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Abstract Dissolved primary production released into seawater by marine phytoplankton is a major source of carbon fueling heterotrophic bacterial production in the ocean. The composition of the organic compounds released by healthy phytoplankton is poorly known and difficult to assess with existing chemical methods. Here, expression of transporter and catabolic genes by three model marine bacteria ( Ruegeria pomeroyi DSS-3, Stenotrophomonas sp. SKA14, and Polaribacter dokdonensis MED152) was used as a biological sensor of metabolites released from the picoeukaryote Micromonas commoda RCC299. Bacterial expression responses indicated that the three species together recognized 38 picoeukaryote metabolites. This was consistent with the Micromonas expression of genes for starch metabolism and synthesis of peptidoglycan-like intermediates. A comparison of the hypothesized Micromonas exometabolite pool with that of the diatom Thalassiosira pseudonana CCMP1335, analyzed previously with the same biological sensor method, indicated that both phytoplankton released organic acids, nucleosides, and amino acids, but differed in polysaccharide and organic nitrogen release. Future ocean conditions are expected to favor picoeukaryotic phytoplankton over larger-celled microphytoplankton. Results from this study suggest that such a shift could alter the substrate pool available to heterotrophic bacterioplankton.
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Dynamic reworking of marine diatom endometabolomes in response to temperature and a model bacterium
ABSTRACT A large annual carbon flux occurs through the surface ocean’s labile dissolved organic carbon (DOC) pool, with influx dominated by phytoplankton-derived metabolites and outflux by heterotrophic bacterioplankton uptake. We addressed the dynamics of this carbon flow between microbial primary and secondary producers through analysis of theThalassiosira pseudonanaCCMP1335 endometabolome, a proxy for the labile DOC released upon phytoplankton lysis, as temperature and bacterial presence were altered. Diatom strains acclimated at one of three different temperatures (14°C, 20°C, or 28°C) were cultured either axenically or with the bacteriumRuegeria pomeroyiDSS-3, and their endometabolites analyzed by NMR. Median concentration variation between conditions was ~1.5-fold across all identified endometabolites. Those with roles as osmolytes varied most, exhibiting concentration differences up to 170-fold across conditions with the largest variations triggered by the presence/absence of the heterotrophic bacterium. Differential expression observed for diatom metabolite synthesis pathways suggested changes in synthesis rates as a mechanism for endometabolome remodeling. Consistent with expectations of high turnover by heterotrophic bacteria, endometabolite mean lifetimes in a DOC pool were <2 h to 12 h. IMPORTANCEThe role of labile DOC in the transfer of marine carbon between phytoplankton and heterotrophic bacteria was first recognized 40 years ago, yet the identity and dynamics of phytoplankton metabolites entering the labile DOC pool are still poorly known. Using metabolome and transcriptome profiling, we found highly variable composition and concentration of diatom endometabolites, depending on growth conditions and arising over time frames as short as a single growth cycle. This strong response to external conditions, both biotic and abiotic, suggests that the chemical composition of phytoplankton intracellular pools released during lysis shift with ocean conditions. As phytoplankton cell lysis is one of the largest sources of labile dissolved compounds in the ocean, dynamic compositional changes in the metabolites released to heterotrophic bacteria have implications for the fate of surface ocean carbon.
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- Award ID(s):
- 1948104
- PAR ID:
- 10674678
- Editor(s):
- Makhalanyane, Thulani P
- Publisher / Repository:
- ISME Communications
- Date Published:
- Journal Name:
- mSystems
- Volume:
- 11
- Issue:
- 1
- ISSN:
- 2379-5077
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1128/msystems.01036-25
