1887

Abstract

Non-polio enteroviruses are a ubiquitous and divergent group of non-enveloped RNA viruses. Novel types are reported regularly in addition to over 100 known types; however, mechanisms of emergence of novel types remain obscure. Here, the 33 most common types represented by 35–629 non-redundant partial VP1 sequences in GenBank were studied in parallel using Bayesian coalescent molecular clock analysis to investigate common evolutionary trends among enterovirus types. Inferred substitution rates were in the range of 0.41×10 to 3.07×10 substitutions per site per year. The most recent common ancestors of known isolates of each type presumably existed between 55 and 200 years ago. Phylogenetic analysis results suggested that global type populations underwent bottlenecks that could repeatedly reset the common ancestor dates. Nevertheless, species-level analysis suggested that the contemporary enterovirus types emerged within the last millennium. Analysis of 2657 complete VP1 sequences of the 24 most common types indicated that the type criterion based upon 75 % nucleotide sequence identity remains generally valid, despite exponential growth of the number of known sequences and a high rate of mutation fixation. However, in few types there was evidence that enteroviruses can drift slightly beyond the type threshold, up to 73 % identity, and both amino acid and nucleotide sequences should be considered for type identification. Analysis of sequence distances within types implied that sequence-identity-based identification of genotypes is rational within some, but not all, types and distinct genotype cut-offs (9–20 %) may be useful for different types.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000966
2017-11-02
2019-09-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/12/2968.html?itemId=/content/journal/jgv/10.1099/jgv.0.000966&mimeType=html&fmt=ahah

