Solar Energy Powered Microbial Fuel Cell with a Reversible

Dec 4, 2009 - The solar energy powered microbial fuel cell is an emerging technology for electricity generation via electrochemically active microorga...
3 downloads 10 Views 2MB Size
Download PDF
Environ. Sci. Technol. 2010, 44, 532–537

Solar Energy Powered Microbial Fuel Cell with a Reversible Bioelectrode DAVID P.B.T.B. STRIK, HUBERTUS V.M. HAMELERS,* AND CEES J.N. BUISMAN Sub-Department of Environmental Technology, Wageningen University, Bomenweg 2, P.O. Box 8129, 6700 EV Wageningen, The Netherlands

Received August 11, 2009. Revised manuscript received November 9, 2009. Accepted November 19, 2009.

The solar energy powered microbial fuel cell is an emerging technology for electricity generation via electrochemically active microorganisms fueled by solar energy via in situ photosynthesized metabolites from algae, cyanobacteria, or living higher plants. A general problem with microbial fuel cells is the pH membrane gradient which reduces cell voltage and power output. This problem is caused by acid production at the anode, alkaline production at the cathode, and the nonspecific proton exchange through the membrane. Here we report a solution for a new kind of solar energy powered microbial fuel cell via development of a reversible bioelectrode responsible for both biocatalyzed anodic and cathodic electron transfer. Anodic produced protons were used for the cathodic reduction reaction which held the formation of a pH membrane gradient. The microbial fuel cell continuously generated electricity and repeatedly reversed polarity dependent on aeration or solar energy exposure. Identified organisms within biocatalyzing biofilm of the reversible bioelectrode were algae, (cyano)bacteria and protozoa. These results encourage application of solar energy powered microbial fuel cells.

Introduction The solar energy powered microbial fuel cell is an emerging technology for direct renewable energy production from solar energy via organic matter produced by organisms like algae (1), cyanobacteria (2), and higher plants (3, 4). Like any chemical fuel cell, a microbial fuel cell (MFC) primarily consists of an anode and a cathode. At the bioanode, microorganisms, such as bacteria or algae act as biocatalyst, that oxidize organic matter and transfer electrons directly or via mediators to the bioelectrode. In a MFC electrons flow from the anode to the cathode. At the cathode, a chemical or microbiological assisted reduction reaction takes place that, for example, reduces the supplemented oxygen to water, ferricyanide to ferrocyanide (5), nitrate to nitrogen gas (6), Fe3+ to Fe2+ (7), or when additional energy is applied to the electrons, reduces protons to hydrogen (8). A general problem with MFCs, which must be overcome in order for them to succeed, is the pH membrane gradient problem which reduces the cell potential as described by the Nernst equation. The gradient is the result of acidification at the anode caused by microbial fuel oxidation and proton * Corresponding author phone: +31 317 483447; fax: +31 317, 482108: e-mail: [email protected]. 532

9

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 44, NO. 1, 2010

production, alkaline production at the cathode by oxygen reduction with hydroxyl production and nonspecific cation exchange transport through the membrane by the presence and transport cations present in higher concentrations than protons (9-13). The accumulation of protons or hydroxyl ions can be tempered under lab scale conditions by using buffers (13-16), microbial fuel cells without membranes (17), or looping anolyte over the cathode (18). However, these measures have all drawbacks which reduce the energy recovery of the fuel cell (9, 11). Further development of present and new concepts is of utmost importance to solve the pH membrane gradient problem (9). Besides the pH membrane gradient problem, biocathodes in MFCs need further development as they show high overpotentials and thus energy loss (11, 12, 19, 20). In the case of oxygen reducing biocathodes, for example, mass transfer of oxygen is limiting the current in fuel cells (19, 21). A solution toward this problem is the open air biocathode (22) which reduces oxygen mass transfer limitation but still faces charge transfer resistance. Furthermore, the supply of oxygen as a final electron acceptor for cathodes reduces the net energy output of MFC as aeration is energy demanding (19, 20). Thus, there is a challenge solve the pH membrane gradient problem and use low energy input biocathodes. The objective of this study was to develop a solar energy powered microbial fuel cell with a reversible bioelectrode as solution for the pH membrane gradient problem. Such a reversible bioelectrode should be able to perform alternately anodic and cathodic reactions. This way anodic produced protons do not need to be transported through the membrane but can be used to reduce oxygen in the same compartment without causing a persistently pH membrane gradient. For this purpose we developed a biocathode inoculated with nitrifying sludge which was thereafter illuminated and further inoculated with phototrophic microorganisms. Then the next phenomenon was observed: during illumination the bioelectrode mainly functioned as in situ oxygen producing and reducing biocathode, and during the dark period, the bioelectrode mainly functioned as bioanode. So a reversible bioelectrode was be able to perform alternately anodic and cathodic reactions. This way the pH membrane gradient problem was solved and a low energy biocathode was developed.

