Methyl Sulfide Production by a Novel Carbon Monoxide Metabolism in Methanosarcina acetivorans

Methyl sulfides including dimethyl sulfide and methanethiol form a central component in Earth's sulfur cycle by linking marine and terrestrial sulfur pools. Here we report the novel metabolic production of dimethyl sulfide (DMS) and methanethiol by the methanogen Methanosarcina acetivorans when cultured using carbon monoxide (CO) as the sole carbon and energy source. Parallel cultures with increasing initial sulfide concentrations showed both added growth and enhanced methyl sulfide production suggesting energy conservation. Free energy changes during the reaction are favorable and are likely to be more energetic than other non-methanogenic CO pathways under the marine sediment conditions where M. acetivorans was isolated. We additionally demonstrate methanogenesis inhibition by CO, and propose that methyl sulfide production can be a mechanism for energy production when exposed to a CO stress. Methyl sulfides are known methanogenic substrates, and methyl sulfides produced in the presence of CO can be used as an energy substrate when the CO burden is lifted. To the best of our knowledge this metabolism is both the first documented case of a methanogen producing DMS and the first documented metabolism showing DMS production from a CO carbon source. Analyzing this microbial link between global carbon and sulfur pools can both lead to a better understanding of modern nutrient cycling as well as provide insights to early Earth environments which likely supported methanogenic communities under atmospheres of high CO partial pressures. Potentially significant methyl sulfide production during Earth's early history may make methyl sulfides a biologic indicator when searching for life on other planets.