1887

Abstract

The genus harbours mostly insect-transmitted viruses that cause severe disease in humans, livestock and wildlife. Thus far, only three alphaviruses with a host range restricted to insects have been found in mosquitoes from the Old World, namely Eilat virus (EILV), Taï Forest alphavirus (TALV) and Mwinilunga alphavirus (MWAV). In this study, we found a novel alphavirus in one mosquito sampled in Panama. The virus was isolated in C6/36 mosquito cells, and full genome sequencing revealed an 11 468 nt long genome with maximum pairwise nucleotide identity of 62.7 % to Sindbis virus. Phylogenetic analyses placed the virus as a solitary deep rooting lineage in a basal relationship to the Western equine encephalitis antigenic complex and to the clade comprising EILV, TALV and MWAV, indicating the detection of a novel alphavirus, tentatively named Agua Salud alphavirus (ASALV). No growth of ASALV was detected in vertebrate cell lines, including cell lines derived from ectothermic animals, and replication of ASALV was strongly impaired above 31 °C, suggesting that ASALV represents the first insect-restricted alphavirus of the New World.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution NonCommercial License.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001344
2020-01-01
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/jgv/101/1/96.html?itemId=/content/journal/jgv/10.1099/jgv.0.001344&mimeType=html&fmt=ahah

References

  1. Chen R, Mukhopadhyay S, Merits A, Bolling B, Nasar F et al. ICTV virus taxonomy profile: Togaviridae . J Gen Virol 2018
    [Google Scholar]
  2. Hermanns K, Zirkel F, Kopp A, Marklewitz M, Rwego IB et al. Discovery of a novel alphavirus related to Eilat virus. J Gen Virol 2017; 98:43–49 [View Article]
    [Google Scholar]
  3. 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]
  4. Chen W, Foo S-S, Sims NA, Herrero LJ, Walsh NC et al. Arthritogenic alphaviruses: new insights into arthritis and bone pathology. Trends Microbiol 2015; 23:35–43 [View Article]
    [Google Scholar]
  5. Zacks MA, Paessler S, alphaviruses E. Encephalitic alphaviruses. Vet Microbiol 2010; 140:281–286 [View Article]
    [Google Scholar]
  6. Garcia-Moreno M, Sanz MA, Carrasco L. A viral mRNA motif at the 3'-untranslated region that confers translatability in a cell-specific manner. Implications for virus evolution. Sci Rep 2016; 6:19217 [View Article]
    [Google Scholar]
  7. Ou JH, Trent DW, Strauss JH. The 3'-non-coding regions of alphavirus RNAs contain repeating sequences. J Mol Biol 1982; 156:719–730 [View Article]
    [Google Scholar]
  8. Pfeffer M, Kinney RM, Kaaden OR. The alphavirus 3'-nontranslated region: size heterogeneity and arrangement of repeated sequence elements. Virology 1998; 240:100–108 [View Article]
    [Google Scholar]
  9. Weston J, Villoing S, Bremont M, Castric J, Pfeffer M et al. Comparison of two aquatic alphaviruses, salmon pancreas disease virus and sleeping disease virus, by using genome sequence analysis, monoclonal reactivity, and cross-infection. J Virol 2002; 76:6155–6163 [View Article]
    [Google Scholar]
  10. Forrester NL, Palacios G, Tesh RB, Savji N, Guzman H et al. Genome-Scale phylogeny of the alphavirus genus suggests a marine origin. J Virol 2012; 86:2729–2738 [View Article]
    [Google Scholar]
  11. Nasar F, Palacios G, Gorchakov RV, Guzman H, Da Rosa APT et al. Eilat virus, a unique alphavirus with host range restricted to insects by RNA replication. Proc Natl Acad Sci U S A 2012; 109:14622–14627 [View Article]
    [Google Scholar]
  12. Halbach R, Junglen S, van Rij RP. Mosquito-specific and mosquito-borne viruses: evolution, infection, and host defense. Curr Opin Insect Sci 2017; 22:16–27 [View Article]
