Kent, D.B., Davis, J.A., Anderson, L.C.D., Rea, B.A., 1995. Transport of chromium and
selenium in a pristine sand and gravel aquifer: role of adsorption processes.
Water Resour. Res. 31, 1041e1050.
Kornhauser, C., Wrobel, K., Wrobel, K., et al., 2002. Possible adverse effect of
chromium in occupational exposure of tannery workers. Ind. Health 40,
207e213.
Krishna, K.R., Philip, L., 2005. Bioremediation of Cr(VI) in contaminated soils.
J. Hazard Mater. 121 (1e3), 109e117.
Kumar, D., Tripathi, D.K., Chauhan, D.K., 2014. Phytoremediation potential and
nutrient status of Barringtonia acutangula Gaerth. tree seedlings grown under
different chromium (CrVI) treatments. Biol. Trace Elem. Res. 157, 164e174.
Lenntech Water Treatment and Air Purification, 2004. Water Treatment. Published
by Lenntech,Rotterdamseweg, Netherlands.
Liu, K., Jiang, J., Shi, X., Gabrys, H., Walczak, T., Swartz, H., 1995. Low-frequency EPR
study of Chromium(V) formation from chromium(VI) in living plants. Biochem.
Biophys. Res. Commun. 206 (3), 829e834.
Losi, M.E., Amrhein, C., Frankenberger, W.T., 1994. Environmental biochemistry of
chromium. Rev. Environ. Contam. Toxicol. 136, 92.
Lotfy, S.M., Mostafa, A.Z., 2014. Phytoremediation of contaminated soil with cobalt
and chromium. J. Geochem. Explor. 144, 367e373.
Lu, Z., Ouyang, X., Zhang, W., Lu, X., 2013. Isolation of Cr(VI) resistant bacteria and
exploration of Cr(VI) removal mechanism of strain n-9. Appl. Mech. Mater.
295e298, 74e77.
Lytle, C.M., Lytle, F.W., Yang, N., Qian, J.H., Hansen, D., Zayed, A., Terry, N., 1998.
 R. Jobby et al. / Chemosphere 207 (2018) 255e266
Reduction of Cr(VI) to Cr(III) by wetland plants: potential for in situ heavy metal
detoxification. Environ. Sci. Technol. 32, 3087e3093.
Mahmoud, M.S., Mohamed, S.A., 2017. Calcium alginate as an eco-friendly sup-
porting material for baker's yeast strain in chromium bioremediation. Housing
Build. Nat. Res. Center J. 13, 245e254.
Maingi, F.M., Mbuvi, H.M., Nganga, M.M., 2016. Remediation of water contaminated
with Cr6þ and Cd2þ using aluminophosphates derived from ashes of tea leaves
and pumpkin seed. Chem. Mater. Res. 8, 94e102.
Mangkoedihardjo, S., Ratnawati, R., Alfianti, N., 2008. Phytoremediation of hex-
avalent chromium polluted soil using Pterocarpus indicus and Jatropha curcas L.
World Appl. Sci. J. 4, 338e342.
Mant, C., Costa, S., Williams, J., Tambourgi, E., 2006. Phytoremediation of chromium
by model constructed wetland. J. Bioresourc. Technol. 97, 1767e1772.
Martorell, M.M., Ferna
ndez, P.M., Farin
~ a, J.I., Figueroa, L.I.C., 2012. Cr(VI) reduction
by cell-free extracts of Pichia jadinii and Pichia anomala isolated from textile-
dye factory effluents. Int. Biodeterior. Biodegrad. 71, 80e85.
McCullough, J., Hazen, T., Benson, S., Blaine-Meyying, F., Palmisano, A.C., 1999.
Bioremediation of Metals and radionuclides.US Dept. Of Energy. Office of Bio-
logical and Environmental Research, Germantown. MC 20874.
Medeiros, M.G., Rodrigues, A.S., Batoreu, M.C., Laires, A., Rueff, J., Zhitkovich, A.,
2003. Elevated levels of DNA-protein crosslinks and micronuclei in peripheral
lymphocytes of tannery workers exposed to trivalent chromium. Mutagenesis
18, 19e24.
Megharaj, M., Avudainayagam, S., Naidu, R., 2003. Toxicity of hexavalent chromium
and its reduction by bacteria isolated from soil contaminated with tannery
waste. Curr. Microbiol. 47, 51e54.
Meranger, J.C., Subramanian, K.S., Chalifoux, C., 1979. A national survey of cadmium,
chromium, copper, lead, zinc, calcium and magnesium in Canadian drinking
water supplies. Environ. Sci. Technol. 13, 707.
