Activated Carbon Cloth as Anode for Sulfate Removal in a Microbial

Environ. Sci. Technol. 2008, 42, 4971–4976

Activated Carbon Cloth as Anode for Sulfate Removal in a Microbial Fuel Cell FENG ZHAO,† NELLI RAHUNEN,‡ JOHN R. VARCOE,† AMREESH CHANDRA,† CLAUDIO AVIGNONE-ROSSA,‡ ALFRED E. THUMSER,‡ AND R O B E R T C . T . S L A D E * ,† Chemical Sciences, Biological Sciences, University of Surrey, Guildford, GU2 7XH, United Kingdom

Received February 6, 2008. Revised manuscript received April 2, 2008. Accepted April 9, 2008.

By employing the sulfate-reducing bacterium Desulfovibrio desulfuricans we demonstrate the possibility of electricity generation in a microbial fuel cell (MFC) with concomitant sulfate removal. This approach is based on an in situ anodic oxidative depletion of sulfide produced by D. desulfuricans. Three different electrode materials, graphite foil (GF), carbon fiber veil (CFV), and high surface area activated carbon cloth (ACC), were evaluated for sulfide electrochemical oxidation. In comparison to CFV and GF electrodes, ACC was a superior materialforsulfideadsorptionandoxidationandshowedsignificant potential for harvesting energy from sulfate-rich solutions in the form of electricity. Sulfate (3.03 g dm-3) was removed from a bacterial suspension, which represented 99% removal. A maximum power density of 0.51 mW cm-2 (normalized to geometric electrode area) was obtained with a one-chamber, airbreathing cathode and continuous flow MFC operated in batch mode at 22 °C.

Introduction Sulfate-rich wastewaters are generated by many processes: they are present in waste streams from animal husbandry, mining, food processing, the pharmaceutical industry, pulp and paper wastewater, etc (1). Numerous adverse effects from pollution by sulfur compounds are already known: (a) they affect the aquatic ecosystem by increased acidity; (b) the odors of wastewaters are commonly from generation of sulfur compounds when sulfate-reducing bacteria use sulfate as a terminal electron acceptor for respirations (2, 3); and (c) such gaseous sulfur-based compounds raise serious health risks and can be corrosive to metals and concrete. For these reasons, a large amount of effort and expense has been undertaken to treat sulfate-rich wastewater. Biological sulfate reduction has been recognized as an efficient method (4); however, the main problem related to this process is due to generation of sulfide that inhibits bacterial growth, decreases the rate of sulfate reduction, and causes physical or biological constraints that may lead to process failure (5). The lack of development of a low-cost, high-efficiency desulfurization process remains the principal barrier for treatment of sulfaterich wastewaters. * Corresponding author phone: +44 1483 682588; fax: +44 1483 686851; e-mail: [email protected]. † Chemical Sciences. ‡ Biological Sciences. 10.1021/es8003766 CCC: $40.75

Published on Web 06/03/2008

 2008 American Chemical Society

Utilizing microbial metabolism to produce an electrical current from the degradation of organic/inorganic matter provides an elegant solution for simultaneous wastewater treatment and electricity generation; these systems are termed microbial fuel cells (MFCs) and represent a clean and renewable energy resource. To date little research effort has been reported regarding development of MFCs for sulfate removal from wastewater treatment: Habermann et al. (6) reported a MFC where the sulfate was biologically reduced to sulfide, which was then catalytically oxidized to sulfate on a metal hydroxide-modified graphite anode; Cooney et al. (7) utilized the same anodic reaction mechanism (see following) for electricity generation in a MFC where charcoal was used as the anode D . desulfuricans...

anode

sulfate 98 sulfide 98 sulfate

(1)

Rabaey et al. (8, 9) developed a MFC that used graphitic granule anode and ferricyanide for the cathodic reaction, where a different anodic oxidation mechanism was reported compared with earlier work (6, 7), and involved removal of sulfate (8) and sulfide (9) from wastewater with solid sulfur deposition on the anode Paracoccus...

