Process Biochemistry 38 (2002) 89 /99 www.elsevier.

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Determination of the equilibrium, kinetic and thermodynamic parameters of the batch biosorption of nickel(II) ions onto Chlorella vulgaris
Z. Aksu *
Department of Chemical Engineering, Hacettepe University, Beytepe, 06532 Ankara, Turkey Received 16 November 2001; received in revised form 29 January 2002; accepted 19 February 2002

Abstract Although the search for new and innovative treatment technologies has focused attention on the metal binding capacities of various microorganisms, the kinetics of the metal uptake process and the description of the thermal properties of biosorption remain essentially unknown. Biosorption equilibrium, kinetics and thermodynamics of nickel(II) ions to Chlorella vulgaris were studied in a batch system with respect to temperature and initial metal ion concentration. Algal biomass exhibited the highest nickel(II) uptake capacity at 45 8C at an initial nickel(II) ion concentration of 250 mg l (1 and an initial pH of 4.5. Biosorption capacity increased from 48.1 to 60.2 mg g (1 with an increase in temperature from 15 to 45 8C at this initial nickel(II) concentration. Freundlich, Langmuir and Redlich /Peterson isotherm models were applied to experimental equilibrium data of nickel(II) biosorption depending on temperature. Equilibrium data fitted very well to all the equilibrium models in the studied concentration range of nickel(II) ions at all the temperatures studied. The saturation type kinetic model was applied to experimental data at different temperatures changing from 15 to 45 8C to describe the batch biosorption kinetics assuming that the external mass transfer limitations in the system can be neglected and biosorption is chemical sorption controlled. The activation energy of biosorption (EA) was determined as 25.92 kJ mole (1 using the Arrhenius equation. Using the thermodynamic equilibrium coefficients obtained at different temperatures, the thermodynamic constants of biosorption (DG , DH and DS 8) were also evaluated. # 2002 Elsevier Science Ltd. All rights reserved.
Keywords: Biosorption; Nickel(II); Chlorella vulgaris ; Equilibrium; Kinetic; Thermodynamic; Stirred batch reactor

1. Introduction Mining and metallurgy of nickel, stainless steel, nickel electroplating, battery and accumulator manufacturing, pigments and ceramic industries wastewaters contain undesired amount of nickel(II) ions. The main techniques utilized for treatment of nickel(II) bearing waste streams include precipitation, evaporation, adsorption, ion exchange, membrane processing, solvent extraction, etc. These methods have been found to be limited, since they often involve high capital and operational costs and may also be associated with the generation of secondary wastes which present treatment problems [1 /4]. Using microorganisms as biosorbents for heavy metals offers a

* Tel.: '/90-312-2977400; fax: '/90-312-2992124. E-mail address: kmu@hacettepe.edu.tr (Z. Aksu).

potential alternative to existing methods for detoxification and for recovery of these components from industrial wastewaters. The special surface properties of microorganisms enable them to adsorb different kinds of pollutants from solutions. This passive bioaccumulation process (biosorption) has distinct advantages over conventional methods, the process does not produce chemical sludges (i.e. non-polluting), it could be highly selective, more efficient, easy to operate and hence cost effective for the treatment of large volumes of wastewaters containing low pollutant concentrations [2 /23]. Biosorption in natural or uncontrolled situations typically involves a combination of active and passive transport mechanisms starting with the diffusion of the metal ion to the surface of the microbial cell. Once the metal ion has diffused to the cell surface, it will bind to sites on the cell surface which exhibit some chemical

0032-9592/02/$ - see front matter # 2002 Elsevier Science Ltd. All rights reserved. PII: S 0 0 3 2 - 9 5 9 2 ( 0 2 ) 0 0 0 5 1 - 1