Mohanty, K., Jha, M., Meikap, B.C., Biswas, M.N., 2005. Removal of chromium(VI)
from dilute aqueous solutions by activated carbon developed from Terminalia
arjuna nuts activated with zinc chloride. Chem. Eng. Sci. 60, 3049e3059.
Mona, S., Kaushik, A., Kaushik, C.P., 2011. Biosorption of chromium(VI) by spent
cyanobacterial biomass from a hydrogen fermenter using Box-Behnken model.
Int. Biodeterior. Biodegrad. 65, 656e663.
Morais, P.V., Branco, R., Francisco, R., 2011. Chromium resistance strategies and
toxicity: what makes Ochrobactrum tritici 5bvl1 a strain highly resistant. Bio-
metals 24, 401e410.
Morales-Barrera, L., Cristiani-Urbina, E., 2008. Hexavalent chromium removal by a
Trichoderma inhamatum fungal strain isolated from tannery effluent. Water, Air,
Soil Pollut. 187, 327e336.
Morales-Barrera, L., Flor de Ma
rıa Guil
len-Jiḿenez, Ortiz-Moreno, Alicia, Villegas-
Garrido, Thelma Lilia, Sandoval-Cabrera, Antonio, Hern


andez- Rod
rıguez, Cesar
Hugo, Cristiani-Urbina, Eliseo, 2008. Isolation, identification and characteriza-
tion of a Hypocrea awa strain with high Cr(VI) reduction potential. J. Biochem.
Eng. 40, 284e292.
Moussavi, G., Barikbin, B., 2010. Biosorption of chromium(VI) from industrial
wastewater onto Pistachio hull waste biomass. Chem. Eng. J. 162, 893e900.
Mrudula, P., Jamwal, S., Samuel, J., Chandrasekaran, N., Mukherjee, A., 2012.
Enhancing the hexavalent chromium bioremediation potential of Acinetobacter
junii VITSUKMW2 using statistical design experiments. J. Microbiol. Biotechnol.
22, 1767e1775.
Pal, S., Vimala, Y., 2011. Bioremediation of chromium from fortified solutions by
phanerochaete chrysosporium (MTCC 787). J. Bioremed. Biodegrad. 2, 127.
https://doi.org/10.4172/2155-6199.1000127.
Papp, J.F., 2004. Chromium use by market in the United States. In: 10th International
Ferroalloys Congress. Proc: Marshalltown, South Africa, The South African
Institute of Mining and Metallurgy, Cape Town, South Africa, pp. 770e778.
Park, D., Yun, Y.S., Jo, J.H., Park, J.M., 2000. Biosorption process for treatment of
electroplating wastewater containing Cr(VI): laboratory-scale feasibility test.
Ind. Eng. Chem. Res. 45, 5059e5065.
Pechova, A., Pavlata, L., 2007. Chromium as an essential nutrient: a review. Vet. Med.
52, 1e18.
Philip, L., Iyengar, L., Venkobachar, 1998. Chromium(VI) reduction from Bacillus
coagulans isolated from contaminated soil. J. Environ. Eng. 124, 165e1170.
Rana, P., Mohan, N., Rajagopal, C., 2004. Electrochemical removal of chromium from
wastewater by using carbon aerogel electrodes. Water Res. 38, 2811e2820.
́
Rani, A., Kumar, A., Goel, R., 2008. Bioremediation a natural approach for heavy
metal contaminated site. In: Saikia, R. (Ed.), Microbial Biotechnology. New India
Publishing, India, pp. 207e227.
Reeves, R.D., 2003. Tropical hyperaccumulators of metals and their potential for
phytoextraction. Plant Soil 249, 57e65.
Revathi, K., Haribabu, T.E., Sudha, N., 2011. Phytoremediation of chromium
contaminated soil using sorghum plant. Int. J. Environ. Sci. 2, 429e440.
Rezaei, H., 2013. Biosorption of chromium by using Spirulina sp. Arab. J. Chem. 9,
846e853.
Romanenko, V.I., Korenkov, V.N., 1977. A pure culture of bacterial cells assimilating
chromates and bichromates as hydrogen acceptors when grown under anaer-
obic conditions. Mikrobiologiya 46, 414e417.
Roundhill, D., Koch, H., 2002. Methods and techniques for the selective extraction
and recovery of oxoanions. Chem. Soc. Rev. 31 (1), 60e67.
Santiago, M., Santhamani, S., 2010. Remediation of chromium contaminated soils:
potential for phyto and bioremediation. In: 19th World Congress of Soil Science.
