JOURNAL OF BIOSCIENCE AND BIOENGINEERING Vol. 106, No. 6, 528536. 2008 DOI: 10.1263/jbb.106.

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2008, The Society for Biotechnology, Japan

REVIEW
Recent Developments in Microbial Fuel Cell Technologies for Sustainable Bioenergy
Kazuya Watanabe1,2
Research Center for Advanced Science and Technology, The University of Tokyo, 4-6-1 Komaba, Meguro-ku, Tokyo 153-8904, Japan1 and Hashimoto Light Energy Conversion Project, ERATO, JST, Hongo, Bunkyo-ku, Tokyo 113-8656, Japan2
Received 24 July 2008/Accepted 26 September 2008

Microbial fuel cells (MFCs) are devices that exploit microbial catabolic activities to generate electricity from a variety of materials, including complex organic waste and renewable biomass. These sources provide MFCs with a great advantage over chemical fuel cells that can utilize only purified reactive fuels (e.g., hydrogen). A developing primary application of MFCs is its use in the production of sustainable bioenergy, e.g., organic waste treatment coupled with electricity generation, although further technical developments are necessary for its practical use. In this article, recent advances in MFC technologies that can become fundamentals for future practical MFC developments are summarized. Results of recent studies suggest that MFCs will be of practical use in the near future and will become a preferred option among sustainable bioenergy processes.
[Key words: biomass, wastewater, sustainable energy]

Owing to the recent shortage of fossil fuels and significant influences of global warming, readily available biomass has attracted much attention as a sustainable energy source (1). Unlike fossil fuels, biomass is renewable, and its use is often regarded as carbon neutral. Two main biomass types are used as energy sources: those that are produced for energy generating purposes (e.g., corn) and those that are present in waste materials (e.g., wastewater from food industries and sludge from sewerage). The former type is typically used for bioethanol production (2), while the latter is used for methane and hydrogen production via anaerobic digestion (3, 4). Environmental and economic concerns suggest that it is advisable to use the latter biomass type more widely and efficiently for bioenergy generation (5). Currently, anaerobic digestion processes are widely used in the treatment of organic wastes (3, 4); these processes produce biogas (e.g., methane) that can be converted to heat or electricity. Researchers have also attempted to develop processes for practical hydrogen-gas production coupled with anaerobic digestion, since hydrogen is considered more valuable than methane (6). Recently, the microbial fuel cell (MFC) has been considered as an attractive future option for the treatment of organic wastes and the recovery of bioenergy from these wastes (7). The MFC is a device that exploits microbial catabolic activities to generate electricity from organic matter (7). Workers have proposed several advantages of MFC over the anaerobic biogas technology. First,
e-mail: watanabe@light.t.u-tokyo.ac.jp phone: +81-(0)3-5452-5849 fax: +81-(0)3-5452-5749
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electricity is the most convenient form of energy for human activities, whereas the conversion of biogas to electricity results in a significant energy loss (more than 60%) (5). Second, MFC can be applied to some wastewater types that are not suitable for biogas processes, including low-strength wastewater, wastewater whose major components are volatile fatty acids, and those containing high concentrations of nitrogen and/or sulfur (5, 8). MFC technology has not yet been applied to practical waste material treatments. This is primarily because it is an emerging technology and much time is required for technical maturation. Another reason is that its process performance is considered low when compared to its competitors (e.g., methanogenic anaerobic digesters). In particular, it has been considered difficult to construct large-scale, highly efficient MFC reactors. On average, modern methanogenic digesters treat organic wastes at efficiencies of ~820 kg chemical oxygen demand units per m3 of reactor volume per day (7), equivalent to ~12003000 watts per m3. Given that wasteto-gas, and gas-to-electricity conversion efficiencies are typically 80%, and 40%, respectively, these methanogenic digesters generate electricity at ~380960 watts per m3. These organic-treatment and electricity-generation efficiency values are considered as targets of studies in improving MFC performance. However, when developing an MFC process as an alternative to wastewater-treatment facilities (e.g., an activated-sludge process), the organic-treatment efficiency, and the quality of the treated water become more important than energy efficiency. This type of situation may be an attractive application for MFC technology, since its energy re-

