471 © IWA Publishing 2012 Water Science & Technology | 65.

3 | 2012

Biosorption of chromium(VI), nickel(II) and Remazol Blue

by Rhodotorula muciloginosa biomass
Nalan Oya San and Gönül Dönmez

ABSTRACT
Nalan Oya San
The passive removal of commonly used reactive dye and two heavy metals, from aqueous solutions
Institute of Biotechnology,
by inexpensive biomaterial, yeast Rhodotorula muciloginosa biomass, termed biosorption, was Ankara University,
06100 Beşevler-Ankara,
studied with respect to pH, initial dye concentration and initial metal ion concentration. The biomass Turkey

exhibited maximum dye and chromium(VI) uptake at pH 5 and pH 6 for nickel(II) in media containing Nalan Oya San
Gönül Dönmez (corresponding author)
50 mg/L heavy metal and 50 mg/L remazol blue. It was found that the highest chromium(VI) removal Faculty of Science,
Department of Biology,
yields measured were 31.3% for 49.0 mg/l initial chromium(VI) concentrations. The nickel(II) removal
06100 Beşevler-Ankara,
yield was 32.5% for 22.3 mg/L. Higher R. Blue removal yields were obtained, such as 77.1% for Turkey
E-mail: gdonmez@ankara.edu.tr
117.5 mg/L. The maximum dye biosorption yield was investigated in medium with a constant dye
(∼50 mg/L) and increasing heavy metal concentration. In the medium with 48.8, 103.8 and 151.8 mg/L
chromium(VI) and constant dye concentration, the maximum chromium(VI) biosorption was 7.4, 9.3
and 17.1%, whereas the maximum dye biosorption was 61.6, 56.6 and 55.9%. The maximum nickel(II)
biosorptions in the medium with dye were 38.1, 22.1 and 8.8% at 23.7, 37.7 and 60.1 mg/L nickel(II)
concentrations. In these media, dye biosorptions were 93.9, 86.4 and 93.3%, respectively.
Key words | biosorption, heavy metal, reactive dye, wastewater treatment, yeast

INTRODUCTION

A great number of industries such as textile, printing, paper
and pulp, iron-steel, pesticide, paint, solvent, and pharma-
ceuticals consume large volumes of water, and organic
based chemicals. These chemicals show a large difference
in chemical composition such as molecular weight, tox-
icity, etc. In addition, effluents of these industries contain
undesired quantities of these pollutants and need to be trea-
ted (Lloyd-Jones et al. ; Aksu ). The heavy metal
pollution is of greatest concern among the kinds of
environmental pollution because of high toxicity and mobi-
lity of heavy metals. In addition, colour removal has been
the target of great attention in the last few years due to
these highly coloured industrial effluents substantially
affecting visibility and photosynthesis in the water and
being toxic to the aquatic life due to the presence of
metals, chlorides and other compounds (Chapman & Kim-
stach ; Slokar & Le Marechal ; Mahony et al.
). Many synthetic dyestuffs and heavy metals are resist-
ant to biological degradation that cannot be biodegraded
due to their complex aromatic molecular structures; so,
colour and heavy metal removals by traditional biological
processes are difficult (Ozcan & Ozcan ; Ahmad
et al. ). Lately, many physical and chemical treatment
methods including adsorption, filtration, chemical coagu-
lation, precipitation, electrodialysis, membrane separation
and oxidation have been used for the treatment of dye
and heavy metal containing effluents. Some of these tech-
niques have been shown to be effective, although they
have limitations such as overall cost, regeneration pro-
blems, limit versatility and secondary pollutants (Ong
et al. ; Crini ). Biosorption is an effective technol-
ogy using inactive and dead biomasses to remove pollutant
from aqueous solutions in the absence of metabolic activity
necessary for intracellular accumulation (Ileri & Mavituna
; Esposito et al. ; Davis et al. ). On the other
hand, biosorption represents passive interactions of the
cell wall with metal ions. These reactions include adsorp-
tion, ion exchange reactions with functional groups at the
cell surface, and surface reactions. Metal ion binding sites
which are localized at the cell surface include carboxylic,
hydroxyl, and phosphate groups of lipids, proteins,
and polysaccharides (Beveridge ; Yalçın et al. ).

