1887

Abstract

Every year, tick-borne encephalitis virus (TBEV) causes severe central nervous system infection in 10 000 to 15 000 people in Europe and Asia. TBEV is maintained in the environment by an enzootic cycle that requires a tick vector and a vertebrate host, and the adaptation of TBEV to vertebrate and invertebrate environments is essential for TBEV persistence in nature. This adaptation is facilitated by the error-prone nature of the virus’s RNA-dependent RNA polymerase, which generates genetically distinct virus variants called quasispecies. TBEV shows a focal geographical distribution pattern where each focus represents a TBEV hotspot. Here, we sequenced and characterized two TBEV genomes, JP-296 and JP-554, from questing Ixodes ricinus ticks at a TBEV focus in central Sweden. Phylogenetic analysis showed geographical clustering among the newly sequenced strains and three previously sequenced Scandinavian strains, Toro-2003, Saringe-2009 and Mandal-2009, which originated from the same ancestor. Among these five Scandinavian TBEV strains, only Mandal-2009 showed a large deletion within the 3′ non-coding region (NCR), similar to the highly virulent TBEV strain Hypr. Deep sequencing of JP-296, JP-554 and Mandal-2009 revealed significantly high quasispecies diversity for JP-296 and JP-554, with intact 3′NCRs, compared to the low diversity in Mandal-2009, with a truncated 3′NCR. Single-nucleotide polymorphism analysis showed that 40 % of the single-nucleotide polymorphisms were common between quasispecies populations of JP-296 and JP-554, indicating a putative mechanism for how TBEV persists and is maintained within its natural foci.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000704
2017-04-01
2019-09-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/3/413.html?itemId=/content/journal/jgv/10.1099/jgv.0.000704&mimeType=html&fmt=ahah

References

  1. Dobler G. Zoonotic tick-borne flaviviruses. Vet Microbiol 2010; 140: 221– 228 [CrossRef] [PubMed]
    [Google Scholar]
  2. Mansfield KL, Johnson N, Phipps LP, Stephenson JR, Fooks AR et al. Tick-borne encephalitis virus – a review of an emerging zoonosis. J Gen Virol 2009; 90: 1781– 1794 [CrossRef] [PubMed]
    [Google Scholar]
  3. Simmonds P, Becher P, Collett MS, Gould EA, Heinz FX et al. Flaviviridae. 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 London: Elsevier Academic Press; 2012; pp. 1003– 1020
    [Google Scholar]
  4. Dobler G, Hufert F, Pfeffer M, Essbauer S. Tick-borne encephalitis: from microfocus to human disease. Prog Parasitol 2011; 2: 323– 331 [Crossref]
    [Google Scholar]
  5. Süss J. Tick-borne encephalitis 2010: epidemiology, risk areas, and virus strains in Europe and Asia – an overview. Ticks Tick Borne Dis 2011; 2: 2– 15 [CrossRef] [PubMed]
    [Google Scholar]
  6. Pettersson JH, Golovljova I, Vene S, Jaenson TG. Prevalence of tick-borne encephalitis virus in Ixodes ricinus ticks in northern Europe with particular reference to Southern Sweden. Parasit Vectors 2014; 7: 102 [CrossRef] [PubMed]
    [Google Scholar]
  7. Gritsun TS, Venugopal K, Zanotto PM, Mikhailov MV, Sall AA et al. Complete sequence of two tick-borne flaviviruses isolated from Siberia and the UK: analysis and significance of the 5′ and 3′-UTRs. Virus Res 1997; 49: 27– 39 [CrossRef] [PubMed]
    [Google Scholar]
  8. Wallner G, Mandl CW, Kunz C, Heinz FX. The flavivirus 3′-noncoding region: extensive size heterogeneity independent of evolutionary relationships among strains of tick-borne encephalitis virus. Virology 1995; 213: 169– 178 [CrossRef] [PubMed]
    [Google Scholar]
  9. Melik W, Nilsson AS, Johansson M. Detection strategies of tick-borne encephalitis virus in Swedish Ixodes ricinus reveal evolutionary characteristics of emerging tick-borne flaviviruses. Arch Virol 2007; 152: 1027– 1034 [CrossRef] [PubMed]
