Skip to main content
SpringerLink
Log in

Novel adenovirus associated with common tern (Sterna hirundo) chicks

  • Annotated Sequence Record
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Adenoviruses have been identified in a wide variety of avian species, and in some species, they have been shown to cause disease and increase mortality. As part of an endeavor to investigate viruses associated with common terns (Sterna hirundo), a novel adenovirus was identified in fecal samples from two common terns on Gull Island, Lake Ontario, Canada. The coding-complete genome sequence of the new adenovirus is 31,094 bp, containing 28 putative genes, and this is the first adenovirus to be associated with terns. The virus was identified in two out of 13 fecal samples from tern chicks, and it was found to be most closely related to duck adenovirus 1, with the DNA polymerase sharing 58% amino acid sequence identity. Phylogenetic analysis based on DNA polymerase protein sequences showed that the new virus forms a distinct sub-branch within the atadenovirus clade and likely represents a new species in this genus.

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

Data availability

The sequence described in this study has been deposited in the GenBank database under accession no. MW067004. The raw reads were deposited in SRA under project PRJNA780509; SRA accession no. SRR16948610.

References

  1. Knowles DP (2017) Chapter 10—adenoviridae. In: MacLachlan NJ, Dubovi EJ (eds) Fenner’s veterinary virology, 5th edn. Academic Press, Boston, pp 217–227

    Google Scholar 

  2. Harrach B, Benkö M, Both GW, Brown M, Davison AJ, Echavarría M, Hess M, Kajon A, Lehmkuhl HD, Mautner V, Mittal SK, Wadell G (2012) Family—Adenoviridae. In: King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy. Elsevier, San Diego, pp 125–141

    Google Scholar 

  3. Salzmann E, Muller E, Marschang RE (2021) Detection of Testadenoviruses and Atadenoviruses in Tortoises and Turtles in Europe. J Zoo Wildl Med 52:223–231

    Article  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

    Article  CAS  Google Scholar 

  5. Kajan GL, Kecskemeti S, Harrach B, Benko M (2013) Molecular typing of fowl adenoviruses, isolated in Hungary recently, reveals high diversity. Vet Microbiol 167:357–363

    Article  CAS  Google Scholar 

  6. Del Valle FP, Camba SI, Umali DV, Sasai K, Shirota K, Katoh H, Tajima T (2020) Research note: molecular and pathologic characterization of avian adenovirus isolated from the oviducts of laying hens in eastern Japan. Poult Sci 99:2459–2468

    Article  Google Scholar 

  7. Mukai Y, Tomita Y, Kryukov K, Nakagawa S, Ozawa M, Matsui T, Tomonaga K, Imanishi T, Kawaoka Y, Watanabe T, Horie M (2019) Identification of a distinct lineage of aviadenovirus from crane feces. Virus Genes 55:815–824

    Article  CAS  Google Scholar 

  8. Kumar R, Sturos M, Porter RE, Singh A, Armien AG, Goyal SM, Mor SK (2021) An outbreak of Fowl aviadenovirus A-associated gizzard erosion and ulceration in captive bobwhite quail (Colinus virginianus). Avian Dis 65:52–58

    PubMed  Google Scholar 

  9. Marek A, Kajan GL, Kosiol C, Harrach B, Schlotterer C, Hess M (2014) Complete genome sequences of pigeon adenovirus 1 and duck adenovirus 2 extend the number of species within the genus Aviadenovirus. Virology 462–463:107–114

    Article  Google Scholar 

  10. Huang Y, Kang H, Dong J, Li L, Zhang J, Sun J, Zhang J, Sun M (2020) Isolation and partial genetic characterization of a new duck adenovirus in China. Vet Microbiol 247:108775

    Article  CAS  Google Scholar 

  11. Zhang X, Zhong Y, Zhou Z, Liu Y, Zhang H, Chen F, Chen W, Xie Q (2016) Molecular characterization, phylogeny analysis and pathogenicity of a Muscovy duck adenovirus strain isolated in China in 2014. Virology 493:12–21

