Extracellular electron transfer drives efficient H₂-independent methylotrophic methanogenesis byMethanomassiliicoccus,a seventh order methanogen

Abstract

Methylotrophic methanogenesis is achieved via methyl group dismutation or H2reduction. This study reports extracellular electron droving efficient methylotrophic methanogenesis. The 7thorder methanogenMethanomassiliicoccus luminyensisexclusively implements H2-dependent methylotrophic methanogenesis, but strain CZDD1 isolated from paddy soil possessed a higher methane-producing rate in coculture withClostridium malenominatumCZB5 or the electrogenicGeobacter metallireducens.Chronoamperometry detected current production from CZB5, and current consumption accompanied CH4production in a methanol-containing electrochemical culture of CZDD1. This demonstrated thatM. luminyensiswas capable of both direct species electron transfer (DIET) and extracellular electron transfer (EET) in methylotrophic methanogenesis. EET and DIET also enabled CZDD1 to produce methane from dimethyl arsenate. Differential transcriptomic analysis on H2-versus EET- and DIET-cocultures suggested that a membrane-bound Fpo-like complex and archaella ofM. luminyensisCZDD1 could accept extracellular electrons. Given the ubiquitous environmental distribution ofMethanomassiliicoccusstrains, EET driven methylotrophic methanogenesis may contribute significantly to methane emission.