1887

Abstract

Phylogenetic analyses can give new insights into the evolutionary history of viruses, especially of viruses with segmented genomes. However, sequence information for many viral families or genera is still limited and phylogenies based on single or short genome fragments can be misleading. We report the first genetic analysis of all three genome segments of Wyeomyia group viruses Wyeomyia, Taiassui, Macaua, Sororoca, Anhembi and Cachoeira Porteira (BeAr328208) in the genus of the family . In addition, Tucunduba and Iaco viruses were identified as members of the Wyeomyia group. Features of Wyeomyia group members that distinguish them from other viruses in the Bunyamwera serogroup and from other orthobunyaviruses, including truncated NSs sequences that may not counteract the host’s interferon response, were characterized. Our findings also suggest genome reassortment within the Wyeomyia group, identifying Macaua and Tucunduba viruses as M-segment reassortants that, in the case of Tucunduba virus, may have altered pathogenicity, stressing the need for whole-genome sequence information to facilitate characterization of orthobunyaviruses and their phylogenetic relationships.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.039479-0
2012-05-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/93/5/1023.html?itemId=/content/journal/jgv/10.1099/vir.0.039479-0&mimeType=html&fmt=ahah

References

  1. Aguilar P. V., Morrison A. C., Rocha C., Watts D. M., Beingolea L., Suarez V., Vargas J., Cruz C., Guevara C. other authors 2010; Guaroa virus infection among humans in Bolivia and Peru. Am J Trop Med Hyg 83:714–721 [View Article][PubMed]
    [Google Scholar]
  2. Aitken T. H., Spence L. 1963; Virus transmission studies with Trinidadian mosquitoes. III. Cache Valley virus. West Indian Med J 12:128–132[PubMed]
    [Google Scholar]
  3. Aitken T. H., Spence L., Jonkers A. H., Anderson C. R. 1968; Wyeomyia-virus isolations in Trinidad, West Indies. Am J Trop Med Hyg 17:886–888[PubMed]
    [Google Scholar]
  4. Akashi H., Gay M., Ihara T., Bishop D. H. 1984; Localized conserved regions of the S RNA gene products of bunyaviruses are revealed by sequence analyses of the Simbu serogroup Aino virus. Virus Res 1:51–63 [View Article][PubMed]
    [Google Scholar]
  5. Akashi H., Kaku Y., Kong X., Pang H. 1997; Antigenic and genetic comparisons of Japanese and Australian Simbu serogroup viruses: evidence for the recovery of natural virus reassortants. Virus Res 50:205–213 [View Article][PubMed]
    [Google Scholar]
  6. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410[PubMed] [CrossRef]
    [Google Scholar]
  7. Anderson C. R., Aitken T. H., Spence L. P., Downs W. G. 1960; Kairi virus, a new virus from Trinidadian forest mosquitoes. Am J Trop Med Hyg 9:70–72[PubMed]
    [Google Scholar]
  8. Beaty B. J., Calisher C. H., Shope R. E. 1989; Arboviruses. In Diagnostic Procedures for Viral, Rickettsial, and Chlamydial Infections, 6th edn. pp. 797–855 Edited by Schmidt N. J., Emmons R. W. Washington, DC: American Public Health Association;
    [Google Scholar]
  9. Beaty B. J., Calisher C. H., Shope R. E. 1995; Arboviruses. In Diagnostic Procedures for Viral, Rickettsial, and Chlamydial Infections, 7th edn. pp. 189–212 Edited by Lennette E. H., Lennette D. A., Lennette E. T. Washington, DC: American Public Health Association;
    [Google Scholar]
  10. Bishop D. H. L. 1996; Biology and molecular biology of bunyaviruses. In The Bunyaviridae pp. 19–61 Edited by Elliott R. M. New York, London: Plenum Press; [CrossRef]
    [Google Scholar]
  11. Bishop D. H. L., Calisher C. H., Casals J., Chumakov M. P., Gaidamovich S. Y., Hannoun C., Lvov D. K., Marshall I. D., Oker-Blom N. other authors 1980; Bunyaviridae . Intervirology 14:125–143 [View Article][PubMed]
