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Chromium (VI) biosorption and removal of

chemical oxygen demand by Spirulina platensis
from wastewater-supplemented culture medium
a a a a
Clinei D. Magro , Maitê C. Deon , Andreia De Rossi , Christian O. Reinehr , Marcelo
a a
Hemkemeier & Luciane M. Colla
a
Laboratory of Fermentations, Course of Environmental Engineering, College of Engineering
and Architecture , University of Passo Fundo , Passo Fundo , Rio Grande do Sul , Brazil
Published online: 04 Jul 2012.

To cite this article: Clinei D. Magro , Maitê C. Deon , Andreia De Rossi , Christian O. Reinehr , Marcelo Hemkemeier & Luciane
M. Colla (2012) Chromium (VI) biosorption and removal of chemical oxygen demand by Spirulina platensis from wastewater-
supplemented culture medium, Journal of Environmental Science and Health, Part A: Toxic/Hazardous Substances and
Environmental Engineering, 47:12, 1818-1824

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 Journal of Environmental Science and Health, Part A (2012) 47, 1818–1824
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ISSN: 1093-4529 (Print); 1532-4117 (Online)

DOI: 10.1080/10934529.2012.689539

Chromium (VI) biosorption and removal of

chemical oxygen demand by Spirulina platensis
from wastewater-supplemented culture medium

CLINEI D. MAGRO, MAITÊ C. DEON, ANDREIA DE ROSSI, CHRISTIAN O. REINEHR,

MARCELO HEMKEMEIER and LUCIANE M. COLLA
Laboratory of Fermentations, Course of Environmental Engineering, College of Engineering and Architecture, University of Passo
Fundo, Passo Fundo, Rio Grande do Sul, Brazil
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The inappropriate discharge of wastewater containing high concentrations of toxic metals is a serious threat to the environment.
Given that the microalga Spirulina platensis has demonstrated a capacity for chromium VI (Cr (VI) biosorption, we assessed the ideal
concentration of chromium-containing wastewater required for maximum removal of Cr (VI) and chemical oxygen demand (COD)
from the environment by using this microalga. The Paracas and Leb-52 strains of S. platensis, with initial wastewater concentrations
of 0%, 12.5%, 25%, and 50%, were cultured in Zarrouk medium diluted to 50% under controlled air, temperature, and lighting
conditions. The cultures were maintained for 28 days, and pH, biomass growth, COD, and Cr (VI) were assessed. The wastewater
concentration influenced microalgal growth, especially at high concentrations. Removal of 82.19% COD and 60.92% Cr (VI) was
obtained, but the COD removal was greater than the Cr (VI) removal in both strains of S. platensis.
Keywords: Biosorption, Spirulina platensis, Chromium (VI), COD.