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quirement should be small compared to conventional activated-sludge processes. Recently, numerous studies have been performed on MFC technologies, and high-performance laboratory-scale reactors have been reported (see below). In this article, after a brief explanation on MFC fundamentals, recent developments in MFC technologies are summarized with a focus on technologies that may be useful in practical applications of MFCs in the future. MFC FUNDAMENTALS Microbiological fundamentals Microbes utilize organic compounds as energy and carbon sources. In order to generate energy for growth, organics are decomposed, and chemical energy is released (i.e., fermentation). In addition, high-energy electrons released from organics are transferred to oxidized chemicals (i.e., electron acceptors, such as molecular oxygen) to conserve electrochemical energy (i.e., respiration). In microbial cells, electrons released from organics are initially accepted by intercellular electron-shuttling compounds (e.g., nicotinamide adenine dinucleotide [NAD]), and subsequently transferred to electron acceptors via respiratory electron-transport chains. If a mechanism is present by which electrons released from organics can be transferred from any step in the intercellular electron-transfer pathway to an extracellular electrode (i.e., anode), then microbial oxidation of organics can be coupled with electricity generation (i.e., an MFC). Microbial extracellular electron transfer was first discovered in 1911 by Potter, who demonstrated that electrical energy can be produced, albeit small amounts, from cultures of Escherichia coli and Saccharomyces using platinum electrodes (9). This important discovery remained mostly unnoticed until researchers in the 1980s found that water-soluble electron shuttles (i.e., mediators such as methylene blue, thionine, and 2-hydroxy-1,4-naphthoquinone) artificially added to microbial media could enhance electron transfer from microbial cells to anodes (10). For instance, Bennetto et al. used Proteus vulgaris as a biocatalyst and thionine as a mediator to generate electricity from sucrose (11). Such mediators penetrate bacterial cells in an oxidized form, interact with reducing agents within the cell (e.g., NADH, NADPH, and reduced cytochromes), and are reduced. Reduced mediators then diffuse out of the cells, and on reaching the anode surface are oxidized by the release of electrons. In the 1990s, it was reported that some bacterial species are able to self-mediate extracellular electron transfer at substantial rates. These bacteria were considered to actively utilize electrodes for conserving the electrochemical energy required for their growth (i.e., electrode respiration). This bacterial ability was first described by Kim et al. (12), who showed that a ferric iron-reducing bacterium Shewanella putrefaciens grew on lactate by utilizing an electrode as the sole electron acceptor without the addition of an artificial mediator. Subsequently, many bacterial species have been reported that are capable of performing such electrode respiration (13, 14); including Shewanella oneidensis (13), Geobacter sulfurreducens (14, 15), Pseudomonas aeruginosa (16), and Clostridium butyricum (17). Some of these

bacteria self-produce mediator compounds (16, 17), while others utilize cell-surface cytochromes that directly contact electrodes and transfer electrons (13, 14, 15, 18). Some, e.g., Shewanella oneidensis, are known to utilize both mechanisms for extracellular electron transfer (19). Most importantly, recent studies have shown that naturally occurring microbial communities ubiquitously have the ability to selftransfer electrons to anodes (13, 2022). These discoveries facilitate the construction of MFCs that do not require addition of artificial mediator(s). Since mediators are costly, and some of them are toxic, MFCs based on self-mediating bacteria are more suitable for practical applications. Reactor configurations Either single- or double-chamber MFC reactors can be constructed for electricity generation based on microbial oxidation of organic matter (7). Figure 1A and 1B presents basic configurations of MFC reactors and their electrochemical reactions. In both cases, electrons released by microbes are captured by an anode and transferred to a cathode according to the potential gradient (Ecell) between them. The electrons are used in cathode chemical reactions, in which protons released at the anodes and diffusively transferred to the cathodes are also utilized, thereby completing an electric circuit. Cathode reactions are dependent on the species of electron acceptor and catalyst (see below). Ambient oxygen is the most commonly used electron acceptor, while other oxidants such as ferricyanide have also been used (7). As a catalyst, platinum is widely used for oxygen reduction, while microbes can also serve as cathode catalysts (i.e., biocathode [23]). In double-chamber MFCs (Fig. 1A), liquids in the anode and cathode chambers are separated by a proton exchange membrane (PEM) so as to create a potential difference between them. Organics are injected into the anode chamber under anaerobic conditions, while oxygen (or another oxidant, e.g., ferricyanide) is supplied to the cathode chamber. Many types of double-chamber MFCs have been reported thus far (7). In contrast, when a membrane-type cathode is used, a single-chamber MFC can be constructed (Fig. 1B). This type of MFC was first demonstrated by Park and Zeikus (24), who developed a Fe3+-graphite cathode with an internal proton-permeable porcelain layer. An oxygen-permeable air-cathode membrane suitable for MFCs was subsequently developed by Liu and Logan (25) and is now widely used. In their system, cathode catalysts (e.g., platinum) are supported on the inside (anode side) of a carbon-cloth membrane. The catalysts reduce oxygen molecules diffusing through the diffusion layer on the outside (air-facing side). Excess oxygen can diffuse through the air-cathode membrane and serve as an electron acceptor for microbes in the anode medium. To minimize this electron loss, a PEM can be placed at the inner surface of the air-cathode membrane (25); however, this treatment may not be necessary when the oxygen-diffusion rate of the diffusion layer is low. Evaluation of MFCs performance MFCs are used for generating electrical energy and can be used in the treatment of organic waste. It is important to consider both these purposes when evaluating MFCs (7). Table 1 summarizes the parameters that have been used for evaluating MFCs performance. Among them, Rint, OCV, and Pmax (maximum power) are obtained by analyzing a polarization curve (Fig. 2). A

