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Novel anelloviruses identified in buccal swabs of Antarctic fur seals

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Abstract

Viral diversity associated with Antarctic wildlife remains poorly studied. Nonetheless, over the past 5 years, there has been a concerted effort using viral metagenomics approaches to identify and characterize viruses associated with Antarctic pinniped and avian species. Here we used a viral metagenomics approach to identify circular DNA viruses in buccal swab samples from Antarctic fur seals (Arctocephalus gazella) breeding on Livingston Island, Antarctica during the 2016/2017 field season. We identified two new lineages of anelloviruses, torque teno Arctocephalus gazella virus (TTAgV)-1 (2083 nts) and -2 (2127–2143 nts), which are most closely related to and cluster with a previously identified anellovirus associated with California sea lions (Zalophus californianus) sharing ~ 60% genome-wide pairwise identity. The ORF1 of TTAgVs share 26–41% amino acid similarity to the ORF1 of other previously identified pinniped-associated anelloviruses.

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Data availability

All sequence data reported in this study has been deposited in GenBank (https://www.ncbi.nlm.nih.gov/genbank/) under Accession #s MG837569–MG837573.

References

  1. Kariminia S, Ahmad SS, Hashim R, Ismail Z (2013) Environmental consequences of Antarctic tourism from a global perspective. Proc Soc Behav Sci 105:781–791

    Article  Google Scholar 

  2. Amesbury MJ, Roland TP, Royles J, Hodgson DA, Convey P, Griffiths H, Charman DJ (2017) Widespread biological response to rapid warming on the Antarctic Peninsula. Curr Biol 27:1616–1622

    Article  CAS  PubMed  Google Scholar 

  3. Daszak P, Cunningham AA, Hyatt AD (2000) Emerging infectious diseases of wildlife—threats to biodiversity and human health. Science 287:443–449

    Article  CAS  PubMed  Google Scholar 

  4. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P (2008) Global trends in emerging infectious diseases. Nature 451:990–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Härkönen L, Dietz R, Reijnders P, Teilmann J, Harding K, Hall A, Brasseur S, Siebert U, Goodman SJ, Jepson PD (2006) A review of the 1988 and 2002 phocine distemper virus epidemics in European harbour seals. Dis Aquat Org 68:115–130

    Article  PubMed  Google Scholar 

  6. Osterhaus AD, Vedder EJ (1988) Identification of virus causing recent seal deaths. Nature 335:20

    Article  CAS  PubMed  Google Scholar 

  7. Zohari S, Neimanis A, Harkonen T, Moraeus C, Valarcher JF (2014) Avian influenza A (H10N7) virus involvement in mass mortality of harbour seals (Phoca vitulina) in Sweden, March through October 2014. Eurosurveillance 19:2–7

    Article  Google Scholar 

  8. Blix AS, Nordoy ES (2007) Ross seal (Ommatophoca rossii) annual distribution, diving behaviour, breeding and moulting, off Queen Maud Land, Antarctica. Polar Biol 30:1449–1458

    Article  Google Scholar 

  9. Laws RM (1984) Antarctic ecology. Academic Press, London

    Google Scholar 

  10. Siniff DB (1991) An overview of the ecology of Antarctic seals. Am Zool 31:143–149

    Article  Google Scholar 

  11. Guinet C, Jouventin P, Weimerskirch H (1999) Recent population change of the southern elephant seal at îles Crozet and îles Kerguelen: the end of the decrease? Antarct Sci 11:193–197

    Article  Google Scholar 

  12. Buck CB, Van Doorslaer K, Peretti A, Geoghegan EM, Tisza MJ, An P, Katz JP, Pipas JM, McBride AA, Camus AC, McDermott AJ, Dill JA, Delwart E, Ng TF, Farkas K, Austin C, Kraberger S, Davison W, Pastrana DV, Varsani A (2016) The ancient evolutionary history of polyomaviruses. PLoS Pathog 12:e1005574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Goraichuk IV, Dimitrov KM, Sharma P, Miller PJ, Swayne DE, Suarez DL, Afonso CL (2017) Complete genome sequences of four avian paramyxoviruses of serotype 10 isolated from rockhopper penguins on the Falkland Islands. Genome Announc 5:e00472-00417

