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ABSTRACT A large annual carbon flux occurs through the surface ocean’s labile dissolved organic carbon (DOC) pool, with influx dominated by phytoplankton-derived metabolites and outflux by heterotrophic bacterioplankton uptake. We addressed the dynamics of this carbon flow between microbial primary and secondary producers through analysis of theThalassiosira pseudonanaCCMP1335 endometabolome, a proxy for the labile DOC released upon phytoplankton lysis, as temperature and bacterial presence were altered. Diatom strains acclimated at one of three different temperatures (14°C, 20°C, or 28°C) were cultured either axenically or with the bacteriumRuegeria pomeroyiDSS-3, and their endometabolites analyzed by NMR. Median concentration variation between conditions was ~1.5-fold across all identified endometabolites. Those with roles as osmolytes varied most, exhibiting concentration differences up to 170-fold across conditions with the largest variations triggered by the presence/absence of the heterotrophic bacterium. Differential expression observed for diatom metabolite synthesis pathways suggested changes in synthesis rates as a mechanism for endometabolome remodeling. Consistent with expectations of high turnover by heterotrophic bacteria, endometabolite mean lifetimes in a DOC pool were <2 h to 12 h. IMPORTANCEThe role of labile DOC in the transfer of marine carbon between phytoplankton and heterotrophic bacteria was first recognized 40 years ago, yet the identity and dynamics of phytoplankton metabolites entering the labile DOC pool are still poorly known. Using metabolome and transcriptome profiling, we found highly variable composition and concentration of diatom endometabolites, depending on growth conditions and arising over time frames as short as a single growth cycle. This strong response to external conditions, both biotic and abiotic, suggests that the chemical composition of phytoplankton intracellular pools released during lysis shift with ocean conditions. As phytoplankton cell lysis is one of the largest sources of labile dissolved compounds in the ocean, dynamic compositional changes in the metabolites released to heterotrophic bacteria have implications for the fate of surface ocean carbon. 

The ocean’s temperature increase has fundamental implications for physiological rates and processes of marine microbes. In this study, a marine diatom Thalassiosira pseudonana CCMP1335 was acclimated for three months at temperatures below (14°C), equal to (20°C), and above (28°C). Heterotrophic bacterium Ruegeria pomeroyi DSS-3 was inoculated into cultures, and transporter expression was compared between temperatures. R. pomeroyi transporter expression leveraged as a biosensor of available diatom exometabolites indicated temperature-related substitution of diatom osmolytes dimethylsulfoniopropionate (DMSP), dihydroxypropanesulfonate (DHPS), and homarine (dominating carbon transfer at lower temperatures) with glycine betaine and choline (dominating at higher temperatures). T. pseudonana endometabolome pools and biosynthetic pathway expression indicated increased availability of amino acids and glycerol-3-phosphate at higher temperatures. Overall trends across datasets supported a greater importance of organic sulfur compounds in diatom-bacterial metabolite transfer at lower temperatures and greater importance of organic nitrogen compounds at higher temperatures. 

These data are from three laboratory studies of co-cultured temperature-acclimated marine microbes and Ruegeria pomeroyi DSS-3. Model systems were established in which temperature-acclimated microbial strains were co-cultured with the heterotrophic bacterium Ruegeria pomeroyi. Cultures of the coccolithophore Emiliania huxleyi CCMP151 were pre-acclimated to three temperature treatments (15°, 20°, and 28° Celsius (C)). Cultures of the diatom Thalassiosira pseudonana CCMP1335 were pre-acclimated to 14°, 20°, and 28°C. Cultures of Synechococcus sp. WH8102 were pre-acclimated to 20°, 24°, and 28°C. The investigators characterized the transcriptomes of both the phytoplankter and heterotrophic bacterium at initial and late exponential growth at the three temperatures. 

Biological nitrogen fixation converts inert di-nitrogen gas into bioavailable nitrogen and can be an important source of bioavailable nitrogen to organisms. This dataset synthesizes the aquatic nitrogen fixation rate measurements across inland and coastal waters. Data were derived from papers and datasets published by April 2022 and include rates measured using the acetylene reduction assay (ARA), 15N2 labeling, or the N2/Ar technique. The dataset is comprised of 4793 nitrogen fixation rates measurements from 267 studies, and is structured into four tables: 1) a reference table with sources from which data were extracted, 2) a rates table with nitrogen fixation rates that includes habitat, substrate, geographic coordinates, and method of measuring N2 fixation rates, 3) a table with supporting environmental and chemical data for a subset of the rate measurements when data were available, and 4) a data dictionary with definitions for each variable in each data table. This dataset was compiled and curated by the NSF-funded Aquatic Nitrogen Fixation Research Coordination Network (award number 2015825). 

