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

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, Rayan Chikhi, Massimo Turina (), Artem Babaian (), Francesco Serio () and Marcos Peña ()
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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
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
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
Francesco Serio: National Research Council of Italy
Marcos Peña: Universidad Politécnica de Valencia-CSIC

Nature Communications, 2023, vol. 14, issue 1, 1-11

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-38301-2

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