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. 2006 Feb 23;151(8):1567–1585. doi: 10.1007/s00705-006-0726-y

Isolation of a variant infectious bronchitis virus in Australia that further illustrates diversity among emerging strains

J Ignjatovic 1, G Gould 1, S Sapats 1
PMCID: PMC7087298  PMID: 16501892

Summary.

Australian infectious bronchitis viruses (IBV) have undergone a separate evolution due to geographic isolation. Consequently, changes occurring in Australian IBV illustrate, independently from other countries, types of variability that could occur in emerging IBV strains. Previously, we have identified two distinct genetic groups of IBV, designated subgroups 1 and 2. IBV strains of subgroup 1 have S1 and N proteins that share a high degree of amino acid identity, 81 to 98% in S1 and 91 to 99% in N. Subgroup 2 strains possess S1 and N proteins that share a low level of identity with subgroup 1 strains: 54 to 62% in S1 and 60 to 62% in N. This paper describes the isolation and characterisation of a third, previously undetected genetic group of IBV in Australia. The subgroup 3 strains, represented by isolate chicken/Australia/N2/04, had an S1 protein that shared a low level of identity with both subgroups 1 and 2: 61 to 63% and 56 to 59%, respectively. However, the N protein and the 3′ untranslated region were similar to subgroup 1: 90 to 97% identical with the N protein of subgroup 1 strains. This N4/02 subgroup 3 of IBV is reminiscent of two other strains, D1466 and DE072, isolated in the Netherlands and in the USA, respectively. The emergence of the subgroup 3 viruses in Australia, as well as the emergence of subgroup 2 in 1988, could not be explained by any of the mechanisms that are currently considered to be involved in generation of IBV variants.

Keywords: Infectious Bronchitis Virus, Hemagglutination Inhibition Test, Avian Infectious Bronchitis Virus, Tracheal Mucus, Avian Pathol

