Microbial Energizers: Fuel Cells That Keep on Going Microbes that produce electricity by oxidizing organic compounds in biomass may someday power useful electronic devices Derek R. Lovley as this happened to you? You have ganisms with the ability to oxidize organic com- a layover between flights, would pounds to carbon dioxide while transferring like to use your computer and cell electrons to electrodes with extraordinarily high H phone, but both sets of batteries efficiencies. Electricigens make it possible to are drained and the nearby electri- convert renewable biomass and organic wastes cal outlets are being used. What if you could directly into electricity without combusting the instead recharge your electronic devices with a fuel, which wastes substantial amounts of en- little sugar from the nearby coffee stand? With ergy as heat. Efforts to eliminate the inefficien- help from electricity-producing microorgan- cies of combustion are behind the recent interest isms, known as electricigens, some day you in hydrogen fuel cells, which oxidize hydrogen might have new options for ignoring the current and reduce oxygen to water while producing “grid” by generating electricity in an alternative, electricity in a controlled chemical reaction. environmentally friendly manner. With electricigens, however, it becomes pos- Electricigens are recently discovered microor- sible to make microbial fuel cells, which offer potential advantages over hydrogen fuel cells. For example, hydrogen fuel cells re- quire a very pure source of a highly explo- Summary sive gas that is difficult to store and distrib- • Electricigenic microorganisms such as ute. Furthermore, hydrogen is derived Geobacter and Rhodoferax efficiently oxidize mainly from fossil fuel rather than renew- organic compounds to carbon dioxide while able sources. In contrast, the energy sources directly transferring electrons to electrodes. for microbial fuel cells are renewable organ- • Electricigen-based microbial fuel cells mark a ics, including some that are dirt cheap. paradigm shift because these cells completely oxidize organic fuels while directly transferring electrons to electrodes without mediators. Geobacteraceae Producing • Although microbial fuel cells are unlikely to produce enough electricity to contribute to the Electricity in Mud national power grid in the short-term, the cells Several years ago, Leonard Tender of the may prove feasible in some specific instances such as covering the local energy needs for pro- Naval Research Laboratories in Washing- Derek R. Lovley is cessing food wastes. ton, D.C., and Clare Reimers of Oregon Distinguished Uni- • Optimizing microbial fuel cells will entail devel- State University in Corvallis developed sys- versity Professor oping a better understanding of how electron tems in which electricigens produce electric- and Director of En- transfers occur along the outer surfaces of elec- ity from mud! When a slab of graphite (the vironmental Bio- tricigens; key challenges include increasing an- anode) is buried in anaerobic marine sedi- technology at the ode surface areas and increasing electricigen ments and then connected to another piece University of Mas- respiration rates. of graphite (the cathode) that is suspended sachusetts, Am- in the overlying aerobic water, electricity herst. Volume 1, Number 7, 2006 / Microbe Y 323 F I G U R E 1 Sediment fuel cell. (A) Prior to deployment in salt marsh sediments on Nantucket Island, Mass. (B) Diagram of sediment fuel cell reactions. (C) Deployed sediment fuel cells. (Photos courtesy of Kelly Nevin, University of Massachusetts-Amherst.) flows between them (Fig. 1). Although this ar- Which Geobacteraceae prove to be prevalent rangement typically produces meager electrical in such samples depends on the specific environ- currents, they are adequate for running analytic ment being tested. For example, if electrodes are monitoring devices similar to those that investi- placed in marine sediments, Desulfuromonas gators place in remote locations such as the species predominate, whereas if the electrodes ocean bottom. are placed in freshwater sediments, Geobacter How do such sediment fuel cells produce elec- species predominate. Although Geobacter and tricity? The simple answer is, with microbes. Desulfuromonas species have similar physiolo- Dawn Holmes, working with Daniel Bond in gies, Desulfuromonas prefer marine salinity, my laboratory, scraped the anode surface with while Geobacter favor freshwater. a razor blade, extracted DNA from those A hallmark of Geobacteraceae is their ability scrapings, and determined what species were to transfer electrons onto extracellular electron present based on their 16S rRNA genes. The acceptors. For example, Geobacter and Desul- surprising result is