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

Mayali, Xavier; Samo, Ty J.; Kimbrel, Jeff A.; Morris, Megan M.; Rolison, Kristina; Swink, Courtney; Ramon, Christina; Kim, Young-Mo; Munoz-Munoz, Nathalie; Nicora, Carrie; Purvine, Sam; Lipton, Mary; Stuart, Rhona K.; Weber, Peter K.

doi:10.1038/s41467-023-41179-9

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

Journal Article · Wed Sep 13 00:00:00 EDT 2023 · Nature Communications

DOI:https://doi.org/10.1038/s41467-023-41179-9· OSTI ID:1999922

; ; ; ; ; ; Ramon, Christina; ; ; ; ; Lipton, Mary; ;

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.

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Research Organization:: Lawrence Livermore National Laboratory (LLNL), Livermore, CA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States). Environmental Molecular Sciences Laboratory (EMSL)

Sponsoring Organization:: USDOE; USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; AC05-76RL01830; AC52-07NA27344

OSTI ID:: 1999922

Alternate ID(s):: OSTI ID: 2222442
OSTI ID: 2229998

Report Number(s):: LLNL--JRNL-836794; PNNL-SA--177688; 5642; PII: 41179

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 14; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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