Molecular-genetic characterization of Avian avulavirus 20 strains isolated from wild birds

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Abstract

Introduction. Previously unknown paramyxovirus strains were isolated from wild birds in 2013-2014 in Kazakhstan and subsequently identified as representatives of the novel Avian avulavirus 20 species. The aims and tasks were molecular genetic characterization of novel avulaviruses and investigation of their phylogenetic relationships.

Material and methods. Embryonated chicken eggs were inoculated with cloacal and tracheal swabs from wild birds with subsequent virus isolation. The complete nucleotide sequences of viral genomes were obtained by massive parallel sequencing with subsequent bioinformatics processing.

Results. By initial infection of chicken embryos with samples from 179 wild birds belonging to the Anatidae, Laridae, Scolopacidae and Charadriidae families, 19 hemagglutinating agents were isolated, and five of them were identified as representatives of new viral species. The study of their sequenced genomes revealed their similarity in size, but there was a significant genetic variability within the species. 2,640 nucleotide substitutions were identified and 273 of them were non-synonymous, influencing the protein structure of viruses. It was shown that isolates Avian avulavirus 20/black-headed gull/ Balkhash/5844/2013 and Avian avulavirus 20 /great black-headed gull/Atyrau/5541/2013 were 86% and 95% respectively identical to the previously described reference strain, indicating a significant evolutionary divergence within species.

Discussion. The authors suggest the existence of two independent lineages - the Caspian, represented by the reference strain Aktau/5976 and Atyrau/5541, as well as the second, geographically significantly distant Balkhash lineage.

Conclusion. The study confirms the role of the birds of the Laridae family as the main reservoir of Avian avulavirus 20 in the avifauna that plays a key role in maintaining viruses of the genus Avulavirus in the biosphere and is a potential natural source for the emergence of new viral variants. Continuous surveillance of them in the wild is one of the most important tasks in ensuring the safety of the poultry industry.

About the authors

K. O. Karamendin

SPC for Microbiology and Virology

Author for correspondence.
Email: kobey.karamendin@gmail.com
ORCID iD: 0000-0003-0829-3330

Kobey O. Karamendin - PhD, DVM, Leading researcher, Laboratory of Viral Ecology.

Almaty, 050010.

Казахстан

M. Kh. Sayatov

SPC for Microbiology and Virology

Email: fake@neicon.ru
ORCID iD: 0000-0003-4740-9156

Almaty, 050010.

Казахстан

A. I. Kydyrmanov

SPC for Microbiology and Virology

Email: fake@neicon.ru
ORCID iD: 0000-0002-8374-6128

Almaty, 050010.

Казахстан

E. T. Kasymbekov

SPC for Microbiology and Virology

Email: fake@neicon.ru
ORCID iD: 0000-0002-8773-4984

Almaty, 050010.

Казахстан

S. E. Asanova

SPC for Microbiology and Virology

Email: fake@neicon.ru
ORCID iD: 0000-0002-7259-5539

Almaty, 050010.

Казахстан

K. D. Daulbayeva

SPC for Microbiology and Virology

Email: fake@neicon.ru
ORCID iD: 0000-0001-5618-3385

Almaty, 050010.

Казахстан

E. Ya. Khan

SPC for Microbiology and Virology

Email: fake@neicon.ru
ORCID iD: 0000-0002-6279-3419

Almaty, 050010.

