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Volume 102, Issue 2

Comparative characterization of the reassortant Orthobunyavirus Ngari with putative parental viruses, Bunyamwera and Batai: characterization and stability Open Access

Abstract

Bunyamwera (BUNV), Batai (BATV) and Ngari (NRIV) are mosquito-borne viruses that are members of the genus in the order Bunyavirales. These three viruses are enveloped with single-stranded, negative-sense RNA genomes consiting of three segments, denoted as Small (S), Medium (M) and Large (L). Ngari is thought to be the natural reassortant progeny of Bunyamwera and Batai viruses. The relationship between these ‘parental’ viruses and the ‘progeny’ poses an interesting question, especially given that there is overlap in their respective transmission ecologies, but differences in their infection host ranges and pathogenesis. We compared the kinetics of these three viruses in a common laboratory system and found no significant difference in growth kinetics. There was, however, a tendency of BATV to have smaller plaques than either BUNV or NRIV. Furthermore, we determined that all three viruses are stable in extracellular conditions and retain infectivity for a week in non-cellular media, which has public health and biosafety implications. The study of this understudied group of viruses addresses a need for basic characterization of viruses that have not yet reached epidemic transmission intensity, but that have the potential due to their infectivity to both human and animal hosts. These results lay the groundwork for future studies of these neglected viruses of potential public and One Health importance.

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  • Accepted:
  • Published Online:
Keyword(s): Batai , Bunyamwera , Bunyavirus , Ngari , Orthobunyavirus and viral stability
Funding
This study was supported by the:
  • United States Agency for International Development (Award BFS- G-11-00002)
    • Principle Award Recipient: RebeccaC Christofferson
© 2021 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2020-12-01
2024-04-28
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References

