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

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...

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Veröffentlicht in:Nature communications Jg. 14; H. 1; S. 2591 - 11
Hauptverfasser: Forgia, Marco, Navarro, Beatriz, Daghino, Stefania, Cervera, Amelia, Gisel, Andreas, Perotto, Silvia, Aghayeva, Dilzara N., Akinyuwa, Mary F., Gobbi, Emanuela, Zheludev, Ivan N., Edgar, Robert C., Chikhi, Rayan, Turina, Massimo, Babaian, Artem, Di Serio, Francesco, de la Peña, Marcos
Format: Journal Article
Sprache:Englisch
Veröffentlicht: London Nature Publishing Group UK 05.05.2023
Nature Publishing Group
Nature Portfolio
Schlagworte:
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Biochemistry, Molecular Biology
Biodiversity
Circular RNA
DNA-directed RNA polymerase
Evolution
Fungi
Fungi - genetics
Genomes
Genomics
Humanities and Social Sciences
Hybrids
Life Sciences
Microbiology and Parasitology
Mitochondria
multidisciplinary
Mycology
Populations and Evolution
Ribozymes
RNA - genetics
RNA polymerase
RNA viruses
RNA Viruses - genetics
RNA, Catalytic - genetics
RNA, Viral - genetics
RNA-Dependent RNA Polymerase - genetics
RNA-directed RNA polymerase
Science
Science (multidisciplinary)
Viroids
Viroids - genetics
Virology
Virus Replication - genetics
Viruses
Fungi
Molecular evolution
Ribozymes
Viral evolution
ISSN:2041-1723, 2041-1723
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Zusammenfassung: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. RNA viruses are defined by linear RNA genomes encoding an RNA-dependent RNA polymerase, while viroid-like elements consist of small, single-stranded, circular RNA genomes that, in some cases, encode self-cleaving catalytic RNAs. Here, the authors identify over 20,000 candidate viroid-like elements, and show that infectious agents of fungi display hybrid features of viroid-like RNAs and RNA viruses.
Bibliographie:ObjectType-Article-1
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PMCID: PMC10162972
ISSN:2041-1723
2041-1723
DOI:10.1038/s41467-023-38301-2