Energy conservation in the gut microbe Methanomassiliicoccus luminyensis is based on membrane‐bound ferredoxin oxidation coupled to heterodisulfide reduction
2019
Kröninger, Lena | Steiniger, Fabian | Berger, Stefanie | Kraus, Sebastian | Welte, Cornelia U. | Deppenmeier, Uwe
Methanomassiliicoccus luminyensis was originally isolated from human feces and belongs to the seventh order of methanogens, the Methanomassiliicoccales, which are only distantly related to other methanogenic archaea. The organism forms methane from the reduction of methylamines or methanol using molecular hydrogen as reductant. The energy‐conserving system in M. luminyensis is unique and the enzymes involved in this process are not found in this combination in members of the other methanogenic orders. In this context our central question was how the organism is able to generate ATP. Energy transduction was dependent on a membrane‐bound ferredoxin: heterodisulfide oxidoreductase composed of reduced ferredoxin as an electron donor, at least one protein in the membrane fraction and the heterodisulfide reductase HdrD, which reduced the electron acceptor CoM‐S‐S‐CoB. Electron transfer of this respiratory chain proceeded with a rate of 145 nmol reduced heterodisulfide min⁻¹·mg⁻¹ membrane protein. Methanomassiliicoccus luminyensis is the first example of a methanogenic archaeon that does not require Na⁺ ions for energy conservation. Only protons were used as coupling ions for the generation of the electrochemical ion gradient. The membrane‐bound F₄₂₀H₂:phenazine oxidoreductase complex (without the electron input module FpoF) probably catalyzed the oxidation of reduced ferredoxin and potentially acted as primary proton pump in this electron transport system. In summary, the energy‐conserving system of M. luminyensis possesses features found in the pathways of hydrogenotrophic and methylotrophic/aceticlastic methanogenesis. Consequently, the composition of the enzymes involved in ion translocation across the cytoplasmic membrane is different from all other methanogenic archaea.
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