Advertisement

Archives of Virology

, Volume 164, Issue 7, pp 1771–1780 | Cite as

A comparative phylogenomic analysis of avian avulavirus 1 isolated from non-avian hosts: conquering new frontiers of zoonotic potential among species

  • Aziz Ul-RahmanEmail author
  • Muhammad Zubair Shabbir
Original Article

Abstract

A number of avian avulavirus 1 (AAvV 1) isolates have been reported from avian and non-avian hosts worldwide with varying clinical consequences. In this regard, robust surveillance coupled with advanced diagnostics, genomic analysis, and disease modelling has provided insight into the molecular epidemiology and evolution of this virus. The genomic and evolutionary characteristics of AAvV 1 isolates originating from avian hosts have been well studied, but those originating from non-avian hosts have not. Here, we report a comparative genomic and evolutionary analysis of so-far reported AAvV 1 isolates originating from hosts other than avian species (humans, mink and swine). Phylogenetic analysis showed that AAvV 1 isolates clustered in five distinct genotypes (I, II, VI, VII and XIII). Further analysis revealed clustering of isolates into clades distant enough to be considered distinct subgenotypes, along with a few substitutions in several significant motifs. Although further investigation is needed, the clustering of AAvV 1 strains isolated from non-avian hosts into novel subgenotypes and the presence of substitutions in important structural and biological motifs suggest that this virus can adapt to novel hosts and therefore could have zoonotic potential.

Notes

Author contributions

AR apprehends the idea. AR and MZS did analysis and manuscript write-up.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This article does not contain studies with animals or humans.

Informed consent

No humans or animals were involved.

