Electricity from anaerobic methane oxidation by a single methanogenic archaeon Methanosarcina barkeri

Anaerobic oxidation of methane (AOM) coupled with electron transfer to electrodes has recently showed great promise for energy harvesting in microbial electrochemical reactors. To date this process has been reported limited to the syntrophic cooperation of archaea and bacteria in mixed cultures. It remains unknown whether pure archaea alone can catalyze electricity production from methane. Here we report the performance of AOM-driven electricity generation by a single methanogen Methanosarcina barkeri. At a poised electrode potential of +300 mV vs. SHE, a maximum current of 649.7 mA m⁻² was achieved from methane with an appreciable Coulombic efficiency up to 86.9%. The electrogenic mechanism analysis demonstrated that M. barkeri donated most of electrons to electrodes directly and secreted soluble redox-active compounds to facilitate indirect extracellular electron transfer (EET). Electrochemical in situ Fourier transform infrared spectra and metabolic inhibitions suggested the methyl-coenzyme M reductase α-subunit (McrA), NiFe hydrogenases and cytochrome proteins were involved in the AOM-EET process. This work provides the first proof of concept for AOM-powered electricity production by a single archaeon via reversed methanogenesis and suggests methanogens may play an important role in coupling AOM with the reduction of solid electron acceptors in natural environments.