    [Google Scholar]
  12. Blakqori G., Delhaye S., Habjan M., Blair C. D., Sánchez-Vargas I., Olson K. E., Attarzadeh-Yazdi G., Fragkoudis R., Kohl A. other authors 2007; La Crosse bunyavirus nonstructural protein NSs serves to suppress the type I interferon system of mammalian hosts. J Virol 81:4991–4999 [View Article][PubMed]
    [Google Scholar]
  13. Bowen M. D., Jackson A. O., Bruns T. D., Hacker D. L., Hardy J. L. 1995; Determination and comparative analysis of the small RNA genomic sequences of California encephalitis, Jamestown Canyon, Jerry Slough, Melao, Keystone and Trivittatus viruses (Bunyaviridae, genus Bunyavirus, California serogroup). J Gen Virol 76:559–572 [View Article][PubMed]
    [Google Scholar]
  14. Bridgen A., Weber F., Fazakerley J. K., Elliott R. M. 2001; Bunyamwera bunyavirus nonstructural protein NSs is a nonessential gene product that contributes to viral pathogenesis. Proc Natl Acad Sci U S A 98:664–669 [View Article][PubMed]
    [Google Scholar]
  15. Briese T., Rambaut A., Lipkin W. I. 2004; Analysis of the medium (M) segment sequence of Guaroa virus and its comparison to other orthobunyaviruses. J Gen Virol 85:3071–3077 [View Article][PubMed]
    [Google Scholar]
  16. Briese T., Bird B., Kapoor V., Nichol S. T., Lipkin W. I. 2006; Batai and Ngari viruses: M segment reassortment and association with severe febrile disease outbreaks in East Africa. J Virol 80:5627–5630 [View Article][PubMed]
    [Google Scholar]
  17. Briese T., Kapoor V., Lipkin W. I. 2007; Natural M-segment reassortment in Potosi and Main Drain viruses: implications for the evolution of orthobunyaviruses. Arch Virol 152:2237–2247 [View Article][PubMed]
    [Google Scholar]
  18. Brockus C. L., Grimstad P. R. 2001; Comparative analysis of G1 glycoprotein-coding sequences of Cache Valley virus (Bunyaviridae: Bunyavirus) isolates. Virus Genes 22:133–139 [View Article][PubMed]
    [Google Scholar]
  19. Calisher C. H. 1996; History, classification, and taxonomy of viruses in the family Bunyaviridae . In The Bunyaviridae pp. 1–17 Edited by Elliott R. M. New York, London: Plenum Press; [CrossRef]
    [Google Scholar]
  20. Calisher C. H., Karabatsos N. 1988; Arbovirus serogroups: definition and geographic distribution. In The Arboviruses: Epidemiology and Ecology pp. 19–57 Edited by Monath T. P. Boca Raton, Florida: CRC Press;
    [Google Scholar]
  21. Calisher C. H., Oro J. G., Lord R. D., Sabattini M. S., Karabatsos N. 1988; Kairi virus identified from a febrile horse in Argentina. Am J Trop Med Hyg 39:519–521[PubMed]
    [Google Scholar]
  22. Campbell W. P., Huang C. 1996; Detection of California serogroup Bunyaviruses in tissue culture and mosquito pools by PCR. J Virol Methods 57:175–179 [View Article][PubMed]
    [Google Scholar]
  23. Casals J., Whitman L. 1960; A new antigenic group of arthropod-borne viruses: the Bunyamwera group. Am J Trop Med Hyg 9:73–77[PubMed]
    [Google Scholar]
  24. Causey O. R., Causey C. E., Maroja O. M., Macedo D. G. 1961; The isolation of arthropod-borne viruses, including members of two hitherto undescribed serological groups, in the Amazon region of Brazil. Am J Trop Med Hyg 10:227–249[PubMed]
    [Google Scholar]
  25. Chenna R., Sugawara H., Koike T., Lopez R., Gibson T. J., Higgins D. G., Thompson J. D. 2003; Multiple sequence alignment with the clustal series of programs. Nucleic Acids Res 31:3497–3500 [View Article][PubMed]
    [Google Scholar]
  26. Clarke D. H., Casals J. 1958; Techniques for hemagglutination and hemagglutination-inhibition with arthropod-borne viruses. Am J Trop Med Hyg 7:561–573[PubMed]
    [Google Scholar]
