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Kinetic modeling and equilibrium studies during cadmium biosorption by dead Sargassum sp. biomass
Bioresource Technology 91 (2004) 249–257
Kinetic modeling and equilibrium studies during cadmium biosorption by dead Sargassum sp. biomass ao Henriques a, Claudio C.V. Cruz a, Antonio Carlos A. da Costa b, Cristiane Assumpcß~ Aderval S. Luna a,* a
b
Department of Analytical Chemistry, Institute of Chemistry, Rio de Janeiro State University, Rua S~ ao Francisco Xavier 524, 20559-900, Rio de Janeiro, Brazil Department of Biochemical Processes Technology, Institute of Chemistry, Rio de Janeiro State University, Rua S~ ao Francisco Xavier 524, 20559-900, Rio de Janeiro, Brazil Received 30 January 2003; received in revised form 30 June 2003; accepted 30 June 2003
Abstract A basic investigation on the removal of cadmium(II) ions from aqueous solutions by dead Sargassum sp. was conducted in batch conditions. The influence of different experimental parameters; initial pH, shaking rate, sorption time, temperature and initial concentrations of cadmium ions on cadmium uptake was evaluated. Results indicated that cadmium uptake could be described by the Langmuir adsorption model, being the monolayer capacity negatively affected with an increase in temperature. Analogously, the adsorption equilibrium constant decreased with increasing temperature. The kinetics of the adsorption process followed a secondorder adsorption, with characteristic constants increasing with increasing temperature. Activation energy of biosorption could be calculated as equal to 10 kcal/mol. The biomass used proved to be suitable for removal of cadmium from dilute solutions. Its maximum uptake capacity was 120 mg/g. It can be considered an optimal result when compared to conventional adsorbing materials. Thus Sargassum sp. has great potential for removing cadmium ions especially when concentration of this metal is low in samples such as wastewater streams. Ó 2003 Elsevier Ltd. All rights reserved. Keywords: Cadmium; Biosorption; Kinetic; Equilibrium; Sargassum sp.
1. Introduction Heavy metals are major pollutants in marine, ground, industrial and even treated wastewaters. Stringent regulations are increasing the demand for new technologies for metal removal from wastewater to attain today’s toxicity-driven limits (Esteves et al., 2000). Cadmium is attracting wide attention of environmentalists as one of the most toxic heavy metals. The major sources of cadmium release into the environment by waste streams are electroplating, smelting, alloy manufacturing, pigments, plastic, battery, mining and refining processes (Tsezos, 2001). Cadmium has been recognized for its negative effects on the environment where it readily accumulates in living systems. Adverse health effects due
*
Corresponding author. Fax: +55-21-2587-7227. E-mail address: [email protected] (A.S. Luna).
0960-8524/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0960-8524(03)00194-9
to cadmium are well documented and it has been reported to cause renal disturbances, lung insufficiency, bone lesions, cancer and hypertension in humans (Yin and Blanch, 1989; Sharma, 1995). Considerable research has been carried out in developing cost-effective heavy metal removal techniques. Physicochemical methods, such as chemical precipitation, chemical oxidation or reduction, filtration, electrochemical treatment, application of membrane technology, evaporation recovery, solvent extraction and ion-exchange processes, have been traditionally employed for heavy metal removal from industrial wastewater. However, these techniques may be ineffective or extremely expensive, especially when the metals are dissolved in large volumes of solution at relatively low concentrations (around 1–100 lg/ml) (Valdman and Leite, 2000). The use of biological materials for recovering heavy metals from contaminated industrial effluent has emerged as a potential alternative method to
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conventional techniques (Figueira et al., 2000). There are distinct approaches to this question using both living and nonliving biomass (Gin et al., 2002; Cervantes et al., 2001; Cossich et al., 2002). There are significant practical limitations to methods that employ living microbial systems. Perhaps the most significant limitation is the inhibition of microbial growth when the concentration of metal ions is too high or when significant amounts of metal ions are adsorbed by the microorganism. Nonviable cells accumulate heavy metal ions to an extent that is similar or greater than that of living ones (Guo et al., 2000), since the changes that occur in the cell structure after its inactivation affect adsorption in a positive manner (Da Costa and Duta, 2001). For metal removal, the use of nonviable or denaturated biomass cells may be preferable, since large quantities are readily and economically available as by-products of biotechnology industries (Jalali et al., 2002). The uptake of heavy metal ions can take place by entrapment in the cellular structure and subsequent sorption onto the binding sites present in the cellular structure. This method of uptake is independent of the biological metabolic cycle and is known as ‘‘biosorption’’ or ‘‘passive uptake’’. The heavy metal uptake can also involve its passage into the cell across the cell membrane through the cell metabolic cycle. This mode of metal capture is referred to as ‘‘active uptake’’ (Kapoor et al., 1999). Therefore biosorption is a process that uses any biomass to sorb ions from aqueous solutions. If one considers that nonviable biomass is not biologically active, its metal uptake can be regarded as a passive adsorption process and, thus, be correlated with mathematical sorption models as the Langmuir and Freundlich equations. The major advantages of biosorption include: (i) low cost, (ii) high efficiency of heavy metal removal from diluted solutions, (iii) regeneration of the biosorbent and (iv) the possibility of metal recovery. It has been reported that the biomass of brown algae of the Sargassum genus possesses a metal binding capacity superior to other organic and inorganic sorbents (Holan and Volesky, 1995). Da Costa and De Francßa (1996) compared the biosorptive performance of different types of seaweed (brown, red and green) and reported that Sargassum sp. proved to be the best accumulator of heavy metals due to its high biosorption capacity associated to a low equilibrium concentration. Biosorption of cadmium ions by different living and nonliving biomass have been studied by several authors (Kapoor et al., 1999; Aksu, 2001; Kaewsarn and Yu, 2001; V azquez et al., 2002; Benguella and Benaissa, 2002; Gin et al., 2002). However, little is known on their removal from aqueous solution using Sargassum sp., which showed promising characteristics when used as sorbent for removal of heavy metal ions.
Therefore, in the present work, the adsorption of cadmium ions by Sargassum sp. was studied by investigating the influence of different experimental parameters on cadmium uptake, such as sorption time, initial pH, agitation speed, temperature, and cadmium concentration. The experimental data were correlated to different kinetic and adsorption models and the corresponding parameters were determined as well as their dependence on temperature. These parameters are considered fundamental for further studies involving the scale-up of the process for continuous studies.
2. Methods 2.1. Seaweed The biomass used was the brown seaweed Sargassum sp. (Chromophyta) collected from the Northeastern coast of Brazil. Intact Sargassum sp. was collected from the sea, sampled, extensively washed with distilled water to remove particulate material from its surface, and oven-dried at 343 K for 24 h. From a bulk sample harvested from the sea, 1 kg of biomass was sub-sampled for use in the experiments. In order to ensure that homogeneous samples were used, standard sampling techniques were applied. Dried biomass was cut, ground in a mortar with pestle and subsequently sieved, and the fraction of 0.3–0.7 mm was selected for use in the sorption tests. 2.2. Cadmium solutions Stock cadmium solution (1000 lg/ml) was prepared by dissolving 1.7911 g of cadmium chloride monohydrate (Merck, Darmstadt, Germany) in 100 ml of deionized distilled water (DDW) and diluting quantitatively to 1000 ml using DDW. Cadmium solutions of desired concentration were prepared by adequate dilution of the stock solution with DDW. 2.3. Determination of the cadmium contents in the solutions The concentration of cadmium in the solutions before and after the equilibrium was determined by flame atomic absorption spectrometry (FAAS) using a PerkinElmer AAnalyst 300 (PerkinElmer Corp., Norwalk, CT, USA) atomic absorption spectrometer equipped with deuterium arc background corrector, an air–acetylene burner and controlled by IBM personal computer (International Business Machines Co., New York, USA). The hollow cathode lamp was operated at 4 mA and the analytical wavelength was set at 228.2 nm.
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Glassware and polypropylene flasks were immersed in 10% v/v HNO3 (Vetec, Rio de Janeiro, Brazil) overnight and rinsed several times with DDW. 2.4. Batch biosorption studies Batch biosorption experiments were performed using 100 mg of dried biomass added to 25 ml of cadmium solution in 500 ml polypropylene flasks. The flasks were placed on a rotating shaker (Tecnal, Piracicaba, Brazil) with constant shaking at 150 rpm. For the kinetic study, the initial cadmium concentration was 20 lg/ml and the working pH was that of the solution (pH ¼ 5.5). The sorption time was varied between 3 and 120 min and the temperatures evaluated were 298, 313 and 328 K. At predetermined times, the flasks were removed from the shaker and the solutions were separated from the biomass by filtration through filter paper (Whatman no. 40, ashless, Whatman, Inc., London, UK). The equilibrium isotherms were determined at similar experimental conditions, varying cadmium initial concentration in the range of 20–1000 lg/ml and using an equilibrium time of 2 h. The effect of initial pH on the equilibrium uptake of cadmium ions was investigated between 2.0 and 6.0. The experiments were performed using 100 mg of dried biomass added to 25 ml of 20 lg/ml cadmium solution in 500 ml polypropylene flasks. The flasks were shaken at 150 rpm, at 298 K for 2 h. The initial pH was adjusted using 0.10 mol/l HCl or 0.10 mol/l NaOH solutions. The optimum speed of agitation was determined from experiments carried out at 298 K for 2 h, using 100 mg of Sargassum sp. and 25 ml of 20 lg/ml cadmium solution without adjustment of pH. The 500 ml polypropylene flasks were placed on a rotating shaker and the shaking rate varied between 0 (without agitation) and 200 rpm. All biosorption experiments were done in duplicate.