Paracoccus... + anode

sulfate 98 sulfide 98 sulfur

(2)

Applications of MFCs are currently limited because of low power densities generated. Utilization of higher surface area electrode materials appears to be a general trend for achieving increased power output (10). Activated carbon is notable as an odor adsorbent for wastewater treatment applications (11, 12). Adsorptive removal (13) and catalytic oxidation of hydrogen sulfide (14, 15) have also been successfully demonstrated with activated carbon cloth (ACC), which has the advantage of having a high specific surface area, mechanical integrity, and ease of handling. To the best of our knowledge, there has been no reported use of ACC as a MFC anode. In this study, three different carbon-based materials, ACC, carbon fiber veil (CFV), and graphite foil (GF), were evaluated for in situ electrochemical sulfide oxidation. The sulfatereducing bacterium D. desulfuricans was used as biocatalyst for sulfate reduction in solution. A one-chamber, airbreathing cathode and continuous flow MFC was designed for obtaining high power output and achieving highly efficient sulfate removal.

Experimental Section Anode Materials. Two different activated carbon cloths (ACCs), denoted as CTEX-20 and CTEX-27, were obtained from MAST Carbon Advanced Products Ltd. U.K. Graphite foil (GF) is commercially available from SGL Technologies GmbH, Germany. Carbon fiber veil (CFV) was supplied by Technical Fiber Products Limited, U.K. Electrode Preparation. ACC, CFV, and GF were cut to size for use as the working electrodes with titanium wires (Advent, 0.5 mm thick) inserted as the terminal. The reference electrode was a Ag/AgCl type (BASi, 3.0 mol dm-3 NaCl, +0.196 V versus standard hydrogen electrode at 25 °C). If not mentioned otherwise, all potentials reported were converted to the SHE reference scale. Platinum wire or CFV served as counter electrode in a standard electrochemical threeelectrode chamber. VOL. 42, NO. 13, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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For fuel cell testing, the CTEX-20 ACC was used as the anode and long titanium wires were knitted into the ACC to improve electrical conductivity and provide the connection terminal (Figure S1, Supporting Information). The cathode for oxygen reduction was made from an assembly consisting of an ELAT electrode (E-Tek division of BASF) and Nafion115 proton exchange membrane (PEM, DuPont). Nafion was pretreated with sequential boiling in aqueous H2O2 (6% V/V), H2O, H2SO4 (0.5 mmol dm-3), and H2O and then stored in deionized water before being hot pressed to the ELAT electrode. ELAT is a carbon cloth electrode with 0.5 mg cm-2 geometric loading on one side using 20% mass Pt on Vulcan XC-72 carbon black and PTFE binder. The ELAT electrode was coated with Nafion ionomer (Aldrich, 5% mass dispersions in an alcohol/water mixed solvent) and dried in air to a constant Nafion mass loading of 0.5 mg cm-2 (16, 17) as is standard for traditional H2/air PEM fuel cells. The airbreathing cathode was fabricated by pressing the ELAT electrode to the Nafion-115 PEM with 120 kg cm-2 force at 135 °C for 3 min. The electrode assembly was stored in deionized water until use. Microbial Cultures. D. desulfuricans strain Essex 6 (DSM 642) was purchased from the DSMZ (German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany). D. desulfuricans was grown anaerobically at 22 °C in a medium containing Na2SO4 (4.5 g dm-3), MgSO4 · 7H2O (0.06 g dm-3), FeSO4 · 7H2O (0.004 g dm-3), KH2PO4 (0.5 g dm-3), NH4Cl (1.0 g dm-3), CaCl2 · 6H2O (0.06 g dm-3), sodium lactate (6.0 g dm-3), yeast extract (1.0 g dm-3), sodium citrate (0.3 g dm-3), resazurin (0.001 g dm-3), sodium thioglycolate (0.1 g dm-3), and ascorbic acid (0.1 g dm-3). The pH of fresh medium in a half-filled serum bottle was adjusted to 7.5 with NaOH (aq, 2 mol dm-3), and the headspace was completely replaced by nitrogen prior to autoclaving at 121 °C for 15 min. The same medium served as electrolyte solution in potentiostatic tests and as artificial wastewater in batch mode MFC experiments. Ion Chromatography. A Dionex DX-100 ion chromatograph with a ED 40 electrochemical detector was used to determine the concentration of sulfate ions in the phosphate buffer and culture medium (filtered using a syringe filter of pore size 0.45 µm prior to the test). The eluent was Na2CO3 (3.5 mmol dm-3) and NaHCO3 (1 mmol dm-3) aqueous buffer solution. Energy-Dispersive X-ray. An EDX detector on a Hitachi S2300 SEM was used for elemental analysis of electrodes. After the batch mode operation the electrodes were rinsed with deionized water and stored at 30 °C for 48 h before analysis. Electrochemical Measurements. Potentiostatic experiments were carried out in a sealed three-electrode chamber using a computer-controlled Autolab potentiostat/galvanostat (EcoChemie, Netherlands). The culture medium and phosphate buffer (50 mmol dm-3, pH 7.5) were used as the electrolyte under anaerobic conditions. The concentrations of sulfide in the solutions were detected using a previously reported electrochemical method (18, 19) with the ACC or CFV working electrode held at 0.40 V with current recording. For long-term and multicycle operation, the elemental sulfur on the ACC surface was dissolved in chloroform for anode regeneration. The ohmic internal resistance of the MFCs was determined (16, 20) by electrochemical impedance spectroscopy using a Solartron Analytical 1260 frequency response analyzer operating in conjunction with a Solartron Analytical 1287 potentiostat/galvanostat in the frequency range from 1 MHz to 10 Hz and with a potential perturbation signal of 10 mV rms. Microbial Fuel Cell Construction and Operation. A onechamber, air-breathing cathode, continuous flow-type MFC, 4972