doi: 10.2166/wst.2012.872
 472 N. O. San & G. Dönmez | Biosorption of heavy metals and dye by Rhodotorula muciloginosa
In addition, the use of dead biomass appears to be more
attractive as compared with live biomass, as heavy
metals or other toxic pollutants have little influence on
the biosorption process. Besides, there is no requirement
for the supplement with any nutrients for maintaining
growth of dead biomass. Metal ions, chromium(VI) and
nickel(II) were chosen for biosorption studies with regard
to their wide and common use in industry and potential
pollution impact. Hexavalent chromium from electroplat-
ing and similar industries has been reported to be toxic
to animals and humans; it is known to be carcinogenic
and to create ecological problems (Mungasavalli et al.
; Chatterjee et al. ). Nickel(II) has been used in
many processes such as electroplating, leather tanning,
wood preservation, pulp processing, steel manufacturing,
plastics pigments, mining and metallurgical processes
then discharged into the environment (Aksu & Dönmez
; Gupta et al. ). Compared with nickel(IV),
nickel(II) is a more toxic and carcinogenic metal. This situ-
ation is due to its toxic effects on living systems, so strict
limits have been stipulated for discharge of nickel(II) into
the environment. R. Blue which was used in this study is
a reactive dye. Reactive dyes are typically azobased chro-
mophores combined with different types of reactive
groups e.g. chlorotriazine, vinyl sulfone. Reactive dyes are
different from the the other classes of dyes that bind to
the textile fibers, e.g. cotton, through covalent bonds.
They are used extensively in textile industries because of
they have bright colours, simple application techniques
and low energy consumption. Therefore their removal is
of great importance (Sumathi & Manju ; Robinson
et al. ). A variety of biomaterials have been investigated
as biosorbents, such as bacteria (Vijayaraghavan & Yun
), fungi (Aksu et al. ), algae (Apiratikul & Pavasant
), agricultural wastes (Sud et al. ), industrial waste
(Wang & Chen ) and other polysaccharide materials
(Crini & Badot ). Yeasts are a better crude biosorbent
material for the removal of heavy metal ions or dyes
because of their unicellular structure and high growth
rate (Aksu & Dönmez ). In addition, yeast cells can
be easily cultivated into inexpensive growth media, and
have the potential for bioremediation of wastes at lower
pH values (Vasudevan et al. ; Malik ). Much of
the work on the biosorption focusing on the uptake of
single pollutants such as cadmium and lead biosorption
by the Rhodotorula genus of yeast has been documented
(Cho & Kim ; Li & Yuan ). In practice, waste-
waters are polluted with multiple components. For this
reason, in this study, a process of biosorption of
Water Science & Technology | 65.3 | 2012
chromium(VI) and nickel(II) and R. Blue dye onto
R. muciloginosa was investigated in medium with an
increasing heavy metal and dye concentration and constant
dye (approximately 50 mg/L) and increasing heavy metal
concentration. These heavy metals and dye were chosen
because of their widespread use in Turkish industry with
relatively high consumption rate and being quite common
pollutants in wastewaters from the textile industry. As
little is known of the biosorption of heavy metals and
dyes to yeast biomass, the biosorptive properties of the
microorganism for heavy metals and dye should be investi-
gated. In addition, the understanding of the biosorptive
function of dead R. muciloginosa is essential for the
design of a process that makes efficient use of such a
biosorbent.
METHODS
Dye and heavy metal solutions
The stock solutions of chromium(VI) and nickel(II) were
prepared by dilution of K2Cr2O7 (Merck) and NiSO4
(Merck) to a final concentration of 1 g/L of chromium(VI)
and nickel(II). The test solutions containing R. Blue reactive
dye were prepared by diluting 2 g/L of stock solution of the
dye. Appropriate volumes of the stock solutions were added
to the media.
Isolation of yeast
Samples uptake from textile wastewaters was centrifuged
and spread on (0.1 mL) the Petri plates containing mol-
asses media with 50 mg/L R. Blue and 50 mg/L heavy
metal (chromium and nickel) and incubated at 30 ± 1 C.
W
The composition of the growth medium is molasses sol-
ution (nearly equivalent to 10 g/L sucrose), 1.0 g/L
NH4SO4 and 0.5 g/L KH2PO4 (Aksu & Dönmez ).
Agar (15 g/L) was added for plates. The pH of the
growth medium was adjusted to pH 5 for nickel(II) and
pH 6 for R. Blue and chromium(VI) by dilute (0.01 mol/L)
and concentrated (1 mol/L) H2SO4 or NaOH solutions.
Cells from microcolonies on these plates were isolated
and purified and streaked repeatedly on the molasses
medium agar plate with R. Blue and heavy metals. The
W
pure cultures were kept at 4 C and were transferred to
molasses media including R. Blue and heavy metals every
3 months.
 473 N. O. San & G. Dönmez | Biosorption of heavy metals and dye by Rhodotorula muciloginosa Water Science & Technology | 65.3 | 2012

PCR and sequencing (2), respectively.

