Skip to main content
bioRxiv
  • Home
  • About
  • Submit
  • ALERTS / RSS
Advanced Search
New Results

Genetic determinism of phage-bacteria coevolution in natural populations

Damien Piel, Maxime Bruto, Yannick Labreuche, Francois Blanquart, Sabine Chenivesse, Sophie Lepanse, Adèle James, Rubén Barcia-Cruz, Javier Dubert, Bruno Petton, Erica Lieberman, K. Mathias Wegner, Fatima A. Hussain, Kathryn M. Kauffman, Martin F. Polz, David Bikard, Sylvain Gandon, Frédérique Le Roux
doi: https://doi.org/10.1101/2021.05.05.442762
Damien Piel
1Ifremer, Unité Physiologie Fonctionnelle des Organismes Marins, ZI de la Pointe du Diable, CS 10070, F-29280 Plouzané, France
2Sorbonne Universités, UPMC Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, F-29688 Roscoff cedex, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Maxime Bruto
2Sorbonne Universités, UPMC Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, F-29688 Roscoff cedex, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Yannick Labreuche
1Ifremer, Unité Physiologie Fonctionnelle des Organismes Marins, ZI de la Pointe du Diable, CS 10070, F-29280 Plouzané, France
2Sorbonne Universités, UPMC Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, F-29688 Roscoff cedex, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Francois Blanquart
3Centre for Interdisciplinary Research in Biology (CIRB), Collège de France, CNRS, INSERM, PSL Research University, Paris, France
4Infection Antimicrobials Modelling Evolution, UMR 1137, INSERM, Université de Paris, Paris, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Sabine Chenivesse
2Sorbonne Universités, UPMC Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, F-29688 Roscoff cedex, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Sophie Lepanse
2Sorbonne Universités, UPMC Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, F-29688 Roscoff cedex, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Adèle James
2Sorbonne Universités, UPMC Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, F-29688 Roscoff cedex, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Rubén Barcia-Cruz
2Sorbonne Universités, UPMC Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, F-29688 Roscoff cedex, France
5Department of Microbiology and Parasitology, CIBUS-Faculty of Biology, Universidade de Santiago de Compostela, Santiago de Compostela, Spain
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Javier Dubert
2Sorbonne Universités, UPMC Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, F-29688 Roscoff cedex, France
6Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Bruno Petton
1Ifremer, Unité Physiologie Fonctionnelle des Organismes Marins, ZI de la Pointe du Diable, CS 10070, F-29280 Plouzané, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Erica Lieberman
7Eligo Bioscience, Paris, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
K. Mathias Wegner
8AWI - Alfred Wegener Institut - Helmholtz-Zentrum für Polar- und Meeresforschung, Coastal Ecology, Waddensea Station Sylt, Hafenstrasse 43, 25992 List, Germany
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Fatima A. Hussain
6Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Kathryn M. Kauffman
6Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA, USA
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Martin F. Polz
6Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA, USA
9Division of Microbial Ecology, Centre for Microbiology and Environmental Systems Science, University of Vienna, Vienna, Austria
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
David Bikard
10Synthetic Biology Group, Department of Microbiology, Institut Pasteur, Paris 75015, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Sylvain Gandon
11CEFE (UMR 5175 CNRS - Université de Montpellier - Université Paul Valéry - EPHE), Montpellier, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
Frédérique Le Roux
1Ifremer, Unité Physiologie Fonctionnelle des Organismes Marins, ZI de la Pointe du Diable, CS 10070, F-29280 Plouzané, France
2Sorbonne Universités, UPMC Paris 06, CNRS, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, CS 90074, F-29688 Roscoff cedex, France
  • Find this author on Google Scholar
  • Find this author on PubMed
  • Search for this author on this site
  • For correspondence: frederique.le-roux@sb-roscoff.fr
  • Abstract
  • Full Text
  • Info/History
  • Metrics
  • Supplementary material
  • Preview PDF
Loading

