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Marine picocyanobacteria of the Prochlorococcus and Synechococcus genera have been longtime considered as autotrophic organisms. However, compelling evidence published over the last 15 years shows that these organisms can use different organic compounds containing key elements to survive in oligotrophic oceans, such as N (amino acids, amino sugars), S (dimethylsulfoniopropionate, DMSP), or P (ATP). Furthermore, marine picocyanobacteria can also take up glucose and use it as a source of carbon and energy, despite the fact that this compound is devoid of limiting elements and can also be synthesized by using standard metabolic pathways. This review will outline the main findings suggesting mixotrophy in the marine picocyanobacteria Prochlorococcus and Synechococcus , and its ecological relevance for these important primary producers.

Unicellular algae, termed phytoplankton, greatly impact the marine environment by serving as the basis of marine food webs and by playing central roles in the biogeochemical cycling of elements. The interactions between phytoplankton and heterotrophic bacteria affect the fitness of both partners. It is becoming increasingly recognized that metabolic exchange determines the nature of such interactions, but the underlying molecular mechanisms remain underexplored. Here, we investigated the molecular and metabolic basis for the bacterial lifestyle switch, from coexistence to pathogenicity, in Sulfitobacter D7 during its interaction with Emiliania huxleyi , a cosmopolitan bloom-forming phytoplankter. To unravel the bacterial lifestyle switch, we analyzed bacterial transcriptomes in response to exudates derived from algae in exponential growth and stationary phase, which supported the Sulfitobacter D7 coexistence and pathogenicity lifestyles, respectively. In pathogenic mode, Sulfitobacter D7 upregulated flagellar motility and diverse transport systems, presumably to maximize assimilation of E. huxleyi -derived metabolites released by algal cells upon cell death. Algal dimethylsulfoniopropionate (DMSP) was a pivotal signaling molecule that mediated the transition between the lifestyles, supporting our previous findings. However, the coexisting and pathogenic lifestyles were evident only in the presence of additional algal metabolites. Specifically, we discovered that algae-produced benzoate promoted the growth of Sulfitobacter D7 and hindered the DMSP-induced lifestyle switch to pathogenicity, demonstrating that benzoate is important for maintaining the coexistence of algae and bacteria. We propose that bacteria can sense the physiological state of the algal host through changes in the metabolic composition, which will determine the bacterial lifestyle during interaction.

The ability of marine bacteria to direct their movement in response to chemical gradients influences inter-species interactions, nutrient turnover, and ecosystem productivity. While many bacteria are chemotactic towards small metabolites, marine organic matter is predominantly composed of large molecules and polymers. Yet, the signalling role of these large molecules is largely unknown. Using in situ and laboratory-based chemotaxis assays, we show that marine bacteria are strongly attracted to the abundant algal polysaccharides laminarin and alginate. Unexpectedly, these polysaccharides elicited stronger chemoattraction than their oligo- and monosaccharide constituents. Furthermore, chemotaxis towards laminarin was strongly enhanced by dimethylsulfoniopropionate (DMSP), another ubiquitous algal-derived metabolite. Our results indicate that DMSP acts as a methyl donor for marine bacteria, increasing their gradient detection capacity and facilitating their access to polysaccharide patches. We demonstrate that marine bacteria are capable of strong chemotaxis towards large soluble polysaccharides and uncover a new ecological role for DMSP in enhancing this attraction. These navigation behaviours may contribute to the rapid turnover of polymers in the ocean, with important consequences for marine carbon cycling. The ability of marine bacteria to direct their movement in response to chemical gradients influences inter-species interactions, nutrient turnover, and ecosystem productivity. Here, Clerc et al. show that marine bacteria are strongly attracted to algal polysaccharides, and this chemotactic behaviour is enhanced by dimethylsulfoniopropionate (DMSP), a ubiquitous algal metabolite.

Algae produce massive amounts of dimethylsulfoniopropionate (DMSP), which fuel the organosulfur cycle 1 , 2 . On a global scale, several petagrams of this sulfur species are produced annually, thereby driving fundamental processes and the marine food web 1 . An important DMSP transformation product is dimethylsulfide, which can be either emitted to the atmosphere 3 , 4 or oxidized to dimethylsulfoxide (DMSO) and other products 5 . Here we report the discovery of a structurally unusual metabolite, dimethylsulfoxonium propionate (DMSOP), that is synthesized by several DMSP-producing microalgae and marine bacteria. As with DMSP, DMSOP is a low-molecular-weight zwitterionic metabolite that carries both a positively and a negatively charged functional group. Isotope labelling studies demonstrate that DMSOP is produced from DMSP, and is readily metabolized to DMSO by marine bacteria. DMSOP was found in near nanomolar amounts in field samples and in algal culture media, and thus represents—to our knowledge—a previously undescribed biogenic source for DMSO in the marine environment. The estimated annual oceanic production of oxidized sulfur from this pathway is in the teragram range, similar to the calculated dimethylsulfide flux to the atmosphere 3 . This sulfoxonium metabolite is therefore a key metabolite of a previously undescribed pathway in the marine sulfur cycle. These findings highlight the importance of DMSOP in the marine organosulfur cycle. A structurally unusual zwitterionic metabolite, dimethylsulfoxonium propionate (DMSOP), is synthesized by several dimethylsulfoniopropionate-producing microalgae and marine bacteria and is readily metabolized into dimethylsulfoxide by marine bacteria, expanding our knowledge of the marine organosulfur cycle.

