1887

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Volume 101, Issue 2

Effect of AlbB on a positive-sense RNA negev-like virus: a novel virus persistently infecting mosquitoes and cells Free

Abstract

The mosquito is the primary vector of several medically important arboviruses. The endosymbiotic bacterium, , has emerged as a means of blocking transmission of arboviruses such as dengue and Zika viruses. One strain that has shown potential in field trials is AlbB, a naturally occurring strain of the Asian tiger mosquito . When transinfected into , AlbB exhibits strong virus inhibition. In addition to modulating arboviruses, also modulates some insect-specific viruses. Here, we explored the effect of on the virome of the cell line Aa23 naturally infected with AlbB and also a stably transinfected recipient cell line (Aag2.AlbB). RNA sequencing and bioinformatic analysis on both cell lines revealed an 11 kb genome of a single-stranded positive-sense RNA negev-like virus related to the recently proposed negevirus taxon. We denoted this novel virus as Aedes albopictus negev-like virus (AalNLV). Tetracycline clearance of from Aa23 cells did not significantly affect AalNLV levels, while in Aag2.AlbB cells, a significant increase in virus genome RNA copies was observed. We further investigated the inhibitory effect of AlbB on AalNLV and another positive-sense RNA virus, cell fusing agent virus, which is present in Aag2 cells and known to be suppressed by AlbB suppressed both viruses, with the effect on AalNLV being more striking. The findings from this study further supplement our understanding of the complex interaction between , host and virome.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Aedes aegypti , insect-specific viruses , negevirus , RNA-Seq and Wolbachia
Funding
This study was supported by the:
  • Australian Research Council (Award DP150101782)
    • Principle Award Recipient: Sassan Asgari
© 2020 The Authors
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2019-12-17
2024-04-25
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References