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FIGURE 1. Schematic of the laboratory-scale prototype one-chamber, air-breathing cathode, continuous flow MFC. was constructed in Perspex as shown in Figure 1. The volume of liquid in the chamber was 18 cm3. The ACC anode with a projected geometric size of 1.5 cm2 was located at the end of the chamber, and the distance between the anode and the air-breathing cathode (1.5 cm2) was set between 3 and 5 mm. A Ag/AgCl reference electrode was used to record the individual electrode potentials to analyze the MFC performances. This MFC configuration was developed taking into account both the electrochemical and the biological requirements (21–24) and the desired simultaneous high-power outputs; it represents an elegant solution that allows for investigation of electrode performance and bacterial evolution. For fuel cell operation (Figure S2), 1 cm3 of D. desulfuricans culture was inoculated into 100 cm3 of fresh medium in a serum bottle for 4 days at 22 °C for sulfide accumulation in order to obtain high power output; the culture was then recycled throughout the MFC chamber, which was purged with N2 prior to the experiment. Current and potential measurements (24) were carried out in a continuous flow batch mode using a digital multimeter (Integra 2700 series equipped with 7700 multiplexer, Keithley Instruments, Inc., Cleveland, OH) interfaced to a personal computer for data collection. For determination of the power output curve a variable resistance box (10 kΩ to 1 Ω) was used as the external load. In this study the second tests of potential and current curve were recorded and analyzed; the current density and power generation density were normalized to the geometric electrode area of electrode (the anode and the cathode are of the same size). All electrochemical experiments and MFC operations were carried out at 22 ( 0.5 °C unless mentioned otherwise.

Results and Discussions Evaluation of the Electrodes in Bacteria-Free Phosphate Buffer. In previous related MFC studies (6–8), bacteria reduced sulfate to sulfide with subsequent oxidation on the surface of anodes to yield the electricity; the consensus is that when the anode is capable of efficiently oxidizing sulfide at room temperature, it can provide a high MFC power output. To evaluate different anode materials for sulfide oxidation at neutral pH, potentiostatic investigations were undertaken