251
2.6. Statistical analysis Tests of a hypothesis are often considered as tests of significance. The test results will present statistical significance if the null hypothesis is rejected. Otherwise they will not present statistical significance. Actual hypothesis tests are based on the sampling distribution of t, as defined in the formula below. This formula is used to compare the values of two experimental means. This t value is distributed with N1 þ N2 2 degrees of freedom rffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi N1 þ N2 X 1 X 2 ¼ tspooled N1 N2 where ðX 1 X 2 Þ represents the difference between two experimental means; and spooled represents the pooled standard deviation. In this case, we make the assumption that the pooled standard deviation is a good estimate of both sm1 and sm2 , where sm is the standard deviation of the mean. The p-value for a test result represents the degree of rarity of that result, as the null hypothesis is true (Skoog et al., 1996).
3. Results and discussion The influence of several operational parameters; temperature, initial pH, time and shaking rate on biosorption of cadmium ions by Sargassum sp. was investigated. The results were expressed as the amount of cadmium ions adsorbed on dried algae at any time (q, mg/g), adsorbed cadmium ions per gram of Sargassum sp. at equilibrium (qe , mg/g), concentration of cadmium ions that remain in solution at the equilibrium (Ce , lg/ml) and fraction of cadmium adsorbed Xa , % ¼ 1 Ce 100. C0
3.1. Influence of shaking rate 2.5. Metal uptake The cadmium uptake was calculated by the simple concentration difference method. The initial concentration, C0 (lg/ml) and metal concentration at any time, Ct (lg/ml) were determined by FAAS and the metal uptake q (mg metal ion/g Sargassum sp.) was calculated from the mass balance as follows: q¼
ðC0 Ct Þ V w 1000
ð1Þ
where V is the volume of solution in ml and w the mass of sorbent in g. Preliminary experiments had shown that cadmium adsorption losses to the flask walls and to the filter paper were negligible.
In order to determine the optimal shaking rate, the uptake of cadmium ions by Sargassum sp. was evaluated while varying the agitation rate from 0 (without agitation) to 200 rpm. Based on Fig. 1 it appears that cadmium uptake increases with the increase in shaking rate (q ¼ 3:9 mg/g in absence of agitation and 4.8 mg/g at 100 rpm), the maximum adsorption capacity of algae at equilibrium being attained for agitation rates greater than 100 rpm (q ¼ 5:0 mg/g). This indicates that a shaking rate in the range 100–200 rpm is sufficient to assure that all the cell wall binding sites are made readily available for cadmium uptake, so the effect of external film diffusion on biosorption rate can be ignored in any engineering analysis. For the sake of convenience 150 rpm was chosen for further experiments.
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6
6
5
5
4
4
qe (mg/g)
q (mg/g)
252
3
T = 298K
2
3 2
T = 298K
1
C0 = 20 µg/mL
C0 = 20 µg/mL 1
0
0 0
50
100
150
200
250
0
1
2
shaking rate (rpm) Fig. 1. Influence of shaking rate on cadmium uptake by Sargassum sp.
3 4 initial pH
5
6
7
Fig. 2. Effect of the initial pH on equilibrium cadmium uptake by Sargassum sp.
3.2. Influence of initial pH The pH level is one of the most important parameters on biosorption of metal ions from aqueous solutions (Kapoor et al., 1999; Aksu, 2001; Zhang et al., 1998). Regarding Sargassum sp., its high content of ionizable groups (carboxyl groups from mannuronic and guluronic acids) on the cell wall polysaccharides, makes it, at least in theory, very liable to the influence of the medium’s pH. As shown in Fig. 2, the uptake of free ionic cadmium depends on pH, increasing with the increase on pH from 2.0 to 3.0 and then reaching a plateau in the range 3.0–6.0. Similar trends were also observed by Da Costa (1997). At pH lower than 3.0, cadmium(II) removal was inhibited possibly as result of a competition between hydrogen and cadmium ions on the sorption sites, with an apparent preponderance of hydrogen ions. With an increase in pH, the negative charge density on the biomass surface increases due to deprotonation of the metal binding sites and thus increases metal biosorption. The initial pH values investigated were lower than 7.0 since insoluble cadmium hydroxide starts precipitating from the solutions at higher pH values, making true sorption studies impossible.
3.3. Effect of temperature on cadmium biosorption equilibrium The equilibrium uptakes and the fraction of cadmium adsorbed obtained at different temperatures and initial cadmium concentrations are compared in Table 1. The results show that the temperature affects cadmium ions uptake, an effect that is significant only for cadmium initial concentrations greater than 390 lg/ml (t test; P ¼ 0:05). In these cases, the capacity of cadmium adsorption at equilibrium decreases with increasing temperature in the range 298–328 K, indicating that the process of cadmium(II) ions sorption by Sargassum sp. is exothermic, as also observed for the systems Cd(II)– chitin (303–323 K) (Benguella and Benaissa, 2002) and Cd(II)–Chlorella vulgaris (298–323 K) (Aksu, 2001). Regarding the influence of the initial concentration of cadmium ions, the equilibrium sorption capacity of the biomass increased with increasing the initial cadmium ions concentration up to 1000 lg/ml while the fraction of cadmium adsorbed presented the opposite trend. The difference between bulk and surface metal ions concentration is one of the driving-forces to overcome the resistances to adsorption process. In the absence of
Table 1 Equilibrium uptakes (qe ) and fraction of cadmium removed (Xa , %) by Sargassum sp. at different temperatures and initial concentrations (C0 , lg/ml) (any points selected) 298 K
313 K
328 K
C0 (lg/ml)
qe (mg/g)
Xa (%)
C0 (lg/ml)
qe (mg/g)
Xa (%)
C0 (lg/ml)
qe (mg/g)
Xa (%)
20.6 49.1 98.2 245 393 491 982
5.04 (0.12)a 12.1 (0.2) 24.1 (0.5) 56.9 (1.2) 85.8 (1.7) 98.0 (2.0) 114 (2)
98.2 98.3 98.2 92.7 87.4 79.8 46.5
20.6 49.1 98.2 245 393 491 925
5.00 (0.15) 11.9 (0.2) 23.9 (0.6) 54.3 (1.1) 77.6 (1.8) 93.2 (2.0) 99.8 (2.3)
97.1 97.0 97.4 88.3 79.1 75.9 43.1
20.6 51.4 103 257 411 514 925
5.00 (0.13) 12.4 (0.3) 24.5 (0.5) 53.8 (1.2) 73.2 (1.7) 77.5 (2.0) 93.6 (2.2)
96.9 96.6 95.4 84.7 71.5 60.3 40.5
a
(2.0) (1.9) (2.0) (1.8) (2.0) (2.6) (2.0)
(1.9) (2.0) (2.1) (1.9) (1.9) (2.5) (2.1)
(2.0) (1.9) (2.1) (1.8) (1.9) (2.6) (1.9)
Figures in parenthesis are standard deviations obtained for triplicate measurements of the parameter for two identical samples ðn ¼ 6Þ.
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mass-transfer resistances (as is the case of our experiments), surface and bulk concentrations are identical and hence the increasing on initial concentration of cadmium ions will enhance the adsorption process, as observed in Table 1. Constant values of qe are observed for equilibrium concentrations greater than 400 lg/ml, suggesting that above this level of solute, solid–liquid equilibrium is probably limited by the diffusion of the cadmium ions towards the negative charged metalsequestering sites on the surface of the seaweed; that is, the algae surface does not display free sites for metal uptake, being saturated.