Experimental Section Microbial Fuel Cell Setup. A flat plate microbial fuel cell (projected surface area 290 cm2; same as the membrane area) was used similar to the MFC described (23) as shown in Figure 1. The flat plate MFC consisted of seven Plexiglas plates sized 28 cm (height) by 28 cm (width) by 1.3 cm (thick), containing ring shaped gaskets and bolted together. The MFC was a two chamber MFC with a anode chamber (including the counter electrode) and cathode chamber (including the reversible bioelectrode). Figure 1 shows the location of the graphite felt (19.0 × 19.0 cm; thickness: 3 mm, FMI Composites Ltd., Galashiels, Scotland), of the reversible bioelectrode (cathode chamber), the cation exchange membrane (fumasep FBM, FuMA-tech GmbH, St. Ingbert, Germany), and a similar graphite felt for the counter electrode (anode chamber). Supporting Information (SI) Figure S1 shows pictures of the used plates of the MFC of which some were described in more detail in ref 7. The cooling mantle plates were connected to a cooling bath filled with tap water (Fulabo F10, Germany, temperature control at 30 °C). The artificial solar energy was supplied with a 400 W MASTER 10.1021/es902435v

 2010 American Chemical Society

Published on Web 12/04/2009

FIGURE 1. Picture of solar energy powered microbial fuel cell. (1) illumination, (2) massive plate, (3) flow channel plate as cooling mantle, (4) massive plate, (5) flow channel plate for reversible bioelectrode, (6) first flow channel plate for counter electrode, (7) second flow channel plate for counter electrode, (8) flow channel plate as cooling mantle, (9) site of graphite felt of reversible bioelectrode, (10) site of cation exchange membrane, (11) site of graphite felt of counter electrode. SON-T PIA Green Power lamp (Philips) by illumination at the side of the cathode chamber (reversible bioelectrode). The distance between the lamp and the reversible bioelectrode was 25 cm. PAR (photosynthetically active radiation) was 450 µmol/m2.s at biofilms surface. The light was time switch controlled resulting in a continuous illumination period of 14 h/d. The applied external resistance during operation was 1000 ohm. The anode compartment of the MFC was covered with aluminum foil (not shown on picture in Figure 1). The anolyte and catholyte, with both a volume of total 2 and 1.1 L respectively, were continuously circulated by peristaltic pumps with a flow rate of respectively 6 and 4 L/h as described. The cathode flask contained also a sparger to be able to pump ambient air with an aquarium pump at a flow rate of 12 L/h. The circulation circuit contained the online sensors and was placed in a temperature-controlled room at 30 °C (SI Figure S1). Data Acquisition and Analytical Methods. On and offline data as well as calculation methods potentials, pH, dissolved oxygen, microbial analyses via scanning electron microscopy, light microscopy, polarization curves, photosynthetic efficiencies, as described in refs 5, 24 were acquired. The biofilm of the bioelectrode was further analyzed by phytoplankton pulse amplitude modulation (PHYTO-PAM) (Heinz Walz, Germany) to determine the groups of phototrophic micro organisms. PHYTO-PAM analyses chlorophyll concentrations (ChlF0) based on F0 fluorescence and in addition it uses four different excitation wavelengths, which allows the separation between cyanobacteria, green algae, and diatoms (25). To determine the Coulombic efficiency of the oxygen reducing biocathode, oxygen respiration and current was measured without oxygen supply using a sealed cathode compartment without gas phase. Cathode and anode potentials were measured vs Ag/AgCl electrodes (PreSens, Germany). Experimental Procedures. The reversible bioelectrode was developed following three development phases: (i) the oxygen reducing biocathode, (ii) the in situ oxygen producing and reducing biocathode, and (iii) the reversible bioelectrode. Phase 1 was the start-up of the bioanode and development of oxygen reducing biocathode. The anode compartment of MFC was started with anolyte solution containing a Hoagland nutrient solution (24) supplemented with a phosphate buffer