Introduction Given the increase in wastewater production, it is

Water and soil contamination by toxic metals is a serious
environmental problem.[1] These toxic metals accumulate in
the environment and may eventually affect the food chain,
causing several dangerous effects in humans.[2,3] Chromium
easily leaches into the water table, reservoirs, and rivers used
as sources of water for the population.[4] Residue in the soil
can be taken up by plants, which will later be eaten by
humans and animals.[3]
As discussed by Ruotolo and Gubulin,[5] wastewater con-
taining hexavalent chromium cannot be discharged directly
into water bodies or into the sewage system because of its
high toxicity, which is confirmed by its carcinogenic ac-
tivity. Thus, industries should adjust their processes and
technologies aimed at reducing the effects of contamina-
tion by toxic metals should be developed to minimize the
environmental impact.
Address correspondence to Luciane M. Colla, Laboratory of Fer-
mentations, Course of Environmental Engineering, College of
Engineering and Architecture, University of Passo Fundo, Cam-
pus I, km 171, BR 285, P.O. Box 611, CEP 99001-970, Passo
Fundo, RS, Brazil; E-mail: lmcolla@upf.br
Received December 16, 2011.
necessary to seek technically and economically efficient
alternatives to reduce pollution levels.[6] Several methods
have been used for the removal of metal ions from solu-
tions, including chemical precipitation,[7] ion exchange,[8]
adsorption,[9,10] and electrochemical treatment,[11] but they
are not always efficient. In addition, they are prohibitively
expensive,[1] especially when applied to diluted metal
solutions.[6] Therefore, the search for new technologies in
wastewater treatment, with advantages in addition to the
cost-effectiveness of the process, has inspired interest in
the biosorption process.[1]
Biosorption is defined as the uptake of toxic metals by
living or dead microorganisms (biomass).[6] According to
Pietrobelli et al.,[12] biosorption is an efficient alternative to
conventional wastewater treatments because the microor-
ganisms absorb metals and promote self-regeneration of
the wastewater, thereby qualifying the process. Thus, the
biosorption process is a thriving technology with expand-
ing applications for the treatment and final polishing of
wastewater containing toxic metals.[13]
Different biological materials have been used for biosorp-
tion of toxic metals, such as bacteria,[14–16] algae,[17,18]
and aquatic macrophytes.[13–19] Among the microorgan-
isms used, algae have been widely utilized as biomass in
the biosorption of toxic metals because of their abundance
 Spirulina platensis used for Cr (VI) biosorption and chemical oxygen demand removal
and structural richness, replacing conventional resins.[20]
The advantages of algal biomass include low cost and good
efficiency.[1] Algae can be used in the treatment of residual
waters, biological detoxification, and control of toxic met-
als in natural waters or in industrially contaminated waters
because they can accumulate metals in their external wall
through physical, chemical, and biological mechanisms.[21]
Algae have become an important source for studies on
the removal of toxic metals from wastewaters because
of their capacity to retain and immobilize these com-
pounds.[22] In this scenario, Spirulina platensis is prominent
because this microalga has shown a large capacity to re-
move metal ions from aqueous solutions.[23,24]
Viacelli et al.[25] investigated the potential of S. platen-
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sis in the removal of cadmium and lead from synthetic
wastewaters and reported efficiencies of 98% and 99%, re-
spectively. Other algae have been used: Sargassum sp. was
used by Saravanan et al.[17] for the removal of chromium
and zinc, with success rates of 65% and 53%, respectively.
Gupta et al.[26] assessed chromium VI (Cr (VI)) biosorption
by using the biomass from filamentous algae of the genus
Spirogyra, and they noted the removal of approximately
14.7 × 103 mg of metal per kg of dry weight of biomass at
an initial concentration of 5 mg/L. To corroborate the ad-
vantages of using microalgae for wastewater treatment, it is
necessary to conduct studies that prove the great potential
of these microorganisms to remove toxic metals.
Because of the numerous environmental and human
health problems caused by the inappropriate discharge of
chromium-containing wastewater, efficient solutions that
promote the proper treatment of this wastewater have been
sought to prevent wastewater discharge with high concen-
trations of this metal, which would lead to an imbalance in
natural environmental conditions. Therefore, in this study,
we aimed to assess the ideal concentration of chromium-
containing wastewater for maximum removal of Cr (VI)
and chemical oxygen demand (COD) by S. platensis.
Materials and methods
Wastewater collection and characterization
The wastewater was provided by the Laboratory of Soil
Analysis of the School of Agronomy and Veterinary
Medicine, Universidade de Passo Fundo (UPF), South-
ern Brazil. The wastewater was characterized in terms of
pH, COD, Cr (VI), suspended solids, and settleable solids,
according to the methods described in the Standard meth-
ods for the analysis of water and wastewater published by
the American Public Health Association (APHA).[27]
Microorganism and inoculum maintenance
We used the Leb-52 and Paracas strains of S. platensis,
available at the Laboratory of Fermentations of Universi-
dade de Passo Fundo. The microalgae were kept in a non-
1819
sterile thermostat-controlled oven aerated by diaphragm
pumps at 30◦ C, with a 12-h photoperiod and illumina-
tion of 1,800 lux provided by 20-W fluorescent lamps. The
Zarrouk[28] medium, which is the standard medium used for
the cultivation of this microalga, was diluted to 50% with
sterile distilled water and was used for inoculum mainte-
nance.
Experiment planning and culture conditions
The effect of the strain (either Leb-52 or Paracas) and the
initial concentration of chromium-containing wastewater
(0%, 12.5%, 25%, and 50%) on microalgal growth, Cr (VI)
biosorption, and COD removal were assessed by a 21.41
Multilevel Factorial Design, as described in Table 3. The
experiments were performed in 2-L Erlenmeyer flasks with
an initial medium volume of 1.8 L and initial inoculum
concentration of 0.15 g/L in a thermostat-controlled oven
at 30◦ C, a 12-h photoperiod, illumination of 1,800 lux, and
constant aeration. The Zarrouk[28] medium was used as
culture medium for wastewater dilution.
Analytical determinations
Samples were collected daily from the culture media to de-
termine pH and cell concentration. The pH of the samples
was measured using a DIGIMED pH meter (model DM-
22). Cell concentration was calculated using a predefined
ratio (standard curve) of cell concentration (g·L−1) to the
absorbance of cultures at 670 nm. The cultures were main-
tained for 28 days, and the maximum biomass concentra-
tions (Cmax ) and maximum specific growth rate (µmax ) for
each experiment were obtained from biomass concentra-
tion results relative to time. The maximum specific growth
rate was obtained by the exponential regression of cell con-
centration in the logarithmic growth phase versus culture
time, which was calculated using Eq. 1, where µ = specific
growth rate (d−1), x = biomass cell concentration (g·L−1),
and t = time (d).
On the basis of maximum specific growth rates, the time
necessary for biomass duplication, which is known as gen-
eration time (gt), was calculated using Eq. 2, where gt =
generation time (d) and µmax = maximum specific growth
rate (d−1).



