Biosorption of Tungsten by Escherichia coli for an Environmentally

Biosorption of Tungsten by Escherichia coli for an Environmentally Friendly Recycling System. Takashi Ogi*, Yuma Sakamoto, Asep Bayu Dani Nandiyanto, ...
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Biosorption of Tungsten by Escherichia coli for an Environmentally Friendly Recycling System Takashi Ogi,* Yuma Sakamoto, Asep Bayu Dani Nandiyanto, and Kikuo Okuyama Department of Chemical Engineering, Hiroshima University, 1-4-1 Kagamiyama, Hiroshima 739-8527, Japan S Supporting Information *

ABSTRACT: In this study, tungsten (W) recovery via biosorption using Escherichia coli was assessed to establish an environmentally friendly recycling system for W. The recovery fraction of soluble WVI was highly dependent on the solution pH, and E. coli cells exhibited the highest WVI uptake capacity for an initial pH of 1.08−2.56. Fourier transform infrared analysis revealed that carboxyl and phosphate functional groups on the surface of the bacteria play a crucial role in adsorption of WVI. Equilibrium and kinetic modeling of WVI biosorption showed that the equilibrium adsorption data fit the Langmuir isotherm model better than the Freundlich model. Kinetic studies revealed that WVI adsorption followed a pseudo-second-order rate model. WVI was recovered by desorption and heating, and adjustment of the pH enabled 95.8% WVI desorption from the E. coli cells. Heating at 1000 °C for 2 h under atmospheric conditions produced concentrates with relatively high concentrations of WVI (97.1% WO3).

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INTRODUCTION Tungsten (W), which is a rare and valuable metal, has the highest melting point of all metals, as well as high strength, thermostability, and abrasion resistance. Accordingly, this metal is widely used for machine-part cutting tools, mill rollers, electric-lamp filaments, thermal shield plates, and catalysts for denitration of exhaust gases and removal of organic materials.1,2 Because use of this metal is likely to increase in the near future, it is becoming increasingly important to develop processes for WVI recovery from wastes. A variety of methods have been developed for recovery of soluble WVI from wastewater by chemical precipitation using alkaline solutions,3 solvent extraction,4 and ion-exchange techniques;1 however, these methods have significant disadvantages. Specifically, they have high reagent and/or energy requirements, generate toxic sludge or other waste products, and are expensive. In the case of ion-exchange methods, large amounts of eluents are required for desorption of WVI ions, which results in the production of a large amount of wastewater. Therefore, individuals from many disciplines are faced with the challenging task of developing more economical and effective technologies for WVI recovery. Metal biotechnology, defined as biological technology that uses the reactions of various metals in metabolism and chemical binding by living organisms and biomolecules, has attracted a great deal of attention for its potential for application in environmental protection and sustainability.5−7 In metal biotechnology, biosorption is a candidate for alternative metal recovery technologies because it has low operating costs, minimizes the volumes of chemical and/or biological sludges to be handled, and is highly efficient for detoxifying effluents.8−10 Furthermore, certain types of biomasses can bind and concentrate metals from even very dilute aqueous solutions. Among the biosorption methods for metals, bacterial biosorption has attracted a great deal of attention because bacteria are extremely abundant and versatile microorganisms © 2013 American Chemical Society

that constitute a significant fraction of the living terrestrial biomass. There have been many studies of the biosorption of various metal ions including PbII, ZnII, CuII, FeII, CrVI, NiII, PdII, PtIV, UVI, AuIII, AgI, ReVII, and InIII using bacterial species,9−13 and several researchers have investigated isotherm modeling for bacterial biosorption.14−17 Malekzadeh et al. conducted a thorough investigation of the biosorption of WVI by a Bacillus sp., as well as the effects of parameters such as the pH, initial WVI and cell concentration, live activity, and addition of other cations on the adsorption capacity.18 However, the bacteria used in their study were not common. Investigations of WVI biosorption using easily available and inexpensive bacteria are therefore important for industrial applications. In this study, we used Escherichia coli as the bacterial biosorbent because it has a rapid cultivation rate, is easy to obtain, and is both inexpensive and safe. In this study, the effects of various environmental parameters, such as the solution pH, temperature, and initial concentrations of WVI and bacterial cells on the recovery fraction of WVI, were investigated. Equilibrium and kinetic models of WVI biosorption were then used to analyze the biosorption mechanism. Furthermore, the recovery of WVI from WVI-adsorbed bacteria was achieved by a desorption and heating process.