253
Langmuir equation can be described by the linearized form: Ce 1 1 ¼ þ Ce qe Q0 KL Q0
ð3Þ
By plotting ðCe =qe Þ versus Ce , Q0 and KL can be determined if a straight line is obtained. While Langmuir isotherm assumes that enthalpy of adsorption is independent of the amount adsorbed, the empirical Freundlich equation, based on sorption on heterogeneous surface, can be derived assuming a logarithmic decrease in the enthalpy of adsorption with the increase in the fraction of occupied sites and is given by:
3.4. Equilibrium modeling qe ¼ KF Ce1=n
qe ¼
Q0 KL Ce 1 þ KL Ce
ð2Þ
where Q0 (mg/g) is the maximum amount of metal ion per unit weight of algae to form a complete monolayer on the surface and KL is the equilibrium adsorption constant which is related to the affinity of the binding sites. Q0 represents a practical limiting adsorption capacity when the surface is fully covered with metal ions and allows the comparison of adsorption performance, particularly in the cases where the sorbent did not reach its full saturation in experiments (Aksu, 2001). The
ð4Þ
where KF and n are the Freundlich constants characteristics of the system, indicating the adsorption capacity and adsorption intensity, respectively. Eq. (4) can be linearized in logarithmic form (5) and the Freundlich constants can be determined. log qe ¼ log KF þ
1 log Ce n
ð5Þ
The linearized form of Langmuir and Freundlich adsorption isotherms obtained at 298, 313 and 328 K are given in Figs. 3 and 4, respectively, whereas Table 2 presents the correspondent constants along with the coefficients of correlation ðRÞ associated at each linearized model. The comparison of the latter ðRÞ indicates that Langmuir isotherm best fits the experimental results over the experimental range studied, since it presents the greater coefficients of correlation at all temperatures. As can be seen in Table 2, the maximum value for the limiting capacity of Sargassum sp. for cadmium(II) ions (Q0 ¼ 120 mg/g) was obtained at 298 K, a slight decrease being observed with the increase in sorption temperature. Similar trends were observed for KL , indicating
8
Ce/qe (mg.g/mL.µg)
Analysis of equilibrium data is important for developing an equation that can be used to compare different biomaterials under different operational conditions and to design and optimize an operating procedure (Benguella and Benaissa, 2002). Several isotherm equations have been used for the equilibrium modeling of biosorption systems. Among these, two are commonly used and have been applied for this study, the Freundlich and Langmuir isotherms. Both represent the equilibrium amount of metal removed ðqe Þ as a function of the equilibrium concentration ðCe Þ of metal ions in the solution, corresponding to the equilibrium distribution of ions between aqueous and solid phases as the initial concentration increases. To measure each isotherm, initial cadmium concentrations were varied while the biomass weight in each sample was kept constant. Equilibrium periods of 2 h for sorption experiments were used to ensure equilibrium conditions. This time was chosen considering the results of kinetics of cadmium removal by Sargassum sp., which will be further presented (Section 3.5). The Langmuir equation assumes that (i) the solid surface presents a finite number of identical sites which are energetically uniform; (ii) there is no interactions between adsorbed species, meaning that the amount adsorbed has no influence on the rate of adsorption; (iii) a monolayer is formed when the solid surface reaches saturation. It assumes the form:
6
4
298K 313K 328K
2
0 0
200
400
600
800
Ce (µg/mL) Fig. 3. Linearized Langmuir adsorption isotherms of cadmium(II) ions by Sargassum sp. at different temperatures.
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studied conditions. The dependence of Freundlich constants with temperature was also quite inconsistent, confirming that this model is not the best to describe the biosorption equilibrium of cadmium(II) ions by the seaweed.
1000
3.5. Biosorption kinetics of cadmium ions
10
298K 313K 328K
1 0.1
1
10
100
1000
Ce (µg/mL) Fig. 4. Linearized Freundlich adsorption isotherms of cadmium(II) ions by Sargassum sp. at different temperatures.
that the affinity of the seaweed for cadmium(II) ions decreases as the temperature of sorption increases. These results are consistent with the effect of temperature on qe discussed previously in Section 3.3. Both the values of Q0 and KL obtained at 298 K are higher than those reported for the sorption of cadmium(II) ions on other biomaterials such as chitin (Q0 ¼ 15:3 mg/g, KL ¼ 3710 l/g mol, at 298 K) (Benguella and Benaissa, 2002) and C. vulgaris (Q0 ¼ 111 mg/g, KL ¼ 2810 l/ g mol, at 293 K) (Aksu, 2001), confirming the applicability of Sargassum sp. as sorbent for heavy metal ions. Since KL is an equilibrium constant, its dependence with temperature can be used to estimate both enthalpy ðDH Þ and entropy ðDSÞ associated to the biosorption process. ln KL ¼
Based on Fig. 5 there is an increase in the adsorption of cadmium ions with the increase in sorption time, regardless of the temperature studied. The uptake equilibrium was achieved after 30 min and no remarkable changes were observed for higher reaction times (not shown in Fig. 5). The curves indicate that the rate of adsorption is high in the first few minutes of the process. It decreases until the equilibrium is reached. The shape of q versus time curves are similar to those reported by different authors concerning other Cd(II)–biomass systems (Benguella and Benaissa, 2002; Aksu, 2001; Vazquez et al., 2002; Kapoor et al., 1999). It can also be observed that temperature influences the adsorption rate, although its effect is not remarkably noticed in the equilibrium uptake, as previously seen in Table 1. As mentioned by Aksu (2001), the fast biosorption kinetics observed is typical for biosorption of metals involving no energy-mediated reactions, where metal removal from solution is due to purely physicochemical interactions between biomass and metal solution.
6 5
DG DH DS ¼ þ RT RT R
ð6Þ 4
The plot of ln KL as a function of 1=T yields a straight line from which DH equal to )5.2 kcal/mol and DS equal to 0.9 cal/mol K were calculated. The negative value of DH confirms the exothermic character of biosorption on Cd(II)–Sargassum sp. system whereas the low value of DS indicates that no remarkable change on entropy occurs. Regarding the corresponding coefficients of correlation obtained, we conclude that the model of Freundlich is not adequate for modeling the isotherm of the removal of cadmium(II) ions by Sargassum sp. in the
q (mg/g)
qe (mg/g)
100
C0 = 20 µg/mL
3
298 K 313 K 328 K
2 1 0 0
5
10 time (min)
15
20
Fig. 5. Influence of sorption time on cadmium ions uptake by Sargassum sp. at different temperatures.
Table 2 Freundlich and Langmuir adsorption constants associated to adsorption isotherms of cadmium(II) ions on Sargassum sp. at different temperatures T (K)
Freundlich constants KF
n
R
Q0 (mg/g)
KL (l/g mol)
R
298 313 328
13.9 (1.4)a 14.6 (2.0) 13.2 (2.6)
2.45 (0.03) 2.92 (0.02) 3.06 (0.02)
0.941 0.955 0.977
120 (1) 103 (1) 98 (2)
8678 (1305) 6655 (1571) 3916 (881)
0.997 0.999 0.997
a
Figures in parenthesis are standard deviations ðn ¼ 20Þ.
Langmuir constants
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3.6. Kinetic modeling
255
Eq. (10) can be rearranged and linearized to obtain:
dq ¼ k1;ads ðqe qÞ ð7Þ dt where qe and q are the amounts of adsorbed metal ions on the biosorbent at equilibrium and at any time t, respectively (mg/g), and k1;ads is the Lagergren rate constant of the first-order biosorption. Integrating (7) between the limits, t ¼ 0 to t ¼ t and q ¼ 0 to q ¼ qe , Eq. (8) is obtained: k1;ads t ð8Þ 2:303 Linear plots of logðqe qÞ versus t indicate the applicability of this kinetic model (Aksu, 2001). However, to adjust Eq. (8) to the experimental data, the value of qe (equilibrium sorption capacity) must be pre-estimated by extrapolating the experimental data to t ¼ 1. The second model is based on the fact that cadmium ions displace alkaline-earth ions (Ca2þ or Mg2þ ) from the algae biosorption sites (De Francßa et al., 2002) and, therefore, with respect to the biosorption sites the metal ions sorption can be considered to be a pseudo-secondorder reaction. The observed kinetics can be modeled assuming that the rate of occupation of adsorption sites is proportional to the square of the number of unoccupied sites logðqe qÞ ¼ log qe
dq 2 ¼ k2;ads ðqe qÞ ð9Þ dt where k2;ads is the rate constant of second-order biosorption (g/mg min). Integrating (9) for the boundary conditions t ¼ 0 to t ¼ t and q ¼ 0 to q ¼ qe , Eq. (10), which corresponds to the integrated rate law for a second-order reaction, is obtained: 1 1 ¼ þ k2;ads t qe q qe
ð10Þ
t 1 1 ¼ þ t q k2;ads q2e qe
ð11Þ
The plot t=q versus t should give a straight line if secondorder kinetics are applicable and qe and k2;ads can be determined from the slope and intercept of the plot, respectively. It is important to notice that for the application of this model the experimental estimation of qe is not necessary. Aiming at evaluating the biosorption kinetics of cadmium ions, the pseudo-first-order and pseudo-second-order kinetic models were used to fit the experimental data. The plot of the linearized form of the pseudo-first-order model at the three studied temperatures for a 20 lg/ml initial cadmium concentration is shown in Fig. 6. Only the data corresponding to the first 30 min are adjusted since after this period the experimental data deviated considerably from those theoretical (not shown in the figure). The Lagergren first-order rate constant ðk1;ads Þ and qe determined from the model are presented in Table 3 along with the corresponding correlation coefficients. The dependence of the firstorder rate constant with temperature was unexpected (maximum at the intermediate temperature, 313 K) and the coefficients of correlation obtained at various temperatures were lower than those found for the pseudo-second-order model. However, the most important feature of this model is that it fails to estimate qe . 7.39 298K 313K 328K
2.72
(qe - q) (mg/g)
There have been several reports (Aksu, 2001; Benguella and Benaissa, 2002; Kapoor et al., 1999; Zhang et al., 1998) on the use of different kinetic models to adjust the experimental data of heavy metals adsorption on biomass. One of them is the pseudo-firstorder Lagergren model that considers that the rate of occupation of adsorption sites is proportional to the number of unoccupied sites
1.00 0.37 0.14 0.05 0.02 0.01 0.00 0
5
10
15
20
25
30
35
time (min) Fig. 6. Linearized Lagergren pseudo-first-order kinetic model for cadmium(II) ions uptake by Sargassum sp. at different temperatures.
