1887

Abstract

The genus includes a range of mosquito-specific viruses in addition to well-known medically important arboviruses. Isolation and comprehensive genomic analyses of viruses in mosquitoes collected in Bolivia resulted in the identification of three novel flavivirus species. Psorophora flavivirus (PSFV) was isolated from . The coding sequence of the PSFV polyprotein shares 60 % identity with that of the -associated lineage II insect-specific flavivirus (ISF), Marisma virus. Isolated PSFV replicates in both - and -derived cells, but not in mammalian Vero or BHK-21 cell lines. Two other flaviviruses, Ochlerotatus scapularis flavivirus (OSFV) and Mansonia flavivirus (MAFV), which were identified from and respectively, group with the classical lineage I ISFs. The protein coding sequences of these viruses share only 60 and 40 % identity with the most closely related of known lineage I ISFs, including Xishuangbanna aedes flavivirus and Sabethes flavivirus, respectively. Phylogenetic analysis suggests that MAFV is clearly distinct from the groups of the current known -associated lineage I ISFs. Interestingly, the predicted amino acid sequence of the MAFV capsid protein is approximately two times longer than that of any of the other known flaviviruses. Our results indicate that flaviviruses with distinct features can be found at the edge of the Bolivian Amazon basin at sites that are also home to dense populations of human-biting mosquitoes.

Funding
This study was supported by the:
  • JP16H06429, JP16K21723
    • Principle Award Recipient: HirofumiSawa
  • 20K21298, JP20wm0225018
    • Principle Award Recipient: OrbaYasuko
  • JP19H03112
    • Principle Award Recipient: KeitaMatsuno
  • JP16H05805
    • Principle Award Recipient: HirofumiSawa
  • 19H04843
    • Principle Award Recipient: SoNakagawa
  • JP16H06431
    • Principle Award Recipient: HirofumiSawa
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/content/journal/jgv/10.1099/jgv.0.001518
2021-01-08
2021-10-22
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References

  1. Saba Villarroel PM, Nurtop E, Pastorino B, Roca Y, Drexler JF et al. Zika virus epidemiology in Bolivia: a seroprevalence study in volunteer blood donors. PLoS Negl Trop Dis 2018; 12:e0006239 [View Article]
    [Google Scholar]
  2. Roca Y, Baronti C, Revollo RJ, Cook S, Loayza R et al. Molecular epidemiological analysis of dengue fever in Bolivia from 1998 to 2008. Vector Borne Zoonotic Dis 2009; 9:337–344 [View Article]
    [Google Scholar]
  3. Venegas EA, Aguilar PV, Cruz C, Guevara C, Kochel TJ et al. Ilheus virus infection in human, Bolivia. Emerg Infect Dis 2012; 18:516–518 [View Article]
    [Google Scholar]
  4. Laemmert HW, Hughes TP. The virus of Ilhéus encephalitis; isolation, serological specificity and transmission. J Immunol 1947; 55:61–67
    [Google Scholar]
  5. Turell MJ, O'Guinn ML, Jones JW, Sardelis MR, Dohm DJ et al. Isolation of viruses from mosquitoes (Diptera: Culicidae) collected in the Amazon Basin region of Peru. J Med Entomol 2005; 42:891–898 [View Article]
    [Google Scholar]
  6. Vieira CJdaSP, Andrade CD, Kubiszeski JR, Silva DJFda, Barreto ES, Vieira C, Silva D et al. Detection of Ilheus virus in mosquitoes from Southeast Amazon, Brazil. Trans R Soc Trop Med Hyg 2019; 113:424–427 [View Article]
    [Google Scholar]
  7. Organization PAH Geographic spred of Chkungunya in the Americas; 2018
  8. Stollar V, Thomas VL. An agent in the Aedes aegypti cell line (Peleg) which causes fusion of Aedes albopictus cells. Virology 1975; 64:367–377 [View Article]
    [Google Scholar]
  9. Patterson EI, Villinger J, Muthoni JN, Dobel-Ober L, Hughes GL. Exploiting insect-specific viruses as a novel strategy to control vector-borne disease. Curr Opin Insect Sci 2020; 39:50–56 [View Article]
    [Google Scholar]
  10. (WRBU) TWRBU Mosquito identification resources. http://wrbu.si.edu/aors/aors_Keys.html ; 2019
  11. Segura MNO. Atlas de Culicídeos na Amazônia brasileira: características específicas de insetos hematófagos da família Culicidae: Instituto evandro chagas; 2007
  12. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 1994; 3:294–299
    [Google Scholar]
  13. Patel P, Landt O, Kaiser M, Faye O, Koppe T et al. Development of one-step quantitative reverse transcription PCR for the rapid detection of flaviviruses. Virol J 2013; 10:58 [View Article]
