1887

Abstract

Understanding the potential for host range shifts and expansions of RNA viruses is critical to predicting the evolutionary and epidemiological paths of these pathogens. As arthropod-borne viruses (arboviruses) experience frequent spillover from their amplification cycles and are generalists by nature, they are likely to experience a relatively high frequency of success in a range of host environments. Despite this, the potential for host expansion, the genetic correlates of adaptation to novel environments and the costs of such adaptations in originally competent hosts are still not characterized fully for arboviruses. In the studies presented here, we utilized experimental evolution of St. Louis encephalitis virus (SLEV; family , genus ) in the line of tick cells to model adaptation to a novel invertebrate host. Our results demonstrated that levels of adaptation and costs in alternate hosts are highly variable among lineages, but also that significant fitness increases in tick cells are achievable with only modest change in consensus genetic sequence. In addition, although accumulation of diversity may at times buffer against phenotypic costs within the SLEV swarm, an increased proportion of variants with an impaired capacity to infect and spread on vertebrate cell culture accumulated with tick cell passage. Isolation and characterization of a subset of these variants implicates the NS3 gene as an important host range determinant for SLEV.

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2014-06-01
2024-12-04
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References

  1. Chamberlain R. W. 1980; History of St. Louis encephalitis. In St. Louis Encephalitis pp. 3–61 Edited by Monath T. P. Washington, DC: American Public Health Association;
    [Google Scholar]
  2. Chao L. 1990; Fitness of RNA virus decreased by Muller’s ratchet. Nature 348:454–455 [View Article][PubMed]
    [Google Scholar]
  3. Ciota A. T., Kramer L. D. 2010; Insights into arbovirus evolution and adaptation from experimental studies. Viruses 2:2594–2617 [View Article][PubMed]
    [Google Scholar]
  4. Ciota A. T., Lovelace A. O., Jones S. A., Payne A., Kramer L. D. 2007a; Adaptation of two flaviviruses results in differences in genetic heterogeneity and virus adaptability. J Gen Virol 88:2398–2406 [View Article][PubMed]
    [Google Scholar]
  5. Ciota A. T., Lovelace A. O., Ngo K. A., Le A. N., Maffei J. G., Franke M. A., Payne A. F., Jones S. A., Kauffman E. B., Kramer L. D. 2007b; Cell-specific adaptation of two flaviviruses following serial passage in mosquito cell culture. Virology 357:165–174 [View Article][PubMed]
    [Google Scholar]
  6. Ciota A. T., Ngo K. A., Lovelace A. O., Payne A. F., Zhou Y., Shi P.-Y., Kramer L. D. 2007c; Role of the mutant spectrum in adaptation and replication of West Nile virus. J Gen Virol 88:865–874 [View Article][PubMed]
    [Google Scholar]
  7. Ciota A. T., Jia Y., Payne A. F., Jerzak G., Davis L. J., Young D. S., Ehrbar D., Kramer L. D. 2009; Experimental passage of St. Louis encephalitis virus in vivo in mosquitoes and chickens reveals evolutionarily significant virus characteristics. PLoS ONE 4:e7876 [View Article][PubMed]
    [Google Scholar]
  8. Ciota A. T., Ehrbar D. J., Van Slyke G. A., Willsey G. G., Kramer L. D. 2012; Cooperative interactions in the West Nile virus mutant swarm. BMC Evol Biol 12:58 [View Article][PubMed]
    [Google Scholar]
  9. Deardorff E. R., Fitzpatrick K. A., Jerzak G. V., Shi P. Y., Kramer L. D., Ebel G. D. 2011; West Nile virus experimental evolution in vivo and the trade-off hypothesis. PLoS Pathog 7:e1002335 [View Article][PubMed]
    [Google Scholar]
  10. Díaz L. A., Albrieu Llinás G., Vázquez A., Tenorio A., Contigiani M. S. 2012; Silent circulation of St. Louis encephalitis virus prior to an encephalitis outbreak in Cordoba, Argentina (2005). PLoS Negl Trop Dis 6:e1489 [View Article][PubMed]
    [Google Scholar]
  11. Duarte E., Clarke D., Moya A., Domingo E., Holland J. 1992; Rapid fitness losses in mammalian RNA virus clones due to Muller’s ratchet. Proc Natl Acad Sci U S A 89:6015–6019 [View Article][PubMed]
    [Google Scholar]
  12. Duarte E. A., Novella I. S., Ledesma S., Clarke D. K., Moya A., Elena S. F., Domingo E., Holland J. J. 1994; Subclonal components of consensus fitness in an RNA virus clone. J Virol 68:4295–4301[PubMed]