TABLE 1. Analysis of Sulfide Electrochemical Oxidation Productsa before experiment

experiment 1 2 3

FIGURE 2. Current-time plots of (a) ACC, (b) CFV, and (c) GF placed in stirred bacteria-free phosphate buffer (50 mmol dm-3, pH 7.5). The electrodes (1 cm2) were potentiostatically held at a potential of 0.20 V versus Ag/AgCl, and sulfide was added in the buffer at 180 s. at a constant potential (0.20 V versus Ag/AgCl). The electrolyte was bacteria-free phosphate buffer (50 mmol dm-3, pH 7.5) in a sealed three-electrode chamber, and sulfide was added to the buffer during the measurements. In the absence of sulfide, all electrodes (ACC, CFV, and GF) showed similar performances for the first 3 min as shown in Figure 2. After 180 s, sulfide (3.0 mmol dm-3) was added to the electrolyte and the following results were observed. (i) All currents instantaneously increased, and maximum stable current densities of 2.66 (ACC), 0.35 (CFV), and 0.13 mA cm-2(GF) were obtained. The ACC produced the highest current density that was a factor of 7.6 higher when compared to the CFV and a factor of 20 compared to the GF. (ii) The current produced by the electrodes was dependent on the concentration of sulfide in the buffer (data not shown), and stirring the solution increased the current density, which indicates that oxidation of sulfide was a diffusion-controlled process. These studies demonstrated that ACC anode is a superior material for sulfide oxidation. In contrast, CFV yielded an inferior performance, and the GF electrode exhibited slow electrode kinetics for sulfide oxidation. The long-term capability of ACC toward sulfide oxidation was also investigated (Figures S3 and S4, Supporting Information). When 3.0 mmol dm-3 sulfide was initially added to the stirred phosphate buffer, the current instantaneously increased from microampere level to a maximum of 2.7 mA, stabilized about 800 s, and then declined by the decreased concentration of sulfide to approximate 0.01 mA after 5 h. At 20 h, 3.3 mmol dm-3 sulfide was added to the same solution and a maximum current density of 2.1 mA cm-2 was achieved. Sulfide, in principle, can be simultaneously oxidized to elemental sulfur and/or polysulfide species (Sn2-, n ) 2-5; these polysulfides are unstable and can react with sulfur to form other species) in neutral solution because equilibrium potentials for these processes are close (25, 26); further oxidation, in parallel or consecutively, can then occur depending on the prevailing experimental conditions (e.g., sulfate can be generated on increased anode potential). These results (Figure S3, Supporting Information) indicate that the ACC’s capability for sulfide oxidation was decreased, possibly by deposition of elemental sulfur, one of the oxidation products of sulfide, on the electrode surface. When sulfide was added for a third time to the solution at 36 h (in total 9.3 mmol dm-3 sulfide was added in the whole experiment, equivalent to 0.893 g dm-3 sulfate), the 1 cm2 ACC still achieved a maximum current of 1.0 mA (3 times higher than the 0.35 mA observed using the CFV electrode with only 3.0 mmol dm-3 sulfide addition). Moreover, after removing the sulfur from ACC (6 cycles, Figure S4, Supporting Information), it reached 1.6 mA cm-2, a high anode current density,

sulfide (mmol dm-3)

after experiment

sulfate (mmol dm-3)

sulfide (mmol dm-3)

sulfate (mmol dm-3)

reaction time (h)

31.69 31.69

n.d. n.d. n.d.

0.32 ( 0.16 0.78 ( 0.13 0.03 ( 0.02

18 140 140

15.0

a n.d. ) not detected. Experiment 1: Initial sulfide concentration was 15.0 mmol dm-3 in the bacteria-free buffer. Experiment 2: Initially 4.5 g dm-3 Na2SO4 (31.69 mmol dm-3 sulfate) was present in the D. desulfuricans culture. Experiment 3: Same conditions as experiment 2 except that 0.4 g of sodium lactate was added to 100 cm3 of culture medium at 120 h.

