Advertisement

Divergent coronaviruses detected in wild birds in Brazil, including a central park in São Paulo

  • Carla M. Barbosa
  • Edison L. Durigon
  • Luciano M. Thomazelli
  • Tatiana Ometto
  • Roberta Marcatti
  • Marcello Shiavo Nardi
  • Daniel M. de Aguiar
  • João Batista Pinho
  • Maria Virginia Petry
  • Isaac Simão Neto
  • Patrícia Serafini
  • Roberta Costa Rodrigues
  • Severino Mendes de Azevedo Junior
  • Luiz Gustavo B. Góes
  • Jansen de AraujoEmail author
Veterinary Microbiology - Research Paper
  • 1 Downloads

Abstract

Coronaviruses are single-stranded positive-sense RNA viruses associated with important avian diseases. Their relatively high rates of mutation and recombination frequencies allow them to adapt to new hosts and ecological niches. Although Brazil has 18% of global avian species diversity, studies regarding the presence of avian viral diseases in wild birds in South America are scarce. In this study, we performed a retrospective analysis of the presence of CoVs in 746 wild birds. Oropharyngeal and cloacal swabs were obtained and placed together in vials containing VTM transport medium collected in different regions of Brazil between 2006 and 2013. Screening for viral nucleic acid was performed using conventional RT-PCR and pancoronavirus nested PCR. Positive samples were characterized by partial sequencing of the RNA-dependent RNA polymerase (RdRp) gene, and ensuing phylogenetic analysis was performed to investigate the association between virus epidemiology and bird migration routes. Coronavirus RNA were detected and sequenced from six samples, in which three were related to gammacoronaviruses group and the other three to deltacoronavirus group. Our study documents the presence of CoVs related to avian gamma- and deltacoronaviruses circulating in both urban- and poultry-farm regions of Brazil, implicating wild birds as potential carriers of CoVs which may represent a risk to poultry farms and public health in Brazil.

Keywords

Gammacoronavirus Deltacoronavirus Wild birds Brazil South America 

Notes

Acknowledgments

We thank the field logistic support of field team of Microbiology Department, University of São Paulo, Wildlife Department of São Paulo (DEPAVE), and Laboratory of Ornithology and Marine Animals (LOAM), Universidade do Vale do Rio dos Sinos. We thank Diogo Fiori Ribas, Edna Maria Gomes Cavalcante, and Hiroe. Positive control was kindly provided by Professor Paulo Brandão at the Department of Preventive Veterinary Medicine and Animal Health, School of Veterinary Medicine, University of São Paulo.

Funding

This work was supported by the Fundacão de Amparo a Pesquisa do Estado de São Paulo (FAPESP) (grant numbers 2009/05994-9, 2011/13821-7, 2011/11006-0, 2013/05485-2, 2014/03172-0); the Conselho Nacional de Desenvolvimento a Pesquisa (CNPq) (grant number 477912/2007-9]; CAPES/Newton Foundation (grant number 99999.005126/2015-00); Fundação de Amparo a Pesquisa do Estado do Rio Grande do Sul (FAPERGS No. 09/0574-7); and Wildlife Conservation Society (CWS No. 2008-05 and 2009-05).

Compliance with ethical standards

Conflict of interest

The authors declared that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The procedures involving wild birds were approved by the Brazilian Society of Laboratory Animal Science (SBCAL) of the University of São Paulo, São Paulo, Brazil (protocol number 105/pg.74/book2) and licensed by the Chico Mendes Institute for Biodiversity Conservation (ICMBio/SISBIO), Ministry of the Environment (MMA), under protocol numbers 201/2006 CGFAU, 25895-1, 33602-1, 17565-1, and 14966-11.

Supplementary material

42770_2019_65_MOESM1_ESM.pdf (55 kb)
ESM 1 (PDF 54.7 kb)

