The virulence regulator CovR boosts CRISPR-Cas9 immunity in Group B Streptococcus

Abstract CRISPR-Cas9 immune systems protect bacteria from foreign DNA. However, immune efficiency is constrained by Cas9 off-target cleavages and toxicity. How bacteria regulate Cas9 to maximize protection while preventing autoimmunity is not understood. Here, we show that the master regulator of vi...

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Main Authors: Adeline Pastuszka, Maria-Vittoria Mazzuoli, Chiara Crestani, Léonie Deborde, Odile Sismeiro, Coralie Lemaire, Vanessa Rong, Myriam Gominet, Elise Jacquemet, Rachel Legendre, Philippe Lanotte, Arnaud Firon
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-60871-6
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author Adeline Pastuszka
Maria-Vittoria Mazzuoli
Chiara Crestani
Léonie Deborde
Odile Sismeiro
Coralie Lemaire
Vanessa Rong
Myriam Gominet
Elise Jacquemet
Rachel Legendre
Philippe Lanotte
Arnaud Firon
author_facet Adeline Pastuszka
Maria-Vittoria Mazzuoli
Chiara Crestani
Léonie Deborde
Odile Sismeiro
Coralie Lemaire
Vanessa Rong
Myriam Gominet
Elise Jacquemet
Rachel Legendre
Philippe Lanotte
Arnaud Firon
author_sort Adeline Pastuszka
collection DOAJ
description Abstract CRISPR-Cas9 immune systems protect bacteria from foreign DNA. However, immune efficiency is constrained by Cas9 off-target cleavages and toxicity. How bacteria regulate Cas9 to maximize protection while preventing autoimmunity is not understood. Here, we show that the master regulator of virulence, CovR, regulates CRISPR-Cas9 immunity against mobile genetic elements in Streptococcus agalactiae, a pathobiont responsible for invasive neonatal infections. We show that CovR binds to and represses a distal promoter of the cas operon, integrating immunity within the virulence regulatory network. The CovR-regulated promoter provides a controlled increase in off-target cleavages to counteract mutations in the target DNA, restores the potency of old immune memory, and stimulates the acquisition of new memory in response to recent infections. Regulation of Cas9 by CovR is conserved at the species level, with lineage specificities suggesting different adaptive trajectories. Altogether, we describe the coordinated regulation of immunity and virulence that enhances the bacterial immune repertoire during host-pathogen interaction.
format Article
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institution Kabale University
issn 2041-1723
language English
publishDate 2025-07-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj-art-bb19aa7a56144bd09fbd6018c34b0e3e2025-08-20T03:37:37ZengNature PortfolioNature Communications2041-17232025-07-0116111310.1038/s41467-025-60871-6The virulence regulator CovR boosts CRISPR-Cas9 immunity in Group B StreptococcusAdeline Pastuszka0Maria-Vittoria Mazzuoli1Chiara Crestani2Léonie Deborde3Odile Sismeiro4Coralie Lemaire5Vanessa Rong6Myriam Gominet7Elise Jacquemet8Rachel Legendre9Philippe Lanotte10Arnaud Firon11Université de Tours, INRAE, UMRInstitut Pasteur, Université Paris Cité, Department of MicrobiologyInstitut Pasteur, Université Paris Cité, Biodiversity and Epidemiology of Bacterial Pathogens, Department of Global HealthInstitut Pasteur, Université Paris Cité, Department of MicrobiologyInstitut Pasteur, Université Paris Cité, Department of MicrobiologyUniversité de Tours, INRAE, UMRUniversité de Tours, INRAE, UMRInstitut Pasteur, Université Paris Cité, Department of MicrobiologyInstitut Pasteur, Université Paris Cité, Bioinformatics and Biostatistics HubInstitut Pasteur, Université Paris Cité, Bioinformatics and Biostatistics HubUniversité de Tours, INRAE, UMRInstitut Pasteur, Université Paris Cité, Department of MicrobiologyAbstract CRISPR-Cas9 immune systems protect bacteria from foreign DNA. However, immune efficiency is constrained by Cas9 off-target cleavages and toxicity. How bacteria regulate Cas9 to maximize protection while preventing autoimmunity is not understood. Here, we show that the master regulator of virulence, CovR, regulates CRISPR-Cas9 immunity against mobile genetic elements in Streptococcus agalactiae, a pathobiont responsible for invasive neonatal infections. We show that CovR binds to and represses a distal promoter of the cas operon, integrating immunity within the virulence regulatory network. The CovR-regulated promoter provides a controlled increase in off-target cleavages to counteract mutations in the target DNA, restores the potency of old immune memory, and stimulates the acquisition of new memory in response to recent infections. Regulation of Cas9 by CovR is conserved at the species level, with lineage specificities suggesting different adaptive trajectories. Altogether, we describe the coordinated regulation of immunity and virulence that enhances the bacterial immune repertoire during host-pathogen interaction.https://doi.org/10.1038/s41467-025-60871-6
spellingShingle Adeline Pastuszka
Maria-Vittoria Mazzuoli
Chiara Crestani
Léonie Deborde
Odile Sismeiro
Coralie Lemaire
Vanessa Rong
Myriam Gominet
Elise Jacquemet
Rachel Legendre
Philippe Lanotte
Arnaud Firon
The virulence regulator CovR boosts CRISPR-Cas9 immunity in Group B Streptococcus
Nature Communications
title The virulence regulator CovR boosts CRISPR-Cas9 immunity in Group B Streptococcus
title_full The virulence regulator CovR boosts CRISPR-Cas9 immunity in Group B Streptococcus
title_fullStr The virulence regulator CovR boosts CRISPR-Cas9 immunity in Group B Streptococcus
title_full_unstemmed The virulence regulator CovR boosts CRISPR-Cas9 immunity in Group B Streptococcus
title_short The virulence regulator CovR boosts CRISPR-Cas9 immunity in Group B Streptococcus
title_sort virulence regulator covr boosts crispr cas9 immunity in group b streptococcus
url https://doi.org/10.1038/s41467-025-60871-6
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