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
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
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
Bishop DH (1985) The genetic basis for describing viruses as species. Intervirology 24:79–93
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
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
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
Calisher CH (1988) Evolutionary significance of the taxonomic data regarding bunyaviruses of the family Bunyaviridae. Intervirology 29:268–276
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
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
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
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
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
Eifan SA, Elliott RM (2009) Mutational analysis of the Bunyamwera orthobunyavirus nucleocapsid protein gene. J Virol 83:11307–11317
Elliott RM (1985) Identification of nonstructural proteins encoded by viruses of the Bunyamwera serogroup (family Bunyaviridae). Virology 143:119–126
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
Elliott RM (1997) Emerging viruses: the Bunyaviridae. Mol Med 3:572–577
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
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
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
Gentsch JR, Bishop DL (1979) M viral RNA segment of bunyaviruses codes for two glycoproteins, G1 and G2. J Virol 30:767–770
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
Gibbs CJ Jr , Bruckner EA, Schenker S (1964) A case of Apeu virus infection. Am J Trop Med Hyg 13:108–113
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
Holland J, Domingo E (1998) Origin and evolution of viruses. Virus Genes 16:13–21
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
Huang X, Madan A (1999) CAP3: A DNA sequence assembly program. Genome Res 9:868–877
Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
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
Martin DP, Williamson C, Posada D (2005) RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21:260–262
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
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
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
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
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
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstruction phylogenetic trees. Mol Biol Evol 4:406–425
Sall AA, Zanotto PM, Sene OK, Zeller HG (1999) Genetic reassortment of Rift valley fever virus in nature. J Virol 73:8196–8200
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
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
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
Soldan SS, González-Scarano F (2005) Emerging infectious diseases: the Bunyaviridae. J Neurovirol 11:412–423
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
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
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
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
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
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
Weber F, Elliot RM (2002) Antigenic drift, antigenic shift and interferon antagonists: how bunyaviruses counteract the immune system. Virus Res 88:129–136
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
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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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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DOI: https://doi.org/10.1007/s00705-011-0976-1


