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


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
05 05 2023
Historique:
received: 24 03 2023
accepted: 25 04 2023
medline: 8 5 2023
pubmed: 6 5 2023
entrez: 5 5 2023
Statut: epublish

Résumé

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.

Identifiants

pubmed: 37147358
doi: 10.1038/s41467-023-38301-2
pii: 10.1038/s41467-023-38301-2
pmc: PMC10162972
doi:

Substances chimiques

RNA, Catalytic 0
RNA, Viral 0
RNA 63231-63-0
RNA-Dependent RNA Polymerase EC 2.7.7.48

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2591

Informations de copyright

© 2023. The Author(s).

Références

Virology. 2021 Jan 15;553:51-61
pubmed: 33221630
Algorithms Mol Biol. 2011 Nov 24;6:26
pubmed: 22115189
Nat Methods. 2022 Jun;19(6):679-682
pubmed: 35637307
Arch Virol. 2021 Sep;166(9):2633-2648
pubmed: 34231026
J Virol. 1988 Dec;62(12):4439-44
pubmed: 3184270
Front Cell Infect Microbiol. 2019 Jul 12;9:244
pubmed: 31355150
J Virol. 1992 Mar;66(3):1817-22
pubmed: 1371174
Nat Chem Biol. 2014 Jan;10(1):56-60
pubmed: 24240507
Virus Evol. 2021 Feb 18;7(1):veab016
pubmed: 33708415
Mol Biol Evol. 2021 Jun 25;38(7):3022-3027
pubmed: 33892491
Virus Evol. 2020 Oct 08;6(2):veaa076
pubmed: 33324490
Nucleic Acids Res. 1986 May 12;14(9):3627-40
pubmed: 3714492
Cell. 1990 May 18;61(4):685-96
pubmed: 2160856
Proc Natl Acad Sci U S A. 2020 Feb 18;117(7):3779-3788
pubmed: 32015104
J Comput Biol. 2006 Jun;13(5):1028-40
pubmed: 16796549
Viruses. 2009 Sep;1(2):317-34
pubmed: 21994552
Nature. 2001 Nov 1;414(6859):82-4
pubmed: 11689947
Nucleic Acids Res. 2021 Jun 21;49(11):6375-6388
pubmed: 34096583
Trends Biochem Sci. 2015 Nov;40(11):648-661
pubmed: 26481500
Virus Evol. 2022 Jan 15;8(1):veab107
pubmed: 35223083
Nucleic Acids Res. 1999 Jan 15;27(2):573-80
pubmed: 9862982
Bioinformatics. 2010 Oct 1;26(19):2460-1
pubmed: 20709691
J Mol Biol. 1968 Dec;38(3):367-79
pubmed: 4887876
Cold Spring Harb Perspect Med. 2015 Jul 01;5(7):a021576
pubmed: 26134842
Cell. 2022 May 12;185(10):1728-1744.e16
pubmed: 35460644
Science. 2002 Nov 15;298(5597):1333
pubmed: 12436968
Science. 2009 Mar 6;323(5919):1308
pubmed: 19265013
PeerJ. 2022 Oct 13;10:e14055
pubmed: 36258794
Nucleic Acids Res. 2011 Jan;39(Database issue):D19-21
pubmed: 21062823
J Virol. 1988 Aug;62(8):2674-9
pubmed: 2455816
Cell. 2022 Oct 13;185(21):4023-4037.e18
pubmed: 36174579
Nature. 2022 Feb;602(7895):142-147
pubmed: 35082445
Microbiol Mol Biol Rev. 2020 Mar 4;84(2):
pubmed: 32132243
Annu Rev Microbiol. 2014;68:395-414
pubmed: 25002087
Nucleic Acids Res. 1993 Jul 25;21(15):3597-8
pubmed: 8346046
Bioinformatics. 2013 Nov 15;29(22):2933-5
pubmed: 24008419
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
pubmed: 15034147

Auteurs

Marco Forgia (M)

Institute for Sustainable Plant Protection, National Research Council of Italy, Torino, Italy.

Beatriz Navarro (B)

Institute for Sustainable Plant Protection, National Research Council of Italy, Bari, Italy.

Stefania Daghino (S)

Institute for Sustainable Plant Protection, National Research Council of Italy, Torino, Italy.

Amelia Cervera (A)

Instituto de Biología Molecular y Celular de Plantas, Universidad Politécnica de Valencia-CSIC, Valencia, Spain.

Andreas Gisel (A)

Institute of Biomedical Technologies, National Research Council of Italy, Bari, Italy.
International Institute of Tropical Agriculture, Ibadan, Nigeria.

Silvia Perotto (S)

Department of Life Science and Systems Biology, University of Torino, Torino, Italy.

Dilzara N Aghayeva (DN)

Institute of Botany, Ministry of Science and Education of the Republic of Azerbaijan, Baku, Azerbaijan.

Mary F Akinyuwa (MF)

Department of Agroforestry Ecosystems, Universidad Politécnica de Valencia, Valencia, Spain.
Department of Land, Environment Agriculture and Forestry, Università Degli Studi di Padova, Padova, Italy.
Department of Entomology and Plant Pathology, Auburn University, Auburn, AL, USA.

Emanuela Gobbi (E)

Department of Molecular and Translational Medicine, University of Brescia, Brescia, Italy.

Ivan N Zheludev (IN)

Department of Biochemistry, Stanford University, Stanford, CA, USA.

Robert C Edgar (RC)

Independent Researcher, Corte Madera, CA, USA.

Rayan Chikhi (R)

G5 Sequence Bioinformatics, Department of Computational Biology, Institut Pasteur, Paris, France.

Massimo Turina (M)

Institute for Sustainable Plant Protection, National Research Council of Italy, Brescia, Italy. massimo.turina@ipsp.cnr.it.

Artem Babaian (A)

Department of Molecular Genetics, University of Toronto, Toronto, ON, Canada. a.babaian@utoronto.ca.
Terrence Donnelly Centre for Cellular & Biomolecular Research, University of Toronto, Toronto, ON, Canada. a.babaian@utoronto.ca.

Francesco Di Serio (F)

Institute for Sustainable Plant Protection, National Research Council of Italy, Bari, Italy. francesco.diserio@ipsp.cnr.it.

Marcos de la Peña (M)

Instituto de Biología Molecular y Celular de Plantas, Universidad Politécnica de Valencia-CSIC, Valencia, Spain. rivero@ibmcp.upv.es.

Articles similaires

Populus Soil Microbiology Soil Microbiota Fungi
Humans RNA, Circular Exosomes Cell Proliferation Epithelial-Mesenchymal Transition
DNA Methylation Humans DNA Animals Machine Learning
Plant Diseases Paenibacillus Paenibacillus polymyxa Biological Control Agents Fusarium

Classifications MeSH