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Dimethylsulfoniopropionate (DMSP) is an abundant marine organosulfur compound[1] with roles in stress protection[2, 3], chemotaxis[4], nutrient and sulfur cycling[5] and, potentially, climate regulation[6, 7]. Marine algae and bacteria are considered significant DMSP producers, but many diverse representatives lack known DMSP synthesis genes/enzymes[8, 9]. Here, new DMSP biosynthesis enzymes were identified that considerably increase the number and diversity of potential DMSP-producing organisms, inferring new and significant global DMSP producers. A novel bifunctional DMSP biosynthesis enzyme, DsyGD, identified in the rhizobacterium Gynuella sunshinyii, produces DMSP at levels higher than any other bacterium from methylthiohydroxybutyrate (MTHB) via an N-terminal MTHB S-methyltransferase domain (termed DsyG) and a C-terminal dimethylsulfoniohydroxybutyrate (DMSHB) decarboxylase domain (termed DsyD, which is the first reported enzyme with this activity). DsyGD is also found in some filamentous cyanobacteria, not previously known to produce DMSP. Regulation of DMSP production and dsyGD transcription was consistent with their role in osmoprotection. Indeed, cloned dsyGD conferred osmotolerance to bacteria deficient in osmolyte production, something not previously demonstrated for any known DMSP synthesis gene, and which could be exploited for biotechnology e.g., engineering salt tolerance. DsyGD characterisation led to identification of phylogenetically distinct DsyG-like proteins, termed DSYE, with MTHB S-methyltransferase activity, in diverse and environmentally abundant Chlorophyta, Chlorachniophyta, Ochraphyta, Haptophyta and Bacillariophyta algae. These algae comprise a mix of low, high and previously unknown DMSP producers[10]. Algae containing DSYE, particularly bloom-forming Pelagophyceae species, which we showed to accumulate medium-high intracellular DMSP levels, were globally more abundant DMSP producers than Haptophyta, Dinophyta and Bacillariophyta with DSYB and/or TpMMT. This highlights the potential importance of Pelagophyceae and other DSYE containing algae in global DMSP production and sulfur cycling.

Dimethylsulfoxonium propionate (DMSOP) is a recently identified and abundant marine organosulfur compound with purported roles in oxidative stress protection, global carbon and sulfur cycling1. Diverse algae and bacteria synthesise DMSOP from dimethylsulfoniopropionate (DMSP), which potentially limits the production of climate-active gases e.g., dimethylsulfide (DMS) generated from microbial DMSP cleavage1. Here, DMSOP was found at mM levels in saltmarsh sediment, >10-fold higher than DMSP, and orders of magnitude higher than DMSOP levels previously reported in seawater1. Moreover, we showed bacteria could utilise DMSOP as an osmoprotectant. Some bacteria also cleave DMSOP liberating dimethyl sulfoxide (DMSO), an ubiquitous marine metabolite and acrylate1, but the enzymes responsible and their environmental importance were unknown. Here, we elucidated the DMSOP cleavage mechanism/s in diverse heterotrophic bacteria, e.g., SAR11 clade and Roseobacters, and fungi and phototrophic algae, e.g., Emiliania huxleyi, not previously known to have this activity. All these diverse organisms utilised their DMSP lyase ‘Ddd’ or ‘Alma1’ enzymes, that span five protein families, to cleave DMSOP with similar specific activities to DMSP. Bacteria with DMSP lyases that used DMSP as a carbon source likewise used DMSOP. Furthermore, ddd gene transcription in these bacteria was induced by DMSOP, including dddK in SAR11 strain HTCC1062. We determined the structure of DddK bound to DMSOP and concluded that the catalytic mechanisms of DMSOP cleavage by Ddd enzymes were like those for DMSP. Given the predicted teragram DMSOP production budget1, its newly found abundance in marine sediments, and the abundance of microbial DMSP lyase genes and transcripts in marine environments, DMSOP cleavage is likely a globally significant process influencing global carbon and sulfur fluxes and marine ecological interactions.