References

  1. 1.
    Bande F, Arshad SS, Omar AR et al (2017) Global distributions and strain diversity of avian infectious bronchitis virus: a review. Anim Health Res Rev 18:70–83.  https://doi.org/10.1017/S1466252317000044 CrossRefPubMedGoogle Scholar
  2. 2.
    Marandino A, Pereda A, Tomás G et al (2015) Phylodynamic analysis of avian infectious bronchitis virus in South America. J Gen Virol 96:1340–1346.  https://doi.org/10.1099/vir.0.000077 CrossRefPubMedGoogle Scholar
  3. 3.
    Michael MC, Lai DC (1997) The molecular biology of coronaviruses. Adv Virus Res 65:193–292.  https://doi.org/10.1016/S0065-3527(06)66005-3 Google Scholar
  4. 4.
    Woo PCY, Lau SKP, Huang Y, Yuen K-Y (2009) Coronavirus diversity, phylogeny and interspecies jumping. Exp Biol Med 234:1117–1127.  https://doi.org/10.3181/0903-MR-94 CrossRefGoogle Scholar
  5. 5.
    Su S, Wong G, Shi W et al (2016) Epidemiology, genetic recombination, and pathogenesis of coronaviruses. Trends Microbiol 24:490–502.  https://doi.org/10.1016/j.tim.2016.03.003 CrossRefPubMedGoogle Scholar
  6. 6.
    Chan JFW, To KKW, Tse H et al (2013) Interspecies transmission and emergence of novel viruses: lessons from bats and birds. Trends Microbiol 21:544–555.  https://doi.org/10.1016/j.tim.2013.05.005 CrossRefPubMedGoogle Scholar
  7. 7.
    Cavanagh D, Gelb J Jr (2008) Infectious Bronchitis. In: Saif YM (ed) Dis. Poult, 12th edn. Blackwell, Oxford, pp 117–135Google Scholar
  8. 8.
    Durães-Carvalho R, Caserta LC, Barnabé ACS et al (2015) Coronaviruses detected in Brazilian wild birds reveal close evolutionary relationships with Beta- and Deltacoronaviruses isolated from mammals. J Mol Evol 81:21–23.  https://doi.org/10.1007/s00239-015-9693-9 CrossRefPubMedGoogle Scholar
  9. 9.
    de Araujo J, de Azevedo SM, Gaidet N et al (2014) Avian influenza virus (H11N9) in migratory shorebirds wintering in the Amazon region, Brazil. PLoS One 9:e110141.  https://doi.org/10.1371/journal.pone.0110141 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Dusek RJ, Hallgrimsson GT, Ip HS et al (2014) North Atlantic migratory bird flyways provide routes for intercontinental movement of avian influenza viruses. PLoS One.  https://doi.org/10.1371/journal.pone.0092075
  11. 11.
    Ometto T, Durigon EL, de Araujo J et al (2013) West Nile virus surveillance, Brazil, 2008-2010. Trans R Soc Trop Med Hyg 107:723–730.  https://doi.org/10.1093/trstmh/trt081 CrossRefPubMedGoogle Scholar
  12. 12.
    Dusek RJ, McLean RG, Kramer LD et al (2009) Prevalence of West Nile virus in migratory birds during spring and fall migration. Am J Trop Med Hyg 81:1151–1158.  https://doi.org/10.4269/ajtmh.2009.09-0106 CrossRefPubMedGoogle Scholar
  13. 13.
    Reed KD, Meece JK, Henkel JS, Shukla SK (2003) Birds, migration and emerging zoonoses: West Nile virus, Lyme disease, influenza A and enteropathogens. Clin Med Res 1:5–12.  https://doi.org/10.3121/cmr.1.1.5 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Thomazelli L, de Araujo J, de Ferreira CS et al (2012) Molecular surveillance of the Newcastle disease virus in domestic and wild birds on the north eastern coast and Amazon biome of Brazil. Rev Bras Ciência Avícola 14:01–07.  https://doi.org/10.1590/S1516-635X2012000100001 CrossRefGoogle Scholar
  15. 15.
    CEMAVE-ICMBio (2014) Relatório Anual de rotas e áreas de concentraçào de aves migratórias no Brasil. ICMBio, BrasíliaGoogle Scholar
  16. 16.
    Araujo J, Petry MV, Fabrizio T et al (2018) Migratory birds in southern Brazil are a source of multiple avian influenza virus subtypes. Influenza Other Respir Viruses 12:220–231.  https://doi.org/10.1111/irv.12519 CrossRefPubMedGoogle Scholar
  17. 17.
    Chu DKW, Leung CYH, Gilbert M et al (2011) Avian coronavirus in wild aquatic birds. J Virol 85:12815–12820.  https://doi.org/10.1128/JVI.05838-11 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefPubMedGoogle Scholar
  19. 19.
    Hagemeijer M, Rottier P, Haan C (2012) Biogenesis and dynamics of the coronavirus replicative structures. Viruses 4:3245–3269.  https://doi.org/10.3390/v4113245 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Góes LGB, ACA C, de Carvalho C et al (2016) Genetic diversity of bats coronaviruses in the Atlantic Forest hotspot biome, Brazil. Infect Genet Evol 44:510–513.  https://doi.org/10.1016/j.meegid.2016.07.034 CrossRefPubMedGoogle Scholar
  21. 21.
    Jordan BJ, Hilt DA, Poulson R et al (2015) Identification of avian coronavirus in wild aquatic birds of the central and eastern USA. J Wildl Dis 51:218–221.  https://doi.org/10.7589/2014-03-070 CrossRefPubMedGoogle Scholar
  22. 22.
    Hepojoki S, Lindh E, Vapalahti O, Huovilainen A (2017) Prevalence and genetic diversity of coronaviruses in wild birds, Finland. Infect Ecol Epidemiol 7:1408360.  https://doi.org/10.1080/20008686.2017.1408360 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Prefeitura (2008) Guia dos parques municipais de São Paulo. acessed January, 2018Google Scholar
  24. 24.
    Perlman S, Netland J (2009) Coronaviruses post-SARS: update on replication and pathogenesis. Nat Rev Microbiol 7:439–450.  https://doi.org/10.1038/nrmicro2147 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Scherer AL, Petry MV (2012) Seasonal variation in shorebird abundance in the state of Rio Grande Do Sul, southern Brazil. Wilson J Ornithol 124:40–50.  https://doi.org/10.1676/11-034.1 CrossRefGoogle Scholar
  26. 26.
    Embrapa (2016) Embrapa Suinos e Aves. https://www.embrapa.br/suinos-e-aves/cias/mapas. Accessed 20 May 2016
  27. 27.
    Lau JHN, WPLSLCLCT a. K et al (2012) Discovery of seven novel mammalian and avian coronaviruses in the genus Deltacoronavirus supports bat coronaviruses as the gene source of Alphacoronavirus and Betacoronavirus and avian coronaviruses as the gene source of Gammacoronavirus and Deltacoronavi. J Virol 86:3995–4008.  https://doi.org/10.1128/JVI.06540-11 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    de Lima FES, Gil P, Pedrono M et al (2015) Diverse gammacoronaviruses detected in wild birds from Madagascar. Eur J Wildl Res:635–639Google Scholar
  29. 29.
    Muradrasoli S, Bálint Á, Wahlgren J et al (2010) Prevalence and phylogeny of coronaviruses in wild birds from the bering strait area (Beringia). PLoS One.  https://doi.org/10.1371/journal.pone.0013640
  30. 30.
    Wille M, Muradrasoli S, Nilsson A, Järhult JD (2016) High prevalence and putative lineage maintenance of avian coronaviruses in Scandinavian waterfowl. PLoS One.  https://doi.org/10.1371/journal.pone.0150198
  31. 31.
    Lee Y-J, Kang H-M, Lee E-K et al (2014) Novel reassortant influenza A(H5N8) viruses, South Korea, 2014. Emerg Infect Dis 20:1087–1089.  https://doi.org/10.3201/eid2006.140233 PubMedPubMedCentralGoogle Scholar