Soil Solutions for a Changing World, Brisbane, Australia.
Saranraj, P., Stella, D., Reetha, D., Mythili, K., 2010. Bioadsorption of chromium
265
resistant Enterococcus casseliflavus isolated from tannery effluent.
J. Ecobiotechnol. 2, 17e22.
Sari, A., Tuzen, M., 2008. Biosorption of total chromium from aqueous solution by
red algae (Ceramium virgatum): equilibrium, kinetic and thermodynamic
studies. J. Hazard Mater. 160, 349e355.
Sathishkumar, K., Murugan, K., Benelli, G., Higuchi, A., Rajasekar, A., 2016. Bio-
reduction of hexavalent chromium by Pseudomonas stutzeri L1 and Acineto-
bacter baumannii L2. Ann. Microbiol. 67, 91e98.
Sen, M., Dastidar, M.G., 2010. Chromium removal using various biosorbents. Iran. J.
Environ. Health Sci. Eng. 7, 182e190.
Shahid, M., Shamshad, S., Rafiq, M., Khalid, S., Bibib, I., Khan, N., Niazib, Dumate, C.,
Rashida, M.I., 2017. Chromium speciation, bioavailability, uptake, toxicity and
detoxification in soil-plant system: a review. Chemosphere 178, 513e533.
Shanab, S., Essa, A., Shalaby, E., 2012. Bioremoval capacity of three heavy metals by
some micro algae species (Egyptian Isolates). Plant Signal. Behav. 7, 1e8.
Sharma, S., Adholeya, A., 2011. Detoxification and accumulation of chromium from
tannery effluent and spent chrome effluent by Paecilomyces lilacinus fungi. Int.
Biodeterior. Biodegrad. 65, 309e317.
Shewry, P.R., Peterson, P.J., 1974. The uptake and transport of chromium by barley
seedlings (Hordeum vulgare L.). J. Exp. Bot. 25, 785e797.
Shiller, A.M., Boyle, E.A., 1987. Variability of dissolved trace metals in the Mississippi
River. Geochem. Cosmochim. Acta 51, 3273e3277.
Sibi, G., 2016. Biosorption of chromium from electroplating and galvanizing in-
dustrial effluents under extreme conditions using Chlorella vulgaris. Green
Energy Environ. 1, 172e177.
Singh, R., Kumar, M., Bishnoi, N.R., 2016. Development of biomaterial for chro-
mium(VI) detoxification using Aspergillus flavus system supported with iron.
Ecol. Eng. 91, 31e40.
Singh, S., Kang, S.H., Mulchandani, A., Chenm, W., 2008. Bioremediation: environ-
mental clean-up through pathway engineering. Curr. Opin. Biotechnol. 19,
437e444.
Sivakumar, D., 2016. Biosorption of hexavalent chromium in a tannery industry
wastewater using fungi species. Global J. Environ. Sci. Manag. 2, 105e124.
Srinath, Verma, T., Ramteke, P.W., Garg, S.K., 2002. Chromium (VI) biosorption and
bioaccumulation by chromate resistant bacteria. Tannery Technol. 48, 427e435.
Srivastava, S., Thakur, I.S., 2006. Evaluation of bioremediation and detoxification
potentiality of Aspergillus Niger for removal of hexavalent chromium in soil
microcosm. J. Soil Biol. Biochem. 38, 1904e1911.
Srivastava, S., Ahmad, A.H., Thakur, I.S., 2007. Removal of chromium and penta-
chlorophenol from tannery effluents. Bioresour. Technol. 98, 1128e1132.
Tamil Nadu Pollution Control Board, Nov 2010. Revised Action Plan for Critically
Polluted Area e Ranipet.
Tang, C.Y., Criddle, Q.S., Fu, C.S., Leckie, J.O., 2007. Effect of flux (transmembrane
pressure) and membranes properties on fouling and rejection of reverse
osmosis and nanofiltration membranes treating perfluorooctane sulfonate
containing waste water. J. Environ. Sci. Technol. 41, 2008e2014.
Tangahu, B.V., Sheikh Abdullah, S.R., Basri, H., Idris, M., Anuar, N., Mukhlisin, M.,
2011. A review on heavy metals (As, Pb, and Hg) uptake by plants through
phytoremediation. Int. J. Chem. Eng. 2011. http://doi.org/10.1155/2011/939161.
Thacker, U., Datta, M., 2006. Reduction of toxic chromium and partial localization of
chromium reductase activity in bacterial isolate DM1. World J. Microbiol. Bio-
technol. 21, 891e899.
