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Hybrids of RNA viruses and viroid-like elements replicate in fungi

Author

Listed:
  • Marco Forgia

    (National Research Council of Italy)

  • Beatriz Navarro

    (National Research Council of Italy)

  • Stefania Daghino

    (National Research Council of Italy)

  • Amelia Cervera

    (Universidad Politécnica de Valencia-CSIC)

  • Andreas Gisel

    (National Research Council of Italy
    International Institute of Tropical Agriculture)

  • Silvia Perotto

    (University of Torino)

  • Dilzara N. Aghayeva

    (Ministry of Science and Education of the Republic of Azerbaijan)

  • Mary F. Akinyuwa

    (Universidad Politécnica de Valencia
    Università Degli Studi di Padova
    Auburn University)

  • Emanuela Gobbi

    (University of Brescia)

  • Ivan N. Zheludev

    (Stanford University)

  • Robert C. Edgar

    (Independent Researcher)

  • Rayan Chikhi

    (Institut Pasteur)

  • Massimo Turina

    (National Research Council of Italy)

  • Artem Babaian

    (University of Toronto
    University of Toronto)

  • Francesco Serio

    (National Research Council of Italy)

  • Marcos Peña

    (Universidad Politécnica de Valencia-CSIC)

Abstract

Earth’s life may have originated as self-replicating RNA, and it has been argued that RNA viruses and viroid-like elements are remnants of such pre-cellular RNA world. RNA viruses are defined by linear RNA genomes encoding an RNA-dependent RNA polymerase (RdRp), whereas viroid-like elements consist of small, single-stranded, circular RNA genomes that, in some cases, encode paired self-cleaving ribozymes. Here we show that the number of candidate viroid-like elements occurring in geographically and ecologically diverse niches is much higher than previously thought. We report that, amongst these circular genomes, fungal ambiviruses are viroid-like elements that undergo rolling circle replication and encode their own viral RdRp. Thus, ambiviruses are distinct infectious RNAs showing hybrid features of viroid-like RNAs and viruses. We also detected similar circular RNAs, containing active ribozymes and encoding RdRps, related to mitochondrial-like fungal viruses, highlighting fungi as an evolutionary hub for RNA viruses and viroid-like elements. Our findings point to a deep co-evolutionary history between RNA viruses and subviral elements and offer new perspectives in the origin and evolution of primordial infectious agents, and RNA life.

Suggested Citation

  • Marco Forgia & Beatriz Navarro & Stefania Daghino & Amelia Cervera & Andreas Gisel & Silvia Perotto & Dilzara N. Aghayeva & Mary F. Akinyuwa & Emanuela Gobbi & Ivan N. Zheludev & Robert C. Edgar & Ray, 2023. "Hybrids of RNA viruses and viroid-like elements replicate in fungi," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38301-2
    DOI: 10.1038/s41467-023-38301-2
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    References listed on IDEAS

    as
    1. Robert C. Edgar & Brie Taylor & Victor Lin & Tomer Altman & Pierre Barbera & Dmitry Meleshko & Dan Lohr & Gherman Novakovsky & Benjamin Buchfink & Basem Al-Shayeb & Jillian F. Banfield & Marcos Peña &, 2022. "Petabase-scale sequence alignment catalyses viral discovery," Nature, Nature, vol. 602(7895), pages 142-147, February.
    2. Kourosh Salehi-Ashtiani & Jack W. Szostak, 2001. "In vitro evolution suggests multiple origins for the hammerhead ribozyme," Nature, Nature, vol. 414(6859), pages 82-84, November.
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