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1=n qeq 0KF Ceq

affinity for the metal. This step contain a number of passive accumulation processes and may include adsorption, ion exchange, coordination, complexation, chelation and microprecipitation. Generally, such metal ion adsorption is fast, reversible, and not a limiting factor in bioremoval kinetics when dealing with dispersed cells. Biosorption is often followed by a slower metal binding process in which additional metal ion is bound, often irreversibly. This slow phase of metal uptake can be due to a number of mechanisms, including covalent bonding, surface precipitation, redox reactions, crystallization on the cell surface or, most often, diffusion into the cell interior and binding to proteins and other intracellular sites [2 /23]. Microalgae and marine macroalgae can sequester heavy metal ions by the same adsorption and absorption mechanisms as other microbial biomass. The mechanism of binding metal ions by inactivated algal biomass may depend on the species and ionic charges of metal ion, the algal organism, the chemical composition of the metal ion solution and other external environmental factors such as pH and temperature [2,4,5,8,10,11,14,19 /23]. Although the effects of pH, initial metal ion concentration, biomass concentration on biosorption have been widely studied, information on the effect of temperature is still scanty. The binding of most metals to microorganisms by biosorption is observed to enhance as temperature is increased [3,5,14]. 1.1. Equilibrium parameters of biosorption Equilibrium data, commonly known as adsorption isotherms, are basic requirements for the design of adsorption systems. Classical adsorption models (Langmuir, Freundlich and Redlich /Peterson) were used to describe the equilibrium between adsorbed metal ions on the algal cell (qeq) and metal ions in solution (Ceq) at a constant temperature. The Langmuir equation which is valid for monolayer sorption onto a surface with a finite number of identical sites is given by Eq. (1). qeq 0 Qo bCeq 1 ' bCeq (1)

(2)

where KF and n are the Freundlich constants characteristic on the system. KF and n are indicators of adsorption capacity and adsorption intensity, respectively. Eq. (2) can be linearized in logarithmic form and Freundlich constants can be determined. The Freundlich isotherm is also more widely used but provides no information on the monolayer adsorption capacity, in contrast to the Langmuir model [2 / 4,8,12,18,19,21,24,26]. The three-parameter Redlich /Peterson equation was proposed to improve the fit by the Langmuir or Freundlich equation and is given by Eq. (3). qeq 0 KRP Ceq
b 1 ' aRP Ceq

(3)

where KRP, aRP and b are the Redlich /Peterson parameters. b lies between 0 and 1. For b 0/1 Eq. (3). converts to the Langmuir form. Eq. (3) may be converted into a linear form as written below:   K C ln RP eq (1 0ln aRP 'b ln Ceq (4) qeq The two parameters in the Langmuir and Freundlich equations can be graphically determined. But plotting the left-hand side of Eq. (4). against ln Ceq to obtain the Redlich /Peterson constants is not applicable because of the three unknowns, KRP, aRP and b so the three parameters in the Redlich /Peterson equation are obtained using a least-squares fitting procedure to minimize the deviation between calculated and measured data [25,26].

1.2. Kinetic parameters of biosorption In order to investigate the mechanism of biosorption and potential rate controlling step such as mass transport and chemical reaction processes, kinetic models have been used to test experimental data. In this study it is assumed that the algal particles are spherical and only surface adsorption is occurring. When the biomass is employed as a free cell suspension in a well-agitated batch system, all the cell wall binding sites are made readily available for metal uptake so the effect of external film diffusion on biosorption rate can be assumed not significant and ignored in any engineering analysis. It can be assumed that measured concentrations are equal to cell surface concentrations in this case [21]. The plot of q (the amount of adsorbed metal ion per g of dried algae at any time) versus t (time) can be used to find the initial biosorption rate (rad) by differentiating the plot at t 0/0 as defined in Eq. (5).

where Qo is the maximum amount of the metal ion per unit weight of alga to form a complete monolayer on the surface bound at high Ceq, and b is a constant related to the affinity of the binding sites. Qo represents a practical limiting adsorption capacity when the surface is fully covered with metal ions and assists in the comparison of adsorption performance, particularly in cases where the sorbent did not reach its full saturation in experiments. Qo and b can be determined from the linear plot of Ceq/ qeq versus Ceq [2 /4,8,12,18,19,21,24,26]. The empirical Freundlich equation based on sorption on a heterogeneous surface is given below by Eq. (2).

