Effect of Set Potential on Hexavalent Chromium Reduction and

ARTICLE pubs.acs.org/est

Effect of Set Potential on Hexavalent Chromium Reduction and Electricity Generation from Biocathode Microbial Fuel Cells Liping Huang,†,* Xiaolei Chai,† Guohua Chen,†,‡ and Bruce E Logan§ †

Key Laboratory of Industrial Ecology and Environmental Engineering, Ministry of Education (MOE), School of Environmental Science and Technology, Dalian University of Technology, Dalian 116024, China ‡ Department of Chemical and Biomolecular Engineering, Kowloon, Hong Kong University of Science and Technology, Hong Kong, China § Department of Civil and Environmental Engineering, The Pennsylvania State University, University Park, Pennsylvania 16802, United States

bS Supporting Information ABSTRACT: Setting a biocathode potential at
300 mV improved the subsequent performance of an MFC for Cr(VI) reduction compared to a control (no set potential). With this set potential, the startup time was reduced to 19 days, the reduction of Cr(VI) was improved to 19.7 mg/L d, and the maximum power density was increased to 6.4 W/m3 compared to the control (26 days, 14.0 mg/L d and 4.1 W/m3). Set potentials of
150 mV and
300 mV also improved system performance and led to similarly higher utilization of metabolic energy gained (PMEG) than set potentials of þ200 mV and
450 mV. We observed putative pili at
150 and
300 mV potentials, and aggregated precipitates on bacterial surfaces in both poised and nonpoised controls. These tests show that there are optimal potentials that can be set for developing a Cr(VI) biocathode.

’ INTRODUCTION A microbial fuel cell (MFC) is a device that extracts energy from wastes and wastewaters through biocatalytic reactions.1 Biocathode MFCs, which utilize electrochemically active microorganisms on both the cathode and anode as catalysts, have attracted much attention and are holding great promise for bioremediation and waste treatment as they are self-regenerating and sustainable.2
4 Aerobic biocathode MFCs have been investigated to avoid the need for a metal catalyst on the cathode,5
9 but other reactions at the cathode can accomplish reductive removal of contaminants or the production of value-added products. The range of biocathode applications has therefore expanded to include reduction of pollutants such as NO3
, chloroethenes, 2-chlorophenol, ClO4
, U(VI), Cr(VI)10
16 and CO2,17 and reduction for the value-added product of methane.18,19 Improvements in the performance of anaerobic biocathode systems are needed to increase the current densities and rates of chemical reduction in these systems. Setting electrode potentials is a useful approach for controlling the performance of a bioelectrochemical system.20 Either electrode potential can be set in an MFC or a microbial electrolysis cell (MEC). The main difference is that the overall reaction is not spontaneous in an MEC without this energy input. Only one of the MFC electrode potentials can be controlled, and thus the potential of the other electrode can vary to maintain current required for the reaction at the set electrode potential. The system being examined here is an MFC because the current flow is spontaneous in the absence of the added energy. Setting the r 2011 American Chemical Society

anode potential has been shown to promote enrichment of the biofilm and reduce the startup time of the system, and to increase the subsequent power density due to better acclimation of the exoelectrogenic bacteria.20
25 Relatively fewer studies have been conducted with set cathode potentials,5,8 and bacterial growth on the cathode is not yet well studied.4 Optimized biocathode potentials of 242 mV and 345 mV have been shown to reduce the time for startup and enhance the performance of aerobic biocathode,5,8 but there are no studies on set cathode potentials in the absence of oxygen. Setting the biocathode potential should improve system performance for anaerobic cathodes in a way similar to that achieved for bioanodes. Cr(VI) is a priority toxic chemical present in wastewaters from electroplating, pigment, and lumber and wood product processes. Anaerobic biocathodes MFCs have been used to achieve reduction of Cr(VI) to much less toxic Cr(III) with simultaneous electricity generation, providing a promising application for the reductive treatment of oxidized Cr(VI) to precipitated Cr(OH)3.15,26 Biocathode performance in terms of startup time, Cr(VI) reduction rate as well as electricity production need to be improved. In this study, we investigated the effect of different set biocathode potentials on anaerobic Cr(VI) reduction. Several different potentials (
450,
300,
150 and þ200 mV vs a standard hydrogen Received: November 18, 2010 Accepted: April 25, 2011 Revised: March 15, 2011 Published: April 29, 2011 5025

dx.doi.org/10.1021/es103875d | Environ. Sci. Technol. 2011, 45, 5025–5031

Environmental Science & Technology

ARTICLE

electrode, SHE) were chosen to improve startup time compared to a control MFCs operated only at a fixed external resistance of 200 Ω. Performance was evaluated in terms of Cr(VI) reduction rate, power production, growth yields, and biocatalytic activities. These results provide for the first time a approach for improving the performance of anaerobic biocathodes using Cr(VI) as a terminal electron acceptor.

