Fundamental aspects of biosorption of lead (II) ions onto a Rhodococcus opacus strain for environmental applications

Minerals Engineering 24 (2011) 1619–1624

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Fundamental aspects of biosorption of lead (II) ions onto a Rhodococcus opacus strain for environmental applications B.Y.M. Bueno a, M.L. Torem a,⇑, Roberto J. de Carvalho a, G.A.H. Pino a, L.M.S. de Mesquita b a b

Department of Materials Engineering, Catholic University of Rio de Janeiro, Rua Marquês de São Vicente, 225 Gávea 22453-900 Rio de Janeiro, Brazil National Petroleum Agency, NPA, Rio de Janeiro, Brazil

a r t i c l e

i n f o

Article history: Received 9 October 2008 Accepted 23 August 2011 Available online 25 September 2011 Keywords: Biotechnology Bacteria Environmental Extractive metallurgy

a b s t r a c t Lead is present in different types of industrial effluents, being responsible for environmental pollution. Biosorption of heavy metal ions by biological material is a promising technology with a potential for treating mineral processing wastewater. In this fundamental work, the biosorption of Pb(II) ions from aqueous solutions using the bacteria Rhodococcus opacus was investigated as a function of contact time, initial metal ion concentration and temperature. The equilibrium studies showed that the biosorption is well described through the Langmuir isotherm model in comparison to the Freundlich model in the concentration range studied (20–200 mg/L). The biosorption capacity obtained from Langmuir equation increased from 86.2 to 95.2 mg/g as the temperature was increased from 15 to 35 °C. Experimental data were also tested in terms of biosorption kinetics using pseudo-first order and pseudo-second-order kinetic models. The result showed that the biosorption processes of lead ions followed well pseudosecond-order kinetics and the adsorption rate constant increased with increasing temperature. The activation energy of biosorption (Ea) was determined (30.4 kJ/mol) using the pseudo-second-order rate constants. The positive values of both DH0 and DS0 obtained suggest that the biosorption of lead (II) ion on the R. opacus was spontaneous and endothermic in nature. Ó 2011 Elsevier Ltd. All rights reserved.

1. Introduction Traditional technologies for heavy metal removal, including ionic exchange and precipitation are frequently inefficient and/or expensive when applied for removal of metal ions in low concentrations. New technologies, with acceptable costs, are necessary to reduce the concentration of heavy metals, presents in wastewaters, in the environment to acceptable levels. Biosorption is a general property of living and dead biomass to rapidly bind a determinate compound from even very diluted aqueous solutions. As a specific term, biosorption is used to depict a method that utilizes materials of biological origin (biosorbents formulated from non living biomass) for the removal of target substances from aqueous solutions (Gadd, 2009; Kotrba, 2011). Compared with traditional technologies, biosorption has advantages such as technically feasible and use of cheap material as biosorbents. These can be microorganisms (including bacteria, yeasts, fungi or algae), many of them (especially fungi) are also frequently used for fermentation processes in agro-industries where after enzyme extraction and biochemical transformations their biomass cannot be re-used and constitutes a waste material that is generally poorly

⇑ Corresponding author. Tel.: +55 21 3527 1723; fax: +55 21 3527 1236. E-mail address: [email protected] (M.L. Torem). 0892-6875/$ - see front matter Ó 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.mineng.2011.08.018

valorized. This biomass may be used for the uptake of metal ions (Volesky, 2003; Vásquez et al., 2007, 2008). Compared with conventional methods for removing toxic metals from industrial effluents, such as precipitation with lime and ion exchange, the biosorption process offers several advantages, such as low operating cost, minimization of the volume of chemical and/or biological sludge to be disposed of, high efficiency in detoxifying very dilute effluents and no nutrient requirements. These advantages are the primary incentives for developing full-scale biosorption processes to clean up heavy metal pollution (Muraleedharam et al., 1991; Kuyucak and Volesky, 1988; Wase and Forster, 1997). The operation of biosorption shares many common features with ion-exchange technology and, despite shorter life cycle and less selectivity options, biosorbents could be considered direct competitors of ion exchange resins. The process of biosorption has many attractive features including the selective removal of metals over abroad range of pH and temperature, its rapid kinetics of adsorption and low capital and operation cost (Macek and Mackova, 2011). Lead is widely used in many important industrial applications, such as storage battery, manufacturing, printing pigments, fuels, photographic materials, explosive manufacturing and the industries, such as coating, automotive, storage batteries, aeronautical and steel industries generate large quantities of wastewater containing various concentrations of lead (Iqbal and Edyvean, 2004;

