#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Discovery of the First Insect Nidovirus, a Missing Evolutionary Link in the Emergence of the Largest RNA Virus Genomes


Nidoviruses with large genomes (26.3–31.7 kb; ‘large nidoviruses’), including Coronaviridae and Roniviridae, are the most complex positive-sense single-stranded RNA (ssRNA+) viruses. Based on genome size, they are far separated from all other ssRNA+ viruses (below 19.6 kb), including the distantly related Arteriviridae (12.7–15.7 kb; ‘small nidoviruses’). Exceptionally for ssRNA+ viruses, large nidoviruses encode a 3′-5′exoribonuclease (ExoN) that was implicated in controlling RNA replication fidelity. Its acquisition may have given rise to the ancestor of large nidoviruses, a hypothesis for which we here provide evolutionary support using comparative genomics involving the newly discovered first insect-borne nidovirus. This Nam Dinh virus (NDiV), named after a Vietnamese province, was isolated from mosquitoes and is yet to be linked to any pathology. The genome of this enveloped 60–80 nm virus is 20,192 nt and has a nidovirus-like polycistronic organization including two large, partially overlapping open reading frames (ORF) 1a and 1b followed by several smaller 3′-proximal ORFs. Peptide sequencing assigned three virion proteins to ORFs 2a, 2b, and 3, which are expressed from two 3′-coterminal subgenomic RNAs. The NDiV ORF1a/ORF1b frameshifting signal and various replicative proteins were tentatively mapped to canonical positions in the nidovirus genome. They include six nidovirus-wide conserved replicase domains, as well as the ExoN and 2′-O-methyltransferase that are specific to large nidoviruses. NDiV ORF1b also encodes a putative N7-methyltransferase, identified in a subset of large nidoviruses, but not the uridylate-specific endonuclease that – in deviation from the current paradigm - is present exclusively in the currently known vertebrate nidoviruses. Rooted phylogenetic inference by Bayesian and Maximum Likelihood methods indicates that NDiV clusters with roniviruses and that its branch diverged from large nidoviruses early after they split from small nidoviruses. Together these characteristics identify NDiV as the prototype of a new nidovirus family and a missing link in the transition from small to large nidoviruses.


Vyšlo v časopise: Discovery of the First Insect Nidovirus, a Missing Evolutionary Link in the Emergence of the Largest RNA Virus Genomes. PLoS Pathog 7(9): e32767. doi:10.1371/journal.ppat.1002215
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002215

Souhrn

Nidoviruses with large genomes (26.3–31.7 kb; ‘large nidoviruses’), including Coronaviridae and Roniviridae, are the most complex positive-sense single-stranded RNA (ssRNA+) viruses. Based on genome size, they are far separated from all other ssRNA+ viruses (below 19.6 kb), including the distantly related Arteriviridae (12.7–15.7 kb; ‘small nidoviruses’). Exceptionally for ssRNA+ viruses, large nidoviruses encode a 3′-5′exoribonuclease (ExoN) that was implicated in controlling RNA replication fidelity. Its acquisition may have given rise to the ancestor of large nidoviruses, a hypothesis for which we here provide evolutionary support using comparative genomics involving the newly discovered first insect-borne nidovirus. This Nam Dinh virus (NDiV), named after a Vietnamese province, was isolated from mosquitoes and is yet to be linked to any pathology. The genome of this enveloped 60–80 nm virus is 20,192 nt and has a nidovirus-like polycistronic organization including two large, partially overlapping open reading frames (ORF) 1a and 1b followed by several smaller 3′-proximal ORFs. Peptide sequencing assigned three virion proteins to ORFs 2a, 2b, and 3, which are expressed from two 3′-coterminal subgenomic RNAs. The NDiV ORF1a/ORF1b frameshifting signal and various replicative proteins were tentatively mapped to canonical positions in the nidovirus genome. They include six nidovirus-wide conserved replicase domains, as well as the ExoN and 2′-O-methyltransferase that are specific to large nidoviruses. NDiV ORF1b also encodes a putative N7-methyltransferase, identified in a subset of large nidoviruses, but not the uridylate-specific endonuclease that – in deviation from the current paradigm - is present exclusively in the currently known vertebrate nidoviruses. Rooted phylogenetic inference by Bayesian and Maximum Likelihood methods indicates that NDiV clusters with roniviruses and that its branch diverged from large nidoviruses early after they split from small nidoviruses. Together these characteristics identify NDiV as the prototype of a new nidovirus family and a missing link in the transition from small to large nidoviruses.


