Interspecies Electron Transfer via Hydrogen and Formate Rather than Direct Electrical Connections in Cocultures of Pelobacter carbinolicus and Geobacter sulfurreducens
ABSTRACTDirect interspecies electron transfer (DIET) is an alternative to interspecies H2/formate transfer as a mechanism for microbial species to cooperatively exchange electrons during syntrophic metabolism. To understand what specific properties contribute to DIET, studies were conducted withPelobacter carbinolicus, a close relative ofGeobacter metallireducens, which is capable of DIET.P. carbinolicusgrew in coculture withGeobacter sulfurreducenswith ethanol as the electron donor and fumarate as the electron acceptor, conditions under whichG. sulfurreducensformed direct electrical connections withG. metallireducens. In contrast to the cell aggregation associated with DIET,P. carbinolicusandG. sulfurreducensdid not aggregate. Attempts to initiate cocultures with a genetically modified strain ofG. sulfurreducensincapable of both H2and formate utilization were unsuccessful, whereas cocultures readily grew with mutant strains capable of formate but not H2uptake or vice versa. The hydrogenase mutant ofG. sulfurreducenscompensated, in cocultures, with significantly increased formate dehydrogenase gene expression. In contrast, the transcript abundance of a hydrogenase gene was comparable in cocultures with that for the formate dehydrogenase mutant ofG. sulfurreducensor the wild type, suggesting that H2was the primary electron carrier in the wild-type cocultures. Cocultures were also initiated with strains ofG. sulfurreducensthat could not produce pili or OmcS, two essential components for DIET. The finding thatP. carbinolicusexchanged electrons withG. sulfurreducensvia interspecies transfer of H2/formate rather than DIET demonstrates that not all microorganisms that can grow syntrophically are capable of DIET and that closely related microorganisms may use significantly different strategies for interspecies electron exchange.