Environ. Sci. Technol.

2010, 44, 27282734

Carbon Dioxide Addition to Microbial Fuel Cell Cathodes Maintains Sustainable Catholyte pH and Improves Anolyte pH, Alkalinity, and Conductivity
JEFFREY J. FORNERO, MIRIAM ROSENBAUM, MICHAEL A. COTTA, AND L A R G U S T . A N G E N E N T * , Department of Energy, Environmental and Chemical Engineering, Washington University in St. Louis, One Brookings Drive, CB 1180, St. Louis, Missouri 63130, Department of Biological and Environmental Engineering, Cornell University, 214 Riley-Robb Hall, Ithaca, New York 14853, and Fermentation Biotechnology Research Unit, United States Department of Agriculture, Agricultural Research Service (ARS), National Center for Agricultural Utilization Research (NCAUR), Peoria, Illinois 61604

Received October 20, 2009. Revised manuscript received January 27, 2010. Accepted February 10, 2010.

Bioelectrochemical system (BES) pH imbalances develop due to anodic proton-generating oxidation reactions and cathodic hydroxide-ion-generating reduction reactions. Until now, workers added unsustainable buffers to reduce the pH difference between the anode and cathode because the pH imbalance contributes to BES potential losses and, therefore, power losses. Here, we report that adding carbon dioxide (CO2) gas to the cathode, which creates a CO2/bicarbonate buffered catholyte system, can diminish microbial fuel cell (MFC) pH imbalances in contrast to the CO2/carbonate buffered catholyte system by Torres, Lee, and Rittmann [Environ. Sci. Technol. 2008, 42, 8773]. We operated an air-cathode and liquid-cathode MFC side-byside. For the air-cathode MFC, CO2 addition resulted in a stable catholyte lm pH of 6.61 ( 0.12 and a 152% increase in steadystate power density. By adding CO2 to the liquid-cathode system, we sustained a steady catholyte pH (pH ) 5.94 ( 0.02) and a low pH imbalance (pH ) 0.65 ( 0.18) over a 2-week period without external salt buffer addition. By migrating bicarbonate ions from the cathode to the anode (with an anion-exchange membrane), we increased the anolyte pH (pH ) 0.39 ( 0.31), total alkalinity (494 ( 6 to 582 ( 6 as mg CaCO3/L), and conductivity (1.53 ( 0.49 to 2.16 ( 0.03 mS/cm) relative to the feed properties. We also veried with a phosphate-buffered MFC that our reaction rates were limited mainly by the reactor conguration rather than limitations due to the bicarbonate buffer.