    [Google Scholar]
  14. Orba Y, Hang'ombe BM, Mweene AS, Wada Y, Anindita PD et al. First isolation of West Nile virus in Zambia from mosquitoes. Transbound Emerg Dis 2018; 65:933–938 [View Article]
    [Google Scholar]
  15. Torii S, Orba Y, Hang’ombe BM, Mweene AS, Wada Y et al. Discovery of Mwinilunga alphavirus: a novel alphavirus in Culex mosquitoes in Zambia. Virus Res 2018; 250:31–36 [View Article]
    [Google Scholar]
  16. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 2012; 19:455–477 [View Article]
    [Google Scholar]
  17. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA et al. Full-Length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 2011; 29:644–652 [View Article]
    [Google Scholar]
  18. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article]
    [Google Scholar]
  19. Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 2009; 25:1972–1973 [View Article]
    [Google Scholar]
  20. Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol 2008; 25:1307–1320 [View Article][PubMed]
    [Google Scholar]
  21. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 2011; 27:1164–1165 [View Article]
    [Google Scholar]
  22. Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 2019; 35:4453–4455 [View Article]
    [Google Scholar]
  23. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23:2947–2948 [View Article]
    [Google Scholar]
  24. Kumar S, Stecher G, Tamura K. mega7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 2016; 33:1870–1874 [View Article]
    [Google Scholar]
  25. Almagro Armenteros JJ, Tsirigos KD, Sønderby CK, Petersen TN, Winther O et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol 2019; 37:420–423 [View Article]
    [Google Scholar]
  26. Duckert P, Brunak S, Blom N. Prediction of proprotein convertase cleavage sites. Protein Eng Des Sel 2004; 17:107–112 [View Article]
    [Google Scholar]
  27. Möller S, Croning MD, Apweiler R. Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 2001; 17:646–653 [View Article]
    [Google Scholar]
  28. Hirokawa T, Boon-Chieng S, Mitaku S. SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 1998; 14:378–379 [View Article]
    [Google Scholar]
  29. Buchan DWA, Jones DT. The PSIPRED protein analysis workbench: 20 years on. Nucleic Acids Res 2019; 47:W402–W407 [View Article]
    [Google Scholar]
  30. Jones DT. Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 1999; 292:195–202 [View Article]
    [Google Scholar]
  31. Jones DT, Cozzetto D. DISOPRED3: precise disordered region predictions with annotated protein-binding activity. Bioinformatics 2015; 31:857–863 [View Article]
    [Google Scholar]
  32. Clark DC, Lobigs M, Lee E, Howard MJ, Clark K et al. In situ reactions of monoclonal antibodies with a viable mutant of Murray Valley encephalitis virus reveal an absence of dimeric NS1 protein. J Gen Virol 2007; 88:1175–1183 [View Article]
    [Google Scholar]
  33. Takhampunya R, Kim HC, Tippayachai B, Lee DK, Lee WJ et al. Distribution and mosquito hosts of Chaoyang virus, a newly reported flavivirus from the Republic of Korea, 2008–2011. J Med Entomol 2014; 51:464–474 [View Article]
    [Google Scholar]
  34. Huhtamo E, Putkuri N, Kurkela S, Manni T, Vaheri A et al. Characterization of a novel flavivirus from mosquitoes in northern Europe that is related to mosquito-borne flaviviruses of the tropics. J Virol 2009; 83:9532–9540 [View Article]
    [Google Scholar]
  35. Vázquez A, Sánchez-Seco MP, Palacios G, Molero F, Reyes N et al. Novel flaviviruses detected in different species of mosquitoes in Spain. Vector Borne Zoonotic Dis 2012; 12:223–229 [View Article]
    [Google Scholar]
  36. Huhtamo E, Cook S, Moureau G, Uzcátegui NY, Sironen T et al. Novel flaviviruses from mosquitoes: Mosquito-specific evolutionary lineages within the phylogenetic group of mosquito-borne flaviviruses. Virology 2014; 464-465:320–329 [View Article]
    [Google Scholar]
  37. Korkusol A, Takhampunya R, Hang J, Jarman RG, Tippayachai B et al. A novel flavivirus detected in two Aedes spp. collected near the demilitarized zone of the Republic of Korea. J Gen Virol 2017; 98:1122–1131 [View Article]
    [Google Scholar]