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MATERIALS AND METHODS Bacterial Strain and Growth Conditions. E. coli ATCCPTA-3137 was obtained from the American Type Culture Collection (ATCC). E. coli cells were inoculated into a 500-mL Erlenmeyer flask containing 250 mL of Luria−Bertani broth, after which the flask was sealed with an absorbent cotton stopper and incubated in a temperature-controlled shaker for Received: Revised: Accepted: Published: 14441

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14 h at 37 °C at 110 rpm.19 E. coli cells were then harvested by centrifugation (24310g, 10 min), resuspended in distilled water, and repelleted by centrifugation. This procedure was repeated twice, after which the washed cells were resuspended in distilled water and immediately used in the WVI biosorption experiments. Preparation of W Solutions. A metal solution containing WVI ions was prepared by dissolving a known weight of sodium tungstate(VI) dihydrate (Na2WO4·2H2O) in distilled water. The concentration of WVI ranged from 0.10 to 7.00 mmol/L, and the pH of each test solution was adjusted to the required value with 1.00 mmol/L HCl before adding the bacterial biomass. A biosorbent-free solution was also prepared as a control. Sorption of W by E. coli. In a typical sorption experiment, 5 mL of an E. coli cell suspension was added to 10 mL of an aqueous Na2WO4 solution and the pH was adjusted from 6.62 to 1.08 using HCl. Unless otherwise stated, the experiment was conducted at 22.6 °C for 7 h. The cell concentration in the mixed solution ranged from 0.63 × 109 to 16 × 109 cells/mL. To follow the time course of the microbial WVI adsorption, aliquots of the mixture were periodically withdrawn and the concentration of WVI was determined using inductively coupled plasma atomic emission spectroscopy (ICP-AES; SII, S-3000, Seiko Instruments Inc., Chiba, Japan). Table S1 in the Supporting Information (SI) summarizes the plasma instrumental conditions. As shown in Figure S1 in the SI, the calculated errors of the experimental results were less than 1.0%. The number of E. coli cells in the solution was determined in a Petroff−Hausser counting chamber (Hausser Scientific, Horsham, PA) using a microscope (VHZ450, Keyence, Osaka, Japan). ζ Potential Analysis. The effects of the pH on the ζ potential of E. coli were investigated using a Zetasizer (Nano ZS, Malvern Instruments Ltd., Worcestershire, U.K.). Briefly, 1.00 mL of a bacterial suspension was added to a sample bottle containing 14.00 mL of water. The pH of the solution was then adjusted with 0.10 or 1.00 mol/L HCl solutions. Fourier Transform Infrared (FTIR) Analysis. To investigate the main functional groups responsible for WVI adsorption and the chemical nature of the binding process between WVI and E. coli cells, dried E. coli cells and WVIadsorbed E. coli cells were analyzed by FTIR spectroscopy (PerkinElmer, Spectrum One System). For FTIR analysis, the biomass was centrifuged and dried at 90 °C, after which 10 mg of finely ground biomass was used to make pellets. Transmission Electron Microscopy (TEM) Mapping Analysis. The morphologies of E. coli cells before and after WVI adsorption were analyzed using a transmission electron microscope (JEM-3000F, JEOL, Tokyo, Japan) operated at 297 kV. Elemental analyses of the samples were conducted using an energy-dispersive X-ray spectrometer interfaced with the TEM system. Elemental mapping of the E. coli cells was carried out using the three-windows method, with a postcolumn 90° energy filter system (GIF-2000, Gatan Inc., Warrendale, PA). Isotherm, Thermodynamic, and Kinetic Studies. Isotherm Study. For the isotherm study, the Langmuir and Freundlich models were used to analyze the sorption data obtained at different temperatures and initial WVI concentrations while maintaining the cell concentration at (0.63−4.7) × 109 cells/mL. The Langmuir equation,20 which is valid for monolayer sorption onto a surface with a finite number of identical sites, is given by eq 1:

qe =

Q maxbCe 1 + bCe

(1)

where Qmax (mg/g) is the maximum amount of metal ions adsorbed per unit weight of E. coli cells to form a complete monolayer on the surface bound at a high equilibrium metalion concentration Ce (mg/L) and b (L/mg) is a constant related to the affinity of the binding sites. This equation can be expressed linearly as follows: Ce 1 1 = Ce + qe Q max bQ max

