Abstract
Bacteriophages-bacteria interactions drive rapid evolution of both partners in laboratory studies. To understand how these dynamics unfold in natural environments, we re-sampled a population of Vibrio crassostreae and their phages in an open, animal-associated marine system four years apart. Analysis of over 1000 predominantly virulent phages revealed rapid change of some lineages, but persistence of others, with genomes highly conserved between years. This pattern is consistent with low substitution rates in persistent lineages and may reflect phages overwintering in wild oysters, slow virion decay, and for temperate phages, lysogeny within hosts. Over 600 V. crassostreae strains recovered at both time points assorted into the same major clades. Oyster-associated vibrios have larger genomes and more abundant and diverse mobile genetic elements suggesting that oysters are hotspots for genetic exchange and horizontal gene transfer. Their genomes encode virulence plasmids, prophages carrying anti-phage systems, phage-plasmids, and phage satellites that persist intracellularly as plasmids. Time series analyses revealed weak correlations between phage and bacterial abundances, a pattern compatible with cryptic population dynamics arising from genetic diversity. Together, these results indicate that natural coevolving phage-bacteria populations can exhibit complex dynamics, with rapid replacement of some lineages alongside multi-year persistence of others.
Data availability
The genome sequences of phages and V. crassostreae isolates generated in this study have been deposited in the European Nucleotide Archive (ENA) under BioProjects PRJEB81325 (phages) and PRJEB67885 (bacterial genomes). Accession numbers are listed in Supplementary Data 1 and 4. Column E of Supplementary Data 1 (“Accession”) refers to the submitted GenBank assembly of each newly isolated phage and refers to newly published data. Column G of Supplementary Data 1 (“Host Accession”) refers to the host strain of V. crassostreae used for the isolation of the phage and as consequence of the experimental design, refers to previously published data12. Column D of Supplementary Data 4 (“Accession”) refers to the submitted Genbank assembly of each newly isolated V. crassostreae strain and refers to newly published data.
The Roscoff Culture Collection (https://roscoff-culture-collection.org/), permits access to the biological material (phages and bacteria isolated in the present study, except when stated otherwise, and can be provided from Le Roux lab at Montreal) upon request, with accession numbers listed in Supplementary Data 1 and 4. Source data are provided with this paper.
Code availability
Custom code used in this study is publicly available on Zenodo (https://doi.org/10.5281/zenodo.18717761)
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Acknowledgements
We thank Bruno Petton (Ifremer Brest) for providing oyster juveniles and overseeing in situ experiments, which made the time-series sampling possible. We are grateful to Chloé Berger, Pauline Daszkowski, Justine Groseille, Théo Foutel Rodier, Étienne Levêque, and Mariam Mamba (GV team, Station Biologique de Roscoff, France) for their assistance during sampling and collections, and Carine Diarra (Le Roux lab, Montréal) for technical help. We thank Jorge Moura de Sousa for helpful discussions concerning the biology and classification of phage-satellites and Julien Guglielmini for help running wGRR/GRIS. We thank Léa Verena Zinsli and Otto X. Cordero for valuable comments on the manuscript, and Illumina for reduced pricing of sequencing kits. Editorial support from Stephen Matheson (Life Science Editors) is also warmly acknowledged. This research was enabled in part by the computational resources of Calcul Quebec and the Digital Research Alliance of Canada.
This work was supported by funding from the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program (grant agreement No. 884988, Advanced ERC “DYNAMIC”), the Canada Excellence Research Chairs Program (CERC-2022-00051), and the Fonds de recherche du Québec – Nature et technologies (FRQ-NT, Fonds des leaders John-R.-Evans, grant 44584) awarded to FLR. Substantial support was provided by the Agence Nationale de la Recherche (ANR-20-CE35-0014 “RESISTE”) and the Fonds UdeM-Pasteur pour la découverte de nouveaux antibiotiques et antibactériens, a philanthropic fund at the Courtois Institute in Biomedical Innovation, Faculty of Medicine, University of Montreal, to EPCR and FLR. Biomics Platform, C2RT, Institut Pasteur, Paris, France, is supported by France Génomique (ANR-10-INBS-09) and IBISA (EPCR, LM, and MM).
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F.L.R. conceived the study, F.L.R. and E.P.C.R. supervised the project, and secured funding. K.C., D.P., D.C.G., Y.L., L.M. and F.L.R. conducted the experiments. D.P. and D.C.G. contributed equally. J.L., D.G., C.B. and E.P.C.R. performed the genomic analyses. J.L., KC, DP, DCG, MM, EPCR, and FLR analyzed the data. J.L., E.P.C.R. and F.L.R. wrote the manuscript.
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Liang, J., Cahier, K., Piel, D. et al. Complex temporal dynamics of phage-bacteria populations in an animal-associated marine system. Nat Commun (2026). https://doi.org/10.1038/s41467-026-71398-9
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DOI: https://doi.org/10.1038/s41467-026-71398-9
