Phage-host coevolution in natural populations

Damien Piel (1, 2) , Maxime Bruto (1, 2) , Yannick Labreuche (1, 2) , François Blanquart (3) , David Goudenège (1, 2) , Rubén Barcia-Cruz (1, 4) , Sabine Chenivesse (1) , Sophie Le Panse (1, 5, 6) , Adèle James (2) , Javier Dubert (1, 7, 4) , Bruno Petton (2) , Erica Lieberman (8) , K. Mathias Wegner (9) , Fatima A Hussain (7) , Kathryn M Kauffman (7) , Martin F Polz (7, 10) , David Bikard (11) , Sylvain Gandon (12) , Eduardo P C Rocha (13) , Frédérique Le Roux (1, 2)

1 LBI2M - Laboratoire de Biologie Intégrative des Modèles Marins
2 PFOM - Physiologie Fonctionnelle des Organismes Marins
3 CIRB - Centre interdisciplinaire de recherche en biologie
4 USC - Universidade de Santiago de Compostela [Spain]
5 FR2424 - Fédération de recherche de Roscoff
6 SBR - Station biologique de Roscoff = Roscoff Marine Station
7 CEE - Department of Civil and Environmental Engineering [Cambridge]
8 Eligo Bioscience
9 AWI - Alfred-Wegener-Institut, Helmholtz-Zentrum für Polar- und Meeresforschung = Alfred Wegener Institute for Polar and Marine Research = Institut Alfred-Wegener pour la recherche polaire et marine
10 Universität Wien = University of Vienna
11 Biologie de Synthèse - Synthetic biology
12 CEFE - Centre d’Ecologie Fonctionnelle et Evolutive
13 Génomique évolutive des Microbes / Microbial Evolutionary Genomics

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 five 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 cooccurring 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 are underpinned by frequent genetic exchanges with, and between, mobile genetic elements.

Domaines: Microbiologie et Parasitologie; Evolution [q-bio.PE]; Interactions entre organismes

Damien Piel, Maxime Bruto, Yannick Labreuche, François Blanquart, David Goudenège, et al.. Phage-host coevolution in natural populations. Nature Microbiology, 2022, 7 (7), pp.1075-1086. ⟨10.1038/s41564-022-01157-1⟩. ⟨hal-03738913⟩