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Minerals Engineering xxx (2007) xxxxxx

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Biosorption of lead(II), chromium(III) and copper(II)

by R. Opacus: Equilibrium and kinetic studies
B.Y.M. Bueno a, M.L. Torem a,*
, F. Molina a, L.M.S. de Mesquita b

a
Department of Materials Science and Metallurgy, Catholic University of Rio de Janeiro, Rua Marques de Sao Vicente,
225 Gavea, 22453-900 Rio de Janeiro, Brazil
b
National Petroleum Agency, NPA, Brazil

Received 6 June 2007; accepted 18 August 2007

Abstract

Micro-organisms and microbial products can be highly ecient to uptake soluble and particulate forms of metals, particularly from
dilute solutions. The aim of this work was to evaluate the fundamental aspects of the biosorption of Pb(II), Cr(III) and Cu(II) metal
species using Rhodococcus opacus strain. Zeta potential studies and adsorption experiments were carried out in order to evaluate the
sorption metals uptake and the possible interaction mechanisms between the metal species and the surface cell wall. The electrophoretic
studies showed that the presence of the metal species aected the zeta potential proles. Moreover, the equilibrium biomass metals
systems followed the Langmuir isotherm model and the pseudo-second order kinetic model. The inuence of Cr(III) and Cu(II) on Pb(II)
biosorption capacity in binary and ternary systems was evaluated and biosorption capacity of the Pb(II) ions was found to be reduced by
the presence of the other competing metal ions. The nature of possible cellmetal ions interactions was also evaluated by FT-IR and
SEM/EDS analysis. These examinations indicated the involvement of COOH, OH and NH groups in the biosorption process.
 2007 Elsevier Ltd. All rights reserved.

Keywords: Bacteria; Biotechnology; Environmental; Extractive metallurgy; Pollution

1. Introduction along with industrial by-products, as adsorbents (Pino

et al., 2006a,b). These biological materials are known for
The pollution of the environment with toxic heavy met- their potential to adsorb heavy metals. Biosorption of heavy
als is spreading through the world along with industrial metals is one of the most promising technologies involved in
progress. The specic problem associated with heavy met- the removal of toxic metals from industrial waste streams
als in the environment is their accumulation in the food and has been receiving a great deal of attention in recent
chain and their persistence in nature. years, not only as a scientic novelty but also for its poten-
There are several methods for treating metal contami- tial application in industry (Wase and Forster, 1997; Bailey
nant euent such as ion exchange, adsorption, chemical et al., 1999; Sag et al., 2000; Kumar et al., 2006).
precipitation, oxidation, reduction, and reverse osmosis. In the last decade, bacteria, algae and fungi or their sep-
However, many of these approaches can be less cost eec- arated components have been used successfully as biosor-
tive or dicult for practical use. Since, searching for a bent for heavy metal removal. Metal ions uptake by
low-cost and easily available adsorbent has led to the inves- biosorption is complex and may involve the contribution
tigation of materials from agricultural and biological origin, of diusion, adsorption, chelation, complexation, coordi-
nation or micro-precipitation mechanisms, depending on
*
Corresponding author. Tel.: + 55 21 3527 1723; fax: + 55 21 3527
the specic substrate or biomass (Veglio and Beolchini,
1236. 1997). Therefore, this biological phenomenon can be
E-mail address: torem@[Link] (M.L. Torem). aected by many chemical and physical variables like pH,

0892-6875/$ - see front matter  2007 Elsevier Ltd. All rights reserved.
doi:10.1016/[Link].2007.08.013

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2 B.Y.M. Bueno et al. / Minerals Engineering xxx (2007) xxxxxx

