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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. 

Marine biogeochemical cycles are built on interactions between surface ocean microbes, particularly those connecting phytoplankton primary producers to heterotrophic bacteria. However, direct influences of bacteria on phytoplankton physiology are poorly known. In this study, three marine bacteria (Ruegeria pomeroyi DSS-3, Stenotrophomonas sp. SKA14, and Polaribacter dokdonensis MED152) were co-cultured with green alga Micromonas commoda, and the phytoplankter's transcriptome was studied by RNASeq. The presence of each bacterium invoked transcriptomic remodeling by M. commoda after 8 h in co-culture. Some aspects of the algal transcriptomic response were conserved across all three bacteria, while others were restricted to a single bacterium. M. commoda had both rapid and extensive responses to heterotrophic bacteria. 

Abstract The ocean microbe‐metabolite network involves thousands of individual metabolites that encompass a breadth of chemical diversity and biological functions. These microbial metabolites mediate biogeochemical cycles, facilitate ecological relationships, and impact ecosystem health. While analytical advancements have begun to illuminate such roles, a challenge in navigating the deluge of marine metabolomics information is to identify a subset of metabolites that have the greatest ecosystem impact. Here, we present an ecological framework to distill knowledge of fundamental metabolites that underpin marine ecosystems. We borrow terms from macroecology that describe important species, namely “dominant,” “keystone,” and “indicator” species, and apply these designations to metabolites within the ocean microbial metabolome. These selected metabolites may shape marine community structure, function, and health and provide focal points for enhanced study of microbe‐metabolite networks. Applying ecological concepts to marine metabolites provides a path to leverage metabolomics data to better describe and predict marine microbial ecosystems. 

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. 

Abstract The flux of carbon through the labile dissolved organic matter (DOM) pool supports marine microbial communities and represents the fate of approximately half of marine net primary production (NPP). However, the behavior of individual chemical structures that make up labile DOM remain largely unknown. We performed 12 uptake kinetics and two uptake competition experiments on the abundant betaine osmolytes glycine betaine (GBT) and homarine. Combining uptake kinetics with dissolved metabolite measurements, we quantified fluxes through the DOM pool. Fluxes were correlated with particulate concentrations and ranged from 0.53 to 41 and 0.003 to 0.54 nmol L⁻¹ d⁻¹for GBT and homarine, respectively, equivalent to up to 1.2% of NPP. Turnover times of dissolved GBT and homarine ranged from 1 to 57 d. Betaines and sulfoniums such as dimethylsulfoniopropionate competitively inhibited homarine uptake. Our results quantify GBT and homarine cycling and suggest an important role for uptake competition in regulating dissolved metabolite concentrations and fluxes. 

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.