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.