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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 Homarine (N-methylpicolinic acid) is a ubiquitous marine metabolite produced by phytoplankton and noted for its bioactivity in marine animals, yet its microbial degradation pathways are uncharacterized. Here, we identify a conserved operon (homABCDER) that mediates homarine catabolism in bacteria using comparative transcriptomics, mutagenesis, and targeted knockouts. Phylogenetic and genomic analyses show this operon distributed across abundant bacterial clades, including coastal copiotrophs (e.g., Rhodobacterales) and open-ocean oligotrophs (e.g., SAR11, SAR116). High-resolution mass spectrometry revealed N-methylglutamic acid and glutamic acid as key metabolic products of homarine in both model and natural systems, with N-methylglutamate dehydrogenase catalyzing their conversion. Metatranscriptomics showed responsive and in situ expression of hom genes aligned with homarine availability. These findings uncover the genetic and metabolic basis of homarine degradation, establish its ecological relevance, and highlight homarine as a versatile growth substrate that feeds into central metabolism via glutamic acid in diverse marine 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 Oxygen deficient zones (ODZs) are subsurface marine systems that harbour distinct microbial communities, including populations of the picocyanobacteriaProchlorococcusthat can form a secondary chlorophyll maximum (SCM), and low‐oxygen tolerant strains of the globally abundant heterotrophPelagibacter(SAR11). Yet, the small labile molecules (metabolites) responsible for maintaining these ODZ communities are unknown. Here, we compared the metabolome of an ODZ to that of an oxygenated site by quantifying 87 metabolites across depth profiles in the eastern tropical North Pacific ODZ and the oxygenated waters of the North Pacific Gyre. Metabolomes were largely consistent between anoxic and oxic water columns. However, the osmolyte glycine betaine (GBT) was enriched in the oxycline and SCM of the ETNP, comprising as much as 1.2% of particulate organic carbon. Transcriptomes revealed two active GBT production pathways, glycine methylation (SDMT/bsmB) expressed byProchlorococcusand choline oxidation (betB) expressed by Gammaproteobacteria. GBT consumption through demethylation involved diverse microbial taxa, with SAR11 contributing nearly half of the transcripts for the initial step of GBT demethylation (BHMT), which is predicted to convert GBT and homocysteine into dimethylglycine and methionine, a compound SAR11 cannot otherwise produce. Thus, GBT connects the metabolisms of the dominant phototroph and heterotroph in the oceans. 

Abstract Seasonal cycles within the marginal ice zones in polar regions include large shifts in temperature and salinity that strongly influence microbial abundance and physiology. However, the combined effects of concurrent temperature and salinity change on microbial community structure and biochemical composition during transitions between seawater and sea ice are not well understood. Coastal marine communities along the western Antarctic Peninsula were sampled and surface seawater was incubated at combinations of temperature and salinity mimicking the formation (cold, salty) and melting (warm, fresh) of sea ice to evaluate how these factors may shape community composition and particulate metabolite pools during seasonal transitions. Bacterial and algal community structures were tightly coupled to each other and distinct across sea-ice, seawater, and sea-ice-meltwater field samples, with unique metabolite profiles in each habitat. During short-term (approximately 10-day) incubations of seawater microbial communities under different temperature and salinity conditions, community compositions changed minimally while metabolite pools shifted greatly, strongly accumulating compatible solutes like proline and glycine betaine under cold and salty conditions. Lower salinities reduced total metabolite concentrations in particulate matter, which may indicate a release of metabolites into the labile dissolved organic matter pool. Low salinity also increased acylcarnitine concentrations in particulate matter, suggesting a potential for fatty acid degradation and reduced nutritional value at the base of the food web during freshening. Our findings have consequences for food web dynamics, microbial interactions, and carbon cycling as polar regions undergo rapid climate change. 

Abstract Small, biologically produced, organic molecules called metabolites play key roles in microbial systems where they directly mediate exchanges of nutrients, energy, and information. However, the study of dissolved polar metabolites in seawater and other environmental matrices has been hampered by analytical challenges including high inorganic ion concentrations, low analyte concentrations, and high chemical diversity. Here we show that a cation‐exchange solid‐phase extraction (CX‐SPE) sample preparation approach separates positively charged and zwitterionic metabolites from seawater and freshwater samples, allowing their analysis by liquid chromatography–mass spectrometry. We successfully extracted 69 known compounds from an in‐house compound collection and evaluated the performance of the method by establishing extraction efficiencies (EEs) and limits of detection (pM to low nM range) for these compounds. CX‐SPE extracted a range of compounds including amino acids and compatible solutes, resulted in very low matrix effects, and performed robustly across large variations in salinity and dissolved organic matter concentration. We compared CX‐SPE to an established SPE procedure (PPL‐SPE) and demonstrate that these two methods extract fundamentally different fractions of the dissolved metabolite pool with CX‐SPE extracting compounds that are on average smaller and more polar. We use CX‐SPE to analyze four environmental samples from distinct aquatic biomes, producing some of the first CX‐SPE dissolved metabolomes. Quantified compounds ranged in concentration from 0.0093 to 49 nM and were composed primarily of amino acids (0.15–16 nM) and compatible solutes such as trimethylamine N‐oxide (0.89–49 nM) and glycine betaine (2.8–5.2 nM).