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FIG. 1. MFC configurations and electrochemical reactions. (A) A double-chamber MFC using oxygen as the cathode electron acceptor. (B) A single-chamber air-cathode MFC (25). (C) A single-chamber air cathode MFC with cloth electrode assembly separator (62). (D) A cassette-electrode MFC (63). M, Mediator; CHO, organics; PEM, proton exchange membrane.

TABLE 1. Parameters used for evaluating the MFC performance Parameter Loading rate Effluent quality Treatment efficiency Power density (per volume) Power density (per area) Current density Open-circuit voltage (OCV) Internal resistance (Rint) Coulombic efficiency (CE) Energy efficiency (EE) Unit kg m3 d1 kg m3 % W m3 W m2 A m2 V % % Description An index for describing the performance of MFC as a waste treatment process. An amount of organics (expressed as chemical oxygen demand [COD; kg]) loaded to MFC is normalized to a net anode volume (m3) and time (d). Concentration of organics (COD) in an effluent discharged from the anode chamber. This is also referred to as COD-removal efficiency that is estimated by dividing the COD concentration in the effluent by that in the influent. A power output is normalized to an anode volume or a sum of anode and cathode volumes. In many cases, the maximum power (Pmax) is calculated from the power curve (current vs. power [Fig. 2]) and used as a power output (i.e., a maximum power density). A power output is normalized to an anode area or a cathode area. A Pmax value is often used (Fig. 2). When an electrode structure is complex (e.g., felt or cloth), a projection area is used rather than a real-surface area. A current generated is normalized to an anode area. This is considered to be an index related to the total catabolic activity of microbes in the anode chamber. A voltage between the anode and cathode measured in the absence of current. A difference between the total electromotive force (emf; the potential difference between the cathode and anode) and OCV is regarded as the total potential loss. This is obtained from the slope of the polarization curve (Fig. 2) and is useful to evaluate the total internal loss in an MFC process. This is defined as the ratio of Coulombs measured as the current to the total Coulombs contained in substrates (estimated from the total COD value). If there are alternative electron acceptors present in an anode chamber, this value diminishes. This is calculated as the ratio of power produced by MFC to the heat energy obtained by combustion of substrates added, and is considered to be the most important to evaluate an MFC process as an energy-recovery process.

polarization curve, which represents voltage as a function of current, can be produced by measuring currents (I) at different voltages (Ecell) using a potentiostat. Alternatively, if a

potentiostat is not available, different resistors can be used to measure Ecell at different external loads. In a polarization curve, the relationship between Ecell and I is expressed by

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FIG. 2. Polarization and power curves used for evaluating electrochemical performance of an MFC. SCC, Short circuit current; refer to the text and Table 1 for other abbreviations.

