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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Vydáno v:Nature communications Ročník 14; číslo 1; s. 2591 - 11
Hlavní autoři: 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
Médium: Journal Article
Jazyk:angličtina
Vydáno: London Nature Publishing Group UK 05.05.2023
Nature Publishing Group
Nature Portfolio
Témata:
45/29
45/77
45/88
45/90
45/91
631/181/735
631/326/193
631/326/596/2554
631/337/1910
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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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. 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.
AbstractList 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.
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.
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.
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.
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.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.
ArticleNumber 2591
Author Di Serio, Francesco
Navarro, Beatriz
Gobbi, Emanuela
Aghayeva, Dilzara N.
Chikhi, Rayan
Daghino, Stefania
Zheludev, Ivan N.
Perotto, Silvia
Cervera, Amelia
Akinyuwa, Mary F.
Forgia, Marco
Edgar, Robert C.
Turina, Massimo
Gisel, Andreas
Babaian, Artem
de la Peña, Marcos
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  organization: Institute for Sustainable Plant Protection, National Research Council of Italy
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  organization: Institute of Botany, Ministry of Science and Education of the Republic of Azerbaijan
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  surname: Akinyuwa
  fullname: Akinyuwa, Mary F.
  organization: Department of Agroforestry Ecosystems, Universidad Politécnica de Valencia, Department of Land, Environment Agriculture and Forestry, Università Degli Studi di Padova, Department of Entomology and Plant Pathology, Auburn University
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  organization: Instituto de Biología Molecular y Celular de Plantas, Universidad Politécnica de Valencia-CSIC
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Issue 1
Keywords Fungi
Molecular evolution
Ribozymes
Viral evolution
Language English
License 2023. The Author(s).
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KooninEVGlobal organization and proposed megataxonomy of the virus worldMicrobiol. Mol. Biol. Rev.202084e00061191:CAS:528:DC%2BB3cXhsVeju7%2FF10.1128/MMBR.00061-19321322437062200
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NeriUExpansion of the global RNA virome reveals diverse clades of bacteriophagesCell2022185402340371:CAS:528:DC%2BB38XisFSqtrzL10.1016/j.cell.2022.08.02336174579
KuoMYPSharmeenLDinter-GottliebGTaylorJCharacterization of self-cleaving RNA sequences on the genome and antigenome of human hepatitis delta-virusJ. Virol.198862443944441:CAS:528:DyaL1MXlt1SgsQ%3D%3D10.1128/jvi.62.12.4439-4444.19883184270253552
FloresRViroid replication: rolling-circles, enzymes and ribozymesViruses200913173341:CAS:528:DC%2BD1MXhsVagtLrL10.3390/v1020317219945523185496
SavilleBJCollinsRAA site-specific self-cleavage reaction performed by a novel RNA in neurospora mitochondriaCell1990616856961:CAS:528:DyaK3cXls1OktLk%3D10.1016/0092-8674(90)90480-32160856
FloresRGago-ZachertSSerraPSanjuanRElenaSFViroids: survivors from the RNA world?Annu. Rev. Microbiol.2014683954141:CAS:528:DC%2BC2cXhvVGrsbnE10.1146/annurev-micro-091313-10341625002087
WalkerPJChanges to virus taxonomy and to the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2021)Arch. Virol.2021166263326481:CAS:528:DC%2BB3MXhsV2jt7nN10.1007/s00705-021-05156-134231026
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L Sharmeen (38301_CR10) 1988; 62
A Morgulis (38301_CR30) 2006; 13
CJ Hutchins (38301_CR7) 1986; 14
