Anaerobic methane oxidation coupled to ferrihydrite reduction by Methanosarcina barkeri

Fe(III) has been recognized as a potential electron sink for the anaerobic oxidation of methane (Fe-AOM) in diverse environments. However, most of previous Fe-AOM processes are limited to ANME archaea and the Fe-AOM mechanism remains unclear. Here we investigate, for the first time, the Fe-AOM performance and mechanisms by a single methanogen Methanosarcina barkeri. The results showed that M. barkeri was capable of oxidizing methane to CO2 and reducing ferrihydrite to siderite simultaneously. The presence of methane enhanced both the abundances of redox-active species (such as cytochromes) and electrochemical activity of M. barkeri. The proteomic analyses revealed that M. barkeri up-regulated the expressions of a number of methanogenic enzymes during Fe-AOM, and significantly enriched metabolic pathways of amino acid synthesis and nitrogen fixation. Metabolic inhibition experiments indicated that membrane-bound redox-active components (cytochromes, methanophenazine and F420H2:quinone oxidoreductase) were probably involved in extracellular electron transfer (EET) from cells to ferrihydrite. Overall, these results provide a deep insight into the single‑carbon metabolism and survival strategy for methanogens and suggest that methanogens may play an important role in linking methane and iron cycling in the substrate-limited environments.