Phage–host coevolution in natural populations

Type Article
Date 2022-07
Language English
Author(s) Piel Damien1, 2, Bruto Maxime2, Labreuche Yannick1, 2, Blanquart François3, 4, Goudenège David1, 2, Barcia-Cruz Rubén2, 5, Chenivesse Sabine2, Le Panse Sophie2, James Adele1, Dubert Javier2, 5, 6, Petton BrunoORCID1, Lieberman Erica7, Wegner K. Mathias8, Hussain Fatima A.6, Kauffman Kathryn M.ORCID6, Polz Martin F.ORCID6, 9, Bikard DavidORCID10, Gandon SylvainORCID11, Rocha Eduardo P. C.ORCID12, Le Roux FrederiqueORCID1, 2
Affiliation(s) 1 : Ifremer, Unité Physiologie Fonctionnelle des Organismes Marins, ZI de la Pointe du Diable, Plouzané, France
2 : Sorbonne Université, UPMC Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, Roscoff cedex, France
3 : Centre for Interdisciplinary Research in Biology (CIRB), Collège de France, CNRS, INSERM, PSL Research University, Paris, France
4 : Infection Antimicrobials Modelling Evolution, UMR 1137, INSERM, Université de Paris, Paris, France
5 : Department of Microbiology and Parasitology, CIBUS-Faculty of Biology, Universidade de Santiago de Compostela, Santiago de Compostela, Spain
6 : Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA
7 : Eligo Bioscience, Paris, France
8 : AWI - Alfred Wegener Institut - Helmholtz-Zentrum für Polar- und Meeresforschung, Coastal Ecology, Waddensea Station Sylt, List, Germany
9 : Division of Microbial Ecology, Centre for Microbiology and Environmental Systems Science, University of Vienna, Vienna, Austria
10 : Synthetic Biology Group, Department of Microbiology, Institut Pasteur, Paris, France
11 : CEFE (UMR 5175 CNRS - Université de Montpellier - Université Paul Valéry - EPHE), Montpellier, France
12 : Institut Pasteur, Université de Paris, CNRS UMR3525, Microbial Evolutionary Genomics, Paris, France
Source Nature Microbiology (2058-5276) (Springer Science and Business Media LLC), 2022-07 , Vol. 7 , N. 7 , P. 1075-1086
DOI 10.1038/s41564-022-01157-1
WOS© Times Cited 40

Coevolution between bacteriophages (phages) and their bacterial hosts occurs through changes in resistance and counter-resistance mechanisms. To assess phage–host evolution in wild populations, we isolated 195 Vibrio crassostreae strains and 243 vibriophages during a 5-month time series from an oyster farm and combined these isolates with existing V. crassostreae and phage isolates. Cross-infection studies of 81,926 host–phage pairs delineated a modular network where phages are best at infecting co-occurring hosts, indicating local adaptation. Successful propagation of phage is restricted by the ability to adsorb to closely related bacteria and further constrained by strain-specific defence systems. These defences are highly diverse and predominantly located on mobile genetic elements, and multiple defences are active within a single genome. We further show that epigenetic and genomic modifications enable phage to adapt to bacterial defences and alter host range. Our findings reveal that the evolution of bacterial defences and phage counter-defences is underpinned by frequent genetic exchanges with, and between, mobile genetic elements.

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Piel Damien, Bruto Maxime, Labreuche Yannick, Blanquart François, Goudenège David, Barcia-Cruz Rubén, Chenivesse Sabine, Le Panse Sophie, James Adele, Dubert Javier, Petton Bruno, Lieberman Erica, Wegner K. Mathias, Hussain Fatima A., Kauffman Kathryn M., Polz Martin F., Bikard David, Gandon Sylvain, Rocha Eduardo P. C., Le Roux Frederique (2022). Phage–host coevolution in natural populations. Nature Microbiology, 7(7), 1075-1086. Publisher's official version : , Open Access version :