Zdroje

1. DrakeJWHollandJJ 1999 Mutation rates among RNA viruses. Proc Natl Acad Sci U S A 96 13910 13913

2. JenkinsGMRambautAPybusOGHolmesEC 2002 Rates of molecular evolution in RNA viruses: A quantitative phylogenetic analysis. J Mol Evol 54 156 165

3. SanjuanRNebotMRChiricoNManskyLMBelshawR 2010 Viral Mutation Rates. J Virol 84 9733 9748

4. GorbalenyaAEEnjuanesLZiebuhrJSnijderEJ 2006 Nidovirales: Evolving the largest RNA virus genome. Virus Res 117 17 37

5. MastersPS 2006 The molecular biology of coronaviruses. Adv Virus Res 66 193 292

6. PerlmanSGallagherTSnijderEJ 2008 Nidoviruses Washington, DC ASM Press

7. BrierleyI 1995 Ribosomal frameshifting viral RNAs. J Gen Virol 76 1885 1892

8. PlantEPPerez-AlvaradoGCJacobsJLMukhopadhyayBHennigM 2005 A three-stemmed mRNA pseudoknot in the SARS coronavirus frameshift signal. PLoS Biol 3 1012 1023

9. ZiebuhrJSnijderEJGorbalenyaAE 2000 Virus-encoded proteinases and proteolytic processing in the Nidovirales. J Gen Virol 81 853 879

10. BrianDABaricRS 2005 Coronavirus genome structure and replication. Curr Top Microbiol Immunol 287 1 30

11. PasternakAOSpaanWJMSnijderEJ 2006 Nidovirus transcription: how to make sense … ? J Gen Virol 87 1403 1421

12. EnjuanesLAlmazanFSolaIZunigaS 2006 Biochemical aspects of coronavirus replication and virus-host interaction. Ann Rev Microbiol 60 211 230

13. SawickiSGSawickiDLSiddellSG 2007 A contemporary view of coronavirus transcription. J Virol 81 20 29

14. GorbalenyaAE 2001 Big nidovirus genome - When count and order of domains matter. Adv Exp Med Biol 494 1 17

15. SnijderEJBredenbeekPJDobbeJCThielVZiebuhrJ 2003 Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J Mol Biol 331 991 1004

16. MinskaiaEHertzigTGorbalenyaAECampanacciVCambillauC 2006 Discovery of an RNA virus 3′→5′ exoribonuclease that is critically involved in coronavirus RNA synthesis. Proc Natl Acad Sci U S A 103 5108 5113

17. ChenPJiangMHuTLiuQZChenXSJ 2007 Biochemical characterization of exoribonuclease encoded by SARS coronavirus. J Biochem Mol Biol 40 649 655

18. EckerleLDLuXSperrySMChoiLDenisonMR 2007 High fidelity of murine hepatitis virus replication is decreased in nsp14 exoribonuclease mutants. J Virol 81 12135 12144

19. EckerleLDBeckerMMHalpinRALiKVenterE 2010 Infidelity of SARS-CoV Nsp14-Exonuclease Mutant Virus Replication Is Revealed by Complete Genome Sequencing. PLoS Pathog 6 e1000896

20. DenisonMRGrahamRLDonaldsonEFEckerleLDBaricRS 2011 Coronaviruses An RNA proofreading machine regulates replication fidelity and diversity. RNA Biol 8 270 279

21. HolmesEC 2009 The Evolution and Emergence of RNA Viruses New York Oxford University Press 254

22. BoursnellMEGBrownTDKFouldsIJGreenPFTomleyFM 1987 Completion of the sequence of the genome of the coronavirus avian infectious bronchitis virus. J Gen Virol 68 57 77

23. den BoonJASnijderEJChirnsideEDde VriesAAHorzinekMC 1991 Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily. J Virol 65 2910 2920

24. BelshawRde OliveiraTMarkowitzSRambautA 2009 The RNA Virus Database. Nucl Acids Res 37 D431 D435

25. NgaPTKieuAnhNTCuongVDNamVSHangPTM 2002 Surveillance of Japanese encephalitis in Vietnam (2000–2001). J Hyg Epidemiol XII 5 11

26. RyabovEV 2007 A novel virus isolated from the aphid Brevicoryne brassicae with similarity to Hymenoptera picorna-like viruses. J Gen Virol 88 2590 2595

