Skip to main content

Advertisement

Log in

Molecular characterization of the S1 gene in GI-17 and GI-13 type isolates of avian infectious bronchitis virus (IBV) in Costa Rica, from 2016 to 2019

  • Original Article
  • Published:
VirusDisease Aims and scope Submit manuscript

Abstract

Avian infectious bronchitis is one of the most important respiratory diseases affecting poultry production worldwide. The etiological agent of this disease is the avian infectious bronchitis virus (IBV). We analyzed 14 isolates of IBV obtained from poultry farms in Costa Rica, from 2016 through 2019. We sequenced the S1 region of the genome and the sequences obtained were submitted to GenBank. Phylogenetic analyses showed that the isolates obtained during 2016–2017 belong to the GI-17 lineage and are related to the Georgia 13-type Ga-13/14255/14 and CK/CR/1160/16 variants, with a 96.90–100% nucleotide sequence identity and a 92.25–100% amino acid sequence identity. The main differences were detected in the RBD and HVR-3 regions, where a series of mutations eliminate an N-glycosylation site in 10 out of 11 isolates. The isolates obtained during 2018–2019 belong to the GI-13 lineage and are closely related to the 4/91 vaccine variant, with over 98% sequence identity at the nucleotide and amino acids levels. Variations were detected in the RBD and HVR regions, with a possible N-glycosylation site detected in isolate CK/CR/0632/19. These results indicate that a GA13-like pathogenic variant circulated during the 2016–2017 period and that the 4/91 variant was detected after the introduction of the vaccine. The variations shown in both the GA13-like and 4/91 isolates examined, reveal the need for continuous surveillance of IBV in Costa Rica, to detect new variants that may be introduced to the country or develop during outbreaks. This information is highly relevant for vaccination planning and disease management programs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

the S1 gene sequences obtained from the 14 isolates were uploaded in the genbank database under the accession number MT230562, MT230563, MT230564, MT230565, MT230566, MT230567, MT230568, MT230569, MT230570, MT230571, MT230572, MT230573, MT230574, and MT230575.

Abbreviations

4/91-CR:

4/91 Variant from Costa Rica

BHI:

Brain Heart Infusion Broth

GI-13:

Genotype 1 lineage 13

GI-17:

Genotype 1 lineage 17

GA13:

Georgia 13 variant

GA13-CR:

Georgia 13 variant from Costa Rica

HVR:

Hypervariable region

HVR-1:

Hypervariable region 1

HVR-2:

Hypervariable region 2

HVR-3:

Hypervariable region 3

IBV:

Avian infectious bronchitis virus

LANASEVE:

Laboratorio Nacional de Servicios Veterinarios

RBD:

Receptor-binding domain

SENASA:

Servicio Nacional de Salud Animal (National Service of Animal Health)

SPF:

Specific pathogen free

SPR:

Subtree-Pruning-Regrafting

References

  1. Abozeid HH, Paldurai A, Khattar SK, Afifi MA, El-Kady MF, El-Deeb AH, et al. Complete genome sequences of two avian infectious bronchitis viruses isolated in Egypt: evidence for genetic drift and genetic recombination in the circulating viruses. Infect Genet Evol. 2017;53:7–14.

    Article  CAS  PubMed  Google Scholar 

  2. Abro SH, Ullman K, Belák S, Baule C. Bioinformatics and evolutionary insight on the spike glycoprotein gene of QX-like and Massachusetts strains of infectious bronchitis virus. Virol J. 2012;9:1–9.

    Article  CAS  Google Scholar 

  3. Bande F, Arshad SS, Hair Bejo M, Moeini H, Omar AR. Progress and challenges toward the development of vaccines against avian infectious bronchitis. J Immunol Res. 2015;2015:12.

    Article  Google Scholar 

  4. Bande F, Arshad SS, Omar AR, Bejo MH, Abubakar MS, Abba Y. Pathogenesis and diagnostic approaches of avian infectious bronchitis. Adv Virol. 2016;2016:1–11.

    Google Scholar 

  5. Bande F, Arshad SS, Omar AR, Hair-Bejo M, Mahmuda A, Nair V. Global distributions and strain diversity of avian infectious bronchitis virus: a review. Anim Heal Res Rev. 2017;18:70–83.

