Abstract
We describe the isolation of a novel flavivirus, isolated from a pool of mosquitoes identified as Culex (Culex) chidesteri collected in 2010 in the Pantanal region of west-central Brazil. The virus is herein designated Nhumirim virus (NHUV) after the name of the ranch from which the mosquito pool was collected. Flavivirus RNA was detected by real-time RT-PCR of homogenized mosquitoes and from the corresponding C6/36 culture supernatant. Based on full-genome sequencing, the virus isolate was genetically distinct from but most closely related to Barkedji virus (BJV), a newly described flavivirus from Senegal. Phylogenetic analysis demonstrated that NHUV grouped with mosquito-borne flaviviruses forming a clade with BJV. This clade may be genetically intermediate between the Culex-borne flaviviruses amplified by birds and the insect-only flaviviruses.
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References
King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (2012) Virus taxonomy: ninth report of the international committee on taxonomy of viruses. Elsevier Academic Press, San Diego
Nogueira RMR, de Araújo JM, Schatzmayr HG (2007) Dengue viruses in Brazil, 1986–2006. Rev Panam Salud Publica 22(5):358–363
Câmara FP, de Carvalho LM, Gomes AL (2013) Demographic profile of sylvatic yellow fever (SYF) in Brazil from 1973 to 2008. Trans R Soc Trop Med Hyg 107(5):324–327
Lopes OS, Coimbra TLM, Sacchetta LA, Calisher CH (1978) Emergence of a new arbovirus disease in Brazil: isolation and characterization of the etiologic agent, Rocio virus. Am J Epidemiol 107:444–449
Mondini A, Cardeal IL, Lázaro E, Nunes SH, Moreira CC, Rahal P, Maia IL, Franco C, Góngora DV, Góngora-Rubio F, Cabrera EM, Figueiredo LT, da Fonseca FG, Bronzoni RV, Chiaravalloti-Neto F, Nogueira ML (2007) Saint Louis encephalitis virus, Brazil. Emerg Infect Dis 13(1):176–178
Batista WC, Tavares GSB, Vieira DS, Honda ER, Pereira SS, Tada MS (2011) Notification of the first isolation of Cacipacore virus in a human in the State of Rondônia, Brazil. Revista da Sociedade Brasileira de Medicina Tropical 44(4):528–530
Nassar ES, Coimbra TLM, Rocco IM, Pereira LE, Ferreira IB, de Souza LT, de Souza DM, Ueda-Ito M, Moura JP, Bergo RC (1997) Human disease caused by an arbovirus closely related to Ilheus virus: report of five cases. Intervirology 40:247–252
Rodrigues SG, Azevedo RSS, Martins LC, Nunes MRT, Araújo GCB, Monteiro HAO, Segura MNO, Travassos da Rosa ES, Travassos da Rosa JFS, Vasconcelos HB, Vasconcelos PFC (2004) Estudo eco-epidemiológico na área do projeto salobo, Marabá-Pará: Isolamento e identificação de amostras de arbovírus. III Simpósio Internacional sobre arbovírus dos trópicos e febres hemorrágicas. 30 de novembro a 04 de dezembro de 2004, Belém, Pará
Machado DC, Mondini A, dos Santos Santana V, Yonamine PT, Chiaravalloti Neto F, Zanotto PM, Nogueira ML (2012) First identification of Culex flavivirus (Flaviviridae) in Brazil. Intervirology 55(6):475–483
Maruyama SR, Castro-Jorge LA, Ribeiro JMC, Gardinassi LG, Garcia GR, Brandão LG, Rodrigues AR, Okada MI, Abrão EP, Ferreira BR, Fonseca BAL, Miranda-Santos IKF (2014) Characterisation of divergent flavivirus NS3 and NS5 protein sequences detected in Rhipicephalus microplus ticks from Brazil. Mem Inst Oswaldo Cruz 109(1):38–50
Pauvolid-Corrêa A, Morales MA, Levis S, Figueiredo LT, Couto-Lima D, Campos Z, Nogueira MF, da Silva EE, Nogueira RM, Schatzmayr HG (2011) Neutralising antibodies for West Nile virus in horses from Brazilian Pantanal. Mem Inst Oswaldo Cruz 106(4):467–474
Pauvolid-Corrêa A, Campos Z, Juliano R, Velez J, Nogueira RMR, Komar N (2014) Serological evidence of widespread circulation of West Nile virus and other flaviviruses in Pantanal equines, Brazil. PLoS Negl Trop Dis 8(2):e2706