Introduction
Bioelectrochemical system (BES) technology holds promise to produce environmentally benign and sustainable energy
* Corresponding author tel.: +1-607-255-2480; fax: +1-607-2554080; e-mail: la249@cornell.edu. Washington University in St. Louis. Cornell University. National Center for Agricultural Utilization Research (NCAUR).
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from wastewaters, replace energy intensive wastewater treatment processes, and produce chemical products (1-6). A BES can be congured as a microbial fuel cell (MFC), or as a microbial electrolysis cell (MEC) by adding an externally applied potential (7-9). With either conguration, microbes oxidize organic substrates to supply electrons to the anode. The electrons then travel through an external circuit to the cathode and participate in reduction reactions (2, 4, 5, 10). Associated with these reactions is the generation of protons and hydroxide ions (with an oxygen reduction reaction [ORR]) in the anolyte and catholyte, respectively, which creates a BES pH imbalance in systems with membranes. The ion migration, which satises the electroneutrality constraint, does not relieve the pH imbalance because cations or anions other than protons or hydroxide ions (dependent upon ionexchange membrane selection) mediate the charge balance (11-15). And since the pH imbalance produces a 0.059 V/pH BES potential loss, minimizing the pH imbalance is necessary for maximizing BES power densities (14). In most lab-scale BESs with liquid catholytes, these potential losses are omitted by using nonsustainable phosphate buffer electrolytes. However, with the intention of developing realistic BESs, novel sustainable solutions have to be developed. Air-cathode BESs may be even more susceptible to pH imbalance losses than liquid-cathode BESs because of the small liquid volume that permeates across an air-cathode membrane (16). Within the limited catholyte volume (i.e., catholyte lm), ORR reactions more quickly increase the catholyte hydroxide ion concentration, and therefore the pH, compared to liquid-cathode BESs. To mitigate an air-cathode pH increase, Torres et al. performed a ground-breaking study to demonstrate the concept of adding carbon dioxide (CO2) to an air-cathode to buffer the pH shift and increase the power density (17). The CO2 reacted with hydroxide ions to form carbonate species (CO32- and HCO3-), which became the highest concentration anions in the catholyte. With an anion exchange membrane (AEM), the carbonate species were transported from the cathode to the anode to maintain electroneutrality and, in essence, served as the vehicle to transfer hydroxide ions and this stabilized the catholyte pH. While the pH of the air-cathode liquid lm was not reported, Torres et al. did nd that CO32was the primary carbonate species migrating (17). On the basis of carbonate species equilibrium, we estimated the catholyte pH to be g10.5, and therefore, the cathode pH remained much higher than the anolyte pH (7.3 to 7.5), resulting in a BES pH imbalance of 3.1 (17, 18). The authors identied the slow rate of CO2 absorption into the catholyte as a limitation factor for the use of carbonate species as hydroxide ion carriers (17). Under conditions of sufcient CO2 absorption, we calculated that the catholyte pH could theoretically be maintained between 3.92 and 5.63 with bicarbonate as the dominating ion species (details in the Supporting Information [SI]) (19). Since this would reduce the pH imbalance, increase the ORR potential, and therefore increase the power density; we hypothesized that a CO2/bicarbonate buffered catholyte would improve MFC performance in comparison to the CO2/ carbonate buffered catholyte system described by Torres et al. (17). Our objective was, thus, to determine if continuous CO2 addition to an air-cathode and a liquid-cathode MFC with an engineered system to provide sufcient CO2 absorption would create a CO2/bicarbonate buffered catholyte system that could theoretically diminish the pH imbalance. In addition, we examined the inuence of the bicarbonate ion migration on anolyte properties (pH, alkalinity, and
10.1021/es9031985 2010 American Chemical Society

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 44, NO. 7, 2010

Published on Web 02/24/2010

FIGURE 1. MFC-LC catholyte circulation with CO2 contactor column. The catholyte is at CO2 equilibrium ([H+] ) 1.15 10-6; [HCO3-] ) 8.0 10-3) before entering the MFC cathode chamber. Within the cathode chamber, the oxygen reduction reaction generates eight hydroxide ions (per mol acetate), which increases the catholyte hydroxide ion concentration. To maintain electroneutrality, eight bicarbonate ions migrate from the cathode to anode. The catholyte exiting the MFC, therefore, has a higher hydroxide ion and lower bicarbonate ion concentration than the catholyte entering the cathode. Within the CO2 contact column, the catholyte is exposed to 100% CO2 gas while passing over a high surface area packing to ensure sufcient CO2 absorption. After absorption, the eight CO2 molecules hydrate and dissociate to produce eight protons, which combine with the hydroxide ions, and eight bicarbonate ions as a reaction product. Thus, the cathode hydroxide ion production is neutralized, the bicarbonate ions lost to migration are replenished, CO2 equilibrium is restored, and the pH remains stable. conductivity) and identied the rate-limiting step in achieving higher power densities. To test our hypotheses, we used two 10-L MFCs with AEMs; one operated as an air-cathode and the other one as a liquid-cathode. The air-cathode MFC, which only had a small volume of water in the cathode chamber that permeated from the anolyte, was operated with an air/CO2 mixture (MFC-AC) and with air-only (MFC-AO). The liquid-cathode MFC, which was lled with water, was operated with a CO2/bicarbonate buffered catholyte (MFCLC), nonbuffered air-only catholyte (MFC-LO), and conventional phosphate-buffered catholyte (MFC-LP). Louis, MO) the following: glacial acetic acid, 0.268 mL; 4 M sodium hydroxide, 0.265 mL; yeast extract (Difco Laboratories, Inc., Detroit, MI), 0.025 g; NH4Cl, 0.03 g; K2SO4, 0.006 g; FeCl2 4H2O, 0.033 g; K2HPO4, 0.033 g; NaHCO3, 1.0 g; iron citrate, 0.011 g; NaCl, 0.25 g; KCl, 0.1 g; CaCl2, 0.1 g; MgCl2 6H2O, 0.1 g; and trace elements, 1.0 mL modied from refs 20 and 21. Feed to the MFC anodes was distributed through six nozzles (for each MFC), evenly spaced and placed on alternating opposing sides along the length of the MFCs (Figures S2 and S3 of the SI). The anolyte for each MFC was recirculated (58 ( 0.3 L/day) from the top to the bottom of the bioreactor. The anolyte efuent owed through a liquid degasser to separate the biogas for measurement prior to anolyte discharge. The cathode of the air-cathode MFC was supplied directly either with a humidied air/CO2 mixture (79% air/21% CO2 mixture for the MFC-AC or solely air for the MFC-AO) at a rate of 410 L/day. The air-cathode had a drain line and collection ask that was used to collect cathode permeate water (<10 mL/day). In addition, the air-cathode chamber was ushed with reverse osmosis (RO) water on a weekly basis to prevent the formation of salt deposits (the pH of this ush water was monitored). For the liquid-cathode MFC, RO water (with or without CO2 addition for MFC-LC and MFC-LO, respectively) or a 0.1-M phosphate buffer solution (for MFC-LP) was recirculated at a rate of 295 L/day through a CO2 contact column and degassers (Figure 1). Air at a rate of 410 L/day was injected into the catholyte before it entered the MFC cathode. In tests with CO2 addition, the recirculating catholyte passed a CO2 contactor column where it was exposed to 100% CO2 gas at a rate of 86 L/day before returning to the MFC. On a daily basis, 35 mL of CO2-catholyte water was exchanged with RO water and 15 mL water was relled to accommodate evaporation (2.5% of total catholyte liquid for both). During steady-state operating periods, the MFCs were operated with an average external resistance of 10 (MFC-AC), 20 (MFC-AO), 6.7 (MFC-LC), 6 (MFC-LO), and 6 (MFC-LP). The MFCs were maintained at room
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Materials and Methods

