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The marine archaeon Methanosarcina acetivorans contains a putative NAD + -independent d -lactate dehydrogenase (D-iLDH/glycolate oxidase) encoded by the MA4631 gene, belonging to the FAD-oxidase C superfamily. Nucleotide sequences similar to MA4631 gene, were identified in other methanogens and Firmicutes with >90 and 35–40% identity, respectively. Therefore, the lactate metabolism in M. acetivorans is reported here. Cells subjected to intermittent pulses of oxygen (air-adapted; AA-Ma cells) consumed lactate only in combination with acetate, increasing methane production and biomass yield. In AA-Ma cells incubated with d -lactate plus [14C]- l -lactate, the radioactive label was found in methane, CO 2 and glycogen, indicating that lactate metabolism fed both methanogenesis and gluconeogenesis. Moreover, d -lactate oxidation was coupled to O 2 -consumption which was sensitive to HQNO; also, AA-Ma cells showed high transcript levels of gene dld and those encoding subunits A (MA1006) and B (MA1007) of a putative cytochrome bd quinol oxidase, compared to anaerobic control cells. An E. coli mutant deficient in dld complemented with the MA4631 gene, grew with d -lactate as carbon source and showed membrane-bound d -lactate:quinone oxidoreductase activity. The product of the MA4631 gene is a FAD-containing monomer showing activity of iLDH with preference to d -lactate. The results suggested that air adapted M. acetivorans is able to co-metabolize lactate and acetate with associated oxygen consumption by triggering the transcription and synthesis of the D-iLDH and a putative cytochrome bd : methanophenazine (quinol) oxidoreductase. Biomass generation and O 2 consumption, suggest a potentially new oxygen detoxification mechanism coupled to energy conservation in this methanogen. [Display omitted] • Air-adapted Methanosarcina acetivorans can grow in presence of acetate + lactate. • Lactate was oxidized in the presence of O 2 , producing methane, glycogen and biomass. • D-iLDH and cyt bd oxidase transcripts increased in cells showing high O 2 -consumption. • Respiration linked to lactate oxidation was sensitive to HQNO and partially to azide. • Lactate oxidation potentially through cytochromes, consumed the otherwise toxic O 2. [ABSTRACT FROM AUTHOR]