    Article  Google Scholar 

  14. Hurt AC, Su YC, Aban M, Peck H, Lau H, Baas C, Deng YM, Spirason N, Ellstrom P, Hernandez J, Olsen B, Barr IG, Vijaykrishna D, Gonzalez-Acuna D (2016) Evidence for the introduction, reassortment, and persistence of diverse influenza a viruses in Antarctica. J Virol 90:9674–9682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hurt AC, Vijaykrishna D, Butler J, Baas C, Maurer-Stroh S, Silva-de-la-Fuente MC, Medina-Vogel G, Olsen B, Kelso A, Barr IG, Gonzalez-Acuna D (2014) Detection of evolutionarily distinct avian influenza a viruses in Antarctica. mBio 5:e01098-01014

    Article  CAS  Google Scholar 

  16. Lee SY, Kim JH, Park YM, Shin OS, Kim H, Choi HG, Song JW (2014) A novel adenovirus in Chinstrap penguins (Pygoscelis antarctica) in Antarctica. Viruses 6:2052–2061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Lee SY, Kim JH, Seo TK, No JS, Kim H, Kim WK, Choi HG, Kang SH, Song JW (2016) Genetic and molecular epidemiological characterization of a novel adenovirus in Antarctic penguins collected between 2008 and 2013. PLoS ONE 11:e0157032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Neira V, Tapia R, Verdugo C, Barriga G, Mor S, Ng TFF, Garcia V, Del Rio J, Rodrigues P, Briceno C, Medina RA, Gonzalez-Acuna D (2017) Novel avulaviruses in penguins, Antarctica. Emerg Infect Dis 23:1212–1214

    Article  PubMed  PubMed Central  Google Scholar 

  19. Park YM, Kim JH, Gu SH, Lee SY, Lee MG, Kang YK, Kang SH, Kim HJ, Song JW (2012) Full genome analysis of a novel adenovirus from the South Polar skua (Catharacta maccormicki) in Antarctica. Virology 422:144–150

    Article  CAS  PubMed  Google Scholar 

  20. Van Doorslaer K, Ruoppolo V, Schmidt A, Lescroel A, Jongsomjit D, Elrod M, Kraberger S, Stainton D, Dugger KM, Ballard G, Ainley DG, Varsani A (2017) Unique genome organization of non-mammalian papillomaviruses provides insights into the evolution of viral early proteins. Virus Evol 3:vex027

    PubMed  PubMed Central  Google Scholar 

  21. Varsani A, Frankfurter G, Stainton D, Male MF, Kraberger S, Burns JM (2017) Identification of a polyomavirus in Weddell seal (Leptonychotes weddellii) from the Ross Sea (Antarctica). Arch Virol 162:1403–1407

    Article  CAS  PubMed  Google Scholar 

  22. Varsani A, Kraberger S, Jennings S, Porzig EL, Julian L, Massaro M, Pollard A, Ballard G, Ainley DG (2014) A novel papillomavirus in Adélie penguin (Pygoscelis adeliae) faeces sampled at the Cape Crozier colony, Antarctica. J Gen Virol 95:1352–1365

    Article  CAS  PubMed  Google Scholar 

  23. Varsani A, Porzig EL, Jennings S, Kraberger S, Farkas K, Julian L, Massaro M, Ballard G, Ainley DG (2015) Identification of an avian polyomavirus associated with Adélie penguins (Pygoscelis adeliae). J Gen Virol 96:851–857

    Article  CAS  PubMed  Google Scholar 

  24. Smeele ZE, Burns JM, Van Doorsaler K, Fontenele RS, Waits K, Stainton D, Shero MR, Beltran RS, Kirkham AL, Berngartt R, Kraberger S, Varsani A (2018) Diverse papillomaviruses identified in Weddell seals. J Gen Virol 99:549–557

    Article  PubMed  Google Scholar 

  25. Van Doorslaer K, Kraberger S, Austin C, Farkas K, Bergeman M, Paunil E, Davison W, Varsani A (2018) Fish polyomaviruses belong to two distinct evolutionary lineages. J Gen Virol 99:567–573

    Article  PubMed  PubMed Central  Google Scholar 

  26. Smeele ZE, Ainley DG, Varsani A (2018) Viruses associated with Antarctic wildlife: from serology based detection to identification of genomes using high throughput sequencing. Virus Res 243:91–105