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91

dq dt

0rad
t00

(5)

1.3. Thermodynamic parameters of biosorption The biosorption process of metal ions can be summarized by the following reversible process which represents a heterogeneous equilibrium. Metal ion in solution l Metal ion(Biosorbent
? The apparent equilibrium constant (K c ) of the biosorption is defined as:

From experimental data, it was shown that the initial biosorption rate is proportional to the first power of the initial metal ion concentration at lower bulk metal ion concentrations and at higher metal ion concentrations, the rate becomes independent of initial metal ion concentration. Eq. (6) can be used to describe the rate of biosorption very accurately in both situations. This kind of rate equation is also defined as saturation type. rad 0 k1 Co 1 ' ko Co (6)

K? 0 c

Cad;eq Ceq

(8)

where k1 and ko are the rate constants of saturation type biosorption which k1 shows the rate constant of firstorder biosorption reaction and ko shows the rate constant of zero-order biosorption reaction. A straight line of 1/rad versus 1/Co suggests the applicability of this kinetic model and k1 and ko can be determined from the slope and intercept of the plot. This model predicts the adsorption behavior over the whole studied concentration range of metal ion and is in agreement with an adsorption mechanism being the rate controlling step [16,24]. The first-order rate constant of the biosorption reaction (k1) is expressed as a function of temperature by the following Arrhenius type relationship:   (EA (7) k1 0Ao exp RT where Ao is the frequency factor, E is the activation energy of sorption, R is the gas constant and T is the solution temperature. When ln k1 is plotted versus 1/T , a straight line with slope */EA/R is obtained. The magnitude of activation energy may give an idea about the type of sorption. Two main types of adsorption may occur, physical and chemical. In physical adsorption the equilibrium is usually rapidly attained and easily reversible, because the energy requirements are small. The activation energy for physical adsorption is usually no more than 4.2 kJ mol(1 (1.0 kcal mol(1), since the forces involved in physical adsorption are weak. Chemical adsorption is specific and involves forces much stronger than in physical adsorption. So the activation energy for chemical adsorption is of the same magnitude as the heat of chemical reactions. Two kinds of chemical adsorption are encountered, activated and, less frequently, nonactivated. Activated chemical adsorption means that the rate varies with temperature according to a finite activation energy (between 8.4 and 83.7 kJ mol (1) in the Arrhenius equation (high EA). In nonactivated chemical adsorption, chemisorption occurs very rapidly, suggesting the activation energy is near zero [24].

where Cad,eq is the concentration of metal ion on the adsorbent at equilibrium. In this case the activity should be used instead of concentration in order to obtain the standard thermodynamic equilibrium constant (Ko) of c ? the biosorption system. If infinite dilution value of K c can be found by calculating the apparent equilibrium ? constant (K c ) at different initial concentrations of metal ion and extrapolating to zero, this value will give Ko. c The Ko value is used in the following equation to c determine the Gibbs free energy of biosorption (DG0) at 25 8C.
o DGo 0(RT ln Kc

(9)

The Gibbs free energy indicates the degree of spontaneity of the adsorption process and the higher negative value reflects a more energetically favorable adsorption. The equilibrium constant may be expressed in terms of enthalpy change of biosorption (DH8) and entropy change of biosorption (DS 8) as a function of temperature. The relationship between the Ko and temperature is c given by the vant Hoff equation:
o ln Kc 0

DS R

DH  RT

(10)

