Dietzgen RG, Calisher CH, Kurath G, Kuzman IV, Rodriguez LL, Stone DM, Tesh RB, Tordo N, Walker PJ, Wetzel T, Whitfield AE, 2012. Rhabdoviridae. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ, eds. Virus Taxonomy, Ninth Report of the International Committee on Taxonomy of Viruses. San Diego, CA: Elsevier, 654–681.
Kuzmin IV, Novella IS, Dietzgen RG, Padhi A, Rupprecht CE, 2009. The rhabdoviruses: biodiversity, phylogenetics, and evolution. Infect Genet Evol 9: 541–553.
Kuzmin IV, Walker PJ, 2016. Vector-borne rhabdoviruses. Vasilakis N, Gubler DJ, eds. Arboviruses: Molecular Biology, Evolution and Control. Norfolk, VA: Caister Academic Press, 389.
Longdon B, Obbard DJ, Jiggins FM, 2010. Sigma viruses from three species of Drosophila form a major new clade in the rhabdovirus phylogeny. Proc Biol Sci 277: 35–44.
Li CX, Shi M, Tian JH, Lin XD, Kang YJ, Chen LJ, Qin XC, Xu J, Holmes EC, Zhang YZ, 2015. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife 4: e05378.
Vasilakis N, Castro-Llanos F, Widen SG, Aguilar PV, Guzman H, Guevara C, Fernandez R, Auguste AJ, Wood TG, Popov V, Mundal K, Ghedin E, Kochel TJ, Holmes EC, Walker PJ, Tesh RB, 2014. Arboretum and Puerto Almendras viruses: two novel rhabdoviruses isolated from mosquitoes in Peru. J Gen Virol 95: 787–792.
Vasilakis N, Forrester NL, Palacios G, Nasar F, Savji N, Rossi SL, Guzman H, Wood TG, Popov V, Gorchakov R, Gonzalez AV, Haddow AD, Watts DM, da Rosa AP, Weaver SC, Lipkin WI, Tesh RB, 2013. Negevirus: a proposed new taxon of insect-specific viruses with wide geographic distribution. J Virol 87: 2475–2488.
Lohse M, Bolger AM, Nagel A, Fernie AR, Lunn JE, Stitt M, Usadel B, 2012. RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Res 40: W622–W627.
Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, Birol I, 2009. ABySS: a parallel assembler for short read sequence data. Genome Res 19: 1117–1123.
Langmead B, Salzberg SL, 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359.
Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP, 2011. Integrative genomics viewer. Nat Biotechnol 29: 24–26.
Edgar RC, 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725–2729.
Talavera G, Castresana J, 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56: 564–577.
Vasilakis N, Widen S, Mayer SV, Seymour R, Wood TG, Popov V, Guzman H, Travassos da Rosa AP, Ghedin E, Holmes EC, Walker PJ, Tesh RB, 2013. Niakha virus: a novel member of the family Rhabdoviridae isolated from phlebotomine sandflies in Senegal. Virology 444: 80–89.
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ, 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.
Green TJ, Zhang X, Wertz GW, Luo M, 2006. Structure of the vesicular stomatitis virus nucleoprotein-RNA complex. Science 313: 357–360.
Luo M, Green TJ, Zhang X, Tsao J, Qiu S, 2007. Conserved characteristics of the rhabdovirus nucleoprotein. Virus Res 129: 246–251.
Ribeiro EA, Favier A, Gerard FCA, Leyrat C, Brutscher B, Blondel D, Ruigrok RWH, Blackledge M, Jamin M, 2008. Solution structure of the C-terminal nucleoprotein-RNA binding domain of the vesicular stomatitis virus phosphoprotein. J Mol Biol 382: 525–538.
Karlin D, Ferron F, Canard B, Longhi S, 2003. Structural disorder and modular organization in Paramyxovirinae N and P. J Gen Virol 84: 3239–3252.
Walker PJ, Firth C, Widen SG, Blasdell KR, Guzman H, Wood TG, Paradkar PN, Holmes EC, Tesh RB, Vasilakis N, 2015. Evolution of genome size and complexity in the Rhabdoviridae. PLoS Pathog 11: e1004664.
Spiropoulou CF, Nichol ST, 1993. A small highly basic protein is encoded in overlapping frame within the P gene of vesicular stomatitis virus. J Virol 67: 3103–3110.
Peluso RW, Richardson JC, Talon J, Lock M, 1996. Identification of a set of proteins (C′ and C) encoded by the bicistronic P gene of the Indiana serotype of vesicular stomatitis virus and analysis of their effect on transcription by the viral RNA polymerase. Virology 218: 335–342.
