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.