Interspecies Electron Transfer via Hydrogen and Formate Rather than Direct Electrical Connections in Cocultures of Pelobacter carbinolicus and Geobacter sulfurreducens

Department of Microbiology, University of Massachusetts, Amherst, Massachusetts, USA.
Applied and Environmental Microbiology (Impact Factor: 3.67). 08/2012; 78(21):7645-51. DOI: 10.1128/AEM.01946-12
Source: PubMed


Direct 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 with Pelobacter carbinolicus, a close relative of Geobacter metallireducens, which is capable of DIET. P. carbinolicus grew in coculture with Geobacter sulfurreducens with ethanol as the electron donor and fumarate as the electron acceptor, conditions under which G. sulfurreducens formed direct electrical connections with G. metallireducens. In contrast to the cell aggregation associated with DIET, P. carbinolicus and G. sulfurreducens did not aggregate. Attempts to initiate cocultures with a genetically modified strain of G. sulfurreducens incapable of both H2 and formate utilization were unsuccessful, whereas cocultures readily grew with mutant strains capable of formate but not
H2 uptake or vice versa. The hydrogenase mutant of G. sulfurreducens compensated, 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 of G. sulfurreducens or the wild type, suggesting that H2 was the primary electron carrier in the wild-type cocultures. Cocultures were also initiated with strains of G. sulfurreducens that could not produce pili or OmcS, two essential components for DIET. The finding that P. carbinolicus exchanged electrons with G. sulfurreducens via 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.

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    • "Multiple lines of evidence (Rotaru et al., 2012; Shrestha et al., 2013a,b; Summers et al., 2010) suggested that the electron transfer between the species was via the Geobacter pili that have metallic-like conductivity (Malvankar et al., 2011; Reguera et al., 2005). The possibility of interspecies H 2 /formate transfer was ruled out by the fact that G. metallireducens is unable to metabolize ethanol with the production of H 2 or formate (Rotaru et al., 2012; Shrestha et al., 2013a,b), and the fact that interspecies electron exchange remained effective when the co-cultures were initiated with a G. sulfurreducens strain incapable of H 2 and formate uptake, because the genes encoding formate dehydrogenase and an uptake hydrogenase were deleted (Rotaru et al., 2012). "
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    • "DIET has been shown possible in the absence of conductive materials via biological electrical connections such as pili1314151617. For example, Geobacter metallireducens and Geobacter sulfurreducens grew in co-culture via DIET in a medium with ethanol as the electron donor and fumarate as the electron acceptor13. The two organisms needed to cooperate in order to metabolize ethanol and grow, because G. metallireducens can utilize ethanol as an electron donor, but is unable to use fumarate as an electron acceptor18, whereas G. sulfurreducens cannot use ethanol as an electron donor, but can reduce the electron acceptor, fumarate19. "
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