DH 8 and DS 8 can be obtained from the slope and intercept of a vant Hoff plot of ln Ko versus 1/T c [3,27,28]. Although a large number of publications have recently suggested using living and nonliving algae for accumulation and removing heavy metals from polluted water, there seems to be no study which reports all the equilibrium, kinetic and thermodynamic modeling of nickel(II) biosorption due to temperature by dried Chlorella vulgaris , a green microalgae, in a batch system in a wide range of nickel(II) concentration. The binding capacity of C. vulgaris for nickel(II) was shown as a function of temperature and initial nickel(II) concentration in this study. The sorption phenomena were expressed by the Langmuir, Freundlich and Redlich / Peterson adsorption models and the effect of temperature on the model constants was investigated. Only a limited number of studies have so far been focused on the kinetic analysis of biosorption of metal ions in the

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literature so the experimental data were also analyzed using the saturation type adsorption kinetic model and kinetic constants were calculated depending on temperature. The activation energy of the biosorption process, which is an indicator of biosorption type and biosorption mechanism, was also evaluated using these kinetic constants. Since the evaluation of the heat change of the biosorption process is very important for reactor design, the thermodynamics of the biosorption process was also investigated.

reached. Samples (5 ml) were taken before mixing the biosorbent solution and nickel(II) ion bearing solution and at pre-determined time intervals (0, 5, 10, 15, 30, 60 and 120 min) for the residual metal ion concentration in the solution. Before analysis the samples were centrifuged at 4000 rpm for 3 min and the supernatant fraction was analyzed for the remaining nickel(II) ions. Uptake values were determined as the difference between the initial nickel(II) concentration and the one in the supernatant. All experiments were carried out at least twice. Values used in calculations were the arithmetic averages of the experimental data. 2.4. Analysis of nickel(II) ions

2. Experimental 2.1. Microorganism and growth conditions C. vulgaris , a green alga, obtained from Sammlung von Algen Kulturen Pflanzen Physiologisches Institut, Universitat Gottingen, West Germany was used for this study. C. vulgaris was grown at 25 8C as described previously [5]. The pH was adjusted to 7.2 with diluted H2SO4 and NaOH solutions. 2.2. Preparation of algae and nickel(II) solutions for biosorption After 4 /5 days of growth, algal cells were centrifuged at 4000 (2000 )/g) rpm at laboratory temperature for 5/ 6 min and then washed twice with double-distilled water and dried at 60 8C. For the biosorption studies, 10 g of dried algae was suspended in 100 ml of distilled water, and homogenized for 30 min in a homogenizer (Janke and Kunkel, IKA-Labortechnick, Ultra Turrax T25Germany) at 8000 rpm and then stored in the refrigerator. Ten milliliter dried algal suspension was contacted with 90 ml of solution containing a known concentration of nickel(II) ion at the desired temperature and pH. Nickel(II) solutions were prepared by diluting 1.0 g l (1 of stock nickel(II) solution which was obtained by dissolving a weighed quantity of anhydrous nickel(II) sulphate in double-distilled and de-ionized water. The range of concentrations of prepared nickel(II) solutions changed between 50 and 250 mg l (1. The pH of each solution was adjusted to pH 4.5 with diluted or concentrated H2SO4 and NaOH solutions before mixing the algae solution. This pH value was determined as the optimum pH value for the nickel(II) biosorption from the previous studies [14]. 2.3. Batch biosorption studies Experiments were conducted in 250 ml Erlenmeyer flasks containing 100 ml of nickel(II) synthetic solutions. Flasks were agitated on a shaker at 150 rpm constant shaking rate for 120 min to ensure equilibrium was The concentration of residual nickel(II) in the biosorption medium was determined with an Unicam 929 atomic absorption spectrophotometer with the detection limit of 0.063 ppm at the wavelength of 232 nm.