Ecell(V) = OCV(V) I(A) Rint()

(1)

where Ecell is the cell voltage at a current (I) (see Table 1 for other abbreviations). Rint is equivalent to the slope of the polarization curve (7). Power (P) is calculated as P(W) = I(A) Ecell(V) (2) Thus, a power curve (Fig. 2) can be obtained based on the polarization curve (7). In addition, polarization curves of anode and cathode potentials against a reference electrode (e.g., standard hydrogen and Ag/AgCl electrodes) provide valuable information in identifying the rate-limiting step (7). Recently, volumetric ohmic resistance (Rint multiplied by the reactor volume [ m3]) has been proposed as an important index for comparing MFC reactors of different sizes (26). It has been suggested that this parameter can be related to organic removal efficiency, and an important challenge in MFC development is the scale-up of a reactor without increasing its volumetric ohmic resistance (26). Comparing the performance of different MFC reactors is possible by using the parameters presented in Table 1. However, the parameters calculated for MFCs are largely dependent on operational conditions, and attention should be paid to direct comparisons of performance data from different studies. For example, higher CE and EE values are obtained for MFCs treating non-fermentable substrates (e.g., acetate) than those treating fermentable substrates (e.g., glucose) (27). In general, complex organic matter is associated with low CE values. Thus, it is important to describe operational conditions in detail, when reporting the performance data of MFCs. RECENT TECHNICAL DEVELOPMENTS A distinct feature of an MFC is that its performance is largely dependent on hardware rather than on microbial activity. As described above, electricity generation in an MFC is accomplished by (i) microbial catabolism, (ii) electron transfer from microbes to the anode (anode performance), (iii) reduction of electron acceptors at the cathode (cathode performance), and (iv) proton transfer from the anode to cathode. All four processes influence the total MFC performance, and studies have been performed to improve each of these processes. In addition, reactor configuration largely

influences the performance of each of the above processes and the total MFC performance. Recent technical developments have attempted to improve these processes and reactor configuration. Microbial catabolic activities Although an MFC can be operated by inoculating a pure bacterial culture, naturally occurring microbial communities should be used in practical applications to generate electricity from organic wastes (28). Similar to other microbiological waste treatment processes (e.g., methanogenic digesters and activated-sludge processes), the structure and activity of the microbial community depend on environmental parameters (e.g., pH, oxidation/reduction potential, ionic strength, and temperature). However, it can be difficult to anticipate how these parameters affect microbial communities. Since these environmental parameters also affect other processes (e.g., the protontransfer efficiency, and anode performance) in MFCs, their effects on the microbial activity should be critically evaluated. For example, it has been reported that the type and concentration of buffer chemicals primarily affects protontransfer efficiency (29), thereby influencing the structure and activity of the anode microbial community. Anaerobic sludge has been commonly used as an inoculum for MFCs (30, 31), while wastewater (25, 32) and soil (22, 33) have also been used. Limited studies have systematically investigated the effects of inocula on the startup and performance of MFCs. For example, Kim et al. evaluated procedures to acclimatize microbial communities of MFC for electricity generation (31). They compared performances of MFCs inoculated with untreated anaerobic sludge, a ferric iron-enriched microbial community, and an anode-biofilm from an MFC. The anode biofilm-inoculated MFC performance was superior to anaerobic sludge-inoculated MFC, while enrichment with ferric iron had a negative effect on the performance (31). Hence, they suggested that MFC startup is most successful when biofilm harvested from the anode of an existing MFC is applied to a new MFC. In another study, serial enrichment of the bacteria on the anode of an MFC resulted in increased power output and a change in the bacterial community (30). Many studies have analyzed the microbial community structures in MFCs using molecular phylogenetic techniques (e.g., 16S rRNA gene sequence analyses), and some community structure trends have been reported (26). In a comparison of microbial communities in eight different MFC settings, the phylum Proteobacteria was most frequently detected, followed by phyla Firmicutes and Bacteroidetes (26). However, no specific ubiquitous microorganism has been detected in different MFCs, and it is difficult to link such community-structure information to assessment of microbial activity and MFC-reactor performance. Electrochemical techniques analyze how electrons are transferred to the anode (7, 30) and may be more useful than phylogenetic community information for managing MFC systems (e.g., to control the reduction/oxidation potential in the anode chamber). Anodes The material and structure of the anode can affect microbial attachment, electron transfer, and, in some cases, direct substrate oxidation. Carbon-based materials (e.g., carbon cloth or graphite felt) are frequently used for