Experimental Setup. Two identical tubular, upow MFCs (UMFCs) were used. Each UMFC consisted of an inner cathode chamber (total and net volume of 1.96 and 1.64 L, respectively) and an outer anode chamber (total and net volume of 8.49 and 5.80 L, respectively) separated by a tubular AEM. The cathode (with platinum catalyst) and anode were made of graphitized (unsized) carbon fabric cloth. Details of the experimental setup and gures are included in the SI. The liquid-cathode MFC included a catholyte circulation system with two small liquid degassers that were open to the atmosphere, and a clear PVC CO2 contact column (75 cm long 6 cm ID) lled with high surface area packing (Figure 1 and Figure S2 of the SI). Anodic gas production was measured with a gas meter (Ritter MGC-1 Milligas Counter, Bochum, Germany). Operation. The anolyte inoculum was a homogenized granular sludge from an upow anaerobic bioreactor at a brewery (Anheuser Busch-Inbev, Inc., St. Louis, MO). Acetate synthetic wastewater (480 mg/L total chemical oxygen demand [TCOD] concentration) was fed to each of the MFCs at a continuous ow rate of 12.7 L/day (11-h anode hydraulic retention time). A mechanical agitator (Model 5vb, EMI Inc.; Clinton, CT) slowly mixed the feed container. The synthetic wastewater consisted of (per liter of deionized water; all chemicals, unless noted, were from Sigma Aldrich, St.

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TABLE 1. Steady-State Anolyte Feed Properties, Anolyte Effluent Properties, and Catholyte Properties
feeda anolyte properties total COD (mg/L) soluble COD (mg/L) soluble COD removal efciency (%) pH total alkalinity (as mg CaCO3/L) conductivity (mS/cm) biogas volume (cm3/day) biogas composition (%CH4/%CO2) catholyte properties pH inlet pH total alkalinity (as mg CaCO3/L) conductivity (mS/cm) ion analysis-sodium (mg/L) ion analysis-potassium (mg/L) ion analysis-phosphorus (mg/L) overall properties pH imbalance [pH]
a

MFC-ACb 335 ( 53 334 ( 36 32 ( 6 6.95 ( 0.49 591 ( 38 1.99 ( 0.07 NA 72/12 6.61 ( 0.12

MFC-AOc 424 ( 17 399 ( 26 18 ( 2 7.30 ( 0.12 586 ( 8 2.15 ( 0.12 1 70/13 9.0

MFC-LCd 384 ( 45 388 ( 45 20 ( 6 6.59 ( 0.16 582 ( 3 2.16 ( 0.03 1 70/14 5.94 ( 0.02 5.48 ( 0.07 400 ( 4 0.48 ( 0.34 1.61 ( 0.04 0.40 ( 0.04 ND 0.65