(K2HPO4 and KH2PO4; 20 mM and pH 7.0) and batch fed with potassium acetate start concentration: 20 mM. When acetate was depleted, 5 mL of a 2 M stock solution of potassium acetate was added. The anode of the MFC was inoculated with 10 mL effluent containing microorganism of another MFC which had been running on acetate (14). The pH of the anolyte was controlled with 0.1 M NaOH to maintain a minimum pH of 7 (controller of Endress + Hauser Liquisys S, The Netherlands; modified by Workshop Wageningen University for pH control). The cathode compartment of the MFC was started with catholyte solution containing a Hoagland nutrient solution (24) with additional a phosphate buffer K2HPO4 and KH2PO4; 20 mM and pH 7.0 and 61 mM NaHCO3. The oxygen reducing biocathode was inoculated with fresh sludge of the domestic wastewater treatment plant of Bennekom (The Netherlands) on day 1 and 6. The air pump was turned on to supply oxygen to the cathode compartment. The pH of the catholyte was controlled with 0.1 M HCl to maintain a maximum pH of 7.6 (controller of Endress + Hauser Liquisys S, The Netherlands; modified by Workshop Wageningen University for pH control). Phase 2 was the development of the in situ oxygen producing and reducing biocathode. Therefore, on day 42 of the experiment the illumination was started 14 h on and 10 h off, the aeration of the cathode compartment was stopped and the cathode compartment was sealed from the atmosphere to prevent further oxygen supply. The biocathode was further inoculated with surface water samples of River Renkums Beekdal (Renkum, The Netherlands) and Lake De Lange Jan (Tilburg, The Netherlands). Phase 3 was the development of the reversible bioelectrode. Therefore, the bioanode was replaced by a phosphate buffered (K2HPO4 and KH2PO4; 20 mM and pH 7.0) ferro/ ferri cyanide solution (K4[FeCN6].3H2O, 50 mM; K3[FeCN6], 50 mM) on day 126. In between, the anode compartment was cleaned with demiwater to remove the remaining anolyte of the bioanode compartment. This setup was operated for 22 days. During the reversible bioelectrode operation the bioelectrode pH control was turned off. The pH control of the ferrous/ferric cyanide counter electrode maintained.

Results and Discussion In-Situ Oxygen Producing and Reducing Biocathode. First the oxygen reducing biocathode was developed by inoculation with sludge of a municipal wastewater treatment plant, and by supply of oxygen during the first 41 days of the experiment. The electrochemically active microorganisms at the biocathode, so-called biocatalysts, use the electrode to obtain electrons for their metabolism and use oxygen as final electron acceptor. Herewith overpotential was reduced while the micro organisms employ a part of the released energy for their metabolism (14, 19, 26). A polarization curve of the biocathode performance (SI Figure S2) shows that the oxygen reducing biocathode shows higher current densities at the same potential than the chemical oxygen reducing cathode with even higher oxygen concentrations and was thus enhancing performance (27, 28). The Coulombic efficiency of oxygen reduction at the biocathode was 84%; which means that the remaining 16% of oxygen was likely used for microbial respiration with another electron donor. The oxygen reducing biocathode was transformed into a novel in situ oxygen producing and reducing biocathode during days 42-125. Therefore, at day 42, the oxygen reducing biocathode was inoculated with surface water samples containing algae and a diversity of noncharacterized microorganisms. In this period the external oxygen supply was stopped, the biocathode was closed from the outside environment, an overpressure valve was installed to release produced gaseous oxygen, and the biocathode was illuminated with artificial solar energy 14 h per day. Within VOL. 44, NO. 1, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