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Nomenclature b Ce Ca C0 Ea h k1 k2 K 00 M

langmuir adsorption constant (l/mg) residual metal ion concentration at equilibrium (mg/l) amount of lead (II) adsorbed on the biosorbent per liter the solution at equilibrium (mg/l) initial lead (II) ion concentration (mg/l) activation energy of sorption (kJ/mol) initial rate of sorption (mg/gmin) pseudo-first order biosorption rate constant (min1) pseudo-second order biosorption rate constant (g/ mgmin) thermodynamic equilibrium constant of the biosorption system sorbent dosage (g/l)

qe qmax qt R R2 T t DG0 DH0 DS0

amount of lead (II) ion adsorbed on the sorbent at equilibrium (mg/g) langmuir adsorption constant (mg/g) amount of lead (II) ion adsorbed on the sorbent at any time(mg/g) universal gas constant (8.314 J/mol K) correlation coefficient solution temperature (°C, K) time for biosorption (min, h) the Gibbs free energy of biosorption (kJ/mol) enthalpy change of biosorption (kJ/mol) entropy change of biosorption (J/mol K)

Sekhar et al., 2004; Selatnia et al., 2004). Lead is a highly toxic and cumulative poison, can damage the nervous system, kidneys, and reproductive system, particularly in children. The EPA requires lead in drinking water not to exceed 0.015 mg/L. Hence, keeping all the above aspects in view, the biosorption of lead (II) ion onto Rhodococcus opacus was investigated in the present study with respect to temperature and initial metal ion concentration. The biosorption equilibrium was modeled by using the Langmuir and Freundlich isotherm models and the effect of temperature on these model constants was investigated. The thermodynamic parameters of the biosorption process were also evaluated. Further, the kinetics of sorption was determined and the activation energy, which gives an indication of biosorption mechanism, was evaluated using these kinetic constants.

then measured in atomic absorption spectrophotometer (Perkin Elmer 1100B) with an air acetylene flame. The equilibrium data were obtained using the same procedure as the kinetic experiment but with a fixed contact time of 120 min to ensure the equilibrium sate of sorption process. The investigation was performed with the initial metal ion concentration range of 20–200 mg/L. The effect of temperature was also investigated in the range of 15–35 °C.

2. Materials and methods

qe ¼

2.1. Microorganism and growth conditions

where qe: amount of metal ion adsorbed on biosorbent (mg/g) at equilibrium, Co: initial metal ion concentration in solution (mg/L), Ce: residual metal ion concentration at equilibrium in solution (mg/l), V: volume of the medium (L), and M: amount of the biomass used in the reaction mixture (g).

R. opacus obtained from the Culture Collection of the tropical foundation of searches and technology André Tosello-São Paulo, was used in this study. The bacterium was grown at 28 °C (carefully controlled) in agitated liquid media containing, yeast extract, 3 g/L; peptone, 5 g/L; glucose, 10 g/L; malt extract 3.0 g/L. The medium was sterilized by autoclaving at a pressure 1 atm. The pH was adjusted to 7.2 with diluted KOH solutions. Growth was allowed to proceed for 24 h on a horizontal shaker operating at 150 rpm. After the microorganism growth, the culture was separated by centrifugation, and the obtained solid material was washed with deionized water and suspended in NaCl 0.1 mM and later being sterilized at 1 atm of pressure during 20 min. The cellular quantification was determined by dry weight. 2.2. Batch biosorption studies The experiments were performed by mixing 0.2 g of biomass in 100 ml of the synthetic metal ion solutions at 20 mg/L. Analytical grade lead reagent in nitrate form (Pb(NO3)2) was used. The pH was initially adjusted to five for all experiments with 0.1 N HCl and 0.1 N NaOH; the final pH was evaluated and was around 5 ± 0.3. The detailed experimental procedure is described elsewhere (Bueno et al., 2008). The mixture was mixed in a rotary shaker at a rate of 150 rpm where samples were collected within the time interval of 0–120 min. The temperature of the solution was controlled at 25 °C. The biosorbent was separated from the solution by centrifugation for 8 min and metal ion concentration was

2.3. Analysis of lead ions The equilibrium sorption capacity of the biomass at the corresponding equilibrium conditions was determined using a mass balance equation as