27. AltschulSFMaddenTLSchafferAAZhangJZhangZ 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 3389 3402

28. CowleyJADimmockCMSpannKMWalkerPJ 2000 Gill-associated virus of Penaeus monodon prawns: an invertebrate virus with ORF1a and ORF1b genes related to arteri- and coronaviruses. J Gen Virol 81 1473 1484

29. ZukerM 2003 Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31 3406 3415

30. ReederJSteffenPGiegerichR 2007 pknotsRG: RNA pseudoknot folding including near-optimal structures and sliding windows. Nucleic Acids Res 35 W320 W324

31. KimKHLommelSA 1994 Identification and Analysis of the Site of −1 Ribosomal Frameshifting in Red-Clover Necrotic Mosaic-Virus. Virology 200 574 582

32. KimKHLommelSA 1998 Sequence element required for efficient −1 ribosomal frameshifting in red clover necrotic mosaic dianthovirus. Virology 250 50 59

33. GribskovMMcLachlanADEisenbergD 1987 Profile analysis: Detection of distantly related proteins. Proc Natl Acad Sci U S A 84 4355 4358

34. FinnRDTateJMistryJCoggillPCSammutSJ 2008 The Pfam protein families database. Nucleic Acids Res 36 D281 D288

35. GorbalenyaAEKooninEVDonchenkoAPBlinovVM 1989 Coronavirus genome: prediction of putative functional domains in the non-structural polyprotein by comparative amino acid sequence analysis. Nucleic Acids Res 17 4847 4861

36. HeroldJSiddellSGGorbalenyaAE 1999 A human RNA viral cysteine proteinase that depends upon a unique Zn2+-binding finger connecting the two domains of a papain-like fold [published erratum appears in J Biol Chem 1999 Jul 23;274(30):21490]. J Biol Chem 274 14918 14925

37. ImbertIGuillemotJCBourhisJMBussettaCCoutardB 2006 A second, non-canonical RNA-dependent RNA polymerase in SARS coronavirus. EMBO J 25 4933 4942

38. AnandKPalmGJMestersJRSiddellSGZiebuhrJ 2002 Structure of coronavirus main proteinase reveals combination of a chymotrypsin fold with an extra alpha-helical domain. EMBO J 21 3213 3224

39. VelthuisAJWTArnoldJJCameronCEvan den WormSHESnijderEJ 2010 The RNA polymerase activity of SARS-coronavirus nsp12 is primer dependent. Nucleic Acids Res 38 203 214

40. SeybertAPosthumaCCvan DintenLCSnijderEJGorbalenyaAE 2005 A complex zinc finger controls the enzymatic activities of nidovirus helicases. J Virol 79 696 704

41. GorbalenyaAESnijderEJ 1996 Viral cysteine proteinases. Persp Drug Discov Design 6 64 86

42. DecrolyEImbertICoutardBBouvetMLSeliskoB 2008 Coronavirus nonstructural protein 16 is a cap-0 binding enzyme possessing (nucleoside-2′O)-methyltransferase activity. J Virol 82 8071 8084

43. BouvetMDebarnotCImbertISeliskoBSnijderEJ 2010 In Vitro Reconstitution of SARS-Coronavirus mRNA Cap Methylation. PLoS Pathog 6 e1000863

44. IvanovKAHertzigTRozanovMBayerSThielV 2004 Major genetic marker of nidoviruses encodes a replicative endoribonuclease. Proc Natl Acad Sci U S A 101 12694 12699

45. RicagnoSEgloffMPUlfertsRCoutardBNurizzoD 2006 Crystal structure and mechanistic determinants of SARS coronavirus nonstructural protein 15 define an endoribonuclease family. Proc Natl Acad Sci U S A 103 11892 11897

46. BhardwajKPalaninathanSAlcantaraJMOYiLLGuarinoL 2008 Structural and functional analyses of the severe acute respiratory syndrome coronavirus endoribonuclease Nsp15. J Biol Chem 283 3655 3664

47. NedialkovaDDUlfertsRvan den BornELauberCGorbalenyaAE 2009 Biochemical Characterization of Arterivirus Nonstructural Protein 11 Reveals the Nidovirus-Wide Conservation of a Replicative Endoribonuclease. J Virol 83 5671 5682

48. SchutzeHUlfertsRSchelleBBayerSGranzowH 2006 Characterization of White bream virus reveals a novel genetic cluster of nidoviruses. J Virol 80 11598 11609

