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PreprintCited by 93Bacteriophages and microbial interactionsInvertebrate Immune Response MechanismsCRISPR and Genetic Engineering

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A conserved family of immune effectors cleaves cellular ATP upon viral infection

Open access
Rousset, Francois, Yirmiya, Erez, Nesher, Shahar, Brandis, Alexander, Mehlman, Tevie, Itkin, Maxim, Malitsky, Sergey, Millman, Adi, Melamed, Sarah, Sorek, Rotem·2023·Cell
DOI 10.1101/2023.01.24.525353

Preprint — published as 10.1016/j.cell.2023.07.020

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Abstract

Summary: During viral infection, cells can deploy immune strategies that deprive viruses of molecules essential for their replication. In this study, we report a family of immune effectors in bacteria which, in response to phage infection, degrade cellular ATP and dATP by cleaving the N-glycosidic bond between the adenine and sugar moieties. These ATP nucleosidase effectors are widely distributed within multiple bacterial defense systems including CBASS, prokaryotic argonautes and NLR-like proteins, and we show that degradation of (d)ATP during infection halts phage propagation and aborts infection. By analyzing homologs of the immune ATP nucleosidase domain, we discover and characterize Detocs, a new family of bacterial defense systems with a two-component phosphotransfer signaling architecture. The immune ATP nucleosidase domain is also encoded within a diverse set of eukaryotic proteins that have immune-like architectures, and we show biochemically that these eukaryotic homologs preserve the ATP nucleosidase activity. Our findings suggest that ATP and dATP degradation is a cell-autonomous innate immune strategy conserved across the tree of life.

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Metadata

Authors
Rousset, F., Yirmiya, E., Nesher, S., Brandis, A., Mehlman, T., Itkin, M., Malitsky, S., Millman, A., Melamed, S., & Sorek, R.
Affiliations
Weizmann Institute of Science (IL)
Corresponding author
Sorek, Rotem
ORCID
Venue
Cell
Publisher
openRxiv
Published
2023-01-24
Volume
186
Issue
17
Pages
3619-3631.e13
ISSN
0092-8674 (ISSN-L)
DOI
10.1101/2023.01.24.525353
OpenAlex
W4385949307
Cited by
93
References
1
Citations by year
2026: 19 · 2025: 31 · 2024: 27 · 2023: 16
FWCI
15.08
Type
journal article
Language
en
Open access
Locations
  • Cell (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
Funders
  • Knell Family Center for Microbiology, Weizmann Institute of Science
  • Deutsche Forschungsgemeinschaft (464312965, SPP2330)
  • Weizmann Institute of Science
  • Israel Science Foundation (2720/22)
  • Council for Higher Education
  • European Research Council
  • Division of Chemistry
  • H2020 European Research Council (ERC-AdG GA 101018520)
Topics
  • Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
  • Life Sciences › Immunology and Microbiology › Immunology › Invertebrate Immune Response Mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
Keywords
phage infection, two-component systems, prokaryotic Argonaute, ATP degradation, N-glycosidic bond cleavage, cell-autonomous immunity
MeSH terms
Adenosine Triphosphate, Eukaryotic Cells, Humans, N-Glycosyl Hydrolases, Prokaryotic Cells, Virus Diseases

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