Previous studies have suggested that members of theGeobacteraceaecan use electrodes as electron acceptors for anaerobic respiration. In order to better understand this electron transfer process for energy production,Geobacter sulfurreducenswas inoculated into chambers in which a graphite electrode served as the sole electron acceptor and acetate or hydrogen was the electron donor. The electron-accepting electrodes were maintained at oxidizing potentials by connecting them to similar electrodes in oxygenated medium (fuel cells) or to potentiostats that poised electrodes at +0.2 V versus an Ag/AgCl reference electrode (poised potential). When a small inoculum ofG. sulfurreducenswas introduced into electrode-containing chambers, electrical current production was dependent upon oxidation of acetate to carbon dioxide and increased exponentially, indicating for the first time that electrode reduction supported the growth of this organism. When the medium was replaced with an anaerobic buffer lacking nutrients required for growth, acetate-dependent electrical current production was unaffected and cells attached to these electrodes continued to generate electrical current for weeks. This represents the first report of microbial electricity production solely by cells attached to an electrode. Electrode-attached cells completely oxidized acetate to levels below detection (<10 μM), and hydrogen was metabolized to a threshold of 3 Pa. The rates of electron transfer to electrodes (0.21 to 1.2 μmol of electrons/mg of protein/min) were similar to those observed for respiration with Fe(III) citrate as the electron acceptor (E^o′ =+0.37 V). The production of current in microbial fuel cell (65 mA/m²of electrode surface) or poised-potential (163 to 1,143 mA/m²) mode was greater than what has been reported for other microbial systems, even those that employed higher cell densities and electron-shuttling compounds. Since acetate was completely oxidized, the efficiency of conversion of organic electron donor to electricity was significantly higher than in previously described microbial fuel cells. These results suggest that the effectiveness of microbial fuel cells can be increased with organisms such asG. sulfurreducensthat can attach to electrodes and remain viable for long periods of time while completely oxidizing organic substrates with quantitative transfer of electrons to an electrode.

The possibility of providing the acetogenic microorganism Sporomusa ovata with electrons delivered directly to the cells with a graphite electrode for the reduction of carbon dioxide to organic compounds was investigated. Biofilms of S. ovata growing on graphite cathode surfaces consumed electrons with the reduction of carbon dioxide to acetate and small amounts of 2-oxobutyrate. Electrons appearing in these products accounted for over 85% of the electrons consumed. These results demonstrate that microbial production of multicarbon organic compounds from carbon dioxide and water with electricity as the energy source is feasible. IMPORTANCE Reducing carbon dioxide to multicarbon organic chemicals and fuels with electricity has been identified as an attractive strategy to convert solar energy that is harvested intermittently with photovoltaic technology and store it as covalent chemical bonds. The organic compounds produced can then be distributed via existing infrastructure. Nonbiological electrochemical reduction of carbon dioxide has proven problematic. The results presented here suggest that microbiological catalysts may be a robust alternative, and when coupled with photovoltaics, current-driven microbial carbon dioxide reduction represents a new form of photosynthesis that might convert solar energy to organic products more effectively than traditional biomass-based strategies.

Wired for Life: Syntrophic bacteria live on the metabolic by-products of a partner species. The exchange of the by-products accompanies a flow of electrons in the opposite direction that helps some species grow in conditions that would otherwise be unfavorable. In mixed anaerobic cultures of two related Geobacter species, Summers et al. (p. 1413 ) observed that one species evolved to promote the transfer of electrons directly to the other, in large aggregated cell clusters, without coupling to common anaerobic by-products such as hydrogen or formate. Selection pressures in nine parallel populations all resulted in a point mutation that truncated a protein involved in the production of small hairlike projections involved in intercellular communication—pili—and indirectly increased the expression of a c -type multiheme cytochrome responsible for extracellular electron transfer. The evolved aggregates were conductive, suggesting that the direct exchange of electrons between partner species is a possible alternative route to anaerobic syntrophy rather than interspecies hydrogen transfer; indeed, deleting a gene that encodes a hydrogenase involved in hydrogen transfer conferred a growth advantage in the cocultures.