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CRISPR adaptation biases explain preference for acquisition of foreign DNA

Author

Listed:
  • Asaf Levy

    (Weizmann Institute of Science)

  • Moran G. Goren

    (Sackler School of Medicine, Tel Aviv University)

  • Ido Yosef

    (Sackler School of Medicine, Tel Aviv University)

  • Oren Auster

    (Sackler School of Medicine, Tel Aviv University)

  • Miriam Manor

    (Sackler School of Medicine, Tel Aviv University)

  • Gil Amitai

    (Weizmann Institute of Science)

  • Rotem Edgar

    (Sackler School of Medicine, Tel Aviv University)

  • Udi Qimron

    (Sackler School of Medicine, Tel Aviv University)

  • Rotem Sorek

    (Weizmann Institute of Science)

Abstract

CRISPR–Cas (clustered, regularly interspaced short palindromic repeats coupled with CRISPR-associated proteins) is a bacterial immunity system that protects against invading phages or plasmids. In the process of CRISPR adaptation, short pieces of DNA (‘spacers’) are acquired from foreign elements and integrated into the CRISPR array. So far, it has remained a mystery how spacers are preferentially acquired from the foreign DNA while the self chromosome is avoided. Here we show that spacer acquisition is replication-dependent, and that DNA breaks formed at stalled replication forks promote spacer acquisition. Chromosomal hotspots of spacer acquisition were confined by Chi sites, which are sequence octamers highly enriched on the bacterial chromosome, suggesting that these sites limit spacer acquisition from self DNA. We further show that the avoidance of self is mediated by the RecBCD double-stranded DNA break repair complex. Our results suggest that, in Escherichia coli, acquisition of new spacers largely depends on RecBCD-mediated processing of double-stranded DNA breaks occurring primarily at replication forks, and that the preference for foreign DNA is achieved through the higher density of Chi sites on the self chromosome, in combination with the higher number of forks on the foreign DNA. This model explains the strong preference to acquire spacers both from high copy plasmids and from phages.

Suggested Citation

  • Asaf Levy & Moran G. Goren & Ido Yosef & Oren Auster & Miriam Manor & Gil Amitai & Rotem Edgar & Udi Qimron & Rotem Sorek, 2015. "CRISPR adaptation biases explain preference for acquisition of foreign DNA," Nature, Nature, vol. 520(7548), pages 505-510, April.
  • Handle: RePEc:nat:nature:v:520:y:2015:i:7548:d:10.1038_nature14302
    DOI: 10.1038/nature14302
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    Cited by:

    1. Serena Bradde & Marija Vucelja & Tiberiu Teşileanu & Vijay Balasubramanian, 2017. "Dynamics of adaptive immunity against phage in bacterial populations," PLOS Computational Biology, Public Library of Science, vol. 13(4), pages 1-16, April.
    2. Lidiya Lisitskaya & Yeonoh Shin & Aleksei Agapov & Anna Olina & Ekaterina Kropocheva & Sergei Ryazansky & Alexei A. Aravin & Daria Esyunina & Katsuhiko S. Murakami & Andrey Kulbachinskiy, 2022. "Programmable RNA targeting by bacterial Argonaute nucleases with unconventional guide binding and cleavage specificity," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. Jack P. K. Bravo & Cristian Aparicio-Maldonado & Franklin L. Nobrega & Stan J. J. Brouns & David W. Taylor, 2022. "Structural basis for broad anti-phage immunity by DISARM," Nature Communications, Nature, vol. 13(1), pages 1-11, December.

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