    [Google Scholar]
  10. Lauring AS, Andino R. Quasispecies theory and the behavior of RNA viruses. PLoS Pathog 2010; 6: e1001005 [CrossRef] [PubMed]
    [Google Scholar]
  11. Sanjuán R, Nebot MR, Chirico N, Mansky LM, Belshaw R. Viral mutation rates. J Virol 2010; 84: 9733– 9748 [CrossRef] [PubMed]
    [Google Scholar]
  12. Ciota AT, Ngo KA, Lovelace AO, Payne AF, Zhou Y et al. Role of the mutant spectrum in adaptation and replication of West Nile virus. J Gen Virol 2007; 88: 865– 874 [CrossRef] [PubMed]
    [Google Scholar]
  13. Labuda M, Randolph SE. Survival strategy of tick-borne encephalitis virus: cellular basis and environmental determinants. Zentralbl Bakteriol 1999; 289: 513– 524 [CrossRef] [PubMed]
    [Google Scholar]
  14. Moshkin MP, Novikov EA, Tkachev SE, Vlasov VV. Epidemiology of a tick-borne viral infection: theoretical insights and practical implications for public health. Bioessays 2009; 31: 620– 628 [CrossRef] [PubMed]
    [Google Scholar]
  15. Asghar N, Lindblom P, Melik W, Lindqvist R, Haglund M et al. Tick-borne encephalitis virus sequenced directly from questing and blood-feeding ticks reveals quasispecies variance. PLoS One 2014; 9: e103264 [CrossRef] [PubMed]
    [Google Scholar]
  16. Romanova LI, Gmyl AP, Dzhivanian TI, Bakhmutov DV, Lukashev AN et al. Microevolution of tick-borne encephalitis virus in course of host alternation. Virology 2007; 362: 75– 84 [CrossRef] [PubMed]
    [Google Scholar]
  17. Růzek D, Gritsun TS, Forrester NL, Gould EA, Kopecký J et al. Mutations in the NS2B and NS3 genes affect mouse neuroinvasiveness of a Western European field strain of tick-borne encephalitis virus. Virology 2008; 374: 249– 255 [CrossRef] [PubMed]
    [Google Scholar]
  18. Brinkley C, Nolskog P, Golovljova I, Lundkvist Å, Bergström T. Tick-borne encephalitis virus natural foci emerge in western Sweden. Int J Med Microbiol 2008; 298: 73– 80 [CrossRef]
    [Google Scholar]
  19. Charrel RN, Attoui H, Butenko AM, Clegg JC, Deubel V et al. Tick-borne virus diseases of human interest in Europe. Clin Microbiol Infect 2004; 10: 1040– 1055 [CrossRef] [PubMed]
    [Google Scholar]
  20. Jaenson TG, Hjertqvist M, Bergström T, Lundkvist A. Why is tick-borne encephalitis increasing? A review of the key factors causing the increasing incidence of human TBE in Sweden. Parasit Vectors 2012; 5: 184 [CrossRef] [PubMed]
    [Google Scholar]
  21. Weidmann M, Frey S, Freire CC, Essbauer S, Růžek D et al. Molecular phylogeography of tick-borne encephalitis virus in central Europe. J Gen Virol 2013; 94: 2129– 2139 [CrossRef] [PubMed]
    [Google Scholar]
  22. Dridi M, Rosseel T, Orton R, Johnson P, Lecollinet S et al. Next-generation sequencing shows West Nile virus quasispecies diversification after a single passage in a carrion crow (Corvus corone) in vivo infection model. J Gen Virol 2015; 96: 2999– 3009 [CrossRef] [PubMed]
    [Google Scholar]
  23. Whetstone C, Miller J, Bortner D, Van der Maaten M. Changes in the restriction endonuclease patterns of four modified-live infectious bovine rhinotracheitis virus (IBRV) vaccines after one passage in host animal. Vaccine 1989; 7: 527– 532 [CrossRef] [PubMed]
    [Google Scholar]
  24. Khasnatinov MA, Tuplin A, Gritsun DJ, Slovak M, Kazimirova M et al. Tick-borne encephalitis virus structural proteins are the primary viral determinants of non-viraemic transmission between ticks whereas non-structural proteins affect cytotoxicity. PLoS One 2016; 11: e0158105 [CrossRef] [PubMed]
    [Google Scholar]