The exponential phase bacterium was used for 18S rRNA E ¼ ((C0  Cf )=C0 ) × 100% (1)
gene amplification. PCR was carried out by 25 cycles of
W W
denaturation step at 96 C for 10 s, annealing at 50 C for Q ¼ (C0  Cf )V=W (2)
W
5 s and elongation at 60 C for 4 min. The primer set used
in PCR reaction was the D1/D2 region of large-subunit where, C0 (mg/L) and Cf (mg/L) are the initial and residual
rDNA sequencing and phylogenetic analysis was carried concentration of metal ion/dye, respectively. V (L) and W
out as described by Fell et al. () and Biswas et al. (). (g) are the solution volume and the dosage of biosorbent,
respectively.
Preparation of biosorbent: Yeast

Yeast cells were grown in molasses media at pH 5 value at

RESULTS AND DISCUSSION
30 ± 1 C on a rotary shaker for 2 days. The biomass was
W

centrifuged 3.421g for 10 min (Hettich EBA12). The pellet

W Effect of initial pH on chromium(VI), nickel(II) and
was exterminated by autoclaving (Alp CL-40M) at 121 C
for 15 min. 1.25 g of assassinate biomass was added to the
biosorption flasks according to the biomass found in pre-
vious bioaccumulation studies (Ertugrul et al. ).
Biosorption studies
The experiments were performed in 250 ml Erlenmeyer
flasks containing solutions of different R. Blue concen-
trations 50, 100, 200, and 400 mg/L, chromium(VI)
concentration 50–150 mg/L and nickel(II) concentration
50–100 mg/L in 100 mL water. Samples (3 mL) were taken
at the end of 1 h and centrifuged at 3.421g for 10 min. The
supernatant was analyzed for the remaining dye and heavy
metal concentration.
Analytical methods
A 3 mL sample was taken from each flask, at the end of a 1 h
incubation period. Dissolved dye concentrations of R. Blue
in the biosorption medium were measured calorimetrically
using a spectrophotometer (Shimadzu UV 2001, Japan).
The absorbance of the colour of R. Blue was read at
600 nm. The concentration of nickel(II) in the supernatant
was determined spectrophotometrically at 340 nm by using
sodium diethyl dithiocarbamate as the complexing agent
for nickel(II), respectively (Snell & Snell ). The concen-
tration of chromium(VI) in the supernatant was determined
spectrophotometrically at 540 nm using diphenylcarbazide
reagent in acid solution as the complexing agent for chro-
mium(VI). Experiments were conducted in triplicate and
the results are the average of triplicate measurements.
Finally, the percentage biosorption (E, %) and uptake
capacity (Q, mg/g) were calculated by Equations (1) and
Remazol Blue uptakes
The pH of metal and/or dye solution plays an important role
in the whole biosorption process and particularly in the
adsorption capacity, influencing the surface charge of the
biosorbent, degree of ionization of the species present in
the solution and the dissociation of functional groups on
the active sites of biosorbent, and the solution metal and
dye chemistries. Optimal pH for the biosorption exper-
iments was found in previous bioaccumulation
experiments by Ertugrul et al. (). According to these
experiments, optimal pH values for the yeast cells to
remove the pollutants were, pH 6 for only dye and chro-
mium(VI) and dye, and pH 5 for nickel(II) and dye in
media containing 50 mg/L heavy metal and 50 mg/L
R. Blue. Low pH has been found to favour adsorption of
dyes and heavy metals (Bai & Abraham ) by the biomass
of yeast and fungi.
Single effect of initial dye and heavy metal
concentration on biosorption
R. Blue biosorption by R. mucilaginosa was investigated at
different initial dye concentrations between 54.9, 117.5,
173.5 and 365.1 mg/L at pH 6. As shown in Figure 1, maxi-
mum dye biosorption yield was 77.1% for 117.5 mg/L. The
yeast species was capable of removing more than 50% of
the colouring material at 50 mg/L of initial dye concen-
tration. This suggests that the adsorbent capacities of all
the biosorbents were most effectively utilized in solutions
of this initial dye concentration. Reactive dye biosorption
was also reported in previous studies performed with dried
yeast cells. For example Aksu & Dönmez () reported
 474 N. O. San & G. Dönmez | Biosorption of heavy metals and dye by Rhodotorula muciloginosa Water Science & Technology | 65.3 | 2012