Table 3 Comparison between adsorption rate constants, qe estimated and coefficients of correlation associated to the Lagergren pseudo-first-order and to the pseudo-second-order kinetic models (C0 ¼ 20 lg/ml, w ¼ 0:100 g, V ¼ 25 ml, pH 5.5, agitation rate 150 rpm) T (K)
First-order kinetic model 1
298 313 328 a
qe;exp (mg/g)
Second-order kinetic model
k1;ads (min )
qe (mg/g)
R
k2;ads (g/mg min)
qe (mg/g)
R
0.191 (0.011)a 0.248 (0.013) 0.200 (0.019)
1.38 (0.69) 1.32 (0.53) 0.52 (0.12)
0.984 0.986 0.962
0.440 (0.054) 0.770 (0.188) 2.114 (0.388)
5.08 (0.01) 5.01 (0.01) 5.00 (0.01)
1.000 1.000 1.000
Figures in parenthesis are standard deviations (n ¼ 10 first-order kinetic model; n ¼ 20 second-order kinetic model).
5.04 5.00 5.00
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As can be seen in Table 3, qe estimated by this model differs significantly of those measured experimentally, so suggesting that the biosorption is not a first-order reaction. On the other hand, by plotting t=q against t for the studied temperatures, a straight line is obtained in all cases (Fig. 7) and the second-order rate constant (k2;ads ) and qe values were determined from the plots. Both parameters and the correspondent coefficients of correlation are also presented in Table 3. The results show that on increasing sorption temperature the secondorder rate constant also increases indicating that biosorption of cadmium(II) ions on Sargassum sp. is an activated process. The correlation coefficients for the second-order kinetic model are equal to 1 for all temperatures and the theoretical values of qe also agree very well with the experimental ones. Both facts suggest that the sorption of cadmium(II) ions follows the secondorder kinetic model, which relies on the assumption that biosorption may be the rate-limiting step. The second-order rate constant is expressed as a function of temperature by an Arrhenius-type correlation:
k2;ads
E ¼ k0 exp Rg T
ð12Þ
where k0 is the temperature independent factor (g/ mg min), E is the activation energy of sorption (kcal/ mol), Rg is the gas constant (1.987 cal/mol K) and T is the sorption temperature (K). The corresponding linear plot of ln k2;ads as a function of 103 =T is shown in Fig. 8. From the slope of this plot, the activation energy for the biosorption was found as 10 kcal/mol, showing that cadmium(II) biosorption process by Sargassum sp. is an activated one, which confirm its chemical nature (i.e. chemisorption). The results confirm that Sargassum sp. has potential to remove cadmium ions with a high biosorption capacity (120 mg/g or 1.07 mmol/g), a value that is comparable to those observed for microalgae (111 mg/g or 0.99 mmol/g, Aksu, 2001) and considerably higher than values obtained with conventional ion-exchange resins (Table 4). The results obtained also showed that initial pH, temperature, shaking rate and initial metal ion concentration affected the uptake capacity of the biosorbent.
30 2.72
20
k2,ads(g/mg.min)
t/q (min.g/mg)
25
15 10
298K 313K 328K
5
1.00
0.37
0.14
0 0
20
40
60
80
100
120
140
3.25
3.00
time (min)
103/T(K-1)
Fig. 7. Linearized pseudo-second-order kinetic model for cadmium(II) ions uptake by Sargassum sp. at different temperatures.
Fig. 8. Arrhenius plot for k2;ads .
Table 4 Cadmium(II) adsorption capacities of reported sorbents Adsorbent
qmax (mmol/g)
Reference
Rhizopus arrhizus Penicillium chrysogenum Pseudomonas aeruginosa Saccharomyces cerevisiae Peat moss Clinoptilonite Fe(III)/Cr(III) hydroxide Duolite GT-73 Granulated activated carbon Pre-treated Durvillaea potatorum Pre-treated Padina sp. Chlorella vulgaris Sargassum sp.
0.27 0.39 0.38 0.34 0.20 0.21 0.42 0.59 0.07 1.12 0.53 0.99 1.07
Tobin et al. (1993) Fourest et al. (1994) Chang et al. (1997) Matheickal et al. (1991) Gosset et al. (1986) Curkovic et al. (1997) Namasivayam and Ranganathan (1995) Matheickal et al. (1991) Ramos et al. (1997) Matheickal et al. (1999) Kaewsarn and Yu (2001) Aksu (2001) This study
3.50
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4. Conclusions The Langmuir adsorption model effectively described the biosorption equilibrium of cadmium(II) ions on Sargassum sp. in the studied conditions. The monolayer capacity was greater at 298 K, slightly decreasing with the increasing temperature. The Langmuir adsorption equilibrium constant also decreased with the increase in temperature confirming the exothermic character of the sorption process. Assuming the batch biosorption 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. Biosorption kinetics of cadmium(II) ions onto biomass followed a second-order adsorption kinetics. The second-order kinetic constants increased with increasing temperature and the activation energy of biosorption was evaluated as 10 kcal/mol. The pseudo-second-order kinetic modeling can be used to find important parameters for a bioreactor design.
Acknowledgements The authors thank Eng. Wallace Magalh~ aes Antunes, Institute of Chemistry––UERJ, for his aid in FAAS analysis.
References Aksu, Z., 2001. Equilibrium and kinetic modeling of cadmium(II) biosorption by C. vulgaris in a batch system: effect of temperature. Sep. Purif. Technol. 21, 285–294. Benguella, B., Benaissa, H., 2002. Cadmium removal from aqueous solution by chitin: kinetic and equilibrium studies. Water Res. 36, 2463–2474. Cervantes, C., Campos-Garcia, J., Devars, S., Gutierrez-Corona, F., Loza-Tavera, H., Torres-Guzman, J.C., Moreno-Sanchez, R., 2001. Interactions of chromium with microorganisms and plants. FEMS Microbiol. Rev. 25, 335–347. Chang, J.S., Law, R., Chang, C.C., 1997. Biosorption of lead, copper and cadmium by biomass of Pseudomonas aeruginosa PU21. Water Res. 31, 1651–1658. Cossich, E.S., Tavares, C.R.G., Ravagnani, T.M.K., 2002. Biosorption of chromium(III) by Sargassum sp. biomass. Electron. J. Biotechnol. 5, 133–140. Curkovic, L., Stefanovic, S.C., Filipan, T., 1997. Metal ion exchange by natural and modified zeolites. Water Res. 31, 1379–1382. Da Costa, A.C.A., 1997. An emerging biotechnology for metal containing waste water treatment. Ed. CETEM/CNPq, Rio de Janeiro, Brazil, 100 pp. Da Costa, A.C.A., De Francßa, F.P., 1996. Cadmium sorption by biosorbent seaweeds: adsorption isotherms and some process conditions. Sep. Sci. Technol. 31, 2373–2393. Da Costa, A.C.A., Duta, F.P., 2001. Bioaccumulation of copper, zinc, cadmium and lead by Bacillus sp., Bacillus cereus, Bacillus sphaericus and Bacillus subtilis. Braz. J. Microbiol. 32, 1–5. De Francßa, F.P., Tavares, A.P.M., Da Costa, A.C.A., 2002. Calcium interference with continuous biosorption of zinc by Sargassum sp.