ionic strength, biomass concentration and presence of dif- Chang and Chen (1998) studied the biosorption of cop-
ferent heavy metals in solution. All these factors have to per(II), lead(II) and cadmium(II) ions on P. aeruginosa and
be investigated in order to better understand how this phe- the multimetal adsorption results showed that lead and
nomenon takes place and to optimize the operating copper signicantly inhibited the adsorption of cadmium,
conditions. while the eects of cadmium on the adsorption of copper
Biosorption process oers the advantages of low operat- and lead were limited. Leung et al. (2001) studied the bio-
ing costs, possibility of metal recovery, potential biosor- sorption of lead, copper and nickel among 12 bacteries iso-
bent regeneration, minimization of the volume of lated from activated sludge. The increasing order of anity
chemical and/or biological sludge to be disposed of and of the tree metals toward P. pseudoalcaligenes was Ni <
high eciency in detoxifying very dilute liquid streams Cu < Pb. Abu AL-Rub et al. (2006) studied the biosorption
(Volesky, 2001; GO ksungur et al., 2005). of copper ions using C. vulgaris algal cells; they reported
While the works on single species of heavy metal ions that the copper biosorption was eective and dependent
uptake by various kinds of micro-organisms is increasing, on equilibrium pH and biosorbent dose. Kapoor et al.
the combined eects of two or more metals in the biosorp- (1997) showed that the fungi Aspergillus niger was capable
tion process is still modest (Chang and Chen, 1998). The to signicantly remove heavy metals such as lead, cadmium
combined eects of two or more components on micro- and copper from aqueous solutions. The experimental
organism biosorption also depend on the number of pollu- results suggested that carboxylate and amine groups be
tant competing for binding sites, pollutant combination, important in metal ion biosorption on Aspergillus niger
levels of pollutant concentration, order of pollutant addi- biomass.
tion and residence time (McKay and Forster, 1997). In this fundamental work, a competitive biosorption
Copper, lead and chromium ions were chosen for bio- study of lead(II), copper(II) and chromium(III) on R. opa-
sorption studies with regard to their wide use in industry cus was developed. Electrophoretic studies were carried out
and potential pollution impact. Copper is not accurately in order to evaluate the inuence of metal speciation on R.
toxic to humans but its extensive use and increasing levels opacus zeta potential curves. Adsorption equilibrium and
in the environment may cause serious health problems. kinetic works were carried out to evaluate the removal
Lead is a highly toxic and cumulative poison, can damage capacity of R. opacus as a function of pH, biosorbent con-
the nervous system, kidneys, and reproductive system, par- centration, initial metal ions concentration and contact
ticularly in children (Niu et al., 1993). Lead can contami- time. The adsorption study was also supported by infrared
nate the environment from anthropogenic sources as well spectroscopy (FT-IR) and scanning electron microscopy
as natural geochemical processes (Volesky, 2003; Dursun (SEMEDS) experiments to analyze the interaction of the
et al., 2003), this metal is widely used in many important metal species and the cell surface wall.
industrial applications, such as storage battery, manufac-
turing, printing pigments, fuels, photographic materials, 2. Material and methods
explosive manufacturing, coating, automotive, aeronauti-
cal and steel industries (Jalali et al., 2002; Iqbal and Edyv- 2.1. Micro-organisms and growth conditions
ean, 2004; Sekhar et al., 2004; Selatnia et al., 2004). In
addition, chromium is released into the environment by a R. opacus obtained from the culture collection of the
large number of processes such as electroplating, leather Tropical Foundation of Researches and Technology Andre
tanning, wood preservation, pulp processing, steel manu- Tosello-Sao Paulo, was used in this study. The bacterium
facturing, photographic material, corrosive paints, etc. was grown at 28 C (carefully controlled) in agitated liquid
(Ramos et al., 1994; Gaballah and Kilbertus, 1998). This media containing, yeast extract, 3 g l1; peptone, 5 g l1;
metal is of major concern because of their larger usages glucose, 10 g l1; malt extract 3.0 g l1. The medium was
in developing countries and their non degradability nature. sterilized by autoclaving at a pressure 1 atm. The pH was
Due to their toxic eects on living systems, the US EPA has adjusted to 7.2 with diluted KOH solutions. Growth was
set the maximum contaminant concentration level for allowed to proceed for 24 h on a horizontal shaker operat-
Cr(VI) in domestic water supplies at 0.05 mg l1, while ing at 150 rpm. After the micro-organism growth, the cul-
total Cr(including Cr(III), Cr(VI) and its other forms) is ture was separated by centrifugation, and the obtained
regulated to below 2 mg l1 (Baral and Engelken, 2002). solid material was washed with deionized water and sus-
Although the removal of these metal ions from aqueous pended in NaCl 0.1 mM and later being sterilized at
solutions by many organisms, including Aspergillus niger, 1 atm of pressure during 20 min.
Chlorella vulgaris, Ecklonia radiate, Pseudomonas aerugin- The cellular quantication was determined by dry
osa PU21, Saccharomyces cerevisiae and Neurospora crassa weight.
species has been previously reported (Kapoor et al., 1997;
Abu AL-Rub et al., 2006; Matheickal et al., 1997; Chang 2.2. Metal solutions
et al., 1997; Mapolelo and Torto, 2004; Kiran et al.,
2005), there is a lack of information about the sorption The test solutions single lead(II), copper(II) and chro-
ability of R. opacus in the literature. mium(III) were prepared by diluting 1000 mg l1 of stock

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solutions of lead(II), copper(II) and chromium(III) to the The equilibrium sorption capacity of the biomass at the
desired concentration. Stock solution of lead(II) copper(II) corresponding equilibrium conditions was calculated using
and chromium(III) were obtained by dissolving quantities a mass balance equation as in Eq. (1).
of PbCl2, Cu(NO3)2 3H2O, and Cl3Cr 6(H2O), in 1 liter Co  Ce
of deionized water, respectively. The pH of the solutions qe V 1
M
was adjusted to a desired value with 0.1 N HCl and
0.1 N NaOH. where qe is the amount of the metal uptake by the biomass
(mg g1) in the equilibrium; Co is initial metal ion concen-
tration in solution (mg l1); Ce is the equilibrium metal ion
2.3. Zeta potential measurements
concentration in solution (mg l1); V is volume of the med-
ium (l); and M is the amount of the biomass used in the
In order to study the possible biosorption mechanisms,
reaction mixture (g).
the zeta potential of the micro-organism cells was mea-
Infrared spectra of the R. opacus and metal ions loaded
sured before and after the metal ions adsorption using
biomass were obtained using a Nicolet 2000 spectrometer
the microelectrophoretic apparatus Zeta Meter (Zeta
with resolution of 4 cm1 using 120 scans. For this study,
Meter System 3.0+). NaCl was used as an indierent
10 mg of nely ground biomass was encapsulated in
electrolyte.
500 mg of KBr in order to prepare a translucent sample
disk.
2.4. Batch biosorption experiments In order to observe how the sorption of metal ions on
the cell surface would alter its morphology and to further
The factors that aect the adsorption rate and uptake conrm the identity of metal ions on the cell mass, SEM
capacity of the biosorbent were examined in a batch sys- (scanning electron microscopy) and EDS (energy dispersive
tem. All batch experiments were carried out with micro- spectrometry) analysis was employed in this study. The
organism suspension in Erlenmeyer asks on a horizontal samples were coated with Au via vapor deposition prior
shaker, operating at 150 rpm, to elucidate the optimum to being introduced to SEMEDS (DSN 960 ZEISS) for
conditions (biosorbent dose, pH, contact time and initial analysis. The secondary electron images of the material
metal ion concentration). depict approximate sizes in the range of a few microns.
The eect of pH on the sorption capacity of R. opacus The EDS analyzer oers in situ elemental analysis.
for Pb(II), Cu(II) and Cr(III) ions was evaluated by equil-
ibrating the sorption mixture containing biomass suspen- 3. Results and discussion
sion (1 g l1) and metal solutions (20 mg l1) at dierent
pH values of 27, after reaching equilibrium the samples 3.1. Electrokinetic studies
were centrifuged for 8 min and the supernatant liquid
was analyzed for residual metal ions. This study investigated the changes in the electrokinetic
The inuence of the contact time (5240 min) on the patterns of R. opacus in the presence of Pb(II), Cu(II) and
metals species sorption was performed in order to quantify Cr(III) at dierent pH values, to determine whether
the equilibrium uptake (qe). The experimental procedure changes in the surface charge of the cells were related to
was similar to the previous pH studies. For the assessment the biosorption of these ions as they could indicate the
of eect of initial metal ion concentration on biosorption at interaction between the metal species and the active site
optimum pH and contact time, metal solutions ranging of the micro-organism cell wall.
from 15 to 200 mg l1 were prepared and used. The exper- Fig. 1 shows the zeta potential curves as a function of
iments was carried out at pH value of 5.0 0.2 for Pb(II) pH for R. opacus before and after Pb(II), Cu(II) and
and 6.0 0.2 for Cu(II) and Cr(III) ions. For all experi- Cr(III) biosorption for the pH range between 2.0 and 7.5.
ments, the temperature was kept around 25 2 C. The results show that the isoelectric point (IEP) of R. opa-
For the determination of biosorption characteristics of cus is around pH 2.8. On the other hand, one may observe
Pb(II), with addition of Cu(II) and Cr(III), the initial con- that the biosorption of Pb(II), Cu(II) and Cr(III) modies
centration of the dominant metal (Pb(II)) was established the zeta potential proles, suggesting that the metal uptake
between 15 and 200 mg l1, while the competing metal occurs onto the active sites of the micro-organism and
ion concentrations were kept constant at 30 mg l1 and shifts the charge reversal and zeta potential curves of R.
mixing them in the experimental apparatus before the addi- opacus for all metal species. The results are in agreement
tion of the bacterial suspension. with the work of Matis and Zouboulis (1994).The R. opa-
cus was net negatively charged at pH values above its iso-
2.5. Analytical methods electric point. On the other hand, in the presence of Pb(II),
Cu(II) and Cr(III), one may observe a shift on the previous
The concentrations of non adsorbed Pb(II), Cu(II) and R. opacus IEP value, probably due to a smooth electro-
Cr(III) ions by R. opacus were determinated in atomic static adsorption of the single metallic species. The second
absorption spectrophotometer (Perkin Elmer 1100B). charge reversal may be related to the specic adsorption of

