Single-Cell Measurements of Marine Bacterial Transcription Reveal the Importance of Dimethylsulfoniopropionate (DMSP) Hotspots in Ocean Sulfur Cycling

Chemical transformations mediated by marine bacteria influence biogeochemical cycling processes over global scales, but are often governed by ecological interactions occurring at microscales which are difficult to study and quantify using conventional experimental methods. Here, we present the first single-cell measurements of the transcriptional response of marine bacteria to different concentrations of dimethylsulfoniopropionate (DMSP), a pivotal compound within ocean carbon and sulfur cycling and a key chemical currency in marine microbial interactions. We engineered fluorescent reporter strains of Ruegeria pomeroyi DSS-3, a bacterium that has the capacity to employ two competing DMSP catabolic pathways: demethylation (channeling carbon and sulfur into the microbial food web) and cleavage (producing dimethylsulfide (DMS), a gas responsible for the largest flux of biogenic sulfur from the ocean to the atmosphere). Time-resolved measurements of the expression of demethylation and cleavage pathways illustrated that external DMSP concentration dictates the relative expression of these two degradation pathways. Preferential expression of demethylation was observed at DMSP concentrations below 1 μM, with a gradual switch to the cleavage pathway as bacteria fulfill their sulfur requirements with increasing DMSP concentrations (>10 μM). Both pathways were upregulated in the presence of DMSP, but only at high concentrations (>1 μM for demethylation and >60 nM for cleavage) characteristic of hotspots, such as the vicinity of phytoplankton cells. In a spatially-resolved co-incubation experiment between DMSP-producing Symbiodiniaceae phytoplankton cells and engineered R. pomeroyi bacteria, increasing DMSP concentrations close to phytoplankton cells led to increasing cleavage pathway expression. This pattern indicates that bacterial exploitation of microscale chemical gradients of DMSP may be a profound determinant of the fate of carbon and sulfur in the pelagic ocean.