Single-cell isotope tracing reveals functional guilds of bacteria associated with the diatom Phaeodactylum tricornutum

Xavier Mayali (), Ty J. Samo, Jeff A. Kimbrel, Megan M. Morris, Kristina Rolison, Courtney Swink, Christina Ramon, Young-Mo Kim, Nathalie Munoz-Munoz, Carrie Nicora, Sam Purvine, Mary Lipton, Rhona K. Stuart and Peter K. Weber
Additional contact information
Xavier Mayali: Lawrence Livermore National Laboratory
Ty J. Samo: Lawrence Livermore National Laboratory
Jeff A. Kimbrel: Lawrence Livermore National Laboratory
Megan M. Morris: Lawrence Livermore National Laboratory
Kristina Rolison: Lawrence Livermore National Laboratory
Courtney Swink: Lawrence Livermore National Laboratory
Christina Ramon: Lawrence Livermore National Laboratory
Young-Mo Kim: Pacific Northwest National Laboratory
Nathalie Munoz-Munoz: Pacific Northwest National Laboratory
Carrie Nicora: Pacific Northwest National Laboratory
Sam Purvine: Pacific Northwest National Laboratory
Mary Lipton: Pacific Northwest National Laboratory
Rhona K. Stuart: Lawrence Livermore National Laboratory
Peter K. Weber: Lawrence Livermore National Laboratory

Nature Communications, 2023, vol. 14, issue 1, 1-13

Abstract: Abstract Bacterial remineralization of algal organic matter fuels algal growth but is rarely quantified. Consequently, we cannot currently predict whether some bacterial taxa may provide more remineralized nutrients to algae than others. Here, we quantified bacterial incorporation of algal-derived complex dissolved organic carbon and nitrogen and algal incorporation of remineralized carbon and nitrogen in fifteen bacterial co-cultures growing with the diatom Phaeodactylum tricornutum at the single-cell level using isotope tracing and nanoSIMS. We found unexpected strain-to-strain and cell-to-cell variability in net carbon and nitrogen incorporation, including non-ubiquitous complex organic nitrogen utilization and remineralization. We used these data to identify three distinct functional guilds of metabolic interactions, which we termed macromolecule remineralizers, macromolecule users, and small-molecule users, the latter exhibiting efficient growth under low carbon availability. The functional guilds were not linked to phylogeny and could not be elucidated strictly from metabolic capacity as predicted by comparative genomics, highlighting the need for direct activity-based measurements in ecological studies of microbial metabolic interactions.

Date: 2023
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DOI: 10.1038/s41467-023-41179-9

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