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25 40
20 Pb(II)
15 Cu(II)
30 Cr(III)
Zeta Potential (mv)

10
5

q e (mg/g)
0
-5 20
-10
-15 R. opacus
10
-20 R. opacus+Pb (II)
R. opacus+Cu (II)
-25 R. opacus+Cr(III)
-30
0 1 2 3 4 5 6 7 8 0
2 3 4 5 6 7 8 9
pH pH

Fig. 1. Electrokinetic measurements, expressed as zeta potential of cells of Fig. 2. Eect of pH on the Pb(II), Cu(II) and Cr(III) biosorption by R.
R. opacus (0.2 g l1); inuence of solution pH in presence of metals Opacus (initial metal concentration: 20 mg l1; biomass concentration:
(100 mg l1). 1.0 g l1; agitation speed: 150 rpm; contact time: 4 h).

the rst metal hydroxy complexes as Pb(OH)+, Cu(OH)+ the isoelectric point (IEP) for R. opacus is at pH 2.8. At pH

and CrOH2 on the surface cell wall. These results are values above the IEP, it is expected that more ligands with
similar to those depicted by Fuerstenau and Pradip negative charge would be exposed such as carboxyl and
(2005) for oxides and silicates. phosphate groups with subsequent increase in attraction
The authors do believe that the second charge reversal in for positively charged metal ions.
the chromium case may be attributed to the formation of Fig. 2 shows the metals uptake as a function of pH. It is
the Cr mononuclear hydroxy species. According to the lit- observed that the best results occurred at pH 5.0 for Pb(II)
erature the predominant species in the pH range between and pH 6.0 for Cu(II) and Cr(III), respectively, where

3.5 and 8.0 are CrOH2+ and CrOH2 (Refs. King, 1982; around 95%, 52% and 70% of metallic species were uptaken
Stumm and Morgan, 1996; Zouboulis and Kydros, 1995). by the biomass.
The third charge reversal may be attributed to the hetero- The same trend was observed by several authors that
coagulation of Cr(OH)3 negatively charged on the surface investigated the eect of pH on biosorption of heavy metal

cell. Once the pH is increased the formation of CrOH4 by using dierent biomaterials, as Neurospora Crassa Sar-
is thermodynamically feasible and also may contribute to gassum wightii, Aspergillus avus, Olive stone, Cladonia
the negative charge of the bacteria surface. rangiformis hom and P. putida (Kiran et al., 2005; Vijay-
According to Stratton et al. (2002), the lipids contained araghavan and Prabu, 2006; Akar and Tunali, 2006; Fiol
in the cell walls of R. opacus include free lipid, glicolipid, et al., 2006; Ekmekyapar et al., 2006; Uslu and Tanyol,
phospholipid and carboxyl groups that would present an- 2006).
ity for the metallic cations. Fein et al. (1997) found that The dierent pH binding values for these components
some functional groups of gram positive bacteria have an could be due to the nature of the chemical interactions of
anity for certain metal ions, which leads to metal binding. each component with the microbial cells. At highly acidic
These results also support the R. opacus zeta potential pH values, metal cations and protons compete for binding
behavior in this work. sites on cell wall, which results in a lower metal uptake.

3.2. The eect of solution pH 3.3. The eect of biosorbent dose on biosorption

It well know that pH has a signicant eect on the sol- The eect of biosorbent concentration on the uptake of
ubility, speciation and biosorption capacity of heavy met- single lead(II), copper(II) and chromium(III) ions is shown
als (Sheng et al., 2004; Abu Al-Rub et al., 2004). The in Fig. 3. The bacterial concentration ranged from 0.5 to
dierent pH sorption proles for various heavy metal ions 2.5 g l1 to determine the eects of micro-organism concen-
may be related to the nature of chemical interactions of tration on the adsorption rate.
each metal with the biomass (Kiran et al., 2005). It was observed that, the eect of biomass dose on Pb(II)
The increasing in metal removal with increasing pH can and Cr(III) uptake was similar. With the increasing of the
be also explained using the analogy between the reaction of dose of biosorbent, the removal was increased. This obser-
metal hydrolysis and the reaction between the binding sites vation can be attributed to the increase of the adsorption
of the sorbent and the metal, where in both reactions, the surface area and the availability of free adsorption sites.
bond for hydrogen is broken and hydrogen ions are Pb(II) and Cr(III) removal eciency were the maximum
released and substituted by the metal (Tipping, 2002; at 1 g l1 of biosorbent. Nevertheless, further increments
Pagnanelli et al., 2003). In this study, another reason for in biosorbent concentration led to a decrease in the
increasing removal of the metals with increasing pH is that removal of Pb(II) and Cr(III) ions (Fig. 3). This can be