  38. Harrison JJ, Hobson-Peters J, Colmant AMG, Koh J, Newton ND et al. Antigenic characterization of new lineage II insect-specific flaviviruses in Australian mosquitoes and identification of host restriction factors. mSphere 2020; 5: [View Article]
    [Google Scholar]
  39. Colmant AMG, Hobson-Peters J, Bielefeldt-Ohmann H, van den Hurk AF, Hall-Mendelin S. A new clade of insect-specific flaviviruses from Australian. mSphere 2017; 2:
    [Google Scholar]
  40. Zhang X, Guo X, Fan H, Zhao Q, Zuo S et al. Complete genome sequence of Menghai flavivirus, a novel insect-specific flavivirus from China. Arch Virol 2017; 162:1435–1439 [View Article]
    [Google Scholar]
  41. Fan H, Zhao Q, Guo X, Sun Q, Zuo S et al. Complete genome sequence of Xishuangbanna flavivirus, a novel mosquito-specific flavivirus from China. Arch Virol 2016; 161:1723–1727 [View Article]
    [Google Scholar]
  42. McLean BJ, Hobson-Peters J, Webb CE, Watterson D, Prow NA et al. A novel insect-specific flavivirus replicates only in Aedes-derived cells and persists at high prevalence in wild Aedes vigilax populations in Sydney, Australia. Virology 2015; 486:272–283 [View Article]
    [Google Scholar]
  43. Weaver SC, Reisen WK. Present and future arboviral threats. Antiviral Res 2010; 85:328–345 [View Article]
    [Google Scholar]
  44. Ryan SJ, Carlson CJ, Mordecai EA, Johnson LR. Global expansion and redistribution of Aedes-borne virus transmission risk with climate change. PLoS Negl Trop Dis 2019; 13:e0007213 [View Article]
    [Google Scholar]
  45. Alencar J, Pacheco JB, Dos Santos Silva J, Silva SOF, Guimarães Anthony Érico. Influence of climatic factors on Psorophora (Janthinosoma) Albigenu in Pantanal landscape, Mato Grosso state, Brazil. J Am Mosq Control Assoc 2018; 34:177–181 [View Article][PubMed]
    [Google Scholar]
  46. Turell MJ, Jones JW, Sardelis MR, Dohm DJ, Coleman RE et al. Vector competence of Peruvian mosquitoes (Diptera: Culicidae) for epizootic and enzootic strains of Venezuelan equine encephalomyelitis virus. J Med Entomol 2000; 37:835–839 [View Article]
    [Google Scholar]
  47. Groot H, Morales A, Vidales H. Virus isolations from forest mosquitoes in San Vicente de Chucuri, Colombia. Am J Trop Med Hyg 1961; 10:397–402 [View Article]
    [Google Scholar]
  48. Serra OP, Cardoso BF, Ribeiro AL, Santos FA, Slhessarenko RD. Mayaro virus and dengue virus 1 and 4 natural infection in culicids from Cuiabá, state of Mato Grosso, Brazil. Mem Inst Oswaldo Cruz 2016; 111:20–29 [View Article]
    [Google Scholar]
  49. Mucci LF, Júnior RP, de Paula MB, Scandar SA, Pacchioni ML et al. Feeding habits of mosquitoes (Diptera: Culicidae) in an area of sylvatic transmission of yellow fever in the state of São Paulo, Brazil. J Venom Anim Toxins Incl Trop Dis 2015; 21:6 [View Article]
    [Google Scholar]
  50. Öhlund P, Lundén H, Blomström AL. Insect-specific virus evolution and potential effects on vector competence. Virus Genes 2019; 55:127–137 [View Article]
    [Google Scholar]
  51. Hobson-Peters J, Harrison JJ, Watterson D, Hazlewood JE, Vet LJ et al. A recombinant platform for flavivirus vaccines and diagnostics using chimeras of a new insect-specific virus. Sci Transl Med 2019; 11:eaax7888 [View Article]
    [Google Scholar]
  52. Tan TY, Fibriansah G, Kostyuchenko VA, Ng T-S, Lim X-X et al. Capsid protein structure in Zika virus reveals the flavivirus assembly process. Nat Commun 2020; 11:895 [View Article]
    [Google Scholar]
  53. Dokland T, Walsh M, Mackenzie JM, Khromykh AA, KH E. West Nile virus core protein; tetramer structure and ribbon formation. Structure 2004; 12:1157–1163
    [Google Scholar]
  54. Oliveira ERA, Mohana-Borges R, de Alencastro RB, Horta BAC. The flavivirus capsid protein: structure, function and perspectives towards drug design. Virus Res 2017; 227:115–123 [View Article]
    [Google Scholar]
  55. Sotcheff S, Routh A. Understanding flavivirus capsid protein functions: the tip of the iceberg. Pathogens 2020; 9:42 [View Article]
    [Google Scholar]
  56. Jones CT, Ma L, Burgner JW, Groesch TD, Post CB et al. Flavivirus capsid is a dimeric alpha-helical protein. J Virol 2003; 77:7143–7149 [View Article]
    [Google Scholar]
  57. Ma L, Jones CT, Groesch TD, Kuhn RJ, Post CB. Solution structure of dengue virus capsid protein reveals another fold. Proc Natl Acad Sci U S A 2004; 101:3414–3419 [View Article]
    [Google Scholar]
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