Full genome analysis of Australian infectious bronchitis viruses suggests frequent recombination events between vaccine strains and multiple phylogenetically distant avian coronaviruses of unknown origin

Veterinary Microbiology

Volumn 197, Issue , 2016, Pages 27-38

  Quinteros, José A ^a   Lee, Sang Won ^a,b   Markham, Philip F ^a   Noormohammadi, Amir H ^a   Hartley, Carol A ^a   Legione, Alistair R ^a   Coppo, Mauricio J C ^a   Vaz, Paola K ^a   Browning, Glenn F ^a  

^a THE UNIVERSITY OF MELBOURNE   (Australia)

^b Konkuk University   (South Korea)

Author keywords

Full genome sequences; Infectious bronchitis virus; Recombinants; Recombination; Unknown avian coronaviruses; Vaccine recombinants

Indexed keywords

NUCLEOTIDE; VIRUS GLYCOPROTEIN; VIRAL PROTEIN; VIRUS VACCINE;

ARTICLE; AUSTRALIA; AVIAN CORONAVIRUS; AVIAN INFECTIOUS BRONCHITIS VIRUS; GENE SEQUENCE; GENOME ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PHYLOGENY; VIRUS GENE; VIRUS GENOME; VIRUS ISOLATION; VIRUS RECOMBINATION; VIRUS STRAIN; WILD TYPE; AMINO ACID SEQUENCE; ANIMAL; CHICKEN; CORONAVIRUS INFECTIONS; GENETIC REASSORTMENT; GENETICS; METABOLISM; POULTRY DISEASES; VETERINARY; VIROLOGY;

AMINO ACID SEQUENCE; ANIMALS; AUSTRALIA; CHICKENS; CORONAVIRUS INFECTIONS; GENOME, VIRAL; INFECTIOUS BRONCHITIS VIRUS; PHYLOGENY; POULTRY DISEASES; REASSORTANT VIRUSES; VIRAL PROTEINS; VIRAL VACCINES;

EID: 84995530452     PISSN: 03781135     EISSN: 18732542     Source Type: Journal    
DOI: 10.1016/j.vetmic.2016.11.003     Document Type: Article

References (49)