MFC-LPe 254 ( 42 249 ( 42 49 ( 8 6.80 ( 0.39 552 ( 61 1.91 ( 0.04 NA 71/11 6.46 ( 0.03 1198 ( 67 8.43 ( 0.19 NA 0.34

477 ( 21 490 ( 17 6.55 ( 0.11 495 ( 9 1.60 ( 0.32

NA NA NA 0.34

0.37 0.11 ND 1.7

Feed data is a composite from all experimental runs. Feed data for the individual experiments is not shown. b MFC-AC: air-cathode MFC with air/CO2 mix. c MFC-AO: air-cathode MFC with air only. d MFC-LC: liquid-cathode MFC with CO2 saturation. e MFC-LP: liquid-cathode MFC with phosphate buffer catholyte. Data for MFC-LO (liquid-cathode MFC with air only) is not shown because stable conditions were not achieved (experimental run was stopped to prevent unstable conditions). Data ( 1 SD. For empty elds, the data analysis was not applicable. NA-not available. ND-not detectable

temperature (23 ( 1 C). They were in continuous operation for 10 weeks prior to data gathering to ensure a welldeveloped anodic bacterial community and stable performance. The total operating period for each system was 20 weeks. Analyses. The potential (E) across a resistor (R, Ohmite Ohm-Ranger, Skokie, IL) was measured using a digital multimeter (2700 + 7700 multiplexer, Keithley Instruments, Inc., Cleveland, OH). The current density was calculated as I ) E/RV, and the power density was calculated as P ) E2/RV, where V is the net liquid volume of the anode chamber. We developed polarization curves by changing the external resistance stepwise from 11 M to 0 during a 7-h period. For data points adjacent to the maximum MFC power, 30min intervals were used between resistance changes. The internal resistance correlates to the maximum power density found during polarization tests. TCOD, soluble COD (SCOD) (closed-reux titrimetric method), total alkalinity (TALK) (end point pH titration), and volatile fatty acids (VFA) (distillation method), were measured according to procedures described in ref 22. Conductivity was determined with a conductivity electrode (MI-900, Microelectrodes, Inc., Bedford, NH). Methane and CO2 gas analysis was performed with a gas chromatograph (Series 350 Gow-Mac, Bethlehem, PA, with a 6 ft 1/8 in. o.d., 80/100 mesh Hayesep Q column (Supelco) and a thermal conductivity detector). The pH level was measured with a hand-held meter (Oakton pH 6, Vernon Hills, IL). Catholyte sodium, potassium, and phosphorus concentrations were measured using inductively coupled plasma-mass spectrometry (ICP-MS, Agilent Technologies 7500ce, Santa Clara, CA). All operating runs were performed in triplicate with the exception of MFC-LO, which lasted 30 h and did not include a polarization test. Biogas production and pH levels were recorded daily. Coulombic efciencies (CEs) were calculated according to ref 20. Feed and operating conditions, with the exception of polarization tests, were held constant during the steady-state data acquisition periods. The pH imbalance potential losses were calculated based on the absolute difference between the anode and cathode pH, and a potential loss of 0.059 V/pH (14).
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Results and Discussion

