Multi-omics uncovers nutrient stress-driven interactions in a synthetic Prymnesium parvum holobiont, with vitamin B12-limitation revealing mutualism
Abstract
Microalgal-bacterial interactions are central to nutrient cycling and ecosystem functioning in marine habitats, yet the mechanisms structuring these associations under defined nutrient constraints remain poorly resolved. Using a synthetic 15-member bacterial community (SynCom) and controlled nitrogen (N), phosphorus (P), and vitamin B12-limitation, we investigated how nutrient scarcity shapes the physiology, metabolism, and transcriptional activity of the harmful alga Prymnesium parvum and its associated microbiota. Under N- and P-limitation, the SynCom had minimal impact on algal growth despite nutrient-dependent shifts in toxin production and metabolite profiles. In contrast, B12-limitation triggered a strong mutualistic interaction in which the SynCom enabled a three-fold increase in algal biomass and drove restructuring of intracellular and extracellular metabolomes, including the accumulation of ectoine and membrane-associated lipids and the depletion of thiamine-like and stress-associated metabolites. Metabarcoding revealed stable community composition but enrichment of B12-producing taxa under B12-limited conditions, while metatranscriptomics uncovered functional divergence among SynCom members. Bacteria displayed contrasting response strategies, including nutrient-responsive specialists and transcriptionally flexible generalists maintaining gene expression across all nutrient regimes. B12-producers (Marinovum algicola, Roseobacter sp., Halomonas sp.) upregulated cobalamin biosynthesis exclusively under B12-limitation, whereas several B12-auxotrophic taxa induced B12-transport and B12-requiring enzymes, indicating active vitamin exchange within the holobiont. P. parvum displayed transcriptional programs specific to each nutrient limitation, with B12-limited co-cultures shifting toward growth-associated gene expression despite constitutive expression of the B12-dependent metH gene. These results demonstrate that vitamin auxotrophy acts as a key metabolic lever reorganizing holobiont function, driving reciprocal benefits and reprogramming algal-bacterial metabolism in our synthetic system.
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BibTeX
@article{patron2026multiomics,
title = {{Multi-omics uncovers nutrient stress-driven interactions in a synthetic Prymnesium parvum holobiont, with vitamin B12-limitation revealing mutualism}},
author = {Lou Patron and Florian Petrilli and Anaelle Bout and Marinna Gaudin and Lena Gouhier and Clarisse Hubert and Damien Réveillon and Samuel Chaffron and Enora Briand and Matthieu Garnier},
journal = {ISME Communications},
year = {2026},
month = nov,
doi = {10.1093/ismeco/ycag142},
url = {https://hal.science/hal-05854100v1},
note = {CC BY},
}
RIS
TY - JOUR
TI - Multi-omics uncovers nutrient stress-driven interactions in a synthetic Prymnesium parvum holobiont, with vitamin B12-limitation revealing mutualism
AU - Lou Patron
AU - Florian Petrilli
AU - Anaelle Bout
AU - Marinna Gaudin
AU - Lena Gouhier
AU - Clarisse Hubert
AU - Damien Réveillon
AU - Samuel Chaffron
AU - Enora Briand
AU - Matthieu Garnier
PY - 2026
DA - 2026/11/05
JO - ISME Communications
DO - 10.1093/ismeco/ycag142
UR - https://hal.science/hal-05854100v1
AB - Microalgal-bacterial interactions are central to nutrient cycling and ecosystem functioning in marine habitats, yet the mechanisms structuring these associations under defined nutrient constraints remain poorly resolved. Using a synthetic 15-member bacterial community (SynCom) and controlled nitrogen (N), phosphorus (P), and vitamin B12-limitation, we investigated how nutrient scarcity shapes the physiology, metabolism, and transcriptional activity of the harmful alga Prymnesium parvum and its associated microbiota. Under N- and P-limitation, the SynCom had minimal impact on algal growth despite nutrient-dependent shifts in toxin production and metabolite profiles. In contrast, B12-limitation triggered a strong mutualistic interaction in which the SynCom enabled a three-fold increase in algal biomass and drove restructuring of intracellular and extracellular metabolomes, including the accumulation of ectoine and membrane-associated lipids and the depletion of thiamine-like and stress-associated metabolites. Metabarcoding revealed stable community composition but enrichment of B12-producing taxa under B12-limited conditions, while metatranscriptomics uncovered functional divergence among SynCom members. Bacteria displayed contrasting response strategies, including nutrient-responsive specialists and transcriptionally flexible generalists maintaining gene expression across all nutrient regimes. B12-producers (Marinovum algicola, Roseobacter sp., Halomonas sp.) upregulated cobalamin biosynthesis exclusively under B12-limitation, whereas several B12-auxotrophic taxa induced B12-transport and B12-requiring enzymes, indicating active vitamin exchange within the holobiont. P. parvum displayed transcriptional programs specific to each nutrient limitation, with B12-limited co-cultures shifting toward growth-associated gene expression despite constitutive expression of the B12-dependent metH gene. These results demonstrate that vitamin auxotrophy acts as a key metabolic lever reorganizing holobiont function, driving reciprocal benefits and reprogramming algal-bacterial metabolism in our synthetic system.
SN - 2730-6151
ER -