1. Ammayappan, A., Upadhyay, C., Gelb, J. Jr., Vakharia, V.N., Complete genomic sequence analysis of infectious bronchitis virus Ark DPI strain and its evolution by recombination. J. Virol., 5, 2008, 157.
2. Armesto, M., Cavanagh, D., Britton, P., The replicase gene of avian coronavirus infectious bronchitis virus is a determinant of pathogenicity. PLoS One, 4(10), 2009, e7384.
3. Arvidson, Y., Tannock, G.A., Zerbes, M., Ignjatovic, J., Efficacy of Australian vaccines against recent isolates of avian infectious bronchitis viruses. Aust. Vet. J. 68:6 (1991), 211–212.
4. Boni, M.F., Posada, D., Feldman, M.W., An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176:2 (2007), 1035–1047.
5. Boots, A.H., Kusters, J., Zeijst, B.M., Hensen, E., The nucleocapsid protein of IBV comprises immunodominant determinants recognized by T-cells. Cavanagh, D., Brown, T.D., (eds.) Coronaviruses and their Diseases, vol. 276, 1991, Springer, US, 189–197.
6. Cavanagh, D., Davis, P.J., Darbyshire, J.H., Peters, R.W., 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. 67:7 (1986), 1435–1442.
7. Chen, Y., Cai, H., a, Pan J., Xiang, N., Tien, P., Ahola, T., Guo, D., Functional screen reveals SARS coronavirus nonstructural protein nsp14 as a novel cap N7 methyltransferase. Proc. Natl. Acad. Sci. U. S. A. 106:9 (2009), 3484–3489.
8. Chen, Y., Tao, J., Sun, Y., Wu, A., Su, C., Gao, G., Cai, H., Qiu, S., Wu, Y., Ahola, T., Guo, D., Structure-function analysis of severe acute respiratory syndrome coronavirus RNA cap guanine-N7-methyltransferase. J. Virol. 87:11 (2013), 6296–6305.
9. Chousalkar, K.K., Cheetham, B.F., Roberts, J.R., Effects of infectious bronchitis virus vaccine on the oviduct of hens. Vaccine 27:10 (2009), 1485–1489.
10. Cumming, R.B., The etiology of uraemia of chickens. Aust. Vet. J., 38(11), 1962 (554-554).
11. Eckerle, L.D., Becker, M.M., Halpin, R.A., Li, K., Venter, E., Lu, X., Scherbakova, S., Graham, R.L., Baric, R.S., Stockwell, T.B., Spiro, D.J., Denison, M.R., Infidelity of SARS-CoV nsp14-exonuclease mutant virus replication is revealed by complete genome sequencing. PLoS Pathog., 6(5), 2010, e1000896.
12. Gelman, A., Rubin, D.B., Inference from iterative simulation using multiple sequences. Stat. Sci. 7:4 (1992), 457–472.
13. Gibbs, M.J., Armstrong, J.S., Gibbs, A.J., Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:7 (2000), 573–582.
14. Hewson, K.A., Ignjatovic, J., Browning, G.F., Devlin, J.M., Noormohammadi, A.H., Infectious bronchitis viruses with naturally occurring genomic rearrangement and gene deletion. Arch. Virol. 156:2 (2011), 245–252.
15. Hewson, K.A., Noormohammadi, A.H., Devlin, J.M., Browning, G.F., Schultz, B.K., Ignjatovic, J., Evaluation of a novel strain of infectious bronchitis virus emerged as a result of spike gene recombination between two highly diverged parent strains. Avian Pathol. 43:3 (2014), 249–257.
16. Hon, C.-C., Lam, T.-Y., Shi, Z.-L., Drummond, A.J., Yip, C.-W., Zeng, F., Lam, P.-Y., Leung, F.C.-C., Evidence of the recombinant origin of a bat severe acute respiratory syndrome (SARS)-like coronavirus and its implications on the direct ancestor of SARS coronavirus. J. Virol. 82:4 (2008), 1819–1826.
17. Huson, D.H., Bryant, D., Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23:2 (2006), 254–267.
18. Ignjatovic, J., Galli, L., The S1 glycoprotein but not the N or M proteins of avian infectious bronchitis virus induces protection in vaccinated chickens. Arch. Virol. 138:1–2 (1994), 117–134.
19. Ignjatovic, J., Sapats, S.I., Ashton, F., A long-term study of Australian infectious bronchitis viruses indicates a major antigenic change in recently isolated strains. Avian Pathol. 26:3 (1997), 535–552.
20. Ignjatovic, J., Gould, G., Sapats, S., Isolation of a variant infectious bronchitis virus in Australia that further illustrates diversity among emerging strains. Arch. Virol. 151:8 (2006), 1567–1585.
21. International Committee on Taxonomy of Viruses, 2015. Retrieved from http://www.ictvonline.org/virusTaxonomy.asp.
22. Jackwood, M.W., de Witt, J.J., Infectious bronchitis. Swayne, D.E., Glisson, J.R., McDougald, L.R., Nolan, L.K., Suarez, D.L., Nair, V.L., (eds.) Diseases of Poultry, 13th ed., 2013, John Wiley & Sons, Inc., 39–159.
23. Jackwood, M.W., Boynton, T.O., Hilt, D.A., McKinley, E.T., Kissinger, J.C., Paterson, A.H., Robertson, J., Lemke, C., McCall, A.W., Williams, S.M., Jackwood, J.W., Byrd, L.A., Emergence of a group 3 coronavirus through recombination. Virology 398:1 (2010), 98–108.
24. Jia, W., Karaca, K., Parrish, C.R., Naqi, S.A., A novel variant of avian infectious bronchitis virus resulting from recombination among three different strains. Arch. Virol. 140:2 (1995), 259–271.