Copyright information

© Sociedade Brasileira de Microbiologia 2019

Authors and Affiliations

  • Carla M. Barbosa
    • 1
  • Edison L. Durigon
    • 1
  • Luciano M. Thomazelli
    • 1
  • Tatiana Ometto
    • 1
  • Roberta Marcatti
    • 2
  • Marcello Shiavo Nardi
    • 2
  • Daniel M. de Aguiar
    • 3
  • João Batista Pinho
    • 4
  • Maria Virginia Petry
    • 5
  • Isaac Simão Neto
    • 6
  • Patrícia Serafini
    • 7
  • Roberta Costa Rodrigues
    • 8
  • Severino Mendes de Azevedo Junior
    • 9
  • Luiz Gustavo B. Góes
    • 1
  • Jansen de Araujo
    • 1
    Email author
  1. 1.Institute of Biomedical SciencesUniversity of Sao PauloSão PauloBrazil
  2. 2.Wildlife and Green Areas DepartmentSão Paulo MunicipalitySão PauloBrazil
  3. 3.Laboratório de Virologia e Rickettsioses, Hospital VeterinárioUniversidade Federal de Mato GrossoCuiabáBrazil
  4. 4.Laboratório de Ecologia de Aves, Instituto de BiociênciasUniversidade Federal de Mato GrossoCuiabáBrazil
  5. 5.Universidade do Vale do Rio dos Sinos (UNISINOS)São LeopoldoBrazil
  6. 6.Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio)BrasíliaBrazil
  7. 7.Centro Nacional de Pesquisa e Conservação de Aves Silvestres (CEMAVE)CabedeloBrazil
  8. 8.Universidade Federal da Paraíba (UFPB)João PessoaBrazil
  9. 9.Universidade Federal Rural de Pernambuco (UFRPE)RecifeBrazil

Personalised recommendations