Казахстан

References

  1. Alexander D.J. Newcastle disease, other avian paramyxoviruses, and pneumovirus infections. In: Diseases of Poultry. Ames, IA, USA: Iowa State Press; 2003.
  2. Saif Y.M., Mohan R., Ward L., Senne D.A., Panigrahy B., Dearth R.N. Natural and experimental infection of turkeys with avian paramyxovirus-7. Avian Dis. 1997; 41(2): 326-9.
  3. Alexander D.J. Newcastle disease and other avian paramyxoviridae infections. In: Diseases of Poultry. Ames, IA, USA: Iowa State Press; 1997.
  4. Jung A., Grund C., Muller I., Rautenschlein S. Avian paramyxovirus serotype 3 infection in Neopsephotus, Cyanoramphus, and Neophema species. J. Avian Med. Surg. 2009; 23(3): 205-8. Doi: https://doi.org/10.1647/2008-022.1
  5. Nerome K., Nakayama M., Ishida M., Fukumi H. Isolation of a new avian paramyxovirus from budgerigar (Melopsittacus undulatus). J. Gen. Virol. 1978; 38(2): 293-301. Doi: https://doi.org/10.1099/0022-1317-38-2-293
  6. Gough R.E., Alexander D.J. Avian paramyxovirus type 4 isolated from a ringed teal (Calonetta leucophrys). Vet. Rec. 1984; 115(25-26): 653. Doi: https://doi.org/10.1136/vr.115.25-26.653
  7. Stallknecht D.E., Senne D.A., Zwank PJ., Shane S.M., Kearney M.T. Avian paramyxoviruses from migrating and resident ducks in coastal Louisiana. J. Wildl. Dis. 1991; 27(1): 123-8. Doi: https://doi.org/10.7589/0090-3558-27.1.123
  8. Alexander D.J., Hinshaw V.S., Collins M.S., Yamane N. Characterization of viruses which represent further distinct serotypes (PMV-8 and PMV-9) of avian paramyxoviruses. Arch. Virol. 1983; 78(1-2): 29-36. Doi: https://doi.org/10.1007/bf01310856
  9. Stanislawek W.L., Wilks C.R., Meers J., Horner G.W., Alexander D.J., Manvell R.J., et al. Avian paramyxoviruses and influenza viruses isolated from mallard ducks (Anas platyrhynchos) in New Zealand. Arch. Virol. 2002; 147(7): 1287-302. Doi: https://doi.org/10.1007/s00705-002-0818-2
  10. Turek R., Gresikova M., Thmova B. Isolation of influenza A virus and paramyxoviruses from sentinel domestic ducks. Acta Virol. 1984; 28(2): 156-8.
  11. Chang PC., Hsieh M.L., Shien J.H., Graham D.A., Lee M.S., Shieh H.K. Complete nucleotide sequence of avian paramyxovirus type 6 isolated from ducks. J. Gen. Virol. 2001; 82(Pt. 9): 2157-68. Doi: https://doi.org/10.1099/0022-1317-82-9-2157
  12. Miller P.J., Afonso C.L., Spackman E., Scott M.A., Pedersen J.C., Senne D.A., et al. Evidence for a new avian paramyxovirus serotype 10 detected in rockhopper penguins from the Falkland Islands. J. Virol. 2010; 84(21): 11496-504. Doi: https://doi.org/10.1128/JVI.00822-10
  13. Briand F.X., Henry A., Massin P, Jestin V. Complete genome sequence of a novel avian paramyxovirus. J. Virol. 2012; 86(14): 7710. Doi: https://doi.org/10.1128/JVI.00946-12
  14. Terregino C., Aldous E.W., Heidari A., Fuller C.M., De Nardi R., Manvell R.J., et al. Antigenic and genetic analyses of isolate APMV/wigeon/ Italy/3920-1/2005 indicate that it represents a new avian paramyxovirus (APMV-12). Arch. Virol. 2013; 158(11): 2233-43. Doi: https://doi.org/10.1007/s00705-013-1735-2
  15. Yamamoto E., Ito H., Tomioka Y, Ito T. Characterization of novel avian paramyxovirus strain APMV/Shimane67 isolated from migratory wild geese in Japan. J. Vet. Med. Sci. 2015; 77(9): 1079-85. Doi: https://doi.org/10.1292/jvms.14-0529
  16. Karamendin K., Kydyrmanov A., Seidalina A., Asanova S., Sayatov M., Kasymbekov E., et al. Complete genome sequence of novel avian paramyxovirus (APMV-13) isolated from a wild bird in Kazakhstan. Genome Announc. 2016; 4(3): pii e00167-16. Doi: https://doi.org/10.1128/genomeA.00167-16
  17. Goraichuk I., Sharma P., Stegniy B., Muzyka D., Pantin-Jackwood M.J., Gerilovych A., et al. Complete genome sequence of an avian paramyxovirus representative of putative new serotype 13. Genome Announc. 2016; 4(4): pii e00729-16. Doi: https://doi.org/10.1128/genomeA.00729-16
  18. Thampaisarn R., Bui V.N., Trinh D.Q., Nagai M., Mizutani T., Omatsu T., et al. Characterization of avian paramyxovirus serotype 14 a novel serotype isolated from a duck fecal sample in Japan. Virus Res. 2017; 228: 46-57. Doi: https://doi.org/10.1016/j.virusres.2016.11.018
  19. Lee H.J., Kim J.Y., Lee Y.J., Lee E.K., Song B.M., Lee H.S., et al. Novel Avian Paramyxovirus (Putative Serotype 15) Isolated from Wild Birds. Front. Microbiol. 2017; 8: 786. Doi: https://doi.org/10.3389/fmicb.2017.00786
  20. Thomazelli L.M., de Araujo J., Fabrizio T., Walker D., Reischak D., Ometto T., et al.
  21. Novel avian paramyxovirus (APMV-15) isolated from a migratory bird in South America. PLoS One. 2017; 12(5): e0177214. Doi: https://doi.org/10.1371/journal.pone.0177214