’ MATERIALS AND METHODS MFC Configuration. A tubular two-chamber reactor was used based on the design of Clauwaert et al.13 A detailed description of the MFC structure is available in the Supporting Information (SI). Graphite granules (Sanye Co., Beijing, China) were used for the cathode and a graphite brush was used for the anode.27 The net working volumes were 85 mL for the cathode chamber and 43 mL for the anode chamber. Before installation, these materials were cleaned as previously described.13 A reference electrode (Ag/AgCl electrode, 195 mV versus SHE) was used to obtain cathode and anode potentials. All reactors were wrapped in aluminum foil to exclude light. Inoculation and Operation. The cathode was inoculated using primary clarifier effluent from Lingshui wastewater treatment plant (Dalian, China). The cathode medium (pH 7.0) consisted of (g/L): KH2PO4, 4.4; K2HPO4, 3.4; NaHCO3, 1.0; NH4Cl, 1.3; KCl, 0.78; MgCl2, 0.2; CaCl2, 0.0146; NaCl, 0.5; and 1.0 mL of trace elements.13 The bioanode was developed in a separate MFC (originally inoculated using wastewater) that was operated for 3 months with acetate as the electron donor. The medium used for the anode was the same as the cathode, except NaHCO3 was replaced by 1.0 g/L of acetate. Five sets of MFCs were operated at set cathode potentials of
450 mV (P
450),
300 mV (P
300),
150 mV (P
150), 200 mV (Pþ200) (vs SHE) and at a fixed resistance of 200 Ω (R200) (triplicate reactors). During the startup period and during each cycle, samples were periodically withdrawn and analyzed for soluble Cr(VI). At the end of certain cycles, biomass production and maximum power density were also analyzed. After each cycle, new medium containing 20 mg/L of Cr(VI), prepared by dissolving analytical grade K2Cr2O7, was added to the cathode chamber. Anodic solution was periodically refreshed (once every two days) in order to keep the stable potential of
0.27 ( 0.04 V in the anode chamber. In order to compare the performances of reactors set at potentials and MFC condition (no set potential), reactors started up at a set potential of
300 mV were switched to a fixed resistance of 200 Ω (MFC mode) on several different days (3, 9, 13, and 19, and at the end of the acclimation period) and examined for maximum power production by obtaining polarization curves, and for individual electrode potentials. All tests were conducted at 22 ( 3 °C. Analyses. The cathode, anode and reference electrode (vs SHE) were connected to the three-electrode system of a potentiostat (Leici, Shanghai, China) which was used to set a cathode potential. The current was monitored by a data logger (Leici, Shanghai, China). The cathode and anode were working and counter electrodes, respectively, with an Ag/AgCl reference electrode in the cathode. All potentials shown here were corrected to SHE. The method for calculating power density is provided in SI. Polarization data was obtained by feeding the reactors, leaving them in open circuit mode for 2 h, and then running linear sweep voltammetry (LSV) at a scan rate of

Figure 1. Current output during startup period under different cathodic set potentials (A:
300 mV (O), no bacterial catalyst control ()); B:
150 mV (4), C: þ200 mV (0)).

0.1 mV/s. The bioelectrochemical behavior of cathodic biofilms was examined using cyclic voltammetry (CV) and a three electrodes configuration with a potentiostat (CHI 650A, Chenhua, Shanghai). The potential was scanned between
0.5 and þ0.5 V (vs SHE) at a scan rate of 10 mV/s, with data recorded to a personal computer connected to the potentiostat. Methods for the analysis of residual soluble Cr(VI), soluble Cr(III), precipitated Cr(III) (Cr(OH)3), biomass and hydrogen gas in the cathode chamber is described in the SI. Biofilm morphology and precipitates on the biocathode were examined using a scanning electron microscope coupled with energy dispersive spectrometer (SEMEDS, Hitachi 450, Japan). Prior to observation, the electrodes was collected and fixed overnight with 2% (v/v) paraformaldehyde and 2% (v/v) glutaraldehyde in 0.1 M cacodylate buffer (pH 7.5, 4 °C), followed by washing and dehydration in water/ethanol solutions. Samples were then coated with Au/Pt before SEM observation.