RC Edgar (38301_CR33) 2004; 32
U Neri (38301_CR25) 2022; 185
EV Koonin (38301_CR6) 2020; 84
A Babaian (38301_CR19) 2022; 10
CE Weinberg (38301_CR17) 2021; 49
RC Edgar (38301_CR32) 2010; 26
FHC Crick (38301_CR2) 1968; 38
S Brunak (38301_CR16) 2002; 298
M de la Peña (38301_CR41) 2021; 7
R Flores (38301_CR5) 2022; 8
M Mirdita (38301_CR20) 2022; 19
J Hirzmann (38301_CR36) 1993; 21
V Pallas (38301_CR38) 1987; 68
38301_CR1
M Rizzetto (38301_CR11) 2015; 5
RC Edgar (38301_CR14) 2022; 602
G Benson (38301_CR31) 1999; 27
MASC Picarelli (38301_CR40) 2019; 9
MYP Kuo (38301_CR9) 1988; 62
A Roth (38301_CR42) 2014; 10
S Sutela (38301_CR12) 2020; 6
K Salehi-Ashtiani (38301_CR29) 2001; 414
W Gilbert (38301_CR3) 1986; 319
L Qu (38301_CR27) 2022; 185
R Lorenz (38301_CR35) 2011; 6
EP Nawrocki (38301_CR18) 2013; 29
R Flores (38301_CR4) 2014; 68
R Flores (38301_CR22) 2009; 1
R Leinonen (38301_CR15) 2011; 39
M Forgia (38301_CR13) 2021; 553
K Tamura (38301_CR34) 2021; 38
JM Buzayan (38301_CR8) 1986; 323
BJ Saville (38301_CR23) 1990; 61
RL Bian (38301_CR26) 2020; 117
RM Jimenez (38301_CR21) 2015; 40
S Gago (38301_CR28) 2009; 323
38301_CR37
38301_CR39
PJ Walker (38301_CR24) 2021; 166
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– reference: PicarelliMASCExtreme diversity of mycoviruses present in isolates of Rhizoctonia solani AG2-2 LP from Zoysia japonica from BrazilFront. Cell. Infect. Microbiol.201992441:CAS:528:DC%2BB3cXjs1Gmsrk%3D10.3389/fcimb.2019.00244313551506640214
– reference: SavilleBJCollinsRAA site-specific self-cleavage reaction performed by a novel RNA in neurospora mitochondriaCell1990616856961:CAS:528:DyaK3cXls1OktLk%3D10.1016/0092-8674(90)90480-32160856
– reference: WeinbergCEOlzogVJEckertIWeinbergZIdentification of over 200-fold more hairpin ribozymes than previously known in diverse circular RNAsNucleic Acids Res.202149637563881:CAS:528:DC%2BB3MXit1CrtL7M10.1093/nar/gkab454340965838216279
– reference: NeriUExpansion of the global RNA virome reveals diverse clades of bacteriophagesCell2022185402340371:CAS:528:DC%2BB38XisFSqtrzL10.1016/j.cell.2022.08.02336174579
– reference: JimenezRMPolancoJALuptakAChemistry and biology of self-cleaving ribozymesTrends Biochem. Sci.2015406486611:CAS:528:DC%2BC2MXhs1Orsb3P10.1016/j.tibs.2015.09.001264815004630146
– reference: WalkerPJChanges to virus taxonomy and to the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2021)Arch. Virol.2021166263326481:CAS:528:DC%2BB3MXhsV2jt7nN10.1007/s00705-021-05156-134231026
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– reference: RothAA widespread self-cleaving ribozyme class is revealed by bioinformaticsNat. Chem. Biol.20141056601:CAS:528:DC%2BC3sXhslygtLjO10.1038/nchembio.138624240507
– reference: FloresRViroid replication: rolling-circles, enzymes and ribozymesViruses200913173341:CAS:528:DC%2BD1MXhsVagtLrL10.3390/v1020317219945523185496
– reference: BianRLFacilitative and synergistic interactions between fungal and plant virusesProc. Natl Acad. Sci. USA2020117377937882020PNAS..117.3779B1:CAS:528:DC%2BB3cXjsFyht7c%3D10.1073/pnas.1915996117320151047035501
– reference: TamuraKStecherGKumarSMEGA11 Molecular Evolutionary Genetics Analysis Version 11Mol. Biol. Evol.202138302230271:CAS:528:DC%2BB3MXitlCktrfN10.1093/molbev/msab120338924918233496
– reference: CrickFHCOrigin of genetic codeJ. Mol. Biol.1968383673791:CAS:528:DyaF1MXksVSiug%3D%3D10.1016/0022-2836(68)90392-64887876
– reference: SharmeenLKuoMYPDintergottliebGTaylorJAntigenomic RNA of human hepatitis delta-virus can undergo self-cleavageJ. Virol.198862267426791:CAS:528:DyaL1cXlt1egtrg%3D10.1128/jvi.62.8.2674-2679.19882455816253699
– reference: EdgarRCPetabase-scale sequence alignment catalyses viral discoveryNature20226021421472022Natur.602..142E1:CAS:528:DC%2BB38XitFGmu78%3D10.1038/s41586-021-04332-235082445