(2) 21

The empirical Freundlich adsorption isotherm is obtained on the assumption that sorption takes place on a heterogeneous adsorbent surface, where the sorption energy distribution decreases exponentially. This equation is applicable to multilayer adsorption and is expressed by the following equation: qe = KCe1/ n

(3)

where K and n are the Freundlich constants, which represent the adsorption capacity and adsorption intensity of the sorbent, respectively. Equation 3 can be linearized by taking logarithms, giving log qe =

1 log(Ce) + log K n

(4)

from which the Freundlich constants can be determined. Thermodynamic Study. Both energy and entropy factors must be considered to determine whether a process will occur spontaneously. The process of WVI biosorption can be represented by a reversible process, WVI ion solution ⇔ WVI−E. coli, which is a heterogeneous equilibrium. For such equilibrium reactions, the Gibbs free energy (ΔG0) is determined by the following equation: ΔG0 = −RT ln K 0C

(5)

where R is the universal gas constant [8.314 J/(mol·K)], T is the absolute temperature in kelvin, and KC0 is the equilibrium constant. The Gibbs free energy indicates the degree of spontaneity of the adsorption process, and a more negative value reflects a more energetically favorable adsorption process. The relationship between the equilibrium constant, KC0 , and the temperature is given by the van’t Hoff equation: ln K 0C =

ΔS0 ΔH0 − R RT

(6)

The entropy change of biosorption, ΔS0, and the enthalpy change of biosorption, ΔH0, can be obtained from the slope and intercept of a van’t Hoff plot of ln KC0 versus 1/T.22−24 Kinetic Study. For the kinetic study, the values of the rate constants at different temperatures were also determined. Several isotherm kinetic equations have been reported in previous studies in which equilibrium modeling of biosorption systems was conducted. In this study, pseudo-first-order and pseudo-second-order rate equations were used to fit the experimental sorption data for WVI ions on E. coli. Lagergren’s pseudo-first-order rate expression25 is generally described by the following equation:

dqt dt 14442

= k1(qe − qt )

(7)

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where qe and qt are the amounts of WVI ions (mmol/g) adsorbed on the sorbent at equilibrium and at time t, respectively, and k1 is the rate constant (min−1). When the boundary conditions t = 0 and qt = 0 are integrated and applied to t = t and qt = qe, eq 7 takes the form log(qe − qt ) = log qe −

k1 t 2.303

(8)

The rate constant was obtained from the slope of the linear plot of log(qe − qt) against t. The sorption data were also analyzed in terms of a pseudo-second-order mechanism26 described by dqt dt

= k 2(qe − qt )2

(9)

Figure 1. Time course of soluble WVI concentration during the biosorption experiment using 1.8 × 109 cells/mL resting cells of E. coli at different pH values of (▲) pH 6.62, (◆) pH 4.63, (●) pH 1.93, (▼) pH 1.37, and (■) pH 1.08, and (Δ) sterile control without E. coli.

where k2 is the rate constant of pseudo-second-order biosorption [g/(mmol/min)]. When the boundary conditions t = 0 and qt = 0 are integrated and applied to t = t and qt = qe, eq 9 becomes qt =

t 1/k 2qe 2 + t /qe

(10)

which has a linear form of t 1 1 = + t 2 qt qe k 2qe

(11)

Upon replacing the initial sorption rate k2qe2 by h, we get 1 1 t = + t h qt qe

(12)

The biosorption rate constant (k) and qe values were determined from the slope and intercept of the plot of t/qt against time t. Recovery of W from E. coli (Desorption and Heating). In this study, desorption and heating of bacterial cells were used to recover WVI from E. coli. For the desorption experiments, WVI-adsorbed samples were equilibrated at a temperature of 25.0 °C with 0.100 mol/L NaOH for 2 h. Drying and heating processes were used to prepare W concentrates from the WVIadsorbed bacteria. After exposure to a Na2WO4 solution, the E. coli cells were centrifuged and dried at 120 °C for 2 h in a drying oven. The dried sample was then heated at 1000 °C for 2 h in a furnace under atmospheric conditions. The concentration of WVI in the concentrate was measured using ICP spectroscopy. The crystal structure of the obtained powder sample after heating was also investigated using powder X-ray diffraction (XRD; Rigaku, Tokyo, Japan, RINT 2200 V) with Cu Kα radiation.