demonstrating superior performance of ACC for sulfide oxidation for long-term operation. When bacterial communities are used to treat wastewater, sulfate (sulfide, etc.) may be produced by bacterial sulfur oxidation or disproportionation. In this study, no sulfate anions and no bacterial cells were added to the buffer during these potentiostatic experiments so that the anodic oxidation product of sulfide could be easily detected and analyzed (discussed in Table 1 above). Evaluation of the Electrodes in Medium. The electrodes (ACC and CFV) were evaluated for their ability of in situ oxidation of sulfide produced by D. desulfuricans at 22 °C. Figure 3a presents the potentiostatic results using CFV as the working electrode; the electrolyte was fresh medium that was pumped to a sealed chamber and then inoculated with 1 cm3 D. desulfuricans culture. After a lag time (approximately 38 h) electricity generation was observed. The current increase was dependent on the sulfide concentration, which was concomitant with the exponential growth of the D. desulfuricans population in the culture, i.e., the current reached a maximum when the rate of the biologically formed sulfide reached a maximum at 68 h, which was followed by a decline in electricity generation due to exhaustion of substrate and/ or sulfate. The performance of ACC for in situ oxidation of sulfide in medium was also investigated (Figure 3b). The process of bacterial cultivation was different from that of CFV (see the caption of Figure 3). The current generation behavior with the ACC electrode was similar to that with the CFV electrode (Figure 3a) but with increased current generation (1.30 mA maximum with CFV and 5.16 mA for ACC); the current of the ACC electrode dependent on sulfide concentration was observed immediately (no lag time), i.e., there was no possibility of direct electron transfer because the residence time of the bacterium in the system is too short for bacterial cells to attach to the ACC surface (if this is at all possible), the anode electrons were from sulfide oxidation in this case. Further experiments may help to elucidate if other mechanisms of electron transfer between bacteria and ACC are operating. These studies demonstrated that the ACC exhibited higher efficiency in situ sulfide oxidation in medium when compared to CFV; the rate of bacterial metabolism was limiting since the current densities obtained with both anode types were lower than those obtained with bacteria-free phosphate buffer, i.e., the rate of sulfate reduction by D. desulfuricans at 22 °C is the limiting step as both electrode materials did not reach their oxidation capability. Analysis of Sulfide Oxidation Products. After batch experiments (Figure 3b), the ACC electrode was removed VOL. 42, NO. 13, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

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FIGURE 4. Proposed pathways of sulfate removal in MFC. Reactions 1 and 2 are biological metabolism-based reactions; reactions 3 and 4 are chemical in nature.

FIGURE 3. Current generation in batch potentiostatic operation. The electrodes were held at a potential of 0.20 V vs Ag/AgCl. (a) CFV electrode (30 cm2) was placed into 100 cm3 of medium inoculated with 1 cm3 of D. desulfuricans culture in a sealed three-electrode chamber. (b) A 1 cm3 amount of D. desulfuricans inoculum was added to 100 cm3 of fresh medium in a sealed serum bottle, and after 2 days the culture was anaerobically pumped to the three-electrode chamber containing ACC electrode (20 cm2). from the chamber and rinsed with deionized water to eliminate any sulfate species on the ACC surface for EDX analysis. Only elemental carbon was detected in the pretest ACC electrode (Figure S5a, Supporting Information), indicating that the starting ACC was sulfur free, whereas elemental sulfur was observed on the post-test electrode surfaces where the sulfide had been oxidized to solid sulfur (Figure S5b, Supporting Information). In order to detect the presence of other reaction products, ion chromatography was used to measure the sulfate concentration in the bacteria-free phosphate buffer and bacterial solutions after operation. The ACC electrode was held at a constant potential of 0.20 V versus Ag/AgCl and an initial 15.0 mmol dm-3 sulfide was present in the phosphate buffer at the start of the experiment; the current was monitored until it decreased to the background level (microampere magnitude), i.e., no detective sulfide remained in the solution. In experiment 1 (Table 1) 0.3 mmol dm-3 sulfate was produced by sulfide oxidization, which represented a conversion of 2% (approximately 9% sulfide was oxidized to sulfite and thiosulfate; data not shown). Sulfide can be oxidized to elemental sulfur when the anode potential is g-0.27 V in aqueous solution at neutral pH (25), but consecutive electrochemical oxidation of sulfide to sulfate (sulfite or thiosulfate, etc.) requires a high positive overpotential (26) even though thermodynamics predicts that sulfide can be consecutively oxidized, e.g., solid sulfur deposition 4974