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100 60
Experimental data: Pb(II) y = 0.2083x - 0.0714
80 50 Experimental data: Cu(II)
% Metal Removal

Experimental data: Cr(III)

40 y = 0.1493x + 0.4737
60

t/ qt
30 y = 0.11x + 0.3774
40
Pb(II) 20
20 Cu(II)
Cr(III) 10
0
0 0.5 1 1.5 2 2.5 3 0
Biosorbent concentration, g.l-1 0 30 60 90 120 150 180 210 240 270
contact time (min)
Fig. 3. Eect of the biomass concentration of R. Opacus in the
biosorption of Pb(II), Cu(II) and Cr(III) ions (initial metal concentration: Fig. 5. Kinetic model of pseudo-second order for the uptake of Pb(II),
20 mg l1; pH: 5.0 for Pb(II) and pH: 6.0 for Cu(II) and Cr(III); agitation Cu(II) and Cr(III) using R. opacus (pH: 5.0; biomass concentration:
speed: 150 rpm; contact time: 4 h). 2.0 g l1, time of contact: 4 h).

explained by the formation of aggregates during biosorp- (Kumar et al., 2006; Fiol et al., 2006; Pan et al., 2006;
tion, which takes place at high biomass concentrations Abu AL-Rub et al., 2006).
causing a decrease of the eective adsorption area as Fig. 5 shows the pseudo-second order equations for the
depicted by Ekmekyapar et al. (2006). Considering the pre- biosorption of the metallic species. It is observed that the
vious results, all experiments were carried out with a R. model ts very well the data obtained, where the correla-
opacus concentration of 1.0 g l1 for lead and chromium tion coecients were greater than 0.99. The calculated
removal. In the case of Cu(II), a R. opacus concentration qeq values of the pseudo-second order kinetic model for
of 2.0 g l1 was used for all others experiments. the R. opacus were also closer to the experimental qexeq val-
ues than those obtained from the pseudo rst order kinetic
model (Table 1). The heavy metals with due attention to
3.4. The eect of contact time their experimental qeq values are arranged as follows:
Pb(II) > Cr(III) > Cu(II).
The eect of the contact time (5 min to 4 h) in the bio- Similar results were also found using Tectona grandis
sorption of Pb(II), Cu(II) and Cr(III) by R. opacus is L.f., Olive stone, Bacillus cereus, Chlorella vulgaris, Cepha-
shown in Fig. 4. losporium aphidicola (Kumar et al., 2006; Fiol et al., 2006;
Fig. 4 shows the eect of the contact time on the metal Pan et al., 2006; Abu AL-Rub et al., 2006; Tunali et al.,
uptake. It is observed a quick adsorption for Pb(II) fol- 2006) to the biosorption of metallic ions. The kinetic exper-
lowed by Cr(III) and Cu(II). The maximum removal for imental data properly correlated with the pseudo-second
all metallic species occurred in 60 min where the uptake order kinetic model.
was 95%, 52% and 70%, respectively for Pb(II), Cu(II) In many cases, the rst-order equation of Lagergreen
and Cr(III). After this period, the equilibrium was reached. does not t well to the whole range of contact time and
Similar results were observed in many studies using dier- is generally applicable over the initial stage of the adsorp-
ent biosorbents on the uptaking of dierent heavy metals tion process (Ho and Mckay, 1998).The rst order kinetic
process has been used for reversible reaction with an equi-
10 librium being established between liquid and solid phases.
Whereas, the pseudo-second order kinetic model assumes
8 that the rate limiting step may be chemical adsorption (Sri-
vastava et al., 2006). Several authors that studied sorption
6
of divalent metals on heterogeneous sorbents reported that
q t (mg/g)

most of metal sorption kinetics follows pseudo-second

order mechanism (Reddad et al., 2002; Ho, 2004). It is
4
more likely to predict that the adsorption behavior may
Pb(II):20mg/L
involve valency forces through sharing of electrons
2 Cu(II):20mg/L
between transition metal cations and adsorbent.
Cr(III):20mg/L
0
0 30 60 90 120 150 180 210 240 270 3.5. The eect of initial concentration of lead, copper and
Contact Time (min) chromium ions
Fig. 4. The Eect of the contact time on Pb(II), Cu(II) and Cr(III) ions
biosorption by R. Opacus (biomass concentration: 2 g l1; pH: 5.0 for Fig. 6 presents the metallic uptake as a function of the
Pb(II) and pH: 6.0 for Cu(II) and Cr(III); agitation speed: 150 rpm). equilibrium concentration. One may realize that the

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Table 1
Kinetic parameters for the biosorption of Pb(II), Cu(II) and Cr(III) on R. opacus
Adsorbate Experimental Pseudo rst order kinetic Pseudo-second order kinetic
1 1 1
qexp (mmol g ) qeq (mmol g ) k1 (min ) R 2
qeq (mmol g1) k2 103 (g mmol1 min1) R2
2
Pb(II) 0.043 0.022 5.04 10 0.8751 0.044 0.154 0.9992
Cu(II) 0.074 0.004 0.71 102 0.0256 0.075 9.60 0.9999
Cr(III) 0.125 0.025 3.06 102 0.8502 0.129 9.04 0.9998

120 The Freundlich isotherm is a nonlinear sorption model.

Pb(II) This model proposes a monolayer sorption with a hetero-
100 Cu(II) geneous energetic distribution of active sites, accompanied
Cr(III)
by interactions between adsorbed molecules. The general
80
form of this model is:
q e (mg.g-1)

