Dimethylsulphoniopropionate (DMSP) is one of the Earth’s most abundant organosulphur molecules, a signalling molecule, a key nutrient for marine microorganisms, and the major precursor for gaseous dimethyl sulphide (DMS). DMS, another infochemical in signalling pathways, is important in global sulphur cycling2, and affects the Earth’s albedo, and potentially climate, via sulphate aerosol and cloud condensation nuclei production. It was thought that only eukaryotes produce significant amounts of DMSP, but here we demonstrate that many marine heterotrophic bacteria also produce DMSP, likely using the same methionine (Met) transamination pathway as macroalgae and phytoplankton10. We identify the first DMSP synthesis gene in any organism, dsyB, which encodes the key methyltransferase enzyme of this pathway and is a reliable reporter for bacterial DMSP synthesis in marine alphaproteobacteria. DMSP production and dsyB transcription are upregulated by increased salinity, nitrogen limitation and lower temperatures in our model DMSP-producing bacterium Labrenzia aggregata LZB033. With significant numbers of dsyB homologues in marine metagenomes, we propose that bacteria likely make a significant contribution to oceanic DMSP production. Furthermore, since DMSP production is not solely associated with obligate phototrophs, the process need not be confined to the photic zones of marine environments, and as such may have been underestimate
Dimethylsulfoniopropionate (DMSP) is a globally important organosulfur molecule and the major precursor for dimethyl sulfide. These compounds are important info-chemicals, key nutrients for marine microorganisms, and are involved in global sulfur cycling, atmospheric chemistry and cloud formation. DMSP production was thought to be confined to eukaryotes, but heterotrophic bacteria can also produce DMSP through the pathway used by most phytoplankton , and the DsyB enzyme catalysing the key step of this pathway in bacteria was recently identified . However, eukaryotic phytoplankton probably produce most of Earth's DMSP, yet no DMSP biosynthesis genes have been identified in any such organisms. Here we identify functional dsyB homologues, termed DSYB, in many phytoplankton and corals. DSYB is a methylthiohydroxybutryate methyltransferase enzyme localized in the chloroplasts and mitochondria of the haptophyte Prymnesium parvum, and stable isotope tracking experiments support these organelles as sites of DMSP synthesis. DSYB transcription levels increased with DMSP concentrations in different phytoplankton and were indicative of intracellular DMSP. Identification of the eukaryotic DSYB sequences, along with bacterial dsyB, provides the first molecular tools to predict the relative contributions of eukaryotes and prokaryotes to global DMSP production. Furthermore, evolutionary analysis suggests that eukaryotic DSYB originated in bacteria and was passed to eukaryotes early in their evolution.
Dimethylsulfoniopropionate (DMSP) and its catabolite dimethyl sulfide (DMS) are key marine nutrients 1,2 , with roles in global sulfur cycling 2 , atmospheric chemistry 3 , signalling 4,5 and, potentially, climate regulation 6,7. DMSP production was previously thought to be an oxic and photic process, mainly confined to the surface oceans. 2 However, here we show that DMSP concentrations and DMSP/DMS synthesis rates were higher in surface marine sediment from e.g., saltmarsh ponds, estuaries and the deep ocean than in the overlying seawater. A quarter of bacterial strains isolated from saltmarsh sediment produced DMSP (up to 73 mM), and previously unknown DMSPproducers were identified. Most DMSP-producing isolates contained dsyB 8 , but some alphaproteobacteria, gammaproteobacteria and actinobacteria utilised a methionine methylation pathway independent of DsyB, previously only associated with higher plants. These bacteria contained a methionine methyltransferase 'mmtN' gene-a marker for bacterial DMSP synthesis via this pathway. DMSP-producing bacteria and their dsyB and/or mmtN transcripts were present in all tested seawater samples and Tara Oceans bacterioplankton datasets, but were far more abundant in marine surface sediment. Approximately 10 8 bacteria per gram of surface marine sediment are predicted to produce DMSP, and their contribution to this process should be included in future models of global DMSP production. We propose that coastal and marine sediments, which cover a large part of the Earth's surface, are environments with high DMSP and DMS productivity, and that bacteria are important producers within them. Approximately eight billion tonnes of DMSP is produced by phytoplankton in the Earth's surface oceans annually 9. However, surface sediment from saltmarsh ponds, an estuary and the deep ocean (with high pressures and no light) contained DMSP levels (5-128 nmol DMSP g-1) that were up to ~three orders of magnitude higher than the overlying seawater (0.01-0.70 nmol DMSP ml-1) (Fig. 1a-b, Supplementary Tables 1a and 2), a phenomenon also observed in 10,11. DMSP concentration decreased with depth, being much lower in anoxic sediment, but even in deeper sediments the concentration was approximately an order of magnitude higher than in the overlying seawater (Supplementary Table 1a). This study focused on DMSP synthesis in coastal surface sediments, where DMSP concentrations were highest. The
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