  1. Briese T, Bird B, Kapoor V, Nichol ST, Lipkin WI. Batai and Ngari viruses: M segment reassortment and association with severe febrile disease outbreaks in East Africa. J Virol 2006; 80:5627–5630 [View Article][PubMed]
     [Google Scholar]
  2. Tauro LB, Rivarola ME, Lucca E, Mariño B, Mazzini R et al. First isolation of Bunyamwera virus (Bunyaviridae family) from horses with neurological disease and an abortion in Argentina. Vet J 2015; 206:111–114 [View Article][PubMed]
     [Google Scholar]
  3. Gerrard SR, Li L, Barrett AD, Nichol ST. Ngari virus is a Bunyamwera virus reassortant that can be associated with large outbreaks of hemorrhagic fever in Africa. J Virol 2004; 78:8922–8926 [View Article][PubMed]
     [Google Scholar]
  4. Bowen MD, Trappier SG, Sanchez AJ, Meyer RF, Goldsmith CS et al. A reassortant bunyavirus isolated from acute hemorrhagic fever cases in Kenya and Somalia. Virology 2001; 291:185–190 [View Article][PubMed]
     [Google Scholar]
  5. Groseth A, Weisend C, Ebihara H. Complete genome sequencing of mosquito and human isolates of Ngari virus. J Virol 2012; 86:13846–13847 [View Article][PubMed]
     [Google Scholar]
  6. Fuller F, Bishop DH. Identification of virus-coded nonstructural polypeptides in bunyavirus-infected cells. J Virol 1982; 41:643–648 [View Article][PubMed]
     [Google Scholar]
  7. Odhiambo C, Venter M, Limbaso K, Swanepoel R, Sang R et al. Genome sequence analysis of in vitro and in vivo phenotypes of Bunyamwera and Ngari virus isolates from northern Kenya. PLoS One 2014; 9:e105446 [View Article][PubMed]
     [Google Scholar]
  8. Dutuze MF, Nzayirambaho M, Mores CN, Christofferson RC. A review of Bunyamwera, batai, and ngari viruses: understudied Orthobunyaviruses with potential one health implications. Front Vet Sci 2018; 5:69 [View Article][PubMed]
     [Google Scholar]
  9. Szemiel AM, Failloux AB, Elliott RM. Role of Bunyamwera Orthobunyavirus NSs protein in infection of mosquito cells. PLoS Negl Trop Dis 2012; 6:p. e1823 [View Article][PubMed]
     [Google Scholar]
  10. Riblett AM, Doms RW. Making Bunyaviruses talk: interrogation tactics to identify host factors required for infection. Viruses 2016; 8:130 13 05 2016 [View Article][PubMed]
     [Google Scholar]
  11. Medlock JM, Snow KR, Leach S. Possible ecology and epidemiology of medically important mosquito-borne arboviruses in Great Britain. Epidemiol Infect 2007; 135:466–482 [View Article][PubMed]
     [Google Scholar]
  12. Liu H, Shao X-qun, Hu B, Zhao J-jun, Zhang L et al. Isolation and complete nucleotide sequence of a Batai virus strain in inner Mongolia, China. Virol J 2014; 11:138 [View Article][PubMed]
     [Google Scholar]
  13. Singh KR, Pavri KM. Isolation of Chittoor virus from mosquitoes and demonstration of serological conversions in sera of domestic animals at Manjri, Poona, India. Indian J Med Res 1966; 54:220–224[PubMed]
     [Google Scholar]
  14. Gaidamovich SY, Obukhova VR, Vinograd AI, Klisenko GA, Melnikova EE et al. Olkya-an arbovirus of the Bunyamwera group in the U.S.S.R. Acta Virol 1973; 17:444[PubMed]
     [Google Scholar]
  15. Lambert AJ, Lanciotti RS. Consensus amplification and novel multiplex sequencing method for S segment species identification of 47 viruses of the Orthobunyavirus, Phlebovirus, and Nairovirus genera of the family Bunyaviridae . J Clin Microbiol 2009; 47:2398–2404 [View Article][PubMed]
     [Google Scholar]
  16. Nashed NW, Olson JG, el-Tigani A. Isolation of Batai virus (Bunyaviridae:Bunyavirus) from the blood of suspected malaria patients in Sudan. Am J Trop Med Hyg 1993; 48:676–681 [View Article][PubMed]
     [Google Scholar]
  17. Smithburn KC, Haddow AJ, Mahaffy AF. A neurotropic virus isolated from Aedes mosquitoes caught in the Semliki Forest. Am J Trop Med Hyg 1946; 26:189–208 [View Article][PubMed]
     [Google Scholar]
  18. Zeller HG, Diallo M, Angel G, Traoré-Lamizana M, Thonnon J et al. [Ngari virus (Bunyaviridae: Bunyavirus). First isolation from humans in Senegal, new mosquito vectors, its epidemiology]. Bull Soc Pathol Exot 1996; 89:12–16[PubMed]
     [Google Scholar]
  19. Eiden M, Vina-Rodriguez A, El Mamy BO, Isselmou K, Ziegler U et al. Ngari virus in goats during Rift Valley fever outbreak, Mauritania, 2010. Emerg Infect Dis 2014; 20:2174–2176 [View Article][PubMed]
     [Google Scholar]
  20. Institute, E.A.V.R East African Virus Research Institute Report for 1967 Entebbe, Uganda: East African Virus Research Institute; 1967 p 25
     [Google Scholar]
  21. Jäckel S, Eiden M, El Mamy BO, Isselmou K, Vina-Rodriguez A et al. Molecular and serological studies on the Rift Valley fever outbreak in Mauritania in 2010. Transbound Emerg Dis 2013; 60 Suppl 2:31–39 [View Article][PubMed]
     [Google Scholar]
  22. Burleson FG, Chambers TM, Wiedbrauk DL. Virology: a Laboratory Manual Elsevier; 2014
     [Google Scholar]
  23. Kokernot RH, Heymann CS, Muspratt J, Wolstenholme B. Studies on arthropod-borne viruses of Tongaland. V. isolation of Bunyamwera and Rift Valley fever viruses from mosquitoes. S Afr J Med Sci 1957; 22:71–80[PubMed]
     [Google Scholar]
  24. Kawiecki AB, Christofferson RC. Zika virus-induced antibody response enhances dengue virus serotype 2 replication in vitro. J Infect Dis 2016; 214:1357–1360 [View Article][PubMed]
     [Google Scholar]