    Article  Google Scholar 

  6. Belouzard S, Millet JK, Licitra BN, Whittaker GR. Mechanisms of coronavirus cell entry mediated by the viral spike protein. Viruses. 2012;4:1011–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bhuiyan MSA, Amin Z, Bakar AMSA, Saallah S, Yusuf NHM, Shaarani SM, et al. Factor influences for diagnosis and vaccination of avian infectious bronchitis virus (Gammacoronavirus) in chickens. Vet Sci. 2021;8:47.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Binns MM, Boursnell ME, Cavanagh D, Pappin DJ, Brown TDK. Cloning and sequencing of the gene encoding the spike protein of the coronavirus IBV. J Gen Virol. 1985;66:719–26.

    Article  CAS  PubMed  Google Scholar 

  9. Bouwman KM, Parsons LM, Berends AJ, De Vries RP, Cipollo JF, Verheije MH. Three amino acid changes in avian coronavirus spike protein allow binding to kidney tissue. J Virol. 2020;94:e01363-1419.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Carstens EB. Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2009). Arch Virol. 2010;155:133–46.

    Article  CAS  PubMed  Google Scholar 

  11. Cavanagh D. Coronavirus avian infectious bronchitis virus. Vet Resarch. 2007;38:281–97.

    Article  CAS  Google Scholar 

  12. Cavanagh D, Gelb J. Infectious Bronchitis. In: Saif YM, Fadly AM, Glisson JR, McDougald LR, Nolan L, Swayne DE, editors. Dis Poult. 12th ed. Iowa, USA: Blackwell Publishing; 2008. p. 117–36.

    Google Scholar 

  13. Chu VC, McElroy LJ, Chu V, Bauman BE, Whittaker GR. The avian coronavirus infectious bronchitis virus undergoes direct low-pH-dependent fusion activation during entry into host cells. J Virol. 2006;80:3180–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. de Wit JJ, Cook JKA. Factors influencing the outcome of infectious bronchitis vaccination and challenge experiments. Avian Pathol. 2014;43:485–97.

    Article  PubMed  CAS  Google Scholar 

  15. de Fraga AP, Gräf T, Pereira CS, Ikuta N, Fonseca AS, Kazantzi F, et al. Phylodynamic analysis and molecular diversity of the avian infectious bronchitis virus of chickens in Brazil. Infect Genet Evol. 2018;61:77–83.

    Article  PubMed  PubMed Central  Google Scholar 

  16. de Wit JJ, Cook JK, van der Heijden HM. Infectious bronchitis virus variants: a review of the history, current situation and control measures. Avian Pathol. 2011;40:223–35.

    Article  Google Scholar 

  17. Durães-Carvalho R, Caserta LC, Barnabé AC, Martini MC, Simas PV, Santos MM, et al. Phylogenetic and phylogeographic mapping of the avian coronavirus spike protein-encoding gene in wild and synanthropic birds. Virus Res. 2015;201:101–12.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Gallardo RA, Van Santen VL, Toro H. Host intraspatial selection of infectious bronchitis virus populations. Avian Dis. 2010;54:807–13.

    Article  PubMed  Google Scholar 

  19. Gelb J Jr, Weisman Y, Ladman BS, Meir R. S1 gene characteristics and efficacy of vaccination against infectious bronchitis virus field isolates from the United States and Israel (1996 to 2000). Avian Pathol. 2005;34:194–203.

    Article  CAS  PubMed  Google Scholar 

  20. Gong H, Ni R, Qiu R, Wang F, Yan W, Wang K, et al. Evaluation of a novel recombinant strain of infectious bronchitis virus emerged from three attenuated live vaccine strains. Microb Pathog. 2022;164:105437.

    Article  CAS  PubMed  Google Scholar 

  21. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21.

    Article  CAS  PubMed  Google Scholar 

  22. Guzman M, Hidalgo H. Live attenuated infectious bronchitis virus vaccines in poultry: modifying local viral populations dynamics. Animals. 2020;10:2058.