60 1=n
qe K F  C f 3
40 1
where KF (mg g ) is the adsorption capacity and n is re-
20
lated to the adsorption intensity of the adsorbent. The log-
arithmic form of Eq. (3) is:
0
0 30 60 90 120 150 180 210 240
1
ln qe ln k F ln C e 4
Ce (mg.l-1) n
Fig. 6. Eect of the concentration of the metallic ion in the biosorption of where KF and 1/n can be determined from the linear plot of
Pb(II), Cr(III) and Cu(II) ions by R. opacus (biomass concentration: log(qe) versus log(Ce). The equilibrium data of lead and
1 g l1; pH: 5.0; agitation speed: 150 rpm; contact time: 4 h). copper ions adsorption by R. opacus obtained at 298 K
was applied to Langmuir and Freundlich models. The rel-
increase of the equilibrium concentration leads to an ative parameters and correlation coecients (R2) were
increase in the metallic uptake. This observation is deeply listed in Table 2.
connected with the metallic concentration gradient with The mono-component Langmuir constant, qmax, repre-
respect to the active and available sites of R. opacus, which sents the monolayer saturation at equilibrium or the total
means that the values of qe increased with the increasing of capacity of R. opacus for lead, copper and chromium ions.
the initial metal ions concentrations. The adsorption data for all metals provided a better t
It is important to point out that the equilibrium sorption to the Langmuir isotherm (Fig. 7). From Table 2, the
studies determine the capacity of the sorbent, which can be maximum loading capacities of R. opacus was obtained
described by a sorption isotherm, characterized by certain as 94.3 mg g1 for lead, 32.2 mg g1 for copper and
constant whose values express the surface properties and 72.9 mg g1 for chromium, so the ability of Pb(II) adsorp-
anity of the sorbent. Sorption equilibrium is established tion on R. opacus is bigger than Cu(II) and Cr(III). From
when the concentration of sorbate in the bulk solution is Table 2, the magnitude of KF showed a high Pb(II) adsorp-
in dynamic balance with that of the interface (Ho and tive capacity of R. opacus. Table 2 also indicates that n is
Mckay, 2000). Equilibrium relationships between sorbent greater than unity, indicating that lead, chromium and
and sorbate are described by sorption isotherms, many dif- copper ions are favorably adsorbed by R. opacus biomass.
ferent isotherm models have been proposed for the adsorp- The sorption capacity parameter obtained from a batch
tion of solutes in a liquid solution onto a solid surface. experiment is useful in providing information about eec-
Langmuir model is probably the most popular isotherm tiveness of metal-biosorbent system.
models due to its simplicity and its good agreement with Compared to other biosorbents, the adsorptive capacity
experimental data. of Pb(II), Cu(II) and Cr(III) adsorption on R. opacus is
The Langmuir model represents one of the rst theoret-
ical treatments of nonlinear sorption and suggests that Table 2
uptake occurs on a homogeneous surface by monolayer Adsorption constants estimated from simulations with Langmuir and
sorption with out interaction between adsorbed molecules. Freundlich models for isotherms of Pb(II), and Cu(II) using R. opacus as
the biosorbent
In addition, the model assumes uniform energies of adsorp-
tion onto the surface and no transmigration of the adsor- Adsorbate Langmuir model Freundlich model
bate. The Langmuir isotherm is represented in the qmax b R2 KF n R2
following equation: (mmol g1) (l mmol1) (l g1)
Pb(II) 0.455 14.59 0.9706 18.44 3.15 0.8562
Ce 1 1 Cr(III) 1.404 1.08 0.9292 3.02 1.61 0.8354
Ce 2
qe b  qmax qmax Cu(II) 0.506 3.74 0.9857 5.33 2.91 0.9699

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8
Pb(II)
Cu(II)
6 Cr(III) y = 0.0302x + 0.6554

Ce /q e
4
y = 0.0137x + 0.6596

2
y = 0.0103x + 0.1848

0
0 30 60 90 120 150 180 210 240
Ce (mg.l-1 )

Fig. 7. Langmuir equation to the biosorption of Pb(II) and Cu(II) onto R. opacus.

better than others biosorbents. Similar biosorption results the biomass may take place, resulting in a competition for
for lead(II) and copper(II) ions using tectona grandis L.f., the adsorption sites on the surface. As a consequence, the
thuja orientalis Ekclonia maxima, and sargassum wightii rst component has a smaller parking space and its uptake
were found to follow the Langmuir model (Kumar et al., is decreased (Akar et al., 2005).
2006; Nuhoglu and Oguz, 2003; Vijayaraghavan and Among various factors that aect the biosorption pref-
Prabu, 2006; Feng and Aldrich, 2004). erences of a sorbent, binding of metal ions on biomaterials
largely depends on physicochemical properties of the
metallic species. It has been reported that metal removal
3.6. Competitive biosorption increases with the increase in the ionic radio (Mattuschka
and Straube, 1993; Chong and Volesky, 1995; Sag et al.,
Wastewaters usually contain more than single metal. 2002), which follows the order Pb(II) > Cu(II) > Cr(III).
The presence of more than one metal in wastewater is The dierences in sorption anities may also be attributed
expected to cause interactive eects depending on many to dierences in the electronegativity of the atoms, which
reasons, such as the number of metals competing for bind- also follows the order Pb(II) > Cu(II) > Cr(III) as
ing sites; the metal concentration; and the nature and bio- described in the literature (Stumm and Morgan, 1996).
sorbent dose. The greater the electronegativity or ionic radio, the greater
The results of the biosorption of the binary Pb(II) and is the anity, which also explains the signicant suppres-
Cu(II), and the ternary Pb(II), Cu(II) and Cr(III) system sion of lead uptake in the presence of copper and the mod-
on R. opacus biomass is shown in Fig. 8. The results show erate eect of chromium on lead biosorption.
that the presence of copper ions resulted in the inhibition in Sharma et al. (2007) studied the biosorption of Cd(II),
lead uptake, and this observation was much more signi- Cr(III) and Ni(II) in ternary mixture on unmodied shelled
cant than those in the presence of chromium and copper moringa oleifera seeds (SMOS) and were compared with the
ions together. single metal solution. The order of sorption Cd(II) >
In the presence of the other metals ions in solution, Cr(III) > Ni(II) for the SMOS obtained was consistent
chemical interactions between these species as well as with with the physicochemical properties of metal under study.
Akar and Tunali (2006) examined the characteristics of the
80 Pb(II) and Cu(II) biosorption onto Aspergillus avus. The
Pb(II)

