Single-cell bacterial transcription measurements reveal the importance of dimethylsulfoniopropionate (DMSP) hotspots in ocean sulfur cycling

Abstract

Dimethylsulfoniopropionate (DMSP) is a pivotal compound in marine biogeochemical cycles and a key chemical currency in microbial interactions. Marine bacteria transform DMSP via two competing pathways with considerably different biogeochemical implications: demethylation channels sulfur into the microbial food web, whereas cleavage releases sulfur into the atmosphere. Here, we present single-cell measurements of the expression of these two pathways using engineered fluorescent reporter strains of Ruegeria pomeroyi DSS-3, and find that external DMSP concentration dictates the relative expression of the two pathways. DMSP induces an upregulation of both pathways, but only at high concentrations (>1 μM for demethylation; >35 nM for cleavage), characteristic of microscale hotspots such as the vicinity of phytoplankton cells. Co-incubations between DMSP-producing microalgae and bacteria revealed an increase in cleavage pathway expression close to the microalgae's surface. These results indicate that bacterial utilization of microscale DMSP hotspots is an important determinant of the fate of sulfur in the ocean.

Uptake of Dimethylsulfoniopropionate (DMSP) by Natural Microbial Communities of the Great Barrier Reef (GBR), Australia

“…The relative abundances of the different DMSP degradation genes over time showed variable behaviours for the two locations. In agreement with the DLAb data, all degradation genes increased in relative abundance with time at the inner reef site, suggesting that sulfur demands were met quickly [27], after which cleavage to DMS dominated. For the outer reef site, the relative abundance of genes was higher in the DMSP-amended samples compared to the controls, indicating that the microbial community from the outer reef was partially advantaged by DMSP enrichment, but overall abundances declined over time.…”

“…KORDI-100, has been found to have a DMSP lyase gene [ 77 ]. Given that Prochlorococcus and SAR11 were present in high relative abundances at both sites, the fact that DMSP showed higher accumulated in the small fraction of the outer reef, suggests that rather than differences in microbial community composition, it was the metabolic state of the community driving this difference, whereby the bacterial community of the outer reef site were preferentially taking up DMSPd to meet their sulfur and carbon demands for growth [ 21 , 27 ]. Given the difference in depth of the two sites and therefore potentially different mixing regimes, the influence of mechanistic controls, such as UV-A dose [ 58 ], on the bacterial switch cannot be ruled out as a potential driver of the differences between sulfur demand for the two sites.…”

“…As such, we hypothesise that the DLAp measure in these GBR waters is likely attributable to the high DMSP-producing dinoflagellates that dominated the phytoplankton communities at both sites. For the bacterial fractions, the high rates of DLAb of the inner reef suggest that DMSP concentrations may have exceeded the necessary levels to cover the sulfur demands of the bacterioplankton community, and therefore much of the excess was cleaved to DMS [ 21 , 26 , 27 ]. In contrast, outside the reef, it is likely that most of the added DMSP was utilised to meet the sulfur demands of the bacterioplankton community.…”

“…The second pathway, known as the cleavage pathway [ 19 ], splits DMSP into the climatically active aerosol dimethyl sulfide (DMS) and acrylate, or other carbon-containing molecules depending on the Ddd derivative [ 24 , 25 ]. It has been hypothesised, in what has been termed the ‘bacterial switch’, that bacteria will preferentially utilise the demethylation pathway when there is a need to produce protein for growth, and once that demand is satisfied, they will switch to using the lyase pathway, catabolising the remaining DMSP to DMS [ 21 , 26 , 27 ]. This ‘switching’ mechanism has recently been shown to work concurrently rather than mutually exclusively in bacteria and is driven by DMSP availability [ 27 ], suggesting that both pathways can act in concert, but the relative reliance on each will differ depending on DMSP concentration and metabolic conditions.…”

How Do Quorum-Sensing Signals Mediate Algae–Bacteria Interactions?

“…Both this unique cohort of bacteria and physical properties of an alga cell forms the basis of the phycosphere: a unique microenvironment surrounding algae, which is distinct from the rest of the water column. It is within the phycosphere that the majority of interactions between algae and bacteria take place [ 14 ].…”