DMSP synthesis genes distinguish two types of DMSP producer phenotypes.

Dimethylsulfoniopropionate (DMSP) is an important organic carbon and sulfur source in the surface ocean that fuels microbial activity and significantly impacts Earth's climate. After three decades of research, the cellular role(s) of DMSP and environmental drivers of production remain enigmatic. Recent work suggests that cellular DMSP concentrations, and changes in these concentrations in response to environmental stressors, define two major groups of DMSP producers: high DMSP producers that contain ≥ 50 mM intracellular DMSP and low DMSP producers that contain < 50 mM. Here we show that two recently described DMSP synthesis genes (DSYB and TpMT2) may differentiate these two DMSP phenotypes. A survey of prokaryotic and eukaryotic isolates found a significant correlation between the presence of DSYB and TpMT2 genes and previous measurements of high and low DMSP concentrations, respectively. Phylogenetic analysis demonstrated that DSYB and TpMT2 form two distinct clades. DSYB and TpMT2 were also found to be globally abundant in in situ surface communities, and their taxonomic annotations were similar to those observed for isolates. The strong correlation of the DSYB and TpMT2 synthesis genes with high and low producer phenotypes establishes a foundation for direct quantification of DMSP producers, enabling significantly improved predictions of DMSP in situ.

Evidence for contrasting roles of dimethylsulfoniopropionate production in Emiliania huxleyi and Thalassiosira oceanica.

Dimethylsulfoniopropionate (DMSP) is a globally abundant marine metabolite and a significant source of organic carbon and sulfur for marine microbial ecosystems with the potential to influence climate regulation. However, the physiological function of DMSP has remained enigmatic for >30 yr. Recent insight suggests that there are different physiological roles for DMSP based on the cellular DMSP concentrations in producers. Differential production of DMSP was tested with multiple physiological experiments that altered nitrate availability, salinity and temperature to create stressed growth and target different metabolic conditions in Emiliania huxleyi, a high DMSP producer and Thalassiosira oceanica, a low DMSP producer. Emiliania huxleyi intracellular DMSP did not respond to metabolically imbalanced conditions, while Thalassiosira oceanica intracellular DMSP was significantly correlated to stressed growth rate across all conditions tested and exhibited a plastic response on a timescale of hours in nonsteady-state. The previous assumption that proposed DMSP mechanism(s) can be universally applied to all producers is shown to be unlikely. Rather, two distinct ecological roles for DMSP likely exist that differ by producer type, where: (1) the primary role of DMSP in high producers is a constitutive compatible solute; and (2) DMSP production in low producers is a finely tuned stress response.

The Microbiological Drivers of Temporally Dynamic Dimethylsulfoniopropionate Cycling Processes in Australian Coastal Shelf Waters.

The organic sulfur compounds dimethylsulfoniopropionate (DMSP) and dimethyl sulfoxide (DMSO) play major roles in the marine microbial food web and have substantial climatic importance as sources and sinks of dimethyl sulfide (DMS). Seasonal shifts in the abundance and diversity of the phytoplankton and bacteria that cycle DMSP are likely to impact marine DMS (O) (P) concentrations, but the dynamic nature of these microbial interactions is still poorly resolved. Here, we examined the relationships between microbial community dynamics with DMS (O) (P) concentrations during a 2-year oceanographic time series conducted on the east Australian coast. Heterogenous temporal patterns were apparent in chlorophyll a (chl a) and DMSP concentrations, but the relationship between these parameters varied over time, suggesting the phytoplankton and bacterial community composition were affecting the net DMSP concentrations through differential DMSP production and degradation. Significant increases in DMSP were regularly measured in spring blooms dominated by predicted high DMSP-producing lineages of phytoplankton (Heterocapsa, Prorocentrum, Alexandrium, and Micromonas), while spring blooms that were dominated by predicted low DMSP-producing phytoplankton (Thalassiosira) demonstrated negligible increases in DMSP concentrations. During elevated DMSP concentrations, a significant increase in the relative abundance of the key copiotrophic bacterial lineage Rhodobacterales was accompanied by a three-fold increase in the gene, encoding the first step of DMSP demethylation (dmdA). Significant temporal shifts in DMS concentrations were measured and were significantly correlated with both fractions (0.2-2 µm and >2 µm) of microbial DMSP lyase activity. Seasonal increases of the bacterial DMSP biosynthesis gene (dsyB) and the bacterial DMS oxidation gene (tmm) occurred during the spring-summer and coincided with peaks in DMSP and DMSO concentration, respectively. These findings, along with significant positive relationships between dsyB gene abundance and DMSP, and tmm gene abundance with DMSO, reinforce the significant role planktonic bacteria play in producing DMSP and DMSO in ocean surface waters. Our results highlight the highly dynamic nature and myriad of microbial interactions that govern sulfur cycling in coastal shelf waters and further underpin the importance of microbial ecology in mediating important marine biogeochemical processes.