  27. Claros M. G., von Heijne G. 1994; TopPred II: an improved software for membrane protein structure predictions. Comput Appl Biosci 10:685–686[PubMed]
    [Google Scholar]
  28. de Souza Lopes O., de Abreu Sacchetta L., Fonseca I. E. M., Lacerda J. P. G. 1975; Bertioga (Guama group) and Anhembi (Bunyamwera group), two new arboviruses isolated in São Paulo, Brazil. Am J Trop Med Hyg 24:131–134[PubMed]
    [Google Scholar]
  29. Downs W. G., Spence L., Aitken T. H., Whitman L. 1961; Cache Valley virus, isolated from a Trinidadian mosquito, Aedes scapularis . West Indian Med J 10:13–15[PubMed]
    [Google Scholar]
  30. Drummond A. J., Ashton B., Buxton S., Cheung M., Cooper A., Heled J., Kearse M., Moir R., Stones-Havas S. other authors 2011; Geneious v5.5. http://www.geneious.com
  31. Dunn E. F., Pritlove D. C., Elliott R. M. 1994; The S RNA genome segments of Batai, Cache Valley, Guaroa, Kairi, Lumbo, Main Drain and Northway bunyaviruses: sequence determination and analysis. J Gen Virol 75:597–608 [View Article][PubMed]
    [Google Scholar]
  32. Eifan S. A., Elliott R. M. 2009; Mutational analysis of the Bunyamwera orthobunyavirus nucleocapsid protein gene. J Virol 83:11307–11317 [View Article][PubMed]
    [Google Scholar]
  33. Estrada D. F., De Guzman R. N. 2011; Structural characterization of the Crimean-Congo hemorrhagic fever virus Gn tail provides insight into virus assembly. J Biol Chem 286:21678–21686 [View Article][PubMed]
    [Google Scholar]
  34. Fauquet C. M., Mayo M. A., Maniloff J., Desselberger U., Ball L. A. editors 2005 Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses London, San Diego: Elsevier Academic Press;
    [Google Scholar]
  35. Fazakerley J. K., Gonzalez-Scarano F., Strickler J., Dietzschold B., Karush F., Nathanson N. 1988; Organization of the middle RNA segment of snowshoe hare Bunyavirus. Virology 167:422–432[PubMed] [CrossRef]
    [Google Scholar]
  36. Forshey B. M., Guevara C., Laguna-Torres V. A., Cespedes M., Vargas J., Gianella A., Vallejo E., Madrid C., Aguayo N. other authors 2010; Arboviral etiologies of acute febrile illnesses in Western South America, 2000–2007. PLoS Negl Trop Dis 4:e787 [View Article][PubMed]
    [Google Scholar]
  37. Gerrard S. R., Li L., Barrett A. D., Nichol S. T. 2004; Ngari virus is a Bunyamwera virus reassortant that can be associated with large outbreaks of hemorrhagic fever in Africa. J Virol 78:8922–8926 [View Article][PubMed]
    [Google Scholar]
  38. Huang C., Shope R. E., Spargo B., Campbell W. P. 1996; The S RNA genomic sequences of Inkoo, San Angelo, Serra do Navio, South River and Tahyna bunyaviruses. J Gen Virol 77:1761–1768 [View Article][PubMed]
    [Google Scholar]
  39. Iroegbu C. U., Pringle C. R. 1981; Genetic interactions among viruses of the Bunyamwera complex. J Virol 37:383–394[PubMed]
    [Google Scholar]
  40. Jin H., Elliott R. M. 1992; Mutagenesis of the L protein encoded by Bunyamwera virus and production of monospecific antibodies. J Gen Virol 73:2235–2244 [View Article][PubMed]
    [Google Scholar]
  41. Käll L., Krogh A., Sonnhammer E. L. 2004; A combined transmembrane topology and signal peptide prediction method. J Mol Biol 338:1027–1036 [View Article][PubMed]
    [Google Scholar]
  42. Klimas R. A., Thompson W. H., Calisher C. H., Clark G. G., Grimstad P. R., Bishop D. H. 1981; Genotypic varieties of La Crosse virus isolated from different geographic regions of the continental United States and evidence for a naturally occurring intertypic recombinant La Crosse virus. Am J Epidemiol 114:112–131[PubMed]
    [Google Scholar]
  43. Krogh A., Larsson B., von Heijne G., Sonnhammer E. L. 2001; Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580 [View Article][PubMed]
    [Google Scholar]
