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Fueled by light, phytoplankton produce the organic matter that supports ocean ecosystems and carbon sequestration. Ocean change impacts microbial metabolism with repercussions for biogeochemical cycling. Light fuels photosynthesis and organic matter production by primary producers in the sunlit ocean. The quantity and quality of the organic matter produced influence community function, yet in situ measurements of metabolites, the products of cellular metabolism, over the diel cycle are lacking. We evaluated community-level biochemical consequences of oscillations of light in the North Pacific Subtropical Gyre by quantifying 79 metabolites in particulate organic matter from 15 m every 4 h over 8 days. Total particulate metabolite concentration peaked at dusk and represented up to 2% of total particulate organic carbon (POC). The concentrations of 55/79 (70%) individual metabolites exhibited significant 24-h periodicity, with daily fold changes from 1.6 to 12.8, often greater than those of POC and flow cytometry-resolvable biomass, which ranged from 1.2 to 2.8. Paired metatranscriptome analysis revealed the taxa involved in production and consumption of a subset of metabolites. Primary metabolites involved in anabolism and redox maintenance had significant 24-h periodicity and diverse organisms exhibited diel periodicity in transcript abundance associated with these metabolites. Compounds with osmotic properties displayed the largest oscillations in concentration, implying rapid turnover and supporting prior evidence of functions beyond cell turgor maintenance. The large daily oscillation of trehalose paired with metatranscriptome and culture data showed that trehalose is produced by the nitrogen-fixing cyanobacterium Crocosphaera , likely to store energy for nighttime metabolism. Together, paired measurements of particulate metabolites and transcripts resolve strategies that microbes use to manage daily energy and redox oscillations and highlight dynamic metabolites with cryptic roles in marine microbial ecosystems. IMPORTANCE Fueled by light, phytoplankton produce the organic matter that supports ocean ecosystems and carbon sequestration. Ocean change impacts microbial metabolism with repercussions for biogeochemical cycling. As the small molecule products of cellular metabolism, metabolites often change rapidly in response to environmental conditions and form the basis of energy and nutrient management and storage within cells. By pairing measurements of metabolites and gene expression in the stratified surface ocean, we reveal strategies of microbial energy management over the day-night cycle and hypothesize that oscillating metabolites are important substrates for dark respiration by phytoplankton. These high-resolution diel measurements of in situ metabolite concentrations form the basis for future work into the specific roles these compounds play in marine microbial communities.

Microscopic phytoplankton transform 100 million tons of inorganic carbon into thousands of different organic compounds each day. The structure of each chemical is critical to its biological and ecosystem function, yet the diversity of biomolecules produced by marine microbial communities remained mainly unexplored, especially small polar molecules which are often considered the currency of the microbial loop. Phytoplankton transform inorganic carbon into thousands of biomolecules that represent an important pool of fixed carbon, nitrogen, and sulfur in the surface ocean. Metabolite production differs between phytoplankton, and the flux of these molecules through the microbial food web depends on compound-specific bioavailability to members of a wider microbial community. Yet relatively little is known about the diversity or concentration of metabolites within marine plankton. Here, we compare 313 polar metabolites in 21 cultured phytoplankton species and in natural planktonic communities across environmental gradients to show that bulk community metabolomes reflect the chemical composition of the phytoplankton community. We also show that groups of compounds have similar patterns across space and taxonomy, suggesting that the concentrations of these compounds in the environment are controlled by similar sources and sinks. We quantify several compounds in the surface ocean that represent substantial understudied pools of labile carbon. For example, the N-containing metabolite homarine was up to 3% of particulate carbon and is produced in high concentrations by cultured Synechococcus , and S-containing gonyol accumulated up to 2.5 nM in surface particles and likely originates from dinoflagellates or haptophytes. Our results show that phytoplankton composition directly shapes the carbon composition of the surface ocean. Our findings suggest that in order to access these pools of bioavailable carbon, the wider microbial community must be adapted to phytoplankton community composition. IMPORTANCE Microscopic phytoplankton transform 100 million tons of inorganic carbon into thousands of different organic compounds each day. The structure of each chemical is critical to its biological and ecosystem function, yet the diversity of biomolecules produced by marine microbial communities remained mainly unexplored, especially small polar molecules which are often considered the currency of the microbial loop. Here, we explore the abundance and diversity of small biomolecules in planktonic communities across ecological gradients in the North Pacific and within 21 cultured phytoplankton species. Our work demonstrates that phytoplankton diversity is an important determinant of the chemical composition of the highly bioavailable pool of organic carbon in the ocean, and we highlight understudied yet abundant compounds in both the environment and cultured organisms. These findings add to understanding of how the chemical makeup of phytoplankton shapes marine microbial communities where the ability to sense and use biomolecules depends on the chemical structure.