References

  1. Akin A, Lin TL, Wu CC, Bryan TA, Hooper T, Schrader D. Nucleocapsid protein gene sequence analysis reveals close genomic relationship between turkey coronavirus and avian infectious bronchitis virus. Acta Virol. 2001;45:31–38. [PubMed] [Google Scholar]
  2. Bijlenga G, Cook JKA, Gelb J, Jr, de Wit Development and use of the H strain of avian infectious bronchitis virus from the Netherlands as a vaccine: a review. Avian Pathol. 2004;33:550–557. doi: 10.1080/03079450400013154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Breslin JJ, Smith LG, Fuller FJ, Guy JS. Sequence analysis of the turkey coronavirus nucleocapsid protein gene and 3′ untranslated region identifies the virus as a close relative of infectious bronchitis virus. Virus Res. 1999;65:187–193. doi: 10.1016/S0168-1702(99)00117-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brooks JE, Rainer AC, Parr RL, Woolcock P, Hoerr F, Collisson EW. Comparison of envelope through 5B sequences of infectious bronchitis coronaviruses indicates recombination occurs in the envelope and membrane genes. Virus Res. 2004;100:191–198. doi: 10.1016/j.virusres.2003.11.016. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Casais R, Dove B, Cavanagh D, Britton P. Recombinant avian infectious bronchitis virus expressing a heterologous spike gene demonstrates that the spike protein is a determinant of cell tropism. J Virol. 2003;77:9084–9089. doi: 10.1128/JVI.77.16.9084-9089.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cavanagh D. A nomenclature for avian coronavirus isolates and the question of species status. Avian Pathol. 2001;30:109–115. doi: 10.1080/03079450120044506. [DOI] [PubMed] [Google Scholar]
  7. Cavanagh D, Naqi S. Infectious bronchitis. In: Saif YM, Barnes HJ, Glisson JR, Fadly AM, McDougald LR, Swayne DE, editors. Diseases of poultry. Ames: Iowa State Press; 2003. pp. 101–119. [Google Scholar]
  8. Cavanagh D, Davis PJ, Darbysire JH, Peters RW (1986) Coronavirus IBV: virus retaining spike glycopolypeptide S2 but not S1 is unable to induce virus-neutralizing or haemagglutination-inhibiting antibody, or induce chicken tracheal protection. J Gen Virol: 1435–1442 [DOI] [PubMed]
  9. Cavanagh D, Davis PJ, Mockett APA. Amino acids within hypervariable region 1 of avian coronavirus IBV (Massachusetts serotype) spike glycoprotein are associated with neutralization epitopes. Virus Res. 1988;11:141–150. doi: 10.1016/0168-1702(88)90039-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cavanagh D, Davis PJ, Cook JKA, Li D, Kant A, Koch G. Location of the amino acid differences in the S1 spike glycoprotein subunit of closely related serotypes of infectious bronchitis virus. Avian Pathol. 1992;21:33–43. doi: 10.1080/03079459208418816. [DOI] [PubMed] [Google Scholar]
  11. Cavanagh D, Mawditt K, Sharma M, Drury SE, Ainsworth HL, Britton P, Gough RE. Detection of a coronavirus from turkey poults in Europe genetically related to infectious bronchitis virus of chickens. Avian Pathol. 2001;30:355–368. doi: 10.1080/03079450120066368. [DOI] [PubMed] [Google Scholar]
  12. Cavanagh D, Mawditt K, Welchman D, de B, Britton P, Gough RE. Coronaviruses from pheasants (Phasianus colchicus) are genetically closely related to coronaviruses of domestic fowl (infectious bronchitis virus) and turkeys. Avian Pathol. 2002;31:81–93. doi: 10.1080/03079450120106651. [DOI] [PubMed] [Google Scholar]
  13. De Wit JJ. Detection of infectious bronchitis viruses. Avian Pathol. 2000;29:71–93. doi: 10.1080/03079450094108. [DOI] [PubMed] [Google Scholar]
  14. Farsang A, Ros C, Renström LHM, Baule C, Soós T, Belák S. Molecular epizootiology of infectious bronchitis virus in Sweden indicating the involvement of a vaccine strain. Avian Pathol. 2002;31:229–236. doi: 10.1080/03079450220136530. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gelb JRJ, Keeler CL, Jr, Nix WA, Rosenberger JK, Cloud SS. Antigenic and S1 genomic characterization of the Delaware variant serotype of infectious bronchitis virus. Avian Dis. 1997;41:661–669. doi: 10.2307/1592158. [DOI] [PubMed] [Google Scholar]
  16. González JM, Gomez-Puertas P, Cavanagh D, Gorbalenya AE, Enjuanes L. A comparative sequence analysis to revise the current taxonomy of the family Coronaviridae. Arch Virol. 2003;148:2207–2235. doi: 10.1007/s00705-003-0162-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Guy JS. Turkey coronavirus is more closely related to avian infectious bronchitis virus than to mammalian coronaviruses: a review. Avian Pathol. 2000;29:207–212. doi: 10.1080/03079450050045459. [DOI] [PubMed] [Google Scholar]
  18. Ignjatovic J, McWaters PG. Monoclonal antibodies to three structural proteins of avian infectious bronchitis virus: characterisation of epitopes and antigenic differentiation of Australian strains. J Gen Virol. 1991;72:2915–2922. doi: 10.1099/0022-1317-72-12-2915. [DOI] [PubMed] [Google Scholar]
  19. Ignjatovic J, Galli L. The S1 glycoprotein but not N or M proteins of avian infectious bronchitis virus induces protection in vaccinated chickens. Arch Virol. 1994;138:117–134. doi: 10.1007/BF01310043. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ignjatovic J, Galli L. Immune responses to structural proteins of avian infectious bronchitis virus. Avian Pathol. 1995;24:313–332. doi: 10.1080/03079459508419072. [DOI] [PubMed] [Google Scholar]
  21. Ignjatovic J, Ashton F. Detection and differentiation of avian infectious bronchitis viruses using a monoclonal antibody-based ELISA. Avian Pathol. 1996;25:721–736. doi: 10.1080/03079459608419177. [DOI] [PubMed] [Google Scholar]
  22. Ignjatovic J, Sapats SA, Ashton F. A long-term study of Australian infectious bronchitis viruses indicates a major antigenic changes in recently isolated strains. Avian Pathol. 1997;26:535–552. doi: 10.1080/03079459708419233. [DOI] [PubMed] [Google Scholar]
