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Identification of a phylogenetically distinct orthobunyavirus from group C

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Abstract

Apeu virus (APEUV) (family Bunyaviridae, genus Orthobunyavirus) was plaque purified and characterised by serological and molecular analysis. Neutralising assays confirmed cross-reactivity between purified APEUV clones and the Caraparu virus complex of group C orthobunyaviruses. Partial sequencing of the L, M and S segments of one APEUV clone (APEUV-CL5) was carried out. A phylogenetic tree constructed with the L amino acid sequences clustered APEUV-CL5 within the genus Orthobunyavirus, confirming its serological classification. Analysis of M segment sequences clustered APEUV-CL5 in the Caraparu virus complex (Group C), in agreement with serological tests and previous molecular characterisation. However, the sequence of the nucleocapsid gene (N) gave low identity values when compared to those of the group C viruses. The phylogenetic tree based on N nucleotide sequences clustered APEUV-CL5 next to the California and Bwamba groups. This remarkable S nucleotide variability suggests that APEUV-CL5 could be a genetic reassortant and that this evolutionary mechanism is present in the history of the group C viruses.

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References

  1. Aquino VH, Figueiredo LT (2004) Linear amplification followed by single primer polymerase chain reaction to amplify unknown DNA fragments: complete nucleotide sequence of Oropouche virus M RNA segment. J Virol Methods 115:51–57

    Article  PubMed  CAS  Google Scholar 

  2. Bernardes-Terzian AC, de-Moraes-Bronzoni RV, Drumond BP, Da Silva-Nunes M, da-Silva NS, Urbano-Ferreira M, Sperança MA, Nogueira ML (2009) Sporadic oropouche virus infection, acre, Brazil. Emerg Infect Dis 15:348–350

    Article  PubMed  Google Scholar 

  3. Bishop DH (1985) The genetic basis for describing viruses as species. Intervirology 24:79–93

    Article  PubMed  CAS  Google Scholar 

  4. Bowen MD, Trappier SG, Sanchez AJ, Meyer RF, Goldsmith CS, Zaki SR, Dunster LM, Peters CJ, Ksiazek TG, Nichol ST (2001) A reassortant bunyavirus isolated from acute hemorrhagic fever cases in Kenya and Somalia. Virology 291:185–190

    Article  PubMed  CAS  Google Scholar 

  5. Bridgen A, Weber F, Fazakerley JK, Elliott RM (2001) Bunyamwera bunyavirus nonstructural protein NSs is a nonessential gene product that contributes to viral pathogenesis. Proc Natl Acad Sci USA 98:664–669

    Article  PubMed  CAS  Google Scholar 

  6. Brito Magalhães CL, Quinan BR, Novaes RFV, Santos JR, Kroon EG, Bonjardim CA, Ferreira PCP (2007) Caraparu virus (group C Orthobunyavirus): sequencing and phylogenetic analysis based on the conserved region 3 of the RNA polymerase gene. Virus Genes 35:681–684

    Article  PubMed  Google Scholar 

  7. Calisher CH (1988) Evolutionary significance of the taxonomic data regarding bunyaviruses of the family Bunyaviridae. Intervirology 29:268–276

    PubMed  CAS  Google Scholar 

  8. Calisher CH (1996) History, classification, and taxonomy of viruses in the family Bunyaviridae. In: Elliott RM (ed) The Bunyaviridae. Plenum Press, New York, pp 1–17

    Google Scholar 

  9. Casals J, Whitman L (1961) Group C, a new serological group of hitherto undescribed arthropod-borne viruses. Immunological studies. Am J Trop Med Hyg 10:250–258

    PubMed  CAS  Google Scholar 

  10. Causey OR, Causey CE, Maroja OM, Macedo DG (1961) The isolation of arthropod-born viruses including members of two hitherto undescribed serological groups, in the Amazon Region of Brazil. Am J Trop Med Hyg 10:227–249

    PubMed  CAS  Google Scholar 

  11. De Mucha Macias J, Davalos Mata A, Ochoa Larios ME, Zarate Aquino ML (1969) Experimental infection using Apeu virus in mice (Mus musculus albinus). Histopathological injuries. Salud Publica Mex 11:323–338

    PubMed  CAS  Google Scholar 

  12. Dulbecco R (1952) Production of plaques in monolayer tissue cultures by single particles of an animal virus. Proc Natl Acad Sci USA 38:747–752

    Article  PubMed  CAS  Google Scholar 

  13. Eifan SA, Elliott RM (2009) Mutational analysis of the Bunyamwera orthobunyavirus nucleocapsid protein gene. J Virol 83:11307–11317