Pauvolid-Corrêa A, Kenney JL, Couto-Lima D, Campos ZM, Schatzmayr HG, Nogueira RM, Brault AC, Komar N (2013) Ilheus virus isolation in the Pantanal, west-central Brazil. PLoS Negl Trop Dis 7(7):e2318
Calisher CH, Karabatsos N, Dalrymple JM, Shope RE, Porterfield JS, Westaway EG, Brandt WE (1989) Antigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera. J Gen Virol 70(1):37–43
Pauvolid-Corrêa A, Tavares FN, Alencar J, Silva J dos S, Murta M, Serra-Freire NM, Pellegrin AO, Gil-Santana H, Guimarães AE, Silva EE (2010) Preliminary investigation of Culicidae species in South Pantanal, Brazil and their potential importance in arbovirus transmission. Rev Inst Med Trop Sao Paulo 52(1):17–24
Crabtree MB, Nga PT, Miller BR (2009) Isolation and characterization of a new mosquito flavivirus, Quang Binh virus, from Vietnam. Arch Virol 154:857–860
Cook S, Moureau G, Harbach RE, Mukwaya L, Goodger K, Ssenfuka F, Gould E, Holmes EC, de Lamballerie X (2009) Isolation of a novel species of flavivirus and a new strain of Culex flavivirus (Flaviviridae) from a natural mosquito population in Uganda. J Gen Virol 90:2669–2678
Junglen S, Kopp A, Kurth A, Pauli G, Ellerbrok H, Leendertz FH (2009) A new flavivirus and a new vector: characterization of a novel flavivirus isolated from Uranotaenia mosquitoes from a tropical rain forest. J Virol 83:4462–4468
Hobson-Peters J, Yam AW, Lu JW, Setoh YX, May FJ, Kurucz N, Walsh S, Prow NA, Davis SS, Weir R, Melville L, Hunt N, Webb RI, Blitvich BJ, Whelan P, Hall RA (2013) A new insect-specific flavivirus from northern Australia suppresses replication of West Nile virus and Murray Valley encephalitis virus in co-infected mosquito cells. PLoS One 8(2):e56534
De La Fuente J, Estrada-Pena A, Venzal JM, Kocan KM, Sonenshine DE (2008) Overview: ticks as vectors of pathogens that cause disease in humans and animals. Front Biosci 13:6938–6946
Aragão HB, Fonseca F (1961) Notas de Ixodologia. VIII Lista e chave para os representantes da fauna ixodológica brasileira. Mem Inst Oswaldo Cruz 59(2):115–151
Beaty BJ, Calisher CH, Shope RE (1995) Arboviruses. In: Lennette EH, Lennette DA, Lennette ET (eds) Diagnostic procedures for viral, rickettsial and chlamydial infections, 7th edn. American Public Health Association, Washington DC, pp 189–212
Moureau G, Temmam S, Gonzalez JP, Charrel RN, Grard G, de Lamballerie X (2007) A real-time RT-PCR method for the universal detection and identification of flaviviruses. Vector Borne Zoonotic Dis 7(4):467–477
Kuno G, Chang GJ, Tsuchiya KR, Karabatsos N, Cropp CB (1998) Phylogeny of the genus Flavivirus. J Virol 72(1):73–83
Langevin SA, Bent ZW, Solberg OD, Curtis DJ, Lane PD, Williams KP, Schoeniger JS, Sinha A, Lane TW, Branda SS (2013) Peregrine: a rapid and unbiased method to produce strand-specific RNA-Seq libraries from small quantities of starting material. RNA biology 10(4):502–515
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17.1:10–12
Magoc T, Salzberg S (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 29(7):644–652
Langmead B, Salzberg S (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359
Ondov BD, Bergman NH, Phillippy AM (2011) Interactive metagenomic visualization in a Web browser. BMC Bioinform 12(1):385
Vasconcelos PFC, da Rosa APA T, Pinheiro FP, da Rosa JFST (2005) Arboviroses. In: Focaccia R, Veronesi R (ed) Tratado de infectologia, vol 1. Atheneu, São Paulo, pp 289–302
Figueiredo LT, Badra SJ, Pereira LE, Szabó MP (1999) Report on ticks collected in the Southeast and Mid-West regions of Brazil: analyzing the potential transmission of tick-borne pathogens to man. Rev Soc Bras Med Trop 32(6):613–619
Gaunt MW, Sall AA, de Lamballerie X, Falconar AK, Dzhivanian TI, Gould EA (2001) Phylogenetic relationships of flaviviruses correlate with their epidemiology, disease association and biogeography. J Gen Virol 82(8):1867–1876
