Updated project metadata. Identification of the peptides composing the enriched multisubunit enzymes natively purified from the microbial enrichment, based on gel bands obtained by native electrophoresis. The anaerobic oxidation of alkanes is a microbial process occurring in deep-sea hydrocarbon seeps that plays a key ecological role in these exotic niches. The metabolic capacity of anaerobic ethane oxidation, involving uncharted biochemistry, was reported in two archaeal species depending on sulfate-reducing partner bacteria. This study deciphers the molecular basis of the CO2-generating steps of ethanotrophy by characterising the native archaeal enzymes isolated from a thermophilic enrichment. While other microorganisms couple these steps to ferredoxin reduction, we found that the CO-dehydrogenase and the formylmethanofuran-dehydrogenase are bound to F420-reductase modules. The crystal structures of these multi-metalloenzyme complexes revealed electronic bridges coupling C1-oxidation to F420-reduction. Accordingly, both systems exhibit robust F420-reductase activities, which are not detected in methanogenic or methanotrophic relative organisms. We speculate that the whole catabolism of these archaea is reoriented towards F420-reduction, which facilitates the electron transfer to the sulfate-reducing partner, therefore representing the driving force of ethanotrophy.