1 dx
µ= . (1)
x dt
ln 2
gt = (2)
µmax
Cr (VI) and COD concentrations were determined us-
ing the absorbance of the samples measured using a spec-
trophotometer at 540 nm and 600 nm (Standard methods
for the analysis of water and wastewater, published by the
APHA[27]), respectively, and the results were calculated
 1820 Magro et al.
Table 1. Characterization of chromium-rich wastewater. Table 2. Legal limits for total chromium discharge in selected
countries.
Coefficient of
Parameter Mean ± SD variation (%) Legal limits for chromium discharge
(mg·L−1)
COD (mg·L−1) 2, 005.00 ± 18.81 0.94
Cr VI (mg·L−1) 23.40 ± 0.06 0.26 Country Superficial water Sewage systems
Suspended solids (mg·L−1) 240.98 ± 20.95 8.69
Settleable solids (mL·L−1) 2.07 ± 0.06 2.79 Austria 4.0 15
pH 1.69 ± 0.01 0.34 Brazil 0.5 0.5
France 1.0 –
Italy 2.0 4.0
Portugal 2.0 2.0
using specific standard curves for each parameter at the Spain 2.0 4.0
initial time, 7 days, 14 days, 21 days, and 28 days. Cr (VI)
and COD removal rates were obtained using Equation 3, Source: Adapted from Tahir and Naseem.[39]
where Cf = final concentration (mg·L−1) and Ci = initial
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concentration (mg·L−1). Cr (VI) and COD removal data waters and sewage systems (Table 2). As outlined in Table 2,
were analyzed using analysis of variance and Tukey’s test Brazil is one of the most restrictive countries when it comes
to compare mean values. to the discharge of chromium-containing wastewaters, with