  44. Lambert A. J., Lanciotti R. S. 2009; Consensus amplification and novel multiplex sequencing method for S segment species identification of 47 viruses of the Orthobunyavirus, Phlebovirus, and Nairovirus genera of the family Bunyaviridae . J Clin Microbiol 47:2398–2404 [View Article][PubMed]
    [Google Scholar]
  45. Leonard V. H. J., Kohl A., Osborne J. C., McLees A., Elliott R. M. 2005; Homotypic interaction of Bunyamwera virus nucleocapsid protein. J Virol 79:13166–13172 [View Article][PubMed]
    [Google Scholar]
  46. Léonard V. H., Kohl A., Hart T. J., Elliott R. M. 2006; Interaction of Bunyamwera orthobunyavirus NSs protein with mediator protein MED8: a mechanism for inhibiting the interferon response. J Virol 80:9667–9675 [View Article][PubMed]
    [Google Scholar]
  47. Margulies M., Egholm M., Altman W. E., Attiya S., Bader J. S., Bemben L. A., Berka J., Braverman M. S., Chen Y. J. other authors 2005; Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380[PubMed]
    [Google Scholar]
  48. Mohamed M., McLees A., Elliott R. M. 2009; Viruses in the Anopheles A, Anopheles B, and Tete serogroups in the Orthobunyavirus genus (family Bunyaviridae) do not encode an NSs protein. J Virol 83:7612–7618 [View Article][PubMed]
    [Google Scholar]
  49. Mores C. N., Turell M. J., Dyer J., Rossi C. A. 2009; Phylogenetic relationships among orthobunyaviruses isolated from mosquitoes captured in Peru. Vector Borne Zoonotic Dis 9:25–32 [View Article][PubMed]
    [Google Scholar]
  50. Müller R., Poch O., Delarue M., Bishop D. H., Bouloy M. 1994; Rift Valley fever virus L segment: correction of the sequence and possible functional role of newly identified regions conserved in RNA-dependent polymerases. J Gen Virol 75:1345–1352 [View Article][PubMed]
    [Google Scholar]
  51. Nielsen H., Krogh A. 1998; Prediction of signal peptides and signal anchors by a hidden Markov model. In Proceedings of the Sixth International Conference on Intelligent Systems for Molecular Biology (ISMB6), Montreal, Canada pp. 122–130 Palo Alto, CA: AAAI Press;
    [Google Scholar]
  52. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. 1997; Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6 [View Article][PubMed]
    [Google Scholar]
  53. Nunes M. R., Travassos da Rosa A. P., Weaver S. C., Tesh R. B., Vasconcelos P. F. 2005; Molecular epidemiology of group C viruses (Bunyaviridae, Orthobunyavirus) isolated in the Americas. J Virol 79:10561–10570 [View Article][PubMed]
    [Google Scholar]
  54. Pinheiro F. P., Travassos da Rosa A., Vasconcelos P. F. 1994; Guaroa and other Bunyamwera group fevers. In Handbook of Zoonoses, Section B: Viral Zoonosis, 2nd edn. pp. 217–218 Edited by Beran G. W. Boca Raton, FL: CRC Press;
    [Google Scholar]
  55. Plassmeyer M. L., Soldan S. S., Stachelek K. M., Roth S. M., Martín-García J., González-Scarano F. 2007; Mutagenesis of the La Crosse Virus glycoprotein supports a role for Gc (1066–1087) as the fusion peptide. Virology 358:273–282 [View Article][PubMed]
    [Google Scholar]
  56. Poch O., Sauvaget I., Delarue M., Tordo N. 1989; Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J 8:3867–3874[PubMed]
    [Google Scholar]
  57. Quan P. L., Palacios G., Jabado O. J., Conlan S., Hirschberg D. L., Pozo F., Jack P. J., Cisterna D., Renwick N. other authors 2007; Detection of respiratory viruses and subtype identification of influenza A viruses by GreeneChipResp oligonucleotide microarray. J Clin Microbiol 45:2359–2364 [View Article][PubMed]
    [Google Scholar]
  58. Reese S. M., Blitvich B. J., Blair C. D., Geske D., Beaty B. J., Black W. C. IV 2008; Potential for La Crosse virus segment reassortment in nature. Virol J 5:164 [View Article][PubMed]
    [Google Scholar]