References

  1. Tapparel C, Siegrist F, Petty TJ, Kaiser L. Picornavirus and enterovirus diversity with associated human diseases. Infect Genet Evol 2013;14:282–293 [CrossRef][PubMed]
    [Google Scholar]
  2. Nathanson N, Kew OM. From emergence to eradication: the epidemiology of poliomyelitis deconstructed. Am J Epidemiol 2010;172:1213–1229 [CrossRef][PubMed]
    [Google Scholar]
  3. Wright PW, Strauss GH, Langford MP. Acute hemorrhagic conjunctivitis. Am Fam Physician 1992;45:173–178[PubMed]
    [Google Scholar]
  4. Palacios G, Oberste MS. Enteroviruses as agents of emerging infectious diseases. J Neurovirol 2005;11:424–433 [CrossRef][PubMed]
    [Google Scholar]
  5. Solomon T, Lewthwaite P, Perera D, Cardosa MJ, Mcminn P et al. Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect Dis 2010;10:778–790 [CrossRef]
    [Google Scholar]
  6. Lashkevich VA, Koroleva GA, Lukashev AN, Denisova EV, Katargina LA. Enterovirus uveitis. Rev Med Virol 2004;14:241–254 [CrossRef][PubMed]
    [Google Scholar]
  7. Oberste MS, Feeroz MM, Maher K, Nix WA, Engel GA et al. Characterizing the picornavirus landscape among synanthropic nonhuman primates in Bangladesh, 2007 to 2008. J Virol 2013;87:558–571 [CrossRef][PubMed]
    [Google Scholar]
  8. Harvala H, Sharp CP, Ngole EM, Delaporte E, Peeters M et al. Detection and genetic characterization of enteroviruses circulating among wild populations of chimpanzees in Cameroon: relationship with human and simian enteroviruses. J Virol 2011;85:4480–4486 [CrossRef][PubMed]
    [Google Scholar]
  9. Oberste MS, Maher K, Kilpatrick DR, Flemister MR, Brown BA et al. Typing of human enteroviruses by partial sequencing of VP1. J Clin Microbiol 1999;37:1288–1293[PubMed]
    [Google Scholar]
  10. Nix WA, Oberste MS, Pallansch MA. Sensitive, seminested PCR amplification of VP1 sequences for direct identification of all enterovirus serotypes from original clinical specimens. J Clin Microbiol 2006;44:2698–2704 [CrossRef][PubMed]
    [Google Scholar]
  11. Knowles NJ, Hovi T, Hyypia T, King AMQ, Lindberg AM et al. Family Picornaviridae. In King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. (editors) Virus Taxonomy Classification and nomenclature of viruses Ninth report of the International Committee on Taxonomy of Viruses San Diego: Elsevier Inc.; 2012; pp.855–880
    [Google Scholar]
  12. Mombo IM, Lukashev AN, Bleicker T, Brünink S, Berthet N et al. African non-human primates host diverse enteroviruses. PLoS One 2017;12:e0169067 [CrossRef][PubMed]
    [Google Scholar]
  13. Oberste MS, Feeroz MM, Maher K, Nix WA, Engel GA et al. Naturally acquired picornavirus infections in primates at the Dhaka zoo. J Virol 2013;87:572–580 [CrossRef][PubMed]
    [Google Scholar]
  14. Mcwilliam Leitch EC, Cabrerizo M, Cardosa J, Harvala H, Ivanova OE et al. Evolutionary dynamics and temporal/geographical correlates of recombination in the human enterovirus echovirus types 9, 11, and 30. J Virol 2010;84:9292–9300 [CrossRef][PubMed]
    [Google Scholar]
  15. Lukashev AN, Shumilina EY, Belalov IS, Ivanova OE, Eremeeva TP et al. Recombination strategies and evolutionary dynamics of the Human enterovirus A global gene pool. J Gen Virol 2014;95:868–873 [CrossRef][PubMed]
    [Google Scholar]
  16. Lukashev AN, Lashkevich VA, Ivanova OE, Koroleva GA, Hinkkanen AE et al. Recombination in circulating Human enterovirus B: independent evolution of structural and non-structural genome regions. J Gen Virol 2005;86:3281–3290 [CrossRef][PubMed]
    [Google Scholar]
  17. Blomqvist S, Bruu AL, Stenvik M, Hovi T. Characterization of a recombinant type 3/type 2 poliovirus isolated from a healthy vaccinee and containing a chimeric capsid protein VP1. J Gen Virol 2003;84:573–580 [CrossRef][PubMed]
    [Google Scholar]
  18. Martín J, Samoilovich E, Dunn G, Lackenby A, Feldman E et al. Isolation of an intertypic poliovirus capsid recombinant from a child with vaccine-associated paralytic poliomyelitis. J Virol 2002;76:10921–10928 [CrossRef][PubMed]
    [Google Scholar]
  19. Lukashev AN. Role of recombination in evolution of enteroviruses. Rev Med Virol 2005;15:157–167 [CrossRef][PubMed]
    [Google Scholar]
  20. Sadeuh-Mba SA, Bessaud M, Massenet D, Joffret ML, Endegue MC et al. High frequency and diversity of species C enteroviruses in Cameroon and neighboring countries. J Clin Microbiol 2013;51:759–770 [CrossRef][PubMed]
    [Google Scholar]
  21. Bailly JL, Mirand A, Henquell C, Archimbaud C, Chambon M et al. Phylogeography of circulating populations of human echovirus 30 over 50 years: nucleotide polymorphism and signature of purifying selection in the VP1 capsid protein gene. Infect Genet Evol 2009;9:699–708 [CrossRef][PubMed]
    [Google Scholar]
  22. Henquell C, Mirand A, Richter J, Schuffenecker I, Böttiger B et al. Phylogenetic patterns of human coxsackievirus B5 arise from population dynamics between two genogroups and reveal evolutionary factors of molecular adaptation and transmission. J Virol 2013;87:12249–12259 [CrossRef][PubMed]
    [Google Scholar]
  23. Yarmolskaya MS, Shumilina EY, Ivanova OE, Drexler JF, Lukashev AN. Molecular epidemiology of echoviruses 11 and 30 in Russia: different properties of genotypes within an enterovirus serotype. Infect Genet Evol 2015;30:244–248 [CrossRef][PubMed]
    [Google Scholar]