 the lowest allowable level (0.5 mg·L−1) for both superficial
cf
Removal(%) = 1 − · 100 (3) waters and sewage systems.
ci Given the maximum allowable levels for the discharge
of chromium-containing wastewaters, one can see that the
wastewater assessed in this study is contaminated by high
Results and discussion levels of Cr (VI) (23.40 mg·L−1), a contamination value
that far exceeds values established by state, national, and
Wastewater characterization international environmental laws. However, it should be
stressed that the wastewater used in this study was later
The high pollutant load of the wastewater is shown by treated at a wastewater treatment plant (WTP).
COD and Cr (VI) values (Table 1). In Brazil, wastewater
discharge is regulated by Resolution 357/2005 and is com-
plemented by Resolution 397/2008, both of which were es- Microalgal growth and Cr (VI) and COD removal
tablished by the Brazilian National Environmental Council Figures 1 and 2 show graphs of biomass concentration
(CONAMA) from the Ministry of Environment. However, (g.L−1) versus culture time (d) for the experiments of the
in the case of COD, these federal resolutions do not estab- multilevel factorial design. Table 3 presents the microal-
lish any standards for wastewater discharge, but state laws gal growth parameters obtained during cultivation as well
set maximum limits for this parameter. as the Cr (VI) and COD removal rates at the end of the
In the state of Rio Grande do Sul, Resolution 128/2006, experiment.
issued by the State Environmental Council (CONSEMA)
from the State Department of Environmental Protection,
establishes discharge standards according to wastewater
flow, limiting COD discharge to 400 mg·L−1 for the lowest
flow. Internationally, the U.S. Environmental Protection
Agency (EPA) restricts COD discharge to 120 mg·L−1.[29]
This indicates a high concentration of organic load
in the wastewater because the COD concentration
(2,005 mg·L−1) is 5-fold higher than the concentration
allowed by Brazilian laws.
The maximum overall chromium concentration in
wastewaters allowed by CONAMA’s Resolution 357/2005
is 0.5 mg·L−1 of chromium. CONAMA’s Resolution
397/2008 sets maximum values of 1.0 mg·L−1 and
0.1 mg·L−1 for Cr (III) and Cr (VI), respectively. The state
of Rio Grande do Sul CONSEMA’s Resolution 128/2006 Fig. 1. Cell concentration (g·L−1) versus culture time (d) for Spir-
establishes a maximum discharge of 0.1 mg·L−1 for Cr (VI). ulina platensis Paracas. Experiment 1 (0% wastewater), experi-
In other countries, there are specific laws that govern the ment 2 (12.5% wastewater), experiment 3 (25% wastewater), and
maximum allowable discharge of this metal into superficial experiment 4 (50% wastewater).
 Spirulina platensis used for Cr (VI) biosorption and chemical oxygen demand removal 1821
Table 3. Experimental conditions, initial chromium concentration in relation to the initial wastewater concentration, microalgal
growth patterns, and Cr (VI) and COD removal rates.
Wastewater Cr (VI)
concentration Cr (VI)i max C µmax
log removal (%) COD removal
Exp. Strain (X1 ) (%) (X2 ) (mg·L−1) (g·L−1) (d −1) gt (d) (d) R2 ± SD (%) ± SD

1 Paracas (−1) 0.0% (−2) 0.000 2.08 0.076 9.12 0–25 0.98 0.00 0.00
2 Paracas (−1) 12.5% (−1) 2.925 1.38 0.060 11.55 0–25 0.98 58.55 ± 0.09 81.37 ± 3.16
3 Paracas (−1) 25.0% (+1) 5.850 0.51 0.090 7.70 0–6 0.98 47.94 ± 0.15 80.42 ± 6.22
4 Paracas (−1) 50.0% (+2) 11.700 0.58 0.072 9.62 0–8 0.96 52.11 ± 0.60 77.76 ± 2.49
5 Leb-52 (+1) 0.0% (−2) 0.000 2.76 0.095 7.30 0–21 0.96 0.00 0.00
6 Leb-52 (+1) 12.5% (−1) 2.925 1.21 0.069 10.00 0–15 0.90 60.92 ± 0.10 81.02 ± 2.65
7 Leb-52 (+1) 25.0% (+1) 5.850 0.86 0.060 11.55 0–19 0.93 53.01 ± 0.15 78.06 ± 4.31
8 Leb-52 (+1) 50.0% (+2) 11.700 0.46 0.105 6.60 0–7 0.96 45.71 ± 0.51 77.33 ± 5.24
Cr (VI)i = Initial Cr (VI) concentration; max C = maximum cell concentration; µmax = maximum specific growth rate; gt = generation time;
log =
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time values used in the exponential regression; R2 = coefficients of determination of the regression.

