Integrating metagenome-scale metabolic models and metabolomics to explore candidate biochemical interactions in cultivated Microcystis phycospheres
Abstract
Favored by global changes, freshwater cyanobacterial harmful blooms generate major ecological, economic, and public health challenges. Microcystis, one of the most widespread cyanobacterial genera, grows within a phycosphere where specialized interactions with its microbiome occur, that are suspected to influence bloom appearance and its potential toxicity. Using a combination of metagenomics, metabolomics, and metabolic modeling, we characterized the culture-associated phycospheres of 12 Microcystis strains isolated from a French pond. The distribution of metabolic reactions within Microcystis was consistent with their genospecies, whereas the metabolic landscape at the community level diverged from cyanobacterial phylogeny, indicating partial functional decoupling between cyanobacteria and their associated microbiomes. Bacteria associated with the simplified phycospheres substantially expanded the metabolic repertoire of the system, while maintaining functional redundancy within and across communities. On the other hand, endometabolomic profiles were largely driven by cyanobacterial metabolic outputs, whereas exometabolomic analysis did not reveal metabolites involved in exchange processes. Metabolic modeling, together with the identification of toxic specialized metabolites produced by specific biosynthetic gene clusters, further highlighted differences in metabolic potential among phycospheres. Together, these findings deepen the understanding of Microcystis' phycosphere functioning and demonstrate the value of multi-omics systems biology approaches, while suggesting that metabolic complementarity between species and across phycospheres could play a role in bloom-associated microbiome structure.
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BibTeX
@article{audemard2026integrating,
title = {{Integrating metagenome-scale metabolic models and metabolomics to explore candidate biochemical interactions in cultivated Microcystis phycospheres}},
author = {Juliette Audemard and Nicolas Creusot and Julie Leloup and Charlotte Duval and Sébastien Halary and Lou Mary and Mélissa Eon and Thomas Forjonel and Mohamed Mouffok and Rémy Puppo and Elodie Belmonte and Veronique Gautier and Jeanne Got and Marie Lefebvre and Gabriel V Markov and Coralie Muller and Benjamin Marie and Binta Diémé and Clémence Frioux},
journal = {ISME Communications},
year = {2026},
month = aug,
doi = {10.1093/ismeco/ycag226},
url = {https://inria.hal.science/hal-05760845v1},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Integrating metagenome-scale metabolic models and metabolomics to explore candidate biochemical interactions in cultivated Microcystis phycospheres
AU - Juliette Audemard
AU - Nicolas Creusot
AU - Julie Leloup
AU - Charlotte Duval
AU - Sébastien Halary
AU - Lou Mary
AU - Mélissa Eon
AU - Thomas Forjonel
AU - Mohamed Mouffok
AU - Rémy Puppo
AU - Elodie Belmonte
AU - Veronique Gautier
AU - Jeanne Got
AU - Marie Lefebvre
AU - Gabriel V Markov
AU - Coralie Muller
AU - Benjamin Marie
AU - Binta Diémé
AU - Clémence Frioux
PY - 2026
DA - 2026/08/05
JO - ISME Communications
DO - 10.1093/ismeco/ycag226
UR - https://inria.hal.science/hal-05760845v1
AB - Favored by global changes, freshwater cyanobacterial harmful blooms generate major ecological, economic, and public health challenges. Microcystis, one of the most widespread cyanobacterial genera, grows within a phycosphere where specialized interactions with its microbiome occur, that are suspected to influence bloom appearance and its potential toxicity. Using a combination of metagenomics, metabolomics, and metabolic modeling, we characterized the culture-associated phycospheres of 12 Microcystis strains isolated from a French pond. The distribution of metabolic reactions within Microcystis was consistent with their genospecies, whereas the metabolic landscape at the community level diverged from cyanobacterial phylogeny, indicating partial functional decoupling between cyanobacteria and their associated microbiomes. Bacteria associated with the simplified phycospheres substantially expanded the metabolic repertoire of the system, while maintaining functional redundancy within and across communities. On the other hand, endometabolomic profiles were largely driven by cyanobacterial metabolic outputs, whereas exometabolomic analysis did not reveal metabolites involved in exchange processes. Metabolic modeling, together with the identification of toxic specialized metabolites produced by specific biosynthetic gene clusters, further highlighted differences in metabolic potential among phycospheres. Together, these findings deepen the understanding of Microcystis' phycosphere functioning and demonstrate the value of multi-omics systems biology approaches, while suggesting that metabolic complementarity between species and across phycospheres could play a role in bloom-associated microbiome structure.
SN - 2730-6151
ER -