Figure 2. Effect of the pH on the recovery ratio of WVI and ζ potential of E. coli: (a) sorption ratio; (b) ζ potential.

from 7.11 to 2.56. However, further decreases in the solution pH to 1.40 resulted in decreases in the recovery of WVI. To investigate the cause of this phenomenon, the ζ potentials of the cell surfaces were analyzed at various solution pH values (Figure 2b). The ζ potentials of the cell surfaces of E. coli were found to be strongly related to the recovery ratio of WVI. The main chemical species in 1 mmol/L Na2WO4 aqueous solutions is WO42− at pH > 7, whereas at lower pH, the predominant species is HW6O215−. Decreases in the pH of the E. coli cell suspension changed the ζ potential of the cell surface to a positive charge and enhanced the electrostatic force of attraction to HW6O215−. As a result, microbial adsorption occurs more readily when the pH is lower than 2.56. However, at pH < 1.40, the recovery ratio of WVI decreased slightly. This decrease in the recovery ratio of WVI was caused by a decrease in the ζ potential of the cell surface. These findings are similar to those of previous investigations of the biosorption of AsIII using E. coli.19 FTIR Analysis. FTIR spectra of E. coli cells before and after WVI binding were evaluated to obtain a better understanding of the involvement of the main functional groups involved in WVI binding. The characteristic absorption peaks in the IR spectra of the biomass before and after WVI adsorption are shown in

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RESULTS AND DISCUSSION Effects of the Initial pH on W Uptake. Figure 1 shows the effects of the solution pH on the biosorption of soluble WVI by resting cells of E. coli at 22.6 °C. The concentration of E. coli cells was maintained at 1.8 × 109 cells/mL, while the pH of the solution was altered from 6.62 to 1.08. As shown in Figure 1, the aqueous concentration of WVI rapidly decreased when the pH of the Na2WO4 solution was less than 1.93. Specifically, 99.2% of WVI was removed within 1 h by E. coli cells at pH 1.93. However, above pH 4.63, WVI was not removed by E. coli cells. Figure 2a shows the recovery ratio of WVI as a function of the pH after 4 h at pH values of 1.08−7.11. As shown in Figure 2a, the recovery of WVI increased as the solution pH decreased 14443

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Figure 3. FTIR spectra of E. coli before and after WVI adsorption.

Figure 4. Time course of WVI on the bacteria surface based on TEM analysis (a) before adsorption and after (b) 3 min, (c) 30 min, and (d) 420 min and (e) mapping analysis of E. coli cells at 3 min.

Figure 3. In the spectra of the WVI-adsorbed cells, there is a substantial decrease in the absorption intensities of carboxyl and phosphate groups, suggesting interactions of W with carboxyl and phosphate groups (COOH and PO43−). At lower pH, the function of COOH on the surface of bacteria might be changed to COOH+. Thus, the ζ potential and FTIR analysis indicate that it is possible that adsorption of WVI by E. coli occurs because of an electrical interaction between the bacterial surface (E. coli−COOH+) and WVI anion. TEM Mapping Analysis. The time course of the adsorption of aqueous WVI by E. coli was monitored using TEM imaging (Figure 4a−d) and mapping analysis (Figure 4e). This experiment was conducted at 22.6 °C and pH 1.80 using 0.90 × 109 cells/mL resting cells of E. coli. The TEM image indicated that E. coli cells were intact, even at low pH. In the early stage of adsorption, the contrast of the bacteria sample in the image (Figure 4b) was almost the same as that before sorption (Figure 4a). However, the contrast was gradually enhanced as the operating time increased (Figure 4c,d), indicating an increase in adsorbed WVI concentration on the bacteria surface. To confirm the WVI adsorption, mapping