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(Phaeophyta) in tubular laboratory reactors. Bioresour. Technol. 83, 159–163. Esteves, A.J.P., Valdman, E., Leite, S.G.F., 2000. Repeated removal of cadmium and zinc from an industrial effluent by waste biomass Sargassum sp. Biotechnol. Lett. 22, 499–502. Figueira, M.M., Volesky, B., Ciminelli, V.S.T., Roddick, F., 2000. Biosorption of metals in brown seaweed biomass. Water Res. 34, 196–204. Fourest, E., Canal, C., Roux, J.C., 1994. Improvement of heavy metal biosorption by mycelial dead biomass (Rhizopus arrhizus, Mucor miehei and Penicillium chrysogenum): pH control and cation activation. FEMS Microbiol. Rev. 28, 21–28. Gin, K.Y.-H., Tang, Y.-Z., Aziz, M.A., 2002. Derivation and application of a new model for heavy metal biosorption by algae. Water Res. 36, 1313–1323. Gosset, T., Transcart, J.L., Thevenot, D.R., 1986. Batch metal removal by peat: kinetics and thermodynamics. Water Res. 20, 21–26. Guo, P., Wang, J., Li, X., Zhu, J., Reinert, T., Heitmann, J., Spemann, D., Vogt, J., Flagmeyer, R.H., Butz, T., 2000. Study of metal bioaccumulation by nuclear microprobe analysis of algae fossils and living algae cells. Nucl. Instrum. Methods Phys. Res. B 161, 801–807. Holan, Z.R., Volesky, B., 1995. Accumulation of cadmium, lead and nickel by fungal and wood biosorbents. Appl. Biochem. Biotechnol. 53, 133–142. Jalali, R., Ghafourian, H., Asef, Y., Davarpanah, S.J., Sepehr, S., 2002. Removal and recovery of lead using nonliving biomass of marine algae. J. Hazard. Mater. 92, 253–262. Kaewsarn, P., Yu, Q., 2001. Cadmium(II) removal from aqueous solution by pre-treated biomass of marine algae Padina sp. Environ. Pollut. 112, 209–213. Kapoor, A., Viraraghavan, T., Cullimore, D.R., 1999. Removal of heavy metals using the fungus Aspergillus niger. Bioresour. Technol. 70, 95–104. Matheickal, J.T., Iyengar, L., Venkobachar, C., 1991. Sorption and desorption of Cu(II) by Ganoderma lucidum. Water Pollut. Res. J. Canada 26, 187–200. Matheickal, J.T., Yu, Q., Woodburn, G.M., 1999. Biosorption of cadmium(II) from aqueous solution by pre-treated biomass of marine algae Durvillaea potatorum. Water Res. 33, 335–343. Namasivayam, C., Ranganathan, K., 1995. Removal of Cd(II) from waste water by adsorption on waste Fe(III)/Cr(III) hydroxide. Water Res. 29, 1737–1744. Ramos, R.L., Mendez, J.R.R., Barron, J.M., Rubio, L., Coronado, R.G.M., 1997. Adsorption of Cd(II) from aqueous solution onto activated carbon. Water Sci. Technol. 35, 205–211. Sharma, Y.C., 1995. Economic treatment of cadmium(II)-rich hazardous waste by indigenous material. J. Appl. Interface Sci. 173, 66–70. Skoog, D.A., West, D.M., Holler, F.J., 1996. Fundamentals of Analytical Chemistry. Saunders College Publishing, Orlando, USA. Tobin, J.M., L’homme, B., Roux, J.C., 1993. Immobilisation protocols and effects on cadmium uptake by Rhizopus arrhizus biosorbents. Biotech. Technol. 7, 739–744. Tsezos, M., 2001. Biosorption of metals. The experience accumulated and the outlook for technology development. Hydrometallurgy 59, 241–243. Valdman, E., Leite, S.G.F., 2000. Biosorption of Cd, Zn and Cu by Sargassum sp. waste biomass. Bioprocess. Eng. 22, 171–173. lvarez, J., Freire, S., L Vazquez, G., Gonzalez-A opez-Lorenzo, M., Antorrena, G., 2002. Removal of cadmium and mercury ions from aqueous solution by sorption on treated Pinus pinaster bark: kinetics and isotherms. Bioresour. Technol. 82, 247–251. Yin, J., Blanch, H.W., 1989. A bio-mimetic cadmium adsorbent: design, synthesis, and characterization. Biotech. Bioeng. 34, 180–188. Zhang, L., Zhao, L., Yu, Y., Chen, C., 1998. Removal of lead from aqueous solution by non-living Rhizopus nigricans. Water Res. 32, 1437–1444.
Kinetic modeling and equilibrium studies during cadmium biosorption by dead Sargassum sp. biomass ao Henriques a, Claudio C.V. Cruz a, Antonio Carlos A. da Costa b, Cristiane Assumpcß~ Aderval S. Luna a,* a
b
Department of Analytical Chemistry, Institute of Chemistry, Rio de Janeiro State University, Rua S~ ao Francisco Xavier 524, 20559-900, Rio de Janeiro, Brazil Department of Biochemical Processes Technology, Institute of Chemistry, Rio de Janeiro State University, Rua S~ ao Francisco Xavier 524, 20559-900, Rio de Janeiro, Brazil Received 30 January 2003; received in revised form 30 June 2003; accepted 30 June 2003
Abstract A basic investigation on the removal of cadmium(II) ions from aqueous solutions by dead Sargassum sp. was conducted in batch conditions. The influence of different experimental parameters; initial pH, shaking rate, sorption time, temperature and initial concentrations of cadmium ions on cadmium uptake was evaluated. Results indicated that cadmium uptake could be described by the Langmuir adsorption model, being the monolayer capacity negatively affected with an increase in temperature. Analogously, the adsorption equilibrium constant decreased with increasing temperature. The kinetics of the adsorption process followed a secondorder adsorption, with characteristic constants increasing with increasing temperature. Activation energy of biosorption could be calculated as equal to 10 kcal/mol. The biomass used proved to be suitable for removal of cadmium from dilute solutions. Its maximum uptake capacity was 120 mg/g. It can be considered an optimal result when compared to conventional adsorbing materials. Thus Sargassum sp. has great potential for removing cadmium ions especially when concentration of this metal is low in samples such as wastewater streams. Ó 2003 Elsevier Ltd. All rights reserved. Keywords: Cadmium; Biosorption; Kinetic; Equilibrium; Sargassum sp.
1. Introduction Heavy metals are major pollutants in marine, ground, industrial and even treated wastewaters. Stringent regulations are increasing the demand for new technologies for metal removal from wastewater to attain today’s toxicity-driven limits (Esteves et al., 2000). Cadmium is attracting wide attention of environmentalists as one of the most toxic heavy metals. The major sources of cadmium release into the environment by waste streams are electroplating, smelting, alloy manufacturing, pigments, plastic, battery, mining and refining processes (Tsezos, 2001). Cadmium has been recognized for its negative effects on the environment where it readily accumulates in living systems. Adverse health effects due
*
Corresponding author. Fax: +55-21-2587-7227. E-mail address: [email protected] (A.S. Luna).
0960-8524/$ - see front matter Ó 2003 Elsevier Ltd. All rights reserved. doi:10.1016/S0960-8524(03)00194-9
to cadmium are well documented and it has been reported to cause renal disturbances, lung insufficiency, bone lesions, cancer and hypertension in humans (Yin and Blanch, 1989; Sharma, 1995). Considerable research has been carried out in developing cost-effective heavy metal removal techniques. Physicochemical methods, such as chemical precipitation, chemical oxidation or reduction, filtration, electrochemical treatment, application of membrane technology, evaporation recovery, solvent extraction and ion-exchange processes, have been traditionally employed for heavy metal removal from industrial wastewater. However, these techniques may be ineffective or extremely expensive, especially when the metals are dissolved in large volumes of solution at relatively low concentrations (around 1–100 lg/ml) (Valdman and Leite, 2000). The use of biological materials for recovering heavy metals from contaminated industrial effluent has emerged as a potential alternative method to
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conventional techniques (Figueira et al., 2000). There are distinct approaches to this question using both living and nonliving biomass (Gin et al., 2002; Cervantes et al., 2001; Cossich et al., 2002). There are significant practical limitations to methods that employ living microbial systems. Perhaps the most significant limitation is the inhibition of microbial growth when the concentration of metal ions is too high or when significant amounts of metal ions are adsorbed by the microorganism. Nonviable cells accumulate heavy metal ions to an extent that is similar or greater than that of living ones (Guo et al., 2000), since the changes that occur in the cell structure after its inactivation affect adsorption in a positive manner (Da Costa and Duta, 2001). For metal removal, the use of nonviable or denaturated biomass cells may be preferable, since large quantities are readily and economically available as by-products of biotechnology industries (Jalali et al., 2002). The uptake of heavy metal ions can take place by entrapment in the cellular structure and subsequent sorption onto the binding sites present in the cellular structure. This method of uptake is independent of the biological metabolic cycle and is known as ‘‘biosorption’’ or ‘‘passive uptake’’. The heavy metal uptake can also involve its passage into the cell across the cell membrane through the cell metabolic cycle. This mode of metal capture is referred to as ‘‘active uptake’’ (Kapoor et al., 1999). Therefore biosorption is a process that uses any biomass to sorb ions from aqueous solutions. If one considers that nonviable biomass is not biologically active, its metal uptake can be regarded as a passive adsorption process and, thus, be correlated with mathematical sorption models as the Langmuir and Freundlich equations. The major advantages of biosorption include: (i) low cost, (ii) high efficiency of heavy metal removal from diluted solutions, (iii) regeneration of the biosorbent and (iv) the possibility of metal recovery. It has been reported that the biomass of brown algae of the Sargassum genus possesses a metal binding capacity superior to other organic and inorganic sorbents (Holan and Volesky, 1995). Da Costa and De Francßa (1996) compared the biosorptive performance of different types of seaweed (brown, red and green) and reported that Sargassum sp. proved to be the best accumulator of heavy metals due to its high biosorption capacity associated to a low equilibrium concentration. Biosorption of cadmium ions by different living and nonliving biomass have been studied by several authors (Kapoor et al., 1999; Aksu, 2001; Kaewsarn and Yu, 2001; V azquez et al., 2002; Benguella and Benaissa, 2002; Gin et al., 2002). However, little is known on their removal from aqueous solution using Sargassum sp., which showed promising characteristics when used as sorbent for removal of heavy metal ions.