    [Google Scholar]
  13. Ebel G. D., Fitzpatrick K. A., Lim P. Y., Bennett C. J., Deardorff E. R., Jerzak G. V., Kramer L. D., Zhou Y., Shi P. Y., Bernard K. A. 2011; Nonconsensus West Nile virus genomes arising during mosquito infection suppress pathogenesis and modulate virus fitness in vivo . J Virol 85:12605–12613 [View Article][PubMed]
    [Google Scholar]
  14. Greene I. P., Wang E., Deardorff E. R., Milleron R., Domingo E., Weaver S. C. 2005; Effect of alternating passage on adaptation of sindbis virus to vertebrate and invertebrate cells. J Virol 79:14253–14260 [View Article][PubMed]
    [Google Scholar]
  15. Holland J. J., de la Torre J. C., Clarke D. K., Duarte E. 1991; Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. J Virol 65:2960–2967[PubMed]
    [Google Scholar]
  16. Jerzak G., Bernard K. A., Kramer L. D., Ebel G. D. 2005; Genetic variation in West Nile virus from naturally infected mosquitoes and birds suggests quasispecies structure and strong purifying selection. J Gen Virol 86:2175–2183 [View Article][PubMed]
    [Google Scholar]
  17. Jerzak G. V., Brown I., Shi P. Y., Kramer L. D., Ebel G. D. 2008; Genetic diversity and purifying selection in West Nile virus populations are maintained during host switching. Virology 374:256–260 [View Article][PubMed]
    [Google Scholar]
  18. Kassen R. 2002; The experimental evolution of specialists, generalists, and the maintenance of diversity. J Evol Biol 15:173–190 [View Article]
    [Google Scholar]
  19. Kopp A., Gillespie T. R., Hobelsberger D., Estrada A., Harper J. M., Miller R. A., Eckerle I., Müller M. A., Podsiadlowski L. other authors 2013; Provenance and geographic spread of St. Louis encephalitis virus. MBio 4:e00322-13 [View Article][PubMed]
    [Google Scholar]
  20. Kramer L. D., Chandler L. J. 2001; Phylogenetic analysis of the envelope gene of St. Louis encephalitis virus. Arch Virol 146:2341–2355 [View Article][PubMed]
    [Google Scholar]
  21. Martínez M. A., Carrillo C., González-Candelas F., Moya A., Domingo E., Sobrino F. 1991; Fitness alteration of foot-and-mouth disease virus mutants: measurement of adaptability of viral quasispecies. J Virol 65:3954–3957[PubMed]
    [Google Scholar]
  22. McLean R. G., Francy D. B., Monath T. P., Calisher C. H., Trent D. W. 1985; Isolation of St. Louis encephalitis virus from adult Dermacentor variabilis (Acari: Ixodidae). J Med Entomol 22:232–233[PubMed] [CrossRef]
    [Google Scholar]
  23. Mitchell C. J., Gubler D. J., Monath T. P. 1983; Variation in infectivity of Saint Louis encephalitis viral strains for Culex pipiens quinquefasciatus (Diptera: Culicidae). J Med Entomol 20:526–533[PubMed] [CrossRef]
    [Google Scholar]
  24. Monath T. P., Heinz F. X. 1996; Flaviviruses. In Fields Virology, 3rd edn. pp. 961–1034 Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  25. Moudy R. M., Meola M. A., Morin L. L., Ebel G. D., Kramer L. D. 2007; A newly emergent genotype of West Nile virus is transmitted earlier and more efficiently by Culex mosquitoes. Am J Trop Med Hyg 77:365–370[PubMed]
    [Google Scholar]
  26. Novella I. S. 2004; Negative effect of genetic bottlenecks on the adaptability of vesicular stomatitis virus. J Mol Biol 336:61–67 [View Article][PubMed]
    [Google Scholar]
  27. Novella I. S., Ebendick-Corpus B. E. 2004; Molecular basis of fitness loss and fitness recovery in vesicular stomatitis virus. J Mol Biol 342:1423–1430 [View Article][PubMed]
    [Google Scholar]
  28. Novella I. S., Hershey C. L., Escarmis C., Domingo E., Holland J. J. 1999; Lack of evolutionary stasis during alternating replication of an arbovirus in insect and mammalian cells. J Mol Biol 287:459–465 [View Article][PubMed]
    [Google Scholar]
  29. Novella I. S., Ball L. A., Wertz G. W. 2004; Fitness analyses of vesicular stomatitis strains with rearranged genomes reveal replicative disadvantages. J Virol 78:9837–9841 [View Article][PubMed]
    [Google Scholar]
  30. Novella I. S., Ebendick-Corpus B. E., Zárate S., Miller E. L. 2007; Emergence of mammalian cell-adapted vesicular stomatitis virus from persistent infections of insect vector cells. J Virol 81:6664–6668 [View Article][PubMed]
    [Google Scholar]
