Two Novel <i>S</i> ‐methyltransferases Confer Dimethylsulfide Production in <i>Actinomycetota</i>

Hydrogen sulfide (H₂S), methanethiol (MeSH), and dimethylsulfide (DMS) are abundant sulfur gases with crucial roles in global sulfur cycling, chemotaxis, and climate regulation. Microorganisms can S-methylate H₂S and MeSH, which can be cytotoxic, to yield non-toxic DMS via MddA or MddH enzymes in largely terrestrial or marine environments, respectively. However, the potential of many important and abundant bacteria like Actinomycetota is underestimated due to unknown Mdd enzymes. Here, two novel S-adenosine-methionine-dependent H₂S and MeSH S-methyltransferases, MddM1 and MddM2 are identified, in the DMS-producing actinomycete Mycolicibacterium poriferae (M. poriferae) ZYF656, isolated from the Mariana Trench. M. poriferae ZYF656 MddM1 and MddM2 likely detoxify H₂S and MeSH and alleviate oxidative stress, since mddM1 and mddM2 transcription is induced by H₂S, MeSH, and oxidative stress, and their expression in E. coli enhances H₂S, MeSH, and oxidative stress tolerance. MddM1 and/or MddM2 are in >50% of actinomycetota, including the model Streptomyces species, S. venezuelae, but are also seen in some Chloroflexota, Acidobacteriota, and Proteobacteria. mddM1 is always more abundant than mddM2 in diverse environments and is prevalent in soils and marsh sediments. This study highlights the significance of H₂S- and MeSH-dependent DMS production and, principally, of Actinomycetota in global DMS production and sulfur cycling.