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The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA

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  • Josiane E. Garneau

    (de microbiologie et de bio-informatique, Faculté des sciences et de génie, Groupe de recherche en écologie buccale, Faculté de médecine dentaire, Félix d’Hérelle Reference Center for Bacterial Viruses, Université Laval)

  • Marie-Ève Dupuis

    (de microbiologie et de bio-informatique, Faculté des sciences et de génie, Groupe de recherche en écologie buccale, Faculté de médecine dentaire, Félix d’Hérelle Reference Center for Bacterial Viruses, Université Laval)

  • Manuela Villion

    (de microbiologie et de bio-informatique, Faculté des sciences et de génie, Groupe de recherche en écologie buccale, Faculté de médecine dentaire, Félix d’Hérelle Reference Center for Bacterial Viruses, Université Laval)

  • Dennis A. Romero

    (Danisco USA Inc., 3329 Agriculture Drive)

  • Rodolphe Barrangou

    (Danisco USA Inc., 3329 Agriculture Drive)

  • Patrick Boyaval

    (Danisco France SAS, Boîte Postale 10, F-86220 Dangé-Saint-Romain, France)

  • Christophe Fremaux

    (Danisco France SAS, Boîte Postale 10, F-86220 Dangé-Saint-Romain, France)

  • Philippe Horvath

    (Danisco France SAS, Boîte Postale 10, F-86220 Dangé-Saint-Romain, France)

  • Alfonso H. Magadán

    (de microbiologie et de bio-informatique, Faculté des sciences et de génie, Groupe de recherche en écologie buccale, Faculté de médecine dentaire, Félix d’Hérelle Reference Center for Bacterial Viruses, Université Laval)

  • Sylvain Moineau

    (de microbiologie et de bio-informatique, Faculté des sciences et de génie, Groupe de recherche en écologie buccale, Faculté de médecine dentaire, Félix d’Hérelle Reference Center for Bacterial Viruses, Université Laval)

Abstract

Bacteria and Archaea have developed several defence strategies against foreign nucleic acids such as viral genomes and plasmids. Among them, clustered regularly interspaced short palindromic repeats (CRISPR) loci together with cas (CRISPR-associated) genes form the CRISPR/Cas immune system, which involves partially palindromic repeats separated by short stretches of DNA called spacers, acquired from extrachromosomal elements. It was recently demonstrated that these variable loci can incorporate spacers from infecting bacteriophages and then provide immunity against subsequent bacteriophage infections in a sequence-specific manner. Here we show that the Streptococcus thermophilus CRISPR1/Cas system can also naturally acquire spacers from a self-replicating plasmid containing an antibiotic-resistance gene, leading to plasmid loss. Acquired spacers that match antibiotic-resistance genes provide a novel means to naturally select bacteria that cannot uptake and disseminate such genes. We also provide in vivo evidence that the CRISPR1/Cas system specifically cleaves plasmid and bacteriophage double-stranded DNA within the proto-spacer, at specific sites. Our data show that the CRISPR/Cas immune system is remarkably adapted to cleave invading DNA rapidly and has the potential for exploitation to generate safer microbial strains.

Suggested Citation

  • Josiane E. Garneau & Marie-Ève Dupuis & Manuela Villion & Dennis A. Romero & Rodolphe Barrangou & Patrick Boyaval & Christophe Fremaux & Philippe Horvath & Alfonso H. Magadán & Sylvain Moineau, 2010. "The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA," Nature, Nature, vol. 468(7320), pages 67-71, November.
  • Handle: RePEc:nat:nature:v:468:y:2010:i:7320:d:10.1038_nature09523
    DOI: 10.1038/nature09523
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    Citations

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    Cited by:

    1. Kuang Hu & Chia-Wei Chou & Claus O. Wilke & Ilya J. Finkelstein, 2024. "Distinct horizontal transfer mechanisms for type I and type V CRISPR-associated transposons," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. Xuan Zou & Xiaohong Xiao & Ziran Mo & Yashi Ge & Xing Jiang & Ruolin Huang & Mengxue Li & Zixin Deng & Shi Chen & Lianrong Wang & Sang Yup Lee, 2022. "Systematic strategies for developing phage resistant Escherichia coli strains," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Pierre Aldag & Marius Rutkauskas & Julene Madariaga-Marcos & Inga Songailiene & Tomas Sinkunas & Felix Kemmerich & Dominik Kauert & Virginijus Siksnys & Ralf Seidel, 2023. "Dynamic interplay between target search and recognition for a Type I CRISPR-Cas system," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Xieshuting Deng & Wei Sun & Xueyan Li & Jiuyu Wang & Zhi Cheng & Gang Sheng & Yanli Wang, 2024. "An anti-CRISPR that represses its own transcription while blocking Cas9-target DNA binding," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    5. Eman A. Ageely & Ramadevi Chilamkurthy & Sunit Jana & Leonora Abdullahu & Daniel O’Reilly & Philip J. Jensik & Masad J. Damha & Keith T. Gagnon, 2021. "Gene editing with CRISPR-Cas12a guides possessing ribose-modified pseudoknot handles," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    6. Matteo Ciciani & Michele Demozzi & Eleonora Pedrazzoli & Elisabetta Visentin & Laura Pezzè & Lorenzo Federico Signorini & Aitor Blanco-Miguez & Moreno Zolfo & Francesco Asnicar & Antonio Casini & Anna, 2022. "Automated identification of sequence-tailored Cas9 proteins using massive metagenomic data," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    7. Cécile Philippe & Carlee Morency & Pier-Luc Plante & Edwige Zufferey & Rodrigo Achigar & Denise M. Tremblay & Geneviève M. Rousseau & Adeline Goulet & Sylvain Moineau, 2022. "A truncated anti-CRISPR protein prevents spacer acquisition but not interference," Nature Communications, Nature, vol. 13(1), pages 1-8, December.

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