AUTHOR=Ouboter Heleen T. , Berben Tom , Berger Stefanie , Jetten Mike S. M. , Sleutels Tom , Ter Heijne Annemiek , Welte Cornelia U. 

TITLE=Methane-Dependent Extracellular Electron Transfer at the Bioanode by the Anaerobic Archaeal Methanotroph “Candidatus Methanoperedens”

JOURNAL=Frontiers in Microbiology

VOLUME=Volume 13 - 2022

YEAR=2022

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2022.820989

DOI=10.3389/fmicb.2022.820989

ISSN=1664-302X

ABSTRACT=Anaerobic methanotrophic (ANME) archaea have recently been reported to be capable of using insoluble extracellular electron acceptors via extracellular electron transfer. In this study, we investigated extracellular electron transport by a microbial community dominated by ‘Candidatus Methanoperedens’ archaea at the anode of a bioelectrochemical system poised at 0 V vs standard hydrogen electrode, in this way measuring current as a direct proxy of extracellular electron transport by this community. After inoculation of the bioelectrochemical system, the maximum current density was 274 mA m-2 (stable current up to 39 mA m-2). Concomitant conversion of 13CH4 into 13CO2 demonstrated that current production was methane-dependent, with 38% of the current attributed directly to methane supply. Based on current production and methane uptake in a closed system, the coulombic efficiency was about 17%. Polarization curves demonstrated that the current was limited by microbial activity at potentials above 0 V. The metatranscriptome of the inoculum was mined for expression of c-type cytochromes potentially used for extracellular electron transfer, leading to the identification of several multiheme c-type cytochrome-encoding genes among the most abundant transcripts in ‘Ca. Methanoperedens’. Our study provides strong indications of extracellular electron transfer in ANME archaea and describes a system in which ANME-mediated extracellular electron transport can be investigated under laboratory conditions, providing new research opportunities for mechanistic studies and possibly the generation of axenic ANME cultures.