International Biodeterioration & Biodegradation 119 (2017) 87e95

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International Biodeterioration & Biodegradation

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Biosorption of hexavalent chromium by microorganisms

Francielo Vendruscolo a, *, Glalber Luiz da Rocha Ferreira a,
Nelson Roberto Antoniosi Filho b
a
Escola de Agronomia, Universidade Federal de Goia
s, P.O., Zip Code 74.690-900, Goia
^nia, GO, Brazil
b
Laborato
rio de M
~o e Separaça
etodos de Extraça ~o, Instituto de Química, Universidade Federal de Goia
s, Zip Code 74.690-900, Goia
^nia, GO, Brazil

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

Article history: Microorganisms perform an important function in the bioremediation of contaminated soils, water and
Received 17 July 2016 effluents. Bacteria, fungi, yeasts and microalgae and cyanobacteria, are low-cost biotechnological tools
Received in revised form for the treatment of large volumes of complex effluents containing Cr(VI). As from the selection and
4 October 2016
identification of new microorganisms and the evolution of Modern Biotechnology, molecular techniques
Accepted 5 October 2016
Available online 11 October 2016
and the characteristics of microorganisms such as their versatility and capacity to adapt to different
environments, permit that the biosorption of Cr(VI) be an alternative for the removal of contaminants.
Variations in the cell composition, morphology and way of growth, as also a study of the operational
Keywords:
Biosorption
conditions, allow for the application of aerobic or anaerobic microorganisms, live or dead, in the removal
Microbial biosorbents of Cr(VI). Thus the characteristics of the biosorbents applied in the removal of Cr(VI), the biosorption
Heavy metals processes, reactors and bioreactors, and the research developed with a view to the biosorption will be
Microbial biomass discussed in this review.
Cr(VI) © 2016 Elsevier Ltd. All rights reserved.
Bioreactors

1. Introduction activity co-factors; iii-inhibiting vital enzymes such as oxidative

The population growth and potential increase in industrial ac-
tivity in recent decades have contributed to a worsening of envi-
ronmental problems, such as, for example, water pollution.
Industrial effluents are generated by the incorporation of organic
and inorganic contaminants, in addition to disposing of metals such
as chromium, lead, mercury, cadmium and selenium. They are
frequently launched into the soil and water as from various
polluting sources, such as foundries, tanneries, textile, microelec-
tronic, fertilizer and pesticide industries, mining activity and other
industrial activities.
Studies have provided evidence that in addition to water and
soil contamination, there has been contamination of rice and soy-
bean (Silva et al., 2014), of mango orchards (Silva et al., 2012a,b), of
birds and swine (Alkmim Filho et al., 2014), of cattle (Souza et al.,
2009), amphibians (Fernando et al., 2016), and of wild animals
(Curi et al., 2012). The toxicity of heavy metals is reproduced by
individual action mechanisms of specific natures: i-exerting
immunosuppressive activity, reducing the activity or efficiency of
the immune system; ii-competing at fixation sites of enzyme
* Corresponding author.
E-mail address: francielo160679@ufg.br (F. Vendruscolo).
phosphorylation and iv-altering cell structures, principally in the
lipoprotein zone of membranes (Strandberg et al., 1981).
The maximum permitted discharge level of total Cr into sur-
face and potable waters has been set to below 0.05 mg l
1 by the
Environmental Protection Agency (USA) (Baral and Engelken,
2002) and the European Union (EC, 1998). Industrial effluents
containing Cr(VI) are often released into natural water resources
without proper treatment, resulting in anthropogenic contami-
nation (Viti et al., 2003; Cefalu and Hu, 2004; Cheung and Gu,
2007). Chromium stands out due to its wide range of use in in-
dustrial processes. It is used in the production of steel and metal
alloys, cement, galvanized plastic, tanneries, paints, fertilizers
and fungicides. It can be present in waters and liquid effluents in
the hexavalent form as chromate (CrO4)
2 or dichromate
(Cr2O7)
2 salts or as chromic oxide, in addition to being highly
water soluble and all forms of the metal can be toxic, depending
on the concentration.
It has been estimated that Cr(VI) is about a hundred times more
toxic than Cr(III). Cr(III) is essential to human metabolism, being
involved in the maintenance of glucose, cholesterol and triglyceride
levels, and playing an essential role as a nutrient for live organisms
(Frois et al., 2011). It should be remembered that Cr(III) can oxidize
in nature, transforming into its more toxic form, Cr(VI).

http://dx.doi.org/10.1016/j.ibiod.2016.10.008
0964-8305/© 2016 Elsevier Ltd. All rights reserved.
