In subsurface methanogenic ecosystems, the ubiquity of methylated-compound-using archaea—methylotrophic methanogens1–4—implies that methylated compounds have an important role in the ecology and carbon cycling of such habitats. However, the origin of these chemicals remains unclear5,6 as there are no known energy metabolisms that generate methylated compounds de novo as a major product. Here we identified an energy metabolism in the subsurface-derived thermophilic anaerobe Zhaonella formicivorans7 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 electrons8–10. 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.
