Every year microorganisms in Earth’s oceans, their margins and marine sediments make over eight billion tonnes of the sulfurous anti-stress molecule dimethylsulfoniopropionate (DMSP) to cope with environmental stresses encountered in their habitat, including high salinity, low temperatures and oxidative stress. When DMSP is released from these organisms into the environment, it constitutes an important signalling molecule and nutrient source for diverse marine microbes through catabolic pathways. This catabolism yields >300 million tonnes of the climate-cooling gas and signalling molecule dimethylsulfide (DMS) via DMSP lyase enzymes and methanethiol through DMSP demethylation.
Recently, another marine organosulfur compound called dimethylsulfoxonium propionate (DMSOP) was discovered and shown to be made in million tonne quantities from the microbial oxidation of DMSP1. Critically, when DMSP is oxidised to DMSOP, it cannot be cleaved to DMS. Instead, a few marine bacterial strains and algae were reported to cleave DMSOP to generate the ubiquitous metabolite dimethylsulfoxide (DMSO), via unknown mechanisms, in a novel step of the marine sulfur cycle. Thus, a significant consequence of DMSOP synthesis is that it potentially limits the release of climate-cooling DMS from DMSP – a phenomenon not considered in models for the global production and effects of this important gas.
In this study, we used functional genomics to establish that the model bacterium Alcaligenes faecalis used its DMSP lyase DddY as the major enzyme to cleave DMSOP and generate DMSO and acrylate. Next, we examined the DMSOP lyase activity of all the other known bacterial and eukaryotic DMSP lyases and showed that DMSOP cleavage is a universal trait for these very diverse enzymes. Thus, this work vastly expanded the known diversity of DMSOP degraders – from being confined to a few bacterial strains to being present in the most abundant groups of marine bacteria (SAR11 and Roseobacters), eukaryotic algae, and pathogenic fungi. We also solved the crystal structures of DMSP lyases in complex with DMSOP and discovered that these enzymes use a similar catalytic mechanism to cleave both DMSP and DMSOP.
Next, we deciphered physiological roles for this novel organosulfur compound in microbes that produce or accumulate it. We showed that important groups of marine bacteria i.e. Oceanospirillales and SAR11, used DMSOP as sole carbon and/or sulfur source for growth and that the expression of their DMSP lyases-encoding genes was induced by this substrate. In addition to its previously proposed function as antioxidant, we demonstrated that DMSOP could confer osmotolerance to salinity conditions typical of seawater.
Knowing the enzymes involved in DMSP and now DMSOP cleavage, enabled us to study the abundance, diversity and biogeography of microorganisms potentially degrading these organosulfur compounds in diverse environments. We found that a good proportion of eukaryotes and bacteria in Earth’s oceans and marine sediments contain and express these lyases genes, suggesting that the cleavage of DMSP and DMSOP are likely significant processes in marine sulfur cycling. A major limiting factor is the availability of DMSOP in marine systems, where DMSP is generally far more abundant than its oxygenated product. However, in this study we established an unappreciated abundance of DMSOP in marine sediment environments, particularly saltmarshes, which contained DMSOP levels above those for DMSP and were orders of magnitude higher than concentrations in seawater. This work highlighted that DMSOP synthesis and degradation are likely prevalent in marine sediments and that the previously predicted annual million tonne DMSOP budget is vastly underestimated. In conclusion, DMSOP cycling is likely a significant process influencing carbon and sulfur cycles and ecological interactions.
This exciting new work identifying who, how, why and where marine microbes use the recently discovered organosulfur compound DMSOP, it is fruit of an international collaboration between scientists from diverse disciplines including molecular microbiology, evolutionary ecology, protein structure and biochemistry, bioinformatics and analytical science. These findings constitute the basis for Dr. Ornella Carrión’s fellowship application to continue advancing our understanding of the cycling and environmental magnitude of DMSOP and it is potential effects on DMSP/DMS fluxes and climate.
1. Thume, K. et al. The metabolite dimethylsulfoxonium propionate extends the marine organosulfur cycle. Nature. 563, 412-415 (2018).