9

533

FIGURE 2. Long-term performance of the oxygen producing and reducing biocathode MFC. (a) Current density at 1000 Ohm external resistance and dissolved oxygen vs time. (b) Biocathode and bioanode potential (vs Ag/AgCl) vs time. 2 days after the inoculation the color of the biocathode changed from brown in to green and the dissolved oxygen concentration increased to 12 mg/L, which indicated the growth of oxygenic microorganisms. Finally, a 1 cm thick phototrophic biofilm containing algae, cyanobacteria and other bacteria evolved at the cathode. During illumination, photosynthetically produced oxygen was available as final electron acceptor for the microbial catalyzed cathodic oxygen reduction. The in situ oxygen production promotes application of low energy input biocathodes for MFCs powered by solar energy and MFC sediment systems. This because these systems concur low oxygen concentrations or difficult oxygen supply and because oxygen supply consumes energy and is not needed when oxygen is produced in situ (3, 19). In the dark period oxygen was depleted and the current density dropped typically from 26 to 5 mA/m2 and recovered after the illumination was turned on (Figure 2). During illumination the Coulombic efficiency of oxygen reduction at the cathode was typically 3%. This means that 3% of the consumed oxygen was reduced to water which means that the remaining 97% of oxygen consumption was used for remaining processes like microbial respiration. Because reduction reactions took place without oxygen, other final electron acceptors like, for examle, nitrate or ferric iron, must have been present (6, 23). During illumination the biocathode potential was typically 0.23 V (vs Ag/AgCl) at a current density of 26 mA/m2 which was higher than a oxygen reducing cathode at a comparable pH and oxygen concentration while no microorganisms are present (SI Figure S2). Thus, presence of microorganisms at the cathode enhanced performance, hence a so-called microbially catalyzed biocathode was developed (19, 27, 28). Solar Energy Powered Microbial Fuel Cell with a Reversible Bioelectrode. The new phenomenon of the reversible bioelectrode was induced on day 126 when the bioanodic electrode was replaced with a reversible ferrous/ ferric cyanide couple and phosphate buffer. The bioelectrode operated as in situ oxygen producing and reducing biocathode during illumination, and reversed polarity during the dark period, and therefore changed into an anode (Figure 3a and b). This polarity reversal was observed from the first 534

9

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 44, NO. 1, 2010

FIGURE 3. Long-term performance of the reversible bioelectrode MFC. (a) Current density at 1000 Ohm external resistance and dissolved oxygen vs time (anodic current is positive and cathodic current is negative). (b) Bioelectrode and counter electrode potential (vs Ag/AgCl) vs time. (c) pH vs time. dark period on and resulted in typical alternating current production presented in Figure 3a. Evidently, microorganisms and electron donors were present to provide conditions for biocatalyzed anodic electron transfer since there was no additional inoculation of microorganisms or external supply of electron donors. During illumination, photosynthetic produced oxygen increased from 0 up to 20 mg/L in the bulk solution under stable biocathodic current densities of around 3.3 mA/m2. The cathode bioelectrode potential was then 0.12 V (vs Ag/AgCl) which is 0.03 V higher than under oxygen reducing conditions while no microorganisms were present (SI Figure S2); hence, the bioelectrode still catalyzed to some extent the biocathodic reduction reaction. In the dark period the oxygen concentration dropped, and typically at an oxygen concentration of 7 mg/L, the current changed from around 3.3 mA/m2 cathodic into an anodic current of around 10 mA/m2. Within 5 h the oxygen concentration dropped to 0 mg/L, as it was used for aerobic respiration by micro organisms present in mixed phototrophic biofilm (29). The bioelectrode potential stabilized at a typical bioanode potential of -0.45 V vs (Ag/AgCl) at oxygen depleted conditions (15). Complex Biofilm Produces in Situ Electron Donor and Acceptor. The evolved reversible bioelectrode was unique in its function because it was responsible for biocatalyzed anodic and cathodic electron transfer while producing electrical power. Up to now only bioelectrodes with mixed populations were developed which could operate in one direction (20, 26-28). There are some reports on Geobacter sulfurreducens which can produce current in bioanodes and can

