Seasonal Exometabolites Are Regulated by Essential Microbial Metabolisms in the Oligotrophic Ocean

Predictions of how the biogeochemical reservoir of marine dissolved organic matter (DOM) will respond to future ocean changes are limited by bulk characterizations that mask a complex network of thousands of individual microbe-molecule interactions. The marine microbial community regulates the transformation and fate of organic carbon by utilizing DOM molecules as the products and reactants of their diverse enzymatic functions. Linking these molecules with the microbial taxa responsible for their utilization requires characterization of both microbial activity and the resulting metabolic footprint. Here we present a time series of the seasonal dynamics of both the exometabolome and the bacterioplankton community at the Bermuda Atlantic Time series Study (BATS) site and show that metabolic functions are greater predictors of DOM composition than microbial taxonomy. Putative exometabolite identifications (gonyol, glucose 6-sulfate, succinate, and trehalose) indicate that at least a portion of the exometabolome contains rapidly remineralized, labile molecules. We hypothesize that observations of seasonal accumulation of these labile molecules result from decoupled enrichments of microbial production and consumption enzymes. Critically, we found the composition of seasonal DOM features was more stable inter-annually than the microbial community structure. By estimating redundancy in the BATS metagenomes of metabolisms responsible for cycling these molecules, we propose a paradigm whereby microbial metabolisms that are essential, either to all or to a subset of marine microbes, determine DOM composition. The molecular-level characterization of DOM achieved herein greatly enhances possibilities for connecting the mechanisms behind the DOM-microbe network that cycle Earth’s largest reservoir of organic carbon.Significance statement Marine dissolved organic matter (DOM) is a major carbon reservoir that serves as a critical control on Earth’s climate. Marine DOM production and removal is largely regulated by microbial activity, but a mechanistic understanding of these processes is lacking. By analyzing individual molecules of DOM across a three-year ocean time series with ultrahigh-resolution mass spectrometry, we found the composition of DOM molecules is more stable inter-annually than the microbial community. We suggest that while the identity of marine microbes may change, essential metabolisms within microbial communities are maintained and thus result in less variability of the DOM composition. Therefore, comprehensive and mechanistic knowledge of metabolic functions and pathways will be critical to predicting the response of marine DOM to future climate-driven changes.### Competing Interest StatementThe authors have declared no competing interest.