  1. Calvez E, Guillaumot L, Millet L, Marie J, Bossin H et al. Genetic diversity and phylogeny of Aedes aegypti, the main arbovirus vector in the Pacific. PLoS Negl Trop Dis 2016; 10:e0004374 [View Article]
     [Google Scholar]
  2. Lourenço-de-Oliveira R, Failloux A-B. Lessons learned on Zika virus vectors. PLoS Negl Trop Dis 2017; 11:e0005511 [View Article]
     [Google Scholar]
  3. Hall RA, Bielefeldt-Ohmann H, McLean BJ, O'Brien CA, Colmant AMG et al. Commensal viruses of mosquitoes: host restriction, transmission, and interaction with arboviral pathogens. Evol Bioinform Online 2016; 12:35–44 [View Article]
     [Google Scholar]
  4. Hobson-Peters J, Yam AWY, Lu JWF, Setoh YX, May FJ et al. 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 2013; 8:e56534 [View Article]
     [Google Scholar]
  5. Hall-Mendelin S, McLean BJ, Bielefeldt-Ohmann H, Hobson-Peters J, Hall RA et al. The insect-specific palm creek virus modulates West Nile virus infection in and transmission by Australian mosquitoes. Parasit Vectors 2016; 9:414 [View Article]
     [Google Scholar]
  6. Schultz MJ, Frydman HM, Connor JH. Dual insect specific virus infection limits arbovirus replication in Aedes mosquito cells. Virology 2018; 518:406–413 [View Article]
     [Google Scholar]
  7. Zhang G, Asad S, Khromykh AA, Asgari S. Cell fusing agent virus and dengue virus mutually interact in Aedes aegypti cell lines. Sci Rep 2017; 7:6935 [View Article]
     [Google Scholar]
  8. Bian G, Xu Y, Lu P, Xie Y, Xi Z. The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti . PLoS Pathog 2010; 6:e1000833 [View Article]
     [Google Scholar]
  9. Schultz MJ, Isern S, Michael SF, Corley RB, Connor JH et al. Variable inhibition of Zika virus replication by different Wolbachia strains in mosquito cell cultures. J Virol 2017; 91:e00339–00317 [View Article]
     [Google Scholar]
  10. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH. How many species are infected with Wolbachia?- a statistical analysis of current data. FEMS Microbiol Lett 2008; 281:215–220 [View Article]
     [Google Scholar]
  11. Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ. The incidence of bacterial endosymbionts in terrestrial arthropods. Proc Biol Sci 2015; 282:20150249 [View Article]
     [Google Scholar]
  12. Blagrove MSC, Arias-Goeta C, Failloux A-B, Sinkins SP. Wolbachia strain wMel induces cytoplasmic incompatibility and blocks dengue transmission in Aedes albopictus . Proc Natl Acad Sci USA 2012; 109:255–260 [View Article]
     [Google Scholar]
  13. Dobson SL. Reversing Wolbachia-based population replacement. Trends Parasitol 2003; 19:128–133 [View Article]
     [Google Scholar]
  14. Sicard M, Bonneau M, Weill M. Wolbachia prevalence, diversity, and ability to induce cytoplasmic incompatibility in mosquitoes. Current Opinion in Insect Science 2019; 34:12–20 [View Article]
     [Google Scholar]
  15. Hoffmann AA, Ross PA, Rašić G. Wolbachia strains for disease control: ecological and evolutionary considerations. Evol Appl 2015; 8:751–768 [View Article]
     [Google Scholar]
  16. Osborne SE, Iturbe-Ormaetxe I, Brownlie JC, O'Neill SL, Johnson KN. Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans . Appl Environ Microbiol 2012; 78:6922–6929 [View Article]
     [Google Scholar]
  17. Dutton TJ, Sinkins SP. Strain-specific quantification of Wolbachia density in Aedes albopictus and effects of larval rearing conditions. Insect Mol Biol 2004; 13:317–322 [View Article]
     [Google Scholar]
  18. Johnson K. The impact of Wolbachia on virus infection in mosquitoes. Viruses 2015; 7:5705–5717 [View Article]
     [Google Scholar]
  19. Ant TH, Herd CS, Geoghegan V, Hoffmann AA, Sinkins SP. The Wolbachia strain wAu provides highly efficient virus transmission blocking in Aedes aegypti . PLoS Pathog 2018; 14:e1006815 [View Article]
     [Google Scholar]
  20. Lu P, Bian G, Pan X, Xi Z. Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLoS Negl Trop Dis 2012; 6:e1754 [View Article]
     [Google Scholar]
  21. Parry R, Bishop C, De Hayr L, Asgari S. Density-dependent enhanced replication of a densovirus in Wolbachia-infected Aedes cells is associated with production of piRNAs and higher virus-derived siRNAs. Virology 2019; 528:89–100 [View Article]
     [Google Scholar]
  22. Amuzu HE, McGraw EA. Wolbachia-based dengue virus inhibition is not tissue-specific in Aedes aegypti . PLoS Negl Trop Dis 2016; 10:e0005145 [View Article]
     [Google Scholar]
  23. Fattouh N, Cazevieille C, Landmann F. Wolbachia endosymbionts subvert the endoplasmic reticulum to acquire host membranes without triggering ER stress. PLoS Negl Trop Dis 2019; 13:e0007218 [View Article]
     [Google Scholar]
  24. Wu M, Sun LV, Vamathevan J, Riegler M, Deboy R et al. Phylogenomics of the reproductive parasite Wolbachia pipientis wMel: a streamlined genome overrun by mobile genetic elements. PLoS Biol 2004; 2:E69 [View Article]
     [Google Scholar]
  25. Caragata EP, Rancès E, Hedges LM, Gofton AW, Johnson KN et al. Dietary cholesterol modulates pathogen blocking by Wolbachia . PLoS Pathog 2013; 9:e1003459 [View Article]
     [Google Scholar]
  26. White PM, Serbus LR, Debec A, Codina A, Bray W et al. Reliance of Wolbachia on High Rates of Host Proteolysis Revealed by a Genome-Wide RNAi Screen of Drosophila Cells. Genetics 2017; 205:1473–1488 [View Article]
     [Google Scholar]
  27. Rancès E, Ye YH, Woolfit M, McGraw EA, O'Neill SL. The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLoS Pathog 2012; 8:e1002548 [View Article]
     [Google Scholar]
  28. Pan X, Pike A, Joshi D, Bian G, McFadden MJ et al. The bacterium Wolbachia exploits host innate immunity to establish a symbiotic relationship with the dengue vector mosquito Aedes aegypti . ISME J 2018; 12:277–288 [View Article]
     [Google Scholar]
  29. Raquin V, Valiente Moro C, Saucereau Y, Tran F-H, Potier P et al. Native Wolbachia from Aedes albopictus blocks Chikungunya virus infection in cellulo . PLoS One 2015; 10:e0125066 [View Article]