3. Results and discussion Analysis of biosorption data is important for developing equilibrium, kinetic and thermodynamic equations that can be used for design purposes. The biosorption of nickel(II) ions to C. vulgaris was investigated as a function of temperature and initial nickel(II) concentration. The equilibrium, kinetic and thermodynamic results are given as units of adsorbed nickel(II) ion quantity per g of dried biomass at any time and at equilibrium (q ; qeq: mg g(1) adsorbed and unadsorbed nickel(II) ion concentrations in solution at equilibrium, respectively (Cad,eq; Ceq: mg l (1) and initial biosorption rate (rad; mg g(1 min (1) obtained from the slope of q versus time (min) plot at t0/0. 3.1. Effect of temperature on nickel(II) biosorption The equilibrium uptake of nickel(II) ions to the dried green alga was affected by temperature and increased with increasing temperature up to 45 8C (Fig. 1). It was observed that 48.2 mg nickel(II) per g of dried algae was adsorbed at the equilibrium at 45 8C. Nickel(II) biosorption was endothermic thus the extent of adsorption increased with increasing temperature. The sorption of nickel(II) ions by dried C. vulgaris may involve not only physical but also chemical sorption. This effect may be due to the fact that at higher temperatures an increase in active sites occurs due to bond rupture. Fig. 2 shows the biosorption kinetics of nickel(II) ion removal at 15, 25, 35 and 45 8C by plotting the nickel(II) uptake capacity, q , versus time. The biosorption capacity increased with increasing contact time and temperature and a larger amount of nickel(II) was removed by dried C. vulgaris in the first 10 min of

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93

Fig. 1. The effect of temperature on the equilibrium nickel(II) sorption capacity of C. vulgaris (initial pH 4.5; Co, 100 mg l (1; X , 1.0 g l (1, Agitation rate:150 rpm).

contact time. Equilibrium was established in 30 /60 min at the end of a rapid biosorption for all the temperatures studied. After an equilibrium time of 120 min, no more nickel(II) was adsorbed. The metal uptake versus time curves at different temperatures are single, smooth and continuous leading to saturation, suggesting possible monolayer coverage of nickel(II) ions on the surface of the biosorbent. The observed rapid kinetics has also significant practical importance as it will facilitate the

scale-up of the process to smaller reactor volumes ensuring efficiency and economy. 3.2. Effect of initial nickel(II) concentration on temperature-dependent biosorption The initial concentration provides an important driving force to overcome all mass transfer resistance of nickel(II) between the aqueous and solid phases.

Fig. 2. The biosorption curves of nickel(II) ions obtained at 100 mg l (1 initial nickel(II) concentration at different temperatures (Initial pH, 4.5; X , 1.0 g l (1; agitation rate, 150 rpm).

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Table 1 The effect of initial nickel(II) concentration and temperature on the initial biosorption rate and equilibrium uptake capacity of C. vulgaris Co (mg l (1) 15 8C 52.4 78.1 104.0 158.5 245.7 25 8C 42.4 70.5 100.2 148.3 259.0 35 8C 52.2 74.0 102.9 156.2 245.0 45 8C 48.0 76.4 102.1 153.0 250.0 qeq (mg g (1) rad (mg g (1 min (1)

25.0 30.4 35.3 41.0 48.1 31.2 36.2 42.0 47.3 55.6 36.2 40.0 46.3 52.5 58.3 35.4 43.0 48.2 53.7 60.2

3.0 4.3 5.0 6.3 7.1 3.4 4.5 5.6 6.6 7.4 4.5 5.6 6.3 7.2 7.7 5.0 5.9 6.6 7.5 8.0

Hence a higher initial concentration of nickel(II) will increase the adsorption rate. Such an effect was clearly demonstrated in Table 1 with respect to temperature. The initial biosorption rate of nickel(II) ions and the equilibrium sorption capacity of biomass increased with both increasing initial nickel(II) ion concentration up to 250 mg l (1 and increasing temperature up to 45 8C. At 15 8C, when the initial nickel(II) ion concentration increased from 52.4 to 245.7 mg l (1, the initial biosorption rate and the loading capacity of dried biomass increased from 3.0 to 7.1 mg g(1 min(1 and 25.0 to 48.1 mg g(1, respectively. Since cells offer a finite number of surface binding sites, uptake showed saturation at higher metal ion concentrations. The temperature also influenced both the initial biosorption rate and equilibrium metal uptake as shown in Table 1. With the change in temperature from 15 to 45 8C, the uptake capacity increased from 48.1 to 60.2 mg g(1 and initial biosorption rate increased from 7.1 to 8.0 mg g(1 min (1 at 250 mg l (1 initial nickel(II) ion concentration. 3.3. Determination of equilibrium model constants Analysis of the equilibrium data is important to develop an equation which accurately represents the results and which could be used for design purposes. Several isotherm equations have been used for the equilibrium modeling of biosorption systems. Three of