CO2 Addition to Air-Cathodes Effectively Stabilizes Cathode pH, Minimizes the MFC pH Imbalance, and Improves Power. Adding CO2 with a partial pressure of 0.21 atm to the air-cathode of MFC-AC decreased the catholyte pH from 9.0 to 6.6 compared to MFC-AO, which reduced the pH imbalance from 1.7 to 0.34 (absolute number; the pH for MFC-AC was lower in the cathode than the anode; Table 1). Compared to the estimated numbers from Torres et al., our MFC-AC CO2/bicarbonate buffer system reduced the pH imbalance (pH ) 0.3 vs 3.1est.) and associated potential loss (0.020 V vs 0.183 Vest.) (17). The latter study discussed limitations of CO2 absorption into the catholyte as the reason why the pH imbalances were not further minimized and why no further improvement in performance was observed when the partial pressure of CO2 was increased from 0.02 to 0.10 atm. We are not completely sure why absorption for the Torres at el. study was limited while ours was not; one difference was that the ratio of our cathode to anode surface area was much larger than theirs. This larger area may have sustained a relatively larger water lm in which CO2 could absorb more readily. Regardless, our work shows that, besides electroneutrality maintenance already observed by Torres et al. (17), the CO2/ bicarbonate buffer system is also able to minimize the BES pH imbalance. Steady-state power densities increased when CO2 gas was added to the air-cathode MFC, with MFC-AC producing 152% more power than MFC-AO (2.55 vs 1.01 W/m3) (Table 2). Moreover, the maximum power determined in polarization tests was 92% higher for MFC-AC than for MFC-AO (3.00 ( 0.35 vs 1.56 ( 0.19 W/m3, respectively) (Figure 2A). Both a reduction in pH imbalance and a reduction in ohmic losses between MFC-AC and MFC-AO can explain the difference in performance. First, the lower pH imbalance of 0.34 compared to 1.7 resulted in a lower potential loss of 0.02 V compared to 0.10 V for the MFC-AC and MFC-AO, respectively, resulting in higher power outputs. Second, because of a higher CO2 partial pressure in MFC-AC (PCO2 ) 0.21 atm) than in MFC-AO (atmospheric PCO2 ) 3.85 10-4 atm), the calculated catholyte bicarbonate ion concentration for MFCAC was much higher ([HCO3-] ) 5.48 10-5 vs 2.44 10-6

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 44, NO. 7, 2010

FIGURE 2. MFC polarization and power curves. (A) Polarization (open symbols) and power curves (lled symbols) for the air-cathode MFCs including the air/CO2 mixture, MFC-AC (2), and the air-only, MFC-AO ((). (B) Polarization (open symbols) and power curves (lled symbols) for the liquid-cathode MFCs including the CO2/bicarbonate buffered catholyte, MFC-LC (b), and the phosphate buffered catholyte, MFC-LP (9). (C) Anode potentials of MFC-AC (2) and MFC-AO ((). Cathode potential readings were not obtained for the air-cathode MFC. (D) Anode and cathode potentials vs the current density are shown for MFC-LC (b) and MFC-LP (9). Data points represent an average of three experiments with the accompanying standard deviation error bars.

TABLE 2. Steady-State Current, Power, and Coulombic Efficiency Data

parameter external resistancea () cell potential (V) anode potential (V) cathode potential (V) current (A) current density (A/m3) power (W) power density (W/m3) coulombic efciency (%) MFC-ACb 10 0.3841 ( 0.0070 -0.2997 ( 0.0140 NA 0.038 ( 0.002 6.63 ( 0.30 0.015 ( 0.013 2.55 ( 0.23 14.1 ( 3.6 MFC-AOc 20 0.3528 ( 0.0274 -0.3340 ( 0.0004 NA 0.017 ( 0.001 2.96 ( 0.24 0.006 ( 0.001 1.02 ( 0.16 11.2 ( 2.6 MFC-LCd 6.7 0.4069 ( 0.0230 -0.2963 ( 0.0160 0.1739 ( 0.0130 0.062 ( 0.007 10.66 ( 1.16 0.025 ( 0.001 4.32 ( 0.26 37.2 ( 11.5 MFC-LPe 6.0 0.4478 ( 0.0200 -0.2910 ( 0.0110 0.1483 ( 0.0250 0.075 ( 0.003 12.87 ( 0.57 0.034 ( 0.003 5.77 ( 0.52 17.6 ( 2.8

a The optimum external resistance for steady-state operation was determined in polarization tests. b MFC-AC: air-cathode MFC with air/CO2 mix. c MFC-AO: air-cathode MFC with air only. d MFC-LC: liquid-cathode MFC with CO2 saturation. e MFC-LP: liquid-cathode MFC with phosphate buffer catholyte. Data for MFC-LO (liquid-cathode MFC with air only) is not shown because stable conditions were not achieved (experimental run was stopped to prevent unstable conditions). Data ( 1 SD.