Therefore, in the present work, the adsorption of cadmium ions by Sargassum sp. was studied by investigating the influence of different experimental parameters on cadmium uptake, such as sorption time, initial pH, agitation speed, temperature, and cadmium concentration. The experimental data were correlated to different kinetic and adsorption models and the corresponding parameters were determined as well as their dependence on temperature. These parameters are considered fundamental for further studies involving the scale-up of the process for continuous studies.
2. Methods 2.1. Seaweed The biomass used was the brown seaweed Sargassum sp. (Chromophyta) collected from the Northeastern coast of Brazil. Intact Sargassum sp. was collected from the sea, sampled, extensively washed with distilled water to remove particulate material from its surface, and oven-dried at 343 K for 24 h. From a bulk sample harvested from the sea, 1 kg of biomass was sub-sampled for use in the experiments. In order to ensure that homogeneous samples were used, standard sampling techniques were applied. Dried biomass was cut, ground in a mortar with pestle and subsequently sieved, and the fraction of 0.3–0.7 mm was selected for use in the sorption tests. 2.2. Cadmium solutions Stock cadmium solution (1000 lg/ml) was prepared by dissolving 1.7911 g of cadmium chloride monohydrate (Merck, Darmstadt, Germany) in 100 ml of deionized distilled water (DDW) and diluting quantitatively to 1000 ml using DDW. Cadmium solutions of desired concentration were prepared by adequate dilution of the stock solution with DDW. 2.3. Determination of the cadmium contents in the solutions The concentration of cadmium in the solutions before and after the equilibrium was determined by flame atomic absorption spectrometry (FAAS) using a PerkinElmer AAnalyst 300 (PerkinElmer Corp., Norwalk, CT, USA) atomic absorption spectrometer equipped with deuterium arc background corrector, an air–acetylene burner and controlled by IBM personal computer (International Business Machines Co., New York, USA). The hollow cathode lamp was operated at 4 mA and the analytical wavelength was set at 228.2 nm.
C.C.V. Cruz et al. / Bioresource Technology 91 (2004) 249–257
Glassware and polypropylene flasks were immersed in 10% v/v HNO3 (Vetec, Rio de Janeiro, Brazil) overnight and rinsed several times with DDW. 2.4. Batch biosorption studies Batch biosorption experiments were performed using 100 mg of dried biomass added to 25 ml of cadmium solution in 500 ml polypropylene flasks. The flasks were placed on a rotating shaker (Tecnal, Piracicaba, Brazil) with constant shaking at 150 rpm. For the kinetic study, the initial cadmium concentration was 20 lg/ml and the working pH was that of the solution (pH ¼ 5.5). The sorption time was varied between 3 and 120 min and the temperatures evaluated were 298, 313 and 328 K. At predetermined times, the flasks were removed from the shaker and the solutions were separated from the biomass by filtration through filter paper (Whatman no. 40, ashless, Whatman, Inc., London, UK). The equilibrium isotherms were determined at similar experimental conditions, varying cadmium initial concentration in the range of 20–1000 lg/ml and using an equilibrium time of 2 h. The effect of initial pH on the equilibrium uptake of cadmium ions was investigated between 2.0 and 6.0. The experiments were performed using 100 mg of dried biomass added to 25 ml of 20 lg/ml cadmium solution in 500 ml polypropylene flasks. The flasks were shaken at 150 rpm, at 298 K for 2 h. The initial pH was adjusted using 0.10 mol/l HCl or 0.10 mol/l NaOH solutions. The optimum speed of agitation was determined from experiments carried out at 298 K for 2 h, using 100 mg of Sargassum sp. and 25 ml of 20 lg/ml cadmium solution without adjustment of pH. The 500 ml polypropylene flasks were placed on a rotating shaker and the shaking rate varied between 0 (without agitation) and 200 rpm. All biosorption experiments were done in duplicate.
251
2.6. Statistical analysis Tests of a hypothesis are often considered as tests of significance. The test results will present statistical significance if the null hypothesis is rejected. Otherwise they will not present statistical significance. Actual hypothesis tests are based on the sampling distribution of t, as defined in the formula below. This formula is used to compare the values of two experimental means. This t value is distributed with N1 þ N2 2 degrees of freedom rffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi N1 þ N2 X 1 X 2 ¼ tspooled N1 N2 where ðX 1 X 2 Þ represents the difference between two experimental means; and spooled represents the pooled standard deviation. In this case, we make the assumption that the pooled standard deviation is a good estimate of both sm1 and sm2 , where sm is the standard deviation of the mean. The p-value for a test result represents the degree of rarity of that result, as the null hypothesis is true (Skoog et al., 1996).
3. Results and discussion The influence of several operational parameters; temperature, initial pH, time and shaking rate on biosorption of cadmium ions by Sargassum sp. was investigated. The results were expressed as the amount of cadmium ions adsorbed on dried algae at any time (q, mg/g), adsorbed cadmium ions per gram of Sargassum sp. at equilibrium (qe , mg/g), concentration of cadmium ions that remain in solution at the equilibrium (Ce , lg/ml) and fraction of cadmium adsorbed Xa , % ¼ 1 Ce 100. C0
3.1. Influence of shaking rate 2.5. Metal uptake The cadmium uptake was calculated by the simple concentration difference method. The initial concentration, C0 (lg/ml) and metal concentration at any time, Ct (lg/ml) were determined by FAAS and the metal uptake q (mg metal ion/g Sargassum sp.) was calculated from the mass balance as follows: q¼
ðC0 Ct Þ V w 1000
ð1Þ
where V is the volume of solution in ml and w the mass of sorbent in g. Preliminary experiments had shown that cadmium adsorption losses to the flask walls and to the filter paper were negligible.
In order to determine the optimal shaking rate, the uptake of cadmium ions by Sargassum sp. was evaluated while varying the agitation rate from 0 (without agitation) to 200 rpm. Based on Fig. 1 it appears that cadmium uptake increases with the increase in shaking rate (q ¼ 3:9 mg/g in absence of agitation and 4.8 mg/g at 100 rpm), the maximum adsorption capacity of algae at equilibrium being attained for agitation rates greater than 100 rpm (q ¼ 5:0 mg/g). This indicates that a shaking rate in the range 100–200 rpm is sufficient to assure that all the cell wall binding sites are made readily available for cadmium uptake, so the effect of external film diffusion on biosorption rate can be ignored in any engineering analysis. For the sake of convenience 150 rpm was chosen for further experiments.
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6
6
5
5
4
4
qe (mg/g)
q (mg/g)
252
3
T = 298K
2
3 2
T = 298K
1
C0 = 20 µg/mL
C0 = 20 µg/mL 1
0
0 0
50
100
150
200
250
0
1
2
shaking rate (rpm) Fig. 1. Influence of shaking rate on cadmium uptake by Sargassum sp.
3 4 initial pH
5
6
7
Fig. 2. Effect of the initial pH on equilibrium cadmium uptake by Sargassum sp.
3.2. Influence of initial pH The pH level is one of the most important parameters on biosorption of metal ions from aqueous solutions (Kapoor et al., 1999; Aksu, 2001; Zhang et al., 1998). Regarding Sargassum sp., its high content of ionizable groups (carboxyl groups from mannuronic and guluronic acids) on the cell wall polysaccharides, makes it, at least in theory, very liable to the influence of the medium’s pH. As shown in Fig. 2, the uptake of free ionic cadmium depends on pH, increasing with the increase on pH from 2.0 to 3.0 and then reaching a plateau in the range 3.0–6.0. Similar trends were also observed by Da Costa (1997). At pH lower than 3.0, cadmium(II) removal was inhibited possibly as result of a competition between hydrogen and cadmium ions on the sorption sites, with an apparent preponderance of hydrogen ions. With an increase in pH, the negative charge density on the biomass surface increases due to deprotonation of the metal binding sites and thus increases metal biosorption. The initial pH values investigated were lower than 7.0 since insoluble cadmium hydroxide starts precipitating from the solutions at higher pH values, making true sorption studies impossible.