’ RESULTS AND DISCUSSION Effect of Set Potential on Startup Times. Biocathodes at set potentials ranging from
300 to þ200 mV produced currents ranging from 0.17 mA to 0.87 mA, compared to 0.03
0.05 mA for the abiotic controls during startup. In the initial period during startup (Figure 1A, cycle 1, days 0 to 5), the reactor at a set potential of
300 mV produced a maximum current of 0.23 mA, compared to 0.17 mA at
150 mV and 0.10 mA at þ200 mV (Figure 1B). After 9 cycles, the current output increased to 0.87 mA (day 21) at
300 mV and to 0.74 mA at
150 mV, and these currents were repeatable over the subsequent cycles. These results illustrate that the cathode potential had a significant effect on the biocathode startup time and current. A set potential of
300 mV resulted in the shortest startup time with the highest current output. A much lower current of 0.15 mA was produced at a positive set potential of þ200 mV over 28 days acclimation period (Figure 1C). The ability of microorganisms to perform electron transfer in MFCs is considered to be a fortuitous consequence of their capacity for other forms of extracellular electron transfer because electrodes are not natural electron acceptors or donors.28 An 5026

dx.doi.org/10.1021/es103875d |Environ. Sci. Technol. 2011, 45, 5025–5031

Environmental Science & Technology

Figure 2. Cr(VI) reduction as a function of acclimation time (A and B), voltage output (C and D) and power density (E and F) as a function of current density, and electrode potentials (G) with (A, C, E, and G) or without (B, D, F, and G) a set potential of
300 mV.

optimal set potential can provide an appropriate selective pressure for adaptation of microorganisms.5,24,28 This selective and evolutionary pressure can lead to the enhancement of the ability of microorganisms for electrochemical interaction with electrodes as well as improved current production, which is associated with clear differences in the properties of the outer surfaces of the cells.28 Therefore, the present results also indicate an adaptive evolution of the biofilm that was facilitated by setting the right potential of the biocathode system. This result was similar to that observed with adaptive evolution for enhanced current production in a bioanode system.25 Cr(VI) Reduction and Maximum Power Densities during Startup. During startup (Figure 2A), the rate of Cr(VI) reduction at a set potential of
300 mV increased from a change of 13.0 mg/L within 4.8 days (2.7 mg/L d) in the first cycle, to a complete removal within 1.0 day (19.7 mg/L d) in cycle 8 (day 19) (Figure 2A). After cycle 8, the removal rate of Cr(VI) was unchanged. In the control (Figure 2B, external resistor of 200 Ω), the Cr(VI) reduction rate (10.0 mg/L d) (cycle 8, day 19) continued to increase over time to 14.0 mg/L d on day 26 (cycle 11). Soluble Cr(III) was undetectable and the produced Cr(III) was mainly present as precipitated Cr(OH)3 on the cathode electrode. By use of a mass balance between two cycles and under a MFC conditions, the recovery of precipitated Cr(OH)3 on the cathode reached around 94 ( 8% whereas