  31. Novella I. S., Presloid J. B., Smith S. D., Wilke C. O. 2011; Specific and nonspecific host adaptation during arboviral experimental evolution. J Mol Microbiol Biotechnol 21:71–81 [View Article][PubMed]
    [Google Scholar]
  32. Parrish C. R., Holmes E. C., Morens D. M., Park E. C., Burke D. S., Calisher C. H., Laughlin C. A., Saif L. J., Daszak P. 2008; Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol Mol Biol Rev 72:457–470 [View Article][PubMed]
    [Google Scholar]
  33. Payne A. F., Binduga-Gajewska I., Kauffman E. B., Kramer L. D. 2006; Quantitation of flaviviruses by fluorescent focus assay. J Virol Methods 134:183–189 [View Article][PubMed]
    [Google Scholar]
  34. Reisen W. K. 2003; Epidemiology of St. Louis encephalitis virus. Adv Virus Res 61:139–183 [View Article][PubMed]
    [Google Scholar]
  35. Remold S. K., Rambaut A., Turner P. E. 2008; Evolutionary genomics of host adaptation in vesicular stomatitis virus. Mol Biol Evol 25:1138–1147 [View Article][PubMed]
    [Google Scholar]
  36. Rodrigues S. G., Nunes M. R., Casseb S. M., Prazeres A. S., Rodrigues D. S., Silva M. O., Cruz A. C., Tavares-Neto J. C., Vasconcelos P. F. 2010; Molecular epidemiology of Saint Louis encephalitis virus in the Brazilian Amazon: genetic divergence and dispersal. J Gen Virol 91:2420–2427 [View Article][PubMed]
    [Google Scholar]
  37. Ruiz-Jarabo C. M., Arias A., Baranowski E., Escarmís C., Domingo E. 2000; Memory in viral quasispecies. J Virol 74:3543–3547 [View Article][PubMed]
    [Google Scholar]
  38. Ruíz-Jarabo C. M., Arias A., Molina-París C., Briones C., Baranowski E., Escarmís C., Domingo E. 2002; Duration and fitness dependence of quasispecies memory. J Mol Biol 315:285–296 [View Article][PubMed]
    [Google Scholar]
  39. Schuffenecker I., Iteman I., Michault A., Murri S., Frangeul L., Vaney M. C., Lavenir R., Pardigon N., Reynes J. M. other authors 2006; Genome microevolution of chikungunya viruses causing the Indian Ocean outbreak. PLoS Med 3:e263 [View Article][PubMed]
    [Google Scholar]
  40. Scott T. W., Weaver S. C., Mallampalli V. L. 1994; Evolution of mosquito-borne viruses. In The Evolutionary Biology of Viruses pp. 293–324 Edited by Morse S. S. New York: Raven Press;
    [Google Scholar]
  41. Shi P.-Y., Kauffman E. B., Ren P., Felton A., Tai J. H., Dupuis A. P. II, Jones S. A., Ngo K. A., Nicholas D. C. other authors 2001; High-throughput detection of West Nile virus RNA. J Clin Microbiol 39:1264–1271 [View Article][PubMed]
    [Google Scholar]
  42. Smith M. G., Blattner R. J., Heys F. M. 1944; The isolation of the St. Louis encephalitis virus from chicken mites (Dermanyssus gallinae) in nature. Science 100:362–363 [View Article][PubMed]
    [Google Scholar]
  43. Smith-Tsurkan S. D., Wilke C. O., Novella I. S. 2010; Incongruent fitness landscapes, not tradeoffs, dominate the adaptation of vesicular stomatitis virus to novel host types. J Gen Virol 91:1484–1493 [View Article][PubMed]
    [Google Scholar]
  44. Turell M. J., O’Guinn M. L., Jones J. W., Sardelis M. R., Dohm D. J., Watts D. M., Fernandez R., Travassos da Rosa A., Guzman H. other authors 2005; Isolation of viruses from mosquitoes (Diptera: Culicidae) collected in the Amazon Basin region of Peru. J Med Entomol 42:891–898 [View Article][PubMed]
    [Google Scholar]
  45. Turner P. E., Elena S. F. 2000; Cost of host radiation in an RNA virus. Genetics 156:1465–1470[PubMed]
    [Google Scholar]
  46. Turner P. E., Morales N. M., Alto B. W., Remold S. K. 2010; Role of evolved host breadth in the initial emergence of an RNA virus. Evolution 64:3273–3286 [View Article][PubMed]
    [Google Scholar]
  47. Vasilakis N., Deardorff E. R., Kenney J. L., Rossi S. L., Hanley K. A., Weaver S. C. 2009; Mosquitoes put the brake on arbovirus evolution: experimental evolution reveals slower mutation accumulation in mosquito than vertebrate cells. PLoS Pathog 5:e1000467 [View Article][PubMed]
    [Google Scholar]
  48. Woelk C. H., Holmes E. C. 2002; Reduced positive selection in vector-borne RNA viruses. Mol Biol Evol 19:2333–2336 [View Article][PubMed]
    [Google Scholar]
  49. Woolhouse M. E., Taylor L. H., Haydon D. T. 2001; Population biology of multihost pathogens. Science 292:1109–1112 [View Article][PubMed]
    [Google Scholar]
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