    Article  PubMed Central  Google Scholar 

  23. Guzman M, Sáesnz L, Hidalgo H. Molecular and antigenic characterization of GI-13 and GI-16 avian infectious bronchitis virus isolated in Chile from 2009 to 2017 regarding 4/91 vaccine introduction. Animals. 2019;9:656.

    Article  PubMed Central  Google Scholar 

  24. Han Z, Zhang T, Xu Q, Gao M, Chen Y, Wang Q, et al. Altered pathogenicity of a tl/CH/LDT3/03 genotype infectious bronchitis coronavirus due to natural recombination in the 5’- 17 kb region of the genome. Virus Res. 2016;213:140–8.

    Article  CAS  PubMed  Google Scholar 

  25. Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–5.

    Article  CAS  PubMed  Google Scholar 

  26. Ignjatović J, Sapats S. Avian infectious bronchitis virus. Rev Sci Tech Int des Epizoot. 2000;19:493–508.

    Article  Google Scholar 

  27. Jackwood MW. Impact of respiratory diseases with special emphasis to emerging infectious bronchitis virus. Proc sixty-fifth West Poult Dis Conf. 2016;116–7.

  28. Jackwood MW, Jordan BJ. Molecular evolution of infectious bronchitis virus and the emergence of variant viruses circulating in the United States. Avian Dis. 2021;65:629–34.

    Article  Google Scholar 

  29. Jiménez C, Cortés R, Ramírez M, Prendas J, Arrieta E, Lindahl J, et al. Diagnosis and epidemiology of IBV infections in Costa Rica. IV Symp Avian Corona-and Pneumovirus Infect Rauischholzhausen, Ger 20-23. 2004;39–49.

  30. Johnson FB. Transport of viral specimens. Clin Microbiol Rev. 1990;3:120–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Kamble NM, Pillai AS, Gaikwad SS, Shukla SK, Khulape SA, Dey S, et al. Evolutionary and bioinformatic analysis of the spike glycoprotein gene of H120 vaccine strain protectotype of infectious bronchitis virus from India. Biotechnol Appl Biochem. 2016;63:106–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Kasem S, Abdel-Kader A, Tahoon A, Shaban H. Phylogentic analysis of recent infectious bronchitis virus isolates from broiler chicken farms in Kafrelsheikh. Egypt Beha Vet Med J. 2015;29:189–95.

    Google Scholar 

  33. Koch G, Kant A, Cook JK, Cavanagh D. Epitopes of neutralizing antibodies are localized within three regions of the S1 spike protein of infectious bronchitis virus. Second Int Symp Infect Bronchitis, World Vet Poult Assoc Rauischholzhausen. 1991;154–60.

  34. Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B. Partitionfinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol. 2016;34:772–3.

    Google Scholar 

  35. Legnardi M, Tucciarone CM, Franzo G, Cecchinato M. Infectious bronchitis virus evolution, diagnosis and control. Vet Sci. 2020;7:79.

    Article  PubMed Central  Google Scholar 

  36. Leow BL, Syamsiah Aini S, Faizul Fikri MY, Muhammad Redzwan S, Khoo CK, Ong GH, et al. Molecular characterization of avian infectious bronchitis virus isolated in Malaysia during 2014–2016. Trop Biomed. 2018;35:1092–106.

    CAS  PubMed  Google Scholar 

  37. Leyson C, França M, Jackwood M, Jordan B. Polymorphisms in the S1 spike glycoprotein of Arkansas-type infectious bronchitis virus ( IBV ) show differential binding to host tissues and altered antigenicity. Virology. 2016;498:218–25.

    Article  CAS  PubMed  Google Scholar 

  38. Lindahl J. Infectious bronchitis virus and infectious bursal disease virus; a study performed at the Universidad Nacional of Costa Rica Sveriges lantbruksuniv. (Doctoral dissertation, Sveriges lantbruksuniv); 2004.

  39. Loomis LN, Cunningham CH, Gray ML, Thorp F Jr. Pathology of the chicken embryo infected with infectious bronchitis virus. Am J Vet Res. 1950;11:245–51.

    CAS  PubMed  Google Scholar 

  40. Mahmood ZH, Sleman RR, Uthman AU. Isolation and molecular characterization of Sul/01/09 avian infectious bronchitis virus, indicates the emergence of a new genotype in the Middle East. Vet Microbiol. 2011;150:21–7.

