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 B 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.

Dimethylsulfoniopropionate (DMSP) is an important labile component of the marine dissolved organic matter pool that is produced by the majority of eukaryotic marine phytoplankton and by many prokaryotes. Despite decades of research, the contribution of different environmental drivers of DMSP production to regional and seasonal variability remains unknown. A synthesis of the current state‐of‐knowledge suggested that approximately half of confirmed DMSP producers are low producers (intracellular DMSP < 50 mM). Low DMSP producers (LoDPs; e.g., diatoms) were shown to strongly regulate intracellular DMSP concentrations (~ 16‐fold change) as a predictable function of nutrient stress. By comparison, high DMSP producers (HiDPs; e.g., coccolithophores) showed very little response (~ 1.5‐fold change). To assess the importance of differential DMSP production by low and high producers, DMSP concentrations were predicted for two time‐series sites (a high‐ and low‐productivity site) and for the global ocean by explicitly incorporating both community composition and mechanistic nutrient stress. Despite large, predictable intracellular DMSP changes, low producers contributed less than 5% to global DMSP. This indicates that, while variations in DMSP production by low producers could be important for predicting microbial interactions and low producer physiology, it is not necessary for predicting global DMSP concentrations. Our analysis suggests that community composition, particularly HiDP biomass, is the dominant driver of variability in in situ DMSP concentrations, even in low‐productivity regions where high producers are typically the subdominant group. Accurate predictions of in situ DMSP concentrations require improved representation of subdominant community dynamics in ecosystem models and remote‐sensing algorithms.

Concentrations of dimethylsulfoniopropionate (DMSP), dimethylsulfide (DMS), and DMS flux are reported for the Great Barrier Reef (GBR), Great Barrier Reef Lagoon (GBRL), and Coral Sea. Generally higher concentrations of dimethylsulfoniopropionate and DMS occurred in coral reef waters, compared with GBRL concentrations. DMS flux from GBR coral reefs in summer ranged from nondetectable to 153 μmol m−2 d−1 (mean 6.4), while winter fluxes ranged from 0.02 to 15 μmol m−2 d−1 (mean 2.4). No significant seasonal difference in DMS flux occurred for the GBRL. High DMSw concentrations and DMS fluxes periodically occur at coral reefs during very low tides and elevated sea surface temperatures (SSTs). For the GBRL and GBR coral reefs there was a significant correlation between seawater DMSw concentrations and SST (p < 0.001), up to temperatures of 30 °C. During coral bleaching DMS flux from reefs almost completely shuts down when SSTs are >30 °C. The GBRL and associated coral reefs emit 439 and 32 MmolS per year, respectively. Cyclones on average produce 170 MmolS to the GBR atmosphere in summer. This amount can markedly increase during severe cyclones such as severe tropical Cyclone Debbie in March 2017. Overall, the annual DMS emission estimate from the GBRL and coral reefs in the GBR is 0.64 GmolS, with cyclones contributing 27% or greater of the annual emission estimate, depending on the cyclone intensity. Oxidation of atmospheric DMS can potentially affect solar radiation, SSTs, low‐level cloud cover, and rainfall causing cooling and warming of the climate in the GBR region as recent modeling predicts.

The production and consumption of organic matter by marine organisms plays a central role in the marine carbon cycle. Labile organic compounds (metabolites) are the major currency of energetic demands and organismal interaction, but these compounds remain elusive because of their rapid turnover and concomitant minuscule concentrations in the dissolved organic matter pool. Organic osmolytes are a group of small metabolites synthesized at high intracellular concentrations (mM) to regulate cellular osmolarity and have the potential to be released as abundant dissolved substrates. Osmolytes may represent an essential currency of exchange among heterotrophic prokaryotes and primary and secondary producers in marine food webs. For example, the well-known metabolite dimethylsulfoniopropionate (DMSP) is used as an osmolyte by some phytoplankton and can be subsequently metabolized by 60% of the marine bacterial community, supplying up to 13% of the bacterial carbon demand and 100% of the bacterial sulfur demand. While marine osmolytes have been studied for decades, our understanding of their cycling and significance within microbial communities is still far from comprehensive. Here, we surveyed the genes responsible for synthesis, breakdown, and transport of 14 key osmolytes. We systematically searched for these genes across marine bacterial genomes (n = 897) and protistan transcriptomes (n = 652) using homologous protein profiles to investigate the potential for osmolyte metabolisms. Using the pattern of gene presence and absence, we infer the metabolic potential of surveyed microbes to interact with each osmolyte. Specifically, we identify: (1) complete pathways for osmolyte synthesis in both prokaryotic and eukaryotic marine microbes, (2) microbes capable of transporting osmolytes but lacking complete synthesis and/or breakdown pathways, and (3) osmolytes whose synthesis and/or breakdown appears to be specialized and is limited to a subset of organisms. The analysis clearly demonstrates that the marine microbial loop has the genetic potential to actively recycle osmolytes and that this abundant group of small metabolites may function as a significant source of nutrients through exchange among diverse microbial groups that significantly contribute to the cycling of labile carbon.

Summary 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.