FIGURE 4. Polarization properties. (a) Oxygen producing and reducing biocathode potential in the dark (oxygen concentration ) 0 mg/L; pH 7.0 ( 0.2); Reversible bioelectrode potential during illumination (oxygen concentration ) 19 ( 1 mg/L; pH 7.0 ( 0.2) and in the dark (oxygen concentration ) 0 mg/L; pH 7.0 ( 0.2. vs current density.) (b) Reversible bioelectrode power density vs current density during illumination (oxygen concentration ) 19 ( 1 mg/L; pH 7.0 ( 0.2) and in the dark (oxygen concentration ) 0 mg/L; pH 7.0 ( 0.2). accept electrons from a cathode while reducing fumarate to succinate (30, 31). However, if a system like this would be operated as a reversible bioelectrode, energy supply would be needed as the anodic reaction occurs at a higher energy level than the cathodic reaction. Here we report the first reversible biofilm which can produce electrical power. The phototrophic activity of the bioelectrode can explain the reason for coexistence of groups of micro organisms responsible for anodic and/or cathodic electron transfer. This is because phototrophic biofilms typically have steep light, redox, and chemical gradients which enforce stratifications in microbial communities (29). PHYTO-PAM (data not shown), scanning electron microscopy and light microscopy morphological microbial analysis (SI Figure S3) of the reversible bioelectrode confirmed the presence of different groups of micro organisms including bacteria. Identified were unicellular green algae, unicellular and filamentous cyano bacteria, and grazing protozoa, likely Trinema enchelys. Growth of autotrophic microorganisms was promoted as bicarbonate was present in the medium. Since it was a mixed biofilm it could not be revealed which microbial species were actually responsible for the anodic and/or cathodic biocatalytic activity. Operation of the microbial fuel cell with alternating illumination without microorganisms at the bioelectrode and the ferrous/ferric cyanide couple at the counter electrode resulted in no current generation (data not shown). Thus the present microorganisms were a prerequisite for operation of the reversible bioelectrode and thus responsible for both biocatalyzed anodic and cathodic electron transfer. We can conclude that the developed fuel cell was solar energy powered. This because chemical energy stored by microorganisms obtained by photosynthesis and possibly by biocathodic reduction reactions, were the only available electron donor. Reversible Bioelectrode with Higher Anodic than Cathodic Power and Current Densities. The maximum power density and derived internal resistance of the reversible bioelectrode during cathodic current were 3.1 mW/m2 and 384 Ohm. During anodic current the bioelectrode achieved 41 mW/m2 with an 102 Ohm internal resistance (Figure 4). The maximum power of the bioelectrode during biocathodic electron transfer was 2 orders of magnitude lower than other reports on biocathodes (27, 28, 32), which shows room for improvement of current densities (5). The microbial fuel cell with the reversible bioelectrode generated continuous power until the end of the experiment period of 22 days with in

