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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 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 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).