Extracellular electron transfer based methylotrophic methanogenesis in paddy soil and the prevalent Methanomassiliicoccus

The biogenic methane contributes obviously to global warming, and direct interspecies electron transfer (DIET) driven CO2 reductive methanogenesis is one of the important methanogenic pathways. Here we report DIET-driven methylotrophic methanogenesis in paddy soil and the prevalent Methanomassiliicoccus. M. luminyensis CZDD1 exhibited a 1.9-fold higher methanol-derived methanogenic rate when cocultured with Clostridium malenominatum than its H2-dependent monoculture. Coculturing with Geobacter metallireducens, a known extracellular electron producer, CZDD1 showed the same efficient methanol-derived methane production, thus identified DIET-based methylotrophic methanogenesis. Chronoamperometry detected efficient methane production by M. luminyensis CZDD1 and two paddy soils from methanol and dimethylarsenate in accompany with current consumption. Differential transcriptomics predicted a membrane-bound Fpo-like complex of CZDD1 for uptake of extracellular electrons. Co-occurrence of Methanomassiliicoccaceae with Geobacteraceae and Clostridiaceae was found in five Chinese paddy soils, and Methanomassiliicoccus is ubiquitously distributed among various anoxic environments. Therefore, DIET-driven methylotrophic methanogenesis can be an important mechanism in methane emission. Prevalence of Methanomassiliicoccus was found to be co-occurring with Geobacter and Clostridium in Chinese soils suggesting that direct interspecies electron transfer is an important mechanism for methane emissions in paddy soils, according to co-culturing experiments with bacterial strains coupled with field sampling and chronoamperometry.