Bioresource Technology 96 (2005) 103–109

Biosorption of cadmium and lead ions by ethanol treated

waste baker’s yeast biomass
Yekta G€ €
oksungur, Sibel Uren, Ulgar G€
uvencß *

_
Department of Food Engineering, Engineering Faculty, Ege University, 35100 Bornova, Izmir, Turkey
Received 10 February 2003; received in revised form 15 March 2003; accepted 10 April 2003
Available online 6 May 2004

Abstract
The biosorption of cadmium and lead ions from artificial aqueous solutions using waste baker’s yeast biomass was investigated.
The yeast cells were treated with caustic, ethanol and heat for increasing their biosorption capacity and the highest metal uptake
values (15.63 and 17.49 mg g
1 for Cd2þ and Pb2þ , respectively) were obtained by ethanol treated yeast cells. The effect of initial
metal concentration and pH on biosorption by ethanol treated yeast was studied. The Langmuir model and Freundlich equation
were applied to the experimental data and the Langmuir model was found to be in better correlation with the experimental data. The
maximum metal uptake values (qmax , mg g
1 ) were found as 31.75 and 60.24 for Cd2þ and Pb2þ , respectively. Competitive bio-
sorption experiments were performed with Cd2þ and Pb2þ together with Cu2þ and the competitive biosorption capacities of the yeast
biomass for all metal ions were found to be lower than in non-competitive conditions.

2004 Elsevier Ltd. All rights reserved.

Keywords: Cadmium; Lead; Biosorption; Saccharomyces cerevisiae; Adsorption isotherms

1. Introduction tions is one of the most promising technologies which

The intensification of industrial activity during recent
years is greatly contributing to the increase of heavy
metals in the environment, mainly in the aquatic systems
(Marques et al., 2000). Conventional methods like
chemical precipitation and ion exchange used for
removing dissolved heavy metal ions from wastewaters
have significant disadvantages including incomplete
metal removal, requirements for expensive equipment
and monitoring systems, high reagent or energy
requirements or generation of toxic sludge or other
waste products that require disposal (Aksu et al., 1999).
These disadvantages of conventional systems together
with the need for more economical and effective meth-
ods for the removal of metals from wastewaters has
resulted in the development of new separation technol-
ogies. Biosorption which is a property of certain types of
inactive, dead microbial biomass to bind and concen-
trate heavy metals from even very dilute aqueous solu-
*
Corresponding author. Fax: +90-232-3427592.
E-mail address: ulgar@food.ege.edu.tr (U. G€
uvencß).
can be used for this purpose (Veglio et al., 1996; Vole-
sky, 1999). Biosorption process offers the advantages of
low operating costs, minimization of the volume of
chemical and/or biological sludge to be disposed of and
high efficiency in detoxifying very dilute effluents
(Marques et al., 2000).
In the concept of biosorption, several physical or
chemical processes may be involved such as physical
and/or chemical adsorption, ion exchange, coordina-
tion, complexation, chelation and microprecipitation.
Biomass cell walls, consisting mainly of polysaccharides,
proteins and lipids offer many functional groups which
can bind metal ions such as carboxylate, hydroxyl, sul-
phate, phosphate and amino groups. In addition to
these functional binding groups, polysaccharides often
have ion exchange properties (Sag and Kutsal, 1996;
Veglio et al., 1996; Zouboulis et al., 1999). Non-living
biomass appears to present specific advantages in com-
parison to the use of living microorganisms. Killed cells
may be stored or used for extended periods at room
temperature, they are not subject to metal toxicity and
nutrient supply is not necessary. Moreover pretreatment
and killing of biomass either by physical or chemical

0960-8524/$ - see front matter
2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biortech.2003.04.002
104 Y. G€oksungur et al. / Bioresource Technology 96 (2005) 103–109
treatments (Brady et al., 1994; Huang et al., 1990;
Zouboulis et al., 1999) or crosslinking (Leusch et al.,
1995) are known to improve the biosorption capacity of
biomass. It has also been reported that cell wall soluble
proteins, which make complexes with metal ions can be
fixed by some denaturation processes such as heat and
ethanol treatment. Deactivated yeast cells do not release
protein and exhibit higher metal ion removal capacity
than live yeast (Huang et al., 1990).