    Article  PubMed  CAS  Google Scholar 

  14. Elliott RM (1985) Identification of nonstructural proteins encoded by viruses of the Bunyamwera serogroup (family Bunyaviridae). Virology 143:119–126

    Article  PubMed  CAS  Google Scholar 

  15. Elliott RM (1989) Nucleotide sequence analysis of the large (L) genomic RNA segment of Bunyamwera virus, the prototype of the family Bunyaviridae. Virology 171:426–436

    Article  Google Scholar 

  16. Elliott RM (1997) Emerging viruses: the Bunyaviridae. Mol Med 3:572–577

    PubMed  CAS  Google Scholar 

  17. Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) (2005) Committee on taxonomy of viruses (ICTV) virus taxonomy. Classification and nomenclature of viruses. 8th ICTV report. Academic Press/Elsevier, San Diego

  18. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  19. Forshey BM, Guevara C, Laguna-Torres VA, Cespedes M, Vargas J, Gianella A, Vallejo E, Madrid C, Aguayo N, Gotuzzo E, Suarez V, Morales AM, Beingolea L, Reyes N, Perez J, Negrete M, Rocha C, Morrison AC, Russell KL, Blair PJ, Olson JG, Kochel TJ, NMRCD Febrile Surveillance Working Group (2010) Arboviral etiologies of acute febrile illnesses in Western South America, 2000–2007. PLoS Negl Trop Dis 4(8):e787

    Article  PubMed  Google Scholar 

  20. Gentsch JR, Bishop DL (1979) M viral RNA segment of bunyaviruses codes for two glycoproteins, G1 and G2. J Virol 30:767–770

    PubMed  CAS  Google Scholar 

  21. Gerrard SR, Li L, Barrett AD, Nichol ST (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

    Article  PubMed  CAS  Google Scholar 

  22. Gibbs CJ Jr , Bruckner EA, Schenker S (1964) A case of Apeu virus infection. Am J Trop Med Hyg 13:108–113

    Google Scholar 

  23. Henderson WW, Monroe MC, St Jeor SC, Thayer WP, Rowe JE, Peters CJ, Nichol ST (1995) Naturally occurring Sin Nombre virus genetic reassortants. Virology 214:602–610

    Article  PubMed  CAS  Google Scholar 

  24. Holland J, Domingo E (1998) Origin and evolution of viruses. Virus Genes 16:13–21

    Article  PubMed  CAS  Google Scholar 

  25. Hronovský V, Benda R (1981) Use of hyperimmune mouse ascitic fluids for arbovirus differentiation by indirect immunofluorescence and conventional serology. Acta Virol 25:295–303

    PubMed  Google Scholar 

  26. Huang X, Madan A (1999) CAP3: A DNA sequence assembly program. Genome Res 9:868–877

    Article  PubMed  CAS  Google Scholar 

  27. Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  28. Kuno G, Mitchell CJ, Chang GJ, Smith GC (1996) Detecting bunyaviruses of the Bunyamwera and California serogroups by a PCR technique. J Clin Microbiol 34:1184–1188

    PubMed  CAS  Google Scholar 

  29. Martin DP, Williamson C, Posada D (2005) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21:260–262

    Article  PubMed  CAS  Google Scholar 

  30. Nichol ST (2001) Bunyaviruses. In: Fields BN, Knipe DM, Howley PM, Griffin DE (eds) Fields virology, 4th edn. Lippincott Williams & Wilkins, Philadelphia, pp 1603–1633

    Google Scholar 

  31. Nunes MRT, Travassos da Rosa APA, Weaver SC, Tesh RB, Vasconcelos PF (2005) Molecular epidemiology of group C viruses (Bunyaviridae, Orthobunyavirus) isolated in the Americas. J Virol 79:10561–10570

    Article  PubMed  CAS  Google Scholar 

  32. Posada D (2006) ModelTest Server: a web-based tool for the statistical selection of models of nucleotide substitution online. Nucleic Acids Res 34:W700–W703

    Article  PubMed  CAS  Google Scholar 

  33. Reese SM, Blitvich BJ, Blair CD, Geske D, Beaty BJ, Black WC (2008) Potential for La Crosse virus segment reassortment in nature. Virol J 5:164

    Article  PubMed  Google Scholar 

  34. Saeed MF, Wang H, Suderman M, Beasley DW, Travassos da Rosa A, Li L, Shope RE, Tesh RB, Barrett AD (2001) Jatobal virus is a reassortant containing the small RNA of Oropouche virus. Virus Res 77:25–30

