The recently isolated methanogen Methanonatronarchaeum thermophilum is an extremely haloalkaliphilic and moderately thermophilic archaeon and belongs to the novel class Methanonatronarchaeia in the phylum Halobacteriota. The knowledge about the physiology and biochemistry of members of the class Methanonatronarchaeia is still limited. It is known that M. thermophilum performs hydrogen or formate-dependent methyl-reducing methanogenesis. Here, we show that the organism was able to grow on all tested C₁-methylated substrates (methanol, trimethylamine, dimethylamine, monomethylamine) in combination with formate or molecular hydrogen. A temporary accumulation of intermediates (dimethylamine or/and monomethylamine) in the medium occurred during the consumption of trimethylamine or dimethylamine. The energy conservation of M. thermophilum was dependent on a respiratory chain consisting of a hydrogenase (VhoGAC), a formate dehydrogenase (FdhGHI), and a heterodisulfide reductase (HdrDE) that were well adapted to the harsh physicochemical conditions in the natural habitat. The experiments revealed the presence of two variants of energy-conserving oxidoreductase systems in the membrane. These included the H₂: heterodisulfide oxidoreductase system, which has already been described in Methanosarcina species, as well as the novel formate: heterodisulfide oxidoreductase system. The latter electron transport chain, which was experimentally proven for the first time, distinguishes the organism from all other known methanogenic archaea and represents a unique feature of the class Methanonatronarchaeia. Experiments with 2-hydroxyphenazine and the inhibitor diphenyleneiodonium chloride indicated that a methanophenazine-like cofactor might function as an electron carrier between the hydrogenase/ formate dehydrogenase and the heterodisulfide reductase.