Sea-ice algae are an important source of primary production in polar regions, yet we have limited understanding of their responses to the seasonal cycling of temperature and salinity. Using a targeted liquid chromatography-mass spectrometry-based metabolomics approach, we found that axenic cultures of the Antarctic sea-ice diatom, Nitzschia lecointei, displayed large differences in their metabolomes when grown in a matrix of conditions that included temperatures of –1 and 4°C, and salinities of 32 and 41, despite relatively small changes in growth rate. Temperature exerted a greater effect than salinity on cellular metabolite pool sizes, though the N- or S-containing compatible solutes, 2, 3-dihydroxypropane-1-sulfonate (DHPS), glycine betaine (GBT), dimethylsulfoniopropionate (DMSP), and proline responded strongly to both temperature and salinity, suggesting complexity in their control. We saw the largest (> 4-fold) response to salinity for proline. DHPS, a rarely studied but potential compatible solute, had the highest intracellular concentrations among all compatible solutes of ~85 mM. When comparing the culture findings to natural Arctic sea-ice diatom communities, we found extensive overlap in metabolite profiles, highlighting the relevance of culture-based studies to probe environmental questions. Large changes in sea-ice diatom metabolomes and compatible solutes over a seasonal cycle could be significant components of biogeochemical cycling within sea ice.

In the surface ocean, phytoplankton transform inorganic substrates into organic matter that fuels the activity of heterotrophic microorganisms, creating intricate metabolic networks that determine the extent of carbon recycling and storage in the ocean. Yet, the diversity of organic molecules and interacting organisms has hindered detection of specific relationships that mediate this large flux of energy and matter. Here, we show that a tightly coupled microbial network based on organic sulfur compounds (sulfonates) exists among key lineages of eukaryotic phytoplankton producers and heterotrophic bacterial consumers in the North Pacific Subtropical Gyre. We find that cultured eukaryotic phytoplankton taxa produce sulfonates, often at millimolar internal concentrations. These same phytoplankton-derived sulfonates support growth requirements of an open-ocean isolate of the SAR11 clade, the most abundant group of marine heterotrophic bacteria. Expression of putative sulfonate biosynthesis genes and sulfonate abundances in natural plankton communities over the diel cycle link sulfonate production to light availability. Contemporaneous expression of sulfonate catabolism genes in heterotrophic bacteria highlights active cycling of sulfonates in situ. Our study provides evidence that sulfonates serve as an ecologically important currency for nutrient and energy exchange between microbial autotrophs and heterotrophs, highlighting the importance of organic sulfur compounds in regulating ecosystem function. Eukaryotic phytoplankton-derived sulfonates support the growth of the heterotrophic bacterial SAR11 clade and this is linked to light availability, indicating that sulfonates support microbial networks in the open ocean.

Complex assemblages of microbes in the surface ocean are responsible for approximately half of global carbon fixation. The persistence of high taxonomic diversity despite competition for a small suite of relatively homogeneously distributed nutrients, that is, ‘the paradox of the plankton’, represents a long-standing challenge for ecological theory. Here we find evidence consistent with temporal niche partitioning of nitrogen assimilation processes over a diel cycle in the North Pacific Subtropical Gyre. We jointly analysed transcript abundances, lipids and metabolites and discovered that a small number of diel archetypes can explain pervasive periodic dynamics. Metabolic pathway analysis of identified diel signals revealed asynchronous timing in the transcription of nitrogen uptake and assimilation genes among different microbial groups—cyanobacteria, heterotrophic bacteria and eukaryotes. This temporal niche partitioning of nitrogen uptake emerged despite synchronous transcription of photosynthesis and central carbon metabolism genes and associated macromolecular abundances. Temporal niche partitioning may be a mechanism by which microorganisms in the open ocean mitigate competition for scarce resources, supporting community coexistence. By integrating time series analyses of transcripts, lipids and metabolites, the authors show that microorganisms in the open ocean partition scarce resources temporally, with different microbial groups expressing nitrogen uptake and assimilation processes at different points throughout the diel cycle.

Most biological diversity on Earth is contained within microbial communities. In the ocean, these communities dominate processes related to carbon fixation and nutrient recycling. Yet, specific factors that determine community composition and metabolic activity are difficult to resolve in complex microbial populations, complicating predictions of microbial processes in a changing ocean. Microbial metabolism generates small organic molecules that reflect both the biochemical and physiological diversity as well as the taxonomic specificity of these biological processes. These small molecules serve as the conduit for taxon-specific signaling and exchange. Here, we use liquid chromatography-mass spectrometry (LC-MS)-based metabolomics to taxonomically categorize 111 metabolites that include small molecules in central and secondary metabolism across 42 taxa representing numerically dominant and metabolically important lineages of microbial autotrophs and heterotrophs. Patterns in metabolite presence-absence broadly reflected taxonomic lineages. A subset of metabolites that includes osmolytes, sulfur-containing metabolites, sugars, and amino acid derivatives provided chemotaxonomic information among phytoplankton taxa. A variety of phytohormones and signaling molecules were predominantly found in the heterotrophic bacteria and archaea, expanding knowledge of metabolites implicated in modulating interactions between microbes. This chemotaxonomic inventory of marine microbial metabolites is a key step in deciphering metabolic networks that influence ocean biogeochemical cycles.