ABSTRACT

Coevolution between bacteriophage (or phage) and their bacterial host is thought to be key for the coexistence of these antagonists. Recent studies have revealed the major role of mobile genetic elements in the emergence of phage resistant hosts but how phage escape these defenses in the wild remained to be explored. Here we show a striking parallel in phage evolving counter defenses to host defenses in natural population. We established a large collection of phages and their bacterial hosts and we explored the genetic structure of their interaction. We find that clearly delineated genomic clusters of phage are specific for distinct clades within a bacterial species, Vibrio crassostreae, yet while all phages can adsorb, only a subset of hosts are killed due to intracellular defense mechanisms. Host genomes contain multiple mobile defense genes and susceptibility to phage is negatively correlated with genome size. Phages also display extensive gene content variation, but their genome size remains conserved. We show that this gene content variation in hosts and phage is due to rapid turnover of genes involved in defense and escape, and that by exchanging anti-defense genes, phages irreversibly switch host. This could be indicative of co-evolution following the matching-allele-model of specificity and the spatial and temporal variability of phage infectivity further suggests that negative-frequency dependent selection drives phage-vibrio coevolutionary dynamics. We propose a “pan-escape system” that can be shared among phages by homologous recombination within a population that infects a bacterial host.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
Back to top
PreviousNext
Posted May 05, 2021.
Download PDF

Supplementary Material

Email

Thank you for your interest in spreading the word about bioRxiv.

NOTE: Your email address is requested solely to identify you as the sender of this article.

Enter multiple addresses on separate lines or separate them with commas.
Genetic determinism of phage-bacteria coevolution in natural populations
(Your Name) has forwarded a page to you from bioRxiv
(Your Name) thought you would like to see this page from the bioRxiv website.
CAPTCHA
This question is for testing whether or not you are a human visitor and to prevent automated spam submissions.
Share
Genetic determinism of phage-bacteria coevolution in natural populations
Damien Piel, Maxime Bruto, Yannick Labreuche, Francois Blanquart, Sabine Chenivesse, Sophie Lepanse, Adèle James, Rubén Barcia-Cruz, Javier Dubert, Bruno Petton, Erica Lieberman, K. Mathias Wegner, Fatima A. Hussain, Kathryn M. Kauffman, Martin F. Polz, David Bikard, Sylvain Gandon, Frédérique Le Roux
bioRxiv 2021.05.05.442762; doi: https://doi.org/10.1101/2021.05.05.442762
Digg logo Reddit logo Twitter logo Facebook logo Google logo LinkedIn logo Mendeley logo
Citation Tools
Genetic determinism of phage-bacteria coevolution in natural populations
Damien Piel, Maxime Bruto, Yannick Labreuche, Francois Blanquart, Sabine Chenivesse, Sophie Lepanse, Adèle James, Rubén Barcia-Cruz, Javier Dubert, Bruno Petton, Erica Lieberman, K. Mathias Wegner, Fatima A. Hussain, Kathryn M. Kauffman, Martin F. Polz, David Bikard, Sylvain Gandon, Frédérique Le Roux
bioRxiv 2021.05.05.442762; doi: https://doi.org/10.1101/2021.05.05.442762

Citation Manager Formats

  • BibTeX
  • Bookends
  • EasyBib
  • EndNote (tagged)
  • EndNote 8 (xml)
  • Medlars
  • Mendeley
  • Papers
  • RefWorks Tagged
  • Ref Manager
  • RIS
  • Zotero
  • Tweet Widget
  • Facebook Like
  • Google Plus One

Subject Area

  • Microbiology
Subject Areas
All Articles
  • Animal Behavior and Cognition (3609)
  • Biochemistry (7585)
  • Bioengineering (5533)
  • Bioinformatics (20825)
  • Biophysics (10344)
  • Cancer Biology (7995)
  • Cell Biology (11653)
  • Clinical Trials (138)
  • Developmental Biology (6617)
  • Ecology (10224)
  • Epidemiology (2065)
  • Evolutionary Biology (13639)
  • Genetics (9557)
  • Genomics (12856)
  • Immunology (7930)
  • Microbiology (19568)
  • Molecular Biology (7675)
  • Neuroscience (42182)
  • Paleontology (308)
  • Pathology (1259)
  • Pharmacology and Toxicology (2208)
  • Physiology (3271)
  • Plant Biology (7058)
  • Scientific Communication and Education (1295)
  • Synthetic Biology (1953)
  • Systems Biology (5433)
  • Zoology (1119)