There are many reviews and reports on algae, bacte-
ria, fungi or higher plants that remove and/or accumu-
late large amounts of heavy metals from their external
environment (Gadd and White, 1993; Veglio and Beol-
chini, 1997; Volesky, 1987; Volesky and Holan, 1995).
The work reported by Volesky and Holan (1995) iden-
tifies organisms that have potential as adsorbents and
establishes also references of adsorbent capacities in
these kind of processes. Among the microorganisms
used for biosorption, Saccharomyces cerevisiae is an
inexpensive, readily available source of biomass for
heavy metal removal from wastewater. Investigations
conducted by several researchers demonstrated that S.
cerevisiae is capable of accumulating heavy metals such
as Cu2þ , Cd2þ , Pb2þ , Zn2þ , Cr2þ and Ni2þ (Brady and
Duncan, 1994; Engl and Kunz, 1995; Huang et al., 1990;
Leusch et al., 1995; Lu and Wilkins, 1996; Volesky and
May Phillips, 1995; Wilhelmi and Duncan, 1995).
The aim of this study was to test and compare treated
(killed) and untreated waste baker’s yeast cells (S. cere-
visiae) for their capacity to adsorb Cd2þ and Pb2þ .
Two adsorption models, the Langmuir model and the
Freundlich equation were applied to the experimental
data obtained for treated yeast biomass and correlations
were found for these models. The results were compared
with the study on Cu2þ biosorption by yeast biomass
treated with sodium hydroxide (G€ oksungur et al., 2003),
which was published elsewhere. Competitive biosorption
of Cd2þ and Pb2þ together with Cu2þ ions were also
studied.
2. Methods
2.1. Microorganism
Waste dried baker’s yeast (S. cerevisiae) was obtained
from Pakmaya Yeast Company, Izmir. This waste yeast
consists of oversieved (>1.5 mm) dried granular yeast
particles.
2.2. Physical and chemical treatments of yeast cells
Ethanol treated cells were prepared by suspending 5 g
of yeast cells in 100 ml of 700 g l
1 ethanol solution for
20 min at room temperature. Caustic treated cells were
prepared by mixing 5 g of yeast cells with 100 ml of
1 mol l
1 NaOH and sterilizing the resulting solution at
121 C for 15 min. After NaOH treatment, yeast cells
were collected by centrifugation (4000g; 10 min) and
washed several times with distilled water to remove ex-
cess NaOH. Heat treated cells were prepared by mixing
5 g of yeast cells with 100 ml of distilled water and
sterilizing the resultant solution at 121 C for 15 min.
After treatments, yeast cells were collected by centrifu-
gation (4000g; 10 min). All the treated cells were dried at
70 C for 12 h and then ground to a gritty consistency to
yield granular biosorbent samples. For the untreated
control sample, baker’s yeast biomass was directly used
in the biosorption experiments.
2.3. Biosorption experiments
The stock solution of Cd2þ and Pb2þ (1 g l
1 )
was prepared by dissolving a weighed quantity of
(CH3 COO)2 Cd Æ 2H2 O and Pb(NO3 )2 in deionized
water. Batch biosorption studies were carried out in a
rotary shaker (B. Braun Certomat) operated at 200 rpm.
In the first group of experiments, the highest metal up-
take was determined for 25 mg l
1 metal ion solutions
for biosorbents prepared from treated and untreated
baker’s yeast cells. The effect of pH and initial concen-
tration of metal ions on biosorption and adsorption
isotherms were determined for biosorbent prepared
from ethanol treated yeast cells with which the highest
metal uptake was obtained. 0.1 g of granular biosorbent
was used in all experiments.