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FIGURE 5. Cell potential curve (O) and power curves (9) of a one-chamber continuous flow MFC using ACC as the anode and an air-breathing cathode in batch operation. Variation bars indicate two tests with different fuel cells. is unavoidable even when the potentials of the electrodes were higher than 0.8 V (19, 27). Experiments 2 and 3 (Table 1) show the changes of sulfate ion concentration in the bacterial solution: 3.04 g dm-3 sulfate was added to D. desulfuricans cultures as the electron acceptor, and 2.97 and 3.03 g dm-3 sulfate were removed from the solution after sulfide oxidation. Figure 4 presents a schematic of the possible pathways for sulfate removal in MFCs labeled reactions 1-4. Sulfate ions can be taken up through the cell membrane of D. desulfuricans as shown in reaction 1, and after several enzymatically catalyzed reduction steps in the cytoplasm (28, 29), sulfide is released into solution where it is adsorbed and oxidized to elemental sulfur and soluble polysulfides at the anode (reaction 3). Reaction 4 is highly dependent on the anode potential. In this study, a small quantity of sulfide was oxidized to sulfate (experiment 1 data in Table 1), which was again reduced to sulfide by D. desulfuricans; therefore, a high level of sulfate was removed from the bacterial solution in experiments 2 and 3. These results suggest that elemental sulfur and/or soluble polysulfide species are the dominant oxidation products in the anode chamber. MFC Power Test. Figure 5 shows the performance curves for the MFC under different external loads (ohmic resistances) in batch mode but with continuous flow of culture medium through the anode chamber. A maximum current density of 2.2 mA cm-2 was obtained with the MFC configuration shown in Figure 1, and a peak power density of 0.51 mW cm-2 was obtained at a current density of 1.3 mA cm-2. This power density is comparable with the highest values for MFCs (0.585 mW cm-2) reported by Rosenbaum et al. (30), in which biohydrogen mainly served as the electron carrier in the anode compartment. It certainly needs to be noted that the MFC conditions (temperature, nature of substrate, and concentrations affects) discussed in the current study was

not optimized for providing the highest possible performance. For instance, the optimum temperature for D. desulfuricans growth is 34-37 °C (2), where bacterial population would allow a faster sulfide production rate compared to the rate observed at room temperature. Thus, a higher power output is obtainable if a MFC was operated at these temperatures since sulfate reduction was the limiting step in the reaction pathway. The ohmic internal resistances of the two MFC were 27 and 38 ohm measured as the high-frequency resistance in impedance spectroscopic data, with an anode-cathode distance in the range 3-5 mm. A high-efficiency anode and “sandwich” configuration membrane electrode assembly yields a high-performance MFC; moreover, the “sandwich” structure of the anode, membrane, and cathode assembly is suitable for removal of bacterially generated sulfide, where the high-efficiency anode and close distance between anode and PEM avoids H2S diffusion into the PEM. This would result in reduction of proton transfer (reducing the ionic conductivity of PEM) on formation of solid sulfur on the surface and/or inside the polymer electrolyte membrane (sulfide chemically oxidized by oxygen diffusion into the PEM from the air cathode). For future work, non-noble metal catalysts, i.e., porphyrins and phthalocyanines (21, 24), will be tested since they are not as affected by sulfide and have the potential for allowing long operational lifetime compared to expensive Pt catalyst. The in situ oxidation of sulfide, the microbial product of sulfate metabolism, in an MFC anode chamber has high potential for sulfate removal from wastewaters compared to traditional methods, where sulfate bioreduction pathways were inhibited by the sulfide end product, the accumulation of which led to an almost complete loss of bacterial sulfate reduction activity (5). The direct electrochemical depletion of microbially synthesized sulfide in solution enhances rates of sulfate bioreduction, i.e., reduction of sulfide concentration leads to an increase in the rate of sulfate reduction according to the change of molar ratio between reaction and production species. An efficient anode will enhance the oxidation of the sulfide produced in the biological sulfate reducing reaction. Additionally, corrosion and odor problems are alleviated by the decrease in sulfide concentration, and the process allows partial recovery of solid and nontoxic elemental sulfur as a bonus. A MFC that uses a high surface area ACC-type anode allows for the in situ depletion of the microbially generated sulfide and represents a solution to renewable electricity production with simultaneous sulfate-rich waste treatment.