total 4.1 kJ/m2 electrical energy. The light energy recovery over the period of the reversible bioelectrode operation was 0.0024%. This refers to the total Joules of generated electricity divided by the total Joules of photosynthetically active light energy wavelengths 400-700 nm. The presence of the reversible counter electrode was the prerequisite for the reversible bioelectrode to be able to operate as an anode. This was illustrated by Figure 4a which shows only anodic current of the reversible bioelectrode with the reversible ferrous/ferric cyanide and not with a bioanode counter electrode. The bioelectrode anodic transferred coulombs (amount of electric charge) were typically 1.9 times higher than the cathodic transferred coulombs. Therefore, not all ferrocyanide was reduced back to ferricyanide during cathodic electron transfer. This means that at some point, the amount of anodic transferred coulombs would be limited by the amount of cathodic electron transferred coulombs. Furthermore, the reversible ferrous/ferric cyanide used here will not be sustainable during long-term operation due to the chemical instability of ferrous/ferric cyanide in aqueous solutions. An alternative counter electrode could be manufactured using electrochemical capacitors that can be charged and discharged for over 500 000 times (33). The Formation of a pH Membrane Gradient Was Held by the Reversible Bioelectrode. The pH membrane gradient is general MFC problem as it reduces cell potential. The problem accounts for solar energy powered MFCs as those treating wastewaters (1, 3, 4, 24). The pH gradient arises from: anodic produced protons which accumulate at the anode causing a pH drop, cathodic produced hydroxyl ions which accumulate at the cathode causing a pH increase, and limited transfer of protons through the membrane (11, 12, 34). With the phenomenon of the reversible bioelectrode, as demonstrated here, it is possible to solve the pH membrane gradient problem. This because anodic produced protons do not need to be transported through the membrane but can be used to reduce oxygen in the same compartment without causing a persistent pH gradient (across the membrane). During the dark period in which the bioelectrode produces anodic current, the pH of the bulk solution dropped due to the accumulation of produced protons Figure 3c. This shows the typical acidification behavior of bioanodes (10, 12, 35). The acidification was partially reversed by illumination. In this period, the pH increased as the result of the consumption of protons during the cathodic reduction reaction in combination with the photosynthetic activity of the bioelectrode VOL. 44, NO. 1, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

9

535

as coherent CO2 consumption causes an increase of pH. Thus there was no permanent accumulation of protons at the anode and hydroxyl ions at the cathode which would lead to an increasing pH gradient causing voltage loss. The pH of the reversible bioelectrode oscillated between 6.7 and 7.2 without pH control for a period of 22 days (experimental period: days 126-148). Proton and alkalinity diffusion from the bioelectrode to the counter electrode was likely causing a pH fluctuation at the counter electrode (Figure 3c). This effect was also seen when the bulk pH of the bioelectrode was higher than the counter electrode which is explained by pH gradients typically present in biofilms (Figure 3c; day 136.5-137) (29). So possibly, the pH within the biofilm was lower than the pH in the bulk solution of the bioelectrode. Polarity Reversal Depends on Aeration or Solar Energy Exposure. Besides illumination, oxygen can also determine the function of the bioelectrode. This was found when the reversible bioelectrode was aerated without illumination. SI Figure S4a shows that the increase of the dissolved oxygen concentration to 5.5 mg/L, due to the aeration, led to reversal of the current direction from bioanode to biocathode. SI Figure S4b shows the bioelectrode and counter electrode potential change, which phenomenon was similar as observed in Figure 3b when the illumination was turned on. The unique reversible bioelectrode holds promise as alternative for anode and cathode catalysts because it can solve the pH membrane gradient problem within several applications. Clearly, further studies to improve power output and long-term performance of reversible bioelectrodes within solar energy powered MFCs are required to reach economical feasible applications.

Acknowledgments We thank the anonymous reviewers for their valuable comments. Also, we thank Miquel Lu ¨ rling of the Aquatic Ecology and Water Quality Management group of Wageningen University, Janneke Tempel of TTIW Wetsus Leeuwarden for their help with microbial analyses and for valuable comments and discussion Kealan De Wit Gell and Adriaan Jeremiasse. This research was funded by SenterNovem, the Dutch governmental agency for sustainability and innovation from the Ministry of Financial Matters grant no. EOSLT06020 and supported by Nuon.

Supporting Information Available Supporting Information includes Figure S1 with additional pictures of the experimental setup, Figure S2 which shows additional polarization curves, Figure S3 which shows photos of the oxygen producing and reducing biocathode, and Figure S4 which shows the effect of aeration on the performance of the reversible bioelectrode. This material is available free of charge via the Internet at http://pubs.acs.org.