References

  1. 1.
    Advisory Committee on Dangerous Pathogens (2004) The approved list of biological agents; categorisation of biological agents according to hazard and categories of containment. Health and Safety Executive Books, Sudbury, pp 1–17Google Scholar
  2. 2.
    Ahad A, Rabbani M, Yaqub T, Mahmood A, Kuthu ZH, Shabbir MZ, Sheikh AA, Gohar H (2013) Detection of antibody to newcastle disease virus in human sera in Pakistan. J Anim Plant Sci 23(4):990–994Google Scholar
  3. 3.
    Aziz-ul-Rahman Munir M, Shabbir MZ (2018) Comparative evolutionary and phylogenomic analysis of Avian avulaviruses 1 to 20. Mol Phylogenet Evol 127:931–951CrossRefGoogle Scholar
  4. 4.
    Aziz-ul-Rahman Wensman JJ, Abubakar M, Shabbir MZ, Rossiter P (2018) Peste des petits ruminants in wild ungulates. Trop Anim Health Prod 51:1815–1819CrossRefGoogle Scholar
  5. 5.
    Baric RS, Yount B, Lindesmith L, Harrington PR, Greene SR, Tseng FC, Davis N, Johnston RE, Klapper DG, Moe CL (2001) Expression and self-assembly of Norwalk virus capsid protein from Venezuelan equine encephalitis virus replicons. J Virol 76(6):3023–3030CrossRefGoogle Scholar
  6. 6.
    Charan S, Mahajan VM, Rai A, Balaya S (1984) Ocular pathogenesis of Newcastle disease virus in rabbits and monkeys. J Comp Pathol 94(1):159–163CrossRefGoogle Scholar
  7. 7.
    Clayton BA (2017) Nipah virus: transmission of a zoonotic paramyxovirus. Curr Opin Virol 22:97–104CrossRefGoogle Scholar
  8. 8.
    Diel DG, da Silva LH, Liu H, Wang Z, Miller PJ, Afonso CL (2012) Genetic diversity of avian paramyxovirus type 1: proposal for a unified nomenclature and classification system of Newcastle disease virus genotypes. Infect Genet Evol 12:1770–1779CrossRefGoogle Scholar
  9. 9.
    Ding Z, Cong YL, Chang S, Wang GM, Wang Z, Zhang QP, Wu H, Sun YZ (2010) Genetic analysis of avian paramyxovirus-1 (Newcastle disease virus) isolates obtained from swine populations in China related to commonly utilized commercial vaccine strains. Virus Genes 41(3):369–376CrossRefGoogle Scholar
  10. 10.
    Falk K, Batts WN, Kvellestad A, Kurath G, Wiik-Nielsen J, Winton JR (2008) Molecular characterisation of Atlantic salmon paramyxovirus (ASPV): a novel paramyxovirus associated with proliferative gill inflammation. Virus Res 133(2):218–227.  https://doi.org/10.1016/j.virusres.2008.01.006 CrossRefGoogle Scholar
  11. 11.
    Goebel SJ, Taylor J, Barr BC, Kiehn TE, Castro-Malaspina HR, Hedvat CV, Rush-Wilson KA, Kelly CD, Davis SW, Samsonoff WA, Hurst KR (2007) Isolation of avian paramyxovirus 1 from a patient with a lethal case of pneumonia. J Virol 81:12709–12714CrossRefGoogle Scholar
  12. 12.
    Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  13. 13.
    Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23(2):254–267CrossRefGoogle Scholar
  14. 14.
    Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451(7181):990CrossRefGoogle Scholar
  15. 15.
    Kloepper TH, Huson DH (2008) Drawing explicit phylogenetic networks and their integration into SplitsTree. BMC Evol Biol 8(1):22CrossRefGoogle Scholar
  16. 16.
    Kuhn JH, Wolf YI, Krupovic M, Zhang YZ, Maes P, Dolja VV, Koonin EV (2019) Classify viruses—the gain is worth the pain. Nature 566:318–320.  https://doi.org/10.1038/d41586-019-00599-8 CrossRefGoogle Scholar
  17. 17.
    Kuiken T, Breitbart M, Beer M, Grund C, Hoper D, van den Hoogen B, Kerkhoffs JH, Kroes AC, Rosario K, van Run P, Schwarz M (2018) Zoonotic infection with pigeon paramyxovirus type 1 linked to fatal pneumonia. J Infect Dis.  https://doi.org/10.1093/infdis/jiy036 Google Scholar
  18. 18.
    Lamb RA, Kolakofsky D (2001) In Paramyxoviridae: the viruses and their replication. In: Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (eds) Field's virology, 5th edn. LippincottWilliams & Wilkins, Philadelphia, PA, pp 1305–1340Google Scholar
  19. 19.
    Miller PJ, Kim LM, Ip HS, Afonso CL (2009) Evolutionary dynamics of Newcastle disease virus. Virology 391:64–72CrossRefGoogle Scholar
  20. 20.
    Mirza AM, Deng R, Iorio RM (1994) Site-directed mutagenesis of a conserved hexapeptide in the paramyxovirus hemagglutinin-neuraminidase glycoprotein: effects on antigenic structure and function. J Virol 68(8):5093–5099Google Scholar
  21. 21.
    Renshaw RW, Glaser AL, Van Campen H, Weiland F, Dubovi EJ (2000) Identification and phylogenetic comparison of Salem virus, a novel paramyxovirus of horses. Virology 270(2):417–429.  https://doi.org/10.1006/viro.2000.0305 CrossRefGoogle Scholar
  22. 22.
    Reperant LA, Kuiken T, Osterhaus AD (2012) Adaptive pathways of zoonotic influenza viruses: from exposure to establishment in humans. Vaccine 30:4419–4434CrossRefGoogle Scholar