    Article  CAS  PubMed  Google Scholar 

  27. Fahsbender E, Burns JM, Kim S, Kraberger S, Frankfurter G, Eilers AA, Shero MR, Beltran R, Kirkham A, McCorkell R, Berngartt RK, Male MF, Ballard G, Ainley DG, Breitbart M, Varsani A (2017) Diverse and highly recombinant anelloviruses associated with Weddell seals in Antarctica. Virus Evol 3:vex017

    Article  PubMed  PubMed Central  Google Scholar 

  28. Biagini P, Bendinelli M, Hino S, Kakkola L, Mankertz A, Niel C, Okamoto H, Raidal S, Teo CG, Todd D (2012)  Family Anelloviridae. In: King AMQ, Adams EB, Carstens EB, Lefkowitz EJ (eds) Virus taxonomy: Ninth report of the international committee on taxonomy of viruses. Academic press, London; Waltham, MA, pp 331-341

    Google Scholar 

  29. Biagini P (2009) Classification of TTV and related viruses (anelloviruses). Curr Top Microbiol Immunol 331:21–33

    CAS  PubMed  Google Scholar 

  30. Davidson I, Shulman LM (2008) Unraveling the puzzle of human anellovirus infections by comparison with avian infections with the chicken anemia virus. Virus Res 137:1–15

    Article  CAS  PubMed  Google Scholar 

  31. Hino S, Miyata H (2007) Torque teno virus (TTV): current status. Rev Med Virol 17:45–57

    Article  CAS  PubMed  Google Scholar 

  32. Ng TF, Suedmeyer WK, Wheeler E, Gulland F, Breitbart M (2009) Novel anellovirus discovered from a mortality event of captive California sea lions. J Gen Virol 90:1256–1261

    Article  CAS  PubMed  Google Scholar 

  33. Bodewes R, Rubio Garcia A, Wiersma LC, Getu S, Beukers M, Schapendonk CM, van Run PR, van de Bildt MW, Poen MJ, Osinga N, Sanchez Contreras GJ, Kuiken T, Smits SL, Osterhaus AD (2013) Novel B19-like parvovirus in the brain of a harbor seal. PLoS ONE 8:e79259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Ng TF, Wheeler E, Greig D, Waltzek TB, Gulland F, Breitbart M (2011) Metagenomic identification of a novel anellovirus in Pacific harbor seal (Phoca vitulina richardsii) lung samples and its detection in samples from multiple years. J Gen Virol 92:1318–1323

    Article  CAS  PubMed  Google Scholar 

  35. Jackman SD, Vandervalk BP, Mohamadi H, Chu J, Yeo S, Hammond SA, Jahesh G, Khan H, Coombe L, Warren RL, Birol I (2017) ABySS 2.0: resource-efficient assembly of large genomes using a Bloom filter. Genome Res 27:768–777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  37. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. 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  PubMed  Google Scholar 

  39. 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  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  41. Letunic I, Bork P (2016) Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res 44:W242–W245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Muhire BM, Varsani A, Martin DP (2014) SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 9:e108277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The molecular work described in this study is supported by Center of Evolution and Medicine Venture Fund (Center of Evolution and Medicine, Arizona State University, USA) grant awarded to AS and AV.

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Authors and Affiliations

Authors

Contributions

MEG collected the samples. AC and SK undertook all the lab work. AV and AC undertook all the bioinformatic analyses. AC, MEG, SK, ACS, and AV wrote the manuscript.

Corresponding author

Correspondence to Arvind Varsani.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

Antarctic fur seal samples were collected under National Marine Fisheries Service Marine Mammal permit #20599, Antarctic Conservation Act permit #2017-012. The data used for the analyses in this manuscript are publicly available in GenBank.

Additional information

Edited by Zhen F. Fu.

GenBank Accession #: MG837569–MG837573.

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Crane, A., Goebel, M.E., Kraberger, S. et al. Novel anelloviruses identified in buccal swabs of Antarctic fur seals. Virus Genes 54, 719–723 (2018). https://doi.org/10.1007/s11262-018-1585-9

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  • DOI: https://doi.org/10.1007/s11262-018-1585-9

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