  59. Rice P., Longden I., Bleasby A. 2000; emboss: the European Molecular Biology Open Software Suite. Trends Genet 16:276–277 [View Article][PubMed]
    [Google Scholar]
  60. Roca-Garcia M. 1944; The isolation of three neurotropic viruses from forest mosquitoes in eastern Colombia. J Infect Dis 75:160–169 [View Article]
    [Google Scholar]
  61. Saeed M. F., Wang H., Nunes M., Vasconcelos P. F., Weaver S. C., Shope R. E., Watts D. M., Tesh R. B., Barrett A. D. 2000; Nucleotide sequences and phylogeny of the nucleocapsid gene of Oropouche virus. J Gen Virol 81:743–748[PubMed]
    [Google Scholar]
  62. Saeed M. F., Li L., Wang H., Weaver S. C., Barrett A. D. 2001a; Phylogeny of the Simbu serogroup of the genus Bunyavirus . J Gen Virol 82:2173–2181[PubMed]
    [Google Scholar]
  63. Saeed M. F., Wang H., Suderman M., Beasley D. W., Travassos da Rosa A., Li L., Shope R. E., Tesh R. B., Barrett A. D. 2001b; Jatobal virus is a reassortant containing the small RNA of Oropouche virus. Virus Res 77:25–30 [View Article][PubMed]
    [Google Scholar]
  64. Schmaljohn C. S., Hooper J. W. 2001; Bunyaviridae: the viruses and their replication. In Fields Virology, 4th edn. pp. 1581–1602 Edited by Knipe D. M., Howley P. M. Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  65. Srihongse S., Johnson C. M. 1965; Wyeomyia subgroup of arbovirus: isolation from man. Science 149:863–864 [View Article][PubMed]
    [Google Scholar]
  66. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011; mega5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739 [View Article][PubMed]
    [Google Scholar]
  67. Travassos da Rosa J. F., Travassos da Rosa A., Vasconcelos P. F., Pinheiro F. P., Rodrigues S. G., Travassos da Rosa E. S., Dias L. B., Cruz A. C. 1998; Arboviruses isolated in the Evandro Chagas Institute, including some described for the first time in the Brazilian Arnazon region, their known hosts, and their pathology for man. In An Overview of Arbovirology in Brazil and Neighbouring Countries pp. 19–31 Edited by Travassos da Rosa A., Travassos da Rosa J. F., Vasconcelos P. F. Belem, Brazil: Instituto Evandro Chagas;
    [Google Scholar]
  68. van Knippenberg I., Carlton-Smith C., Elliott R. M. 2010; The N-terminus of Bunyamwera orthobunyavirus NSs protein is essential for interferon antagonism. J Gen Virol 91:2002–2006 [View Article][PubMed]
    [Google Scholar]
  69. Vasconcelos P. F., Travassos da Rosa A., Degallier N., Travassos da Rosa J. F., Pinheiro F. P. 1992; Clinical and ecoepidemiological situation of human arboviruses in Brazilian Amazonia. Cienc Cult 44:117–124
    [Google Scholar]
  70. Vasconcelos P. F., Travassos da Rosa A., Pinheiro F. P., Shope R. E., Travassos da Rosa J. F., Rodrigues S. G., Degallier N., Travassos da Rosa E. S. 1998; Arboviruses pathogenic for man in Brazil. In An Overview of Arbovirology in Brazil and Neighbouring Countries pp. 72–99 Edited by Travassos da Rosa A., Travassos da Rosa J. F., Vasconcelos P. F. Belem, Brazil: Instituto Evandro Chagas;
    [Google Scholar]
  71. Weber F., Bridgen A., Fazakerley J. K., Streitenfeld H., Kessler N., Randall R. E., Elliott R. M. 2002; Bunyamwera bunyavirus nonstructural protein NSs counteracts the induction of alpha/beta interferon. J Virol 76:7949–7955 [View Article][PubMed]
    [Google Scholar]
  72. Yanase T., Aizawa M., Kato T., Yamakawa M., Shirafuji H., Tsuda T. 2010; Genetic characterization of Aino and Peaton virus field isolates reveals a genetic reassortment between these viruses in nature. Virus Res 153:1–7 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.039479-0
Loading
/content/journal/jgv/10.1099/vir.0.039479-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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