Mechanisms of extracellular electron transfer in anaerobic methanotrophic archaea

Anaerobic methanotrophic (ANME) archaea are environmentally important uncultivated microorganisms mitigating the release of the potent greenhouse gas methane. During methane oxidation ANME archaea engage in extracellular electron transfer (EET) with other microorganisms, metal oxides, and electrodes, through a currently unknown mechanism. To shed light on this mechanism, we cultivated ANME-2d archaea (Ca. Methanoperedens) in bioelectrochemical systems and observed 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) determined by metagenomics and transmission electron microscopy. Electrochemistry and metatranscriptomics indicated that the EET mechanism was similar at various electrode potentials pointing to the involvement of an so far uncharacterized short-range electron transport protein complex and OmcZ nanowires, suggesting a unique EET pathway in all ANME-2 archaea. Our findings furthermore indicate that bioelectrochemical cells might be powerful tools for the cultivation, and possibly isolation, of uncultured electroactive microorganisms.