analysis was conducted for the bacterial sample after 3 min of operating time. As shown in Figure 4e, this sample exhibited W signals along with signals from C, O, and P. The peaks of C, O, and P likely arose from proteins and enzymes present in the bacterial cells. These results demonstrate that WVI ions are homogeneously adsorbed on the E. coli cells, even when there was a very short operating time. Equilibrium Study of W Adsorption. An equilibrium study of WVI adsorption using E. coli cells was performed by investigating the effects of various initial WVI concentrations (0.10−7.00 mmol/L) at different temperatures (22.6−53.0 °C). Cell concentrations were maintained at (0.63−4.7) × 109 cells/mL. Table 1 shows the WVI adsorption results as a function of the initial WVI concentration and temperature at pH values of 1.80−2.52 after 7 h. When the temperature increased from 22.6 to 53.0 °C, the sorption capacity for WVI ions at 0.80 mmol/L increased from 0.86 to 1.36 mmol/g, while the sorption capacity for WVI at 22.6 °C increased from 0.86 to 1.28 mmol/g for 0.80 and 4.00 mmol/L solutions. The effects of the temperature on biosorption were significant at all initial WVI concentrations. 14444

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(0.01 mmol/g),19 ZnII (0.65 mmol/g),29 and CdII (0.49 mmol/ g).29 Thermodynamic Study of W Adsorption. The thermodynamic parameters were calculated using the Langmuir isotherm by replacing the equilibrium constant, KC0 , from eqs 5 and 6, with the Langmuir isotherm constant, b (L/mol). The results are provided in Table 3. Negative values of ΔG0 indicate the feasibility of the process and the spontaneous nature of sorption with a high affinity for WVI by E. coli cells. The standard enthalpy and changes in entropy of the biosorption obtained from a ln KC0 versus 1/T plot were 58.4 kJ/mol and 218.3 J/(mol/K), respectively. The positive value of ΔH0 confirms the endothermic nature of the process. The entropy value, ΔS0, was also positive, suggesting that the affinity of the metal ion for the sorbent could be enhanced by increasing the operating temperature. Kinetic Study of W Adsorption. The values of the rate constants are presented in Table 4 along with the correlation coefficients. The correlation coefficients for the pseudo-firstorder kinetic model at various temperatures were found to be lower than 0.937. In addition, the equilibrium uptake (qe,cal) values calculated from the pseudo-first-order kinetic model did not agree well with the experimental (qe,exp) values. The second-order rate constant, k2 [g/(mmol/min)], also decreased with increasing solution temperature for all of the WVI ion concentrations studied, and the correlation coefficient, r2, for the pseudo-second-order rate equation was greater than 0.992. The theoretical equilibrium uptake (qe,cal) values agreed well with the experimental (qe,exp) data in the case of the pseudosecond-order kinetic model. Taken together, these findings indicated that this sorption system was better described by a second-order than a first-order rate equation. Recovery of W from Dilute Solutions. The ability of E. coli to adsorb WVI from very dilute Na2WO4 solutions was evaluated. In this experiment, the initial bacterial cell concentration was kept constant at 2.0 × 109 cells/mL. As shown in Figure 6, decreasing the WVI concentration resulted in increased recovery fractions of WVI. Specifically, almost 100% of WVI was removed from 0.10 mmol/L aqueous Na2WO4 solutions within 10 min. These results confirmed that the biorecovery system using E. coli cells was effective for the recovery of WVI at very low concentrations. Recovery of W from E. coli. Figure 7 shows the desorption behavior of WVI from the E. coli cells using NaOH at 23.0 °C. In this experiment, E. coli cells adsorbing 0.40 mmol/L of WVI were used for the desorption test. When the pH of the WVIadsorbed bacterial suspension was adjusted to 4.92, 7.81, and

