DNA targeting and interference by a bacterial Argonaute nuclease

Anton Kuzmenko (), Anastasiya Oguienko, Daria Esyunina, Denis Yudin, Mayya Petrova, Alina Kudinova, Olga Maslova, Maria Ninova, Sergei Ryazansky, David Leach, Alexei A. Aravin () and Andrey Kulbachinskiy ()
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Anton Kuzmenko: Institute of Molecular Genetics, Russian Academy of Sciences
Anastasiya Oguienko: Institute of Molecular Genetics, Russian Academy of Sciences
Daria Esyunina: Institute of Molecular Genetics, Russian Academy of Sciences
Denis Yudin: Institute of Molecular Genetics, Russian Academy of Sciences
Mayya Petrova: Institute of Molecular Genetics, Russian Academy of Sciences
Alina Kudinova: Institute of Molecular Genetics, Russian Academy of Sciences
Olga Maslova: Institute of Molecular Genetics, Russian Academy of Sciences
Maria Ninova: California Institute of Technology
Sergei Ryazansky: Institute of Molecular Genetics, Russian Academy of Sciences
David Leach: University of Edinburgh
Alexei A. Aravin: Institute of Molecular Genetics, Russian Academy of Sciences
Andrey Kulbachinskiy: Institute of Molecular Genetics, Russian Academy of Sciences

Nature, 2020, vol. 587, issue 7835, 632-637

Abstract: Abstract Members of the conserved Argonaute protein family use small RNA guides to locate their mRNA targets and regulate gene expression and suppress mobile genetic elements in eukaryotes1,2. Argonautes are also present in many bacterial and archaeal species3–5. Unlike eukaryotic proteins, several prokaryotic Argonaute proteins use small DNA guides to cleave DNA, a process known as DNA interference6–10. However, the natural functions and targets of DNA interference are poorly understood, and the mechanisms of DNA guide generation and target discrimination remain unknown. Here we analyse the activity of a bacterial Argonaute nuclease from Clostridium butyricum (CbAgo) in vivo. We show that CbAgo targets multicopy genetic elements and suppresses the propagation of plasmids and infection by phages. CbAgo induces DNA interference between homologous sequences and triggers DNA degradation at double-strand breaks in the target DNA. The loading of CbAgo with locus-specific small DNA guides depends on both its intrinsic endonuclease activity and the cellular double-strand break repair machinery. A similar interaction was reported for the acquisition of new spacers during CRISPR adaptation, and prokaryotic genomes that encode Ago nucleases are enriched in CRISPR–Cas systems. These results identify molecular mechanisms that generate guides for DNA interference and suggest that the recognition of foreign nucleic acids by prokaryotic defence systems involves common principles.

Date: 2020
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DOI: 10.1038/s41586-020-2605-1

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