Unlike biologically available nitrogen and phosphorus, which are often at limiting concentrations in surface seawater, sulfur in the form of sulfate is plentiful and not considered to constrain marine microbial activity. Nonetheless, in a model system in which a marine bacterium obtains all of its carbon from co-cultured phytoplankton, bacterial gene expression suggests that at least seven dissolved organic sulfur (DOS) metabolites support bacterial heterotrophy. These labile exometabolites of marine dinoflagellates and diatoms include taurine, N -acetyltaurine, isethionate, choline-O-sulfate, cysteate, 2,3-dihydroxypropane-1-sulfonate (DHPS), and dimethylsulfoniopropionate (DMSP). Leveraging from the compounds identified in this model system, we assessed the role of sulfur metabolites in the ocean carbon cycle by mining the Tara Oceans dataset for diagnostic genes. In the 1.4 million bacterial genome equivalents surveyed, estimates of the frequency of genomes harboring the capability for DOS metabolite utilization ranged broadly, from only 1 out of every 190 genomes (for the C2 sulfonate isethionate) to 1 out of every 5 (for the sulfonium compound DMSP). Bacteria able to participate in DOS transformations are dominated by Alphaproteobacteria in the surface ocean, but by SAR324, Acidimicrobiia, and Gammaproteobacteria at mesopelagic depths, where the capability for utilization occurs in higher frequency than in surface bacteria for more than half the sulfur metabolites. The discovery of an abundant and diverse suite of marine bacteria with the genetic capacity for DOS transformation argues for an important role for sulfur metabolites in the pelagic ocean carbon cycle.

The oxidation of dimethyl sulfide (DMS; CH3SCH3), emitted from the surface ocean, contributes to the formation of Aitken mode particles and their growth to cloud condensation nuclei (CCN) sizes in remote marine environments. It is not clear whether other less commonly measured marine-derived, sulfur-containing gases share similar dynamics to DMS and contribute to secondary marine aerosol formation. Here, we present measurements of gas-phase volatile organosulfur molecules taken with a Vocus proton-transfer-reaction high-resolution time-of-flight mass spectrometer during a mesocosm phytoplankton bloom experiment using coastal seawater. We show that DMS, methanethiol (MeSH; CH3SH), and benzothiazole (C7H5NS) account for on average over 90 % of total gas-phase sulfur emissions, with non-DMS sulfur sources representing 36.8 ± 7.7 % of sulfur emissions during the first 9 d of the experiment in the pre-bloom phase prior to major biological growth, before declining to 14.5 ± 6.0 % in the latter half of the experiment when DMS dominates during the bloom and decay phases. The molar ratio of DMS to MeSH during the pre-bloom phase (DMS : MeSH = 4.60 ± 0.93) was consistent with the range of previously calculated ambient DMS-to-MeSH sea-to-air flux ratios. As the experiment progressed, the DMS to MeSH emission ratio increased significantly, reaching 31.8 ± 18.7 during the bloom and decay. Measurements of dimethylsulfoniopropionate (DMSP), heterotrophic bacteria, and enzyme activity in the seawater suggest the DMS : MeSH ratio is a sensitive indicator of the bacterial sulfur demand and the composition and magnitude of available sulfur sources in seawater. The evolving DMS : MeSH ratio and the emission of a new aerosol precursor gas, benzothiazole, have important implications for secondary sulfate formation pathways in coastal marine environments.

