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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 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 Siderophores are strong iron‐binding molecules produced and utilized by microbes to acquire the limiting nutrient iron (Fe) from their surroundings. Despite their importance as a component of the iron‐binding ligand pool in seawater, data on the distribution of siderophores and the microbes that use them are limited. Here, we measured the concentrations and types of dissolved siderophores during two cruises in April 2016 and June 2017 that transited from the iron‐replete, low‐macronutrient North Pacific Subtropical Gyre through the North Pacific Transition Zone (NPTZ) to the iron‐deplete, high‐macronutrient North Pacific Subarctic Frontal Zone (SAFZ). Surface siderophore concentrations in 2017 were higher in the NPTZ (4.0–13.9 pM) than the SAFZ (1.2–5.1 pM), which may be partly attributed to stimulated siderophore production by environmental factors such as dust‐derived iron concentrations (up to 0.51 nM). Multiple types of siderophores were identified on both cruises, including ferrioxamines, amphibactins, and iron‐free forms of photoreactive siderophores, which suggest active production and use of diverse siderophores across latitude and depth. Siderophore biosynthesis and uptake genes and transcripts were widespread across latitude, and higher abundances of these genes and transcripts at higher latitudes may reflect active siderophore‐mediated iron uptake by the local bacterial community across the North Pacific. The variability in the taxonomic composition of bacterial communities that transcribe putative ferrioxamine, amphibactin, and salmochelin transporter genes at different latitudes further suggests that the microbial groups involved in active siderophore production and usage change depending on local conditions. 

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). 

Abstract Ammonia-oxidizing archaea (AOA) are among the most abundant and ubiquitous microorganisms in the ocean, exerting primary control on nitrification and nitrogen oxides emission. Although united by a common physiology of chemoautotrophic growth on ammonia, a corresponding high genomic and habitat variability suggests tremendous adaptive capacity. Here, we compared 44 diverse AOA genomes, 37 from species cultivated from samples collected across diverse geographic locations and seven assembled from metagenomic sequences from the mesopelagic to hadopelagic zones of the deep ocean. Comparative analysis identified seven major marine AOA genotypic groups having gene content correlated with their distinctive biogeographies. Phosphorus and ammonia availabilities as well as hydrostatic pressure were identified as selective forces driving marine AOA genotypic and gene content variability in different oceanic regions. Notably, AOA methylphosphonate biosynthetic genes span diverse oceanic provinces, reinforcing their importance for methane production in the ocean. Together, our combined comparative physiological, genomic, and metagenomic analyses provide a comprehensive view of the biogeography of globally abundant AOA and their adaptive radiation into a vast range of marine and terrestrial habitats.