ARTICLE

nearly 96 ( 3% soluble Cr(VI) was still present in catholyte under an open circuit condition, indicating that a maximum of around 4% Cr(VI) was removed through bioadsorption. Thus the primary method for Cr removal was biochemical reduction. The evolution of maximum power obtained from polarization data using LSV in both set (
300 mV) (Figure 2C and E) and nonset potential MFCs (Figure 2D and F) clearly shows a gradual increase in power production with time. During the first 19 days, the open circuit potential in the set potential MFCs increased from 0.35 V (day 3) to 0.55 V (day 13) (Figure 2C), while the control ranged from 0.20 to 0.42 V over the same period (Figure 2D). Further acclimation did not increase the open circuit potential (Figure 2C). The maximum power by the set potential reactors also gradually increased from 2.0 W/m3 (8.8 A/m3, day 3) to 6.4 W/m3 (21 A/m3, day 19) (Figure 2E), compared to the control (3.2 W/m3 at 13 A/m3, day 19) (Figure 2F). Increasing the acclimation time (day 26 to 33) of the control slightly increased the power from 4.1 W/m3 to 4.7 W/m3, with no further increase after 40 days (Figure 2F). These results show that setting a cathode potential of
300 mV not only increased Cr(VI) reduction rate but also improved subsequent power generation. The improvement in the set potential reactors over time can be seen to be due to the changes in the electrode potentials. A higher cathode potential was produced with the reactors set at
300 mV compared to the other potentials and the fixed resistance MFC (Figure 2G). Anode potentials for both the set potential reactors and the fixed resistance systems were constant in all the cases, demonstrating that the current generation was improved by changes in the cathode. Effect of Set Potentials on Steady State Performance. Following the startup period, the reactors set at
150 mV and
300 mV produced similar results despite differences in performance during startup (SI Figure S-1A). The reactor set at
150 mV removed 19.8 ( 0.5 mg/L of Cr(VI) within 24 h, similar to that of the reactor set at
300 mV (20.2 ( 1.0 mg/L). These removals are better than that of the control, R200 (14.0 ( 0.7 mg/L), and the reactors set at
450 mV (11.9 ( 0.5 mg/L) and at þ200 mV (8.6 ( 0.3 mg/L) (SI Figure S-1A). The maximum power produced by the MFCs also varied depending on the conditions used to startup the reactors (SI Figure S-1B and S-1C). The MFC originally at a set potential of
300 mV produced the highest open circuit potential of 0.55 V and maximum power density of 6.4 W/m3 (21 A/m3), which was close to that produced by the MFC originally operated at
150 mV (0.59 V, and 5.9 W/m3). In contrast, the MFC acclimated at þ200 mV produced an open circuit potential of 0.2 V and a maximum power generation of 0.3 W/m3 (2.6 A/m3). The internal resistance of the MFC originally set at þ200 mV was 243 Ω, compared to only 146 Ω for the P
300 MFC, implying that a set potential of
300 mV stimulated the formation of a more electrochemically active biofilm. Hydrogen was undetectable in the present headspaces of reactors in all tests. Cathode set potentials were less than that theoretically needed for hydrogen evolution under standard conditions (
414 mV). We cannot completely discount the formation of trace amounts of hydrogen gas at the most negative potentials (
300 mV and
450 mV), but certainly there was no hydrogen gas production at
150 mV. The lack of hydrogen production in this study is consistent with abiotic tests (a set potential of
300 mV or
500 mV) by others,16,29
31 and tests at set potentials ranging from
300 mV to
500 mV 5027

dx.doi.org/10.1021/es103875d |Environ. Sci. Technol. 2011, 45, 5025–5031

Environmental Science & Technology with microorganisms.4,16,29
33 For these reasons, the reduction of Cr(VI) was attributed to microorganisms directly accepting electrons from the electrode surface and transferring them to Cr(VI), and not through the use of evolved hydrogen gas. Energy can be conserved to support growth from direct electron transfer from electrodes.4,16 Evaluation of the growth yields possible from electron transfer from electrodes has not yet reported and is a high research priority.4,16 In the case of the present system at a pH of 7.0 and a Cr(VI) concentration of 20 mg/L, Cr(VI) reduction theoretically can occur at a potential of 350 mV. The difference between this thermodynamic potential and the set potential represents the maximum potential to be gained by the cathodic microorganisms. The lower the controlled cathode potential, the more energy cathodic microorganisms will potentially obtain and the quicker microorganisms could grow.5,8 On the other hand, under a selective pressure of a set potential, microbial consortia have a capability of self-regulation permitting the potential of their operative terminal reductases (in case of bioanode) or oxidases (in case of biocathode) reaching a value that is only slightly more reducing/oxidizing than the potential applied to the electrode.22,24 If the potential applied is set too high (in the case of bioanode) or low (in the case of biocathode) and it goes beyond the self-regulation capability of microbial consortia, then the possible energy gain by the cathodic microorganisms will be lost. When cathodes in this study were set at potentials of
150 and
300 mV, theoretical maximum potentials of 500 and 650 mV were available, which was higher than the value of 150 mV obtained at a higher controlled potential of 200 mV, indicating potentially more energy gained by the cathodic microorganisms. However, a set potential of
450 mV may have exceeded the self-regulation capability of the microbial consortia and had no positive effect on power generation and Cr(VI) reduction, although its theoretical maximum potential of 800 mV was high. An optimal set potential of 242 mV with a higher electrochemical activity than the 142 and 342 mV was also observed with biocathodes using O2 as an electron acceptor whereas set potentials of 442 and 542 mV could not even start up the biocathodes.5 Therefore it is presumably the present set potential of
450 mV has led to a lower bacterial activity than the
150 and
300 mV. This was further illustrated by a slower microbial growth as well as a lower possible metabolic energy gained for bacteria growth at the set potential of
450 mV in the following section. Thus, the theoretical maximum potentials of 500 and 650 mV at set potentials of
150 and
300 mV may have provided microbial consortia the best situations for gaining more energy, resulting in quicker growth of electrochemically activity bacteria on the cathode and higher current output and improved Cr(VI) reduction rates. Further illustration of relationship between bacterial activity and set potential was supported by the analysis of biomass and possible metabolic energy gained for bacteria growth described in the following section. Biomass Production and the Possible Metabolic Energy Gained for Bacteria Growth under Different Cathode Potentials. Biomass gradually increased over time for each startup condition in a manner dependent on the set potential (Figure 3A). The reactor set at
300 mV produced the highest biomass, as expected from its better performance compared to the others. The P
150 reactor also had good biomass development compared to the control MFC (R200) and reactors set at potentials of þ200 mV and
450 mV. Biofilm density is important relative to the electrode potential. For exoelectrogenic anode biofilms, higher power production

