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

Abstract

Direct interspecies electron transfer (DIET) is an alternative to interspecies H 2 /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 H 2 and formate utilization were unsuccessful, whereas cocultures readily grew with mutant strains capable of formate but not H 2 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 H 2 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 H 2 /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.

A new model for electron flow during anaerobic digestion: direct interspecies electron transfer to Methanosaeta for the reduction of carbon dioxide to methane

“…16,17 The gene for PilA, the structural protein for electrically conductive pili, was highly expressed (Fig. 2, Table S3 †), as expected 12,15 if the abundant Geobacter species were metabolizing ethanol with direct electron transfer to Methanosaeta.…”

“…Studies with a diversity of mutant strains, decient in key aspects of interspecies H 2 /formate transfer or DIET, as well as genome-wide transcriptomic analysis, demonstrated that H 2 or formate could not be the interspecies electron carrier. 11,12,15 Instead, the co-cultures established electrical connections through the pili of the two Geobacter species, which are electrically conductive.…”

“…12,15 Therefore, in order to overcome the challenges of directly tracking the ow of H 2 or electrons between microorganisms in complex communities we used gene expression patterns as a diagnostic tool to elucidate mechanisms of interspecies electron exchange in the digester aggregates.…”

Microbial dark matter ecogenomics reveals complex synergistic networks in a methanogenic bioreactor

“…For energy-conserving electron disposal, Atribacteria expresses an electron-bifurcating formate dehydrogenase (Wang et al, 2013) and Fd red -dependent energy-conserving membranebound hydrogenase (Figures 2 and 3), suggesting that both formate and H 2 generation may take part in propionate degradation as observed in Syntrophobacter (Harmsen et al, 1998). Moreover, we identify that electron-bifurcating formate dehydrogenase is also encoded by Pelobacter carbinolicus (Pcar_1846-1843), a syntroph dependent on formate transfer (Dubourguier et al, 1986;Rotaru et al, 2012). Although propionate metabolism can be used in the reverse direction fermentatively, we did not detect any pathways for catabolizing fermentative substrates.…”

Role and Potential of Direct Interspecies Electron Transfer in Anaerobic Digestion

“…Summers et al [8] first reported DIET in co-cultures of Geobacter metallireducens and Geobacter sulfurreducens. They observed that DIET can be realized between different species through biological electrical connections by using the multiheme c-type cytochrome OmcS and electrically conductive pili [9]. Subsequently, Kato et al [10] suggested that cell-to-cell electron transfer can also be mediated through nonbiological conductive materials.…”