88 F. Vendruscolo et al. / International Biodeterioration & Biodegradation 119 (2017) 87e95
Cr(VI) shows elevated toxicity, being related to nasal irritation
and ulceration, hypersensibility reactions and contact dermatitis,
chronic bronchitis and emphysema, cause liver and kidney damage,
internal hemorrhage, lung and skin cancer, in addition to damaging
DNA by its interface with the enzyme DNA-polymerase (Harte et al.,
1993; Chhikara et al., 2010). Inhaling and/or ingesting Cr(VI) com-
pounds has been shown to be cancerous due to its easy permeation
of the cell membrane and elevated oxidizing potential, causing lung
and stomach cancer (Frois et al., 2011; Miranda Filho et al., 2011;
Mutongo et al., 2014). The lethal dose (DL50) of Cr(VI) by oral
ingestion in rats, varies from 50 to 100 mg kg
1, a very small value
when compared to the DL50 of Cr(III) of between 1900 and
3300 mg kg
1.
Heavy metals such as Cr(VI) have been removed from industrial
effluents by the application of conventional metal removal tech-
niques such as reverse osmosis, solvent extraction, lime coagula-
tion, ion exchange and chemical precipitation are encountered with
certain major disadvantages such as high energy requirements,
incomplete metal removal and generation of a large quantity of
toxic waste sludge due to various reagents used in a series of
treatment such as reduction of Cr(VI), neutralization of acidic so-
lution and precipitation. (Ahalya et al., 2003; Mane et al., 2011;
Alpatova et al., 2004). Consequently the search for alternative so-
lutions has become of eminent importance, searching for tech-
niques that aid in the removal of these contaminants, such as, for
example, the application of biosorbents, either alone or coupled
with another conventional method already used to remove Cr(VI).
The potential for growth and adaptation of microorganisms
when faced with adverse conditions and their versatility in
biotechnological applications linked to modern biotechnology, has
qualified microorganism as biosorption agents known as bio-
sorbents. The use of biosorbents in the removal of Cr(VI) is a
promising technique when compared to the conventional tech-
niques mentioned above.
To better understand the importance of the theme, a survey was
carried out in the Web of Science database. The terms biosorption
and hexavalent chromium, and biosorption and Cr(VI), were used as
the title words, resulting in 49 and 138 documents, respectively,
with a total of 187 studies carried out between 1991 up to the date
of the survey, carried out on March 15th, 2016. It can be seen that
few studies have been presented in this research area with the
objective of finding new solutions to preserve the environment.
Considering the importance of the socio-environmental impact
created by the presence of Cr(VI) in industrial effluents and by the
deleterious potential for human and animal health, the objective of
the present review was to present and discuss the potentialities of
removing Cr(VI) by applying microbial biosorbents, and discuss the
main characteristics and factors involved in the biosorption
processes.
2. Biosorbents
Biosorption is defined as a passive, rapid, reversible and inde-
pendent metabolic energy process carried out by active or inactive
microorganisms. The biosorption process carried out by way of
biosorbents has been shown to have great potential in the removal
of heavy metals from industrial effluents. This process is repre-
sented by disequilibrium of the surface forces by the contact of a
solid surface with a liquid phase, forming a surface layer of solutes
on the adsorbent and resulting in the accumulation of metals by
physicochemical interactions of metal ions with cell components of
biological species (Buratto et al., 2012).
The search for alternative processes to the conventional treat-
ments for the removal of Cr(VI) makes it possible to use microalgae,
fungi, bacteria and yeasts in biosorption processes. As compared to
conventional methods, these biosorbents show characteristics such
as low cost, high capacity and removal efficiency, reduction in the
generation of chemical and biological residues, low nutritional re-
quirements of the biosorbents and regeneration of the biosorbent
by recovering the metal. The high specific growth rate of many
microorganisms stands out, which makes cell multiplication
possible or even reuse of the microbial biomass in industrial ap-
plications, such as in the case of brewery yeast.
The mechanisms underlying the biosorption process depend on
factors intrinsic and extrinsic to the biosorbents. The nature of the
microbial biomass is one of the most important factors in the choice
of a biosorbent for heavy metals, although other factors, such as cell
viability, specific growth velocity, the nutritional requirements
(substrates and nutrients), the metabolic products and the culture
conditions such as temperature, pH and dissolved oxygen, are
important characteristics in the selection of a biosorbent. In addi-
tion the metallic species and its respective concentration and the
type and composition of the effluent, should also be taken into
consideration when choosing an adequate biosorbent.
The majority of microorganisms exhibit a biphasic response,
represented by the stimulus to cell growth when submitted to low
concentrations and growth inhibition, perceived as from the min-
imal inhibitory concentration (MIC). This represents the lowest
concentration of the contaminant that causes inhibition of micro-
bial growth, and can therefore directly affect the population size,
biological activity and microbial biodiversity (Sadler and Trudinger,
1967; Kavamura and Espo
sito, 2010).