  22. Neira V, Tapia R., Verdugo C., Barriga G., Mor S., Ng T.F.F., et al. Novel Avulaviruses in Penguins Antarctica. Emerg. Infect. Dis. 2017; 23(7): 1212-4. Doi: https://doi.org/10.3201/eid2307.170054
  23. Karamendin K., Kydyrmanov A., Kasymbekov Y., Asanova S., Daulbayeva K., Seidalina A., et al. Novel avian paramyxovirus isolated from gulls in Caspian seashore in Kazakhstan. PLoS One. 2017; 12(12): e0190339. Doi: https://doi.org/10.1371/journal.pone.0190339
  24. Manual of diagnostic tests and vaccines for terrestrial animals. Avian influenza. Available at: https://www.oie.int/en/standard-setting/terrestrial-manual/access-online/
  25. WHO Manual on Animal Influenza Diagnosis and Surveillance. Available at: http://www.wpro.who.int/emerging_diseases/documents/docs/manualonanimalaidiagnosisandsurveillance.pdf
  26. Tong S., Chern S.W., Li Y., Pallansch M., Anderson L.J. Sensitive and Broadly Reactive Reverse Transcription-PCR Assays to Detect Novel Paramyxoviruses. J. Clin. Microbiol. 2008; 46(8): 2652-8. Doi: https://doi.org/10.1128/JCM.00192-08
  27. Nei M., Kumar S. Molecular Evolution and Phylogenetics. New York: Oxford University Press; 2000.
  28. Morgan E.M. Evolutionary relationships of paramyxovirus nucleocapsid-associated proteins. In: Kingsbury D.W., ed. The Paramyxoviruses. New York: Plenum Press; 1991: 163-79.
  29. Paldurai A., Subbiah M., Kumar S., Collins PL., Samal S.K. Complete genome sequences of avian paramyxovirus type 8strains goose/ Delaware/1053/76 and pintail/Wakuya/20/78. Virus Res. 2009; 142(1-2): 144-53. Doi: https://doi.org/10.1016/j.virusres.2009.02.003
  30. Xiao S., Subbiah M., Kumar S., De Nardi R., Terregino C., Collins P.L., et al. Complete genome sequences of avian paramyxovirus serotype 6 prototype strain Hong Kong and a recent novel strain from Italy: evidence for the existence of subgroups within the serotype. Virus Res. 2010; 150(1-2): 61-72. Doi: https://doi.org/10.1016/j.virusres.2010.02.015
  31. The Checklist of the Birds of Kazakhstan. Available at: http://www.birds.kz/v2checklist.php?l=en
  32. Karamendin K., Kydyrmanov A., Seidalina A., Asanova S., Daulbayeva K., Kasymbekov E., et al. Circulation of avian paramyxoviruses in wild birds of Kazakhstan in 2002-2013. Virol. J. 2016; 13: 23. Doi: https://doi.org/10.1186/s12985-016-0476-8
  33. Полный список видов птиц Казахстана. Available at: http://www.birds.kz/v2checklist.php?l=ru
  34. Bogoyavlenskiy A., Beresin V., Prilipov A., Usachev E., Lyapina O., Levandovskaya S., et al. Molecular Characterization of Virulent Newcastle Disease Virus Isolates from Chickens during the 1998 NDV Outbreak in Kazakhstan. Virus Genes. 2000; 31(1): 13-20. Doi: https://doi.org/10.1007/s11262-004-2195-2
  35. Bogoyavlenskiy A., Beresin V., Prilipov A., Usachev E., Lyapina O., Korotetskiy I., et al. Newcastle disease outbreaks in Kazakhstan and Kyrgyzstan during 1998, 2000, 2001, 2003, 2004 and 2005 were caused by viruses of the genotypes VIIb and VIId. Virus Genes. 2009; 39(1): 94-101. Doi: https://doi.org/10.1007/s11262-009-0370-1
  36. Korotetskiy I.S., Bogoyavlenskiy A.P., Prilipov A.G., Usachev E.V., Usacheva O.V., Turmagambetova A.S., et al. Molecular genetic characteristics of cyclic isolates of the Newcastle disease virus isolated on the territory of the Russian Federation, Ukraine, Kazakhstan, and Kyrgyzstan. Voprosy virusologii. 2010; 55(4): 25-9. (in Russian)
  37. Bogoyavlenskiy A., Beresin V., Prilipov A., Usachev E., Korotetskiy I., Zaitceva I., et al. Characterization of Pigeon Paramyxoviruses (Newcastle disease virus) Isolated in Kazakhstan in 2005. Virol. Sin. 2012; 27(2): 93-9. Doi: https://doi.org/10.1007/s12250-012-3234-0
  38. Коротецкий И.С., Богоявленский А.П., Прилипов А.Г., Усачев Е.В., Усачева О.В., Турмагамбетова А.С. и др. Молекулярно-генетическая характеристика велогенных изолятов вируса болезни Ньюкасла, выделенных на территории Российской Федерации, Украины, Казахстана и Киргизии. Вопросы вирусологии. 2010; 55(4): 25-9.
  39. Munir M., Linde A.M., Zohari S., Stahl K., Baule C., Engstrom B., et al. Whole genome sequencing and characterization of a virulent Newcastle disease virus isolated from an outbreak in Sweden. Virus Genes. 2011; 43(2): 261-71. Doi: https://doi.org/10.1007/s11262-011-0636-2
  40. Shengqing Y., Kishida N., Ito H., Kida H., Otsuki K., Kawaoka Y., et al. Generation of velogenic Newcastle disease viruses from a nonpathogenic waterfowl isolate by passaging in chickens. Virology. 2002; 301(2): 206-11. Doi: https://doi.org/10.1006/viro.2002.1539

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Copyright (c) 2019 Karamendin K.O., Sayatov M.K., Kydyrmanov A.I., Kasymbekov E.T., Asanova S.E., Daulbayeva K.D., Khan E.Y.

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