ARTICLE

Figure 3. Biomass production time profiles (A) and biomass production as a function of the possible metabolic energy gained for the bacteria (B) in MFCs operated at different cathode potentials (0: Pþ200, 4: P
150, O: P
300,  : P
450) or a fixed external resistance of 200 Ω ()) during startup period.

was observed from thicker anodic biofilms of Geobacter sulfurreducens.4 For aerobic biocathodes, a certain thickness of biofilm on both graphite plate and stainless steel mesh was helpful in enhancing power output.34 Thus set potentials of
150 and
300 mV in the present study may favor of the formation of a biofilm of optimal thickness for higher power generation. The effect of set potential on biomass can be traced back to the biocathodic electron transfer process, in which electrons from cathode electrode are received by terminal electron acceptors via the direct or indirect transfer and catalysis of microorganisms on the electrode. An applied cathode potential can induce a selective pressure for microorganisms that utilize electron acceptors with a redox potential was slightly more positive than that of the applied potential10,16,22 because these microorganisms may conserve the greatest energy with simultaneous cathode oxidation and reduction of terminal electron acceptors.4 In the case of biocathode using Cr(VI) as a terminal electron acceptor, if the potential energy difference between cathode and microbial electron acceptors is decreased, then the rate of the electrode oxidation reaction will decrease and limit the Cr(VI) reduction rate. Conversely, if the potential energy difference between cathode and microbial electron acceptors is increased, the amount of potential energy provided for microbial utilization decreases. Thus there is a critical potential beyond which bacteria can no longer perform electron transfer efficiently and therefore negatively affect system performance.35 As seen here, potentials of þ200 mV and
450 mV did not improve bacterial growth, while
150 and
300 mV benefited to bacterial growth. Anodic bacteria can obtain metabolic energy by regulating microbial electron donors to the anode potential through an electron transport component with the redox potential compliant with the anode potential.25 Similar to anodic processes, bacteria on the cathode can also obtain metabolic energy by accepting electrons from the cathode and then transferring them to their terminal electron acceptors.4,5 When using microbial consortia, several respiratory pathways may be available, making the community more efficient for maximizing energy recovery at 5028

dx.doi.org/10.1021/es103875d |Environ. Sci. Technol. 2011, 45, 5025–5031

Environmental Science & Technology

ARTICLE

Figure 4. SEM images of bacteria on the cathode poised at
300 mV (A) or acclimated at an external resistance of 200 Ω (R200) (B), and EDS spectra of the bacterial surface precipitates (C) and bare electrode parts (D) with or without set potentials.

different cathode potentials.4 A lower cathode potential makes it more beneficial to the bacteria and thus more metabolic energy may be available for bacterial growth. The possible metabolic energy gained (PMEG) during this process can be calculated in a manner similar to that used for the anode25 as X PMEG ¼ ðE0 acceptor
Ecathode Þ  Q ð1Þ E0acceptor = 0.35 V is the standard potential of electron acceptor (Cr(VI), pH = 7.0)15, Ecathode the set potential (V), and Q(C) the current multiplied by time t(s). Using this relationship, the PMEG was calculated for the different reactors as shown in Figure 3B. Biomass increased with the PMEG, with similar changes noted for the P
150, P
300, and R200 reactors (slope value of 0.31, R2 = 0.91, p = 0.0001, n = 16), whereas the Pþ200 and P
450 had lower slopes of 0.12 (R2 = 0.93, p = 0.03, n = 4) and 0.19 (R2 = 0.95, p = 0.03, n = 4), respectively. These results show that conditions set for the P
150, P
300, and R200 reactors produced similar yields of biomass, and that cathode potentials of 200 mV and
450 mV led to lower utilization rates. Effect of Set Potential on Bacterial Catalysis Activities. Cyclic voltammograms (CVs) were used to understand the effect of the different set potentials on the catalytic activities of the biofilms (SI Figure S-2). The positions of oxidation
reduction peaks indicate redox potential of electron transfer components of the bacteria, while the size of oxidation
reduction peaks reveals electrochemical activity of a biofilm.6 Similar reduction peaks at
0.07 V were observed for the P
300, P
150, and R200 reactors, whereas oxidation peaks increased to 0.14 V for the