Pb(II)+Cu(II) biosorption capacities of Aspergillus avus in the presence

60 of the binary metal mixture were lower than that of non-
Pb(II)+Cu(II)+Cr(III)
competitive conditions. The order of the anity for com-
q e (mg.g )
-1

petitive conditions was as follows (based on mg/g

40
accumulation) Pb(II) > Cu(II). This order was the same
in the noncompetitive conditions. Abu AL-Rub et al.
20 (2006) used powdered Chlorella vulgaris algal cells for cop-
per biosorption. The presence of lead, zinc or both metals
0 in aqueous solutions suppressed the removal of copper
0 30 60 90 120 150 180 210 ions.
-1
Ce (mg.l ) SEM micrographs and EDS spectra obtained before and
Fig. 8. Eect of the presence of other metals in the biosorption of lead in after Pb(II), Cu(II) and Cr(III) biosorption onto R. opacus
R. opacus. (pH 5.0; biomass concentration: 2 g l1, agitation speed: biomass are presented in Figs. 9 and 10, respectively. The
150 rpm, contact time: 4 h). coccus-like shape of R. opacus cells morphology was also

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Fig. 9. Scanning electron microphotographs of the biomass (a) before and (b) after the contact with a Pb(II), Cu(II) and Cr(III) aqueous solution. The pH
of the aqueous medium was 5, the amount of R. opacus was 2 g l1 and the contact time was 4 h.

Fig. 10. Elemental composition of the control biomass (a) before and (b) after the contact with a Pb(II), Cu(II) and Cr(III) aqueous solution. The pH of
the aqueous media was 5, the amount of R. opacus was 2 g l1 and the contact time was 4 h.

conrmed by MEV. These micrographs does not indicated ing an ion exchange mechanism as one of the mechanism of
clearly the presence of new particles over the surface of metal biosorption for this bacteria strain.
Pb(II), Cu(II) and Cr(III) loaded R. opacus cells but the
EDS analysis conrmed the uptake of metal ions which 3.7. FT-IR spectral analysis
revealed lead signals together with the presence of chro-
mium and copper peaks in all spectra. On the other hand, The FT-IR spectra of R. opacus native and metal loaded
for the samples after biosorption, was observed on the EDS biomass in the range of 4004000 cm1 were taken to
spectrum that the peaks of K disappeared (Fig. 9). This obtain information on the nature of the possible cellmetal
observation could suggest that the metallic species has ions interactions, like complexation and presented in Figs.
replaced K+ on the cell wall of R. opacus, thereby signify- 11 and 12. The whole of frequencies of vibrations and their

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2.0 The FT-IR spectra of R. opacus biomass exposed to

3354 metal ions indicated slight changes in the absorption peak
2927 1655 frequencies; it was dicult to interpret how these shifts
1.5
2854 were related with lead and chromium biosorption, also
1541
1076 the absorbance of the peaks in the Pb(II) and Cr(III)
Absorbance

-1 1240
0 mg.l loaded biomass is slightly lower than that in the native
1.0 one. This shift in the absorbance showed that there was a
metal binding process taking place on the surface of the
biomass.
0.5
The analysis of the FT-IR spectra showed the presence
Pb:100
of ionizable functional groups (i.e. carboxyl, hydroxyl
and amino) able to interact with protons or metal ions. It
0.0
4000 3500 3000 2500 2000 1500 1000 500
should be noted that the results obtained at this stage were
Wavenumber (cm )
-1 considered sucient to give an idea about the presence of
functional groups on the R. opacus surface.
Fig. 11. FT-IR spectra of the R. opacus biomass control and after the
contact with Pb(II) ions.
4. Conclusions

2.0 In this study, the ability of R. opacus to bind heavy

metal ions from aqueous solutions was investigated. The
3354
1655
biosorption process has been shown to be aected by pH,
1.5 2927 initial metal concentration, and contact time. Sorption of
1541
2854 1076
Pb(II), Cu(II) and Cr(III) on R. opacus was found to follow
Absorbance

1240
0mg.l
-1 a pseudo-second order kinetic model. The experimental
1.0 data tted well to the Langmuir isotherm model.
50mg.l
-1
The isoelectric point of R. opacus cells was found to
occur at pH 2.8. The presence of Pb(II), Cu(II) and Cr(III)
0.5
100mg.l
-1 aected the zeta potential proles and charge reversals,
which suggest that the metallic species uptake may be
related to the electrostatic interaction of the metal species
0.0
4000 3500 3000 2500 2000 1500 1000 500 with the negatively charged functional groups on the
-1
Wavenumber (cm ) micro-organism surface cell.
The interactions between the metal ions and the func-
Fig. 12. FT-IR spectra of the R. opacus biomass control and after the
contact with Cr(III) ions.
tional groups on the cell wall surface of the biomass were
conrmed by FT-IR and EDS analysis. The functional
groups involved in metal ions biosorption included car-
corresponding groups able to interact with protons or boxyl, hydroxyl and amino groups. The capacity of uptake
metal ions are presented in Table 3. Pb(II) ions by the biomass was reduced by the presence of
The IR spectrum pattern of biomass showed distinct other metallic species in the system.
and sharp absorptions at 3354 cm1 indicative of the exis- R. opacus may be used as a feasible biosorbent for the
tence of the OH groups and NH groups (Akar et al., removal of heavy metal ions and it may be an alternative
2005). The absorption peak at 2922 cm1 can be assigned to more costly methods such as active carbon adsorption,
to CH stretching and the absorption peak at 1654 cm1 solvent extraction and chemical oxidation for removal of sin-
is indicative of C@O group (Selatnia et al., 2004). The gle and binary mixture heavy metal ions from wastewaters.
absorption peak at 1070 cm1 can be assigned to CO
or CN groups (Pan et al., 2006).
Acknowledgements

Table 3 The authors gratefully acknowledge CNPq and FA-

IR absorption bands and corresponding possible groups PERJ for supporting this research. The authors also would
Wavenumber (cm1) Functional group like to acknowledge Professor Maria Isabel Pais da Silva
3354 Bonded hydroxyl group, NH stretching
for the technical support in the infrared experiments.
2927 CH stretching
2854 CH stretching References
1655 C@O stretching of COOH
1541 Amide II band
Abu Al-Rub, F.A., El-Naas, M.H., Benyahia, I., Ashour, I., 2004.
1240 P@O
Biosorption of nickel on blank alginate beads, free and immobilized
1076 CN stretching
algal cells. Process Biochem. 39, 17671773.