Figure 1 | The single effect of initial dye concentration (C0) on the biosorption yield of Figure 3 | The single effect of initial nickel(II) concentration (C0) on the biosorption yield
of R. mucilaginosa (pH: 5; T: 30 ± 1 C; stirring rate: 100 rpm, X: 1.25 g/L).
W
R. mucilaginosa (pH: 6; T: 30 ± 1 C; stirring rate: 100 rpm, X: 1.25 g/L).
W

are metals with a low affinity for biosorption (Holan &

the biosorption capacities and rates of nine yeast species
Volesky ). The higher dye uptake obtained at acidic con-
(S. cerevisiae, S. pombe, K. marxianus, Candida spp.,
ditions may be explained in terms of electrostatic
C. tropicalis, C. lipolytica, C. utilis, C. quilliermendii, and
interactions between the surface of R. mucilaginosa biomass
C. membranaefaciens) for R. Blue reactive dye from aqueous
and anionic dye (Vijayaraghavan & Yun ; Akar &
solutions. Although previous studies have used
Divriklioglu ).
yeasts for removing reactive dye from effluents, the biosorp-
In the experiments with Candida tropicalis and
tion of reactive dye by Rhodotorula spp. has not been
Candida lipolytica, yeasts biosorped 20 mg/L chromium
reported.
(VI) at pH 2 with 25 g/L biomass and 81.37%, while for
Biosorption capacities of the yeast cells at 49, 127.1 and
nickel(II) 0.351 mmol/L and 64.6% in 4 h (Yin et al. ).
165.7 mg/L initial chromium(VI) concentrations and 22.3,
However in our studies, we used less biomass and our exper-
47.7 and 62.2 mg/L initial nickel(II) concentrations, are
iments were more rapid (1 h) than other experiments.
given in Figures 2 and 3. At the end of the experiments,
the highest chromium(VI) removal yields measured were
Simultaneous effect of dye and heavy metal on
31.3% for 49 mg/L concentrations. The nickel(II) removal
biosorption
yield was 32.5% for 22.3 mg/L.
It is clearly seen in Figures 1 and 2 that the R. Blue bio-
Dye and heavy metal biosorption by R. mucilaginosa was
sorption yield of the yeast cells was significantly higher than
investigated at different initial heavy metal concentrations
that of chromium(VI) and nickel(II). The previous studies
at a constant dye concentration. These experiments were
on biosorption indicated that chromium(VI) and nickel(II)
repeated at a fixed dye concentration (39.2–51.2 mg/L) to
determine maximum dye and/or heavy metal biosorption.
The simultaneous effect of dye and heavy metal biosorption
of the yeast cells is given in Figures 4 and 5. In the medium
containing 50 mg/L dye, the chromium(VI) biosorption
stabilized at around 5–17% yield as seen in Figure 4. In the
medium with chromium(VI) after 1 h of incubation,
the dye biosorption was around 55–61% yield. When
the medium contained dye and chromium(VI), the heavy
metal uptake decreased with increasing heavy metal
concentration. In the medium containing nickel(II) there
was about 8–38% nickel(II) and 86–93% dye removal
(Figure 5). Contrary to chromium(VI), dye uptake increased-
with increasing heavy metal concentration. The higher
Figure 2 | The single effect of initial chromium(VI) concentration (C0) on the biosorption
maximum specific heavy metal uptake values for nickel(II)
yield of R. mucilaginosa (pH: 6; T: 30 ± 1 C; stirring rate: 100 rpm, X: 1.25 g/L).
W
were observed in the medium with dye if compared with
 475 N. O. San & G. Dönmez | Biosorption of heavy metals and dye by Rhodotorula muciloginosa Water Science & Technology | 65.3 | 2012

Table 1 | The comparison of the maximum specific metal and dye uptake (Q) obtained at
different heavy metal and dye concentrations (C0) after 1 h biosorption exper-
iments (T: 30 ± 1 C; stirring rate: 100 rpm, X: 1.25 g/L).
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Heavy metal Remazol Blue

Co (mg/L) Q (mg/g) C0 (mg/L) Q (mg/g)

