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Virus Genes

, Volume 55, Issue 6, pp 815–824 | Cite as

Identification of a distinct lineage of aviadenovirus from crane feces

  • Yahiro Mukai
  • Yuriko Tomita
  • Kirill Kryukov
  • So Nakagawa
  • Makoto Ozawa
  • Tsutomu Matsui
  • Keizo Tomonaga
  • Tadashi Imanishi
  • Yoshihiro Kawaoka
  • Tokiko WatanabeEmail author
  • Masayuki HorieEmail author
Original Paper

Abstract

Viruses are believed to be ubiquitous; however, the diversity of viruses is largely unknown because of the bias of previous research toward pathogenic viruses. Deep sequencing is a promising and unbiased approach to detect viruses from animal-derived materials. Although cranes are known to be infected by several viruses such as influenza A viruses, previous studies targeted limited species of viruses, and thus viruses that infect cranes have not been extensively studied. In this study, we collected crane fecal samples in the Izumi plain in Japan, which is an overwintering site for cranes, and performed metagenomic shotgun sequencing analyses. We detected aviadenovirus-like sequences in the fecal samples and tentatively named the discovered virus crane-associated adenovirus 1 (CrAdV-1). We determined that our sequence accounted for approximately three-fourths of the estimated CrAdV-1 genome size (33,245 bp). The GC content of CrAdV-1 genome is 34.1%, which is considerably lower than that of other aviadenoviruses. Phylogenetic analyses revealed that CrAdV-1 clusters with members of the genus Aviadenovirus, but is distantly related to the previously identified aviadenoviruses. The protein sequence divergence between the DNA polymerase of CrAdV-1 and those of other aviadenoviruses is 45.2–46.8%. Based on these results and the species demarcation for the family Adenoviridae, we propose that CrAdV-1 be classified as a new species in the genus Aviadenovirus. Results of this study contribute to a deeper understanding of the diversity and evolution of viruses and provide additional information on viruses that infect cranes, which might lead to protection of the endangered species of cranes.

Keywords

Adenovirus Aviadenovirus Crane Feces Metagenomics 

Notes

Acknowledgements

We thank Dr. Keiko Takemoto (Kyoto University) for her kind help with the bioinformatic analyses. We also thank Naomi Fujimoto and Mikiko Tanaka for technical support. The supercomputing resource was provided by the Human Genome Center (University of Tokyo). This study was supported by the Hakubi Project at Kyoto University (MH); a Grant-in-Aid for Scientific Research on Innovative Areas from the Ministry of Education, Culture, Science, Sports, and Technology (MEXT) of Japan, Grant Numbers 17H05821 (MH), 19H04833 (MH),17H05823 (SN), 19H04843 (SN), 16H06429 (TW), 16K21723 (TW), and 16H06434 (TW); the Cooperative Research Program (Joint Usage/Research Center) of the Institute for Frontier Life and Medial Sciences at Kyoto University (SN); and a Grant for contracted research activity related to crane conservation by the City of Izumi, Japan (MO). This research was commissioned by the Kagoshima Crane Conservation Committee.

Author contributions

MO, TM, KT, YK, TW, and MH designed the study. YM, YT, MO, TW, and MH performed the researches. KK, SN, TI and MH analyzed the data. YM, SN, TW, and MH wrote the paper.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Research involving human participants and/or animals

This article does not contain any studies with human participants or animals, performed by any of the authors.

Informed consent

Informed consent concerns are not applicable.

Supplementary material

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Supplementary file6 (FASTA 37 kb)