49. ChenYCaiHPanJXiangNTienP 2009 Functional screen reveals SARS coronavirus nonstructural protein nsp14 as a novel cap N7 methyltransferase. Proc Natl Acad Sci U S A 106 3484 3489

50. GonzálezJMGomez-PuertasPCavanaghDGorbalenyaAEEnjuanesL 2003 A comparative sequence analysis to revise the current taxonomy of the family Coronaviridae. Arch Virol 148 2207 2235

51. GorbalenyaAE 2008 Genomics and Evolution of the Nidovirales. PerlmanSGallagherTSnijderEJ Nidoviruses Washington ASM Press 15 28

52. GorbalenyaAEKooninEV 1993 Comparative analysis of the amino acid sequences of the key enzymes of the replication and expression of positive-strand RNA viruses. Validity of the approach and functional and evolutionary implications. Sov Sci Rev D Physicochem Biol 11 1 84

53. GorbalenyaAEPringleFMZeddamJLLukeBTCameronCE 2002 The palm subdomain-based active site is internally permuted in viral RNA-dependent RNA polymerases of an ancient lineage. J Mol Biol 324 47 62

54. GorbalenyaAELieutaudPHarrisMRCoutardBCanardB 2010 Practical application of bioinformatics by the multidisciplinary VIZIER consortium. Antiviral Res 87 95 110

55. JosephJSSaikatenduKSSubramanianVNeumanBWBuchmeierMJ 2007 Crystal structure of a monomeric form of severe acute respiratory syndrome coronavirus endonuclease nsp15 suggests a role for hexamerization as an allosteric switch. J Virol 81 6700 6708

56. PosthumaCCNedialkovaDDZevenhoven-DobbeJCBlokhuisJHGorbalenyaAE 2006 Site-directed mutagenesis of the nidovirus replicative endoribonuclease NendoU exerts pleiotropic effects on the arterivirus life cycle. J Virol 80 1653 1661

57. BhardwajKGuarinoLKaoCC 2004 The severe acute respiratory syndrome coronavirus Nsp15 protein is an endoribonuclease that prefers manganese as a cofactor. J Virol 78 12218 12224

58. BhardwajKSunJCHolzenburgAGuarinoLAKaoCC 2006 RNA recognition and cleavage by the SARS coronavirus endoribonuclease. J Mol Biol 361 243 256

59. GuarinoLABhardwajKDongWSunJCHolzenburgA 2005 Mutational analysis of the SARS virus Nsp15 endoribonuclease: Identification of residues affecting hexamer formation. J Mol Biol 353 1106 1117

60. KangHBhardwajKLiYPalaninathanSSacchettiniJ 2007 Biochemical and genetic analyses of murine hepatitis virus nsp15 endoribonuclease. J Virol 81 13587 13597

61. EgloffMPBenarrochDSeliskoBRometteJLCanardB 2002 An RNA cap (nucleoside-2 ′-O-)-methyltransferase in the flavivirus RNA polymerase NS5: crystal structure and functional characterization. EMBO J 21 2757 2768

62. MiSDurbinRHuangHVRiceCMStollarV 1989 Association of the Sindbis virus RNA methytransferase activity with the nonstructural protein nsP1. Virology 170 385 391

63. RozanovMNKooninEVGorbalenyaAE 1992 Conservation of the putative methyltransferase domain: a hallmark of the ‘Sindbis-like’ supergroup of positive-strand RNA viruses. J Gen Virol 73 2129 2134

64. AholaTLaakkonenPVihinenHKaariainenL 1997 Critical residues of Semliki Forest virus RNA capping enzyme involved in methyltransferase and guanylyltransferase-like activities. J Virol 71 392 397

65. ZustRCervantes-BarraganLHabjanMMaierRNeumanBW 2011 Ribose 2 ′-O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. Nat Immunol 12 137 143

66. DaffisSSzretterKJSchriewerJLiJQYounS 2010 2 ′-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 468 452 456

67. DoljaVVKreuzeJFValkonenJPT 2006 Comparative and functional genomics of closteroviruses. Virus Res 117 38 51

68. EigenM 1971 Selforganization of Matter and Evolution of Biological Macromolecules. Naturwissenschaften 58 465 523

69. BelshawRGardnerARarnbaUtAPybusOG 2008 Pacing a small cage: mutation and RNA viruses. Trends Ecol Evol 23 188 193

70. HolmesEC 2009 The Evolutionary Genetics of Emerging Viruses. Ann Rev Ecol Evol Syst 40 353 372

71. EigenM 1996 On the nature of virus quasispecies. Trends Microbiol 4 216 218

72. DomingoE 2007 Virus Evolution. KnipeDMHowleyPMGriffinDELambRAMartinMA Fields Virology Philadelphia Wolters Kluwer, Lippincott Williams & Wilkins 389 421

