Carbon monoxide oxidation expands the known metabolic capacity in anaerobic methanotrophic consortia

Efficient energy metabolism is essential for microorganisms living on the thermodynamic edge. Consortia of anaerobic methane-oxidizing archaea (ANME-2) and sulphate-reducing bacteria (SRB) represent globally relevant syntrophic associations capable of growing with minimal amounts of free energy and can persist when methane becomes limiting. Their potential for physiological plasticity, including the use of electron donors beyond methane is poorly understood. Carbon monoxide (CO) has been reported in seep environments and represents a thermodynamically favourable alternative electron donor due to its low reduction potential. We demonstrate that environmental ANME-SRB consortia can oxidize CO in the absence of methane, in anoxic microcosm experiments using a combination of stable isotope geochemical tracers, metatranscriptomics, and single cell activity measurements (FISH-nanoSIMS). The oxidation of CO was coupled with sulphate-reduction by syntrophic consortia, and, in the absence of sulphate, through CO2 reduction to methane by ANME-2. Under these conditions, the production of methane was one ninth the rate of methanotrophy coupled to sulphate-reduction. Paired single cell FISH-nanoSIMS analysis of anabolic activity indicates that CO respiration appears to support cell maintenance rather than active growth, consistent with the observed down-regulation of energy generating complexes in ANME (e.g., mtr, rnf, etc.). The versatile capability of CO oxidation by anaerobic methanotrophic consortia broadens our understanding of carbon cycling in methane seeps and highlights potential mechanisms of resilience by methanotrophic archaea under changing geochemical regimes.