Various types of biosorbents have been employed in the
removal of heavy metals and other contaminants from effluents,
aiming at biosorption by algae, microalgae and cyanobacteria
(Saravanan et al., 2009; Mane et al., 2011; Monteiro et al., 2011;
Khoubestani et al., 2015; Kwak et al., 2015; Nemr et al., 2015),
fungi (Akar and Tunali, 2006; Khani et al., 2012), yeasts (Ferreira
et al., 2007; Canuto et al., 2007; Martorell et al., 2012; Mahmoud,
2015), bacteria (White et al., 1995; Wierzba, 2010; Chen et al.,
2009; Cabral et al., 2014; Wu et al., 2015; Huang et al., 2016),
sludge (Chen et al., 2015; Michailides et al., 2015), aquatic macro-
phytes (Mo
denes et al., 2009; Lima et al., 2011); plant, fruit and
vegetable residues (Mutongo et al., 2014; Reddy et al., 2014; Huang
et al., 2015; Sultana et al., 2015; Wang et al., 2016); and inorganic
substances (Khelaifia et al., 2016).
Microbial biomass has the capacity to adsorb inorganic con-
taminants due to its cell composition (Fig. 1). The anionic ligands
phosphoryl, carbonyl, sulfhydryl and hydroxyl groups contribute
greatly to the biosorption processes (Volesky, 1987). Depending on
the species, microalgae present a diversified biochemical compo-
sition of carbohydrates, proteins, lipids and fatty acids (Cardoso
et al., 2011). In contrast, the cell walls of fungi, especially the fila-
mentous ones, are composed of polysaccharides such as b-glucan,
chitin and chitosan, glycoproteins, lipids, melanins, D-galactos-
amine polymers and polyuronides, being considered a location
with a prevalence of metal binding sites such as the chemical
groups acetamido, amide, phosphate, amino, amine, sulfhydryl,
carboxyl and hydroxyl (Vimala and Das, 2011).
The fungal cell wall is composed mainly of the polysaccharides
b-1,3 glucan, b-1,6 glucan, mannan-binding protein and a low
concentration of chitin (Fleuri and Sato, 2010), whereas that of
Gram-positive bacteria is constituted of a thick layer composed of
peptidoglycan, responsible for its rigidity. On the other hand the
cell wall of Gram-negative bacteria has a thin layer of peptido-
glycan, conferring greater fragility (Rosa, 2008). Aquatic macro-
phyte biomass is characterized by its chemical composition,
presenting concentrations of proteins, lipids, cell wall fractions and
soluble carbohydrates, together contributing an important nutri-
tional source of vegetable biomass (Henry-Silva and Camargo,
 F. Vendruscolo et al. / International Biodeterioration & Biodegradation 119 (2017) 87e95
Fig. 1. Structures of the principal biosorbents used in the biosorption of heavy metals (modified from Vieira and Volesky, 2000).
2002). When microbial cells show cell viability, they should show
resistance to the culture medium and the probability of making a
domain or growth capacity, as well as the maintenance of metabolic
activity in the contaminated environment.
3. Biosorption of Cr(VI)
The heavy metals belonging to the metal and semi-metal groups
known as metalloids have been widely described in many publi-
cations and in the legislation, with respect to chemical risks and the
need to use these substances in a safe way, associated with the
contamination and potential toxicity to ecosystems, or ecotoxicity
(Duffus, 2002). For these reasons, various methods have been used
to remove potentially toxic metal ions from solutions using con-
ventional methods, but they are not always efficient and are
expensive, principally when applied to dilute metal solutions. Thus
the search for new technologies to treat these effluents, that show
advantages with respect to the cost-benefit relationship have
resulted in an increase in interest in the biosorption process using
biological materials (Carol et al., 2012).
Conventional treatment processes for chromium detoxification
generally involve aqueous reduction of Cr(VI) by a reductant and
subsequent pH adjustment to neutral ranges in order to precipitate
the less soluble Cr(III). However, this process requires large amounts
of chemicals and energy, and therefore is often not economically
feasible. As a result, it has become critical to search for new tech-
niques that can reduce heavy metal concentrations to acceptable
environmental levels, at manageable costs (Villegas et al., 2013).