M) (19). Therefore, due to such elevated catholyte conductivities in MFC-AC, the ohmic potential losses were lower, which resulted in a higher power for the MFC-AC compared to the MFC-AO. Cathode CO2 Addition to Liquid-Cathode MFCs also Minimized pH Imbalances. Adding CO2 to the cathode of a liquid-cathode MFC by including a CO2 contact column established a CO2/bicarbonate buffer replenishment system (Figure 1). This resulted in MFC-LC operating conditions with a steady catholyte pH of 5.9 and a pH imbalance of 0.65 (Table 1) (with daily 2.5% water addition/exchange; see the discussion about CO2/bicarbonate buffer limitations). Without the CO2 addition (MFC-LO), the catholyte pH increased quickly from 5 (RO water) to 7.3 in 24 h. Therefore, we terminated this experiment after 30 h because the cell potential breakdown in this system without catholyte ionic strength caused an imbalance (no steady data reported in Tables 1 and 2). The explanation for the stable catholyte pH and a minimized pH imbalance for the MFC-LC requires consideration of CO2 aqueous chemistry, electroneutrality maintenance, and cathode ORR hydroxide ion production

(Figure 1). Because the MFC-LC catholyte consisted of RO water, which was exposed to air and CO2 gas (for now neglecting anolyte to catholyte cation transport): hydroxide ions (water dissociation), carbonate ions, and bicarbonate ions (CO2 absorption, hydration, and dissociation) were the only catholyte anions (19). At a pH of 5.94, bicarbonate ions were the anions in the highest concentration ([HCO3-] . [CO32-] and [HCO3-] . [OH-]) (details in SI), and therefore, electroneutrality was maintained by the migration of bicarbonate ions. Accordingly, to maintain equilibrium conditions for the CO2/bicarbonate buffer system, the hydroxide ions produced by the ORR were neutralized and the bicarbonate ions that were lost to migration from the cathode to anode were replenished by CO2 absorption, hydration, and dissociation within the CO2 contact column (Figure 1). CO2/Bicarbonate Buffer System Is Limited by the Rate of Ion Migration. A bicarbonate ion migration limitation was evident for the MFC-LC when we compared the cathode and anode potentials throughout an increasing current density (Figure 2D). The cathode potential approached zero at a greater rate than the anode potential, indicating that the
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cathode reaction was rate-limiting. A rate limitation can result from a decreased ow of reactants to and/or products from the ORR catalyst sites, which can be observed as mass transport losses in a polarization curve. The polarization curve at a pH of 5.94 (Figure 2B), however, did not indicate prominent mass transfer losses at higher current densities, which rules mass transport losses out as a prominent limitation. Another possible reactant limitation is provoked by the ion migration in the electrolyte and across the ion exchange membrane (i.e., ohmic losses). Electroneutrality entails the ion ux across the membrane to equal the (charge equivalent of the) electron ux from anode to cathode (i.e., current). In other words, when the ion migration ux is limited, electron transfer reactions are hindered, and therefore, the overall BES performance is limited, too (23). The ion migration ux is directly related to the ion concentration. For MFC-LC, the catholyte bicarbonate concentration is, thus, controlled by the CO2 partial pressure and the pH of the solution and is, therefore, restricted to [HCO3-] ) 8.0 10-3 M (based on TALK). Consequently, the relatively low MFCLC bicarbonate concentration restricted the migration ux, which controlled the electron ux and the cathode ORR potential, and ultimately limited the power density. Several observations support a sluggish bicarbonate migration rate: Evidence 1: Concentrated Phosphate Buffer Improved Performance. We veried this limitation due to the bicarbonate concentration by switching to a 0.1 M phosphate buffered catholyte (pH ) 6.46 ( 0.03), which is conventionally used in BES studies to maintain a stable catholyte pH. As anticipated, the higher concentrated phosphate buffer increased the catholyte conductivity from 0.48 ( 0.34 to 8.43 ( 0.2 mS/cm in comparison to MFC-LC. The phosphate ion concentration gradient ([1.0 10-1 M]cathode to [1.89 10-3 M]anode PO43-) also generated a cathode to anode diffusion ux, which complimented the direction of the phosphate ion migration. Polarization tests (Figure 2A) showed that the MFC-LP maximum power density (6.42 ( 0.40 W/m3) was 17% greater than for MFC-LC (5.33 ( 0.27 W/m3). Unexpectedly, however, the internal resistance remained at 4 for MFC-LP. We had anticipated a decreased internal resistance because of the increased conductivity and diffusion alignment with the migration. This data also indicates that the MFC-LC electrode spacing (i.e., the reactor conguration) may have had a more signicant impact on the internal resistance and maximum power than the ionic catholyte composition. Evidence 2: Cations Were Transported from the Anolyte into the Catholyte Solution. Prior to achieving stable catholyte pH conditions with MFC-LC (pH ) 5.94), the pH in the CO2saturated RO water increased from 5.0 (after introducing them into the cathode