Gubala AJ, Proll DF, Barnard RT, Cowled CJ, Crameri SG, Hyatt AD, Boyle DB, 2008. Genomic characterisation of Wongabel virus reveals novel genes within the Rhabdoviridae. Virology 376: 13–23.
Walker PJ, Kongsuwan K, 1999. Deduced structural model for animal rhabdovirus glycoproteins. J Gen Virol 80: 1211–1220.
Roche S, Bressanelli S, Rey FA, Gaudin Y, 2006. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313: 187–191.
Nieva JL, Madan V, Carrasco L, 2012. Viroporins: structure and biological functions. Nat Rev Microbiol 10: 563–574.
Walker PJ, Dietzgen RG, Joubert DA, Blasdell KR, 2011. Rhabdovirus accessory genes. Virus Res 162: 110–125.
Joubert DA, Blasdell KR, Audsley MD, Trinidad L, Monaghan P, Dave KA, Lieu K, Amos-Ritchie R, Jans DA, Moseley GW, Gorman JJ, Walker PJ, 2014. Bovine ephemeral fever rhabdovirus a1 protein has viroporin-like properties and binds importin b1 and importin 7. J Virol 88: 1591–1603.
Bodewes R, Ruiz-Gonzalez A, Schurch AC, Osterhaus AD, Smits SL, 2014. Novel divergent rhabdovirus in feces of red fox, Spain. Emerg Infect Dis 20: 2172–2174.
Bolling BG, Weaver SC, Tesh RB, Vasilakis N, 2015. Insect-specific virus discovery: significance for the arbovirus community. Viruses 7: 4911–4928.
Shi M, Lin XD, Vasilakis N, Tian JH, Li CX, Chen LJ, Eastwood G, Diao XN, Chen MH, Chen X, Qin XC, Widen SG, Wood TG, Tesh RB, Xu J, Holmes EC, Zhang YZ, 2015. Divergent viruses discovered in arthropods and vertebrates revise the evolutionary history of the Flaviviridae and related viruses. J Virol 90: 659–669.
Kerschner JH, Calisher CH, Vorndam AV, Francy DB, 1986. Identification and characterization of Bahia Grande, Reed Ranch and Muir Springs viruses, related members of the family Rhabdoviridae with widespread distribution in the United States. J Gen Virol 67: 1081–1089.
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The Rhabdoviridae is a diverse family of negative-sense single-stranded RNA viruses, many of which infect vertebrate hosts and are transmitted by hematophagous arthropods. Others appear to be arthropod specific, circulating only within arthropod populations. Herein, we report the isolation and characterization of three novel viruses from mosquitoes collected from the Americas. Coot Bay virus was isolated from Anopheles quadrimaculatus mosquitoes collected in the Everglades National Park, Florida; Rio Chico virus was isolated from Anopheles triannulatus mosquitoes collected in Panama; and Balsa virus was isolated from two pools of Culex erraticus mosquitoes collected in Colombia. Sequence analysis indicated that the viruses share a similar genome organization to Arboretum virus and Puerto Almendras virus that had previously been isolated from mosquitoes collected in Peru. Each genome features the five canonical rhabdovirus structural protein genes as well as a gene encoding a class 1A viroporin-like protein (U1) located between the G and L genes (3′-N-P-M-G-U1-L-5′). Phylogenetic analysis of complete L protein sequences indicated that all five viruses cluster in a unique clade that is relatively deeply rooted in the ancestry of animal rhabdoviruses. The failure of all viruses in this clade to grow in newborn mice or vertebrate cells in culture suggests that they may be poorly adapted to replication in vertebrates.
Financial support: This work was supported in part by contract HHSN272201000040I/HHSN2700004/D4 from the National Institutes of Health. Laboratory work in the United States was funded in part by NIH grant R24 AI120942. Maria Angelica Contreras was supported by Programa de Doctorados Nacionales–Colciencias (Convacatoria 567) PhD Fellowship from Colombia. Gillian Eastwood, and collections in Panama, were supported by a Robert E. Shope International Fellowship from the American Society of Tropical Medicine and Hygiene in 2012; kindly assisted by Jose R. Loaiza, and the Smithsonian Tropical Research Institute. We also acknowledge support from Yale Institute for Biospheric Studies, Center for Ecoepidemiology, and the U.S. National Park Service (Collecting Permit no. EVER-2013-SCI-0032). The field collection in Colombia was funded in part by Colciencias grant 111549326198.