Figures 1 and 2 show that the cultures with chromium-
containing wastewater added to the Zarrouk medium
(experiments 2, 3, 4, 6, 7, and 8) yielded lower biomass
concentrations than the cultures maintained in Zarrouk
medium alone (experiments 1 and 5). This result can
be explained by the fact that Zarrouk medium is the
standard medium used for the cultivation of Spirulina,
and it has the appropriate concentrations of nutrients
necessary for photosynthetic metabolism. The addition of
chromium-containing wastewater and COD requires the
microorganism to adapt to mixotrophic metabolism as the
medium becomes an organic source of carbon and to adapt
to the toxic effect produced by Cr (VI) bioaccumulation.
As the concentration of wastewater, and consequently of
Cr (VI), increases, the maximum biomass concentration
decreases, demonstrating the toxic effect of this metal on
cell metabolism.
Toxic metals can cause adverse effects on biological sys-
tems, indirectly producing breaks in the double-stranded
DNA via oxidative stress.[30] This stress develops because of
an imbalance triggered by excessive production of oxidants
or by a reduction in antioxidants.[31] Zhitkovich[32] assessed
the risks of chromium in potable water and observed that
this metal can cause dysfunctions in cell metabolism by
damaging the DNA through mutations that lead to chro-
mosome breakage and impairment in cell development.
The cell concentrations of 2.08 g/L for the Paracas strain
and 2.76 g/L for the Leb-52 strain that were obtained in
experiments 1 and 5 (standard medium) are consistent with
those reported by other authors for Spirulina cultures that
were maintained in similar temperature and lighting con-
ditions as those used in this study.[33,34] The high cell con-
centrations obtained at the end of experiments 1, 2, 5, and
6 were the result of the microorganisms remaining in the
exponential growth phase for longer periods than in the
other experiments (
log of 25 days, 25 days, 21 days, and
15 days, respectively). Figure 3 shows Cr (VI) (%) removal
in relation to culture time (d), strain, and initial wastewater
concentration (%).