Prochlorococcus and SAR11 are among the smallest and most abundant organisms on Earth. With a combined global population of about 2.7 × 10 28 cells, they numerically dominate bacterioplankton communities in oligotrophic ocean gyres and yet they have never been grown together in vitro. Here we describe co-cultures of Prochlorococcus and SAR11 isolates representing both high- and low-light adapted clades. We examined: (1) the influence of Prochlorococcus on the growth of SAR11 and vice-versa, (2) whether Prochlorococcus can meet specific nutrient requirements of SAR11, and (3) how co-culture dynamics vary when Prochlorococcus is grown with SAR11 compared with sympatric copiotrophic bacteria. SAR11 grew 15–70% faster in co-culture with Prochlorococcus , while the growth of the latter was unaffected. When Prochlorococcus populations entered stationary phase, this commensal relationship rapidly became amensal, as SAR11 abundances decreased dramatically. In parallel experiments with copiotrophic bacteria; however, the heterotrophic partner increased in abundance as Prochlorococcus densities leveled off. The presence of Prochlorococcus was able to meet SAR11’s central requirement for organic carbon, but not reduced sulfur. Prochlorococcus strain MIT9313, but not MED4, could meet the unique glycine requirement of SAR11, which could be due to the production and release of glycine betaine by MIT9313, as supported by comparative genomic evidence. Our findings also suggest, but do not confirm, that Prochlorococcus MIT9313 may compete with SAR11 for the uptake of 3-dimethylsulfoniopropionate (DMSP). To give our results an ecological context, we assessed the relative contribution of Prochlorococcus and SAR11 genome equivalents to those of identifiable bacteria and archaea in over 800 marine metagenomes. At many locations, more than half of the identifiable genome equivalents in the euphotic zone belonged to Prochlorococcus and SAR11 – highlighting the biogeochemical potential of these two groups.

Symbiodiniaceae form associations with extra- and intracellular bacterial symbionts, both in culture and in symbiosis with corals. Bacterial associates can regulate Symbiodiniaceae fitness in terms of growth, calcification and photophysiology. However, the influence of these bacteria on interactive stressors, such as temperature and light, which are known to influence Symbiodiniaceae physiology, remains unclear. Here, we examined the photophysiological response of two Symbiodiniaceae species ( Symbiodinium microadriaticum and Breviolum minutum ) cultured under acute temperature and light stress with specific bacterial partners from their microbiome ( Labrenzia ( Roseibium ) alexandrii , Marinobacter adhaerens or Muricauda aquimarina ). Overall, bacterial presence positively impacted Symbiodiniaceae core photosynthetic health (photosystem II [PSII] quantum yield) and photoprotective capacity (non-photochemical quenching; NPQ) compared to cultures with all extracellular bacteria removed, although specific benefits were variable across Symbiodiniaceae genera and growth phase. Symbiodiniaceae co-cultured with M. aquimarina displayed an inverse NPQ response under high temperatures and light, and those with L. alexandrii demonstrated a lowered threshold for induction of NPQ, potentially through the provision of antioxidant compounds such as zeaxanthin (produced by Muricauda spp . ) and dimethylsulfoniopropionate (DMSP; produced by this strain of L. alexandrii ). Our co-culture approach empirically demonstrates the benefits bacteria can deliver to Symbiodiniaceae photochemical performance, providing evidence that bacterial associates can play important functional roles for Symbiodiniaceae.

Oleaginous microalgae are considered as a promising resource for the production of biofuels. Especially diatoms arouse interest as biofuel producers since they are most productive in carbon fixation and very flexible to environmental changes in the nature. Naturally, triacylglycerol (TAG) accumulation in algae only occurs under stress conditions like nitrogen-limitation. We focused on Phaeodactylum strain Pt4 (UTEX 646), because of its ability to grow in medium with low salinity and therefore being suited when saline water is less available or for wastewater cultivation strategies. Our data show an increase in neutral lipids during nitrogen-depletion and predominantly 16:0 and 16:1(n-7) accumulated in the TAG fraction. The molecular species composition of TAG suggests a remodeling primarily from the betaine lipid diacylglyceroltrimethylhomoserine (DGTS), but a contribution of the chloroplast galactolipid monogalactosyldiacylglycerol (MGDG) cannot be excluded. Interestingly, the acyl-CoA pool is rich in 20:5(n-3) and 22:6(n-3) in all analyzed conditions, but these fatty acids are almost excluded from TAG. Other metabolites most obviously depleted under nitrogen-starvation were amino acids, lyso-phospholipids and tricarboxylic acid (TCA) cycle intermediates, whereas sulfur-containing metabolites as dimethylsulfoniopropionate, dimethylsulfoniobutyrate and methylsulfate as well as short acyl chain carnitines, propanoyl-carnitine and butanoyl-carnitine increased upon nitrogen-starvation. Moreover, the Calvin cycle may be de-regulated since sedoheptulose accumulated after nitrogen-depletion. Together the data provide now the basis for new strategies to improve lipid production and storage in Phaeodactylum strain Pt4.

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. DMSP is a ubiquitous organosulfur compound in the ocean that, once degraded by bacteria, plays key roles in global biogeochemical cycles and climate regulation. Here, the authors use single-cell measurements of transcription to investigate the intricate dynamics of bacterial DMSP degradation.