Methanol transfer supports metabolic syntrophy between bacteria and archaea

Abstract

In subsurface methanogenic ecosystems, the ubiquity of methylated-compound-using archaea—methylotrophic methanogens^1,2,3,4—implies that methylated compounds have an important role in the ecology and carbon cycling of such habitats. However, the origin of these chemicals remains unclear^5,6 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 electrons^8,9,10. 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.