Literature Cited (1) Rosenbaum, M.; Schro¨der, U.; Scholz, F. Utilizing the green alga Chlamydomonas reinhardtii for microbial electricity generation: A living solar cell. Appl. Microbiol. Biotechnol. 2005, 68 (6), 753–756. (2) Tanaka, K.; Tamamushi, R.; Ogawa, T. Bioelectrochemical fuelcells operated by the cyanobacterium, Anabaena variabilis. J. Chem. Technol. Biotechnol. 1985, 35 B (3), 191–197. (3) Strik, D. P. B. T. B.; Hamelers, H. V. M.; Snel, J. F. H.; Buisman, C. J. N. Green electricity production with living plants and bacteria in a fuel cell. Int. J. Energy Res. 2008, 32 (9), 870–876. (4) De Schamphelaire, L.; Van Den Bossche, L.; Hai, S. D.; Ho¨fte, M.; Boon, N.; Rabaey, K.; Verstraete, W. Microbial fuel cells generating electricity from rhizodeposits of rice plants. Environ. Sci. Technol. 2008, 42 (8), 3053–3058. (5) Logan, B. E.; Hamelers, B.; Rozendal, R.; Schro¨der, U.; Keller, J.; Freguia, S.; Aelterman, P.; Verstraete, W.; Rabaey, K. Microbial fuel cells: Methodology and technology. Environ. Sci. Technol. 2006, 40 (17), 5181–5192. 536

9

ENVIRONMENTAL SCIENCE & TECHNOLOGY / VOL. 44, NO. 1, 2010

(6) Clauwaert, P.; Rabaey, K.; Aelterman, P.; De Schamphelaire, L.; Pham, T. H.; Boeckx, P.; Boon, N.; Verstraete, W. Biological denitrification in microbial fuel cells. Environ. Sci. Technol. 2007, 41 (9), 3354–3360. (7) Ter Heijne, A.; Hamelers, H. V. M.; De Wilde, V.; Rozendal, R. A.; Buisman, C. J. N. A bipolar membrane combined with ferric iron reduction as an efficient cathode system in microbial fuel cells. Environ. Sci. Technol. 2006, 40 (17), 5200–5205. (8) Rozendal, R. A.; Hamelers, H. V. M.; Euverink, G. J. W.; Metz, S. J.; Buisman, C. J. N. Principle and perspectives of hydrogen production through biocatalyzed electrolysis. Int. J. Hydrogen. Energy 2006, 31 (12), 1632–1640. (9) Harnisch, F.; Schro¨der, U. Selectivity versus mobility: Separation of anode and cathode in microbial bioelectrochemical systems. ChemSusChem 2009, 2 (10), 921–926. (10) Rozendal, R. A.; Hamelers, H. V. M.; Buisman, C. J. N. Effects of membrane cation transport on pH and microbial fuel cell performance. Environ. Sci. Technol. 2006, 40 (17), 5206–5211. (11) Rozendal, R. A.; Hamelers, H. V. M.; Rabaey, K.; Keller, J.; Buisman, C. J. N. Towards practical implementation of bioelectrochemical wastewater treatment. Trends Biotechnol. 2008, 26 (8), 450–459. (12) Clauwaert, P.; Aelterman, P.; Pham, T. H.; De Schamphelaire, L.; Carballa, M.; Rabaey, K.; Verstraete, W. Minimizing losses in bio-electrochemical systems: The road to applications. Appl. Microbiol. Biotechnol. 2008, 79 (6), 901–913. (13) Sleutels, T. H. J. A.; Hamelers, H. V. M.; Rozendal, R. A.; Buisman, C. J. N. Ion transport resistance in microbial electrolysis cells with anion and cation exchange membranes. Int. J. Hydrogen Energy 2009, 34 (9), 3612–3620. (14) Ter Heijne, A.; Hamelers, H. V. M.; Saakes, M.; Buisman, C. J. N. Performance of non-porous graphite and titanium-based anodes in microbial fuel cells. Electrochim. Acta 2008, 53 (18), 5697–5703. (15) Lee, H. S.; Parameswaran, P.; Kato-Marcus, A.; Torres, C. I.; Rittmann, B. E. Evaluation of energy-conversion efficiencies in microbial fuel cells (MFCs) utilizing fermentable and nonfermentable substrates. Water Res. 2008, 42 (6-7), 1501–1510. (16) Zuo, Y.; Cheng, S.; Call, D.; Logan, B. E. Tubular membrane cathodes for scalable power generation in microbial fuel cells. Environ. Sci. Technol. 2007, 41 (9), 3347–3353. (17) Hu, Z. Electricity generation by a baffle-chamber membraneless microbial fuel cell. J. Power Sources 2008, 179 (1), 27–33. (18) Freguia, S.; Rabaey, K.; Yuan, Z.; Keller, J. Sequential anode-cathode configuration improves cathodic oxygen reduction and effluent quality of microbial fuel cells. Water Res. 2008, 42 (6-7), 1387– 1396. (19) He,Z.;Angenent,L.T.Applicationofbacterialbiocathodesinmicrobial fuel cells. Electroanalysis 2006, 18 (19-20), 2009–2015. (20) Logan, B. E. Exoelectrogenic bacteria that power microbial fuel cells. Nat. Rev. Microbiol. 2009, 7 (5), 375–381. (21) Fornero, J. J.; Rosenbaum, M.; Cotta, M. A.; Angenent, L. T. Microbial fuel cell performance with a pressurized cathode chamber. Environ. Sci. Technol. 2008, 42 (22), 8578–8584. (22) 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 (21), 7564–7569. (23) Ter Heijne, A.; Hamelers, H. V. M.; Buisman, C. J. N. Microbial fuel cell operation with continuous biological ferrous iron oxidation of the catholyte. Environ. Sci. Technol. 2007, 41 (11), 4130–4134. (24) Strik, D. P. B. T. B.; Terlouw, H.; Hamelers, H. V. M.; Buisman, C. J. N. Renewable sustainable biocatalyzed electricity production in a photosynthetic algal microbial fuel cell (PAMFC). Appl. Microbiol. Biotechnol. 2008, 81 (4), 659–668. (25) Lu ¨ rling, M.; Verschoor, A. M. F0-spectra of chlorophyll fluorescence for the determination of zooplankton grazing. Hydrobiology 2003, 491, 145–157. (26) Kim, B. H.; Kim, H. J.; Hyun, M. S.; Park, D. H. Direct electrode reaction of Fe(III)-reducing bacterium, Shewanella putrefaciens. J. Microbiol. Biotechnol. 1999, 9 (2), 127–131. (27) 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 (5), 519–527. (28) Bergel, A.; Fe´ron, D.; Mollica, A. Catalysis of oxygen reduction in PEM fuel cell by seawater biofilm. Electrochem. Commun. 2005, 7 (9), 900–904. (29) Roeselers, G.; Van Loosdrecht, M. C. M.; Muyzer, G. Heterotrophic pioneers facilitate phototrophic biofilm development. Microb. Ecol. 2007, 54 (3), 578–585. (30) Gregory, K. B.; Bond, D. R.; Lovley, D. R. Graphite electrodes as electron donors for anaerobic respiration. Environ. Microbiol. 2004, 6 (6), 596–604.

