Different Routes for Direct Interspecies Electron Transfer with Diverse Electron-Accepting Partners

Direct interspecies electron transfer (DIET) may be most important in methanogenic environments, but studies to date that have examined the mechanisms for electron transfer from electron-donating partners have primarily focused on co-cultures in which fumarate was the terminal electron acceptor. To better understand DIET with methanogens, the transcriptome of Geobacter metallireducens during DIET-based growth with Geobacter sulfurreducens reducing fumarate was compared with the transcriptome of G. metallireducens grown in co-culture with diverse Methanosarcina species. The transcriptome of G. metallireducens co-cultured with G. sulfurreducens was significantly different from those with Methanosarcina. Furthermore, the transcriptome of G. metallireducens grown with Methanosarcina barkeri, which lacks outer-surface cytochromes, was different from the transcriptome of G. metallireducens co-cultured with Methanosarcina acetivorans or Methanosarcina subterranea, which have an outer-surface c-type cytochrome that serves as an electrical connect for DIET. Differences in G. metallireducens expression patterns for c-type cytochrome genes were particularly notable. The impact of deleting G. metallireducens c-type cytochrome genes depended upon the electron-accepting partner. Multiple cytochromes that G. metallireducens required for DIET with G. sulfurreducens and for Fe(III) oxide reduction were not required for DIET with the Methanosarcina species. Porin-cytochrome complexes and e-pili were required for optimal DIET with all partners. Shewanella oneidensis, another electroactive microbe with abundant outer-surface c-type cytochromes, did not grow via DIET. The results demonstrate that the presence of outer-surface cytochromes does not necessarily confer the capacity for DIET, and also emphasize the substantial impact of the physiology of the electron-accepting partner on the physiology of the electron-donating DIET partner.