– – 54.9 2.79 ± 1.8

– – 117.5 7.40 ± 0.9
– – 173.5 7.20 ± 1.35
– – 365.1 10.2 ± 3.45

Cr(VI)
49 1.21 ± 2.5 – –
Figure 4 | The effect of initial chromium(VI) and dye concentrations (C0) on the biosoption
127.1 3.12 ± 2.4 – –
yield of R. mucilaginosa in media with about 50 mg/L dye and increasing
chromium(VI) concentrations (pH: 6; T: 30 ± 1 C; stirring rate: 100 rpm, X: 3.89 ± 1.7 – –
W

165.7
1.25 g/L).
Cr(VI) þ Remazol Blue
48.8 0.23 ± 1.5 51.2 2.53 ± 3.2
103.8 0.77 ± 2.3 51 2.28 ± 1.8
151.8 2.06 ± 1.8 51.3 2.28 ± 1.7
Ni(II)
22.3 0.59 ± 2.5 – –
47.70 0.63 ± 1.4 – –
62.20 0.4 ± 2.3 – –

Ni(II) þ Remazol Blue

23.70 0.73 ± 1.7 37.80 2.83 ± 3.6
37.70 0.68 ± 2.5 33.30 2.29 ± 3.2
60.10 0.38 ± 2.3 39.20 2.92 ± 1.8

Figure 5 | The effect of initial nickel(II) and dye concentrations (C0) on the biosoption yield
of R. mucilaginosa in media with about 50 mg/L dye and increasing nickel(II)
concentrations (pH: 5; T: 30 ± 1 C; stirring rate: 100 rpm, X: 1.25 g/L).
W
the medium without dye. However, the maximum chromium
(VI) uptake values were reduced in the medium. In the same
medium, it was observed that maximum dye uptake values
decreased when the heavy metal concentrations were
increased. Increasing the initial heavy metals concentrations
resulted in decreasing the colour removal efficiency for yeast
species. This was due to the saturation of the sorption sites on
the biosorbent as the concentration of the dye increased.
However, higher biosorption yields were observed at lower
concentrations of dye.
The single and simultaneous effects of increased initial
dye and heavy metal concentrations on maximum specific
dye and heavy metal uptake levels after the biosorption
period are given in Table 1. The specific dye uptake in the
medium without heavy metal increased in parallel to the
dye concentration. The highest specific Remazol Blue
uptake was 10.2 mg/g at 365.1 mg/L dye concentration. In
the media without any dye, chromium(VI) biosorption
increased up to 2.06 mg/g chromium(VI) per g of biomass
at 151.8 mg/L initial chromium(VI) concentration, whereas
nickel(II) biosorption was only 0.63 mg/g per g of biomass
at 47.7 mg/L initial nickel(II) concentration.
In the media containing the dye and heavy metal, the
specific heavy metal uptake increased with increasing
heavy metal concentration. Higher maximum specific
heavy metal uptake values for nickel(II) were observed in
the medium with dye if compared with the medium without
dye. However, the maximum specific chromium(VI) uptake
value was reduced in the medium with dye. In the same
medium, it was observed that maximum specific dye
uptake values decreased when the heavy metal concen-
trations were increased.
CONCLUSIONS
The aim of this work was to use yeast as a biosorbent for the
removal of heavy metals and reactive dye from aqueous
 476 N. O. San & G. Dönmez | Biosorption of heavy metals and dye by Rhodotorula muciloginosa
solutions. The biosorption behavior of both chromium(VI),
nickel(II) and R. Blue on to R. mucilaginosa was investi-
gated with variations of metal and dye concentrations.
This yeast was shown to have a better uptake capacity for
R. Blue compared with chromium(VI) and nickel(II). It
was found that the highest chromium(VI) removal yields
measured were 31.3% for 49.0 mg/L initial chromium(VI)
concentrations. The maximum nickel(II) biosorption in the
medium with dye was 38.1%, at 23.7 mg/L nickel(II) con-
centrations. In addition, in these media R. Blue
biosorption was 93.9% respectively.
This work illustrated an alternative solution for the man-
agement of wastewaters where R. mucilaginosa, fast-
growing yeast compared with fungi and algae, could be, to
some extent, utilized as biosorbent for the removal of
heavy metals and dyes from wastewater.
Conventional technologies to clean up heavy-metal ions
and/or dyes from contaminated waters have been utilized,
but they remain cost ineffective. From this study, the use
of yeast with resistance to heavy metals and/or dyes for
the removal of heavy metals and dyes from contaminated
waters may be a novel and cost-effective alternative.
ACKNOWLEDGEMENT
Financial support was provided by the Scientific and Techni-
cal Research Council of Turkey (TÜBİTAK-BİDEB).
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