Microbial biomass has been used for the biosorption of Cr(VI)
(Table 1). Bacteria (Viera et al., 2003; Conceiça ~o et al., 2007;
Congeevaram et al., 2007; Tarangini et al., 2009; Polti et al., 2011;
Focardi et al., 2012; Ahmad et al., 2013; Robins et al., 2013; Chen
et al., 2014; Ontan~ on et al., 2014; Rath et al., 2014; Loubna et al.,
2015; Mala et al., 2015; Singh et al., 2015; Zheng et al., 2015; Wu
et al., 2015; Liu et al., 2015; Hora and Shetty, 2015; Deng et al.,
2015; Ge et al., 2014 Huang et al., 2016), fungi (Congeevaram
et al., 2007; Chhikara et al., 2010; Sharma and Adholeya, 2011;
Carol et al., 2012; Are
valo-Rangel et al., 2013; Coren ~ o-Alonso
89
et al., 2014; Singh et al., 2016; Chang et al., 2016), microalgae
(Mona et al., 2011; Bertagnolli and Silva, 2013; Kwak et al., 2015;
Munaro et al., 2015; Hackbarth et al., 2016; Souza et al., 2016)
and yeasts (Pas et al., 2004; Ksheminska et al., 2008; Martorell et al.,
2012; Bahafid et al., 2015; Mahmoud, 2015; Sathvika et al., 2015;
Mahmoud and Mohamed, 2015), all showed the ability to remove
Cr(VI) in biosorption processes that could be carried out in batches,
fed batches or in a continuous form. In the laboratory, many studies
have been carried out in batches, but research has shown the need
to work with continuous processes, only interrupting the bio-
sorption for desorption and recovery of the chromium.
The capacity for wastewater treatment is proportional to the
total biomass of a reactor. Advances in microbiology, biochemistry,
biotechnology, and reactor engineering have developed various
types of wastewater bioreactors. Microbial activity is affected by a
number of physicochemical environmental parameters. The factors
that directly impact on bioremediation are energy sources (electron
donors), electron acceptors, nutrients, pH, temperature, and
inhibitory substrates or metabolites (Boopathy, 2000). They are
applied in an isolated way or in consortium or mixed culture, as in
the case of activated sludge, mixtures of different microbial bio-
sorbents which can be applied live or without cell viability. In fact,
many processing residues, such as the case of residues of micro-
algae and filamentous fungi destined for the obtaining of lipids for
the production of biodiesel, can be used in biosorption.
Optimization of biosorption of heavy metals by the classical
method involves changing one independent variable (dosages of
pure or mixed culture, pH, temperature, or time of contact) while
maintaining all others at a fixed level which is extremely time
consuming and expensive for a large number of variables. To
overcome this difficulty, experimental Box-Behnken design under
response surface methodology can be employed to optimize the
biosorption of heavy metals (Clesceri et al., 1998).
3.1. Fungi
Fungi have an important role in the biosphere since they recycle
organic compounds and return them back to nature so they can be
90 F. Vendruscolo et al. / International Biodeterioration & Biodegradation 119 (2017) 87e95

Table 1
Microorganism used on Cr(VI) biosorption.

Biosorbent Factors studied qmax System Reference

Microalgae
Chlorella miniata Metal concentration, pH and biomass dosage 33.0 mg g
1 Batch Han et al. (2007)
Chlorella vulgaris Exposure time, metal concentration, pH and biomass dosage Batch Deng et al. (2006)
Nostoc linckia Temperature, pH, metal concentration and 42.6 mg g
1 Batch Mona et al. (2011)
biomass dosage
Spirulina platensis Exposure time, pH, biomass dosage, agitation and metal concentration 100.0 mg g
1 Batch Magro et al. (2013)
Spirulina sp. Exposure time, metal concentration, temperature, pH, and biomass 90.91 mg g
1 Batch Rezaei (2013)
dosage
Fungi and yeast
Candida sp. Metal concentration and pH 44.38 mg g
1 Batch
n-Jime
Guille
nez et al. (2009)
Candida utilis Immobilized in PVA alginate beads and flow rate of 0.95 mL h
1 Continuous flow Pattanapipitpaisal et al.
bioreactor (2001)
Paecilomyces lilacinus Metal concentration 189.13 mg g
1 Batch Sharma and Adholeya (2011)
Penicillium 75.1 mg g
1 Abigail et al. (2015)
griseofulvum
Bacteria
Arthrobacter viscosus Metal concentration, pH and biomass dosage 13.0 mg g
1 Batch Silva et al. (2012a,b)
Bacillus circulans Metal concentration Batch Khanafari et al. (2008)

1
Bacillus coagulans 39.9 mg g Batch Srinath et al. (2002)
Bacillus megaterium 30.7 mg g
1 Batch Srinath et al. (2002)
Zoogloea ramigera Metal concentration Batch Nourbaksh et al. (1994)

used again. They are versatile microorganisms and are capable of
adapting to adverse environments, characteristics which put them
amongst the main biosorbents studied for the biosorption of Cr(VI),
since they can tolerate Cr(VI) concentrations above 10,000 mg l
1.