R
200 reactor and to 0.23 V for the P
300 reactor. No significant redox peaks were observed in abiotic controls. This shows that the electron transfer capabilities of the biofilms were improved by setting the potentials at
150 mV and
300 mV (SI Figure S-2). Bacteria Morphologies on the Electrode. SEM analysis on the P
150 and P
300 reactors at the end of potentiostatic experiments to examine the morphology of the bacteria on the cathode. The bacteria appeared to be connected with putative pili, and there were noticeable precipitates on the bacterial surfaces (Figure 4A). In the R200 control, no pili like structures were observed although precipitates were also observed (Figure 4B), implying a positive effect of
150 mV and
300 mV on the formation of pili. Precipitates in the biofilm matrix suggest that Cr(VI) reduction occurs outside the cells. Using EDS to examine the composition of the precipitates, Cr signals were detected on the precipitates of both set potential electrodes and the control (Figure 4C) but not on the bare surface of the electrodes (Figure 4D). This illustrates that Cr(VI) reduction was mainly occurring on bacterial surfaces. To achieve chromium removal it may be necessary to use a clarifier (settling) to remove biomass from the cathode. Separation of formed precipitated Cr(III) from the bacteria will also be an issue for practical applications. Outlook. These studies have shown that setting the cathode potential is a viable method for improving biocathode performance for Cr(VI) reduction. The optimum set potential here was
300 mV on the basis of decreased startup time, improved power generation, and higher Cr(VI) reduction rates, compared to control reactors and three other set potentials although this optimal cathode potential may not be extended to other studies 5029

dx.doi.org/10.1021/es103875d |Environ. Sci. Technol. 2011, 45, 5025–5031

Environmental Science & Technology due to the different culture conditions, electrode materials, and inoculum.20 Biological reduction was consistent with the observation of precipitates with a Cr signal on the bacteria and not on the electrode surface. The formation of microbial nanowires on anodes has been found to be needed for maximum power production,36 and their presence is associated with enhancement of current production to anodes at set potentials in both pure and mixed culture reactors.28,37 While it was still unclear if the observed pili was electrically conductive and therefore could be considered to be nanowires, the presence of putative pili observed in the best performing systems (at set potentials of
150 mV and
300 mV) suggested that they are also needed for optimal biocathode performance. Electron transfer from cathode surface to microorganisms is likely a rate limiting step in current production, and thus more work needs to be done to clarify the role of these putative pili in biocathode systems.

’ ASSOCIATED CONTENT

bS

Supporting Information. Reactor structure, power density calculation, biomass and chromium as well as hydrogen analysis methods. This material is available free of charge via the Internet at http://pubs.acs.org.

’ AUTHOR INFORMATION Corresponding Author

*Phone: 86 411 84708546; e-mail: [email protected].

’ ACKNOWLEDGMENT We gratefully acknowledge financial support from the Natural Science Foundation of China (No. 21077017), Program for Changjiang Scholars and Innovative Research Team in University (IRT0813), “Energy þ X” (2008) key programme through Dalian University of Technology, and the support of the King Abdullah University of Science and Technology (KAUST) (Award KUS-I1-003-13). ’ REFERENCES (1) Logan, B. E.; Regan, J. M. Microbial fuel cells: challenges and applications. Environ. Sci. Technol. 2006, 40, 5172–5180. (2) He, Z.; Angenent, L. T. Application of bacterial biocathodes in microbial fuel cells. Electroanalysis 2006, 18, 2009–2015. (3) Huang, L. P.; Regan, J. M.; Quan, X. Electron transfer mechanisms, new applications, and performance of biocathode microbial fuel cells. Biores. Technol. 2011, 102, 316–323. (4) Lovley, D. R. Powering microbes with electricity: direct electron transfer from electrodes to microbes. Environ. Microbiol. Rep. 2011, doi: 10.1111/j.1758-2229.2010.00211.x (5) Liang, P.; Fan, M. Z.; Cao, X. X.; Huang, X. Evaluation of applied cathode potential to enhance biocathode in microbial fuel cells. J. Chem. Technol. Biotechnol. 2009, 84, 794–799. (6) Rabaey, K.; Read, S. T.; Clauwaert, P.; Freguia, S.; Bond, P. L.; Blackall, L. L.; Keller, J. Cathodic oxygen reduction catalyzed by bacteria in microbial fuel cells. ISME J. 2008, 2, 519–527. (7) Rosenbaum, M.; He, Z.; Angenent, L. T. Light energy to bioelectricity: photosynthetic microbial fuel cells. Curr. Opin. Biotechnol. 2010, 21, 259–264. (8) Ter Heijne, A.; Strik, D.P.B.T.B.; Hamelers, H. V. M.; Buisman, C. J. N. Cathode potential and mass transfer determine performance of oxygen reducing biocathodes in microbial fuel cells. Environ. Sci. Technol. 2010, 44, 7151–7156.