Thacker, U., Parikh, R., Shouche, Y., Datta, M., 2006. Hexavalent chromium reduction
by Providencia sp. Process Biochem. 41, 1332e1337.
Tharannum, S., Krishna Murthy, V., Nandini, V., Shruthi, P.T., 2015. Toxic heavy metal
chromium remediation by processed low cost adsorbent- green coconut shell.
J. Sci. Technol. 5, 49e54. The Online.
Thatheyus, A.J., Ramya, D., 2016. Biosorption of chromium using bacteria: an
overview. Sci. Int. 4, 74e79.
Thayaparan, M., Iqbal, S.S., Iqbal, M.C.M., 2015. Phytoremediation potential of Lemna
minor for removal of Cr(VI) in aqueous solution at the optimum nutrient
strength. OUSL J. 9, 97e111.
Turick, C.E., Camp, C.E., Apel, W.A., 1997. Reduction of Cr(6þ) to Cr(3þ) in a packed
bed bioreactor. Appl. Biochem. Biotechnol. 871, 63e65.
US Environmental Protection Agency, 1987. Office of Drinking Water. Health advi-
sorydchromium, Washington, DC.
US Environment Protection Agency, 1995. In Situ Remediation Technology Status
Report. Electrokinetics. EPA 542-K-94e007. April 1995.
USEPA, 2010. IRIS, Toxicological Review of Hexavalent Chromium (2010 External
Review Draft). U.S. Environmental Protection Agency, Washington. DC EPA/635/
R- 10/004A, 2010.
Vankar, P.S., Bajpai, D., 2007. Phytoremediation of Chromium VI of Tannery Effluent
by Trichoderma Sp. In: Conference on Desalination and the Environment.
Sponsored by the European Desalination Society and Center for Research and
Technology Hellas (CERTH), Sani Resort, Halkidiki, Greece. April 22e25.
Vidali, M., 2001. Bioremediation an overview. Pure Appl. Chem. 73, 1163e1172.
Volesky, B., 1990. Biosorption and biosorbents. In: Volesky, B. (Ed.), Biosorption of
Heavy Metals. CRC Press Florida, USA, PP, pp. 3e82.
Volesky, B., 2001. Detoxification of metal-bearing effluents: biosorption for the next
century. Hydrometallurgy 59, 203e216.
Vymazal, J., 1990. Uptake of lead, chromium, cadmium and cobalt by Cladophora
glomerata. Bull. Environ. Contam. Toxicol. 44, 468e472.
Wang, L., Wang, N., Zhu, L., Yu, H., Tang, H., 2008. Photocatalytic reduction of Cr(VI)
over different TiO2 photocatalysts and the effects of dissolved organic species.
J. Hazard Mater. 152, 93e99.
266 R. Jobby et al. / Chemosphere 207 (2018) 255e266

Wang, P., Mori, T., Komori, K., Sasatsu, K., Toda, K., Ohtake, H., 1989. Isolation and Web references
characterization of an Enterobacter cloacae strain that reduces hexavalent
chromium under anaerobic conditions. Appl. Environ. Microbiol. 55,
Atsdr.cdc.gov. (2018). [online] Available at: https://www.atsdr.cdc.gov/toxfaqs/
1665e1669.
tfacts7.pdf [Accessed 11 Feb. 2018].
Wielinga, B., Mizuba, M.M., Hansel, C.M., Fendorf, S., 2001. Iron promoted reduction
Pure Earth, 2018. Fact Sheet: Chromium (2015) - Pure Earth [online] Available at:
of chromate by dissimilatory iron-reducing bacteria. J. Environ. Sci. Technol. 35,
http://www.pureearth.org/fact-sheet-chromium-2015/. (Accessed 11 February
522e527.
2018).
Xingzhen, Q., Xiuxia, L., 1987. Investigation on the natural background values and
Clu-in.org, 2018. CLU-IN | Contaminants > Chromium VI > Treatment Technologies
states of elements in natural water from the upper reaches of the Nenjiang
[online] Available at: https://clu-in.org/contaminantfocus/default.focus/sec/
river. Kexue Tongbao (Foreign Lang. Ed.) 32, 983e987.
chromium_VI/cat/Treatment_Technologies/. (Accessed 10 February 2018).
Zouboulis, A.I., Loukidou, M.X., Matis, K.A., 2004. Biosorption of toxic metals from
aqueous solutions by bacterial strain isolated from metal-polluted soils. Process
Biochem. 39, 909e916.