Under Earth’s surface, cut off from oxygen and nutrients, microorganisms cooperate to decompose buried organic material into natural gas, mainly methane. The mechanisms underlying this process and how these organisms contribute more broadly to carbon flow remain unclear. We investigated a group of microorganisms— methylotrophic methanogens — that is widespread in Earth’s subsurface but is largely excluded from models of subsurface methane generation. These archaea convert the methanol and other methylated compounds into methane. However, a subsurface source of methanol, and thus how methylotrophic methanogens contribute to natural-gas production and carbon flow, are not understood. Here we identified an energy metabolism in the subsurface-derived thermophilic anaerobe Zhaonella formicivorans that catalyses the conversion of formate to methanol, thereby producing methanol without requiring methylated compounds as an input. Cultivation experiments showed that formate-driven methanologenesis is inhibited by the accumulation of methanol. However, this limitation can be overcome through methanol consumption by a methylotrophic partner methanogen, Methermicoccus shengliensis. This symbiosis represents a fourth mode of mutualistic cross-feeding driven by thermodynamic necessity (syntrophy), previously thought to rely on transfer of hydrogen, formate or electrons. The unusual metabolism and syntrophy provide insights into the enigmatic presence of methylated compounds in subsurface methanogenic ecosystems and demonstrate how organisms survive at the thermodynamic limit through metabolic symbiosis.

Syntrophy,interspecies electron transfer,formate metabolism,methanol production,methanogenesis