    Article  CAS  Google Scholar 

  12. Teske L, Rubbenstroth D, Meixner M, Liere K, Bartels H, Rautenschlein S (2017) Identification of a novel aviadenovirus, designated pigeon adenovirus 2 in domestic pigeons (Columba livia). Virus Res 227:15–22

    Article  CAS  Google Scholar 

  13. Kleine A, Hafez HM, Luschow D (2017) Investigations on aviadenoviruses isolated from turkey flocks in Germany. Avian Pathol 46:181–187

    Article  CAS  Google Scholar 

  14. Marek A, Ballmann MZ, Kosiol C, Harrach B, Schlotterer C, Hess M (2014) Whole-genome sequences of two turkey adenovirus types reveal the existence of two unknown lineages that merit the establishment of novel species within the genus Aviadenovirus. J Gen Virol 95:156–170

    Article  CAS  Google Scholar 

  15. Kajan GL, Davison AJ, Palya V, Harrach B, Benko M (2012) Genome sequence of a waterfowl aviadenovirus, goose adenovirus 4. J Gen Virol 93:2457–2465

    Article  CAS  Google Scholar 

  16. Chen S, Cheng A, Wang M, Zhu D, Luo Q, Liu F, Chen X (2009) Detection and localization of a goose adenovirus in experimentally infected goslings, using indirect immunofluorescence with paraffin-embedded tissue sections. Avian Pathol 38:167–174

    Article  CAS  Google Scholar 

  17. Oaks JL, Schrenzel M, Rideout B, Sandfort C (2005) Isolation and epidemiology of falcon adenovirus. J Clin Microbiol 43:3414–3420

    Article  Google Scholar 

  18. Das S, Fearnside K, Sarker S, Forwood JK, Raidal SR (2017) A novel pathogenic aviadenovirus from red-bellied parrots (Poicephalus rufiventris) unveils deep recombination events among avian host lineages. Virology 502:188–197

    Article  CAS  Google Scholar 

  19. Athukorala A, Forwood JK, Phalen DN, Sarker S (2020) Molecular characterisation of a novel and highly divergent passerine adenovirus 1. Viruses 12:1036

    Article  CAS  Google Scholar 

  20. Gottdenker NL, Gregory CR, Ard MB, Lorenz WW, Nilsen RA, Ritchie BW (2019) Histopathologic changes, ultrastructure, and molecular characterization of an adenovirus in a sun conure (Aratinga solstitialis). Avian Dis 63:531–538

    Article  CAS  Google Scholar 

  21. Marques MVR, Marin SY, Couto RM, Ecco R, Resende M, Martins N (2019) Fatal necrotic tracheitis by Aviadenovirus in captive Alagoas curassows (Pauxi mitu) extinct from the wild. Avian Pathol 48:278–283

    Article  Google Scholar 

  22. Shah MS, Ashraf A, Khan MI, Rahman M, Habib M, Chughtai MI, Qureshi JA (2017) Fowl adenovirus: history, emergence, biology and development of a vaccine against hydropericardium syndrome. Arch Virol 162:1833–1843

    Article  CAS  Google Scholar 

  23. Arnold JM, Oswald SA, Nisbet ICT, Pyle P, Patten MA (2020) Common Tern Sterna hirundo, version 1. In: Billerman M (ed) Birds of the world. Cornell Lab of Ornithology, Ithaca. https://doi.org/10.2173/bow.comter.01

    Chapter  Google Scholar 

  24. Arnold JM, Tyerman DJ, Crump D, Williams KL, Oswald SA (2016) Premature feather loss among common tern chicks in Ontario: the return of an enigmatic developmental anomaly. PeerJ 4:1e1959

    Article  Google Scholar 

  25. Arnold JM, Nisbet IC, Oswald SA (2016) Energetic constraint of non-monotonic mass change during offspring growth: a general hypothesis and application of a new tool. J Anim Ecol 85:476–486