Authors' addresses: Maria Angelica Contreras, Programa de Estudio y Control de Enfermedades Tropicales (PECET), Sede de Investigacion Universitaria (SIU), Universidad de Antioquia, Medellin, CO, and Grupo de Investigacion en Sistematica Molecular (GSM), Facultad de Ciencias, Universidad Nacional de Colombia, Medellin, CO, E-mail: maria.contreras@pecet-colombia.org. Gillian Eastwood, Griffin Arbovirus Laboratory, Wadsworth Center, New York State Department of Health, Slingerlands, NY, E-mail: gill2g@hotmail.com. Hilda Guzman, Department of Pathology, University of Texas Medical Branch, Houston, TX, E-mail: hguzman@utmb.edu. Vsevolod Popov and Robert B. Tesh, Department of Pathology, Center for Biodefense and Emerging Infectious Diseases, Center for Tropical Diseases, Institute for Human Infections and Immunity, University of Texas Medical Branch, Galveston, TX, E-mails: vpopov@utmb.edu and rtesh@utmb.edu. Chelsea Savit, Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT, E-mail: savvysavit@gmail.com. Sandra Uribe, Sede de Investigacion Universitaria (SIU), Universidad de Antioquia, Medellin, CO, E-mail: siuribesoto@gmail.com. Laura D. Kramer, Zoonotic Diseases, New York State Department of Health, Slingerlands, NY, and Griffin Arbovirus Laboratory, Wadsworth Center, New York State Department of Health, Albany, NY, E-mail: laura.kramer@health.ny.gov. Thomas G. Wood and Steven G. Widen, Department of Biochemistry and Molecular Biology, University of Texas Medical Branch, Galveston, TX, E-mails: tgwood@utmb.edu and sgwiden@utmb.edu. Durland Fish, Epidemiology and Public Health, Yale University, New Haven, CT, E-mail: durland.fish@yale.edu. Nikos Vasilakis, Department of Pathology, University of Texas Medical Branch, Galveston, TX, and Center for Biodefense and Emerging Infectious Diseases, University of Texas Medical Branch, Galveston, TX, E-mail: nivasila@utmb.edu. Peter J. Walker, CSIRO Health and Biosecurity, Australian Animal Health Laboratory, Geelong, Australia, and School of Biological Sciences, University of Queensland, St Lucia, Australia, E-mail: peter.walker@uq.edu.au.
Dietzgen RG, Calisher CH, Kurath G, Kuzman IV, Rodriguez LL, Stone DM, Tesh RB, Tordo N, Walker PJ, Wetzel T, Whitfield AE, 2012. Rhabdoviridae. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ, eds. Virus Taxonomy, Ninth Report of the International Committee on Taxonomy of Viruses. San Diego, CA: Elsevier, 654–681.
Kuzmin IV, Novella IS, Dietzgen RG, Padhi A, Rupprecht CE, 2009. The rhabdoviruses: biodiversity, phylogenetics, and evolution. Infect Genet Evol 9: 541–553.
Kuzmin IV, Walker PJ, 2016. Vector-borne rhabdoviruses. Vasilakis N, Gubler DJ, eds. Arboviruses: Molecular Biology, Evolution and Control. Norfolk, VA: Caister Academic Press, 389.
Longdon B, Obbard DJ, Jiggins FM, 2010. Sigma viruses from three species of Drosophila form a major new clade in the rhabdovirus phylogeny. Proc Biol Sci 277: 35–44.
Li CX, Shi M, Tian JH, Lin XD, Kang YJ, Chen LJ, Qin XC, Xu J, Holmes EC, Zhang YZ, 2015. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife 4: e05378.
Vasilakis N, Castro-Llanos F, Widen SG, Aguilar PV, Guzman H, Guevara C, Fernandez R, Auguste AJ, Wood TG, Popov V, Mundal K, Ghedin E, Kochel TJ, Holmes EC, Walker PJ, Tesh RB, 2014. Arboretum and Puerto Almendras viruses: two novel rhabdoviruses isolated from mosquitoes in Peru. J Gen Virol 95: 787–792.
Vasilakis N, Forrester NL, Palacios G, Nasar F, Savji N, Rossi SL, Guzman H, Wood TG, Popov V, Gorchakov R, Gonzalez AV, Haddow AD, Watts DM, da Rosa AP, Weaver SC, Lipkin WI, Tesh RB, 2013. Negevirus: a proposed new taxon of insect-specific viruses with wide geographic distribution. J Virol 87: 2475–2488.
Lohse M, Bolger AM, Nagel A, Fernie AR, Lunn JE, Stitt M, Usadel B, 2012. RobiNA: a user-friendly, integrated software solution for RNA-Seq-based transcriptomics. Nucleic Acids Res 40: W622–W627.
Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJ, Birol I, 2009. ABySS: a parallel assembler for short read sequence data. Genome Res 19: 1117–1123.
Langmead B, Salzberg SL, 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359.
Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP, 2011. Integrative genomics viewer. Nat Biotechnol 29: 24–26.