C0  Ce V M

ð1Þ

3. Results and discussion 3.1. Equilibrium studies The adsorption isotherm is the relationship between equilibrium concentration of solute in the solution and equilibrium concentration of solute in the sorbent at constant temperature. Analyzing the results of the isotherm data is important for the description of how solute will interact with a biosorbent and are critical in optimizing the use of biosorbent. In order to investigate the biosorption isotherm, two equilibrium models, the Langmuir and the Freundlich isotherm equations, were analyzed. The theoretical Langmuir sorption isotherm (Langmuir, 1918), suggests monolayer sorption on a homogeneous surface without interaction between sorbed molecules. In addition, the model assumes uniform energies of sorption onto the surface and no transmigration of the sorbate; is often used to describe sorption of a solute from a liquid solution as:

Ce 1 1 ¼ þ Ce qe b:qmax qmax

ð2Þ

where qe is the amount of metal ion adsorbed on biosorbent at equilibrium (mg/g), Ce is the equilibrium metal ion concentration in the

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2.5

5.0

2

4.5

1.5

4.0

1

lnqe

Ce /qe (g/L)

B.Y.M. Bueno et al. / Minerals Engineering 24 (2011) 1619–1624

15 C

3.0

25 C

0.5

35 C

0

0

15

30

45

60

75

90

105

120

3.5

T:15 oC T:25 oC T:35 oC

2.5 135

150

2.0

Ce (mg/L)

1.0

1.5

2.0

2.5

3.0

solution (mg/L), qmax is the monolayer biosorption capacity of the biosorbent (mg/g), and b (L/mg) is the Langmuir constant related to the energy of adsorption. The linear plots of Langmuir isotherm for lead biosorption by R. opacus is illustrated in Fig. 1, this Figure indicates the linear relationship between the amount (mg) of Pb(II) ions adsorbed per unit mass (g) of R. opacus biomass against the concentration of Pb(II) ions remaining in solution (mg/L) to different temperatures. The coefficients of determination (R2) were found to be 0.977; 0.973 and 0.982 for Pb(II) biosorption for temperatures of 15, 25, 35 °C, respectively. These results indicate that the biosorption of the metal ions onto R. opacus biomass fitted well the Langmuir model. The adsorption capacity qmax and energy of adsorption b were determined from the slope and intercept of the plot and are listed in Table 1. In other words, the sorption of Pb(II) ions onto R. opacus was taken place at the functional groups/binding sites on the surface of the biomass which is regarded as monolayer biosorption. The maximum biosorption capacity (qmax) of R. opacus biomass was found as 86.2; 87.7 and 95.2 mg/g for Pb(II) biosorption to 15, 25, 35 °C, respectively. The equilibrium biosorption capacity of lead (II) onto Phaseolus vulgaris L. waste was favored at higher temperatures. An increase in the temperature from 20 to 50 °C leads to an increase in the biosorption capacity from 21.85 ± 0.06 to 23.85 ± 0.04 mg/g at an equilibrium time of 20 min. After equilibrium was attained, the uptake increases with increasing temperature. This effect may be explained by availability of more active sites of biosorbent at higher temperatures (Özcan et al., 2009). The Freundlich isotherm model proposes a monolayer sorption with a heterogeneous energetic distribution of active sites, accompanied by interactions between sorbed molecules. Its sorption isotherm is expressed by the following equation:

1 log qe ¼ log K F þ log C e n

Table 1 The Langmuir and Freundlich isotherm obtained at different temperatures for the adsorption of lead (II) ion onto R. opacus.

288 298 308

4.0

4.5

5.0

5.5

6.0

Fig. 2. Freundlich isotherm plots for the biosorption of Pb(II) onto R. opacus biomass (biomass concentration: 2 g L1; contact time: 4 h; pH: 5.0).

Fig. 2 shows the Freundlich isotherms obtained for the biosorption of Pb(II) ions onto R. opacus biomass. The values of KF and 1/n were found to be 6.18, 6.73, 7.57 and 0.52, 0.53, 0.53 for Pb(II) biosorption to 15, 25 and 35 °C, respectively. Table 1 shows the Freundlich constant and linear correlation coefficient. The 1/n values were between 0 and 1 indicating that the biosorption of Pb(II) onto R. opacus biomass was favorable at studied conditions. The R2 values were found to be 0.952, 0.892 and 0.904 to15, 25 and 35 °C, respectively, indicating that the Freundlich model was not able to adequately to describe the relationship between the amount of Pb(II) and adsorbed by the biomass and its equilibrium concentration in the solution. However, the Langmuir isotherm model best fitted the equilibrium data since it presents higher R2 values. A comparison between the results of this work for R. opacus and others found in the literature has been present in Table 2. The values of Pb(II) uptake found in this work are similar or higher than reported for other biosorbents. Thus, the comparison of adsorption capacities shows that the bacterium is efficient biosorbent for the uptake of lead ion. 3.1.1. Determination of thermodynamic parameter from biosorption studies The thermodynamic parameters reflect the feasibility and spontaneous nature of the process. Thermodynamic parameters such as free energy change, enthalpy change and entropy change can be estimated using equilibrium constants changing with temperature. The biosorption process of lead (II) can be summarized by the following reversible process which represents a heterogeneous equilibrium.