  24. Bessaud M, Razafindratsimandresy R, Nougairède A, Joffret ML, Deshpande JM et al. Molecular comparison and evolutionary analyses of VP1 nucleotide sequences of new African human enterovirus 71 isolates reveal a wide genetic diversity. PLoS One 2014;9:e90624 [CrossRef][PubMed]
    [Google Scholar]
  25. Smura T, Savolainen-Kopra C, Roivainen M. Evolution of newly described enteroviruses. Future Virol 2011;6:109–131 [CrossRef]
    [Google Scholar]
  26. Oberste MS, Maher K, Kilpatrick DR, Pallansch MA. Molecular evolution of the human enteroviruses: correlation of serotype with VP1 sequence and application to picornavirus classification. J Virol 1999;73:1941–1948[PubMed]
    [Google Scholar]
  27. Koonin EV, Wolf YI, Nagasaki K, Dolja VV. The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat Rev Microbiol 2008;6:925–939 [CrossRef][PubMed]
    [Google Scholar]
  28. Lukashev AN, Ivanova OE, Eremeeva TP, Gmyl LV. Analysis of echovirus 30 isolates from Russia and new independent states revealing frequent recombination and reemergence of ancient lineages. J Clin Microbiol 2008;46:665–670 [CrossRef][PubMed]
    [Google Scholar]
  29. Palacios G, Casas I, Cisterna D, Trallero G, Tenorio A et al. Molecular epidemiology of echovirus 30: temporal circulation and prevalence of single lineages. J Virol 2002;76:4940–4949 [CrossRef][PubMed]
    [Google Scholar]
  30. Tee KK, Lam TT, Chan YF, Bible JM, Kamarulzaman A et al. Evolutionary genetics of human enterovirus 71: origin, population dynamics, natural selection, and seasonal periodicity of the VP1 gene. J Virol 2010;84:3339–3350 [CrossRef][PubMed]
    [Google Scholar]
  31. Pallansch M, Roos R. Enteroviruses: Polioviruses, Coxsackieviruses, Echoviruses, and Newer Enteroviruses. In Knipe DM, Howley PM. (editors) Fields Virology, 5th ed.vol. 1 Philadelphia: Lippincott-Raven; 2007; pp.840–893
    [Google Scholar]
  32. Mcwilliam Leitch EC, Bendig J, Cabrerizo M, Cardosa J, Hyypiä T et al. Transmission networks and population turnover of echovirus 30. J Virol 2009;83:2109–2118 [CrossRef][PubMed]
    [Google Scholar]
  33. Khetsuriani N, Lamonte-Fowlkes A, Oberst S, Pallansch MA.Centers for Disease Control and Prevention Enterovirus surveillance-United States, 1970-2005. MMWR Surveill Summ 2006;55:1–20[PubMed]
    [Google Scholar]
  34. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012;29:1969–1973 [CrossRef][PubMed]
    [Google Scholar]
  35. Rao CD, Yergolkar P, Shankarappa KS. Antigenic diversity of enteroviruses associated with nonpolio acute flaccid paralysis, India, 2007-2009. Emerg Infect Dis 2012;18:1833–1840 [CrossRef][PubMed]
    [Google Scholar]
  36. Oberste MS, Maher K, Michele SM, Belliot G, Uddin M et al. Enteroviruses 76, 89, 90 and 91 represent a novel group within the species Human enterovirus A. J Gen Virol 2005;86:445–451 [CrossRef][PubMed]
    [Google Scholar]
  37. Savolainen C, Hovi T, Mulders MN. Molecular epidemiology of echovirus 30 in Europe: succession of dominant sublineages within a single major genotype. Arch Virol 2001;146:521–537 [CrossRef][PubMed]
    [Google Scholar]
  38. Oberste MS, Maher K, Kennett ML, Campbell JJ, Carpenter MS et al. Molecular epidemiology and genetic diversity of echovirus type 30 (E30): genotypes correlate with temporal dynamics of E30 isolation. J Clin Microbiol 1999;37:3928–3933[PubMed]
    [Google Scholar]
  39. Simmonds P. Recombination and selection in the evolution of picornaviruses and other Mammalian positive-stranded RNA viruses. J Virol 2006;80:11124–11140 [CrossRef][PubMed]
    [Google Scholar]
  40. Jorba J, Campagnoli R, de L, Kew O. Calibration of multiple poliovirus molecular clocks covering an extended evolutionary range. J Virol 2008;82:4429–4440 [CrossRef][PubMed]
    [Google Scholar]
  41. Duchêne S, Holmes EC, Ho SY. Analyses of evolutionary dynamics in viruses are hindered by a time-dependent bias in rate estimates. Proc Biol Sci 2014;281:20140732 [CrossRef][PubMed]
    [Google Scholar]
  42. Oberste MS, Nix WA, Kilpatrick DR, Flemister MR, Pallansch MA. Molecular epidemiology and type-specific detection of echovirus 11 isolates from the Americas, Europe, Africa, Australia, southern Asia and the Middle East. Virus Res 2003;91:241–248 [CrossRef][PubMed]
    [Google Scholar]
  43. Brown BA, Maher K, Flemister MR, Naraghi-Arani P, Uddin M et al. Resolving ambiguities in genetic typing of human enterovirus species C clinical isolates and identification of enterovirus 96, 99 and 102. J Gen Virol 2009;90:1713–1723 [CrossRef][PubMed]
    [Google Scholar]
  44. Jiang P, Faase JA, Toyoda H, Paul A, Wimmer E et al. Evidence for emergence of diverse polioviruses from C-cluster coxsackie A viruses and implications for global poliovirus eradication. Proc Natl Acad Sci USA 2007;104:9457–9462 [CrossRef][PubMed]
    [Google Scholar]
  45. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002;30:3059–3066 [CrossRef][PubMed]
    [Google Scholar]
  46. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 1999;41:95–98
    [Google Scholar]
  47. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007;7:214 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000966
Loading
/content/journal/jgv/10.1099/jgv.0.000966
Loading

Data & Media loading...

Supplementary File 1

PDF

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error