The majority of the studies on the biosorption of Cr(VI)
emphasize the adsorption mechanism, and the fact that the anionic
chromate ions bind to positively charged groups on the fungal
biomass. In the study developed by Padma and Bajpai (2008), the
binding sites of Cr(VI) on the surfaces of Trichoderma sp. cells were
carboxyl and amine groups Padma and Bajpai (2008). Sivakumar
(2016) used Aspergillus species for the biosorption of Cr(VI) pre-
sent in a tannery effluent, and showed that the greatest biosorption
of 18.1 mg l
1 occurred at pH 3.0 using A. niger, followed by A. flavus,
A. fumigatus, A. nidulans, A. heteromorphus, A. foetidus and A. vir-
idinutans. Singh et al. (2016) showed that the maximum concen-
tration of Cr(VI) adsorbed by Aspergillus flavus was 16.1 mg g
1,
indicating that the microorganism could be used in pilot plants for
the treatment of effluents containing Cr(VI). In a study carried out
by Chhikara et al. (2010) the fungal biosorbent used was Aspergillus
niger treated with acid and immobilized in a calcium alginate
matrix. The biosorption of the Cr(VI) ion was observed using a
column fed continuously with a filling of spheres containing the
immobilized biosorbent. Fourier Transform Infrared (FTIR) Spec-
troscopy showed alterations in the band patterns due to the hy-
droxyl, carboxyl and amine groups present in the cell wall,
responsible for the biosorption of Cr(VI).
Kumar et al. (2008) submitted Aspergillus niger, Aspergillus
sydoni and Penicillium janthinellum to Cr(VI) biosorption. A 91.3%
removal of Cr(VI) by A. niger was verified at pH 2.0. Abigail et al.
(2015) used Penicillium griseofulvum for the biosorption of Cr(VI)
and applied the Box-Behnken design to optimize the variables. In
thermodynamic terms the parameters indicated that the process
was spontaneous and easy to occur in nature. According to the Box-
Behnken design, the best conditions for biosorption were a bio-
sorbent dose of 2 g l
1, an initial Cr(VI) concentration of 67.8 mg l
1
and a contact time of 37.5 min.
Carol et al. (2012) defend the use of the biosorbent Pleurotus
ostreatus as a cheap and promising adsorbent for the removal of
Cr(VI) from industrial effluents. The adsorption provided by this
fungus is due to the chitosan load present in its cell structure, a
compound derived from deacetylated chitin. The results showed a
maximum adsorption of 5.2 mg of Cr(VI) per gram of biosorbent,
due to the concentration of chitosan present in the fungal cell wall.
Sag and Kutsal (1996) used Rhizopus arrhizus to remove various
heavy metals, amongst which Cr(VI). The removal was greater
when Cr(VI) and Fe(III) were used as the contaminants, indicating
that a combination of chemical elements can result in synergistic or
antagonistic effects.
The majority of studies indicate a sorption process, but pro-
cesses reducing Cr(VI) to Cr(III) also occur. Coren ~ o-Alonso et al.
(2014) showed that Aspergillus niger var tubingensis strain Ed8
reduced Cr(VI) to Cr(III), demonstrating the bio-remedial capacity
of this microorganism, and Are
valo-Rangel et al. (2013) showed the
same capacity for Penicillium sp.
3.2. Yeasts
Yeasts have been little studied for use in biosorption processes,
principally for Cr(VI). However, they are versatile microorganisms
since they develop in both aerobic and anaerobic environments,
principally the Saccharomyces species. In addition to their versa-
tility they show low-cost nutritional requirements, can be obtained
from beverage industries and applied in biosorption processes.
They are safe microorganisms and can be applied both dead and
alive (Wang and Chen, 2006).
Bahafid et al. (2015) studied the removal of Cr(VI) by Cyber-
lindnera fabianii and showed that it was possible to remove 100% of
the chromium from effluent after 48 h of biosorption. However,
they perceived that part of the Cr(VI) was transformed in Cr(III),
leading to the conclusion that the adsorption process was coupled
to reduction. Pas et al. (2004) used Candida intermedia in the bio-
sorption of Cr(III) and Cr(VI), and by way of scanning electronic
microscopy, showed that the minimal inhibitory concentration of
Cr(III) caused alterations in the form and pattern of budding,
whereas the minimal inhibitory concentration of Cr(VI) did not
affect the cell characteristics. Ksheminska et al. (2008) used Pichia
guilliermondii ATCC 201911 (L2) in the biosorption of Cr(III) and
Cr(VI), and showed that the yeast presented greater resistance to
Cr(III), a fact also verified in other studies, given the toxicity of
Cr(VI). Chromate concentrations of 2.0  10
3 mol l
1 caused an
increase in the lag phase and the Cr(VI) concentration decreased in
proportion to cell growth. Apart from these characteristics, the
 F. Vendruscolo et al. / International Biodeterioration & Biodegradation 119 (2017) 87e95
importance of the Cr(VI) reduction mechanism was evident.