    Article  PubMed  CAS  Google Scholar 

  35. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstruction phylogenetic trees. Mol Biol Evol 4:406–425

    PubMed  CAS  Google Scholar 

  36. Sall AA, Zanotto PM, Sene OK, Zeller HG (1999) Genetic reassortment of Rift valley fever virus in nature. J Virol 73:8196–8200

    PubMed  CAS  Google Scholar 

  37. Schmaljohn CS, Nichol ST (2007) Bunyaviridae. In: Fields BN, Knipe DM, Howley PM, Griffin DE (eds) Fields Virology, 5th edn edn. Lippincott Williams & Wilkins, Philadelphia, pp 1741–1778

    Google Scholar 

  38. Shope RE, Causey OR (1962) Further studies on the serological relationships of group C arthropod-borne viruses and the application of these relationships to rapid identification of types. Am J Trop Med Hyg 11:283–290

    PubMed  CAS  Google Scholar 

  39. Shope RE, Whitman L (1966) Nepuyo virus, a new group C agent isolated in Trinidad and Brazil. II Serological studies. Am J Trop Med Hyg 15:772–774

    PubMed  CAS  Google Scholar 

  40. Soldan SS, González-Scarano F (2005) Emerging infectious diseases: the Bunyaviridae. J Neurovirol 11:412–423

    Article  PubMed  Google Scholar 

  41. Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Mol Biol Evol 9:678–687

    PubMed  CAS  Google Scholar 

  42. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  PubMed  CAS  Google Scholar 

  43. van Knippenberg I, Carlton-Smith C, Elliott RM (2010) The N-terminus of Bunyamwera orthobunyavirus NSs protein is essential for interferon antagonism. J Gen Virol 91:2002–2006

    Article  PubMed  Google Scholar 

  44. Vasconcelos HB, Azevedo RS, Casseb SM, Nunes-Neto JP, Chiang JO, Cantuária PC, Segura MN, Martins LC, Monteiro HA, Rodrigues SG, Nunes MR, Vasconcelos PF (2009) Oropouche fever epidemic in Northern Brazil: epidemiology and molecular characterization of isolates. J Clin Virol 44:129–133

    Article  PubMed  CAS  Google Scholar 

  45. Vasconcelos PFC, Da Rosa JF, Da Rosa AP, Degallier N, Pinheiro FP, Sá Filho GC (1991) Epidemiology of encephalitis caused by arbovirus in the Brazilian Amazonia. Rev Inst Med Trop Sao Paulo 33:465–476

    Article  PubMed  CAS  Google Scholar 

  46. Vasconcelos PFC, Travassos da Rosa APA, Pinheiro FP, Shope RE, Travassos da Rosa J F, Rodrigues SG, Degallier N, Travassos da Rosa ES (1998) Arboviruses pathogenic for man in Brazil. In: Travassos da Rosa APA, Travassos da Rosa JFS, Vasconcelos PFC (eds) An overview of arbovirology in Brazil and neighbouring countries. Instituto Evandro Chagas, Belém, Brazil, pp 72–99

  47. Weber F, Elliot RM (2002) Antigenic drift, antigenic shift and interferon antagonists: how bunyaviruses counteract the immune system. Virus Res 88:129–136

    Article  PubMed  CAS  Google Scholar 

  48. Yanase T, Kato T, Yamakawa M, Takayoshi K, Nakamura K, Kokuba T, Tsuda T (2006) Genetic characterization of Batai virus indicates a genomic reassortment between orthobunyaviruses in nature. Arch Virol 151:2253–2260

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors are grateful to colleagues from Virus Laboratory (ICB-UFMG) for their technical and scientific supports. This work was supported by research grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Coordenadoria de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), and Fundação de Amparo a Pesquisa do Estado de Minas Gerais (FAPEMIG). P.C.P. Ferreira, E.G. Kroon, and C.A. Bonjardim are CNPq researchers. We thank Dr. G.S. Trindade and Dr. Jaquelline G. Oliveira for helpful scientific discussions. We thank the Laboratory of Biodiversity and Molecular Evolution (ICB-UFMG), where sequences were determined.

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Correspondence to Paulo César Peregrino Ferreira.

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The S, M, and L nucleotide sequences reported here are available in GenBank under the accession numbers FJ859037, FJ859038, and FJ859039, respectively.

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de Brito Magalhães, C.L., Drumond, B.P., Novaes, R.F.V. et al. Identification of a phylogenetically distinct orthobunyavirus from group C. Arch Virol 156, 1173–1184 (2011). https://doi.org/10.1007/s00705-011-0976-1

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