Predicted shifts in bacterial and algal contributions to DMSP and DMS dynamics during a coastal spring-summer bloom

Ubiquitous marine microalgae and bacteria produce the abundant organosulfur compound dimethylsulfoniopropionate (DMSP) and/or catabolize it to climate-active gases, such as dimethylsulfide (DMS), with major consequences for global biogeochemistry and climate. However, their relative and dynamic roles in DMSP synthesis and catabolism remain poorly resolved, particularly during natural bloom events. Here, we combined metagenomics and metatranscriptomics, with measurements of intracellular/particulate DMSP (DMSPp), DMS concentrations, and DMSPp production rates, as well as microscopy and flow cytometry, to predict the key microbes and enzymes driving DMSP/DMS dynamics during a spring-summer bloom in the Western English Channel. Microalgae and bacteria expressing the DMSP synthesis genes DSYB/DSYE and dsyB were likely major and significant DMSP producers, respectively, except during the largest observed DMSP spike. This spike coincided with elevated Synechococcus and autotrophic flagellate biomass but minimal DMSP synthesis gene expression. Axenic Synechococcus strains contained no detectable DMSP, implying that flagellates with novel DMSP synthesis genes were likely responsible. Microbial DMSP import potential far exceeded catabolism, suggesting strong selection for DMSP uptake. Bacteria were the major predicted DMSP degraders, with DMSP demethylation potential dwarfing cleavage. However, the highest DMS concentrations were linked to Haptophyta expressing the DMSP lyase gene Alma, implying the significance of algal DMSP cleavage. Methanethiol-dependent DMS production was also likely important, with bacterial mddH transcripts coinciding with another major DMS spike. Overall, these results imply dynamic and contrasting roles of microalgae and bacteria, and their pathways, in coastal DMSP/DMS and sulfur cycling.