Lactate oxidation is linked to energy conservation and to oxygen detoxification via a putative terminal cytochrome oxidase in Methanosarcina acetivorans

• Published in: Archives of biochemistry and biophysics 2023-07, Vol.743, p.109667-109667, Article 109667
• Main Authors: Feregrino-Mondragón, R. Daniela, Santiago-Martínez, Michel Geovanni, Silva-Flores, Mayel, Encalada, Rusely, Reyes-Prieto, Adrián, Rodríguez-Zavala, José S., Peña-Ocaña, Betsy Anaid, Moreno-Sánchez, Rafael, Saavedra, Emma, Jasso-Chávez, Ricardo
• Format: Article
• Language: English
• Subjects: Acetate metabolism; Air adaptation; Archaea; Cytochromes; Energy conservation; Methanogenesis; Oxygen detoxification
• ISSN: 0003-9861; 1096-0384
• DOI: 10.1016/j.abb.2023.109667

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, CO2 and glycogen, indicating that lactate metabolism fed both methanogenesis and gluconeogenesis. Moreover, d-lactate oxidation was coupled to O2-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 O2 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 O2, producing methane, glycogen and biomass.•D-iLDH and cyt bd oxidase transcripts increased in cells showing high O2-consumption.•Respiration linked to lactate oxidation was sensitive to HQNO and partially to azide.•Lactate oxidation potentially through cytochromes, consumed the otherwise toxic O2.