Abstract Dissolved primary production released into seawater by marine phytoplankton is a major source of carbon fueling heterotrophic bacterial production in the ocean. The composition of the organic compounds released by healthy phytoplankton is poorly known and difficult to assess with existing chemical methods. Here, expression of transporter and catabolic genes by three model marine bacteria ( Ruegeria pomeroyi DSS-3, Stenotrophomonas sp. SKA14, and Polaribacter dokdonensis MED152) was used as a biological sensor of metabolites released from the picoeukaryote Micromonas commoda RCC299. Bacterial expression responses indicated that the three species together recognized 38 picoeukaryote metabolites. This was consistent with the Micromonas expression of genes for starch metabolism and synthesis of peptidoglycan-like intermediates. A comparison of the hypothesized Micromonas exometabolite pool with that of the diatom Thalassiosira pseudonana CCMP1335, analyzed previously with the same biological sensor method, indicated that both phytoplankton released organic acids, nucleosides, and amino acids, but differed in polysaccharide and organic nitrogen release. Future ocean conditions are expected to favor picoeukaryotic phytoplankton over larger-celled microphytoplankton. Results from this study suggest that such a shift could alter the substrate pool available to heterotrophic bacterioplankton. 

Biological nitrogen fixation is the conversion of dinitrogen (N2) gas into bioavailable nitrogen by microorganisms with consequences for primary production, ecosystem function, and global climate. Here we present a compiled dataset of 4793 nitrogen fixation (N2-fixation) rates measured in the water column and benthos of inland and coastal systems via the acetylene reduction assay, 15N2 labeling, or N2/Ar technique. While the data are distributed across seven continents, most observations (88%) are from the northern hemisphere. 15N2 labeling accounted for 67% of water column measurements, while the acetylene reduction assay accounted for 81% of benthic N2-fixation observations. Dataset median area-, volume-, and mass-normalized N2-fixation rates are 7.1 μmol N2-N m−2 h−1, 2.3 × 10−4 μmol N2-N L−1 h−1, and 4.8 × 10−4 μmol N2-N g−1 h−1, respectively. This dataset will facilitate future efforts to study and scale N2-fixation contributions across inland and coastal aquatic environments. 

Biological nitrogen fixation is a key driver of global primary production and climate. Decades of effort have repeatedly updated nitrogen fixation estimates for terrestrial and open ocean systems, yet other aquatic systems in between have largely been ignored. Here we present an evaluation of nitrogen fixation for inland and coastal waters. We demonstrate that water column and sediment nitrogen fixation is ubiquitous across these diverse aquatic habitats, with rates ranging six orders of magnitude. We conservatively estimate that, despite accounting for less than 10% of the global surface area, inland and coastal aquatic systems fix 40 (30 to 54) teragrams of nitrogen per year, equivalent to 15% of the nitrogen fixed on land and in the open ocean. Inland systems contribute more than half of this biological nitrogen fixation. 

Abstract Phytoplankton-derived metabolites fuel a large fraction of heterotrophic bacterial production in the global ocean, yet methodological challenges have limited our understanding of the organic molecules transferred between these microbial groups. In an experimental bloom study consisting of three heterotrophic marine bacteria growing together with the diatom Thalassiosira pseudonana , we concurrently measured diatom endometabolites (i.e., potential exometabolite supply) by nuclear magnetic resonance (NMR) spectroscopy and bacterial gene expression (i.e., potential exometabolite uptake) by metatranscriptomic sequencing. Twenty-two diatom endometabolites were annotated, with nine increasing in internal concentration in the late stage of the bloom, eight decreasing, and five showing no variation through the bloom progression. Some metabolite changes could be linked to shifts in diatom gene expression, as well as to shifts in bacterial community composition and their expression of substrate uptake and catabolism genes. Yet an overall low match indicated that endometabolome concentration was not a good predictor of exometabolite availability, and that complex physiological and ecological interactions underlie metabolite exchange. Six diatom endometabolites accumulated to higher concentrations in the bacterial co-cultures compared to axenic cultures, suggesting a bacterial influence on rates of synthesis or release of glutamate, arginine, leucine, 2,3-dihydroxypropane-1-sulfonate, glucose, and glycerol-3-phosphate. Better understanding of phytoplankton metabolite production, release, and transfer to assembled bacterial communities is key to untangling this nearly invisible yet pivotal step in ocean carbon cycling. 

Biological nitrogen fixation converts inert di-nitrogen gas into bioavailable nitrogen and can be an important source of bioavailable nitrogen to organisms. This dataset synthesizes the aquatic nitrogen fixation rate measurements across inland and coastal waters. Data were derived from papers and datasets published by April 2022 and include rates measured using the acetylene reduction assay (ARA), 15N2 labeling, or the N2/Ar technique. The dataset is comprised of 4793 nitrogen fixation rates measurements from 267 studies, and is structured into four tables: 1) a reference table with sources from which data were extracted, 2) a rates table with nitrogen fixation rates that includes habitat, substrate, geographic coordinates, and method of measuring N2 fixation rates, 3) a table with supporting environmental and chemical data for a subset of the rate measurements when data were available, and 4) a data dictionary with definitions for each variable in each data table. This dataset was compiled and curated by the NSF-funded Aquatic Nitrogen Fixation Research Coordination Network (award number 2015825).