  25. Sakai M, Yoshii K, Sunden Y, Yokozawa K, Hirano M et al. Variable region of the 3′ UTR is a critical virulence factor in the Far-Eastern subtype of tick-borne encephalitis virus in a mouse model. J Gen Virol 2014; 95: 823– 835 [CrossRef] [PubMed]
    [Google Scholar]
  26. Asghar N, Lee YP, Nilsson E, Lindqvist R, Melik W et al. The role of the poly(A) tract in the replication and virulence of tick-borne encephalitis virus. Sci Rep 2016; 6: 39265 [CrossRef] [PubMed]
    [Google Scholar]
  27. Chare ER, Holmes EC. Selection pressures in the capsid genes of plant RNA viruses reflect mode of transmission. J Gen Virol 2004; 85: 3149– 3157 [CrossRef] [PubMed]
    [Google Scholar]
  28. Mandl CW, Holzmann H, Meixner T, Rauscher S, Stadler PF et al. Spontaneous and engineered deletions in the 3′ noncoding region of tick-borne encephalitis virus: construction of highly attenuated mutants of a flavivirus. J Virol 1998; 72: 2132– 2140 [PubMed]
    [Google Scholar]
  29. Formanová P, Černý J, Bolfíková , Valdés JJ, Kozlova I et al. Full genome sequences and molecular characterization of tick-borne encephalitis virus strains isolated from human patients. Ticks Tick Borne Dis 2015; 6: 38– 46 [CrossRef] [PubMed]
    [Google Scholar]
  30. Domingo E. RNA virus evolution, population dynamics, and nutritional status. Biol Trace Elem Res 1997; 56: 23– 30 [CrossRef] [PubMed]
    [Google Scholar]
  31. Norman R, Bowers RG, Begon M, Hudson PJ. Persistence of tick-borne virus in the presence of multiple host species: tick reservoirs and parasite mediated competition. J Theor Biol 1999; 200: 111– 118 [CrossRef] [PubMed]
    [Google Scholar]
  32. Donoso-Mantke O, Karan LS, Ruzek D. Tick-borne encephalitis virus: a general overview. In Ruzek D. (editor) Flavivirus Encephalitis Rijeka, Croatia: InTech; 2011; pp. 133– 156
    [Google Scholar]
  33. Ebel GD, Kramer LD. Short report: duration of tick attachment required for transmission of powassan virus by deer ticks. Am J Trop Med Hyg 2004; 71: 268– 271 [PubMed] [Crossref]
    [Google Scholar]
  34. Andreassen A, Jore S, Cuber P, Dudman S, Tengs T et al. Prevalence of tick borne encephalitis virus in tick nymphs in relation to climatic factors on the southern coast of Norway. Parasit Vectors 2012; 5: 177 [CrossRef] [PubMed]
    [Google Scholar]
  35. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30: 772– 780 [CrossRef] [PubMed]
    [Google Scholar]
  36. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30: 1312– 1313 [CrossRef] [PubMed]
    [Google Scholar]
  37. Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Gateway Computing Environments Workshop (GCE) New Orleans, LA: IEEE; 2010; pp. 1– 8
    [Google Scholar]
  38. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 2013; 14: R36 [CrossRef] [PubMed]
    [Google Scholar]
  39. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J et al. The sequence alignment/map format and SAMtools. Bioinformatics 2009; 25: 2078– 2079 [CrossRef] [PubMed]
    [Google Scholar]
  40. Mckenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010; 20: 1297– 1303 [CrossRef] [PubMed]
    [Google Scholar]
  41. R Core Team R: A Language and Environment for Statistical Computing Vienna: R Foundation for Statistical Computing; 2013
    [Google Scholar]
  42. Bates D, Mächler M, Bolker B, Walker S. Fitting linear Mixed-Effects models using lme4. J Stat Softw 2015; 67: 1– 48 [Crossref]
    [Google Scholar]
  43. Fox J. Effect displays in R for generalised linear models. J Stat Softw 2003; 8: 1– 27 [CrossRef]
    [Google Scholar]
  44. Hothorn T, Bretz F, Westfall P. Simultaneous inference in general parametric models. Biom J 2008; 50: 346– 363 [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000704
Loading
/content/journal/jgv/10.1099/jgv.0.000704
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