Methane metabolism is among the hallmarks of Archaea, originating very early in their evolution. Other than its two main complexes, methyl-CoM reductase (Mcr) and tetrahydromethanopterin-CoM methyltransferase (Mtr), there exist other genes called "methanogenesis markers" that are believed to participate in methane metabolism. Many of them are Domains of Unknown Function. Here we show that these markers emerged together with methanogenesis. Even if Mcr is lost, the markers and Mtr can persist

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... ulting in intermediate metabolic states related to the Wood-Ljungdahl pathway. Beyond the markers, the methanogenic ancestor was hydrogenotrophic, employing the anaplerotic hydrogenases Eha and Ehb. The selective pressures acting on Eha, Ehb, and Mtr partially depend on their subunits' membrane association. Integrating the evolution of all these components, we propose that the ancestor of all methane metabolizers was an autotrophic H2/CO2 methanogen that could perhaps use methanol but not oxidize alkanes. Hydrogen-dependent methylotrophic methanogenesis has since emerged multiple times independently, both alongside a vertically inherited Mcr or from a patchwork of ancient transfers. Through their methanogenesis genomic remnants, Thorarchaeota and two newly reconstructed order-level lineages in Archaeoglobi and Bathyarchaeota act as metabolically versatile players in carbon cycling of anoxic environments across the globe.