Acknowledgments This research was supported by the U.K.’s Engineering and Physical Sciences Research Council as part of the Supergen 5 Biological Fuel Cells Consortium programme (EP/D047943/ 1). The authors thank Dr. Daniel Driscoll for assistance in ion chromatography, Mr. Paul Leahy for fuel cell construction, and MAST Carbon for provision of ACC samples.

Supporting Information Available Schematic of the anode and MFC configuration used in a batch mode; anode regenerative performance over long-term operation; EDX spectra of ACC anode. This information is available free of charge via the Internet at http://pubs.acs.org.

Literature Cited (1) Lens, P. N. L.; Hulshoff Pol, L. Environmental technologies to treat sulfur pollution. principles and engineering. IWA, London, 2000. (2) Widdel, F.; Pfennig, N. Dissimilatory sulfate- or sulfur-reducing bacteria. In Bergey’s manual of systematic bacteriology, Krieg, N. R., Holt, J. G., Eds.; The Williams & Wilkins: Baltimore, 1984.

(3) Stuetz, R. M.; Fenner, R. A.; Engin, G. Assessment of odours from sewage treatment works by an electronic nose, H2S analysis and olfactometry. Water Res. 1999, 33, 453–461. (4) Lens, P. N. L.; Visser, A.; Janssen, A. J. H.; Hulshoff Pol, L. W.; Lettinga, G. Biotechnological treatment of sulfate-rich wastewaters. Crit. Rev. Environ. Sci. Technol. 1998, 28, 41–88. (5) Hulshoff Pol, L. W.; Lens, P. N. L.; Stams, A. J. M.; Lettinga, G. Anaerobic treatment of sulfate-rich wastewaters. Biodegradation 1998, 9, 213–224. (6) Habermann, W.; Pommer, E.-H. Biological fuel cells with sulphide storage capacity. Appl. Microbiol. Biotechnol. 1991, 35, 128–133. (7) Cooney, M. J.; Roschi, E. Marison, I. W.; Comninellis, Ch.; Stockar, U. Physiological studies with the sulfate-reducing bacterium Desulfibrio desulfuricans: evaluation for use in a bio-fuel cell. Enzyme Microb. Technol. 1996, 18, 358–365. (8) Rabaey, K.; Clauwaert, P.; Aelterman, P.; Verstraete, W. Tubular microbial fuel cells for efficient electricity generation. Environ. Sci. Technol. 2005, 39, 8077–8082. (9) Rabaey, K.; Sompel, K. V.; Maignien, L.; Boon, N.; Aelterman, P.; Clauwaert, P.; Schamphelaire, L. D.; Pham, H. T.; Vermeulen, J.; Verhaege, M.; Lens, P.; Verstraete, W. Microbial fuel cells for sulfide removal. Environ. Sci. Technol. 2006, 40, 5218–5224. (10) Logan, B.; Cheng, S.; Watson, V.; Estadt, G. Graphite fiber brush anodes for increased power production in air-cathode microbial fuel cells. Environ. Sci. Technol. 2007, 41, 3341–3346. (11) Martin, R. J. Activated carbon product selection for water and wastewater treatment. Ind. Eng. Chem. Prod. Res. Dev. 1980, 19, 435–441. (12) Primavera, A.; Trovarelli, A.; Andreussi, P.; Dolcetti, G. The effect of water in the low-temperature catalytic oxidation of hydrogen sulfide to sulfur over activated carbon. Appl. Catal. A: Gen. 1998, 173, 185–192. (13) Gardner, T. H.; Berry, D. A.; Lyons, K. D.; Beer, S. K.; Freed, A. D. Fuel processor integrated H2S catalytic partial oxidation technology for sulfur removal in fuel cell power plants. Fuel 2002, 81, 2157–2166. (14) Le Leuch, L. M.; Subrenat, A.; Le Cloirec, P. Hydrogen sulfide adsorption and oxidation onto activated carbon cloths: applications