  23. Jia W, Naqi SA. Sequence analysis of gene 3, gene 4 and gene 5 of avian infectious bronchitis virus strain CU-T2. Gene. 1997;189:189–193. doi: 10.1016/S0378-1119(96)00847-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Jia W, Karaca K, Parrish CR, Naqi SA. A novel variant of avian infectious bronchitis virus resulting from recombination among three different strains. Arch Virol. 1995;140:259–271. doi: 10.1007/BF01309861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Jonassen CM, Kofstad T, Larsen I-L, Løvland A, Handeland K, Follestad A, Lillehaug A. Molecular identification and characterisation of novel coronaviruses infecting graylag geese (Anser anser), feral pigeons (Columbia livia) and mallards (Anas platyrhynchos) J Gen Virol. 2005;86:1597–1607. doi: 10.1099/vir.0.80927-0. [DOI] [PubMed] [Google Scholar]
  26. Kant A, Koch G, van Roozelaar DJ, Kusters JG, Poelwijk FAJ, van der Zeijst BAM. Location of antigenic sites defined by neutralising monoclonal antibodies on the S1 avian infectious bronchitis virus glycopolypeptide. J Gen Virol. 1992;73:591–596. doi: 10.1099/0022-1317-73-3-591. [DOI] [PubMed] [Google Scholar]
  27. Kusters JG, Niesters HGM, Bleumink-Pluym NMC, Davelaar FG, Horzinek MC, van der Zeijst BAM. Molecular epidemiology of infectious bronchitis virus in the Netherlands. J Gen Virol. 1987;68:343–352. doi: 10.1099/0022-1317-68-2-343. [DOI] [PubMed] [Google Scholar]
  28. Kusters JG, Niesters HGM, Lenstra JA, Horzinek MC, van der Zeijst BAM. Phylogeny of antigenic variants of avian coronavirus IBV. Virology. 1989;138:217–221. doi: 10.1016/0042-6822(89)90058-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kusters JG, Jager EJ, Niesters HGM, van der Zeijst BAM. Sequence evidence for RNA recombination in field isolates of avian coronavirus infectious bronchitis virus. Vaccine. 1990;8:605–608. doi: 10.1016/0264-410X(90)90018-H. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lee CW, Jackwood MW. Evidence of genetic diversity generated by recombination among avian coronavirus IBV. Arch Virol. 2000;145:2135–2148. doi: 10.1007/s007050070044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Lee CW, Jackwood MW. Spike gene analysis of the DE072 strain of infectious bronchitis virus: origin and evolution. Virus Genes. 2001;22:85–91. doi: 10.1023/A:1008138520451. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lee SK, Sung HW, Kwon HM. S1 glycoprotein gene analysis of infectious bronchitis viruses isolated in Korea. Arch Virol. 2004;149:481–494. doi: 10.1007/s00705-003-0225-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Lin TL, Loa CC, Wu CC. Complete sequences of 3′ end coding region for structural protein genes of turkey coronavirus. Virus Res. 2004;106:61–70. doi: 10.1016/j.virusres.2004.06.003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Liu S, Chen J, Chen J, Kond X, Shao Y, Han Z, Feng L, Cai X, Gu S, Liu M. Isolation of avian infectious bronchitis coronavirus from domestic peafowl (Pavo cristatus) and teal (Anas) J Gen Virol. 2005;86:719–725. doi: 10.1099/vir.0.80546-0. [DOI] [PubMed] [Google Scholar]
  35. Mase M, Tsukamoto K, Imai K, Yamaguchi S. Phylogenetic analysis of avian infectious bronchitis virus strains isolated in Japan. Arch Virol. 2004;149:2069–2078. doi: 10.1007/s00705-004-0369-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Page RDM. TREEVIEW: An application to display phylogenetic trees on personal computers. Comput Appl Biosci. 1996;12:357–358. doi: 10.1093/bioinformatics/12.4.357. [DOI] [PubMed] [Google Scholar]
  37. Sapats SI, Ashton F, Wright PJ, Ignjatovic J. Sequence analysis of the S1 glycoprotein of infectious bronchitis viruses: identification of a novel genotypic group in Australia. J Gen Virol. 1996;77:413–418. doi: 10.1099/0022-1317-77-3-413. [DOI] [PubMed] [Google Scholar]
  38. Sapats SI, Ashton F, Wright PJ, Ignjatovic J. Novel variation in the N protein of avian infectious bronchitis virus. Virology. 1996;226:412–417. doi: 10.1006/viro.1996.0670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Shie HK, Shien J-H, Chou H-Y, Shimizau Y, Chen J-N, Chang P-C. Complete nucleotide sequence of S1 and N genes of infectious bronchitis virus isolated in Japan and Taiwan. J Vet Med Sci. 2004;66:555–558. doi: 10.1292/jvms.66.555. [DOI] [PubMed] [Google Scholar]
  40. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997;25:4876–4882. doi: 10.1093/nar/25.24.4876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Williams AK, Wang L, Sneed LW, Collisson EW. Comparative analysis of the nucleocapsid genes of several strains of infectious bronchitis virus and other coronaviruses. Virus Res. 1992;25:213–222. doi: 10.1016/0168-1702(92)90135-V. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Williams AK, Wang L, Sneed LW, Collisson EW. Analysis of a hypervariable region in the 3′ non-coding end of the infectious bronchitis virus genome. Virus Res. 1993;28:19–27. doi: 10.1016/0168-1702(93)90086-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wang L, Junker D, Collisson EW. Evidence of natural recombination within the S1 gene of infectious bronchitis virus. Virology. 1993;192:710–716. doi: 10.1006/viro.1993.1093. [DOI] [PubMed] [Google Scholar]
  44. Wang L, Parr RL, King DJ, Collisson EW. A highly conserved epitope on the spike protein of infectious bronchitis virus. Arch Virol. 1995;140:2201–2213. doi: 10.1007/BF01323240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Zwaagstra KA, Zeijst BAM, van der Kusters JG, van der Zeijst BAM. Rapid detection and identification of avian infectious bronchitis virus. J Clin Microbiol. 1992;30:79–84. doi: 10.1128/jcm.30.1.79-84.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]

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