Recent studies have shown that interspecies electron transfer between chemoheterotrophic bacteria and methanogenic archaea can be mediated by electric currents flowing through conductive iron oxides, a process termed electric syntrophy. In this study, we conducted enrichment experiments with methanogenic microbial communities from rice paddy soil in the presence of ferrihydrite and/or sulfate to determine whether electric syntrophy could be enabled by biogenic iron sulfides. Although supplementation with either ferrihydrite or sulfate alone suppressed methanogenesis, supplementation with both ferrihydrite and sulfate enhanced methanogenesis. In the presence of sulfate, ferrihydrite was transformed into black precipitates consisting mainly of poorly crystalline iron sulfides. Microbial community analysis revealed that a methanogenic archaeon and iron- and sulfate-reducing bacteria (Methanosarcina, Geobacter, and Desulfotomaculum, respectively) predominated in the enrichment culture supplemented with both ferrihydrite and sulfate. Addition of an inhibitor specific for methanogenic archaea decreased the abundance of Geobacter, but not Desulfotomaculum, indicating that Geobacter acquired energy via syntrophic interaction with methanogenic archaea. Although electron acceptor compounds such as sulfate and iron oxides have been thought to suppress methanogenesis, this study revealed that coexistence of sulfate and iron oxide can promote methanogenesis by biomineralization of (semi)conductive iron sulfides that enable methanogenesis via electric syntrophy.

Keywords: Geobacter; Methanosarcina; Methanogenesis; electric syntrophy; iron sulfide.

© 2018 The Authors. MicrobiologyOpen published by John Wiley & Sons Ltd.