these have been applied in this study, Freundlich, Langmuir and Redlich /Peterson isotherms. For each isotherm initial nickel(II) concentrations were varied while the dry cell weight in each sample was held constant. The linearized Langmuir, Freundlich and Redlich / Peterson adsorption isotherms of nickel(II) ions obtained at the temperatures of 15, 25, 35 and 45 8C are given in Figs. 3 /5. An adsorption isotherm is characterized by certain constants which values express the surface properties and affinity of the sorbent and can also be used to find the biosorptive capacity of biomass. The Langmuir, Freundlich and Redlich /Peterson adsorption constants evaluated from the isotherms at different temperatures and their correlation coefficients are also presented in Table 2. High regression correlation coefficients (/0.985) were found at all the temperatures studied, suggesting that all models are very suitable for describing the biosorption equilibrium of nickel(II) by the algal cells in the studied concentration range. The applicability of all the isotherm models to the nickel(II)-dried algae system implies that both monolayer biosorption and heterogeneous surface conditions exit under the experimental conditions used. The sorption of nickel(II) ions on the biomass is thus complex, involving more than one mechanism. From Table 2, the magnitude of KF and n ; the Freundlich constants, showed easy uptake of nickel(II) from aqueous solution with high adsorptive capacity of the dried C. vulgaris , especially at 45 8C. The highest KF and n values were found as 21.22 and 5.00, respectively, at this temperature value. Table 2. also indicated that n is greater than unity, indicating that nickel(II) ions are favorably adsorbed by dried C. vulgaris at all the temperatures studied. The values of KF and n determined from the Freundlich plots increased with the rise in temperature. While the Freundlich model does not describe the saturation behavior of the biosorbent, Qo, the monocomponent Langmuir constant represents the monolayer saturation at equilibrium. The other mono-component Langmuir constant b, corresponds to the concentration at which a nickel(II) ion amount of Qo/2 is bound and indicates the affinity for the binding of nickel(II) ions. A high b value indicates a high affinity. Values of Qo and b for different temperatures were calculated from the Langmuir plots in Fig. 4 and the results are also tabulated in Table 2. The maximum capacity Qo determined from the Langmuir isotherm defines the total capacity of the biosorbent for nickel(II). The adsorption capacity of biosorbent also increased on increasing the temperature. The value of Qo obtained at 45 8C (i. e. maximum uptake and equal to 63.25 mg g (1 0/1.077 mmol g(1) appears to be higher in comparison with the uptake obtained at the other temperatures. A higher value of b also implied

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95

Fig. 3. The linearized Freundlich adsorption isotherms of nickel(II).

strong bonding of nickel(II) to the dried C. vulgaris at this temperature. Relevant adsorption parameters were also calculated according to the three-parameter isotherm of Redlich / Peterson using the least-squares method for nickel(II) ions and are tabulated in Table 2 at different temperatures. Redlich /Peterson constant KRP indicated that the biosorption capacity of biosorbent also increased with increasing temperature. It is noted that b normally lies

between 0 and 1, indicating favorable adsorption. The value of b obtained for nickel(II) biosorption tends to unity for all the temperatures studied, that is the isotherm is approaching the Langmuir form. 3.4. Determination of kinetic constants In order to analyze the biosorption kinetics of nickel(II) ions, the saturation type kinetic model was

Fig. 4. The linearized Langmuir adsorption isotherms of nickel(II).

