Competition and coevolution drive the evolution and the diversification of CRISPR immunity

Martin Guillemet; Hélène Chabas; Antoine Nicot; François Gatchich; Enrique Ortega-Abboud; Cornelia Buus; Lotte Hindhede; Geneviève M. Rousseau; Thomas Bataillon; Sylvain Moineau; Sylvain Gandon

doi:10.1038/s41559-022-01841-9

Competition and coevolution drive the evolution and the diversification of CRISPR immunity

Martin Guillemet, Hélène Chabas, Antoine Nicot, François Gatchich, Enrique Ortega-Abboud, Cornelia Buus, Lotte Hindhede, Geneviève M. Rousseau, Thomas Bataillon, Sylvain Moineau, Sylvain Gandon^*

^*Corresponding author af dette arbejde

Publikation: Bidrag til tidsskrift/Konferencebidrag i tidsskrift /Bidrag til avis › Tidsskriftartikel › Forskning › peer review

10 Citationer (Scopus)

Abstract

The diversity of resistance challenges the ability of pathogens to spread and to exploit host populations. Yet, how this host diversity evolves over time remains unclear because it depends on the interplay between intraspecific competition among host genotypes and coevolution with pathogens. Here we study experimentally the effect of coevolving phage populations on the diversification of bacterial CRISPR immunity across space and time. We demonstrate that the negative-frequency-dependent selection generated by coevolution is a powerful force that maintains host resistance diversity and selects for new resistance mutations in the host. We also find that host evolution is driven by asymmetries in competitive abilities among different host genotypes. Even if the fittest host genotypes are targeted preferentially by the evolving phages, they often escape extinctions through the acquisition of new CRISPR immunity. Together, these fluctuating selective pressures maintain diversity, but not by preserving the pre-existing host composition. Instead, we repeatedly observe the introduction of new resistance genotypes stemming from the fittest hosts in each population. These results highlight the importance of competition on the transient dynamics of host–pathogen coevolution.

Originalsprog	Engelsk
Tidsskrift	Nature Ecology & Evolution
Vol/bind	6
Nummer	10
Sider (fra-til)	1480-1488
Antal sider	9
ISSN	2397-334X
DOI	https://doi.org/10.1038/s41559-022-01841-9
Status	Udgivet - okt. 2022

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10.1038/s41559-022-01841-9

https://www.biorxiv.org/content/biorxiv/early/2022/05/11/2021.11.12.468349.full.pdf

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title = "Competition and coevolution drive the evolution and the diversification of CRISPR immunity",

abstract = "The diversity of resistance challenges the ability of pathogens to spread and to exploit host populations. Yet, how this host diversity evolves over time remains unclear because it depends on the interplay between intraspecific competition among host genotypes and coevolution with pathogens. Here we study experimentally the effect of coevolving phage populations on the diversification of bacterial CRISPR immunity across space and time. We demonstrate that the negative-frequency-dependent selection generated by coevolution is a powerful force that maintains host resistance diversity and selects for new resistance mutations in the host. We also find that host evolution is driven by asymmetries in competitive abilities among different host genotypes. Even if the fittest host genotypes are targeted preferentially by the evolving phages, they often escape extinctions through the acquisition of new CRISPR immunity. Together, these fluctuating selective pressures maintain diversity, but not by preserving the pre-existing host composition. Instead, we repeatedly observe the introduction of new resistance genotypes stemming from the fittest hosts in each population. These results highlight the importance of competition on the transient dynamics of host–pathogen coevolution.",

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author = "Martin Guillemet and H{\'e}l{\`e}ne Chabas and Antoine Nicot and Fran{\c c}ois Gatchich and Enrique Ortega-Abboud and Cornelia Buus and Lotte Hindhede and Rousseau, {Genevi{\`e}ve M.} and Thomas Bataillon and Sylvain Moineau and Sylvain Gandon",

note = "Funding Information: Sequencing data were obtained through the genotyping and sequencing facilities of the Institut des Sciences de l{\textquoteright}Evolution-Montpellier and Labex Centre M{\'e}diterran{\'e}en Environnement Biodiversit{\'e}. We thank D. Tremblay, P.-L. Plante and G. Pageau for technical assistance during the sequencing of the bacterial strains. S.M. acknowledges funding from the Natural Sciences and Engineering Research Council of Canada (Discovery program). S.M. holds a T1 Canada Research Chair in Bacteriophages. H.C. was supported by an ETH Zurich Postdoctoral Fellowship. S.G. acknowledges support from a grant on {\textquoteleft}Phylodynamics for experimentally evolving viruses{\textquoteright} funded by the CNRS-MITI (Mission pour les Initiatives Transverses et Interdisciplinaires) and from the grant no. ANR-17-CE35-0012 from the Agence National de la Recherche. Funding Information: Sequencing data were obtained through the genotyping and sequencing facilities of the Institut des Sciences de l{\textquoteright}Evolution-Montpellier and Labex Centre M{\'e}diterran{\'e}en Environnement Biodiversit{\'e}. We thank D. Tremblay, P.-L. Plante and G. Pageau for technical assistance during the sequencing of the bacterial strains. S.M. acknowledges funding from the Natural Sciences and Engineering Research Council of Canada (Discovery program). S.M. holds a T1 Canada Research Chair in Bacteriophages. H.C. was supported by an ETH Zurich Postdoctoral Fellowship. S.G. acknowledges support from a grant on {\textquoteleft}Phylodynamics for experimentally evolving viruses{\textquoteright} funded by the CNRS-MITI (Mission pour les Initiatives Transverses et Interdisciplinaires) and from the grant no. ANR-17-CE35-0012 from the Agence National de la Recherche. Publisher Copyright: {\textcopyright} 2022, The Author(s), under exclusive licence to Springer Nature Limited.",