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anodes because of their stability in microbial cultures, high electric conductivity, and large surface area. In some cases, carbon-based anodes modified with metals and/or metal oxides increased power production in MFCs. Park and Zeikus (34) constructed composites of graphite, metal (e.g., Fe3+ and Mn4+), and mediator compounds (e.g., neutral red), and reported that current production was enhanced when an electron mediator (Mn4+ or neutral red) was incorporated into a graphite anode. Moreover, treatment of a carbon cloth anode with ammonia gas increased the surface charge of the electrode and improved MFC performance (35). In addition, when phosphate buffer and an anode treated with ammonia gas were used to increase solution conductivity, area and volume power densities of 1970 W m3 and 115 W m3 were recorded, respectively (i.e., 48% higher values compared to those without the two treatments). Moreover, MFC startup time was reduced by 50% (35). Modification of the anode with conductive polymers has also been conducted. Among these polymers, polyaniline (PANI) has been used most frequently; Schrder et al. reported that a platinum electrode covered with PANI achieved a current density one order of magnitude higher than that of an untreated electrode in an MFC inoculated with Escherichia coli (36). Modified PANI polymers, such as fluorinated PANI (37), PANI/carbon nanotube composite (38), and PANI/ titanium dioxide composite (39) were demonstrated to produce higher current densities. It has, however, been pointed out that such organic polymers can serve as microbe growth substrates. For example, PANI was removed from the anode within several hours in the presence of sewage sludge (37). Perfluorinated PANI seems to be more resistant to the microbial attack than unmodified PANI; tetrafluorinated PANI has been reported as intact even after 5 d of incubation with sewage sludge (37). In another study, a gold electrode was coated with a self-assembled monolayer (SAM) and used as an anode in an MFC inoculated with Shewanella putrefaciens (40). Currents produced with gold electrodes coated with various alkanethiol SAMs were compared to that produced with glassy carbon electrodes (40). It was revealed that current production correlated to monolayer molecular chain length and head-group with certain head groups enhancing electronic coupling to the bacteria. Recently, a graphite felt coated with a polymer (polyethyleneimine) and a mediator (9,10-anthraquinone-2,6-disulfate) was used as an anode in a Geobacter-inoculated MFC, and showed a current density of 1.2 A m2 (41). These studies have shown that modification of carbonand metal-based anodes with conductive polymers is a practical approach to enhance MFCs power output. However, care should be taken to ensure the stability of the modified electrodes (37). This would be particularly true in MFCs containing microbial communities (e.g., those derived from anaerobic sludge), since they may possess a wide variety of catabolic abilities. Therefore, in assessing MFCs, it is desirable that the durability of any modified electrodes be reported. Cathodes Reaction efficiency of a cathode is dependent on the concentration and species of the oxidant (electron acceptor), proton availability (discussed in the next section), catalyst performance, and electrode structure. Oxygen in air

