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Cbp1 and Cren7 form chromatin-like structures that ensure efficient transcription of long CRISPR arrays

Author

Listed:
  • Fabian Blombach

    (University College London)

  • Michal Sýkora

    (University College London)

  • Jo Case

    (University College London)

  • Xu Feng

    (Microbial Technology Institute, Shandong University)

  • Diana P. Baquero

    (Institut Pasteur, Université Paris Cité, CNRS UMR6047, Archaeal Virology Unit)

  • Thomas Fouqueau

    (University College London)

  • Duy Khanh Phung

    (University College London)

  • Declan Barker

    (University College London)

  • Mart Krupovic

    (Institut Pasteur, Université Paris Cité, CNRS UMR6047, Archaeal Virology Unit)

  • Qunxin She

    (Microbial Technology Institute, Shandong University)

  • Finn Werner

    (University College London)

Abstract

CRISPR arrays form the physical memory of CRISPR adaptive immune systems by incorporating foreign DNA as spacers that are often AT-rich and derived from viruses. As promoter elements such as the TATA-box are AT-rich, CRISPR arrays are prone to harbouring cryptic promoters. Sulfolobales harbour extremely long CRISPR arrays spanning several kilobases, a feature that is accompanied by the CRISPR-specific transcription factor Cbp1. Aberrant Cbp1 expression modulates CRISPR array transcription, but the molecular mechanisms underlying this regulation are unknown. Here, we characterise the genome-wide Cbp1 binding at nucleotide resolution and characterise the binding motifs on distinct CRISPR arrays, as well as on unexpected non-canonical binding sites associated with transposons. Cbp1 recruits Cren7 forming together ‘chimeric’ chromatin-like structures at CRISPR arrays. We dissect Cbp1 function in vitro and in vivo and show that the third helix-turn-helix domain is responsible for Cren7 recruitment, and that Cbp1-Cren7 chromatinization plays a dual role in the transcription of CRISPR arrays. It suppresses spurious transcription from cryptic promoters within CRISPR arrays but enhances CRISPR RNA transcription directed from their cognate promoters in their leader region. Our results show that Cbp1-Cren7 chromatinization drives the productive expression of long CRISPR arrays.

Suggested Citation

  • Fabian Blombach & Michal Sýkora & Jo Case & Xu Feng & Diana P. Baquero & Thomas Fouqueau & Duy Khanh Phung & Declan Barker & Mart Krupovic & Qunxin She & Finn Werner, 2024. "Cbp1 and Cren7 form chromatin-like structures that ensure efficient transcription of long CRISPR arrays," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45728-8
    DOI: 10.1038/s41467-024-45728-8
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    References listed on IDEAS

    as
    1. Changyi Zhang & Alex P. R. Phillips & Rebecca L. Wipfler & Gary J. Olsen & Rachel J. Whitaker, 2018. "The essential genome of the crenarchaeal model Sulfolobus islandicus," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    2. Fabian Blombach & Thomas Fouqueau & Dorota Matelska & Katherine Smollett & Finn Werner, 2021. "Promoter-proximal elongation regulates transcription in archaea," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
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