References

  1. 1.
    Geoghegan JL, Holmes EC (2017) Predicting virus emergence amid evolutionary noise. Open Biol 7(10):170189.  https://doi.org/10.1098/rsob.170189 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Shi M, Zhang YZ, Holmes EC (2018) Meta-transcriptomics and the evolutionary biology of RNA viruses. Virus Res 243:83–90.  https://doi.org/10.1016/j.virusres.2017.10.016 CrossRefPubMedGoogle Scholar
  3. 3.
    Bodewes R, Ruiz-Gonzalez A, Schapendonk CM, van den Brand JM, Osterhaus AD, Smits SL (2014) Viral metagenomic analysis of feces of wild small carnivores. Virol J 11:89.  https://doi.org/10.1186/1743-422X-11-89 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Honma H, Suyama Y, Nakai Y (2011) Detection of parasitizing coccidia and determination of host crane species, sex and genotype by faecal DNA analysis. Mol Ecol Resour 11(6):1033–1044.  https://doi.org/10.1111/j.1755-0998.2011.03048.x CrossRefPubMedGoogle Scholar
  5. 5.
    Okuya K, Kanazawa N, Kanda T, Kuwahara M, Matsuu A, Horie M, Masatani T, Toda S, Ozawa M (2017) Genetic characterization of an avian H4N6 influenza virus isolated from the Izumi plain, Japan. Microbiol Immunol.  https://doi.org/10.1111/1348-0421.12545 CrossRefPubMedGoogle Scholar
  6. 6.
    Nakagawa H, Okuya K, Kawabata T, Matsuu A, Takase K, Kuwahara M, Toda S, Ozawa M (2018) Genetic characterization of low-pathogenic avian influenza viruses isolated on the Izumi plain in Japan: possible association of dynamic movements of wild birds with AIV evolution. Arch Virol 163(4):911–923.  https://doi.org/10.1007/s00705-017-3698-1 CrossRefPubMedGoogle Scholar
  7. 7.
    Ozawa M, Matsuu A, Tokorozaki K, Horie M, Masatani T, Nakagawa H, Okuya K, Kawabata T, Toda S (2015) Genetic diversity of highly pathogenic H5N8 avian influenza viruses at a single overwintering site of migratory birds in Japan, 2014/15. Euro Surveill 20(20):21132CrossRefGoogle Scholar
  8. 8.
    Ozawa M, Matsuu A, Khalil AM, Nishi N, Tokorozaki K, Masatani T, Horie M, Okuya K, Ueno K, Kuwahara M, Toda S (2019) Phylogenetic variations of highly pathogenic H5N6 avian influenza viruses isolated from wild birds in the Izumi plain, Japan, during the 2016–2017 winter season. Transbound Emerg Dis 66(2):797–806.  https://doi.org/10.1111/tbed.13087 CrossRefPubMedGoogle Scholar
  9. 9.
    Ratnasingham S, Hebert PD (2007) The barcode of life data system. Mol Ecol Notes 7(3):355–364.  https://doi.org/10.1111/j.1471-8286.2007.01678.x CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST+: architecture and applications. BMC Bioinform 10:421.  https://doi.org/10.1186/1471-2105-10-421 CrossRefGoogle Scholar
  11. 11.
    Chen S, Zhou Y, Chen Y, Gu J (2018) fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34(17):i884–i890.  https://doi.org/10.1093/bioinformatics/bty560 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Nurk S, Meleshko D, Korobeynikov A, Pevzner PA (2017) metaSPAdes: a new versatile metagenomic assembler. Genome Res 27(5):824–834.  https://doi.org/10.1101/gr.213959.116 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Shen W, Le S, Li Y, Hu F (2016) SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation. PLoS ONE 11(10):e0163962.  https://doi.org/10.1371/journal.pone.0163962 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Steinegger M, Soding J (2017) MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat Biotechnol 35(11):1026–1028.  https://doi.org/10.1038/nbt.3988 CrossRefPubMedGoogle Scholar
  15. 15.
    Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477.  https://doi.org/10.1089/cmb.2012.0021 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9(4):357–359.  https://doi.org/10.1038/nmeth.1923 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Barnett DW, Garrison EK, Quinlan AR, Stromberg MP, Marth GT (2011) BamTools: a C++ API and toolkit for analyzing and managing BAM files. Bioinformatics 27(12):1691–1692.  https://doi.org/10.1093/bioinformatics/btr174 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780.  https://doi.org/10.1093/molbev/mst010 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    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 CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Marek A, Nolte V, Schachner A, Berger E, Schlotterer C, Hess M (2012) Two fiber genes of nearly equal lengths are a common and distinctive feature of Fowl adenovirus C members. Vet Microbiol 156(3–4):411–417.  https://doi.org/10.1016/j.vetmic.2011.11.003 CrossRefPubMedGoogle Scholar