to odorous gaseous emission treatments. Langmuir 2003, 19, 10869–10877. (15) Boudou, J. P.; Chehimi, M.; Broniek, E.; Siemieniewska, T.; Bimer, J. Adsorption of H2S or SO2 on an activated carbon cloth modified by ammonia treatment. Carbon 2003, 41, 1999–2007. (16) Varcoe, J. R.; Slade, R. C. T.; Wright, G. L.; Chen, Y. Steady-state dc and impedance investigations of H2/O2 alkaline membrane fuel cells with commercial Pt/C, Ag/C, and Au/C Cathodes. J. Phys. Chem. B 2006, 110, 21041–21049. (17) Litster, S.; McLean, G. PEM fuel cell electrodes. J. Power Source 2004, 130, 61–76. (18) Lawrence, J.; Robinson, K. L.; Lawrence, N. S. Electrochemical determination of sulfide at various carbon substrates: a comparative study. Anal. Sci. 2007, 23, 673–676. (19) Wang, Y.; Yan, H.; Wang, E. The electrochemical oxidation and the quantitative determination of hydrogen sulfide on a solid polymer electrolyte based system. J. Electroanal. Chem. 2001, 497, 163–167. (20) Zhao, F.; Wu, X.; Wang, M.; Liu, Y.; Gao, L.; Dong, S. The electrochemical and bioelectrochemical properties of room temperature ionic liquids and carbon composite materials. Anal. Chem. 2004, 76, 4960–4967. (21) Zhao, F.; Harnisch, F.; Schro¨der, U.; Scholz, F.; Bogdanoff, P.; Herrmann, I. Challenges and constraints of using oxygen cathodes in microbial fuel cells. Environ. Sci. Technol. 2006, 40, 5193–5199. (22) Liu, H.; Logan, B. Electricity generation using an air-cathode single chamber microbial fuel cell in the presence and absence of a proton exchange membrane. Environ. Sci. Technol. 2004, 38, 4040–4046. (23) He, Z.; Minteer, S.; Angenent, L. T. Electricity generation from artificial wastewater using an upflow microbial fuel cell. Environ. Sci. Technol. 2005, 39, 5262–5267. (24) Zhao, F.; Harnisch, F.; Schro¨der, U.; Scholz, F.; Bogdanoff, P.; Herrmann, I. Application of pyrolysed iron(II) phthalocyanine and CoTMPP based oxygen reduction catalysts as cathode materials in microbial fuel cells. Electrochem. Commun. 2005, 7, 1405–1410. (25) Pourbaix, M. Atlas of electrochemical equilibria in aqueous solutions; Pergamon Press: Oxford, NY, 1966. (26) Zhdanov, S. I. Encyclopaedia of electrochemistry of the elements; Marcel Dekker: New York, 1975; Vol. 4, Chapter IV-6. VOL. 42, NO. 13, 2008 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

9

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(27) Mohtadi, R.; Lee, W.-K.; Cowan, S.; Van Zee, J. W.; Murthy, M. Effects of hydrogen sulfide on the performance of a PEMFC. Electrochem. Solid State Lett. 2003, 6, A272–274. (28) Shen, Y.; Buick, R. The antiquity of microbial sulfate reduction. Earth Sci. Rev. 2004, 64, 243–272. (29) Mangalo, M.; Meckenstock, R. U.; Stichler, W.; Einsiedl, F. Stable isotope fractionation during bacterial sulfate reduction is

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controlled by reoxidation of intermediates. Geochim. Cosmochim. Acta 2007, 71, 4161–4171. (30) Rosenbaum, M.; Zhao, F.; Schro¨der, U.; Scholz, F. Interfacing electrocatalysis and biocatalysis with tungsten carbide: a highperformance, noble-metal-free microbial fuel cell. Angew. Chem. 2006, 118, 6810–6813.

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