LeadðIIÞ in solution $ leadðIIÞ-biosorbent

ð4Þ

ð3Þ

where KF (L/g) gives a measure of the adsorbent capacity and the slope 1/n is an empirical parameter relating the adsorption intensity, which varies with the heterogeneity of the material.

T (K)

3.5

lnCe

Fig. 1. Linearized Langmuir adsorption isotherm of Pb(II) by R. opacus biomass (biomass concentration: 2 g L1; contact time: 4 h; pH: 5.0).

Freundlich model

Langmuir model

KF (L g1)

1/n

R2

qmax (mg g1)

b (L mg1)

R2

6.18 6.73 7.57

0.52 0.53 0.53

0.952 0.892 0.904

86.2 87.7 95.2

0.029 0.036 0.039

0.977 0.973 0.982

Table 2 Comparison of biosorption capacity (qmax of R. opacus) for lead (II) ions with that of different biomass. Biomass

pH

qmax (mg/g)

Reference

Syzygium cumini L. Parmelina tiliaceae Aspergillus niger Tectona grandis L. f. Olive stone waste Bacillus cereus Cephalosporium niger Neurospora crassa Aspergillus flavus Phanerochaete c. Rhodococcus opacus

6.0 5.0 4.0 5.0 5.5 5.5 5.0 4.0 5.0 6.0 5.0

32.5 75.8 34.7 15.4 9.26 36.7 92.4 43.3 13.5 135.3 87.7

King et al., 2007 Uluozlu et al., 2008 Dursun, 2006 Prasanna Kumar et al. 2006 Fiol et al., 2006 Pan et al., 2007 Tunali et al., 2006 Kiran et al. 2005 Akar and Tunali 2006 Iqbal and Edyvean, 2004 Present study

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The apparent equilibrium constant (K 0c of biosorption is defined as:

K 0c ¼

T (K)

Ca Ce

ð5Þ

where Ca is the amount of lead (II) (mg) adsorbed on the biosorbent per liter the solution at equilibrium and Ce is the residual metal ion (lead (II)) concentration at equilibrium in the solution (mg/L) (the units of the value of Kc are obtained by multiply with 207.2 to convert L/mol to L/mg). (K 0c is also known as distribution coefficient and indicate the capability of the R. opacus to retain lead (II) species and also the extent of its movement in a solution phase (Reddy and Dunn, 1996). The (K 0c value is used in the following equation to determine the free change of the biosorption reaction (Gibbs free energy) (DG0) at 25 °C. 0

DG ¼

RT ln K 0c

ð6Þ

where R is the universal gas constant and T the absolute temperature. The free energy change indicates the degree of spontaneity of the biosorption process and the higher negative value reflects more energetically favorable adsorption. The equilibrium constant may be expressed in terms of enthalpy change of biosorption (DH0) and entropy change of biosorption (DS0) as a function of temperature. 0

ln K 0c ¼

Table 3 Thermodynamic parameter for the sorption of lead (II) ion by R. opacus.

0

DS DH  R RT

ð7Þ

In this study, the thermodynamic parameters have been calculated using the Langmuir isotherm, i.e., by replacing the equilibrium constant, K 0c from Eqs. (6) and (7) by the Langmuir isotherm constant, b (L/mol) (Gupta, 1998) and are given in Table 3. The entropy change of biosorption, DS0, and the enthalpy change of biosorption, DH0 can be obtained from the slope and intercept of a Van´t Hoff plot of ln K 0c versus 1/T (Smith and Van Ness, 1987). 3.2. Kinetic studies and determination of activation energy In order to calculate the activation energy of lead (II) ion sorption on R. opacus, the values of the rate constants at different temperatures were determined. Several isotherm kinetic equations have been used in the literature for the equilibrium modeling of biosorption systems. In this study, the pseudo-first order and pseudo-second order rate equations were applied to fit the experimental sorption data of lead (II) ions on the R. opacus biomass. The pseudo-first order rate expression of Lagregren is generally described by the following equation:

