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Вопросы вирусологии. 2019; 64: 185-192

Молекулярно-генетическая характеристика штаммов Avian avulavirus 20, выделенных от диких птиц

Карамендин К. О., Саятов М. Х., Кыдырманов А. И., Касымбеков Е. Т., Асанова С. Е., Даулбаева К. Д., Хан Е. Я.

https://doi.org/10.36233/0507-4088-2019-64-4-185-192

Аннотация

Введение. В 2013-2014 гг. на территории Казахстана от диких птиц были выделены ранее не описанные в науке штаммы парамиксовирусов, впоследствии идентифицированные как представители нового вида - Avian avulavirus 20.

Цель и задачи исследований заключались в молекулярно-генетической характеристике изолятов новых авулавирусов и определении их филогенетических взаимоотношений.

Материал и методы. Биологическими образцами в виде клоакальных и трахеальных смывов от диких птиц заразили развивающиеся куриные эмбрионы с последующим выделением культуры вирусов. Полные нуклеотидные последовательности геномов вирусов получены методом массового параллельного секвенирования нуклеиновых кислот вирусов с биоинформационной обработкой результатов.

Результаты. При первичном заражении куриных эмбрионов пробами от 179 диких птиц, относящихся к семействам утиные, чайковые, бекасовые и ржанковые, выделены 19 гемагглютинирующих агентов, из которых 5 впоследствии оказались представителями новых видов парамиксовирусов. Исследование секвенированных последовательностей их геномов выявило их идентичность по размерам, но значительную генетическую вариабельность внутри вида. Выявлены 2640 нуклеотидных замен, из них 273 оказались несинонимическими, т.е. оказывали влияние на белковую структуру вирусов. Показано, что изоляты Avian avulavirus 20/озёрная чайка/Балхаш/5844/2013 и Avian avulavirus 20/черноголовый хохотун/Атырау/5541/2013 оказались на 86 и 95% соответственно идентичны ранее описанному референсному штамму, что свидетельствует о значительной эволюционной дивергенции внутри вида. обсуждение. Авторы предполагают существование двух независимых линий - Каспийской, представленной референсным Актау/5976 и Атырау/5541, а также географически значительно отдалённой Балхашской линии. Заключение. Проведённые исследования подтверждают, что птицы семейства чайковые являются основным резервуаром Avian avulavirus 20 в орнитофауне, играют ключевую роль в поддержании авулавирусов в биосфере и представляют потенциальный источник возникновения новых вариантов. Непрерывное наблюдение за ними в дикой природе - одна из важнейших задач при обеспечении безопасности птицеводства.

Список литературы

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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

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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

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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

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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

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Problems of Virology. 2019; 64: 185-192

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

Karamendin K. O., Sayatov M. Kh., Kydyrmanov A. I., Kasymbekov E. T., Asanova S. E., Daulbayeva K. D., Khan E. Ya.

https://doi.org/10.36233/0507-4088-2019-64-4-185-192

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.

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

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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

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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

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