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Fig. 5. The linearized Redlich /Peterson adsorption isotherms of nickel(II).

applied to data. Fig. 6 shows the plots of linearized form of the saturation type kinetic model at all temperatures studied. The rate constants k1 and k0 values determined from Fig. 6. at 15, 25, 35 and 45 8C are compared with the correlation coefficients in Table 3. The correlation coefficients obtained are greater than 0.998 for all temperatures studied. The saturation type rate constants also increased with increasing temperatures. The change of rate constant due to temperature also show the biosorption is sorption rate controlled. Fig. 7 shows the corresponding linear plot of ln k1 against 1/T with a high correlation coefficient of 0.992. The activation energy for the biosorption system of nickel(II) onto C. vulgaris was 25.92 kJ mol (1 derived from the slope of this plot. This value is of the same magnitude as the activation energy of activated chemisorption. These findings showed that nickel(II) biosorption process by C. vulgaris is endothermic and involves chemical sorption.

3.5. Determination of thermodynamic constants of biosorption The Ko value evaluated from the Cad,eq/Ceq versus Ceq c plot (data not shown) as 1.3 was used to find the DG 8 value. The standard Gibbs free energy for the biosorption process was obtained at 25 8C as (/0.649 kJ mole (1 using Eq. (9). The negative value of DG 8 is due to the fact that the biosorption process is spontaneous with high affinity of nickel(II) to dried alga. The standard enthalpy and entropy changes of biosorption determined from the ln Ko versus 1/T plot (Fig. 8) were c 11.10 kJ mole (1 and 0.039 kJ mole (1 K (1, respectively. The positive value of DH8 suggests the endothermic nature of biosorption. The positive value of DS 8 confirms the increased randomness at the solid /solution interface during biosorption.

Table 2 The comparison of the Freundlich, Langmuir and Redlich /Peterson adsorption constants obtained from the Freundlich, Langmuir and Redlich / Peterson adsorption isotherms of nickel(II) by C. vulgaris at different temperatures Temperature (8C) Freundlich model KF [(mg g (1)(mg l (1)n] 15 25 35 45 8.31 18.30 20.22 21.22 n 2.99 4.88 4.97 5.00 R2 0.998 0.985 0.992 0.996 Langmuir model Qo (mg g (1) 54.80 59.72 62.56 63.25 b (l mg (1) 0.0254 0.0503 0.0549 0.0660 R2 0.995 0.992 0.997 0.997 Redlich /Peterson model aRP (l mg(1)b 0.312 0.879 1.022 3.305 KRP (l g (1) 4.47 16.03 24.34 73.97 b 0.760 0.787 0.827 0.811 R2 0.999 0.997 0.999 0.999

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Fig. 6. 1/rad vs. 1/Co plots obtained at different temperatures.

4. Conclusion
Table 3 The comparison of the saturation type kinetic rate constants obtained at different temperatures Temperature (8C) 15 25 35 45 k1 (l g (1 min (1) 0.0781 0.1221 0.1641 0.2180 ko (l mg (1) 0.0062 0.0122 0.0165 0.0231 R2 0.989 0.996 0.988 0.994

Although various kinds of microorganisms are known to have the potential to remove metal ions to very low concentrations and to accumulate large amounts of specific toxic elements, the studies focusing specifically on nickel(II) biosorption, investigating temperature dependence of biosorption process and evaluating equilibrium, kinetic and thermodynamic parameters of the system are very limited. The results obtained in these

Fig. 7. ln k1 vs. 1/T plot.