The yeasts can be used as a single biosorbent, but research in-
dicates yeast immobilization and impregnation methods for the
biosorption of Cr(VI), such as studies carried out by Mahmoud
(2015) using gelatin for yeast impregnation, by Sathvika et al.
(2015) using microwaves and a cellulose biopolymer to immobi-
lize yeasts and produce the biosorbent, and by Mahmoud and
Mohamed (2015) who immobilized yeasts in calcium alginate to
maximize the biosorption of Cr(VI).
3.3. Microalgae
Species of Chlorella, Scenedesmus, Synechocystis and Spirulina,
amongst others, live or dead, have been used in the biosorption of
Cr(VI). They can be applied alone or associated with other bio-
sorbents and, despite showing smaller specific growth velocities as
compared to other microorganisms, biomass residues, such as
those remaining after obtaining lipids in the production of bio-
diesel, can be reused as biosorbents.
€nmez et al. (1999) used Chlorella vulgaris, Scenedesmus obli-
Do
quus and Synechocystis sp. as the biosorbents and concluded that
pH 2.0 was adequate for the greatest removal of Cr(VI), a fact which
altered the total surface load. Chen et al. (2003) determined the
Cr(VI) biosorption capacity of six microalgae. The greatest tolerance
of the microalgae studied when faced with Cr(VI) was that shown
by Scenedesmus quadricauda followed by Selenastrum capriornutum
and Spirulina platensis which removed 20.9, 12.4 and 11.7 mg l
1,
respectively. Kwak et al. (2015) prepared biosorbents as from
Spirulina platensis extracts by adding lithium chloride and dime-
thylsulphoxide and showed a maximum Cr(VI) biosorption capacity
of 41.1 mg g
1 at pH 2.0, five desorption cycles being possible in a
0.1 M NaOH solution, with an efficiency of 70%. Colla et al. (2015)
cultivated Spirulina platensis in culture mediums containing Cr(VI)
and, although growth of the microalga was influenced by the
presence of the contaminant, the biomass removed about 65% of
the Cr(VI), converting 90.4% in Cr(III). Chrorella miniata also showed
the capacity to biosorb and bioreduce Cr(VI) to Cr(III) in studies
carried out by Han et al. (2007). The results of the FTIR showed that
the amino groups of the biomass were the main ones responsible
for the biosorption of Cr(VI) whereas the carboxyl groups were
responsible for the biosorption of Cr(III). In addition to the algae
cited above, other studies have been carried out searching for ap-
plications of these biosorbents in the removal of Cr(VI), such as the
studies conceived by Gomes and Melo (2012), Bertagnolli and Silva
(2013) and Munaro et al. (2015).
3.4. Bacteria
Bacteria, in addition to having nutritional requirements and a
chemical cell composition different from the other microorgan-
isms, generally present higher specific growth velocities than the
other biosorbents, as in the case of fungi. It should be pointed out
that it is difficult to work with the removal of heavy metals via
strictly anaerobic live microorganisms, due to the need to maintain
anaerobiosis during the biosorption process, although in the case of
inactive biosorbents there would be no need for anaerobiosis.
Recently Wu et al. (2015) showed the reduction of Cr(VI) at the
anodes of a microbial fuel cell of Gamma-proteobacteria and bac-
teria in the biofilm. Conceiça ~o et al. (2007) selected twenty mi-
croorganisms from soil contaminated with Cr(VI) and showed that
bacteria of the genera Aeromonas, Aereobacterium, Xanthobacter,
Agrobacterium and Bacillus were capable of adsorbing more than
100 mg l
1 of Cr(VI) in aqueous solution in a 24 h period. The focus
of the study developed by Rengifo-Gallego et al. (2012) was the
biosorption of Cr(VI) as from the association of algae and bacteria
91
exposed to different concentrations of the contaminant under
controlled in vitro conditions. This study was carried out in syn-
thetic sea water in bioreactors with chromium concentrations of 5
and 10 mg l
1, and it was shown that the biosorbent of the exper-
imental treatment using algae associated with bacteria was the
most efficient combination, detecting efficient adsorption with the
concentration of 10 mg l
1, with 87% of the Cr(VI) being biosorbed.
In addition to the phenomenon of biosorption, some studies
have shown the capacity to reduce Cr(VI) to Cr(III) via the pro-
duction of enzymes by Bacillus, which are Gram-positive bacteria,
this, in practice, being more adequate, since the trivalent form is
less toxic. Coupled to this, the microorganisms continue playing
their role of recycling compounds in nature.