– reference: EdgarRCMUSCLE: multiple sequence alignment with high accuracy and high throughputNucleic Acids Res.200432179217971:CAS:528:DC%2BD2cXisF2ks7w%3D10.1093/nar/gkh34015034147390337
– reference: KuoMYPSharmeenLDinter-GottliebGTaylorJCharacterization of self-cleaving RNA sequences on the genome and antigenome of human hepatitis delta-virusJ. Virol.198862443944441:CAS:528:DyaL1MXlt1SgsQ%3D%3D10.1128/jvi.62.12.4439-4444.19883184270253552
– reference: FloresRGago-ZachertSSerraPSanjuanRElenaSFViroids: survivors from the RNA world?Annu. Rev. Microbiol.2014683954141:CAS:528:DC%2BC2cXhvVGrsbnE10.1146/annurev-micro-091313-10341625002087
– reference: KooninEVGlobal organization and proposed megataxonomy of the virus worldMicrobiol. Mol. Biol. Rev.202084e00061191:CAS:528:DC%2BB3cXhsVeju7%2FF10.1128/MMBR.00061-19321322437062200
– reference: ForgiaMIsgandarliEAghayevaDNHuseynovaITurinaMVirome characterization of Cryphonectria parasitica isolates from Azerbaijan unveiled a new mymonavirus and a putative new RNA virus unrelated to described viral sequencesVirology202155351611:CAS:528:DC%2BB3cXisVGitrjJ10.1016/j.virol.2020.10.00833221630
– reference: HirzmannJLuoDHahnenJHobomGDetermination of messenger-RNA 5’-ends by reverse transcription of the cap structureNucleic Acids Res.199321359735981:CAS:528:DyaK3sXlslCqsr0%3D10.1093/nar/21.15.35978346046331478
– reference: NawrockiEPEddySRInfernal 1.1: 100-fold faster RNA homology searchesBioinformatics201329293329351:CAS:528:DC%2BC3sXhslWnsb7N10.1093/bioinformatics/btt509240084193810854
– reference: MorgulisAGertzEMSchafferAAAgarwalaRA fast and symmetric DUST implementation to mask low-complexity DNA sequencesJ. Comput. Biol.2006131028104022554071:CAS:528:DC%2BD28XmtFCmsrs%3D10.1089/cmb.2006.13.102816796549
– reference: BrunakSNucleotide sequence database policiesScience2002298133313331:CAS:528:DC%2BD38XpsFektLs%3D10.1126/science.298.5597.1333b12436968
– reference: GilbertWOrigin of life - the RNA worldNature19863196186181986Natur.319..618G10.1038/319618a0
– reference: EdgarRCSearch and clustering orders of magnitude faster than BLASTBioinformatics201026246024611:CAS:528:DC%2BC3cXht1WhtbzM10.1093/bioinformatics/btq46120709691
– reference: de la PeñaMCeprianRCaseyJLCerveraAHepatitis delta virus-like circular RNAs from diverse metazoans encode conserved hammerhead ribozymesVirus Evol.20217veab01610.1093/ve/veab016337084157936874
– reference: BuzayanJMGerlachWLBrueningGNon-enzymatic cleavage and ligation of RNAs complementary to a plant-virus satellite RNANature19863233493531986Natur.323..349B1:CAS:528:DyaL28XlvVGjsLg%3D10.1038/323349a0
– reference: QuLCircular RNA vaccines against SARS-CoV-2 and emerging variantsCell2022185172817441:CAS:528:DC%2BB38XhtVyis7%2FN10.1016/j.cell.2022.03.044354606448971115
– reference: PallasVNavarroAFloresRIsolation of a viroid-like RNA from hop different from hop stunt viroidJ. Gen. Virol.198768320132051:CAS:528:DyaL1cXht1ylt7s%3D10.1099/0022-1317-68-12-3201
– reference: BabaianAEdgarRCRibovirus classification by a polymerase barcode sequencePeerJ202210e1405510.7717/peerj.14055362587949573346
– reference: LorenzRViennaRNA package 2.0Algorithms Mol. Biol.2011610.1186/1748-7188-6-26221151893319429
– reference: Lambden, P. R., Cooke, S. J., Caul, E. O. & Clarke, I. N. Cloning of noncultivatable human rotavirus by single primer amplification. J. Virol.66, 1817–1822 (1992).
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Snippet 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...
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...
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...
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631/337/1910
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
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Title Hybrids of RNA viruses and viroid-like elements replicate in fungi
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