dqt ¼ k1 ðqe  qt Þ dt

ð8Þ

where qe and qt are the amounts of lead (II) ion, (mg/g) adsorbed on the sorbent at equilibrium, and at time t, respectively, and k1 is the rate constant (min1). Integrating and applying the boundary conditions, t = 0 and qt = 0 to t = t and qt = qe, Eq. (8) takes the form:

logðqe  qt Þ ¼ log qe 

k1 t 2:303

ð9Þ

The rate constant was obtained from the slope of the linear plots of log(qe  qt) against t (figure not shown). The values of the rate constant k1 obtained for various temperatures are given in Table 3 along with the corresponding correlation coefficients. The sorption data were also analyzed in terms of a pseudosecond order mechanism (Ho and McKay, 2000), described by:

288 298 308

K 0c 3

6.01  10 7.46  103 8.08  103

DG0 (kJ mol1)

DH0 (kJ mol1)

DS0 (J mol1K1)

20.83 22.09 23.04

10.98

0.11

dqt ¼ k2 ðqe  qt Þ2 dt

ð10Þ

where k2 is the rate constant of pseudo-second order biosorption (g/ mgmin). Integrating and applying boundary conditions t = 0 and qt = 0 to t = t and qt = qe, Eq. (10) becomes

qt ¼

t 1=k2 q2e þ t=qe

ð11Þ

Which linear form is:

t 1 1 ¼ þ t qt k2 q2e qe

ð12Þ

Replacing the initial sorption rate k2 q2e by h, we get

t 1 1 ¼ þ t qt h qe

ð13Þ

The pseudo-second order biosorption rate constant (k2) and qe values were determined from the slope and intercept of the plots of t/qt against time, t (Fig. 4). The values of the rate constant are present in Table 3 along with the correlation coefficient. As can be seen from Table 4, the correlation coefficients for the pseudofirst order kinetic model at the various temperatures was found to be lower than 0.972. Also, the equilibrium uptake (qe,cal) values calculated from the pseudo-first order kinetic model did not agree well with the experimental (qe,exp) values. It was also noticed that the second order rate constant, k2 (g/mgmin), increased with an increase in temperature of solution and the correlation coefficient, R2, for the pseudo-second order rate equation was greater than 0.985. Further, the theoretical equilibrium uptake (qe,cal) values agreed very well with the experimental (qe,exp) data in the case of pseudo-second order kinetic model. Hence, it was concluded that this sorption system was better described by second order rate equation than by the first order one. The rate of uptake of lead (II) by R. opacus in these studies was controlled by a chemical sorption phenomenon. Moreover, a pseudo-second order model is applied in sorption of lead (II) on R. opacus. As shown in Fig. 3, the variation in temperatures influenced the time required to reach saturation and the data listed in Table 4 shows that the initial sorption rate correlates positively with the temperature. The initial sorption rate varied from 138.7 to 212.7 mg g1 min1 when the temperature changed from 288 to 308 K. The values of the rate constants were found to increase from 0.344 to 0.789 g mg1 min1 with an increase in the solution

Table 4 A comparison of the pseudo-first order and pseudo-second order rate constants at different temperatures (initial concentration, C0: 20 mg L1; biomass concentration: 2 g L1; initial pH: 5.0; agitation speed: 150 rpm). T qe,exp (K) (mg g1)

288 20.05 298 17.57 308 16.65

Pseudo-first order kinetic model

Pseudo-second order kinetic model

qe R2 k1 (min1) (mg g)

qe (mg/ k2 (g/ g) mg min)

0.28 0.07 0.08

9.43 1.57 0.58

0.901 20.08 0.172 17.61 0.147 16.42

0.344 0.429 0.789

h (mg/ g min)

R2

138.7 133.0 212.7

0.999 0.999 0.999

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9.00

-0.2

8.95

8.85

lnk 2

lnK

-0.4

lnK=13,305 -1320,2*(1/T) 2 R =0,9714

8.90

8.80

y=11,578-3661,12(1/T) 2 R =0,9602

-0.6 -0.8

8.75

-1.0

8.70 -1.2

0.00325 0.00330 0.00335 0.00340 0.00345 0.00350

1/T

1/T (K-1)

Fig. 3. Plot of ln K versus 1/T for the adsorption of lead (II) ion by R. opacus.