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Fig. 8. ln Kc vs. 1/T plot.

studies reveal major differences in nickel(II) binding efficacy between species when they are compared for maximum nickel(II) biosorption capacities (The maximum nickel(II) biosorption uptakes by these biosorbents were 30.2, 34.4, 1.4 and 3.0 mg g(1 for the microalgae S. obliquus [14], Synechocystis sp . [14], C. vulgaris [4] and C. miniata [4], respectively; 9.0 mg g(1 for the cyanobacteria Nostoc sp. [10]; 12.7 mg g(1 for the bacterium Arthrobacter sp. [12]; 265.0 mg g(1 for the Gram-negative bacterium P. aeruginosa [17]; 23.9 mg g(1 for activated sludge [6]; 3.9 mg g(1 for the fungus Aspergillus niger [18] and 34.2 mg g(1 for the sieved fruit peel of Citrus reticulata [3]). A comparison of the maximum nickel(II) uptake capacity of dried C. vulgaris (63.25 mg g(1 0/1.077 mmol g(1) with those obtained in the literature shows that this microorganism is more effective in biosorbing this metal. The results obtained show that temperature and initial metal ion concentration highly affected the uptake capacity of the biosorbent. Biosorption increased on increasing both the nickel(II) concentration up to 250 mg l(1 and temperature up to 45 8C. The Freundlich, Langmuir and Redlich /Peterson adsorption models were used for the mathematical description of the biosorption equilibrium of nickel(II) ions to dried C. vulgaris depending on temperature and the isotherm constants evaluated from the isotherms were used to compare the biosorptive capacity of the dried biomass. It was seen that the isotherm constants increased with increasing temperature. Results showed that the adsorption equilibrium data fitted very well to all the models in the studied concentration range at all the temperatures studied. Assuming the batch biosorp-

tion as a single-staged equilibrium operation, the separation process can be mathematically defined using these isotherm constants to estimate the residual concentration of metal ions or amount of biosorbent for desired purification. The suitability of the saturation type kinetic model for the sorption of nickel(II) ions onto biomass was also discussed assuming no effect of mass transfer on the biosorption rate. The results calculated due to this model were found to be in good agreement with the experimental results. Using the first-order kinetic constant of saturation type kinetic model increased with increasing temperature, the activation energy of biosorption was determined as 25.92 kJ mol (1 showing that the biosorption process is endothermic. The obtained kinetic parameters can be used for bioreactor design. It may be suitable to apply such simple kinetic models to a well-agitated batch biosorption system consisting of a free cell suspension neglecting external film diffusion. Thermodynamic constants were also evaluated using equilibrium constants changing with temperature. The negative value of DG 8 indicated the spontaneity and the positive values of DH 8 and DS8 showed the endothermic nature and irreversibility of nickel(II) biosorption, respectively. We believe that application of biosorption by the green alga in purification of waste water for the removal of nickel(II) ions from industrial wastewaters can be suitable for large-scale exploitation by using these kinetic parameters. More studies are needed to optimize the system from the regeneration point of view and economic variances.

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5. Nomenclature Ao aRP b Cad,eq Ceq Co EA k1, ko

? Kc

Ko c KF KRP n q qeq Q0 rad R R2 T X b DG 8 DH 8 DS 8

frequency factor Redlich /Peterson adsorption constant [(l mg (1)b] Langmuir adsorption constant (l mg (1) adsorbed metal ion concentration at equilibrium (mg l (1) residual metal ion concentration at equilibrium (mg l (1) initial metal ion concentration (mg l(1) activation energy of sorption (kJ mole (1) rate constants of saturation type biosorption (l g(1 min(1; l mg (1) the apparent equilibrium constant of the biosorption system the standard thermodynamic equilibrium constant (Ko) of the biosorption system c Freundlich adsorption constant [(mg g(1)(mg l (1)n] Redlich /Peterson adsorption constant (l g(1) Freundlich adsorption constant adsorbed metal ion quantity per g of alga at any time (mg g(1) adsorbed metal ion quantity per g of alga at equilibrium (mg g(1) Langmuir adsorption constant (mg g(1) initial biosorption rate (mg g(1 min (1) gas constant (0/8.314 J mol (1 K (1) correlation coefficient solution temperature (8C, K) alga concentration (g l (1) Redlich /Peterson adsorption constant the Gibbs free energy of biosorption (kJ mole (1) enthalpy change of biosorption (kJ mole(1) entropy change of biosorption (kJ mole (1)

References
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