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doi = "10.1038/s41559-022-01841-9",

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AU - Chabas, Hélène

AU - Nicot, Antoine

AU - Gatchich, François

AU - Ortega-Abboud, Enrique

AU - Buus, Cornelia

AU - Hindhede, Lotte

AU - Rousseau, Geneviève M.

AU - Bataillon, Thomas

AU - Moineau, Sylvain

AU - Gandon, Sylvain

N1 - Funding Information: Sequencing data were obtained through the genotyping and sequencing facilities of the Institut des Sciences de l’Evolution-Montpellier and Labex Centre Méditerranéen Environnement Biodiversité. We thank D. Tremblay, P.-L. Plante and G. Pageau for technical assistance during the sequencing of the bacterial strains. S.M. acknowledges funding from the Natural Sciences and Engineering Research Council of Canada (Discovery program). S.M. holds a T1 Canada Research Chair in Bacteriophages. H.C. was supported by an ETH Zurich Postdoctoral Fellowship. S.G. acknowledges support from a grant on ‘Phylodynamics for experimentally evolving viruses’ funded by the CNRS-MITI (Mission pour les Initiatives Transverses et Interdisciplinaires) and from the grant no. ANR-17-CE35-0012 from the Agence National de la Recherche. Funding Information: Sequencing data were obtained through the genotyping and sequencing facilities of the Institut des Sciences de l’Evolution-Montpellier and Labex Centre Méditerranéen Environnement Biodiversité. We thank D. Tremblay, P.-L. Plante and G. Pageau for technical assistance during the sequencing of the bacterial strains. S.M. acknowledges funding from the Natural Sciences and Engineering Research Council of Canada (Discovery program). S.M. holds a T1 Canada Research Chair in Bacteriophages. H.C. was supported by an ETH Zurich Postdoctoral Fellowship. S.G. acknowledges support from a grant on ‘Phylodynamics for experimentally evolving viruses’ funded by the CNRS-MITI (Mission pour les Initiatives Transverses et Interdisciplinaires) and from the grant no. ANR-17-CE35-0012 from the Agence National de la Recherche. Publisher Copyright: © 2022, The Author(s), under exclusive licence to Springer Nature Limited.

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N2 - The diversity of resistance challenges the ability of pathogens to spread and to exploit host populations. Yet, how this host diversity evolves over time remains unclear because it depends on the interplay between intraspecific competition among host genotypes and coevolution with pathogens. Here we study experimentally the effect of coevolving phage populations on the diversification of bacterial CRISPR immunity across space and time. We demonstrate that the negative-frequency-dependent selection generated by coevolution is a powerful force that maintains host resistance diversity and selects for new resistance mutations in the host. We also find that host evolution is driven by asymmetries in competitive abilities among different host genotypes. Even if the fittest host genotypes are targeted preferentially by the evolving phages, they often escape extinctions through the acquisition of new CRISPR immunity. Together, these fluctuating selective pressures maintain diversity, but not by preserving the pre-existing host composition. Instead, we repeatedly observe the introduction of new resistance genotypes stemming from the fittest hosts in each population. These results highlight the importance of competition on the transient dynamics of host–pathogen coevolution.

AB - The diversity of resistance challenges the ability of pathogens to spread and to exploit host populations. Yet, how this host diversity evolves over time remains unclear because it depends on the interplay between intraspecific competition among host genotypes and coevolution with pathogens. Here we study experimentally the effect of coevolving phage populations on the diversification of bacterial CRISPR immunity across space and time. We demonstrate that the negative-frequency-dependent selection generated by coevolution is a powerful force that maintains host resistance diversity and selects for new resistance mutations in the host. We also find that host evolution is driven by asymmetries in competitive abilities among different host genotypes. Even if the fittest host genotypes are targeted preferentially by the evolving phages, they often escape extinctions through the acquisition of new CRISPR immunity. Together, these fluctuating selective pressures maintain diversity, but not by preserving the pre-existing host composition. Instead, we repeatedly observe the introduction of new resistance genotypes stemming from the fittest hosts in each population. These results highlight the importance of competition on the transient dynamics of host–pathogen coevolution.

KW - Bacteria/genetics

KW - Bacteriophages/genetics

KW - Clustered Regularly Interspaced Short Palindromic Repeats

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Competition and coevolution drive the evolution and the diversification of CRISPR immunity

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