The effect of pH on biosorption was investigated in
the pH ranges of 2.0–8.0 and 2.0–5.0 for Cd2þ and Pb2þ ,
respectively. pH values higher than 6.0 could not be used
due to the rapid precipitation of Pb2þ ions. The pH of
metal solutions were adjusted to the desired value with
either 2 mol l
1 NaOH or 2 mol l
1 H2 SO4 solutions. For
biosorption, 0.1 g of granular biosorbent was added to
100 ml of metal solutions containing 25 mg l
1 of the
desired metal in Erlenmayer flasks. The flasks were agi-
tated on the shaker at 30 C for 3 h. The effect of the
initial metal ion concentration on the biosorption was
studied at pH 6.0 for Cd2þ and at pH 5.0 for Pb2þ ions as
described above except that the concentration of metal
ions in the adsorption medium varied between 5 and 25
mg l
1 . The samples were centrifuged at 4000g for 5 min
and the supernatant liquid was used to determine metal
ions concentration. All biosorption experiments were
done in triplicate and mean values reported.
Competitive biosorption of Cd2þ and Pb2þ together
with Cu2þ from their mixture was investigated in the
same manner. The medium (100 ml) containing 25
mg l
1 of each metal ion was incubated with 0.1 g of
biomass. Samples of 5 ml were taken at the beginning of
adsorption and at certain intervals for 3 h as described
above.
 Y. G€oksungur et al. / Bioresource Technology 96 (2005) 103–109
2.4. Analysis of cadmium and lead ions
Concentrations of Cd2þ and Pb2þ ions in the super-
natant fluids were determined by atomic absorption
spectrophotometer (Varian Spectra AA, 220 Fast
Sequential).
Metal uptake (q) was determined as follows:
q ¼ V  ðCi
Ce Þ=S
where q (metal uptake, mg g
1 ) is the amount of metal
ions adsorbed on the biosorbent, V (ml) is the volume of
metal containing solution in contact with the biosor-
bent, Ci and Ce (mg l
1 ) are the initial and equilibrium
(residual) concentrations of metals in the solution,
respectively and S (g) is the amount of added biosorbent
on dry basis.
3. Results and discussion
3.1. Effect of pretreatment of baker’s yeast on biosorption
capacity
In order to investigate the effect of different pre-
treatments on metal uptake of S. cerevisiae cells, the
cells were treated with ethanol, heat and caustic. Fig. 1
shows the Cd2þ and Pb2þ uptake values obtained by
these cells and untreated cells. As seen in Fig. 1, physical
and chemical treatments of the live yeast cells alter their
metal uptake capacities. The highest metal uptake values
which were 15.63 mg g
1 for Cd2þ and 17.49 mg g
1 for
Pb2þ , were obtained by ethanol treated yeast cells. Heat
and caustic treated cells gave similar metal uptake values
for both metal ions, which were higher than the uptake
values obtained with untreated cells. The higher metal
uptake values obtained by ethanol treated yeast cells
may be explained by the increase in the availability of
binding sites and thereby the improvement in the access
of metal ions to the metal binding sites of yeast cells. In
20
q (metal uptake), mg g-1
15
10
5 5
0 0
1 2
(a)
Fig. 1. Effect of different pretreatments on the (a) Cd2þ and (b) Pb2þ uptake of S. cerevisiae (1. untreated yeast; 2. caustic treated yeast; 3. ethanol
treated yeast; 4. heat treated yeast). The biosorbent concentration was 0.1 g/100 ml (dry mass per volume), initial metal concentration was 24 mg l
1 ,
pH ¼ 4.0.
105
our previous work (G€ oksungur et al., 2003), the effect of
caustic, ethanol and heat pretreatments on Cu2þ bio-
sorption capacity of S. cerevisiae cells were determined.
The highest metal uptake was obtained with caustic
treated yeast cells and this effect of caustic treatment on
metal uptake was explained by the removal of protein
groups of the cell wall that make non-adsorbable pro-
tein complexes with Cu2þ ions. Huang et al. (1990) used
heat, ethanol and acid treated yeast biomass for Cu2þ
removal from dilute solutions and stated that when
proteins are dissolved from the cell wall of yeast cells,
the protein molecules in the liquid phase compete for
Cu2þ ions with the protein molecules on the cell wall and
these Cu2þ ––protein complexes were not adsorbable,
thereby impending the copper binding. They obtained
higher Cu2þ removal capacity with treated yeast cells
than untreated yeast cells by fixing the soluble protein in
the cell wall by some denaturation processes such as
heat and ethanol treatment. Ruiz-Manriquez et al.