73. LauringASAndinoR 2010 Quasispecies Theory and the Behavior of RNA Viruses. PLoS Pathog 6 e1001005

74. QiXXLanSYWangWJScheldeLMDongHH 2010 Cap binding and immune evasion revealed by Lassa nucleoprotein structure. Nature 468 779 783

75. HastieKMKimberlinCRZandonattiMAMacRaeIJSaphireEO 2011 Structure of the Lassa virus nucleoprotein reveals a dsRNA-specific 3′ to 5′ exonuclease activity essential for immune suppression. Proc Natl Acad Sci U S A 108 2396 2401

76. JunglenSKurthAKuehlHQuanPLEllerbrokH 2009 Examining Landscape Factors Influencing Relative Distribution of Mosquito Genera and Frequency of Virus Infection. Ecohealth 6 239 249

77. IgarashiA 1978 Isolation of a Singh's Aedes albopictus cell clone sensitive to Dengue and Chikungunya viruses. J Gen Virol 40 531 544

78. WelshJMcClellandM 1990 Fingerprinting Genomes Using Pcr with Arbitrary Primers. Nucleic Acids Res 18 7213 7218

79. HazeltonPRGelderblomHR 2003 Electron microscopy for rapid diagnosis of infectious agents in emergent situations. Emerg Infect Dis 9 294 303

80. BaoYMFederhenSLeipeDPhamVResenchukS 2004 National Center for Biotechnology Information Viral Genomes Project. J Virol 78 7291 7298

81. BensonDAKarsch-MizrachiILipmanDJOstellJWheelerDL 2008 GenBank. Nucleic Acids Res 36 D25 D30

82. MurzinAGBrennerSEHubbardTChothiaC 1995 SCOP: a structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 247 536 540

83. EddySR 1998 Profile hidden Markov models. Bioinformatics 14 755 763

84. HofmannKStoffelW 1993 TMbase - A database of membrane spanning proteins segments. Biol Chem Hoppe-Seyler 373 166

85. SodingJ 2005 Protein homology detection by HMM-HMM comparison. Bioinformatics 21 951 960

86. JonesDT 1999 Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292 195 202

87. EdgarRC 2004 MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5 113

88. CastresanaJ 2000 Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17 540 552

89. AntonovIVLeontovichAMGorbalenyaAE 2008 BAGG - Blocks Accepting Gaps Generator, version. Available: http://www.genebee.msu.su/~antonov/bagg/cgi/bagg.cgi

90. WaterhouseAMProcterJBMartinDMAClampMBartonGJ 2009 Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25 1189 1191

91. R Development Core Team 2009 R: A Language and Environment for Statistical Computing. Available: http://www.r-project.org

92. PriceALJonesNCPevznerPA 2005 De novo identification of repeat families in large genomes. Bioinformatics 21 I351 I358

93. KroghABrownMMianISSjolanderKHausslerD 1994 Hidden Markov-Models in Computational Biology - Applications to Protein Modeling. J Mol Biol 235 1501 1531

94. ZeddamJLGordonKHJLauberCAlvesCAFLukeBT 2010 Euprosterna elaeasa virus genome sequence and evolution of the Tetraviridae family: Emergence of bipartite genomes and conservation of the VPg signal with the dsRNA Birnaviridae family. Virology 397 145 154

95. DrummondAJRambautA 2007 BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7 214

96. WhelanSGoldmanN 2001 A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18 691 699

97. RambautADrummondAJ 2007 Tracer v1.4, version. Available: http://beast.bio.ed.ac.uk/Tracer

98. DrummondAJHoSYWPhillipsMJRambautA 2006 Relaxed phylogenetics and dating with confidence. PLoS Biol 4 699 710

99. GoodmanSN 1999 Toward evidence-based medical statistics. 2: The Bayes factor. Ann Internal Med 130 1005 1013

100. GuindonSGascuelO 2003 A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52 696 704

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2011 Číslo 9
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#