has commonly been used as a cathode electron acceptor, since it is free and sustainable with no toxic end product. Most hydrogen fuel cells therefore use oxygen as a cathodic oxidant. In many cases, however, this reaction is the ratelimiting step in an MFC (42). The cathode reaction (see Fig. 1) is inefficient when plain carbon or graphite is used as the electrode (28). Therefore, it is necessary to coat it with catalysts (e.g., platinum). One study reported that a platinum modification resulted in 3- to 4-fold higher current than that with a plain graphite cathode (43). Furthermore, the critical oxygen concentration (below which the catalytic reaction decreases) of the Pt-modified cathode was much lower than that of the plain graphite cathode (2.0 mg l1 vs. 6.6 mg l1) (43). This improvement is considered significant, since oxygen diffusion in the cathode chamber can limit the cathode reaction. Oxygen solubility in water is low (e.g., < 8 mg l1 under air-saturated conditions), and when the oxygen consumed by the cathodic reaction exceeds the solubilization rate, the dissolved-oxygen concentration in the cathode chamber decreases to a concentration at which the cathode reaction is suppressed. This phenomenon frequently occurs in double-chamber MFCs (43). The oxygen supply to the cathode can be improved by employing an air-cathode membrane in the single-chamber MFC configuration (25). An air-cathode membrane is an analogue of the cathode used in the membrane electrode assembly (MEA) in hydrogen fuel cells (44). Cheng et al. investigated the thickness of the diffusion layer situated on the air-side of an air-cathode membrane and demonstrated that a four-layer polytetrafluoroethylene (PTFE) structure was appropriate (45). The diffusion layer provided a sufficient amount of oxygen to the platinum catalysts on the inside, while water leakage was minimal. Although this structure has been used widely in laboratory single-chamber MFCs, it would be necessary to optimize the air-cathode structure, reactor by reactor, to increase MFCs performance. Since platinum is costly, researchers have searched for alternative catalysts that are as efficient as platinum in the MFC cathode reaction. Reported alternatives include ferric iron (34, 46), manganese oxides (47), iron complexes (42), and cobalt complexes (42, 48). In single-chamber MFCs, the effects of cathode catalysts (platinum and cobalt tetramethoxyphenylporphyrin [CoTMPP]) and polymer binders (Nafion and PTFE, used for binding catalysts to the carbon surface) on power density have been analyzed (48). The results indicated that the two catalysts had similar performance; however, concerning the binders, Nafion was superior. It was also shown that the amount of Pt loaded on the cathode (from 0.1 to 2 mg/cm2) did not substantially affect power density (48), suggesting that cathodes used in MFCs can contain minimal Pt, and that Pt can be replaced with a nonprecious metal catalyst, such as CoTMPP, with only slightly reduced performance. In another study, Zhao et al. compared oxygen reduction-dependent cathode currents with Pt, pyrolyzed iron (II) phthalocyanine (pyr-FePc), and pyr-CoTMPP as catalysts (42), and also showed that the performance differences were not large. However, it is likely that these conclusions may not be applicable to more efficient MFCs not affected by other critical rate-limiting steps. For example, Zhao et al. also suggested that the physical and chemical

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environments (e.g., pH and ionic concentrations) severely affect thermodynamics and kinetics of cathode oxygen reduction (42). In addition to oxygen, ferricyanide has been used as a cathode electron acceptor in many studies and some of them produced high power outputs (24, 30). An advantage of ferricyanide is its low overpotential, thus low energy loss, in a plain carbon-based electrode, resulting in high cathode potential and power output (7). However, the reaction is onedirectional as re-oxidation by oxygen is very slow, and the catholyte needs to be renewed, which would lead to increase in cost in a large scale operation. Leakage of ferricyanide to the anode chamber through the PEM is another problem. It has therefore been suggested that ferricyanide is applicable only to experimental MFCs. Hexacyanoferrate (49) and permanganate (50) have also been used as electron acceptors. You et al. reported that a double-chamber MFC with permanganate as the cathodic electron acceptor produced more electric power than those with other electron acceptors, e.g., hexacyanoferrate and oxygen (50). This may be attributed to the higher OCP provided by permanganate in the MFC. Moreover, it was shown that pH, unlike permanganate concentration, had a major impact on the OCP (50). In this case, however regeneration of the electron acceptor would also be problematic in practical use. Another MFC cathode option would be a biocathode, in which microorganisms catalyze cathodic reactions (23). Biocathodes may have advantages over abiotic cathodes. For example, construction and operation costs may be reduced, since costly catalysts (e.g., platinum) and mediators are not required. Also, additional values may be produced when used in MFCs; for instance, denitrification (51) could be coupled with the cathode reaction. To date, several studies have examined the utility of biocathodes in MFCs (52, 53). Clauwaert et al. (52) reported the combination of the anode of an acetate-oxidizing tubular microbial fuel cell with an open-air biocathode for electricity production. They showed that electrochemical precipitation of manganese oxides on the cathodic graphite felt decreased the start-up period by approximately 30% versus a non-treated graphite felt, while after the start-up period, cell performances were similar between the pretreated and non-treated cathodic electrodes. Biomineralization of manganese oxide and its resolubilization at the cathode surface had taken place in a biocathode chamber (47, 54). Rhoads et al. (47) have shown that biomineralized manganese oxides, deposited by Leptothrix discophora, were electrochemically reduced at the cathode, demonstrating that these oxides are superior to oxygen when used as cathodic reactants in MFCs. Proton transfer In many MFCs, the efficiency of proton transfer from the anode to the cathode determines the power output. Equivalent amounts of protons and electrons are generated at the anode (Fig. 1). Electrons migrate to the cathode depending on the potential gradient, while protons are transferred to the cathode by diffusion, which is slower than the electron transfer. Thus, proton transfer is the ratelimiting step and a major cause of internal resistance (7, 29). In addition, although a PEM is necessary for generating a potential gradient between the anode and the cathode chambers, it also functions as a proton transfer barrier. Liu and