(1997) used Thiobacillus ferrooxidans cells for Cu2þ
biosorption and found an increase in biosorption
capacity of cells due to NaOH treatment. Yin et al.
(1999) studied biosorption of Cd2þ by using calcium
treated fungal biomass and found that pretreatment of
the biomass with calcium solution and heat improved
the stability and settling property and increased heavy
metal uptake capacities of the biomass. Brady et al.
(1994) and Lu and Wilkins (1996) also found that
caustic treatment of biomass enhanced biosorption
capacity of the biomass.
3.2. Effect of pH
The effect of pH on biosorption was examined in the
pH range of 2.0–8.0 and 2.0–5.0 for cadmium and lead,
respectively. At pH values higher than 6.0, biosorption
studies could not be performed due to the precipitation
of lead ions. Ethanol treated yeast (0.1 g per 100 ml
medium) was used as the biosorbent and a medium
20
q (metal uptake), mg g-1
15
10
3 4 1 2 3 4
(b)
106 Y. G€oksungur et al. / Bioresource Technology 96 (2005) 103–109
pH=2
pH=6
Liquid phase Cd2+ conc., mg l-1
30
25
20
15
10
5 5
0 0
0 5
Fig. 2. Effect of pH on biosorption of Cd2þ and Pb2þ by ethanol treated baker’s yeast cells. The biosorbent concentration was 0.1 g/100 ml (dry mass
per volume), initial metal concentration was 25 mg l
1 .
containing 25 mg l
1 of each metal ion was used as the
biosorption medium. As seen in Fig. 2, the removal of
both Cd2þ and Pb2þ ions from aqueous solution was
affected by medium pH. The biosorption of metal ions
was completed after about five minutes contact with the
biosorbent. The short contact time of biosorbent with
metal solution for biosorption suggests that adsorption
onto the biosorbent surface is the main mechanism of
uptake. The maximum biosorption of heavy metal ions
on the biomass was observed at pH 6.0 for Cd2þ and at
pH 5.0 for Pb2þ . The highest metal uptake values ob-
tained for Cd2þ and Pb2þ ions were 15.38 and 15.59
mg g
1 , respectively.
There was an increase in biosorption capacity of
biomass with increasing pH from 2.0 to 5.0–6.0 for both
metal ions, and it seemed to level off with Cd2þ ions at
pH higher than 6.0. The lowest metal uptake values were
determined at pH 2.0 for both metal ions. At pH values
above the isoelectric point, there is a net negative charge
on the cell wall components and the ionic state of
ligands such as carboxyl, phosphate and amino groups
will be as such to promote reaction with metal cations.
As the pH is lowered, however, the overall surface
charge on the cells will be positive, which will inhibit the
approach of positively charged metal cations. It is likely
that protons will then combine with metal ions for the
ligands and thereby decrease the interaction of metal
ions with the cell components (Sag and Kutsal, 1996).
Several researchers have also investigated the effect of
pH on biosorption of heavy metals by using different
microbial biomass and found similar results with this
study. Say et al. (2001) investigated the biosorption of
Cd2þ , Pb2þ and Cu2þ metal ions by filamentous fungus
Phanerochaete chrysosporium and determined the opti-
mum pH for biosorption as 6.0. Yin et al. (1999)
determined that biosorption capacity of R. arrhizus
pH=4 pH=5
pH=2 pH=3 pH=4 pH=5
pH=7 pH=8
30
Liquid phase Pb2+ conc., mg l-1
25
20
15
10
15 60 120 180 0 5 15 60 120 180 240
t (min) t (min)
biomass increased with increasing pH of the solution
and gave a peak at pH 5.5. Ferraz and Teixeira (1999)
used brewer’s yeast for Pb2þ removal and found that
metal uptake increased with increase in medium pH and
had a maximum value at pH 5.0. Park et al. (1999)
found the optimum pH for Cd2þ uptake as 6.0 for
immobilized Zoogloea ramigera cells.