    [Google Scholar]
  13. Shi M, Lin X-D, Tian J-H, Chen L-J, Chen X et al. Redefining the invertebrate RNA virosphere. Nature 2016; 540:539543 [View Article]
    [Google Scholar]
  14. Chandler JA, Liu RM, Bennett SN. Rna shotgun metagenomic sequencing of northern California (USA) mosquitoes uncovers viruses, bacteria, and fungi. Front Microbiol 2015; 06:185 [View Article]
    [Google Scholar]
  15. Junglen S, Kopp A, Kurth A, Pauli G, Ellerbrok H et al. A new flavivirus and a new vector: characterization of a novel flavivirus isolated from uranotaenia mosquitoes from a tropical rain forest. J Virol 2009; 83:4462–4468 [View Article]
    [Google Scholar]
  16. Junglen S, Korries M, Grasse W, Wieseler J, Kopp A et al. Host range restriction of insect-specific flaviviruses occurs at several levels of the viral life cycle. mSphere 2017; 2: [View Article]
    [Google Scholar]
  17. Marklewitz M, Zirkel F, Kurth A, Drosten C, Junglen S. Evolutionary and phenotypic analysis of live virus isolates suggests arthropod origin of a pathogenic RNA virus family. Proc Natl Acad Sci U S A 2015; 112:7536–7541 [View Article]
    [Google Scholar]
  18. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M et al. Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 2012; 28:1647–1649 [View Article]
    [Google Scholar]
  19. 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]
  20. Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article]
    [Google Scholar]
  21. Vodovar N, Bronkhorst AW, van Cleef KWR, Miesen P, Blanc H et al. Arbovirus-derived piRNAs exhibit a ping-pong signature in mosquito cells. PLoS One 2012; 7:e30861 [View Article]
    [Google Scholar]
  22. Afgan E, Baker D, Batut B, van den Beek M, Bouvier D et al. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res 2018; 46:W537–W544 [View Article]
    [Google Scholar]
  23. Auguste AJ, Carrington CVF, Forrester NL, Popov VL, Guzman H et al. Characterization of a novel Negevirus and a novel bunyavirus isolated from Culex (Culex) declarator mosquitoes in Trinidad. J Gen Virol 2014; 95:481–485 [View Article]
    [Google Scholar]
  24. Kallies R, Kopp A, Zirkel F, Estrada A, Gillespie T et al. Genetic characterization of goutanap virus, a novel virus related to negeviruses, cileviruses and higreviruses. Viruses 2014; 6:4346–4357 [View Article]
    [Google Scholar]
  25. Nunes MRT, Contreras-Gutierrez MA, Guzman H, Martins LC, Barbirato MF et al. Genetic characterization, molecular epidemiology, and phylogenetic relationships of insect-specific viruses in the taxon Negevirus. Virology 2017; 504:152–167 [View Article]
    [Google Scholar]
  26. Travassos da Rosa AP, Turell MJ, Watts DM, Powers AM, Vasconcelos PF et al. Trocara virus: a newly recognized alphavirus (Togaviridae) isolated from mosquitoes in the Amazon Basin. Am J Trop Med Hyg 2001; 64:93–97 [View Article]
    [Google Scholar]
  27. Allison AB, Stallknecht DE, Holmes EC. Evolutionary genetics and vector adaptation of recombinant viruses of the Western equine encephalitis antigenic complex provides new insights into alphavirus diversity and host switching. Virology 2015; 474:154–162 [View Article]
    [Google Scholar]
  28. Bennouna A, Gil P, El Rhaffouli H, Exbrayat A, Loire E et al. Identification of Eilat virus and prevalence of infection among Culex pipiens L. populations, Morocco, 2016. Virology 2019; 530:85–88 [View Article]
    [Google Scholar]
  29. Hikke MC, Verest M, Vlak JM, Pijlman GP. Salmonid alphavirus replication in mosquito cells: towards a novel vaccine production system. Microb Biotechnol 2014; 7:480–484 [View Article]
    [Google Scholar]