  25. Kawiecki AB, Mayton EH, Dutuze MF, Goupil BA, Langohr IM et al. Tissue tropisms, infection kinetics, histologic lesions, and antibody response of the MR766 strain of Zika virus in a murine model. Virol J 2017; 14:82 [View Article][PubMed]
     [Google Scholar]
  26. Elliott RM. Nucleotide sequence analysis of the large (L) genomic RNA segment of Bunyamwera virus, the prototype of the family Bunyaviridae. Virology 1989; 173:426–436 [View Article][PubMed]
     [Google Scholar]
  27. Lees JF, Pringle CR, Elliott RM. Nucleotide sequence of the Bunyamwera virus M RNA segment: conservation of structural features in the bunyavirus glycoprotein gene product. Virology 1986; 148:1–14 [View Article][PubMed]
     [Google Scholar]
  28. Dunn EF, Pritlove DC, Elliott RM. The S RNA genome segments of Batai, Cache Valley, Guaroa, Kairi, Lumbo, main drain and Northway bunyaviruses: sequence determination and analysis. J Gen Virol 1994; 75:597–608 [View Article][PubMed]
     [Google Scholar]
  29. Yanase T, Kato T, Yamakawa M, Takayoshi K, Nakamura K et al. Genetic characterization of Batai virus indicates a genomic reassortment between orthobunyaviruses in nature. Arch Virol 2006; 151:2253–2260 [View Article][PubMed]
     [Google Scholar]
  30. Groseth A, Matsuno K, Dahlstrom E, Anzick SL, Porcella SF et al. Complete genome sequencing of four geographically diverse strains of Batai virus. J Virol 2012; 86:13844–13845 [View Article][PubMed]
     [Google Scholar]
  31. Dilcher M, Sall AA, Hufert FT, Weidmann M. Clarifying Bunyamwera virus riddles of the past. Virus Genes 2013; 47:160–163 [View Article][PubMed]
     [Google Scholar]
  32. Mayton EH, Tramonte AR, Wearing HJ, Christofferson RC. Age-structured vectorial capacity reveals timing, not magnitude of within-mosquito dynamics is critical for arbovirus fitness assessment. Parasit Vectors 2020; 13:310 [View Article][PubMed]
     [Google Scholar]
  33. Faye O, Faye O, Diallo D, Diallo M, Weidmann M et al. Quantitative real-time PCR detection of Zika virus and evaluation with field-caught mosquitoes. Virol J 2013; 10:311 [View Article][PubMed]
     [Google Scholar]
  34. Colavita F, Quartu S, Lalle E, Bordi L, Lapa D et al. Evaluation of the inactivation effect of Triton X-100 on Ebola virus infectivity. J Clin Virol 2017; 86:27–30 [View Article][PubMed]
     [Google Scholar]
  35. Jonges M, Liu WM, van der Vries E, Jacobi R, Pronk I et al. Influenza virus inactivation for studies of antigenicity and phenotypic neuraminidase inhibitor resistance profiling. J Clin Microbiol 2010; 48:928–940 [View Article][PubMed]
     [Google Scholar]
  36. Sprouffske K, Wagner A. Growthcurver: an R package for obtaining interpretable metrics from microbial growth curves. BMC Bioinformatics 2016; 17:172 [View Article][PubMed]
     [Google Scholar]
  37. Rockwood LL. Introduction to Population Ecology John Wiley & Sons; 2015
     [Google Scholar]
  38. Sprouffske K, Wagner A. Growthcurver: an R package for obtaining interpretable metrics from microbial growth curves. BMC Bioinformatics 2016; 17:172 [View Article][PubMed]
     [Google Scholar]
  39. Albornoz A, Hoffmann AB, Lozach P-Y, Tischler ND. Early Bunyavirus-Host cell interactions. Viruses 2016; 8:143 24 05 2016 [View Article][PubMed]
     [Google Scholar]
  40. Dutuze MF, Ingabire A, Gafarasi I, Uwituze S, Nzayirambaho M et al. Identification of bunyamwera and possible other Orthobunyavirus infections and disease in cattle during a rift valley fever outbreak in Rwanda in 2018. Am J Trop Med Hyg 2020; 103:183–189 [View Article][PubMed]
     [Google Scholar]
  41. Sinclair R, Boone SA, Greenberg D, Keim P, Gerba CP et al. Persistence of category a select agents in the environment. Appl Environ Microbiol 2008; 74:555–563 [View Article][PubMed]
     [Google Scholar]
  42. Kallio ER, Klingström J, Gustafsson E, Manni T, Vaheri A et al. Prolonged survival of Puumala hantavirus outside the host: evidence for indirect transmission via the environment. J Gen Virol 2006; 87:2127–2134 [View Article][PubMed]
     [Google Scholar]
  43. Hardestam J, Simon M, Hedlund KO, Vaheri A, Klingström J et al. Ex vivo stability of the rodent-borne Hantaan virus in comparison to that of arthropod-borne members of the Bunyaviridae family. Appl Environ Microbiol 2007; 73:2547–2551 [View Article][PubMed]
     [Google Scholar]
  44. Craig DE, Thomas WJ, DeSanctis AN. Stability of Rift Valley fever virus at 4 C. Appl Microbiol 1967; 15:446–447 [View Article][PubMed]
     [Google Scholar]
  45. Miller WS, Demchak P, Rosenberger CR, Dominik JW. Stability and infectivity of airborne yellow fever and Rift Valley fever viruses.. Army Biological Labs Frederick Md 1962
     [Google Scholar]
  46. de St Maurice A, Nyakarahuka L, Purpura L, Ervin E, Tumusiime A et al. Notes from the Field: Rift Valley Fever Response - Kabale District, Uganda, March 2016. MMWR Morb Mortal Wkly Rep 2016; 65:1200–1201 [View Article][PubMed]
     [Google Scholar]
  47. Rodrigues Hoffmann A, Dorniak P, Filant J, Dunlap KA, Bazer FW et al. Ovine fetal immune response to Cache Valley virus infection. J Virol 2013; 87:5586–5592 [View Article][PubMed]
     [Google Scholar]
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Comparative characterization of the reassortant Orthobunyavirus Ngari with putative parental viruses, Bunyamwera and Batai: in vitro characterization and ex vivo stability
J. Gen. Virol. 102, 001523 (2021); https://doi.org/10.1099/jgv.0.001523
/content/journal/jgv/10.1099/jgv.0.001523
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