Mala et al. (2015) verified the capacity of Bacillus methylo-
trophicus to produce chromate reductase. This extracellular enzyme
showed an initial activity of 212.8 U mg
1 of protein, and applica-
tion of the extract containing the reductase reduced the chromate
by 91.3% in 48 h. Zheng et al. (2015) also verified the capacity of
Bacillus subtilis to reduce Cr(VI) to Cr(III) aerobically, and showed
that the gene nfrA was directly involved in the process of synthe-
sizing the enzyme responsible for the reduction. Other bacteria
have also been studied with a view to reducing Cr(VI) to Cr(III) such
as Pantoea sp. FC 1 (Ontan~ on et al., 2014), Bacillus amyloliquefaciens
(Rath et al., 2014), Escherichia coli (Robins et al., 2013; Liu et al.,
2015), Ochrobactrum sp. (Hora and Shetty, 2015), Serratia sp
(Deng et al., 2015) and Leucobacter sp. (Ge et al., 2014).
4. Bioreactors involved in Cr(VI) biosorption
Basically the biosorption process consists of solid liquid contact
and requires controlled conditions to optimize it. It can be carried
out in batch, fed-batch or continuous forms and the choice of
bioreactor should be associated with the different operational
conditions required for biosorption, such as, for example, aerobi-
cally or anaerobically. Continuous bioreactors have received great
attention due to the importance and technical ease of applying
them in real contaminant removal processes.
Reactors and bioreactors of the following types (Fig. 2): batch
stirred-tank and continuous-flow stirred tank; fixed packed-bed,
fluidized-bed and multiple-bed (Chakraborty et al., 2013; Xu
et al., 2016); airlifts and bubble column (Morales-Barrera and
Cristiani-Urbina, 2006, 2015; Guille
n-Jime
nez et al., 2009; Nassar
et al., 2015), and wetlands (Sultana et al., 2014) have been applied
in Cr(VI) biosorption.
4.1. Airlift and bubble columns
Airlifts (Fig. 2a, b and 2c) and bubble columns (Fig. 2d) are
pneumatically shaken bioreactors that impose low shear stress and
are mainly applied when the microorganisms involved are sensi-
tive. Fig. 2b and c, the riser and downcomer are separated by an
internal baffle or draft tube, air may be sparged into either the draft
tube or the annulus. The function of the aeration is to supply the
demand for dissolved oxygen, as well as promoting the pneumatic
shaking with low shear stress, and such bioreactors are generally
applied in aerobic processes. In the cultivation of filamentous fungi,
they reduce the formation of pellets and allow for the formation of
disperse hyphae and mycelium, which increases the surface contact
area. Of the different types of airlifts, those consisting of concentric
tubes are the most used.
Morales-Barrera and Cristiani-Urbina (2006) carried out a Cr(VI)
biosorption study using Trichoderma viride and verified that
shaking frequencies of 120 rpm caused fragmentation of the
mycelium with a negative effect on biosorption. They pointed out
that the microorganism showed a high biosorption capacity when
92 F. Vendruscolo et al. / International Biodeterioration & Biodegradation 119 (2017) 87e95
Fig. 2. Bioreactors used in the biosorption processes (a) external-loop airlift, (b) internal-loop airlift, (c) internal-loop draft tube, (d) bubble column, (e) batch stirred tank bio-
reactors (f) continuous stirred tank bioreactors, (g) fixed-bed and (h) wastewater lagoon.
cultivated in an airlift. Morales-Barrera and Cristiani-Urbina (2015)
used the same equipment for the biosorption of Cr(VI) by Hypocrea

n-Jime
tawa. Guille
nez et al. (2009), when studying the biosorption
of Cr(VI) by Candida sp. perceived that greater specific growth ve-
locities were obtained when biosorption was carried out in an airlift
as compared to experiments in flasks.
4.2. Batch tank reactors
The majority of biosorption processes are carried out in batches in
mechanically stirred reactors (Fig. 2e). They consist of the first steps
of the biosorption process so as to understand and obtain initial
biosorption responses. Understanding the behavior of the microor-
ganism and its morphological alterations when faced with different
contaminants is essential for the success of biosorption. Such
equipment functions very well for small quantities of industrial ef-
fluents and in situations where the biosorption is seasonal, and can
be carried out in conical flasks or in more sophisticated and better
equipped reactors with mechanical stirring, so as to avoid the for-
mation of concentration gradients during the biosorption process.
The advantages are related to the simplicity and ease of repe-
tition of the experiments, and biosorption can take several hours, to
the contrary of the continuous process. In some Cr(VI) biosorption
situations it is possible to work with feeding the biosorption tank
until the reaction volume is reached.
