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Direct interspecies electron transfer (DIET) is important in diverse methanogenic environments, but how methanogens participate in DIET is poorly understood. Therefore, the transcriptome of  Methanosarcina barkeri  grown via DIET in co-culture with  Geobacter metallireducens  was compared with its transcriptome when grown via H 2  interspecies transfer (HIT) with  Pelobacter carbinolicus . Notably, transcripts for the F 420 H 2  dehydrogenase, Fpo, and the heterodisulfide reductase, HdrABC, were more abundant during growth on DIET. A model for CO 2  reduction was developed from these results in which electrons delivered to methanophenazine in the cell membrane are transferred to Fpo. The external proton gradient necessary to drive the otherwise thermodynamically unfavorable reverse electron transport for Fpo-catalyzed F 420  reduction is derived from protons released from  G. metallireducens  metabolism. Reduced F 420  is a direct electron donor in the carbon dioxide reduction pathway and also serves as the electron donor for the proposed HdrABC-catalyzed electron bifurcation reaction in which reduced ferredoxin (also required for carbon dioxide reduction) is generated with simultaneous reduction of CoM-S-S-CoB. Expression of genes for putative redox-active proteins predicted to be localized on the outer cell surface was higher during growth on DIET, but further analysis will be required to identify the electron transfer route to methanophenazine. The results indicate that the pathways for electron and proton flux for CO 2  reduction during DIET are substantially different than for HIT and suggest that gene expression patterns may also be useful for determining whether  Methanosarcina  are directly accepting electrons from other extracellular electron donors, such as corroding metals or electrodes.

Electron and Proton Flux for Carbon Dioxide Reduction in Methanosarcina barkeri During Direct Interspecies Electron Transfer