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Abu AL-Rub, F.A., El-Naas, M.H., Ashour, I., Al-Marzouqi, M., 2006. using Tectona grandis L.f. leaves powder. J. Hazardous Mater. B137,
Biosorption of copper on Chlorella vulgaris from single binary and 12111217.
ternary metal aqueous solutions. Process Biochem. 41, 457464. Leung, W.C. et al., 2001. Biosorption of heavy metals by bacterial
Akar, T., Tunali, S., Kiran, I., 2005. Botrytis cinerea as a new fungal isolated from activated sludge. Appl. Biochem. Biotechnol. 9193,
biosorbent for removal of Pb(II) from aqueous solutions. Biochem. 171184.
Eng. J. 25, 227235. Mapolelo, M., Torto, N., 2004. Trace enrichment of metal ions in aquatic
Akar, T., Tunali, S., 2006. Biosorption characteristics of Aspergillus avus environments by Saccharomyces cerevisiae. Talanta 64, 3947.
biomass for removal of Pb(II) and Cu(II) ions from an aqueous Matheickal, J.T., Yu, Q., Feltham, J., 1997. Cu(II) binding by E. Radiata
solution. Bioresource Technol. 97, 17801787. biomaterial. Environ. Technol. 18, 2534.
Bailey, S.E., Olin, T.J., Bricka, R.M., Adrian, D.D., 1999. A review of Mattuschka, B., Straube, G., 1993. Biosorption of metals by a waste
potentially low-cost sorbents for heavy metals. Water Res. 33, 2469 biomass. J. Chem. Technol. 58, 5763.
2479. McKay, G., Forster, J.F., 1997. Equilibrium parameters for the sorption
Baral, A., Engelken, R.D., 2002. Chromium-based regulation and of copper, cadmium and zinc ions onto peat. J. Chem. Technol 69,
greening in metal nishing industries in the USA. Environ. Sci. Pollut. 309320.
5, 121133. Matis, K.A., Zouboulis, A.I., 1994. Flotation of cadmium-loaded
Chang, J.-S., Chen, C.-C., 1998. Quantitative analysis and equilibrium biomass. Biotechnol. Bioeng. 44, 354360.
models of selective adsorption in multimetal systems using a bacterial Niu, H., Xu, X.S., Wang, J.H., Volesky, B., 1993. Removal of lead from
biosorbent. Sep. Sci. Technol. 33, 611632. aqueous solutions by Penicillium biomass. Biotechnol. Bioeng. 42, 785
Chang, J.-S., Law, R., Chang, C.-C., 1997. Biosorption of lead, copper 787.
and cadmium by biomass of Pseudomonas aeruginosa, PU21. Water Nuhoglu, Y., Oguz, E., 2003. Removal of copper from aqueous solutions
Res. 31, 16511658. by biosorption on the cone biomass of Thuja orientalis. Process
Chong, K.-H., Volesky, B., 1995. Description of 2-metal biosorption Biochem. 38 (11), 16271631.
equilibria by Langmuir-type. Biotechnol. Bioeng. 47, 451460. Pagnanelli, F., Esposito, L., Veglio, F., 2003. Metal speciation and pH
Dursun, A.Y., Uslu, G., Cuci, Y., Aksu, Z., 2003. Bioaccumulation of eect on Pb, Cu, Zn, and Cd biosorption onto Sphaerotilus natans:
copper(II), lead(II) and chromium (VI) by growing Aspergillus niger. Langmuir-type empirical model. Water Res. 37, 627633.
Process Biochem. 38, 16471651. Pan, J., Ge, X., Liu, R., Tang, G.H., 2006. Characteristic features of
Ekmekyapar, F., Aslan, A., Kemal Bayhan, Y., Cakici, A., 2006. Bacillus cereus cell surfaces with biosorption of Pb(II) ions by AFM
Biosorption of copper(II) by non-living lichen biomass of Cladonia and FT-IR. Colloids Surfaces B: Biointerfaces 52, 8995.
rangiformis hom. J. Hazardous Mater. B137, 293298. Pino, G.H., Mesquita, L.M.S., Torem, M.L., Pinto, G.A.S., 2006a.
Fein, J.B., Daughney, C., Yee, N., Davis, T.A., 1997. A chemical Biosorption of heavy metals by powder of green coconut shell. Sep.
equilibrium model for metal adsorption onto bacterial surfaces. Sci. 41, 14.
Geochimica et Cosmochimica Acta 61 (16), 33193328. Pino, G.H., Mesquita, L.M.S., Torem, M.L., Pinto, G.A.S., 2006b.
Feng, D., Aldrich, C., 2004. Adsorption of heavy metals by biomaterials Biosorption of cadmium by green coconut shell powder. Miner. Eng.
derived from the marine alga Ecklonia maxima. Hydrometallurgy 73, 19, 380387.
110. Ramos, R.L., Martinez, A.J., Coronado, R.M.G., 1994. Adsorption of
Fiol, N., Villaescusa, I., Martinez, M., 2006. Sorption of Pb(II), Ni(II), chromium (VI) from aqueous solutions on activated carbon. Water
Cu(II) and Cd(II) from aqueous solution by olive stone waste. Sep. Sci. Technol. 30 (9), 191197.
Purif. Technol. 50, 132140. Reddad, Z., Gerente, C., Andres, Y., LeCloirec, P., 2002. Adsorption of
Fuerstenau, D.W., Pradip, T., 2005. Zeta potentials in the otation of several metal ions onto a low-cost biosorbent. Kinetic and equilibrium
oxide and silicate minerals. Adv. Colloid Interf. Sci. 114115, 926. studies. Environ. Sci. Technol. 36, 20672073.
Gaballah, I., Kilbertus, G., 1998. Recovery of heavy metals ions through Sag, Y., Kaya, A., Kutsal, T., 2000. Lead, copper and zinc biosorption
decontamination of synthetics solutions and industrial euents using from bicomponent systems modelled by empirical Freundlich iso-
modied barks. J. Geochem. Explor. 62, 241286. therm. Appl. Microbiol. Biotechnol. 53, 338341.
Goksungur, Y., U ren, S., Guvenc, U., 2005. Biosorption of cadmium and Sag, Y., Akeael, B., Kutsal, T., 2002. Ternary biosorption equilibria of
lead ions by ethanol treated waste bakers yeast biomass. Bioresource Cr(VI), Cu(II) and Cd(II) on Rhizopus arrhizus. Sep. Sci. Technol. 37
Technol. 96 (1), 103109. (2), 279309.
Ho, Y.S., Mckay, G., 1998. Kinetic model for lead(II) sorption on to peat. Sekhar, K.C., Kamala, C.T., Chary, N.S., Sastry, A.R.K., Nageswara, R.,
Adsorp. Sci. Technol. 16, 243255. Vairamani, M., 2004. Removal of lead from aqueous solutions using
Ho, Y.S., Mckay, G., 2000. Correlative biosorption equilibrium model for an immobilized biomaterial derived from a plant biomass. J. Hazard
a binary batch system. Chem. Eng. Sci. 55, 817825. Mater. B108, 111117.
Ho, Y.S., 2004. Comment on cadmium removal from aqueous solutions Selatnia, A., Boukazoula, A., Kechid, N., Bakhti, M.Z., Chergui, A.,
by chitin, kinetic and equilibrium studies. Water Res. 38, 29622964. Kerchich, Y., 2004. Biosorption of lead(II) from aqueous solution by a
Iqbal, M., Edyvean, R.G.J., 2004. Biosorption of lead, copper and zinc bacterial dead Streptomyces rimosus biomass. Biochem. Eng. J. 19,
ions on loofa sponge immobilized biomass of Phanerochaete chysos- 127135.
porium. Min. Eng. 17, 217223. Sharma, P., Kumari, P., Srivastava, M.M., Srivastava, S., 2007. Ternary
Jalali, R., Ghafourian, H., Asef, Y., Davarpanah, S.J., Sepehr, S., 2002. biosorption studies of Cd(II), Cr(III) and Ni(II) on shelled Moringa
Removal and recovery of lead using non-living biomass of marine oleifera seeds. Bioresource Technol. 98 (2), 474477.
algae. J. Hazard. Mater. B92, 253262. Sheng, P.X., Ting, Y.P., Chen, J.P., Hong, L., 2004. Sorption of lead,
Kapoor, A., Viraraghavan, T., Cullimore, D.R., 1997. Removal of heavy copper, cadmium, zinc, and nickel by marine algal biomass: charac-
metals using the fungus Aspergillus niger. Bioresource Technol. 70, 95 terization of biosorptive capacity and investigation of mechanism. J.
104. Colloid Interf. Sci. 275, 131141.
King, R.P., 1982. Principles of Flotation. South African Institute of Srivastava, V.C., Swamy, M.M., Mall, I.D., Prasad, B., Mishra, I.M., 2006.
Mining and Metallurgy Johannesburg. Adsorptive removal of phenol by bagasse y ash and activated carbon:
Kiran, I. et al., 2005. Biosorption of Pb(II) and Cu(II) from aqueous equilibrium, kinetics and thermodynamics. Colloids Surf. A272, 89104.
solutions by pretreated biomass of Neurospora crassa. Process Stratton, H., Brooks, P., Griths, P., Seviour, R., 2002. Cell surface
Biochem. 40, 35503558. hydrophobicity and mycolic acid composition of Rhodococcus strains
Kumar, Y.P., King, P., Prasad, V.S., 2006. Equilibrium and kinetic studies isolated from activated sludge foam. J. Ind. Microbiol. Biotechnol. 28,
for the biosorption system of copper(II) ion from aqueous solution 264267.