3.3. Effect of temperature on cadmium biosorption equilibrium The equilibrium uptakes and the fraction of cadmium adsorbed obtained at different temperatures and initial cadmium concentrations are compared in Table 1. The results show that the temperature affects cadmium ions uptake, an effect that is significant only for cadmium initial concentrations greater than 390 lg/ml (t test; P ¼ 0:05). In these cases, the capacity of cadmium adsorption at equilibrium decreases with increasing temperature in the range 298–328 K, indicating that the process of cadmium(II) ions sorption by Sargassum sp. is exothermic, as also observed for the systems Cd(II)– chitin (303–323 K) (Benguella and Benaissa, 2002) and Cd(II)–Chlorella vulgaris (298–323 K) (Aksu, 2001). Regarding the influence of the initial concentration of cadmium ions, the equilibrium sorption capacity of the biomass increased with increasing the initial cadmium ions concentration up to 1000 lg/ml while the fraction of cadmium adsorbed presented the opposite trend. The difference between bulk and surface metal ions concentration is one of the driving-forces to overcome the resistances to adsorption process. In the absence of
Table 1 Equilibrium uptakes (qe ) and fraction of cadmium removed (Xa , %) by Sargassum sp. at different temperatures and initial concentrations (C0 , lg/ml) (any points selected) 298 K
313 K
328 K
C0 (lg/ml)
qe (mg/g)
Xa (%)
C0 (lg/ml)
qe (mg/g)
Xa (%)
C0 (lg/ml)
qe (mg/g)
Xa (%)
20.6 49.1 98.2 245 393 491 982
5.04 (0.12)a 12.1 (0.2) 24.1 (0.5) 56.9 (1.2) 85.8 (1.7) 98.0 (2.0) 114 (2)
98.2 98.3 98.2 92.7 87.4 79.8 46.5
20.6 49.1 98.2 245 393 491 925
5.00 (0.15) 11.9 (0.2) 23.9 (0.6) 54.3 (1.1) 77.6 (1.8) 93.2 (2.0) 99.8 (2.3)
97.1 97.0 97.4 88.3 79.1 75.9 43.1
20.6 51.4 103 257 411 514 925
5.00 (0.13) 12.4 (0.3) 24.5 (0.5) 53.8 (1.2) 73.2 (1.7) 77.5 (2.0) 93.6 (2.2)
96.9 96.6 95.4 84.7 71.5 60.3 40.5
a
(2.0) (1.9) (2.0) (1.8) (2.0) (2.6) (2.0)
(1.9) (2.0) (2.1) (1.9) (1.9) (2.5) (2.1)
(2.0) (1.9) (2.1) (1.8) (1.9) (2.6) (1.9)
Figures in parenthesis are standard deviations obtained for triplicate measurements of the parameter for two identical samples ðn ¼ 6Þ.
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mass-transfer resistances (as is the case of our experiments), surface and bulk concentrations are identical and hence the increasing on initial concentration of cadmium ions will enhance the adsorption process, as observed in Table 1. Constant values of qe are observed for equilibrium concentrations greater than 400 lg/ml, suggesting that above this level of solute, solid–liquid equilibrium is probably limited by the diffusion of the cadmium ions towards the negative charged metalsequestering sites on the surface of the seaweed; that is, the algae surface does not display free sites for metal uptake, being saturated.
253
Langmuir equation can be described by the linearized form: Ce 1 1 ¼ þ Ce qe Q0 KL Q0
ð3Þ
By plotting ðCe =qe Þ versus Ce , Q0 and KL can be determined if a straight line is obtained. While Langmuir isotherm assumes that enthalpy of adsorption is independent of the amount adsorbed, the empirical Freundlich equation, based on sorption on heterogeneous surface, can be derived assuming a logarithmic decrease in the enthalpy of adsorption with the increase in the fraction of occupied sites and is given by:
3.4. Equilibrium modeling qe ¼ KF Ce1=n
qe ¼
Q0 KL Ce 1 þ KL Ce
ð2Þ
where Q0 (mg/g) is the maximum amount of metal ion per unit weight of algae to form a complete monolayer on the surface and KL is the equilibrium adsorption constant which is related to the affinity of the binding sites. Q0 represents a practical limiting adsorption capacity when the surface is fully covered with metal ions and allows the comparison of adsorption performance, particularly in the cases where the sorbent did not reach its full saturation in experiments (Aksu, 2001). The
ð4Þ
where KF and n are the Freundlich constants characteristics of the system, indicating the adsorption capacity and adsorption intensity, respectively. Eq. (4) can be linearized in logarithmic form (5) and the Freundlich constants can be determined. log qe ¼ log KF þ
1 log Ce n
ð5Þ
The linearized form of Langmuir and Freundlich adsorption isotherms obtained at 298, 313 and 328 K are given in Figs. 3 and 4, respectively, whereas Table 2 presents the correspondent constants along with the coefficients of correlation ðRÞ associated at each linearized model. The comparison of the latter ðRÞ indicates that Langmuir isotherm best fits the experimental results over the experimental range studied, since it presents the greater coefficients of correlation at all temperatures. As can be seen in Table 2, the maximum value for the limiting capacity of Sargassum sp. for cadmium(II) ions (Q0 ¼ 120 mg/g) was obtained at 298 K, a slight decrease being observed with the increase in sorption temperature. Similar trends were observed for KL , indicating
8
Ce/qe (mg.g/mL.µg)
Analysis of equilibrium data is important for developing an equation that can be used to compare different biomaterials under different operational conditions and to design and optimize an operating procedure (Benguella and Benaissa, 2002). Several isotherm equations have been used for the equilibrium modeling of biosorption systems. Among these, two are commonly used and have been applied for this study, the Freundlich and Langmuir isotherms. Both represent the equilibrium amount of metal removed ðqe Þ as a function of the equilibrium concentration ðCe Þ of metal ions in the solution, corresponding to the equilibrium distribution of ions between aqueous and solid phases as the initial concentration increases. To measure each isotherm, initial cadmium concentrations were varied while the biomass weight in each sample was kept constant. Equilibrium periods of 2 h for sorption experiments were used to ensure equilibrium conditions. This time was chosen considering the results of kinetics of cadmium removal by Sargassum sp., which will be further presented (Section 3.5). The Langmuir equation assumes that (i) the solid surface presents a finite number of identical sites which are energetically uniform; (ii) there is no interactions between adsorbed species, meaning that the amount adsorbed has no influence on the rate of adsorption; (iii) a monolayer is formed when the solid surface reaches saturation. It assumes the form:
6
4
298K 313K 328K
2
0 0
200
400
600
800
Ce (µg/mL) Fig. 3. Linearized Langmuir adsorption isotherms of cadmium(II) ions by Sargassum sp. at different temperatures.
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C.C.V. Cruz et al. / Bioresource Technology 91 (2004) 249–257
studied conditions. The dependence of Freundlich constants with temperature was also quite inconsistent, confirming that this model is not the best to describe the biosorption equilibrium of cadmium(II) ions by the seaweed.
1000
3.5. Biosorption kinetics of cadmium ions
10
298K 313K 328K
1 0.1
1
10
100
1000
Ce (µg/mL) Fig. 4. Linearized Freundlich adsorption isotherms of cadmium(II) ions by Sargassum sp. at different temperatures.
that the affinity of the seaweed for cadmium(II) ions decreases as the temperature of sorption increases. These results are consistent with the effect of temperature on qe discussed previously in Section 3.3. Both the values of Q0 and KL obtained at 298 K are higher than those reported for the sorption of cadmium(II) ions on other biomaterials such as chitin (Q0 ¼ 15:3 mg/g, KL ¼ 3710 l/g mol, at 298 K) (Benguella and Benaissa, 2002) and C. vulgaris (Q0 ¼ 111 mg/g, KL ¼ 2810 l/ g mol, at 293 K) (Aksu, 2001), confirming the applicability of Sargassum sp. as sorbent for heavy metal ions. Since KL is an equilibrium constant, its dependence with temperature can be used to estimate both enthalpy ðDH Þ and entropy ðDSÞ associated to the biosorption process. ln KL ¼
Based on Fig. 5 there is an increase in the adsorption of cadmium ions with the increase in sorption time, regardless of the temperature studied. The uptake equilibrium was achieved after 30 min and no remarkable changes were observed for higher reaction times (not shown in Fig. 5). The curves indicate that the rate of adsorption is high in the first few minutes of the process. It decreases until the equilibrium is reached. The shape of q versus time curves are similar to those reported by different authors concerning other Cd(II)–biomass systems (Benguella and Benaissa, 2002; Aksu, 2001; Vazquez et al., 2002; Kapoor et al., 1999). It can also be observed that temperature influences the adsorption rate, although its effect is not remarkably noticed in the equilibrium uptake, as previously seen in Table 1. As mentioned by Aksu (2001), the fast biosorption kinetics observed is typical for biosorption of metals involving no energy-mediated reactions, where metal removal from solution is due to purely physicochemical interactions between biomass and metal solution.
6 5
DG DH DS ¼ þ RT RT R
ð6Þ 4
The plot of ln KL as a function of 1=T yields a straight line from which DH equal to )5.2 kcal/mol and DS equal to 0.9 cal/mol K were calculated. The negative value of DH confirms the exothermic character of biosorption on Cd(II)–Sargassum sp. system whereas the low value of DS indicates that no remarkable change on entropy occurs. Regarding the corresponding coefficients of correlation obtained, we conclude that the model of Freundlich is not adequate for modeling the isotherm of the removal of cadmium(II) ions by Sargassum sp. in the
q (mg/g)
qe (mg/g)
100
C0 = 20 µg/mL
3
298 K 313 K 328 K
2 1 0 0
5
10 time (min)
15
20
Fig. 5. Influence of sorption time on cadmium ions uptake by Sargassum sp. at different temperatures.