Table 1. WVI Adsorption Results as a Function of the Initial WVI Concentration and Temperature after 7 h WVI ion uptake capacity [mmol/g] VI

initial W ion concentration [mmol/L] 0.80 1.00 2.00 3.00 4.00

22.6 °C 32.2 °C 39.7 °C 0.86 0.86 1.04 1.18 1.28

0.99 1.00 1.21 1.22 1.27

1.12 1.17 1.29 1.35 1.27

53.0 °C 1.36 1.47 1.69 1.63 1.50

The Langmuir and Freundlich adsorption isotherms for the sorption of WVI by E. coli obtained at temperatures of 22.6, 32.2, 39.7, and 53.0 °C are shown in Figure 5. The Langmuir and Freundlich adsorption constants determined from the isotherms at different temperatures, along with the correlation coefficients, are presented in Table 2. Higher correlation coefficients (r2) were obtained for the Langmuir isotherms than the Freundlich isotherms at all investigated temperatures. These findings clearly show that Langmuir isotherm models provide a better fit for the sorption of WVI by E. coli in the investigated concentration range. The value of the maximum sorption capacity, Qmax, for WVI was higher at 53.0 °C than at other temperatures. The adsorption capacity of the biosorbent was found to increase with increasing temperature (from 1.28 to 1.65 mmol/g), indicating that the process is endothermic. The maximum sorption capacity of E. coli (=1.65 mmol/g) was higher than that of Bacillus sp. MGG-8318 (=0.356 mmol/ g) reported in previous studies,18 which was likely due to differences in the cell wall structure. Indeed, the cell wall structure plays an important role in the biosorption of metal ions. Specifically, Gram-positive bacteria such as Bacillus sp. MGG-8318 normally show lower levels of surface complexation because of the heavily cross-linked peptidoglycan layer, while Gram-negative bacteria such as E. coli have a greater metal binding capacity because their lipopolysaccharide, phospholipids, and proteins are exposed on the cell surface.27 Additionally, our results are in agreement with those of Tsuruta, who reported that some Gram-negative bacteria (Erwinia herbicola, Pseudomonas aeruginosa, and Pseudomonas maltophilia) have a better ability to adsorb gold from aqueous solutions than Gram-positive bacteria.28 When compared with previous studies of maximum biosorption capacities, Qmax, for various metal ions by E. coli, the biosorption capacity for WVI was higher than those for AsΙΙΙ

Figure 5. Adsorption isotherm model of the biosorption of WVI using E. coli based on measurements at temperatures of 22.6, 32.2, 39.7, and 53.0 °C: (a) Langmuir isotherm model; (b) Freundlich isotherm model. 14445

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Table 2. Langmuir and Freundlich Adsorption Constants Evaluated from the Isotherms at Different Temperatures Langmuir constants

Freundlich constants

T [°C]

Qmax [mmol/g]

b [L/mg]

r2

K [(mmol/g)(mmol/L)n]

n

r2

23.6 32.2 39.7 53.0

1.28 1.29 1.30 1.65

13.2 21.2 55.7 111.0

0.997 0.997 0.998 0.999

187.1 973.3 601.5 1067.0

3.9 31.4 9.5 15.3

0.580 0.815 0.771 0.983

Table 3. Thermodynamic Parameters for the Biosorption of WVI Using E. coli T [°C]

KC0 [L/mmol]

ΔG0[kJ/mol]

ΔH0[kJ/mol]

ΔS0[J/(mol/K)]

22.6 32.2 39.7 53.0

13.2 21.2 55.7 111.3

−6.3 −7.8 −10.5 −12.8

58.4

218.3

8.83 by the addition of NaOH, the WVI concentrations rapidly increased to 0.04, 0.39, and 0.38 mmol/L, respectively. The desorption ratios, defined as the ratio of the mass of WVI desorbed to that present on the biomass before desorption, were 95.8% and 91.8% for the samples at pH 7.81 and 8.83, respectively. These results implied the possibility of regeneration of E. coli cells for biosorption of WVI. To prepare WVI concentrates, the WVI-adsorbed bacteria were dried at 120 °C for 4 h. The concentration of WVI in the dried sample, which was calculated from the amount of WVI removed per unit of dried biomass, was approximately 49.2% (w/w), or 535 times the concentration of WVI in the initial solution (9.91 × 10−4 w/w). A heating process was also used to prepare WVI concentrates. WVI-adsorbed bacterial samples were heated at 1000 °C for 2 h in a furnace under atmospheric conditions. After heating, a solid condensate containing 77.0% WVI (WVI/solid condensate) was obtained, which was 837 times the initial concentration of the WVI solution. Figure 8 shows the XRD results for the WVI-adsorbed bacteria after heating. WO3 (JCPDS 71-0131) peaks were found in the XRD patterns of the powder samples. Reevaluation of the WVI concentrates revealed that the solid condensate contained 97.1% WO3 (WO3/solid condensate). Overall, these findings suggest that the WVI recycling system can produce a relatively high concentration of WO3. Figure 9 shows the W recycling process using the ionexchange method and biosorption recycling process proposed in this study for hard materials (WC). When compared with the currently used method, our suggested WVI recycling system has the potential to provide a shorter and ecofriendly process, although other factors such as selectivity of the metal ions need to be further investigated.

