Skip to main content
SpringerLink
Log in

Molecular identification of novel and genetically diverse adenoviruses in Passeriform birds

  • Original Paper
  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

Knowledge about adenoviruses in birds of the order Passeriformes is very scarce. Based on molecular characterizations, only two siadenoviruses, great tit adenovirus 1 and Gouldian finch adenovirus, have been described so far occurring in great tits and Gouldian finches, respectively. Assuming a broader occurrence of adenoviruses, various passeriform birds including pet, zoo, and wild birds were examined using a broad-range PCR targeting a fragment of the adenovirus DNA polymerase gene. Adenoviruses were detected in 25 individual birds belonging to 13 species and seven zoological families (Ploceidae, Fringillidae, Estrildidae, Paridae, Sylviidae, Turdidae, Muscicapidae). The putative viruses were further characterized by sequencing the PCR products and phylogenetic analyses. DNA of adenoviruses affiliating to 3 genera including aviadenovirus, siadenovirus, and atadenovirus was found. Viruses with sequences identical or closely related to great tit adenovirus 1 and Gouldian finch adenovirus 1 were detected in a great tit and in two zebra finches, respectively. Based on polymerase amino acid sequence comparisons, the viruses found in the remaining 22 birds revealed phylogenetic distances larger than 15% to adenoviruses known so far suggesting that they may belong to at least 14 different virus species. In some bird species (great tit, zebra finch, vitelline masked weaver) varying adenovirus genera were detected. These results suggest a broad variety of adenoviruses circulating in passeriform birds.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Harrach B, Benkö M, Both G, Brown M, Davison A, Echavarría M, Hess M, Jones M, Kajon A, Lehmkuhl H (2011) Family adenoviridae. In: King A, Adams M, Carstens E, Lefkowitz E (eds) Virus taxonomy: classification and nomenclature of viruses. In: Ninth report of the International Committee on Taxonomy of Viruses, Elsevier, San Diego, CA, USA, pp 95–111

  2. Ballmann MZ, Harrach B (2016) Detection and partial genetic characterisation of novel avi- and siadenoviruses in racing and fancy pigeons (Columba livia domestica). Acta Vet Hung 64(4):514–528. https://doi.org/10.1556/004.2016.047

    Article  CAS  PubMed  Google Scholar 

  3. Fitzgerald S (2013) Adenovirus infections: introduction. In: Swayne D, Glisson J, McDougald L, Nolan L, Suarez D, Nair V (eds) Diseases of poultry, 13th edn. Wiley-Blackwell, Ames, pp 289–290

    Google Scholar 

  4. Doszpoly A, Wellehan JF Jr, Childress AL, Tarjan ZL, Kovacs ER, Harrach B, Benko M (2013) Partial characterization of a new adenovirus lineage discovered in testudinoid turtles. Infect Genet Evol 17:106–112. https://doi.org/10.1016/j.meegid.2013.03.049

    Article  CAS  PubMed  Google Scholar 

  5. Hess M (2017) Commensal or pathogen—a challenge to fulfil Koch's Postulates. Br Poult Sci 58(1):1–12. https://doi.org/10.1080/00071668.2016.1245849

    Article  CAS  PubMed  Google Scholar 

  6. Schachner A, Matos M, Grafl B, Hess M (2018) Fowl adenovirus-induced diseases and strategies for their control—a review on the current global situation. Avian Pathol 47(2):111–126. https://doi.org/10.1080/03079457.2017.1385724

    Article  CAS  PubMed  Google Scholar 

  7. Shivaprasad HL, Hill D, Todd D, Smyth JA (2004) Circovirus infection in a Gouldian finch (Chloebia gouldiae). Avian Pathol 33(5):525–529. https://doi.org/10.1080/03079450400003585

    Article  CAS  PubMed  Google Scholar 

  8. Joseph HM, Ballmann MZ, Garner MM, Hanley CS, Berlinski R, Erdelyi K, Childress AL, Fish SS, Harrach B, Wellehan JF Jr (2014) A novel siadenovirus detected in the kidneys and liver of Gouldian finches (Erythura gouldiae). Vet Microbiol 172(1–2):35–43. https://doi.org/10.1016/j.vetmic.2014.04.006

    Article  CAS  PubMed  Google Scholar 

  9. Kovacs ER, Janoska M, Dan A, Harrach B, Benko M (2010) Recognition and partial genome characterization by non-specific DNA amplification and PCR of a new siadenovirus species in a sample originating from Parus major, a great tit. J Virol Methods 163(2):262–268. https://doi.org/10.1016/j.jviromet.2009.10.007

    Article  CAS  PubMed  Google Scholar 

  10. International Committee on Taxonomy of Viruses (2014) ICTV Taxonomy history: Great tit siadenovirus A. https://talk.ictvonline.org/taxonomy/p/taxonomy-history?taxnode_id=201852451. Accessed 31 Aug 2019

  11. Rinder M, Schmitz A, Peschel A, Worle B, Gerlach H, Korbel R (2017) Molecular characterization of a recently identified circovirus in zebra finches (Taeniopygia guttata) associated with immunosuppression and opportunistic infections. Avian Pathol 46(1):106–116. https://doi.org/10.1080/03079457.2016.1223272

    Article  CAS  PubMed  Google Scholar 

  12. Schmitz A, Rinder M, Thiel S, Peschel A, Moser K, Reese S, Korbel R (2018) Retrospective evaluation of clinical signs and gross pathologic findings in birds infected with Mycobacterium genavense. J Avian Med Surg 32(3):194–204. https://doi.org/10.1647/2017-261