Table 2 Freundlich and Langmuir adsorption constants associated to adsorption isotherms of cadmium(II) ions on Sargassum sp. at different temperatures T (K)
Freundlich constants KF
n
R
Q0 (mg/g)
KL (l/g mol)
R
298 313 328
13.9 (1.4)a 14.6 (2.0) 13.2 (2.6)
2.45 (0.03) 2.92 (0.02) 3.06 (0.02)
0.941 0.955 0.977
120 (1) 103 (1) 98 (2)
8678 (1305) 6655 (1571) 3916 (881)
0.997 0.999 0.997
a
Figures in parenthesis are standard deviations ðn ¼ 20Þ.
Langmuir constants
C.C.V. Cruz et al. / Bioresource Technology 91 (2004) 249–257
3.6. Kinetic modeling
255
Eq. (10) can be rearranged and linearized to obtain:
dq ¼ k1;ads ðqe qÞ ð7Þ dt where qe and q are the amounts of adsorbed metal ions on the biosorbent at equilibrium and at any time t, respectively (mg/g), and k1;ads is the Lagergren rate constant of the first-order biosorption. Integrating (7) between the limits, t ¼ 0 to t ¼ t and q ¼ 0 to q ¼ qe , Eq. (8) is obtained: k1;ads t ð8Þ 2:303 Linear plots of logðqe qÞ versus t indicate the applicability of this kinetic model (Aksu, 2001). However, to adjust Eq. (8) to the experimental data, the value of qe (equilibrium sorption capacity) must be pre-estimated by extrapolating the experimental data to t ¼ 1. The second model is based on the fact that cadmium ions displace alkaline-earth ions (Ca2þ or Mg2þ ) from the algae biosorption sites (De Francßa et al., 2002) and, therefore, with respect to the biosorption sites the metal ions sorption can be considered to be a pseudo-secondorder reaction. The observed kinetics can be modeled assuming that the rate of occupation of adsorption sites is proportional to the square of the number of unoccupied sites logðqe qÞ ¼ log qe
dq 2 ¼ k2;ads ðqe qÞ ð9Þ dt where k2;ads is the rate constant of second-order biosorption (g/mg min). Integrating (9) for the boundary conditions t ¼ 0 to t ¼ t and q ¼ 0 to q ¼ qe , Eq. (10), which corresponds to the integrated rate law for a second-order reaction, is obtained: 1 1 ¼ þ k2;ads t qe q qe
ð10Þ
t 1 1 ¼ þ t q k2;ads q2e qe
ð11Þ
The plot t=q versus t should give a straight line if secondorder kinetics are applicable and qe and k2;ads can be determined from the slope and intercept of the plot, respectively. It is important to notice that for the application of this model the experimental estimation of qe is not necessary. Aiming at evaluating the biosorption kinetics of cadmium ions, the pseudo-first-order and pseudo-second-order kinetic models were used to fit the experimental data. The plot of the linearized form of the pseudo-first-order model at the three studied temperatures for a 20 lg/ml initial cadmium concentration is shown in Fig. 6. Only the data corresponding to the first 30 min are adjusted since after this period the experimental data deviated considerably from those theoretical (not shown in the figure). The Lagergren first-order rate constant ðk1;ads Þ and qe determined from the model are presented in Table 3 along with the corresponding correlation coefficients. The dependence of the firstorder rate constant with temperature was unexpected (maximum at the intermediate temperature, 313 K) and the coefficients of correlation obtained at various temperatures were lower than those found for the pseudo-second-order model. However, the most important feature of this model is that it fails to estimate qe . 7.39 298K 313K 328K
2.72
(qe - q) (mg/g)
There have been several reports (Aksu, 2001; Benguella and Benaissa, 2002; Kapoor et al., 1999; Zhang et al., 1998) on the use of different kinetic models to adjust the experimental data of heavy metals adsorption on biomass. One of them is the pseudo-firstorder Lagergren model that considers that the rate of occupation of adsorption sites is proportional to the number of unoccupied sites
1.00 0.37 0.14 0.05 0.02 0.01 0.00 0
5
10
15
20
25
30
35
time (min) Fig. 6. Linearized Lagergren pseudo-first-order kinetic model for cadmium(II) ions uptake by Sargassum sp. at different temperatures.
Table 3 Comparison between adsorption rate constants, qe estimated and coefficients of correlation associated to the Lagergren pseudo-first-order and to the pseudo-second-order kinetic models (C0 ¼ 20 lg/ml, w ¼ 0:100 g, V ¼ 25 ml, pH 5.5, agitation rate 150 rpm) T (K)
First-order kinetic model 1
298 313 328 a
qe;exp (mg/g)
Second-order kinetic model
k1;ads (min )
qe (mg/g)
R
k2;ads (g/mg min)
qe (mg/g)
R
0.191 (0.011)a 0.248 (0.013) 0.200 (0.019)
1.38 (0.69) 1.32 (0.53) 0.52 (0.12)
0.984 0.986 0.962
0.440 (0.054) 0.770 (0.188) 2.114 (0.388)
5.08 (0.01) 5.01 (0.01) 5.00 (0.01)
1.000 1.000 1.000
Figures in parenthesis are standard deviations (n ¼ 10 first-order kinetic model; n ¼ 20 second-order kinetic model).
5.04 5.00 5.00
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As can be seen in Table 3, qe estimated by this model differs significantly of those measured experimentally, so suggesting that the biosorption is not a first-order reaction. On the other hand, by plotting t=q against t for the studied temperatures, a straight line is obtained in all cases (Fig. 7) and the second-order rate constant (k2;ads ) and qe values were determined from the plots. Both parameters and the correspondent coefficients of correlation are also presented in Table 3. The results show that on increasing sorption temperature the secondorder rate constant also increases indicating that biosorption of cadmium(II) ions on Sargassum sp. is an activated process. The correlation coefficients for the second-order kinetic model are equal to 1 for all temperatures and the theoretical values of qe also agree very well with the experimental ones. Both facts suggest that the sorption of cadmium(II) ions follows the secondorder kinetic model, which relies on the assumption that biosorption may be the rate-limiting step. The second-order rate constant is expressed as a function of temperature by an Arrhenius-type correlation:
k2;ads
E ¼ k0 exp Rg T
ð12Þ
where k0 is the temperature independent factor (g/ mg min), E is the activation energy of sorption (kcal/ mol), Rg is the gas constant (1.987 cal/mol K) and T is the sorption temperature (K). The corresponding linear plot of ln k2;ads as a function of 103 =T is shown in Fig. 8. From the slope of this plot, the activation energy for the biosorption was found as 10 kcal/mol, showing that cadmium(II) biosorption process by Sargassum sp. is an activated one, which confirm its chemical nature (i.e. chemisorption). The results confirm that Sargassum sp. has potential to remove cadmium ions with a high biosorption capacity (120 mg/g or 1.07 mmol/g), a value that is comparable to those observed for microalgae (111 mg/g or 0.99 mmol/g, Aksu, 2001) and considerably higher than values obtained with conventional ion-exchange resins (Table 4). The results obtained also showed that initial pH, temperature, shaking rate and initial metal ion concentration affected the uptake capacity of the biosorbent.
30 2.72
20
k2,ads(g/mg.min)
t/q (min.g/mg)
25
15 10
298K 313K 328K
5
1.00
0.37
0.14
0 0
20
40
60
80
100
120
140
3.25
3.00
time (min)
103/T(K-1)
Fig. 7. Linearized pseudo-second-order kinetic model for cadmium(II) ions uptake by Sargassum sp. at different temperatures.
Fig. 8. Arrhenius plot for k2;ads .
Table 4 Cadmium(II) adsorption capacities of reported sorbents Adsorbent
qmax (mmol/g)
Reference
Rhizopus arrhizus Penicillium chrysogenum Pseudomonas aeruginosa Saccharomyces cerevisiae Peat moss Clinoptilonite Fe(III)/Cr(III) hydroxide Duolite GT-73 Granulated activated carbon Pre-treated Durvillaea potatorum Pre-treated Padina sp. Chlorella vulgaris Sargassum sp.
0.27 0.39 0.38 0.34 0.20 0.21 0.42 0.59 0.07 1.12 0.53 0.99 1.07
Tobin et al. (1993) Fourest et al. (1994) Chang et al. (1997) Matheickal et al. (1991) Gosset et al. (1986) Curkovic et al. (1997) Namasivayam and Ranganathan (1995) Matheickal et al. (1991) Ramos et al. (1997) Matheickal et al. (1999) Kaewsarn and Yu (2001) Aksu (2001) This study
3.50
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4. Conclusions The Langmuir adsorption model effectively described the biosorption equilibrium of cadmium(II) ions on Sargassum sp. in the studied conditions. The monolayer capacity was greater at 298 K, slightly decreasing with the increasing temperature. The Langmuir adsorption equilibrium constant also decreased with the increase in temperature confirming the exothermic character of the sorption process. Assuming the batch biosorption 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. Biosorption kinetics of cadmium(II) ions onto biomass followed a second-order adsorption kinetics. The second-order kinetic constants increased with increasing temperature and the activation energy of biosorption was evaluated as 10 kcal/mol. The pseudo-second-order kinetic modeling can be used to find important parameters for a bioreactor design.
Acknowledgements The authors thank Eng. Wallace Magalh~ aes Antunes, Institute of Chemistry––UERJ, for his aid in FAAS analysis.
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