(31) Dumas, C.; Basseguy, R.; Bergel, A. Microbial electrocatalysis with Geobacter sulfurreducens biofilm on stainless steel cathodes. Electrochim. Acta. 2008, 53 (5), 2494–2500. (32) Aelterman, P.; Rabaey, K.; Pham, H. T.; Boon, N.; Verstraete, W. Continuous electricity generation at high voltages and currents using stacked microbial fuel cells. Environ. Sci. Technol. 2006, 40 (10), 3388–3394. (33) Miller, J. R.; Burke, A. F. Electrochemical capacitors: challenges and opportunities for real-world applications. Interface 2008, 17 (1), 53–57.

(34) Rozendal, R. A.; Sleutels, T. H. J. A.; Hamelers, H. V. M.; Buisman, C. J. N. Effect of the type of ion exchange membrane on performance, ion transport, and pH in biocatalyzed electrolysis of wastewater. In. Water Sci. Technol. 2008, 57, 1757–1762. (35) Torres, C. I.; Lee, H. S.; Rittmann, B. E. Carbonate species as OH- carriers for decreasing the pH gradient between cathode and anode in biological fuel cells. Environ. Sci. Technol. 2008, 42 (23), 8773–8777.

ES902435V

VOL. 44, NO. 1, 2010 / ENVIRONMENTAL SCIENCE & TECHNOLOGY

9

537