25. Lin, T.L., Loa, C.C., Wu, C.C., Complete sequences of 3’ end coding region for structural protein genes of turkey coronavirus. Virus Res. 106:1 (2004), 61–70.
26. Lole, K.S., Bollinger, R.C., Paranjape, R.S., Gadkari, D., Kulkarni, S.S., Novak, N.G., Ingersoll, R., Sheppard, H.W., Ray, S.C., Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J. Virol. 73:1 (1999), 152–160.
27. Lougovskaia, N.N., Lougovskoi, A.A., Bochkov, Y.A., Batchenko, G.V., Mudrak, N.S., Drygin, V.V., Borisov, A.V., Borisov, V.V., Gusev, A.A., Detection and estimation of avian infectious bronchitis virus antigen by a novel indirect liquid-phase blocking enzyme-linked immunosorbent assay using chicken and rabbit affinity purified immunoglobulins. Avian Pathol. 31:6 (2002), 549–557.
28. Mardani, K., Noormohammadi, A.H., Hooper, P., Ignjatovic, J., Browning, G.F., Infectious bronchitis viruses with a novel genomic organization. J. Virol. 82:4 (2008), 2013–2024.
29. Mardani, K., Noormohammadi, A.H., Ignjatovic, J., Browning, G., Naturally occurring recombination between distant strains of infectious bronchitis virus. Arch. Virol. 155:10 (2010), 1581–1586.
30. Martin, D., Posada, D., Crandall, K., Williamson, C., A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res. Hum. Retrovir. 21:1 (2005), 98–102.
31. Martin, D.P., Lemey, P., Lott, M., Moulton, V., Posada, D., Lefeuvre, P., RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:19 (2010), 2462–2463.
32. Martin, D.P., Murrell, B., Golden, M., Khoosal, A., Muhire, B., RDP4: Detection and analysis of recombination patterns in virus genomes. Virus Evol. 1:1 (2015), 1–5.
33. Minskaia, E., Hertzig, T., Gorbalenya, A.E., Campanacci, V., Cambillau, C., Canard, B., Ziebuhr, J., Discovery of an RNA virus 3' → 5' exoribonuclease that is critically involved in coronavirus RNA synthesis. Proc. Natl. Acad. Sci. U. S. A. 103:13 (2006), 5108–5113.
34. Ovcharenko, I., Loots, G.G., Giardine, B.M., Hou, M., Ma, J., Hardison, R.C., Stubbs, L., Miller, W., Mulan: multiple-sequence local alignment and visualization for studying function and evolution. Genome Res. 15:1 (2005), 184–194.
35. Padidam, M., Sawyer, S., Fauquet, C.M., Possible emergence of new geminiviruses by frequent recombination. Virology 265:2 (1999), 218–225.
36. Posada, D., Crandall, K.A., Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc. Natl. Acad. Sci. U. S. A. 98:24 (2001), 13757–13762.
37. Quinteros, J.A., Markham, P.F., Lee, S.-W., Hewson, K.A., Hartley, C.A., Legione, A.R., Coppo, M.J.C., Vaz, P.K., Browning, G.F., Analysis of the complete genomic sequences of two virus subpopulations of the Australian infectious bronchitis virus vaccine VicS. Avian Pathol. 44:3 (2015), 182–191.
38. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A., Huelsenbeck, J.P., MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:3 (2012), 539–542.
39. Saif, L.J., Coronavirus immunogens. Vet. Microbiol. 37:3–4 (1993), 285–297.
40. Sapats, S.I., Ashton, F., Wright, P.J., Ignjatovic, J., Sequence analysis of the S1 glycoprotein of infectious bronchitis viruses: identification of a novel genotypic group in Australia. J. Gen. Virol. 77 (1996), 413–418.
41. Seo, S.H., Wang, L., Smith, R., Collisson, E.W., The carboxyl-terminal 120-residue polypeptide of infectious bronchitis virus nucleocapsid induces cytotoxic T lymphocytes and protects chickens from acute infection. J. Virol. 71:10 (1997), 7889–7894.
42. Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., Thompson, J.D., Higgins, D.G., Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol., 7(1), 2011 (539).
43. Smith, E.C., Denison, M.R., Implications of altered replication fidelity on the evolution and pathogenesis of coronaviruses. Curr. Opin. Virol. 2:5 (2012), 519–524.
44. Smith, J.M., Analyzing the mosaic structure of genes. J. Mol. Evol. 34:2 (1992), 126–129.
45. Stroehlein, A.J., Young, N.D., Jex, A.R., Sternberg, P.W., Tan, P., Boag, P.R., Hofmann, A., Gasser, R.B., Defining the Schistosoma haematobium kinome enables the prediction of essential kinases as anti-schistosome drug targets. Sci. Rep., 5, 2015, 17759.
46. Thompson, J.D., Higgins, D.G., Gibson, T.J., CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:22 (1994), 4673–4680.
47. Thor, S.W., Hilt, D.A., Kissinger, J.C., Paterson, A.H., Jackwood, M.W., Recombination in avian gamma-coronavirus infectious bronchitis virus. Viruses 3:9 (2011), 1777–1799.
48. Untergasser, A., Cutcutache, I., Koressaar, T., Ye, J., Faircloth, B.C., Remm, M., Rozen, S.G., Primer3—new capabilities and interfaces. Nucl. Acids Res., 40(15), 2012 (e115-e115).
49. Wadey, C.N., Faragher, J.T., Australian infectious bronchitis viruses: identification of nine subtypes by a neutralisation test. Res. Vet. Sci. 30 (1981), 70–74.