Saturn's icy moon Enceladus features chemical signatures consistent with an alkaline soda ocean with H2 production via hydrothermal water-rock reactions. Chemolithoautotrophic methanogenesis is thermodynamically favorable under these conditions, but it is unknown whether CO2 scarcity in the alkaline Enceladus soda ocean limits autotrophy. Here, we show that simulated Enceladus' ocean chemistry containing high concentrations of dissolved inorganic carbon and H2 from mineral-water reactions enables growth of the chemolithoautotroph H2-oxidizing methanogen Methanothermococcus okinawensis until pH 11, far exceeding its previously known pH limit. Transcriptomics revealed that growing cells overcome CO2 scarcity in the simulated Enceladus soda ocean by overexpressing the reductive acetyl-CoA pathway for CO2 fixation, which enabled efficient scavenging of CO2 at extremely low concentrations. The carbon and energy metabolism of M. okinawensis was entirely fueled by the abiotic H2 derived from the simulated Enceladus mineral-water reactions.
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