  30. McLoughlin MF, Graham DA. Alphavirus infections in salmonids-a review. J Fish Dis 2007; 30:511–531 [View Article]
    [Google Scholar]
  31. Bingham AM, Graham SP, Burkett-Cadena ND, White GS, Hassan HK et al. Detection of eastern equine encephalomyelitis virus RNA in North American snakes. Am J Trop Med Hyg 2012; 87:1140–1144 [View Article]
    [Google Scholar]
  32. Graham SP, Hassan HK, Chapman T, White G, Guyer C et al. Serosurveillance of eastern equine encephalitis virus in amphibians and reptiles from Alabama, USA. Am J Trop Med Hyg 2012; 86:540–544 [View Article]
    [Google Scholar]
  33. White G, Ottendorfer C, Graham S, Unnasch TR. Competency of reptiles and amphibians for eastern equine encephalitis virus. Am J Trop Med Hyg 2011; 85:421–425 [View Article]
    [Google Scholar]
  34. Burkett-Cadena ND, Eubanks MD, Hassan HK, Unnasch TR, Guyer C et al. Blood feeding patterns of potential arbovirus vectors of the genus Culex targeting ectothermic hosts. Am J Trop Med Hyg 2008; 79:809–815 [View Article]
    [Google Scholar]
  35. Cupp EW, Zhang D, Yue X, Cupp MS, Guyer C et al. Identification of reptilian and amphibian blood meals from mosquitoes in an eastern equine encephalomyelitis virus focus in central Alabama. Am J Trop Med Hyg 2004; 71:272–276 [View Article]
    [Google Scholar]
  36. Carrasco L, Sanz MA, González-Almela E. The regulation of translation in Alphavirus-Infected cells. Viruses 2018; 10:70 [View Article]
    [Google Scholar]
  37. Wolf YI, Kazlauskas D, Iranzo J, Lucía-Sanz A, Kuhn JH et al. Origins and evolution of the global RNA Virome. mBio 2018; 9: [View Article]
    [Google Scholar]
  38. Hahn CS, Lustig S, Strauss EG, Strauss JH. Western equine encephalitis virus is a recombinant virus. Proc Natl Acad Sci U S A 1988; 85:5997–6001 [View Article]
    [Google Scholar]
  39. Strauss JH, Strauss EG, Alphaviruses Rin. Recombination in alphaviruses. Seminars in Virology 1997; 8:85–94 [View Article]
    [Google Scholar]
  40. Miras M, Sempere RN, Kraft JJ, Miller WA, Aranda MA et al. Interfamilial recombination between viruses led to acquisition of a novel translation-enhancing RNA element that allows resistance breaking. New Phytol 2014; 202:233–246 [View Article]
    [Google Scholar]
  41. Causey OR, Casals J, Shope RE, UDOMSAKDI S, Udomsakdi S. Aura and Una, two new group A arthropod-borne viruses. Am J Trop Med Hyg 1963; 12:777–781 [View Article]
    [Google Scholar]
  42. Rümenapf T, Strauss EG, Strauss JH. Subgenomic mRNA of aura alphavirus is packaged into virions. J Virol 1994; 68:56–62
    [Google Scholar]
  43. Ventoso I. Adaptive changes in alphavirus mRNA translation allowed colonization of vertebrate hosts. J Virol 2012; 86:9484–9494 [View Article]
    [Google Scholar]
  44. Miesen P, Joosten J, van Rij RP. PIWIs go viral: arbovirus-derived piRNAs in vector mosquitoes. PLoS Pathog 2016; 12:e1006017 [View Article]
    [Google Scholar]
  45. Miesen P, Girardi E, van Rij RP. Distinct sets of PIWI proteins produce arbovirus and transposon-derived piRNAs in Aedes aegypti mosquito cells. Nucleic Acids Res 2015; 43:6545–6556 [View Article]
    [Google Scholar]
  46. Morazzani EM, Wiley MR, Murreddu MG, Adelman ZN, Myles KM. Production of virus-derived ping-pong-dependent piRNA-like small RNAs in the mosquito soma. PLoS Pathog 2012; 8:e1002470 [View Article]
    [Google Scholar]
  47. Schnettler E, Donald CL, Human S, Watson M, Siu RWC et al. Knockdown of piRNA pathway proteins results in enhanced Semliki Forest virus production in mosquito cells. J Gen Virol 2013; 94:1680–1689 [View Article]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001344
Loading
/content/journal/jgv/10.1099/jgv.0.001344
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error