    Article  CAS  PubMed  Google Scholar 

  41. . Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. 2010 Gatew Comput Environ Work. IEEE; 2010;1–8

  42. Moore KM, Jackwood MW, Hilt DA. Identification of amino acids involved in a serotype and neutralization specific epitope within the s1 subunit of avian infectious bronchitis virus. Arch Virol. 1997;142:2249–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Nafaji H, Langeroudi AG, Hashemzadeh M, Karimi V, Madagar O, Ghafouri SA, et al. Molecular characterization of infectious bronchitis viruses isolated from broiler chicken farms in Iran, 2014–2015. Arch Virol. 2016;161:53–62.

    Article  CAS  Google Scholar 

  44. Naguib MM, Höper D, Arafa A, Setta AM, Abed M, Monne I, et al. Full genome sequence analysis of a newly emerged QX-like infectious bronchitis virus from Sudan reveals distinct spots of recombination. Infect Genet Evol. 2016;46:42–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Parsons LM, Bouwman KM, Azurmendi H, De Vries RP, Cipollo JF, Verheije MH. Glycosylation of the viral attachment protein of avian coronavirus is essential for host cell and receptor binding. J Biol Chem. 2019;294:7797–809.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Promkuntod N, van Eijndhoven REW, de Vrieze G, Gröne A, Verheije MH. Mapping of the receptor-binding domain and amino acids critical for attachment in the spike protein of avian coronavirus infectious bronchitis virus. Virology. 2014;448:26–32.

    Article  CAS  PubMed  Google Scholar 

  47. Roman T, Silva M, Barbosa J, Gómez L, Hernandez D, Zamora R, et al. Effectiveness of a vaccine program based on the Protectotype® concept against an infectious bronchitis variant virus strain challenge (GA13) in Costa Rica. Proccedings Am Assoc Avian Pathol Annu Meet, 2018, Denver, Color EEUU. 2018;3.

  48. Sela I, Ashkenazy H, Katoh K, Pupko T. GUIDANCE2: accurate detection of unreliable alignment regions accounting for the uncertainty of multiple parameters. Nucleic Acids Res. 2015;43:W7-14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Shan D, Fang S, Han Z, Ai H, Zhao W, Chen Y, et al. Effects of hypervariable regions in spike protein on pathogenicity, tropism, and serotypes of infectious bronchitis virus. Virus Res. 2018;250:104–13.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Shimazaki Y, Watanabe Y, Harada M, Seki Y, Kuroda Y, Fukuda M, et al. Genetic analysis of the S1 gene of 4/91 type infectious bronchitis virus isolated in Japan. J Vet Med Sci. 2009;71:583–8.

    Article  CAS  PubMed  Google Scholar 

  51. Smati R, Silim A, Guertin C, Henrichon M, Marandi M, Arella M, et al. Molecular characterization of three new avian infectious bronchitis virus (IBV) strains isolated in Quebec. Virus Genes. 2002;25:85–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Sumi V, Singh SD, Dhama K, Gowthaman V, Barathidasan R, Sukumar K. Isolation and molecular characterization of infectious bronchitis virus from recent outbreaks in broiler flocks reveals emergence of novel strain in India. Trop Anim Health Prod. 2012;44:1791–5.

    Article  PubMed  Google Scholar 

  53. Thiel V, Siddell SG. Reverse genetics of coronaviruses using vaccinia vectors. In: Enjuanes L, editor. Coronavirus replication reverse genet. Berlin: Heidelberg; 2005. p. 199–227.

    Chapter  Google Scholar 

  54. Umar S, Shah MAAA, Munir MT, Ahsan U, Kaboudi K. Infectious bronchitis virus: evolution and vaccination. Worlds Poult Sci J. 2016;72:49–60.

    Article  Google Scholar 

  55. Valastro V, Holmes EC, Britton P, Fusaro A, Jackwood MW, Cattoli G, et al. S1 gene-based phylogeny of infectious bronchitis virus: an attempt to harmonize virus classification. Infect Genet Evol. 2016;39:349–64.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Van Limbergen T, Dewulf J, Klinkenberg M, Ducatelle R, Gelaude P, Méndez J, et al. Scoring biosecurity in European conventional broiler production. Poult Sci. 2018;97:74–83.