Figure 6. Time course of soluble WVI concentration during the biosorption experiment using 2.0 × 109 cells/mL resting cells of E. coli at different initial WVI concentrations: (•) 0.1 mmol/L (pH 1.81), (■) 0.5 mmol/L (pH 1.84), and (○ and □) sterile controls without E. coli at pH 1.79 and 1.81, respectively.

Figure 7. Desorption of WVI from E. coli at different pH values: (•) pH 4.92, (▲) pH 7.81, (■) pH 8.83, and (○) sterile controls without E. coli. Initial WVI concentration: 0.4 mmol/L. Cell concentration: 2.6 × 109 cells/mL.

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CONCLUSIONS This work presents the results of an investigation of W removal from aqueous solution by biosorption using E. coli cells. The effects of the solution pH, initial W concentration, cell concentration, and operating temperature on the adsorption performance were investigated both experimentally and

Table 4. Values of the Rate Constants for the Biosorption of WVI Using E. coli pseudo-first-order kinetic model

pseudo-second-order kinetic model

T [°C]

qe,exp [mmol/g]

qe,cal [mmol/g]

k1 × 102 [min−1]

r2

qe,cal [mmol/g]

k2 [g/(mmol/min)]

h [mmol/(g/min)]

r2

22.6 32.2 39.7 53.0

0.86 0.99 1.12 1.36

0.63 0.48 0.21 0.20

0.81 1.75 0.79 1.23

0.937 0.753 0.448 0.631

0.88 1.00 1.12 1.36

0.04 0.16 0.29 0.44

0.03 0.16 0.36 0.82

0.992 1.000 0.999 1.000

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ASSOCIATED CONTENT

S Supporting Information *

Plasma instrumental conditions, ICP experiments, and time course of soluble WVI concentration. This material is available free of charge via the Internet at http://pubs.acs.org.

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AUTHOR INFORMATION

Corresponding Author

*Tel: +81-82-424-7850. Fax: +81-82-424-7850. E-mail: ogit@ hiroshima-u.ac.jp. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This research was supported by a Grant-in-Aid for Young Scientists (B) (Grant 23760729) sponsored by the Ministry of Education, Culture, Sports, Science and Technology of Japan and the Steel Foundation for Environmental Protection Technology. The authors also thank Dr. E. Tanabe from the Hiroshima Prefectural Institute of Industrial Science and Technology for help with TEM and chemical mapping analyses.

Figure 8. XRD analysis of WVI-adsorbed bacteria after heating at 1000 °C for 2 h.

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Figure 9. Comparison of the metal biotechnology and currently used methods for W recycling.

NOTATION Qmax (mmol/g): maximum amount of metal ions adsorbed per unit weight of E. coli cells Ce (mg/L): Langmuir constant b (L/mg): Langmuir constant K [(mmol/g)(mmol/L)n]: Freundlich constant n: Freundlich constant ΔG0 (kJ/mol): Gibbs free energy R [J/(mol/K)]: universal gas constant, 8.314 J/(mol/K) T (K): absolute solution temperature KC0 (L/mmol): equilibrium constant ΔS0 [J/(mol/K)]: entropy change of biosorption ΔH0 (J/mol): enthalpy change of biosorption qe (mmol/g): amount of WVI adsorbed on the sorbent at equilibrium qt (mmol/g): amount of WVI adsorbed on the sorbent at time t k1 (min−1): rate constant of pseudo-first-order biosorption k2 [g/(mmol/min)]: rate constant of pseudo-second-order biosorption REFERENCES

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