4.3. Continuous tank reactors
The biosorption carried out in continuous stirred tank reactors is
carried out in a way similar to the batch stirred-tank reactors,
except that the Cr(VI) solution to be treated is fed in continuously
(Fig. 2f). They allow one to study the effects of climatic conditions
and variations in the Cr(VI) concentration faced with the
biochemical and morphological responses, in addition to the pos-
sibility of working with different hydraulic retention times. Bio-
sorption studies in continuous processes are extremely important
in order to evaluate the technical viability of a real process.
The advantages of continuous systems are related to the real
conditions of Cr(VI) biosorption, allowing one to understand the
effects of climatic conditions on a big scale (Fig. 2h), presenting
high productivity with respect to the effluent to be treated, and
consequently of Cr(VI) removal. They allow for adjustments in the
hydraulic retention time as a function of the microbial growth ve-
locity, as well as offering the possibility of working in series with
different reactors. Losses of cell viability and microbial contami-
nation are probably the greatest disadvantages, and must therefore
be controlled to guarantee biosorption efficiency.
4.4. Immobilized reactors
The tendency for the biosorption of Cr(VI) and of other pollut-
ants points to the need to use bioreactors with immobilized bio-
sorbents (Fig. 2g), which increases the working life of the
biosorbent, allows for the promotion of variations in the hydraulic
retention time, and principally allows for the possibility of Cr(VI)
desorption and recovery cycles. The biomass can be immobilized by
different techniques (entrapment, encapsulation and bonding)
onto different polymeric materials, for example polyacrylamide,
alginate, polysulfone, textile fibers and inorganic compounds.
In general inert materials tend to prolong the working life of a
biosorbent increasing its productivity. However the choice must be
made according to the characteristics of the microorganisms and
the properties of the immobilization material. Krishna and Philip
(2005) demonstrated that more than 80% Cr(VI) reduction was
obtained within 4 h with an initial Cr(VI) concentration of
50 mg l
1. The adsorption column of powdered Ganoderma lucidum
was used as a polishing treatment unit, and this removed more
than 95% of Cr(III) within 3 h. This biosystem is a feasible option for
the ex situ treatment of Cr(VI)-contaminated soils. Pal et al. (2013)
studied the immobilization of Bacillus sphaericus AND 303 for Cr(VI)
reduction. The screening of inert matrices for the entrapment of
whole cells indicated that polyvinyl alcohol-alginate was the most
effective one, reducing 87.5% of 20 mM Cr(VI) in 24 h.
 F. Vendruscolo et al. / International Biodeterioration & Biodegradation 119 (2017) 87e95
5. Bioremediation e limitations and potentials
The application of microorganisms in Cr(VI) biosorption pro-
cesses has been studied in different systems. The greatest limita-
tions faced by biosorption processes are related to the metabolic
parameters and responses, which can be influenced by the Cr(VI)
and by the operational conditions applied. Variations in the
morphology, in the specific growth velocity, cell viability, enzyme
synthesis and natural mutation itself, can occur in processes
involving heavy metals. Studies with Cr(VI) removal have shown
good results at pH 2.0, but such pH values are extremely acidic for
microbial cultivations and can compromise cell viability. In addition
some heavy metals can result in morphological alterations favoring
pleomorphic cells (Villegas et al., 2013). The complexity of some
types of effluent imposes some limits on the biosorption processes,
generally when using live microorganisms, since contamination
and dominion of the environment by the contaminating species can
occur. The isolation and identification of chromate reductase pro-
ducing microorganisms and the understanding of the genic
expression for the synthesis of these enzymes has attracted the
attention of research concerning the biosorption of Cr(VI).
Emerging techniques such as cell immobilization, the application of
bioreactors operating in continuous systems, the discovery of new
microorganisms and genetic alterations have been potentially
indicated for biosorption processes so as to circumvent the re-
strictions frequently found.
6. Final considerations
Considering the worldwide growth of industrialization with the
consequent increase in the generation of complex industrial efflu-
ents, in most cases constituted by the presence of Cr(VI) by the
application of microorganisms appears as an emergent, low-cost
biotechnological tool. This tool is versatile in its applications,
since the biosorbents can be applied in their viable or non-viable
forms and the system managed in the batch, fed-batch or contin-
uous forms, in addition to in situ bioremediation. The isolation and
selection of new microorganisms and the genetic alterations would
contribute to the technological advances in the biosorption of
Cr(VI) and of other potentially toxic contaminants. It should be
noted that the various studies with different biosorbents have
shown success in their results with the removal of potentially toxic
metals such as Cr(VI), as presented in this review.
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.ibiod.2016.10.008
Conflicts of interest
The authors declare they have no conflicts of interest.
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