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Programmable RNA targeting by bacterial Argonaute nucleases with unconventional guide binding and cleavage specificity

Author

Listed:
  • Lidiya Lisitskaya

    (Institute of Molecular Genetics, National Research Center “Kurchatov Institute”
    Russian Academy of Sciences)

  • Yeonoh Shin

    (Pennsylvania State University
    Columbia University)

  • Aleksei Agapov

    (Institute of Molecular Genetics, National Research Center “Kurchatov Institute”)

  • Anna Olina

    (Institute of Molecular Genetics, National Research Center “Kurchatov Institute”)

  • Ekaterina Kropocheva

    (Institute of Molecular Genetics, National Research Center “Kurchatov Institute”)

  • Sergei Ryazansky

    (Institute of Molecular Genetics, National Research Center “Kurchatov Institute”)

  • Alexei A. Aravin

    (Division of Biology and Biological Engineering, California Institute of Technology)

  • Daria Esyunina

    (Institute of Molecular Genetics, National Research Center “Kurchatov Institute”)

  • Katsuhiko S. Murakami

    (Pennsylvania State University)

  • Andrey Kulbachinskiy

    (Institute of Molecular Genetics, National Research Center “Kurchatov Institute”
    Russian Academy of Sciences)

Abstract

Argonaute proteins are programmable nucleases that have defense and regulatory functions in both eukaryotes and prokaryotes. All known prokaryotic Argonautes (pAgos) characterized so far act on DNA targets. Here, we describe a new class of pAgos that uniquely use DNA guides to process RNA targets. The biochemical and structural analysis of Pseudooceanicola lipolyticus pAgo (PliAgo) reveals an unusual organization of the guide binding pocket that does not rely on divalent cations and the canonical set of contacts for 5’-end interactions. Unconventional interactions of PliAgo with the 5’-phosphate of guide DNA define its new position within pAgo and shift the site of target RNA cleavage in comparison with known Argonautes. The specificity for RNA over DNA is defined by ribonucleotide residues at the cleavage site. The analysed pAgos sense mismatches and modifications in the RNA target. The results broaden our understanding of prokaryotic defense systems and extend the spectrum of programmable nucleases with potential use in RNA technology.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-32079-5
    DOI: 10.1038/s41467-022-32079-5
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    References listed on IDEAS

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    Cited by:

    1. Xinmi Song & Sheng Lei & Shunhang Liu & Yanqiu Liu & Pan Fu & Zhifeng Zeng & Ke Yang & Yu Chen & Ming Li & Qunxin She & Wenyuan Han, 2023. "Catalytically inactive long prokaryotic Argonaute systems employ distinct effectors to confer immunity via abortive infection," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Xiangkai Zhen & Xiaolong Xu & Le Ye & Song Xie & Zhijie Huang & Sheng Yang & Yanhui Wang & Jinyu Li & Feng Long & Songying Ouyang, 2024. "Structural basis of antiphage immunity generated by a prokaryotic Argonaute-associated SPARSA system," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

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