  23. 23.
    Rohaim MA, El Naggar RF, Helal AM, Hussein HA, Munir M (2017) Reverse spillover of avian viral vaccine strains from domesticated poultry to wild birds. Vaccine 35(28):3523–3527CrossRefGoogle Scholar
  24. 24.
    Römer-Oberdörfer A, Werner O, Veits J, Mebatsion T, Mettenleiter TC (2003) Contribution of the length of the HN protein and the sequence of the F protein cleavage site to Newcastle disease virus pathogenicity. J Gen Virol 84(11):3121–3129CrossRefGoogle Scholar
  25. 25.
    Schmitt AP, Leser GP, Morita E, Sundquist WI, Lamb RA (2005) Evidence for a new viral late domain core sequence, FPIV, necessary for budding of a paramyxovirus. J Virol 79:2988–2997CrossRefGoogle Scholar
  26. 26.
    Shabbir MZ, Akhtar S, Tang Y, Yaqub T, Ahmad A, Mustafa G, Alam MA, Santhakumar D, Nair V (2016) Infectivity of wild bird origin Avian Paramyxovirus serotype 1 and vaccine effectiveness in chickens. J Gen Virol 97(12):3161–3173.  https://doi.org/10.1099/jgv.0.000618 CrossRefGoogle Scholar
  27. 27.
    Shabbir MZ, Nissly RH, Ahad A, Rabbani M, Chothe SK, Sebastian A, Albert I, Jayarao BM, Kuchipudi SV (2018) Complete genome sequences of three related avian avulavirus 1 isolates from poultry farmers in Pakistan. Genome Announc 6(18):e00361-18CrossRefGoogle Scholar
  28. 28.
    Shabbir MZ, Zohari S, Yaqub T, Nazir J, Shabbir MAB, Mukhtar N, Shafee M, Sajid M, Anees M, Abbas M, Khan MT, Ali AA, Ghafoor A, Ahad A, Channa AA, Anjum AA, Kalhoro NH, Ahmad A, Goraya MU, Iqbal Z, Khan SA, Aslam HB, Zehra K, Sohail MU, Yaqub W, Berg M, Munir M (2013) Genetic diversity of Newcastle disease virus in Pakistan: a countrywide perspective. Virol J 10:170–179CrossRefGoogle Scholar
  29. 29.
    Sharma B, Pokhriyal M, Rai GK, Saxena M, Ratta B, Chaurasia M, Yadav BS, Sen A, Mondal B (2012) Isolation of Newcastle disease virus from a non-avian host (sheep) and its implications. Arch Virol 157(8):1565–1567CrossRefGoogle Scholar
  30. 30.
    Shi M, Lin XD, Chen X, Tian JH, Chen LJ, Li K, Wang W, Eden JS, Shen JJ, Liu L, Holmes EC (2018) The evolutionary history of vertebrate RNA viruses. Nature 556(7700):197CrossRefGoogle Scholar
  31. 31.
    Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729.  https://doi.org/10.1093/molbev/mst197 CrossRefGoogle Scholar
  32. 32.
    Tidona CA, Kurz HW, Gelderblom HR, Darai G (1999) Isolation and molecular characterization of a novel cytopathogenic paramyxovirus from tree shrews. Virology 258(2):425–434.  https://doi.org/10.1006/viro.1999.9693 CrossRefGoogle Scholar
  33. 33.
    Aziz-ul-Rahman Yaqub T, Imran M, Habib M, Sohail T, Furqan Shahid M, Munir M, Shabbir MZ (2018) Phylogenomics and infectious potential of avian avulaviruses species-type 1 isolated from healthy green-winged teal (Anas carolinensis) from a wetland sanctuary of Indus River. Avian Dis 62(4):404–415Google Scholar
  34. 34.
    Wang W, Han GZ (2018) The expanding diversity of RNA viruses in vertebrates. Trends Microbiol 26(6):465–466CrossRefGoogle Scholar
  35. 35.
    Wise MG, Sellers HS, Alvarez R, Seal BS (2004) RNA-dependent RNA polymerase gene analysis of worldwide Newcastle disease virus isolates representing different virulence types and their phylogenetic relationship with other members of the Paramyxoviridae. Virus Res 104:71–80CrossRefGoogle Scholar
  36. 36.
    Woo PC, Lau SK, Wong BH, Fan RY, Wong AY, Zhang AJ, Wu Y, Choi GK, Li KS, Hui J, Wang M (2012) Morbillivirus, a previously undescribed paramyxovirus associated with tubulointerstitial nephritis in domestic cats. Proc Natl Acad Sci USA 109(14):5435–5440.  https://doi.org/10.1073/pnas.1119972109 CrossRefGoogle Scholar
  37. 37.
    Woo PC, Lau SK, Wong BH, Wong AY, Poon RW, Yuen KY (2011) Complete genome sequence of a novel paramyxovirus, Tailam virus, discovered in Sikkim rats. J Virol 85(24):13473–13474.  https://doi.org/10.1128/JVI.06356-11 CrossRefGoogle Scholar
  38. 38.
    Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T (2004) The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5(7):730CrossRefGoogle Scholar
  39. 39.
    Yuan X, Wang Y, Yang J, Xu H, Zhang Y, Qin Z, Ai H, Wang J (2012) Genetic and biological characterizations of a Newcastle disease virus from swine in China. Virology 9(1):129CrossRefGoogle Scholar
  40. 40.
    Zhao P, Sun L, Sun X, Li S, Zhang W, Pulscher LA, Chai H, Xing M (2017) Newcastle disease virus from domestic mink, China, 2014. Vet Microbiol 198:104–107CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of MicrobiologyUniversity of Veterinary and Animal SciencesLahorePakistan
  2. 2.Quality Operations LaboratoryUniversity of Veterinary and Animal SciencesLahorePakistan

Personalised recommendations