     [Google Scholar]
  30. Zhang G, Etebari K, Asgari S. Wolbachia suppresses cell fusing agent virus in mosquito cells. J Gen Virol 2016; 97:3427–3432 [View Article]
     [Google Scholar]
  31. Schnettler E, Sreenu VB, Mottram T, McFarlane M. Wolbachia restricts insect-specific flavivirus infection in Aedes aegypti cells. J Gen Virol 2016; 97:3024–3029 [View Article]
     [Google Scholar]
  32. Shi M, Neville P, Nicholson J, Eden J-S, Imrie A et al. High-Resolution metatranscriptomics reveals the ecological dynamics of mosquito-associated RNA viruses in Western Australia. J Virol 2017; 91:e00680–00617 [View Article]
     [Google Scholar]
  33. Vasilakis N, Forrester NL, Palacios G, Nasar F, Savji N et al. Negevirus: a proposed new taxon of insect-specific viruses with wide geographic distribution. J Virol 2013; 87:2475–2488 [View Article]
     [Google Scholar]
  34. 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]
  35. Bigot D, Atyame CM, Weill M, Justy F, Herniou EA et al. Discovery of Culex pipiens associated tunisia virus: a new ssRNA(+) virus representing a new insect associated virus family. Virus Evol 2018; 4:vex040 [View Article]
     [Google Scholar]
  36. Kuchibhatla DB, Sherman WA, Chung BYW, Cook S, Schneider G et al. Powerful sequence similarity search methods and in-depth manual analyses can identify remote homologs in many apparently "Orphan" viral proteins. J Virol 2014; 88:10–20 [View Article]
     [Google Scholar]
  37. O'Brien CA, McLean BJ, Colmant AMG, Harrison JJ, Hall-Mendelin S et al. Discovery and characterisation of Castlerea virus, a new species of negevirus isolated in Australia. Evol Bioinform Online 2017; 13:1176934317691269
     [Google Scholar]
  38. JB X, XH S, Bonizzoni M, Zhong DB, YJ L et al. Comparative transcriptome analysis and RNA interference reveal CYP6A8 and SNPs related to pyrethroid resistance in Aedes albopictus . PLoS Negl Trop Dis 2018; 12:e0006828
     [Google Scholar]
  39. Xiao P, Han J, Zhang Y, Li C, Guo X et al. Metagenomic analysis of Flaviviridae in mosquito viromes isolated from Yunnan Province in China reveals genes from dengue and Zika viruses. Front Cell Infect Microbiol 2018; 8:359 [View Article]
     [Google Scholar]
  40. Hoffmann AA, Iturbe-Ormaetxe I, Callahan AG, Phillips BL, Billington K et al. Stability of the wMel Wolbachia infection following invasion into Aedes aegypti populations. PLoS Negl Trop Dis 2014; 8:e3115 [View Article]
     [Google Scholar]
  41. Jeffries CL, Walker T. Wolbachia biocontrol strategies for arboviral diseases and the potential influence of resident Wolbachia strains in mosquitoes. Curr Trop Med Rep 2016; 3:20–25 [View Article]
     [Google Scholar]
  42. Parry R, Asgari S. Aedes anphevirus: an insect-specific virus distributed worldwide in Aedes aegypti mosquitoes that has complex interplays with Wolbachia and dengue virus infection in cells. J Virol 2018; 92:e00224–00218 [View Article]
     [Google Scholar]
  43. Siozios S, Sapountzis P, Ioannidis P, Bourtzis K. Wolbachia symbiosis and insect immune response. Insect Sci 2008; 15:89–100 [View Article]
     [Google Scholar]
  44. O'Neill SL, Pettigrew MM, Sinkins SP, Braig HR, Andreadis TG et al. In vitro cultivation of Wolbachia pipientis in an Aedes albopictus cell line. Insect Mol Biol 1997; 6:33–39
     [Google Scholar]
  45. Peleg J. Growth of arboviruses in monolayers from subcultured mosquito embryo cells. Virology 1968; 35:617–619 [View Article]
     [Google Scholar]
  46. Pudney M, Varma MGR, Leake CJ. Establishment of cell lines from larvae of culicine (Aedes species) and anopheline mosquitoes. Tca Manual 1979; 5:997–1002 [View Article]
     [Google Scholar]
  47. Igarashi A. Isolation of a Singh's Aedes albopictus cell clone sensitive to dengue and Chikungunya viruses. J Gen Virol 1978; 40:531–544 [View Article]
     [Google Scholar]
  48. Ridley AW, Hereward JP, Daglish GJ, Raghu S, McCulloch GA et al. Flight of Rhyzopertha dominica (Coleoptera: Bostrichidae)—a Spatio-temporal analysis with pheromone trapping and population genetics. J Econ Entomol 2016; 109:2561–2571 [View Article]
     [Google Scholar]
  49. Hussain M, Frentiu FD, Moreira LA, O'Neill SL, Asgari S. Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedes aegypti . Proc Natl Acad Sci USA 2011; 108:9250–9255 [View Article]
     [Google Scholar]
  50. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium . Cell 2009; 139:1268–1278 [View Article]
     [Google Scholar]
  51. 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]
  52. Cock PJA, Chilton JM, Grüning B, Johnson JE, Soranzo N. NCBI BLAST+ integrated into Galaxy. Gigascience 2015; 4:39 [View Article]
     [Google Scholar]
  53. Li W, Godzik A. Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 2006; 22:1658–1659 [View Article]
     [Google Scholar]
  54. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001; 29:45e [View Article]
     [Google Scholar]
  55. Edgar RC. Muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004; 32:1792–1797 [View Article]
     [Google Scholar]
  56. Talavera G, Castresana J. Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst Biol 2007; 56:564–577 [View Article]
     [Google Scholar]
  57. Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu CH et al. Beast 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 2014; 10:e1003537 [View Article]
     [Google Scholar]
  58. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior Summarization in Bayesian phylogenetics using tracer 1.7. Syst Biol 2018; 67:901–904
     [Google Scholar]
  59. Rambaut A. FigTree V1. 4.2, a graphical viewer of phylogenetic trees; 2014
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Effect of Wolbachia wAlbB on a positive-sense RNA negev-like virus: a novel virus persistently infecting Aedes albopictus mosquitoes and cells
J. Gen. Virol. 101, 216 (2020); https://doi.org/10.1099/jgv.0.001361
/content/journal/jgv/10.1099/jgv.0.001361
/content/journal/jgv/10.1099/jgv.0.001361
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