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Asgard archaea defense systems and their roles in the origin of eukaryotic immunity

Author

Listed:
  • Pedro Leão

    (University of Texas at Austin
    University of Texas at Austin
    Radboud University)

  • Mary E. Little

    (University of Texas at Austin)

  • Kathryn E. Appler

    (University of Texas at Austin)

  • Daphne Sahaya

    (University of Texas at Austin)

  • Emily Aguilar-Pine

    (University of Texas at Austin)

  • Kathryn Currie

    (University of Texas at Austin)

  • Ilya J. Finkelstein

    (University of Texas at Austin
    University of Texas at Austin)

  • Valerie Anda

    (University of Texas at Austin
    University of Texas at Austin)

  • Brett J. Baker

    (University of Texas at Austin
    University of Texas at Austin)

Abstract

Dozens of new antiviral systems have been recently characterized in bacteria. Some of these systems are present in eukaryotes and appear to have originated in prokaryotes, but little is known about these defense mechanisms in archaea. Here, we explore the diversity and distribution of defense systems in archaea and identify 2610 complete systems in Asgardarchaeota, a group of archaea related to eukaryotes. The Asgard defense systems comprise 89 unique systems, including argonaute, NLR, Mokosh, viperin, Lassamu, and CBASS. Asgard viperin and argonaute proteins have structural homology to eukaryotic proteins, and phylogenetic analyses suggest that eukaryotic viperin proteins were derived from Asgard viperins. We show that Asgard viperins display anti-phage activity when heterologously expressed in bacteria. Eukaryotic and bacterial argonaute proteins appear to have originated in Asgardarchaeota, and Asgard argonaute proteins have argonaute-PIWI domains, key components of eukaryotic RNA interference systems. Our results support that Asgardarchaeota played important roles in the origin of antiviral defense systems in eukaryotes.

Suggested Citation

  • Pedro Leão & Mary E. Little & Kathryn E. Appler & Daphne Sahaya & Emily Aguilar-Pine & Kathryn Currie & Ilya J. Finkelstein & Valerie Anda & Brett J. Baker, 2024. "Asgard archaea defense systems and their roles in the origin of eukaryotic immunity," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50195-2
    DOI: 10.1038/s41467-024-50195-2
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    References listed on IDEAS

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    1. Florian Tesson & Alexandre Hervé & Ernest Mordret & Marie Touchon & Camille d’Humières & Jean Cury & Aude Bernheim, 2022. "Systematic and quantitative view of the antiviral arsenal of prokaryotes," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    2. Carolien Bastiaanssen & Pilar Bobadilla Ugarte & Kijun Kim & Giada Finocchio & Yanlei Feng & Todd A. Anzelon & Stephan Köstlbacher & Daniel Tamarit & Thijs J. G. Ettema & Martin Jinek & Ian J. MacRae , 2024. "RNA-guided RNA silencing by an Asgard archaeal Argonaute," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Aude Bernheim & Adi Millman & Gal Ofir & Gilad Meitav & Carmel Avraham & Helena Shomar & Masha M. Rosenberg & Nir Tal & Sarah Melamed & Gil Amitai & Rotem Sorek, 2021. "Prokaryotic viperins produce diverse antiviral molecules," Nature, Nature, vol. 589(7840), pages 120-124, January.
    4. Scott M. Hammond & Emily Bernstein & David Beach & Gregory J. Hannon, 2000. "An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells," Nature, Nature, vol. 404(6775), pages 293-296, March.
    5. Katarzyna Zaremba-Niedzwiedzka & Eva F. Caceres & Jimmy H. Saw & Disa Bäckström & Lina Juzokaite & Emmelien Vancaester & Kiley W. Seitz & Karthik Anantharaman & Piotr Starnawski & Kasper U. Kjeldsen &, 2017. "Asgard archaea illuminate the origin of eukaryotic cellular complexity," Nature, Nature, vol. 541(7637), pages 353-358, January.
    6. Laura Eme & Daniel Tamarit & Eva F. Caceres & Courtney W. Stairs & Valerie Anda & Max E. Schön & Kiley W. Seitz & Nina Dombrowski & William H. Lewis & Felix Homa & Jimmy H. Saw & Jonathan Lombard & Ta, 2023. "Inference and reconstruction of the heimdallarchaeial ancestry of eukaryotes," Nature, Nature, vol. 618(7967), pages 992-999, June.
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