ARTICLE

(9) You, S. J.; Ren, N. Q.; Zhao, Q. L.; Wang, J. Y.; Yang, F. L. Power generation and electrochemical analysis of biocathode microbial fuel cell using graphite fiber brush as cathode material. Fuel Cells 2009, 9, 588–596. (10) Aulenta, F.; Canosa, A.; Reale, P.; Rossetti, S.; Panero, S.; Majone, M. Microbial reductive dechlorination of trichloroethene to ethene with electrodes serving as electron donors without the external addition of redox mediators. Biotechnol. Bioeng. 2009, 103, 85–91. (11) Butler, C. S.; Clauwaert, P.; Green, S. J.; Verstraete, W.; Nerenberg, R. Bioelectrochemical perchlorate reduction in a microbial fuel cell. Environ. Sci. Technol. 2010, 44, 4685–4691. (12) Clauwaert, P.; Van der Ha, D.; Boon, N.; Verbeken, K.; Verhaege, M.; Rabaey, K.; Verstraete, W. Open air biocathode enables effective electricity generation with microbial fuel cells. Environ. Sci. Technol. 2007, 41, 7564–7569. (13) Clauwaert, P.; Rabaey, K.; Aelterman, P.; Schamphelaire, L. D.; Pham, T. H.; Boeckx, P.; Boon, N.; Verstraete, W. Biological denitrification in microbial fuel cells. Environ. Sci. Technol. 2007, 41, 3354–3360. (14) Huang, L. P.; Cheng S. A.; Chen, G. H. Bioelectrochemical systems for efficient recalcitrant wastes treatment. J. Chem. Technol. Biotechnol. 2010, DOI: 10.1002/jctb.2551. (15) Tandukar, M.; Huber, S. J.; Onodera, T.; Pavlostathis, S. G. Biological chromium(VI) reduction in the cathode of a microbial fuel cell. Environ. Sci. Technol. 2009, 43, 8159–8165. (16) Strycharz, S. M.; Gannon, S. M.; Boles, A. R.; Franks, A. E.; Nevin, K. P.; Lovley, D. R. Reductive dechlorination of 2-chlorophenol by Anaeromyxobacter dehalogenans with an electrode serving as the electron donor. Environ. Microbiol. Reports 2010, 2, 289–294. (17) Cao, X. X.; Huang, X.; Liang, P.; Boon, N.; Fan, M. Z.; Zhang, L.; Zhang, X. A completely anoxic microbial fuel cell using a photobiocathode for cathodic carbon dioxide reduction. Energy Environ. Sci. 2009, 2, 498–501. (18) Cheng, S. A.; Xing, D. F.; Call, D. F.; Logan, B. E. Direct biological conversion of electrical current into methane by electromethanogenesis. Environ. Sci. Technol. 2009, 43, 3953–3958. (19) Villano, M.; Aulenta, F.; Ciucci, C.; Ferri, T.; Giuliano, A.; Majone, M. Bioelectrochemical reduction of CO2 to CH4 via direct and indirect extracellular electron transfer by a hydrogenophilic methanogenic culture. Biores. Technol. 2010, 101, 3085–3090. (20) Wagner, R. C.; Call, D. I.; Logan, B. E. Optimal set anode potentials vary in bioelectrochemical systems. Environ. Sci. Technol. 2010, 44, 6036–6041. (21) Busalmen, J. P.; Esteve-nunez, A.; Feliu, J. M. Whole cell electrochemistry of electricity-producing microorganisms evidence an adaptation for optimal exocellular electron transport. Environ. Sci. Technol. 2008, 42, 2445–2450. (22) Finkelstein, D. A.; Tender, L. M.; Zeikus, J. G. Effect of electrode potential on electrode-reducing microbiota. Environ. Sci. Technol. 2006, 40, 6990–6995. (23) Srikanth, S.; Mohan, S. V.; Sarma, P. N. Positive anodic poised potential regulates microbial fuel cell performance with the function of open and closed circuitry. Biores. Technol. 2010, 101, 5337–5344. (24) Wang, X.; Feng, Y. J.; Ren, N. Q.; Wang, H. M.; Lee, H.; Li, N.; Zhao, Q. L. Accelerated start-up of two-chambered microbial fuel cells: effect of anodic positive poised potential. Electrochim. Acta 2009, 54, 1109–1114. (25) Wei, J. C.; Liang, P.; Cao, X. X.; Huang, X. A new insight into potential regulation on growth and power generation of Geobacter sulfurreducens in microbial fuel cells based on energy viewpoint. Environ. Sci. Technol. 2010, 44, 3187–3191. (26) Huang, L. P.; Chen, J. W.; Quan, X.; Yang, F. L. Enhancement of hexavalent chromium reduction and electricity production from a biocathode microbial fuel cell. Bioprocess Biosyst. Eng. 2010, 33, 937–945. (27) Logan, B. E.; Cheng, S. A.; 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. (28) Yi, H. N.; Nevin, K. P.; Kim, B. C.; Franks, A. E.; Klimes, A.; Tender, L. M.; Lovley, D. R. Selection of a variant of Geobacter 5030

