Non-enzymatic assimilation of organosulfur compounds at the interface of geochemistry and biochemistry

Dimethyl sulfide (DMS) and dimethyl sulfoxide (DMSO) have important microbial-driven roles in global nutrient cycling, chemotaxis and/or climate regulation. Microbial DMSO and DMS assimilation were thought to require their enzymatic reduction to methanethiol. However, reactive oxygen species were recently shown to mediate methane production from DMS and DMSO. Here, we show that this oxidative mechanism can sustain microbial growth without the need for enzymes to directly reduce DMS or oxidize DMSO. Both, light and heat were effective geochemical drivers of this mechanism that yielded methanesulfonic acid and sulfite, and which mimicked the stepwise oxidation of DMSO by monooxygenases that only enzymatically enhance this oxidation reaction. Furthermore, we demonstrated intracellular DMSO degradation, in which sulfur and the simultaneously released carbon were both utilized by microbes. This study emphasizes that metabolic pathways are not necessarily enzyme-driven, with putatively ancient, non-enzymatic reaction networks taking place at a transition between geochemistry and biochemistry.