3.3. Effect of initial concentrations of cadmium and lead
ions
Biosorption experiments with ethanol treated yeast
cells were conducted using solutions containing 5–25
mg l
1 metal ions. pH 6 and pH 5 were used for Cd2þ
and Pb2þ biosorption experiments, respectively. As seen
in Fig. 3, biosorption was very fast for both metal ions
in the first 5 min and in the remaining time period, final
metal concentrations in the liquid continued to diminish
and reached an equilibrium concentration value.
After biosorption, residual cadmium concentrations
were 1.26, 3.17, 5.04, 8.51, 12.56 mg l
1 and metal up-
take values were 3.29, 7.29, 10.52, 14.36, 15.23 mg g
1
for 4.56, 10.47, 15.57, 22.88, 27.80 mg l
1 initial cad-
mium ion concentrations, respectively. Residual lead
concentrations were 1.05, 2.25, 3.48, 4.60, 6.79 mg l
1
and metal uptake values were 3.91, 7.60, 11.47, 14.85,
17.66 mg g
1 for 4.96, 9.85, 14.95, 19.45, 24.45 mg l
1
initial lead ion concentrations, respectively.
3.4. Adsorption isotherm of cadmium and lead
Cadmium and lead sorption isotherms are shown in
Fig. 4. Ce (mg l
1 ) is the final equilibrium concentration
of metal remaining in the solution and q (mg g
1 ) is the
metal uptake. Two adsorption models, the Langmuir
model and Freundlich equation were applied to the

30
Liquid phase Cd2+ conc., mg l-1
25
20
15
10
5 5
0 0
0 5
Fig. 3. Biosorption of Cd2þ (pH ¼ 6.0) and Pb2þ (pH ¼ 5.0) by ethanol treated baker’s yeast cells at different initial metal concentrations: (¤) 5
mg l
1 ; (n) 10 mg l
1 ; (m) 15 mg l
1 ; (h) 20 mg l
1 ; (d) 25 mg l
1 . The biosorbent concentration was 0.1 g/100 ml (dry mass per volume).
20
Metal uptake (q), mg g-1
16
12
8
4
0 respectively. Say et al. (2001) found the maximum metal
0 3
Equilibrium metal conc. (Ce), mg l-1
Fig. 4. Adsorption isotherms of Cd2þ and Pb2þ by ethanol treated
baker’s yeast: (¤) Cd2þ ; (n) Pb2þ .
experimental data. The correlation coefficients obtained
for cadmium from the Langmuir model and Freundlich
equation were 0.998 and 0.9673, respectively. For lead
ions, the correlation coefficients for the Langmuir model
and Freundlich equation were 0.9986 and 0.990,
respectively. Langmuir equation was more in correlation
with the experimental data. The Langmuir model makes
several assumptions, such as monolayer adsorption and
constant adsorption energy, while the Freundlich
equation deals with heterogeneous surface adsorption
(Zhou and Kiff, 1991). The agreement of the experi-
mental data with the Langmuir model implied that
monolayer adsorption existed for the experimental
conditions used.
The Langmuir model and Freundlich equation
parameters were derived from the fitting of experimental
points. K (l mg
1 ) and n are Freundlich constants which
are indicators of adsorption capacity and adsorption
intensity. K values obtained in this study were 3.080 and
3.865 l mg
1 for Cd2þ and Pb2þ , respectively and n val-
Y. G€oksungur et al. / Bioresource Technology 96 (2005) 103–109 107
30
25
Liquid phase Pb2+ conc., mg l-1
20
15
10
15 60 120 180 0 5 15 60 120 180
t (min) t (min)
ues were 1.450 and 1.195 for Cd2þ and Pb2þ , respec-
tively.
The coefficient b in Langmuir equation is a measure
of the stability of the complex formed between metal
ions and biomass under specified experimental condi-
tions (Say et al., 2001). The small b values (0.092 and
0.066 l mg
1 for Cd2þ and Pb2þ , respectively) obtained in
this research implied strong binding of metal ions to
ethanol treated yeast biomass. Maximum metal uptake
capacities of ethanol treated yeast biomass (qmax ) were
found as 31.75 and 60.24 mg g
1 for Cd2þ and Pb2þ ,
6 9 12 15
uptake between 20.33 and 69.77 mg g
1 for biosorption
of Cd2þ , Pb2þ and Cu2þ by dried fungal biomass. Yin
et al. (1999) found the maximum cadmium uptake
capacity of fungal biomass of R. arrhizus as 62.95
mg g
1 . Mattuschka and Straube (1993) found the metal
uptake values for Cd2þ and Pb2þ as 3.4 and 36.5 mg g
1 ,
respectively for waste biomass of Streptomyces noursei.