    Article  PubMed  Google Scholar 

  13. Schmitz A, Korbel R, Thiel S, Worle B, Gohl C, Rinder M (2018) High prevalence of Mycobacterium genavense within flocks of pet birds. Vet Microbiol 218:40–44. https://doi.org/10.1016/j.vetmic.2018.03.026

    Article  CAS  PubMed  Google Scholar 

  14. Rinder M, Schmitz A, Peschel A, Moser K, Korbel R (2018) Identification and genetic characterization of polyomaviruses in estrildid and fringillid finches. Arch Virol 163(4):895–909. https://doi.org/10.1007/s00705-017-3688-3

    Article  CAS  PubMed  Google Scholar 

  15. Wellehan JF, Johnson AJ, Harrach B, Benko M, Pessier AP, Johnson CM, Garner MM, Childress A, Jacobson ER (2004) Detection and analysis of six lizard adenoviruses by consensus primer PCR provides further evidence of a reptilian origin for the atadenoviruses. J Virol 78(23):13366–13369. https://doi.org/10.1128/jvi.78.23.13366-13369.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Thompson JD, Higgins DG, Gibson TJ (1994) 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):4673–4680. https://doi.org/10.1093/nar/22.22.4673

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance. Syst Biol 59(3):307–321. https://doi.org/10.1093/sysbio/syq010

    Article  CAS  PubMed  Google Scholar 

  18. Lefort V, Longueville JE, Gascuel O (2017) SMS: smart model selection in PhyML. Mol Biol Evol 34(9):2422–2424. https://doi.org/10.1093/molbev/msx149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39(4):783–791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x

    Article  PubMed  Google Scholar 

  20. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35(6):1547–1549. https://doi.org/10.1093/molbev/msy096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS ONE 9(9):e108277. https://doi.org/10.1371/journal.pone.0108277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Harrach B, Tarjan ZL, Benko M (2019) Adenoviruses across the animal kingdom: a walk in the zoo. FEBS Lett 593(24):3660–3673. https://doi.org/10.1002/1873-3468.13687

    Article  CAS  PubMed  Google Scholar 

  23. Chan JF, To KK, Chen H, Yuen KY (2015) Cross-species transmission and emergence of novel viruses from birds. Curr Opin Virol 10:63–69. https://doi.org/10.1016/j.coviro.2015.01.006

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We would like to thank Dana Härtner, Johannes Stadler and Miriam Schiller for excellent technical assistance.

Funding

There was no external funding of the project.

Author information

Authors and Affiliations

  1. Clinic for Birds, Small Mammals, Reptiles and Ornamental Fish, Center for Clinical Veterinary Medicine, University Ludwig-Maximilian of Munich, Sonnenstr. 18, 85764, Oberschleissheim, Germany

    Monika Rinder, Noreen Baas & Rüdiger Korbel

  2. Institute of Poultry Diseases, Free University of Berlin, Berlin, Germany

    Anna Schmitz

Authors
  1. Monika Rinder
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anna Schmitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Noreen Baas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rüdiger Korbel
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MR conceived and designed the experiments. MR, AS, and NB performed the experiments. MR analyzed the data. MR wrote the manuscript. AS, NB, and RK participated in revising the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Monika Rinder.

Ethics declarations

Conflict of interest

The authors declare 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. This article does not contain any studies with human participants performed by any of the authors.

Additional information

Edited by William Dundon.

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Online resource 1

Pairwise genetic distance matrix of aviadenoviruses based on partial polymerase amino acid sequences. Genetic distances (%) were estimated using MEGA X and the Poisson correction model. This analysis involved 18 amino acid sequences. A total of 91 positions was included in the final dataset. The analysis included putative viruses presented in this investigation (printed in bold) and representatives of all recognized aviadenovirus species for which respective sequences were available (GenBank accession numbers are given in brackets). Pairwise genetic distances <5% are marked in light grey, and pairwise genetic distances between 5% and 15% are marked in dark grey. (DOCX 22 kb)

Online resource 2

Pairwise genetic distance matrix of siadenoviruses based on partial polymerase amino acid sequences. Genetic distances (%) were estimated using MEGA X and the Poisson correction model. This analysis involved 19 amino acid sequences. A total of 91 positions was included in the final dataset. The analysis included putative viruses presented in this investigation (printed in bold) and representatives of all recognized siadenovirus species for which respective sequences were available (GenBank accession numbers are given in brackets). Pairwise genetic distances <5% are marked in light grey, and pairwise genetic distances between 5% and 15% are marked in dark grey. (DOCX 20 kb)

Online resource 3

Pairwise genetic distance matrix of atadenoviruses based on partial polymerase amino acid sequences. Genetic distances were estimated using MEGA X and the Poisson correction model. This analysis involved 17 amino acid sequences. A total of 91 positions was included in the final dataset. The analysis included putative viruses presented in this investigation (printed in bold) and representatives of all recognized atadenovirus species for which respective sequences were available (GenBank accession numbers are given in brackets). Pairwise genetic distances <5% are marked in light grey, and pairwise genetic distances between 5% and 15% did not occur. (DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rinder, M., Schmitz, A., Baas, N. et al. Molecular identification of novel and genetically diverse adenoviruses in Passeriform birds. Virus Genes 56, 316–324 (2020). https://doi.org/10.1007/s11262-020-01739-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11262-020-01739-3

Keywords

Search

Navigation