Edgar RC, 2004. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S, 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725–2729.
Talavera G, Castresana J, 2007. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 56: 564–577.
Vasilakis N, Widen S, Mayer SV, Seymour R, Wood TG, Popov V, Guzman H, Travassos da Rosa AP, Ghedin E, Holmes EC, Walker PJ, Tesh RB, 2013. Niakha virus: a novel member of the family Rhabdoviridae isolated from phlebotomine sandflies in Senegal. Virology 444: 80–89.
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ, 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.
Green TJ, Zhang X, Wertz GW, Luo M, 2006. Structure of the vesicular stomatitis virus nucleoprotein-RNA complex. Science 313: 357–360.
Luo M, Green TJ, Zhang X, Tsao J, Qiu S, 2007. Conserved characteristics of the rhabdovirus nucleoprotein. Virus Res 129: 246–251.
Ribeiro EA, Favier A, Gerard FCA, Leyrat C, Brutscher B, Blondel D, Ruigrok RWH, Blackledge M, Jamin M, 2008. Solution structure of the C-terminal nucleoprotein-RNA binding domain of the vesicular stomatitis virus phosphoprotein. J Mol Biol 382: 525–538.
Karlin D, Ferron F, Canard B, Longhi S, 2003. Structural disorder and modular organization in Paramyxovirinae N and P. J Gen Virol 84: 3239–3252.
Walker PJ, Firth C, Widen SG, Blasdell KR, Guzman H, Wood TG, Paradkar PN, Holmes EC, Tesh RB, Vasilakis N, 2015. Evolution of genome size and complexity in the Rhabdoviridae. PLoS Pathog 11: e1004664.
Spiropoulou CF, Nichol ST, 1993. A small highly basic protein is encoded in overlapping frame within the P gene of vesicular stomatitis virus. J Virol 67: 3103–3110.
Peluso RW, Richardson JC, Talon J, Lock M, 1996. Identification of a set of proteins (C′ and C) encoded by the bicistronic P gene of the Indiana serotype of vesicular stomatitis virus and analysis of their effect on transcription by the viral RNA polymerase. Virology 218: 335–342.
Gubala AJ, Proll DF, Barnard RT, Cowled CJ, Crameri SG, Hyatt AD, Boyle DB, 2008. Genomic characterisation of Wongabel virus reveals novel genes within the Rhabdoviridae. Virology 376: 13–23.
Walker PJ, Kongsuwan K, 1999. Deduced structural model for animal rhabdovirus glycoproteins. J Gen Virol 80: 1211–1220.
Roche S, Bressanelli S, Rey FA, Gaudin Y, 2006. Crystal structure of the low-pH form of the vesicular stomatitis virus glycoprotein G. Science 313: 187–191.
Nieva JL, Madan V, Carrasco L, 2012. Viroporins: structure and biological functions. Nat Rev Microbiol 10: 563–574.
Walker PJ, Dietzgen RG, Joubert DA, Blasdell KR, 2011. Rhabdovirus accessory genes. Virus Res 162: 110–125.
Joubert DA, Blasdell KR, Audsley MD, Trinidad L, Monaghan P, Dave KA, Lieu K, Amos-Ritchie R, Jans DA, Moseley GW, Gorman JJ, Walker PJ, 2014. Bovine ephemeral fever rhabdovirus a1 protein has viroporin-like properties and binds importin b1 and importin 7. J Virol 88: 1591–1603.
Bodewes R, Ruiz-Gonzalez A, Schurch AC, Osterhaus AD, Smits SL, 2014. Novel divergent rhabdovirus in feces of red fox, Spain. Emerg Infect Dis 20: 2172–2174.
Bolling BG, Weaver SC, Tesh RB, Vasilakis N, 2015. Insect-specific virus discovery: significance for the arbovirus community. Viruses 7: 4911–4928.
Shi M, Lin XD, Vasilakis N, Tian JH, Li CX, Chen LJ, Eastwood G, Diao XN, Chen MH, Chen X, Qin XC, Widen SG, Wood TG, Tesh RB, Xu J, Holmes EC, Zhang YZ, 2015. Divergent viruses discovered in arthropods and vertebrates revise the evolutionary history of the Flaviviridae and related viruses. J Virol 90: 659–669.
Kerschner JH, Calisher CH, Vorndam AV, Francy DB, 1986. Identification and characterization of Bahia Grande, Reed Ranch and Muir Springs viruses, related members of the family Rhabdoviridae with widespread distribution in the United States. J Gen Virol 67: 1081–1089.
Past two years | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 92 | 92 | 54 |
Full Text Views | 444 | 158 | 1 |
PDF Downloads | 178 | 48 | 0 |