Mechanisms of extracellular electron transfer in anaerobic methanotrophic archaea

Anaerobic methanotrophic (ANME) archaea are environmentally important, uncultivated microorganisms that oxidize the potent greenhouse gas methane. During methane oxidation, ANME archaea engage in extracellular electron transfer (EET) with other microbes, metal oxides, and electrodes through unclear mechanisms. Here, we cultivate ANME-2d archaea ('Ca. Methanoperedens') in bioelectrochemical systems and observe strong methane-dependent current (91-93% of total current) associated with high enrichment of 'Ca. Methanoperedens' on the anode (up to 82% of the community), as determined by metagenomics and transmission electron microscopy. Electrochemical and metatranscriptomic analyses suggest that the EET mechanism is similar at various electrode potentials, with the possible involvement of an uncharacterized short-range electron transport protein complex and OmcZ nanowires. Anaerobic methanotrophic (ANME) archaea are uncultivated microbes that oxidize the greenhouse gas methane and engage in extracellular electron transfer with other microbes, metal oxides, and electrodes. Here, Ouboter et al. observe strong methane-dependent current associated with high enrichment of ANME archaea on the anode, and provide insights into the mechanisms underlying extracellular electron transfer.