Please cite this article in press as: Bueno, B.Y.M. et al., Biosorption of lead(II), chromium(III) and copper(II) ..., Miner. Eng. (2007),
doi:10.1016/[Link].2007.08.013
 ARTICLE IN PRESS

B.Y.M. Bueno et al. / Minerals Engineering xxx (2007) xxxxxx 11

Stumm, W., Morgan, J.J., 1996. Aquatic Chemistry, 3rd ed. John Wiley Vijayaraghavan, K., Prabu, D., 2006. Potential of Sargassum wightii
and Sons, New York. biomass for copper(II) removal from aqueous solutions: Application
Tipping, E., 2002. In: Cation binding by humic substances. Centre for of dierent mathematical models to batch and continuous biosorption
Ecology and Hydrology, Windermere. Cambridge University Press, data. J. Hazardous Mater. B137, 558564.
UK. Volesky, B., 2001. Detoxication of metal-bearing euents. Biosorption
Tunali, S., Akar, T., Ozcan, A.S., Kiran, I., Ozcan, A., 2006. Equilibrium for the next century. Hydrometallurgy 59, 203216.
and kinetics of biosorption of lead(II) from aqueous solutions by Volesky, B., 2003. Sorption and Biosorption. BV Sorbex, Canada.
Cephalosporium aphidicola. Sep. Purif. Technol. 47, 105112. Wase, J., Forster, C., 1997. Biosorbents for Metal Ions. Taylor and
Uslu, G., Tanyol, M., 2006. Equilibrium and thermodynamic parameters Francis Ltd.
of single and binary mixture biosorption of lead(II) and copper ions Zouboulis, A.I., Kydros, K., 1995. Removal of Hexavalent Chromium
onto Pseudomonas putida: Eect of temperature. J. Hazardous Mater. Anions from Solutions by Pyrite Fines. Water Res. 29 (7), 17551760.
135, 8793.
Veglio, F., Beolchini, F., 1997. Removal of metals by biosorption a
review. Hydrometallurgy 44, 301316.

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