de Sousa Lopes O, Sacchetta LA, Francy DB, Jakob W, Calisher CH (1981) Emergence of a new arbovirus disease in Brazil. III. Isolation of Rocio virus from Psorophora ferox (Humboldt, 1819). Am J Epidemiol 113:122–125
Sousa AM (2006) Manifestações neurológicas em surto de dengue no estado de Rondônia. Dissertation. Universidade Federal do Estado do Rio de Janeiro
Morales-Betoulle ME, Monzón Pineda ML, Sosa SM, Panella N, López MR, Cordón-Rosales C, Komar N, Powers A, Johnson BW (2008) Culex flavivirus isolates from mosquitoes in Guatemala. J Med Entomol 45(6):1187–1190
Kim DY, Guzman H, Bueno R Jr, Dennett JA, Auguste AJ, Carrington CV, Popov VL, Weaver SC, Beasley DW, Tesh RB (2009) Characterization of Culex flavivirus (Flaviviridae) strains isolated from mosquitoes in the United States and Trinidad. Virology 386(1):154–159
Huanyu W, Haiyan W, Shihong F, Guifang L, Hong L, Xiaoyan G, Lizhi S, Rayner S, Aiqiang X, Guodong L (2012) Isolation and identification of a distinct strain of Culex flavivirus from mosquitoes collected in Mainland China. Virol J 9:73
Parreira R, Cook S, Lopes Â, de Matos AP, de Almeida AP, Piedade J, Esteves A (2012) Genetic characterization of an insect-specific flavivirus isolated from Culex theileri mosquitoes collected in southern Portugal. Virus Res 167(2):152–161
Evangelista J, Cruz C, Guevara C, Astete H, Carey C, Kochel TJ, Morrison AC, Williams M, Halsey ES, Forshey BM (2013) Characterization of a novel flavivirus isolated from Culex (Melanoconion) ocossa mosquitoes from Iquitos, Peru. J Gen Virol 94(Pt 6):1266–1272
Kolodziejek J, Pachler K, Bin H, Mendelson E, Shulman L, Orshan L (2011) Nowotny N (2013) Barkedji virus, a novel mosquito-borne flavivirus identified in Culex perexiguus mosquitoes, Israel. J Gen Virol 94(Pt 11):2449–2457
Lane J (1953) Neotropical Culicidae. Editora Universidade de São Paulo, São Paulo
Consoli RAGB, Lourenc¸o-de-Oliveira R (1994) Principais mosquitos de importância sanitária no Brasil. Editora Fiocruz, Rio de Janeiro
Lourenço-de-Oliveira R, Heyden R (1986) Some aspects of the ecology of the mosquitoes (Diptera: Culicidade) of an area of plains (grange Calabria) in Jacarepaguá, Rio de Janeiro: IV. Food preferences of hosts and domiciliary frequency. Mem Inst Oswaldo Cruz 81(1):15–27
Almirón WR, Brewer MM (1995) Host preference of Culicidae (Diptera) collected in central Argentina. Rev Saude Publica 29(2):108–114
Forattini OP, de Castro Gomes A, Galati EA, Rabello EX, Iversson LB (1978) Ecological studies on Culicidae mosquitoes in the Serra do Mar system, Brazil. 2. Observations in domiciliary environments. Rev Saude Publica 12((4):476–495
Acknowledgements
Special thanks to Zilca Campos from Embrapa Pantanal for her important contribution to this work. We thank Kristy Burkalther, Janae Stovall, Karen Burroughs and Robert Lanciotti from CDC, who provided laboratory assistance. We thank Thierry Tomich, Marcia Furlan, Marcos Tadeu and all staff from Embrapa Pantanal. Special thanks to Hélcio Reinaldo Gil-Santana from Diptera Laboratory of FIOCRUZ, and Luiz Pellegrin of Geoprocessing Laboratory of Embrapa Pantanal. Financial support: ASM, CNPq, CAPES, Fulbright, CDC, FIOCRUZ, FAPERJ.
The authors declare that they have no conflict of interest.
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Alex Pauvolid-Correˆa was a fulbright doctorate student at CDC.
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Pauvolid-Corrêa, A., Solberg, O., Couto-Lima, D. et al. Nhumirim virus, a novel flavivirus isolated from mosquitoes from the Pantanal, Brazil. Arch Virol 160, 21–27 (2015). https://doi.org/10.1007/s00705-014-2219-8
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DOI: https://doi.org/10.1007/s00705-014-2219-8