    Article  Google Scholar 

  26. Steel O, Kraberger S, Sikorski A, Young LM, Catchpole RJ, Stevens AJ, Ladley JJ, Coray DS, Stainton D, Dayaram A, Julian L, van Bysterveldt K, Varsani A (2016) Circular replication-associated protein encoding DNA viruses identified in the faecal matter of various animals in New Zealand. Infect Genet Evol 43:151–164

    Article  CAS  Google Scholar 

  27. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  Google Scholar 

  28. Nurk S, Meleshko D, Korobeynikov A, Pevzner PA (2017) metaSPAdes: a new versatile metagenomic assembler. Genome Res 27:824–834

    Article  CAS  Google Scholar 

  29. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  Google Scholar 

  30. Bushnell B (2014) BBMap: a fast, accurate, splice-aware aligner. Lawrence Berkeley National Lab LBNL, Berkeley

    Google Scholar 

  31. 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 of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  Google Scholar 

  32. Darriba D, Taboada GL, Doallo R, Posada D (2011) ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27:1164–1165

    Article  CAS  Google Scholar 

  33. Harrach B, Tarjan ZL, Benko M (2019) Adenoviruses across the animal kingdom: a walk in the zoo. FEBS Lett 593:3660–3673

    Article  CAS  Google Scholar 

  34. Doszpoly A, Harrach B, LaPatra S, Benko M (2019) Unconventional gene arrangement and content revealed by full genome analysis of the white sturgeon adenovirus, the single member of the genus Ichtadenovirus. Infect Genet Evol 75:103976

    Article  CAS  Google Scholar 

  35. Stover BC, Muller KF (2010) TreeGraph 2: combining and visualizing evidence from different phylogenetic analyses. BMC Bioinformatics 11:7

    Article  Google Scholar 

Download references

Acknowledgements

We thank Katie Rutt, Laura Ingraham, Anthony Mazza, Jenna Diehl, and Carolyn Degurski for assistance in the field. We also thank Christopher Kyle and Erica Nol for use of lab facilities at Trent University (Canada). Funding from Friends of Presqu’ile helped support fieldwork. B.H. was supported by the National Research, Development and Innovation Office, Hungary (NN140356). The molecular work was supported by Startup funds awarded to A.V. from Arizona State University (USA).

Author information

Authors and Affiliations

  1. The Biodesign Center for Fundamental and Applied Microbiomics, Center for Evolution and Medicine, School of Life Sciences, Arizona State University, Tempe, AZ, 85287, USA

    Simona Kraberger, Kara Schmidlin, Joy M. Custer, Grace Levi & Arvind Varsani

  2. Division of Science, Pennsylvania State University, Berks Campus, Reading, PA, 19610, USA

    Stephen A. Oswald & Jennifer M. Arnold

  3. Veterinary Medical Research Institute, Budapest, 1143, Hungary

    Mária Benkő & Balázs Harrach

  4. Structural Biology Research Unit, Department of Integrative Biomedical Sciences, University of Cape Town, Cape Town, 7925, South Africa

    Arvind Varsani

Authors
  1. Simona Kraberger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen A. Oswald
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jennifer M. Arnold
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kara Schmidlin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Joy M. Custer
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Grace Levi
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mária Benkő
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Balázs Harrach
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Arvind Varsani
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Stephen A. Oswald, Jennifer M. Arnold or Arvind Varsani.

Ethics declarations

Conflict of interest

The authors declare no conflicts of interest.

Ethical approval

All field study activities were approved by Penn State University’s Institutional Animal Care and Use Committee (protocol #45332) and permitted by the Canadian Wildlife Service Migratory Bird Act Scientific Permit CA 0308 and banding permit 10901 from Environment and Climate Change Canada.

Additional information

Handling Editor: Ana Cristina Bratanich.

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kraberger, S., Oswald, S.A., Arnold, J.M. et al. Novel adenovirus associated with common tern (Sterna hirundo) chicks. Arch Virol 167, 659–663 (2022). https://doi.org/10.1007/s00705-021-05324-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-021-05324-3

Search

Navigation