system) to 5.9 over the rst 32 days of operation at a rate of 0.03 pH/day (Figure S4 of the SI). During this period, catholyte ion concentration surveys and polarization tests were performed at pH values of 5.25 and 5.94 (Figure S5 of the SI). Ion survey data indicated that the cation concentration increased from 0.56 mg Na+/L and 0.13 mg K+/L at a pH of 5.25 to 1.61 mg Na+/L and 0.40 mg K+/L at a pH of 5.94 (Table 1), indicating an increasing cation concentration with increasing pH. This makes sense because with every cation-charge equivalent that is transferred from the anode to cathode, one hydroxide ion less (with bicarbonate as the vehicle) is transferred from the cathode to anode to maintain electroneutrality, resulting in a higher catholyte pH. With further rising pH levels (pH > 6.0), the cell potential began to decline because of a decreasing ORR potential (data not shown). Therefore, daily water replenishments (2.5% of the catholyte volume) with RO water (pH 5 at atmospheric CO2 levels) to lower OH- concentrations in the catholyte were established to stabilize the pH at 5.94 and maximize the MFC-LC potential. The polarization tests, which were performed at the lower and the higher pH, further
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revealed a need for cation transfer at a low pH of 5.25, because the bicarbonate concentrations were too low to fulll the required ion migration to maintain electroneutrality. These curves show prominent mass-transport losses at higher current densities for the pH 5.25 plot, whereas the pH 5.94 plot does not indicate such losses (Figure S5 of the SI). At a pH of 5.94, the bicarbonate ion concentration was sufcient to maintain electroneutrality ([HCO3-] ) 8.0 10-3 M) at the rate demanded by the system, and the ohmic losses dominated the polarization curve. This information indicates that cations were transported from the anode to the cathode (0.004% of current, calculations in the SI) to counterbalance sluggish bicarbonate transport, especially during periods with a relatively low bicarbonate concentration (i.e., at a pH of 5-6; pKA1 ) 6.37). We ensured by leak tests that no anolyte to catholyte leakage occurred and calculated the rate of CO2 consumption vs the rate of CO2 hydration to show that the hydration rate was not limiting our buffer system (calculations in the SI). Sufcient CO2 was absorbed to the catholyte to buffer OHformation, but the resulting bicarbonate concentration was still too low to be efciently transported to the anolyte to balance the pH. Therefore, cations moved from the anolyte to catholyte to maintain electroneutrality, as described above. We consider both passive cation diffusion and active cation forcing as driving forces for this cation transport across the AEM. Even though the AEM is designed to retard cation diffusion due to positive charge sites within the membrane pores, some diffusion of cations is likely, especially since the cation concentration gradient is favoring diffusion. At the pH of 5.25, the catholyte bicarbonate ion concentration was relatively low ([HCO3-] ) 6.6 10-4 M) and insufcient to support the migration ux demand with higher current densities. In this situation, active cation forcing may have been the stronger driving force compared to diffusion to transport cations from the anode to the cathode to maintain electroneutrality (we did not quantify diffusion and forcing). Regardless of the relative importance of diffusion and forcing, cation transfer increased the pH and, thus, the catholyte bicarbonate ion concentration (pKA1 ) 6.37). Cation forcing would have become less important when the pH increased further toward the pKA1 (but we prevented a pH increase beyond 5.94). BES Performance Trade-offs with a CO2/Bicarbonate Buffered System. From this analysis, it becomes clear that changes in catholyte pH inuence the CO2/bicarbonate buffered system both positively and negatively and, therefore, performance trade-offs must be considered when selecting for an optimum catholyte pH. Compared to a balanced anolyte/catholyte (i.e., pH ) 0), a catholyte pH greater than the anolyte pH creates a pH imbalance loss and decreases the ORR potential; whereas a catholyte pH lower than the anolyte pH (MFC-AC; MFC-LC; MFC-LP [Table 1]) creates a pH imbalance loss (0.059 V/pH) that is offset by an equivalent ORR potential increase (0.059 V/pH) (24). In addition, the catholyte bicarbonate ion concentration affected the bicarbonate ion concentration gradient across the AEM, and consequently the bicarbonate ion diffusion. Since the catholyte bicarbonate ion concentration was lower than in the anolyte (8.0 10-3 vs 1.7 10-2 M), an anode to cathode bicarbonate ion concentration gradient existed. The bicarbonate ion diffusion, therefore, was moving in opposite direction to the bicarbonate ion migration, which increased ohmic losses in our system (23). A higher catholyte pH and bicarbonate concentration would align the bicarbonate ion diffusion with migration. In addition, a higher catholyte pH and bicarbonate ion concentration would increase the catholyte conductivity, which would decrease the ohmic resistance, however, at the cost of ORR potential losses. Thus, it is critical for an engineer to optimize the pH in this CO2/