Biogeographical and seasonal dynamics of the marine Roseobacter community and ecological links to DMSP-producing phytoplankton.

Ecological interactions between marine bacteria and phytoplankton play a pivotal role in governing the ocean's major biogeochemical cycles. Among these, members of the marine Roseobacter Group (MRG) can establish mutualistic relationships with phytoplankton that are, in part, maintained by exchanges of the organosulfur compound, dimethylsulfoniopropionate (DMSP). Yet most of what is known about these interactions has been derived from culture-based laboratory studies. To investigate temporal and spatial co-occurrence patterns between members of the MRG and DMSP-producing phytoplankton we analysed 16S and 18S rRNA gene amplicon sequence variants (ASVs) derived from 5 years of monthly samples from seven environmentally distinct Australian oceanographic time-series. The MRG and DMSP-producer communities often displayed contemporaneous seasonality, which was greater in subtropical and temperate environments compared to tropical environments. The relative abundance of both groups varied latitudinally, displaying a poleward increase, peaking (MRG at 33% of total bacteria, DMSP producers at 42% of eukaryotic phototrophs) during recurrent spring-summer phytoplankton blooms in the most temperate site (Maria Island, Tasmania). Network analysis identified 20,140 significant positive correlations between MRG ASVs and DMSP producers and revealed that MRGs exhibit significantly stronger correlations to high DMSP producers relative to other DMSP-degrading bacteria (Pelagibacter, SAR86 and Actinobacteria). By utilising the power of a continental network of oceanographic time-series, this study provides in situ confirmation of interactions found in laboratory studies and demonstrates that the ecological dynamics of an important group of marine bacteria are shaped by the production of an abundant and biogeochemically significant organosulfur compound.

The Trichodesmium consortium: conserved heterotrophic co-occurrence and genomic signatures of potential interactions.

The nitrogen (N)-fixing cyanobacterium Trichodesmium is globally distributed in warm, oligotrophic oceans, where it contributes a substantial proportion of new N and fuels primary production. These photoautotrophs form macroscopic colonies that serve as relatively nutrient-rich substrates that are colonized by many other organisms. The nature of these associations may modulate ocean N and carbon (C) cycling, and can offer insights into marine co-evolutionary mechanisms. Here we integrate multiple omics-based and experimental approaches to investigate Trichodesmium-associated bacterial consortia in both laboratory cultures and natural environmental samples. These efforts have identified the conserved presence of a species of Gammaproteobacteria (Alteromonas macleodii), and enabled the assembly of a near-complete, representative genome. Interorganismal comparative genomics between A. macleodii and Trichodesmium reveal potential interactions that may contribute to the maintenance of this association involving iron and phosphorus acquisition, vitamin B12 exchange, small C compound catabolism, and detoxification of reactive oxygen species. These results identify what may be a keystone organism within Trichodesmium consortia and support the idea that functional selection has a major role in structuring associated microbial communities. These interactions, along with likely many others, may facilitate Trichodesmium's unique open-ocean lifestyle, and could have broad implications for oligotrophic ecosystems and elemental cycling.