that such anodes are highly furomonas species support growth by coupling enriched with microorganisms in the family the oxidation of organic compounds to the re- Geobacteraceae. When similar pieces of graph- duction of Fe(III) or Mn(IV) oxides. Further- ite are incubated in sediments but not connected more, these microorganisms can transfer elec- to a cathode in overlying water, there is no such trons to other metals and to the quinone enrichment. moieties of humic substances, which are so large 324 Y Microbe / Volume 1, Number 7, 2006 that they must be reduced outside bac- F I G U R E 2 terial cells. Reducing Fe(III) oxides is an important means for degrading organic matter in aquatic sediments, submerged soils, and subsurface environments. Mo- Calculator –! –! lecular analyses of such environments re- 8 e 8 e veal that, in general, Geobacteraceae are the predominant Fe(III)-reducing micro- organisms in zones in which Fe(III) re- e–! duction is important. 8 Holmes and Bond found that Outlet 2 CO2! 2 O2! O in Geobacteraceae can also use electrodes +! +! 2 + 8 H! + 8 H! as extracellular electron acceptors. Geobacter 8 e–! Both Desulfuromonas and Geobacter –! +! 8 e 8 H species can grow by oxidizing organic ! compounds to carbon dioxide, with Fuel in Outlet electrodes serving as the sole electron Acetate! 4 H2O (C H O )! acceptor. Moreover, more than 95% of 2 4 2 + 2 H2O the electrons derived from oxidizing such organic matter can be recovered as electricity. In sediment fuel cells, Geobacteraceae oxidize organic com- Anode chamber Cathode chamber pounds but, instead of transferring elec- Cation-selective! trons to Fe(III) or Mn(IV), their natural membrane electron acceptors, they transfer elec- Schematic of Geobacter-powered microbial fuel cell. trons onto electrodes (Fig. 1). The elec- trons flow through the electrical circuit to the cathode, where they react with oxygen to form water. would go to the electricigenic microbe via aero- bic respiration. However, the electricigens still recover some energy from electron transfer to Self-Perpetuating, Highly Efficient, the electrode. This energy recovery is very im- Geobacter-Based Microbial Fuel Cells portant because the energy that the electricigens The sediment fuel cell can be recreated with pure conserve allows them to maintain viability and cultures of Geobacter (Fig. 2). The anaerobic to produce electricity as long as fuel is provided. anode chamber contains organic fuel and a Nearly a century ago, M. C. Potter at the graphite electrode. The cathode chamber has a University of Durham in England measured similar electrode and is aerobic. Geobacter electrical currents when electrodes were placed transfers electrons released from oxidized or- in microbial cultures. In this and other studies ganic matter onto the anode. The electrons flow carried out throughout much of the 20th cen- from the anode to the cathode. The two cham- tury, microbes generated electricity by produc- bers are separated by a cation-selective mem- ing soluble, reduced compounds that could react brane that permits the protons that are released abiotically with electrode surfaces. In initial from oxidized organic matter to migrate to the studies these were natural reduced end products cathode side, where they combine with electrons of fermentation or anaerobic respiration such as and oxygen to form water. hydrogen, sulfide, alcohols, or ammonia. How- The cation-selective membrane limits oxygen ever, many of these reduced products react only diffusion to the anode chamber, preventing slowly with electrodes, and other end products, Geobacter from oxidizing the organic fuels with such as organic acids, do not appreciably react the direct reduction of oxygen. By inserting an with electrodes at all. Adding soluble electron electrical circuit within the flow of electrons to acceptors, known as electron shuttles or media- oxygen, energy can be harvested that otherwise tors, enhances current production in such sys- Volume 1, Number 7, 2006 / Microbe Y 325 F I G U R E 3 Geobacter-Based Fuel Cells Mark a Paradigm Shift Although a few years ago fuel cell ex- perts thought that direct electrochemi- cal contact between microorganisms and electrodes was virtually impossible, this mechanism appears to be how Geo- bacteraceae carry out electron transfer to electrodes. Thus, the use of Geo- bacteraceae in microbially based fuel cells marks a paridigm shift. They com- pletely oxidize organic fuels to carbon dioxide while directly transferring elec- trons to electrodes without mediators. There has been no known evolutionary pressure on microorganisms to produce electricity. Therefore, it is hypothesized that Geobacter cells transfer electrons to electrodes via the same mechanisms that they use when reducing extracellu-