Hybrids of RNA viruses and viroid-like elements replicate in fungi
2023
Forgia, M. | Navarro, B. | Daghino, S. | Cervera, A. | Gisel, A. | Perotto, S. | Aghayeva, D.N. | Akinyuwa, M.F. | Gobbi, E. | Zheludev, I.N. | Edgar, R.C. | Chikhi, R. | Turina, M. | Babaian, A. | Serio, F. di | Peña, M. de la
Earth’s lifemay 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 RNAdependent 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.
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