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 −1 for 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.

Absolute Intracellular Concentrations of Selected Metabolites in the Nitzschia lecointei Culture Grown at −1°C and Salinity 32 and the Utqiaġvik, AK Bottom Sea-Ice Sections Concentration (μmol mol C−1)a Compound Culture Field Fold Difference (Culture/Field) DHPS 3100 ± 81 390 ± 100 8 GBT 1200 ± 99 230 ± 97 5 Proline 960 ± 80 180 ± 110 5 Alanine 190 ± 17 120 ± 67 2 Choline 61 ± 6.7 26 ± 17 2 Cysteic acid 27 ± 2.2 15 ± 5.0 2 Valine 24 ± 1.4 13 ± 9.5 2 Histidine 14 ± 1.2 6.8 ± 4.0 2 Phenylalanine 8.5 ± 0.15 4.7 ± 2.4 2 Methionine 6.9 ± 0.5 12 ± 8.9 0.6 Taurine 5.9 ± 1.1 24 ± 17 0.2 Isoleucine 5.8 ± 0.43 2.4 ± 0.83 2 Tryptophan 4.9 ± 0.2 3.0 ± 1.4 2 Isethionic acid 2.9 ± 0.35 120 ± 51 0.02 Sulfolactic acid 1.5 ± 0.61 0.72 ± 0.36 2 Homarine dlb 13 ± 5.3 — Proline betaine ndc 13 ± 5.7 — Trigonelline dl 1.1 ± 0.58 — Hydroxyectoine nd 1.1 ± 0.44 — aValues are mean ± SD, n = 3. Calculation of Potential Compatible Solute-Based Organic Nitrogen Release into the Sea-Ice Environment Nitrogen-Containing Compatible Solute Sea-Ice Bottom Measured Concentration (mmol CS/mol C) Nitrogen Atoms in CS mmol N/mol C 85% Dump of N-Containing CS Sea-Ice Bottom Measured mol C/L (M) CS-Derived mol N/L Estimate (mM) Sea-Ice Bottom Measured [ NO3−2 ] (mM) Proline 1.80E−01 1.00E+00 1.80E−01 Glycine betaine 2.30E−01 1.00E+00 2.30E−01 Homarine 1.32E−02 1.00E+00 1.32E−02 Total 4.23E−01 3.60E−01 1.72E−03 6.17E−04 1.02E−02 The originally published Tables 2 and S6 are also shown for reference: Absolute Intracellular Concentrations of Selected Metabolites in the Nitzschia lecointei Culture Grown at −1°C and Salinity 32 and the Utqiaġvik, AK Bottom Sea-Ice Sections Concentration (μmol mol C–1)a Compound Culture Field Fold Difference (Culture/Field) DHPS 3100 ± 81 390 ± 100 8 GBT 1200 ± 99 230 ± 97 5 Proline 960 ± 80 180 ± 110 5 Alanine 190 ± 17 120 ± 67 2 Choline 61 ± 6.7 26 ± 17 2 Cysteic acid 27 ± 2.2 15 ± 5.0 2 Valine 24 ± 1.4 13 ± 9.5 2 Histidine 14 ± 1.2 6.8 ± 4.0 2 Phenylalanine 8.5 ± 0.15 4.7 ± 2.4 2 Methionine 6.9 ± 0.5 12 ± 8.9 0.6 Taurine 5.9 ± 1.1 24 ± 17 0.2 Isoleucine 5.8 ± 0.43 2.4 ± 0.83 2 Tryptophan 4.9 ± 0.2 3.0 ± 1.4 2 Isethionic acid 2.9 ± 0.35 120 ± 51 0.02 Sulfolactic acid 1.5 ± 0.61 0.72 ± 0.36 2 Homarine dlb 260 ± 110 — Proline betaine ndc 13 ± 5.7 — Trigonelline dl 1.1 ± 0.58 — Hydroxyectoine nd 1.1 ± 0.44 — aValues are mean ± SD, n = 3. Calculation of Potential Compatible Solute-Based Organic Nitrogen Release into the Sea-Ice Environment Nitrogen-Containing Compatible Solute Sea-Ice Bottom Measured Concentration (mmol CS/mol C) Nitrogen Atoms in CS mmol N/mol C 85% Dump of N-Containing CS Sea-Ice Bottom Measured mol C/L (M) CS-Derived mol N/L Estimate (mM) Sea-Ice Bottom Measured [ NO3−2 ] (mM) Proline 1.80E−01 1.00E+00 1.80E−01 Glycine betaine 2.30E−01 1.00E+00 2.30E−01 Homarine 2.64E−01 1.00E+00 2.64E−01 Total 6.74E−01 5.73E−01 1.72E−03 9.83E−04 1.02E−02