Marine Community Metabolomes Carry Fingerprints of Phytoplankton Community Composition

Abstract

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.

Linkages Among Dissolved Organic Matter Export, Dissolved Metabolites, and Associated Microbial Community Structure Response in the Northwestern Sargasso Sea on a Seasonal Scale

“…Advanced technologies such as ultrahigh resolution mass spectrometry enable detection of DOM composition at the molecular or compound level, in addition to specific biomolecules such as TDAA ( Sleighter and Hatcher, 2008 ; Lechtenfeld et al, 2014 ; Kido Soule et al, 2015 ; Medeiros et al, 2015 ; Osterholz et al, 2016 ). Using these techniques, metabolomics, including both particulate and dissolved metabolomics, has primarily been applied to marine culture studies ( Baran et al, 2010 ; Fiore et al, 2015 ; Longnecker et al, 2015 ; Kashfi et al, 2020 ), with more limited applications to field samples ( Durham et al, 2019 ; Johnson et al, 2020 ; Boysen et al, 2021 ; Heal et al, 2021 ). However, seasonal changes of dissolved metabolites in the marine environment are rarely studied.…”

A metabolic lens on phytoplankton physiology

“…This range is similar to that observed within a prior comparative study of the metabolomes of 12 distinct phytoplankton despite the use of different analytical platforms [172]. We observed that 31 and 77 features in negative and positive mode data, respectively, were present within multiple organisms, similar in size to previously reported work evaluating the core metabolome of phytoplankton [173]. Overall, untargeted features were primarily observed within samples belonging to a single organism.…”

Deciphering Metabolic Currencies That Support Marine Microbial Networks

“…Currently, our group is using environmental metatranscriptomics and metabolomics data to identify links between community composition and metabolite exchange across environmental nutrient gradients. Notably, over half of the >300 metabolites detected by Heal et al ( 21 ) could not be identified. It is likely that additional carbon-cycle-relevant currencies are within these unidentified molecules, and continued effort to identify these metabolites is critical.…”

“…We then bioinformatically inferred metabolic pathways and tracked sulfonate dynamics in natural microbial communities of the North Pacific ( 17 ). So far, field observations suggest sulfonate production in phytoplankton is regulated by both light and nutrient availability ( 17 , 18 , 21 ), ideas that we are exploring back in the lab.…”

“…In a more expansive analysis of >300 metabolites from microbial culture and field data, we showed that phytoplankton taxonomy imparts a strong influence on the chemical composition of ocean metabolomes ( 21 ) with many of these metabolites likely to serve as the substrates in phytoplankton-bacterial exchange. Indeed, bacterial community assembly can be predicted by use of individual phytoplankton-derived metabolites ( 22 , 23 ).…”