dx.doi.org/10.1021/es103875d |Environ. Sci. Technol. 2011, 45, 5025–5031

Environmental Science & Technology

ARTICLE

sulfurreducens with enhanced capacity for current production in microbial fuel cells. Biosens. Bioelectron. 2009, 24, 3498–3503. (29) Gregory, K. B.; Bond, D. R.; Lovley, D. R. Graphite electrodes as electron donors for anaerobic respiration. Environ. Microbiol. 2004, 6, 596–604. (30) Strycharz, S. M.; Woodard, T. L.; Johnson, J. P.; Nevin, K. P.; Sanford, R. A.; Frank, E.; L€offler, F. E.; Lovley, D. R. Graphite electrode as a sole electron donor for reductive dechlorination of tetrachlorethene by Geobacter lovleyi. Appl. Environ. Microbiol. 2008, 74, 5943–5947. (31) Aulenta, F.; Reale, P.; Catervi, A.; Panero, S; Majone, M. Kinetics of trichloroethene dechlorination and methane formation by a mixed anaerobic culture in a bio-electrochemical system. Electrochim. Acta 2008, 53, 5300–5305. (32) Rabaey, K.; Rozendal, R. A. Microbial electrosynthesis-revisiting the electrical route for microbial production. Nat. Rev. Microbiol. 2010, 8, 706–716. (33) Nevin, K. P.; Hensley, S. A.; Franks, A. E.; Summers, Z. M.; Ou, J.; Woodard, T. L.; Snoeyenbos-West O. L.; Lovley, D. R. Electrosynthesis of organic compounds from carbon dioxide catalyzed by a diversity of acetogenic microorganisms. Appl. Environ. Microbiol. 2011, DOI: 10. 1128/AEM.02642-10 (34) Behera, M.; Jana, P. S.; Ghangrekar, M. M. Performance evaluation of low cost microbial fuel cell fabricated using earthen pot with biotic and abiotic cathode. Biores. Technol. 2010, 101, 1183–1189. (35) Cheng, K. Y.; Ho, G.; Cord-Ruwisch, R. Affinity of microbial fuel cell biofilm for the anodic potential. Environ. Sci. Technol. 2008, 42, 3828–3834. (36) Reguera, G.; Nevin, K. P.; Nicoll, J. S.; Covalla, S. F.; Woodard, T. L.; Lovley, D. R. Biofilm and nanowire production leads to increased current in Geobacter sulfurreducens fuel cells. Appl. Environ. Microbiol. 2006, 72, 7345–7348. (37) Tremblay, P. L.; Summers, Z. M.; Glaven, R. H.; Nevin, K. P.; Zengler, K.; Barrett, C. L.; Qiu, Y.; Palsson, B. O.; Lovley, D. R. A c-type cytochrome and a transcriptional regulator responsible for enhanced extracellular electron transfer in Geobacter sulfurreducens revealed by adaptive evolution. Environ. Microbiol. 2010, DOI: 10.1111/ j.1462-2920.2010.02302.x

5031

dx.doi.org/10.1021/es103875d |Environ. Sci. Technol. 2011, 45, 5025–5031