Fig. 2. Cell concentration (g·L−1) versus culture time (d) for Spir-
ulina platensis Leb-52. Experiment 5 (0% wastewater), experiment
6 (12.5% wastewater), experiment 7 (25% wastewater), and exper- Fig. 3. Cr (VI) removal (%) in relation to culture time (d), strain,
iment 8 (50% of wastewater). and wastewater (WW) concentration (%).
 1822
The highest Cr (VI) removal amount in the experiments
conducted with the Paracas strain, regardless of the Cr (VI)
concentration, were observed at 28 days of culture (p <
0.05). However, the comparison between removal rates at
28 days and 21 days of culture revealed that, despite statis-
tical differences between removal rates (p < 0.05), the addi-
tional amount of Cr (VI) removed from the culture medium
does not justify maintaining the cultures for an additional
7 days. This observation is valid even if cultures are used in
open raceway ponds and under natural light because of the
costs involved with the shaking system necessary for the
homogenization of cultures in open raceway ponds.
Cr (VI) removal by the Leb-52 strain increased with
culture time for the experiments containing 12.5% and
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25% wastewater (Figure 3). The highest removal amount
(60.92%) was obtained with 12.5% wastewater and 28 days
of culture; this is significantly higher (p < 0.05) than
the other removal amounts under the same conditions.
Interestingly, the Cr (VI) removal rate was greater than
40% at 7 days of culture with an initial 50% wastewater
concentration.
The comparisons of the mean values for Cr (VI) removal
rates (Tukey’s test at 5% significance) for the Leb-52 strain
and 50% wastewater revealed no significant differences be-
tween the removal rates obtained at 7 and 14 days of culture
(p > 0.05) (42 to 43%). However, these rates were higher
(p < 0.05) than those obtained at 21 and 28 days of culture
(∼ 45%). No significant difference (p > 0.05) was observed
between the removal rates at 21 and 28 days of culture.
Cell death occurred in the Leb-52 strain experiment with
50% wastewater, possibly due to a high bioaccumulation
of toxic metal that prevented microalgal growth. After
cell death, flocculation of the microalga was observed,
thus facilitating the separation of cells that contained the
metal.
The removal rates of the toxic metal observed in this
study were similar to those observed in previous reports.
Saravanan et al.[17] reported removal rates of 65% for
chromium by Sargassum sp. Módenes et al.[13] investigated
the biosorption efficiency of dry Egeria densa in the re-
moval of zinc (II) and observed removal amounts greater
than 70%. Lima et al.[19] assessed the biosorption of Cr (III)
by Lemna minor and reported the removal of 12.32 mg·g−1
of the metal and concluded that this biomass was efficient
in the treatment of residual water containing Cr (III).
Figure 4 shows COD removal (%) in relation to culture
time (d), strain, and wastewater concentration (%). For the
Paracas strain, COD removal rates in the experiments with
12.5% wastewater at 14, 21, and 28 days of culture were
around 80%; this value was significantly higher (p < 0.05)
than the COD removal rate at 7 days of culture (71.7%).
Similarly, in the Paracas strain experiments with 25% and
50% wastewater, COD removal rates at 21 and 28 days
of culture were significantly higher (p < 0.05) than those
obtained at 7 and 14 days of culture. Despite the significant
difference between COD removal rates with 12.5% and 50%
Magro et al.
Fig. 4. COD removal (%) in relation to culture time (d), strain,
and wastewater (WW) concentration (%).
wastewater at 21 and 28 days of culture (81% and 77% of
removal, respectively; p < 0.05), it is possible to say that
the addition of 50% wastewater is advantageous because
it contains 4 times the amount of treatable wastewater in
relation to 12.5% wastewater.
A similar analysis can be performed by observing the
COD removal rate obtained with the Leb-52 strain, where
increasing the wastewater concentration in the cultures
reduces COD removal because of the toxic effect of
chromium, which affects cell concentration and, conse-
quently, the COD removal. For this strain, removal rates
from 50% wastewater at 14 and 21 days were not signifi-
cantly different (p < 0.05), which justifies the use of 50%
wastewater for 14 days of culture. Although lower concen-
trations of wastewater yield higher COD removal rates, less
wastewater is treated across the same time interval.
Even though S. platensis is known as an autotrophic
cyanobacterium, this microalga can be mixotrophic[35,36]
in wastewater treatment that consists of the uptake of
organic compounds from culture media associated with
photosynthetic metabolism. However, this does not fully
explain the high efficiency of COD removal obtained
in this study. The increase in pH and the removal of
microalgae from the medium due to cell death might
have also contributed to COD removal. The presence of
heterotrophic bacteria capable of metabolizing the COD
of the wastewater in the bioreactors was ruled out because
the pH of the medium was not conducive for growth in
either the raw wastewater or the culture medium. Another
possible explanation for the efficient COD removal is the
partial removal of COD by aeration.
Biological treatment is sufficiently efficient in remov-
ing organic matter (COD) from wastewater.[37] Mezzomo
et al.[38] investigated COD removal by S. platensis from pig
wastewater and observed removal rates of around 79.3%
 Spirulina platensis used for Cr (VI) biosorption and chemical oxygen demand removal
and 84.3%, thus demonstrating the efficiency of this mi-
croalga in COD removal.
[7]
After analyzing the potential of these S. platensis strains
in chromium and COD removal, we believe that the condi-
tions that yielded higher Cr (VI) removal should be further [8]
investigated in future studies because of the toxicity of this
metal and its effects on the environment and human health.
Therefore, the best Cr (VI) and COD removal results were
[9]
obtained with the Leb-52 strain, 50% wastewater added to
the Zarrouk medium, and 7 days of culture. The culture
maintained for 14 days instead of 7 days has the advantage
of a higher COD removal by the microalga; however, [10]
the number of cells generated for later disposal would also
be higher. In addition, COD removal can be performed [11]
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later by WTP. However, Cr (VI) removal is very important
because it minimizes the deleterious effects of this metal
on the microorganisms used in biological treatment in
[12]
WTPs.
[13]
Conclusions
This study provided important information about Cr (VI) [14]
removal by S. platensis. The Leb-52 strain of this microalga
could remove up to 42% of Cr (VI) from culture media
with 50% wastewater containing 23.40 mg·L−1 of Cr (VI).
[15]
COD removal from these cultures can be as high as 75%
if they are maintained for 14 days. This study demonstrated
that S. platensis can lead to Cr (VI) bioaccumulation. Fur- [16]
ther studies should be performed to assess whether this
microalga can metabolically convert Cr (VI) into Cr (III),
which is less toxic than Cr (VI), and whether chromium re- [17]
moval can be increased if the initial cultures contain higher
cell concentrations.
[18]
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