    Article  PubMed  Google Scholar 

  57. Vasfi Marandi M, Malekan M, Ranjbar MM, Dadashpour Davachi N, Alamian S. Sequencing and in silico multi-aspect analysis of S1 glycoprotein in 793/B serotype of infectious bronchitis virus isolated from in 2003 and 2011. Arch Razi Inst. 2018;73:183–98.

    CAS  PubMed  Google Scholar 

  58. Villalobos-Agüero RA, Ramírez-Carvajal L, Zamora-Sanabria R, León-Rodríguez B, Karkashian-Córdoba J. Molecular characterization of an avian GA13-like Infectious bronchitis virus full-length genome from Costa Rica. VirusDisease. 2021;32:347–53.

    Article  PubMed Central  Google Scholar 

  59. Villareal LYB, Sandri TL, Souza SP, Richtzenhain L, de Wit JJ, Brandao PE. Molecular epidemiology of avian infectious bronchitis in brazil from 2007 to 2008 in breeders, broilers, and layers. Avian Dis. 2010;54:894–8.

    Article  Google Scholar 

  60. Villegas P. Viral diseases of the respiratory system. Poult Sci. 1998;77:1143–5.

    Article  CAS  PubMed  Google Scholar 

  61. Wickramasinghe IN, de Vries RP, Grone A, de Haan CA, Verheije MH. Binding of avian coronavirus spike proteins to host factors reflects virus tropism and pathogenicity. J Virol. 2011;85:8903–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Youn SY, Lee JY, Bae YC, Kwon YK, Kim HR. Genetic and pathogenic characterization of QX(GI-19)-recombinant infectious bronchitis viruses in South Korea. Viruses. 2021;13.

  63. Zanaty A, Naguib MM, El-Husseiny MH, Mady W, Hagag N, Arafa AS. The sequence of the full spike S1 glycoprotein of infectious bronchitis virus circulating in Egypt reveals evidence of intra-genotypic recombination. Arch Virol. 2016;161:3583–7.

    Article  CAS  PubMed  Google Scholar 

  64. Zhang Y, Wang HN, Wang T, Fan WQ, Zhang AY, Wei K, et al. Complete genome sequence and recombination analysis of infectious bronchitis virus attenuated vaccine strain H120. Virus Genes. 2010;41:377–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Zhang X, Deng T, Lu J, Zhao P, Chen L, Qian M, et al. Molecular characterization of variant infectious bronchitis virus in China, 2019: Implications for control programmes. Transbound Emerg Dis. 2020;67:1349–55.

    Article  CAS  PubMed  Google Scholar 

  66. Zhao Y, Liu XY, Cheng JL, Wu YP, Zhang GZ. Molecular characterization of an infectious bronchitis virus strain isolated from northern China in 2012. Arch Virol. 2014;159:3457–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was funded by “Fundación para el Fomento y Promoción de la Investigación y Transferencia de Tecnología Agropecuaria” (FITACORI), Costa Rica, grant number 3-006-115123, and by the “Vicerrectoría de Investigación” and “Sistema de Estudios de Posgrado”, University of Costa Rica.

Funding

The fundings of the study was provided by “Fundación para el Fomento y Promoción de la Investigación y Transferencia de Tecnología Agropecuaria” (FITACORI), Costa Rica, grant number 3-006-115123, and by the “Vicerrectoría de Investigación” and “Sistema de Estudios de Posgrado”, University of Costa Rica.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ricardo A. Villalobos-Agüero.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

All procedures performed in animals were in accordace with the ethical standards of the “Comité Institucional de Cuido y Uso de Animales” (CICUA) of the University of Costa Rica.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 1324 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Villalobos-Agüero, R.A., León, B., Zamora-Sanabria, R. et al. Molecular characterization of the S1 gene in GI-17 and GI-13 type isolates of avian infectious bronchitis virus (IBV) in Costa Rica, from 2016 to 2019. VirusDis. 33, 84–95 (2022). https://doi.org/10.1007/s13337-022-00762-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13337-022-00762-2

Keywords

Navigation