Logan compared the electricity generated by the air-cathode single-chamber MFC in the presence and absence of a PEM (25). They found that in the absence of a PEM maximum power density increased from 262 to 494 W m2, suggesting that PEM removal is a cost-effective approach to increase MFC power output; however, this method is not applicable to double-chamber MFCs. Furthermore, Rozendal et al. pointed out operational problems associated with the application of PEMs (e.g., Nafion, the most commonly used PEM) (55). Cation species (e.g., Na+, K+, NH4+, Ca2+, and Mg2+) penetrate Nafion at similar efficiencies to that for protons, and concentrations of these cation species are typically 105 times higher in MFCs than the proton concentration (at neutral pH), resulting in the accumulation of these cations in the cathode chamber (55). Since protons are consumed in the cathode reaction, the transport of these cation species causes an increase in pH in the cathode chamber and a decrease in MFC performance by lowering the cathode potential (56). A detrimental effect of such cation transport has also been reported for an air-cathode MFC (57). Results of the study indicated that cations (e.g., Na+ and K+) transferred through PEM, accumulated at the surface of the aircathode, thereby adversely affecting the cathode reaction. Slow proton transfer also affects reaction rates at the anode and cathode. The accumulation of protons may suppress microbial activity related to organic oxidation at the anode (29), while low proton availability reduces the cathode reaction. Torres et al. investigated how proton transport inside a biofilm limits electrical current generation by anoderespiring bacteria (29). They focused on analyzing how protons are transferred, and revealed that they were mainly transported out of the biofilm by protonating the conjugate base of the buffer system (e.g., phosphate and carbonate). Proton-transfer efficiency depends on the type of PEM (or a similar membrane that separates the anode and cathode), the type and concentration of buffer, and the distance between the two electrodes (according to the diffusion theory). To reduce the anode-to-cathode distance, a reactor configuration similar to that of the MEA for the hydrogen fuel cell (57, 58) may be useful (see next section for further configuration discussion). Studies have been performed to optimize PEM; for instance, Kim et al. compared cation-exchange, anion-exchange, and ultrafiltration (molecular cutoffs of 0.5, 1, and 3 kilodaltons) membranes to determine their effects on MFCs performance (59). They found that these membranes could be used in MFCs, and that anion-exchange membranes facilitated MFC performance. They also suggested that the anion-exchange membrane could efficiently transfer protons when combined with the conjugate base of the phosphate buffer, implying that buffer molecules play an important role in proton transfer (59). Previously, it was shown that an MFC containing a high phosphate buffer concentration (100 mM) produced more current from wastewater compared with that containing a low concentration (50 mM) (56). In this context, Fan et al. compared phosphate and carbonate buffers at different concentrations to determine their effects on MFCs performance (60). They found that the MFC performed best when they were operated in the presence of 200 mM carbonate buffer at pH 9.0. Reactor configuration Different types of MFC reac-