  21. 21.
    Harrach B, Benkö M, Both G, Brown M, Davison A, Echavarría M, Hess M, Jones M, Kajon A, Lehmkuhl H (2011) Family adenoviridae. Virus taxonomy: classification and nomenclature of viruses. In: Ninth report of the international committee on taxonomy of viruses (2011). Elsevier, San Diego, CA, pp 125–141Google Scholar
  22. 22.
    Tan B, Yang XL, Ge XY, Peng C, Liu HZ, Zhang YZ, Zhang LB, Shi ZL (2017) Novel bat adenoviruses with low G+C content shed new light on the evolution of adenoviruses. J Gen Virol 98(4):739–748.  https://doi.org/10.1099/jgv.0.000739 CrossRefPubMedGoogle Scholar
  23. 23.
    Ojkic D, Nagy E (2000) The complete nucleotide sequence of fowl adenovirus type 8. J Gen Virol 81(Pt 7):1833–1837.  https://doi.org/10.1099/0022-1317-81-7-1833 CrossRefPubMedGoogle Scholar
  24. 24.
    Corredor JC, Garceac A, Krell PJ, Nagy E (2008) Sequence comparison of the right end of fowl adenovirus genomes. Virus Genes 36(2):331–344.  https://doi.org/10.1007/s11262-007-0194-9 CrossRefPubMedGoogle Scholar
  25. 25.
    Griffin BD, Nagy E (2011) Coding potential and transcript analysis of fowl adenovirus 4: insight into upstream ORFs as common sequence features in adenoviral transcripts. J Gen Virol 92(Pt 6):1260–1272.  https://doi.org/10.1099/vir.0.030064-0 CrossRefPubMedGoogle Scholar
  26. 26.
    Marek A, Kosiol C, Harrach B, Kajan GL, Schlotterer C, Hess M (2013) The first whole genome sequence of a Fowl adenovirus B strain enables interspecies comparisons within the genus Aviadenovirus. Vet Microbiol 166(1–2):250–256.  https://doi.org/10.1016/j.vetmic.2013.05.017 CrossRefPubMedGoogle Scholar
  27. 27.
    Ojkic D, Nagy E (2001) The long repeat region is dispensable for fowl adenovirus replication in vitro. Virology 283(2):197–206.  https://doi.org/10.1006/viro.2000.0890 CrossRefPubMedGoogle Scholar
  28. 28.
    Hagiwara S (1988) Wild plants for winter foods in Grus monacha & G. vipio in Izumi, Japan (studies of the Cranes in Izumi, Kagoshima, Japan. 13). Misc Rep Natl Park Nat Stud 19:83–97 (in Japanese) Google Scholar
  29. 29.
    Board of Education in Kagoshima Prefecture (1995) Research report on the long-term crane protective measures investigation studies, 1994 fiscal year (in Japanese) Google Scholar
  30. 30.
    Board of Education in Kagoshima Prefecture (1996) Research report on the long-term crane protective measures investigation studies, 1995 fiscal year (in Japanese) Google Scholar
  31. 31.
    Li PH, Zheng PP, Zhang TF, Wen GY, Shao HB, Luo QP (2017) Fowl adenovirus serotype 4: epidemiology, pathogenesis, diagnostic detection, and vaccine strategies. Poult Sci 96(8):2630–2640.  https://doi.org/10.3382/ps/pex087 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratory of RNA Viruses, Department of Virus ResearchInstitute for Frontier Life and Medical SciencesKyotoJapan
  2. 2.Department of Mammalian Regulatory Network, Graduate School of BiostudiesKyoto UniversityKyotoJapan
  3. 3.Division of Virology, Department of Microbiology and Immunology, Institute of Medical ScienceUniversity of TokyoTokyoJapan
  4. 4.Department of Molecular Life ScienceTokai University School of MedicineTokyoJapan
  5. 5.Joint Faculty of Veterinary Medicine, Laboratory of Animal HygieneKagoshima UniversityKagoshimaJapan
  6. 6.Transboundary Animal Diseases Research Center, Joint Faculty of Veterinary MedicineKagoshima UniversityKagoshimaJapan
  7. 7.United Graduate School of Veterinary ScienceYamaguchi UniversityYamaguchiJapan
  8. 8.Kagoshima Crane Conservation CommitteeIzumiJapan
  9. 9.Department of Molecular Virology, Graduate School of MedicineKyoto UniversityKyotoJapan
  10. 10.Department of Pathobiological Sciences, School of Veterinary MedicineUniversity of Wisconsin-MadisonMadisonUSA
  11. 11.Department of Special Pathogens, International Research Center for Infectious Diseases, Institute of Medical ScienceUniversity of TokyoTokyoJapan
  12. 12.Hakubi Center for Advanced ResearchKyoto UniversityKyotoJapan

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