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bicarbonate buffered system to balance potential losses and gains. With our work, we have shown that the daily addition of RO water was sufcient to maintain this optimized pH for maximized power production. Bicarbonate Migration Inuences Anolyte Properties. Increased pH and TALK. Under steady-state operating conditions, the MFC-LC bicarbonate ion migration increased the anolyte pH (6.57-6.96, pH ) 0.39) and TALK (494-582 as mg CaCO3/L) relative to the feed solution (Table 1), which is benecial for BES wastewater treatment. During the anodic biocatalytic oxidation of organic substrates, typically more protons than bicarbonate ions are produced. The proton generation decreases the anolyte pH and lowers the alkalinity, which can increase pH imbalance potential losses, or, at an extreme, negatively affect the anode microbial community (25). Thus, increasing the anolyte pH and alkalinity with bicarbonate can decrease the pH imbalance, increase the alkalinity, and help maintain a healthy microbial community. Increased Conductivity. The MFC-LC bicarbonate ion migration also increased the anolyte conductivity (1.53-2.16 mS/cm) relative to the feed solution (Table 1). Because some wastewaters have a high organic content and a low conductivity, BES treatment is impaired because of a high anolyte ohmic resistance (26, 27). Thus, an intrinsic increase in anolyte conductivity is desirable. Furthermore, the addition of bicarbonate ions to wastewater is compatible with wastewater treatment objectives, whereas phosphate additions may require subsequent removal to ensure compliance with efuent discharge permit specications. Using a CO2/ bicarbonate instead of a phosphate buffered catholyte, therefore, complements wastewater treatment objectives. Practical Impacts of This Study. By adding CO2 to an air-cathode MFC with sufcient cathode surface area and a liquid-cathode MFC with sufcient gas/liquid exchange, we controlled and sustained the catholyte pH. Bicarbonate migration improved anolyte qualities, which are favorable for decreasing BES potential losses, increasing power densities, and improving BES wastewater treatment. In industrial settings (e.g., breweries), CO2 is available as a waste gas, and an increase in TALK in the wastewater efuent is desirable in anaerobic bioreactors for brewery wastewater treatment. This would make an implementation of this CO2 buffered MFC system very promising due to a signicant cost reduction by offsetting external alkalinity sources (e.g., MgOH2). Calculations at a desired current density of 10 A/m2 (see the SI) showed that CO2 dissolution will not be limiting at higher reactor performance. We believe pressurizing the cathode system (higher gas partial pressure) to increase the ORR potential and bicarbonate ion concentration while minimizing pH imbalance losses (20, 28) will help overcome the bicarbonate migration rate-limitation and increase the power density.

buffer can support high current densities. This information is available free of charge via the Internet at http:// pubs.acs.org.

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Acknowledgments
The nancial support for this work was provided through a specic collaborative agreement between Largus Angenent and the Bioenergy Research Unit, USDA, Agricultural Research Service, Peoria, Illinois, and the National Science Foundation through grant no. 0645021. We thank Brian Wood of Arelco for the provision of the tubular membranes, Pat Harkins for his signicant fabrication contributions, Dan Shannon of Zoltek for the provision of the carbon cloth, and Vipul Borkar for his lab support.

Supporting Information Available

Calculations for the catholyte pH based on the carbon dioxide (CO2) partial pressure, catholyte carbon dioxide gas-liquid transfer rates, cation transport estimate calculations, experimental set-up details, MFC fabrication photos, experimental data, and the question of whether a CO2/bicarbonate

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