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tors have been constructed, including miniature, cylindrical, upflow, and stacked reactors (see Ref. 61 for a review). Those that have been considered to contain potentially useful designs and technologies for constructing large-scale, high-power, practical MFC reactors are discussed below. High power densities have been achieved using small laboratory reactors because they have low ohmic losses (since resistance is proportional to distance) and short proton-diffusion times (since diffusion time is inversely proportional to the distance traveled). For example, high power densities have been reported in small, single-chamber MFC reactors utilizing cloth electrode assemblies (CEA; see Fig. 1C) (60, 62). In these studies, a J Cloth was placed between a carbon-cloth anode and an air-cathode membrane to function as a separator, not as a PEM (Fig. 1C). Protons were found to easily travel through the cloth, and the authors suggested that the cloth reduced oxygen diffusion from the air-cathode to the anode chamber, resulting in high Coulombic efficiency (i.e., 71% vs. 35% in MFCs with and without J Cloth, respectively). In addition, after optimizing the buffer system in the anode chamber, a high power density was recorded (1550 W m3 [60]). This is essentially a modification of an MEA configuration employed in hydrogen fuel cells (57), and a practical MFC would benefit from the use of this configuration. The MEA approach has also been incorporated into a cassette-electrode (CE) MFC (63). The CE was composed of a box-shaped flat cathode, with two air-cathodes on both sides, sandwiched between two PEMs and two graphite-felt anodes (Fig. 1D). If multiple CEs are inserted into an anaerobic tank, an inside-out single-chamber MFC (i.e., CEMFC) with a high electrode surface-to-volume ratio can be created (63). In a previous study (63), a CE-MFC with 12 CEs, a 1.0 l anode volume, and an anode surface area of 1440 cm was constructed, and it was demonstrated that it could treat synthetic wastewater (comprised starch, peptone, and fish extract) at a loading rate of 5.8 kg m3 d1 and a power density of 130 W per m2. The volumetric ohmic resistance of this CE-MFC was estimated to be 0.6 m m3, which was equivalent to the organic loading rate of 10 kg m3 d1 (26). The Coulombic efficiency of the CE-MFC was reported to be approximately 30% (63). The authors suggested that oxygen diffusion into the anode chamber lowered the efficiency. Merits of such a CE-MFC include: (i) it is highly scalable in size and flexible in shape; (ii) it is easy to maintain as a deteriorated CE can be easily replaced; and (iii) it can be placed in existing anaerobic tanks to modify them to CE-MFCs. It is anticipated that the performance of CE-MFCs will be further improved by incorporating the aforementioned advances made in MFC materials. A scale-up strategy was evaluated by Liu et al. (64). They used graphite brush anodes and tubular air-cathodes to construct a 500 ml MFC reactor, and compared its performance with that of a 28 ml MFC in fed-batch mode. The small MFC produced a volumetric power density of 14 W m3, while the large one produced 16 W m3, suggesting that power output can be maintained during reactor scale-up by employing suitable material selection and design strategies. The stacked system has been widely used in hydrogen fuel cells for increasing the power output (65), and has also

been applied to MFCs (66). Aelterman et al. produced a stacked MFC system comprising six individual double-chamber units, and demonstrated that connection of the 6 MFC units in series and parallel increased voltage (up to 2.02 V) and the current (up to 255 mA), respectively (66). In the series connection, however, the MFC voltage may have been affected by microbial limitations. Aelterman et al. suggested that the stack system has the potential to generate useful energy in MFCs (66); however, Oh and Logan pointed out that voltage reversal can occur during stack operation of MFCs (67). In addition, Oh and Logan suggested that a better understanding of the effects of voltage reversal on the power generation by MFC stacks is required in order to efficiently increase voltage production in stacked MFC systems. CONCLUSIONS This article summarizes the recent technical developments in MFCs. Many studies have focused on analysis and improvement of single parts in MFC reactors, and have suggested material and condition improvements for these parts. Although the results of these studies are useful, it is important to note that materials and conditions optimized for one type of MFC are not always optimal for another. This is because MFC functions as a system, and performance of one part may be directly influenced by other parts of the MFC. When developing an MFC reactor, the materials and conditions need to be carefully considered for the reactor to achieve high power output. Recently, power output from MFC reactors has been increasing to the level of the primary power target, and scaleup and durability are now becoming primary areas in MFC research. Based on results of recent studies, costs for construction and operation of a practical MFC process may now be estimated. These estimates will form the bases for decisions of whether practical MFCs can be constructed. A recent review article presented capital cost estimates for a current laboratory scale MFC reactor and that for a future large-scale reactor using less expensive materials (68). In the review, the authors suggested that cathodes and membranes (PEM) are the two most expensive parts in current MFC reactors, and predicted that current collector, membrane, and reactor frame costs will comprise the largest expenditures in future reactors. Taken together, I suggest that the time has come to evaluate MFC technologies in a pilotscale reactor (e.g., 1 m3 or larger). ACKNOWLEDGMENTS
I thank Takefumi Shimoyama, Yoshiyuki Ueno, and Akira Yamazawa for their valuable discussions. This work was supported by the New Energy and Industrial Technology Development Organization (NEDO) of Japan and Japan Science and Technology Agency (JST).

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