t/qt

1,5

1,0

4. Conclusions

0,5

T:15oC T:25oC T:35o C 0

5

10

15

20

25

30

35

time (min) Fig. 4. Pseudo-second order kinetic of lead (II) ion sorption by R. opacus for different temperatures (initial lead (II) ion concentration: 20 mg L1; initial pH: 5.0; biomass concentration: 2 g L1; agitation speed: 150 rpm).

temperatures from 288 to 308 K. However, the equilibrium sorption capacity was little affected by increased temperature. In conventional physisorption systems, increasing temperature usually increases the rate of approach to equilibrium, but decreases the equilibrium capacity (McKay and Porter, 1997). The increase in the pseudo-second order rate constants with increasing temperature may be described by the following equation:

k2 ¼ k0 exp

EA RT

Fig. 5. The variation of ln k2 with 1/T.

(II) on peat is 29.8 kJ mol1. In addition, McKay et al. (1981) reported that the activation energy for the sorption of Telon Blue dye on peat is 26.6 kJ mol1. Again, this value of the activation energy is higher than the normal range of 8–22 kJ mol1 typical of physical adsorption process. The results of this study on the effect of temperature suggest that the sorption rate-controlling step is likely chemical in nature for the sorption of lead (II) on R. opacus.

2,0

0,0

0.00325 0.00330 0.00335 0.00340 0.00345 0.00350




ð14Þ

where k2 is the rate constant of sorption (g mg1 min1), k0 the temperature-independent factor (g mg1 min1), EA the activation energy of sorption (kJ mol1), R the gas constant (8.314 J/mol K) and T the solution temperature (K). There is a linear relationship between the pseudo-second order rate constant and the reciprocal absolute temperature with a correlation coefficient of 0997. The values of k2 were plotted as a function of the reciprocal of the Kelvin temperature and the linear variation is shown in Fig. 5. Hence, the relationship between k and T can be represented in an Arrhenius form as:

k2 ¼ 1:07  105 expð8:314T Þ 30:4

ð15Þ

From Eq. (15), the rate constant of sorption k0 is 1.07  105 g mg1 min1 and the activation energy for sorption EA is 30.4 kJ mol1, which is out of the range (8–22 kJ mol1) of diffusion-controlled processes (Glaston et al., 1941). Ho and McKay (1998) reported that the activation energy for the sorption of lead

The results of the sorption of lead (II) ion onto R. opacus at a pH of 5.0 showed that temperature and initial concentration of metal ion influenced the uptake capacity of the biosorbent. The adsorption equilibrium data fit the Langmuir model better than the Freundlich model in the concentration range (20–200 mg/L) at all the temperatures studied. The maximum lead (II) ion sorption capacity, qmax, on R. opacus was found to have an intermediate value of 89.7 mg/g. The sorption kinetics followed the pseudo-second order rate equation. The biosorption rate constants increased with an increase in temperature. The activation energy of biosorption was determined to be 30.4 kJ/mol showing that the biosorption of lead (II) ions on R. opacus was endothermic. Negative values of DG0 were observed indicating the spontaneous nature of lead (II) ion biosorption on R. opacus. Acknowledgments The authors gratefully acknowledge CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) and FAPERJ (Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro) for supporting this research. References Akar, T., Tunali, T., 2006. Biosorption characteristics of Aspergillus flavus biomass for removal of Pb(II) and Cu(II) ions from an aqueous solution. Bioresource Technology 97, 1780–1787. Bueno, B.Y.M., Torem, M.L., Molina, F., Mesquita, L.M.S., 2008. Biosorption of lead (II), chromium(III) and copper(II) by R. opacus: equilibrium and kinetic studies. Minerals Engineering 21, 65–75. Dursun, A.Y., 2006. A comparative study on determination of the equilibrium, kinetic and thermodynamic parameters of biosorption of copper(II) and lead (II) ions onto pretreated Aspergillus niger. Biochemical Engineering Journal 28 (2), 187–195. Fiol, N., Villaescusa, I., Martínez, M., Miralles, N., Poch, J., Serarols, J., 2006. Sorption of Pb(II), Ni(II), Cu(II) and Cd(II) from aqueous solution by olive stone waste. Separation and Purification Technology 50, 132–140. Gadd, G.M., 2009. Biosorption: critical review of scientific rationale, environmental importance and significance for pollution treatment. Journal of Chemical Technology and Biotechnology 50, 13–28. Glaston, N.S., Laidler, K.J., Eyring, H., 1941. The Theory of Rate Process. McGraw-Hill, New York.

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