Veglio et al. (1996) found the highest value of lead up-
take as 130 mg g
1 when a high biomass (Arthrobacter
sp. cells) concentration of 1.4 g l
1 was used for bio-
sorption. In our previous study (G€ oksungur et al., 2003)
on biosorption of Cu2þ by caustic treated baker’s yeast
cells, the experimental data fitted well to Langmuir
model and the maximum metal uptake was 181.8
mg g
1 . The comparison of the biosorption capacities of
biomass used in this study with those reported in the
literature shows that ethanol treated yeast biomass is
suitable for biosorption processes.
3.5. Competitive biosorption
Competitive biosorption of Cd2þ and Pb2þ together
with Cu2þ ions with ethanol treated yeast cells were
conducted for solution containing 25 mg l
1 of each
metal ions at pH 4 and 5. In our previous study
(G€
oksungur et al., 2003), the highest biosorption
108 Y. G€oksungur et al. / Bioresource Technology 96 (2005) 103–109
capacity of Cu2þ ions was determined with caustic
treated waste baker’s yeast cells; but for comparison,
ethanol treated yeast biomass was also used for bio-
sorption of Cu2þ ions in competitive biosorption
studies. The competitive metal uptake values were 7.35
mg g
1 for Cu2þ , 2.93 mg g
1 for Cd2þ and 7.88 mg g
1
for Pb2þ at pH 5 and 5.38 mg g
1 for Cu2þ , 2.80 mg g
1
for Cd2þ and 6.48 mg g
1 for Pb2þ at pH 4. The
competitive biosorption capacities of the yeast biomass
for all metal ions were lower than non-competitive
conditions. The decreased metal uptake in competitive
conditions was thought to be a response to increased
competition between like charged species for binding
sites of the ethanol treated yeast cells. The order of the
sorption capacity was found as Pb > Cu > Cd for both
pH values. These results are in agreement with the
findings of Ferraz and Teixeira (1999) who determined
that S. cerevisiae had more affinity to lead, showing a
higher uptake capacity and kinetics to this metal
compared to others. In another competitive biosorp-
tion study, Nakajima and Sakaguchi (1986) showed
that lead and copper as well as uranium and mercury
were more readily accumulated by actinomycetes than
zinc, manganese, cobalt, nickel and cadmium. Mat-
tuschka and Straube (1993) determined that chromium
sorption was lower when lead was present in the mix-
ture when S. noursei biomass was used as biosorbant.
Engl and Kunz (1995) used S. cerevisiae for biosorp-
tion studies and found that in single metal solutions
copper and cadmium were bound more strongly than
lead but lead suppressed the removal of the other ions
from mixed solutions.
4. Conclusion
The biosorption properties of the biomass of waste
baker’s yeast (S. cerevisiae) were studied for cadmium
and lead removal. Some pretreatments were done to
increase the biosorption capacity of the biomass and
among the pretreatment methods, ethanol treatment
was found to be superior to the others. Heavy metals
concentration and pH of solution were found to effect
the biosorption capacity of the biomass. The Langmuir
adsorption model and Freundlich equation were used
for mathematical description of the biosorption of Cd2þ
and Pb2þ ions onto ethanol treated yeast biomass and it
was found that the adsorption equilibrium data fitted
well to the Langmuir model. In competitive biosorption
experiments, the biosorption capacities of the yeast
biomass for metal ions were found to be lower than non-
competitive conditions. It seems that the use of readily
available waste S. cerevisiae biomass from fermentation
industries offers an alternative in the removal of metals
from industrial wastewaters.
Acknowledgements
The authors gratefully acknowledge Ege University’s
Scientific Research Project Fund for providing financial
support.
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