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Novel polyomaviruses identified in fecal samples from four carnivore species

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Abstract

Polyomaviruses are oncogenic viruses that are generally thought to have co-evolved with their hosts. While primate and rodent polyomaviruses are increasingly well-studied, less is known about polyomaviruses that infect other mammals. In an effort to gain insight into polyomaviruses associated with carnivores, we surveyed fecal samples collected in the USA from bobcats (Lynx rufus), pumas (Puma concolor), Canada lynxes (Lynx canadensis), and grizzly bears (Ursus arctos). Using a viral metagenomic approach, we identified six novel polyomavirus genomes. Surprisingly, four of the six genomes showed a phylogenetic relationship to polyomaviruses found in prey animals. These included a putative rabbit polyomavirus from a bobcat fecal sample and two possible deer-trophic polyomaviruses from Canada lynx feces. One polyomavirus found in a grizzly bear sample was found to be phylogenetically distant from previously identified polyomaviruses. Further analysis of the grizzly bear fecal sample showed that it contained anelloviruses that are known to infect pigs, suggesting that the bear might have preyed on a wild or domestic pig. Interestingly, a polyomavirus genome identified in a puma fecal sample was found to be closely related both to raccoon polyomavirus 1 and to Lyon-IARC polyomavirus, the latter of which was originally identified in human saliva and skin swab specimens but has since been found in samples from domestic cats (Felis catus).

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Data availability

The sequences described in this study have been deposited in the NCBI GenBank database under accession numbers OM338640-OM338645, BK061592, OP129719, and OP129720.

References

  1. Agueda-Pinto A, Kraberger S, Lund MC, Gortazar C, McFadden G, Varsani A, Esteves PJ (2020) Coinfections of novel polyomavirus, anelloviruses and a recombinant strain of myxoma virus-MYXV-tol identified in Iberian hares. Viruses 12:340

    Article  CAS  Google Scholar 

  2. Alibhai S, Jewell Z, Evans J (2017) The challenge of monitoring elusive large carnivores: An accurate and cost-effective tool to identify and sex pumas (Puma concolor) from footprints. PLoS One 12:e0172065

    Article  Google Scholar 

  3. 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 

  4. 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 19:455–477

    Article  CAS  Google Scholar 

  5. Blinkova O, Victoria J, Li Y, Keele BF, Sanz C, Ndjango JB, Peeters M, Travis D, Lonsdorf EV, Wilson ML, Pusey AE, Hahn BH, Delwart EL (2010) Novel circular DNA viruses in stool samples of wild-living chimpanzees. J Gen Virol 91:74–86

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  7. Brostoff T, Dela Cruz FN, Jr., Church ME, Woolard KD, PesaventoPA, (2014) The raccoon polyomavirus genome and tumor antigen transcription are stable and abundant in neuroglial tumors. J Virol 88:12816–12824

    Article  Google Scholar 

  8. 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  Google Scholar 

  9. Charon J, Buchmann JP, Sadiq S, Holmes EC (2022) RdRp-scan: a bioinformatic resource to identify and annotate divergent RNA viruses in metagenomic sequence data. Virus Evol 8: veac082

  10. Chen L, Qiu Q, Jiang Y, Wang K, Lin Z, Li Z, Bibi F, Yang Y, Wang J, Nie W, Su W, Liu G, Li Q, Fu W, Pan X, Liu C, Yang J, Zhang C, Yin Y, Wang Y, Zhao Y, Zhang C, Wang Z, Qin Y, Liu W, Wang B, Ren Y, Zhang R, Zeng Y, da Fonseca RR, Wei B, Li R, Wan W, Zhao R, Zhu W, Wang Y, Duan S, Gao Y, Zhang YE, Chen C, Hvilsom C, Epps CW, Chemnick LG, Dong Y, Mirarab S, Siegismund HR, Ryder OA, Gilbert MTP, Lewin HA, Zhang G, Heller R, Wang W (2019) Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits. Science 364:eaav6202

  11. Chiappetta CM, Cibulski SP, Lima FES, Varela APM, Amorim DB, Tavares M, Roehe PM (2017) Molecular detection of circovirus and adenovirus in feces of fur seals (Arctocephalus spp.). EcoHealth 14:69–77

    Article  Google Scholar 

  12. Chong R, Shi M, Grueber CE, Holmes EC, Hogg CJ, Belov K, Barrs VR (2019) Fecal viral diversity of captive and wild Tasmanian devils characterized using virion-enriched metagenomics and metatranscriptomics. J Virol 93:e00205

  13. 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 

  14. Dib LV, Palmer JPS, Lima C, Bastos OMP, Uchôa CMA, Amendoeira MRR, Bastos A, Barbosa A (2019) Noninvasive sampling: monitoring of wild carnivores and their parasites. Protected areas, national parks and sustainable future. IntechOpen London, pp 1–13

  15. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinform 5:113

    Article  Google Scholar 

  16. Ehlers B, Anoh AE, Ben Salem N, Broll S, Couacy-Hymann E, Fischer D, Gedvilaite A, Ingenhutt N, Liebmann S, Martin M, Mossoun A, Mugisha L, Muyembe-Tamfum JJ, Pauly M, Perez de Val B, Preugschas H, Richter D, Schubert G, Szentiks CA, Teichmann T, Walter C, Ulrich RG, Wiersma L, Leendertz FH, Calvignac-Spencer S (2019) Novel polyomaviruses in mammals from multiple orders and reassessment of polyomavirus evolution and taxonomy. Viruses 11:930

    Article  CAS  Google Scholar 

  17. Fahsbender E, Altan E, Estrada M, Seguin MA, Young P, Leutenegger CM, Delwart E (2019) Lyon-IARC polyomavirus DNA in feces of diarrheic cats. Microbiol Resour Announc 8:e00550-19

    Article  Google Scholar 

  18. Gheit T, Dutta S, Oliver J, Robitaille A, Hampras S, Combes JD, McKay-Chopin S, Le Calvez-Kelm F, Fenske N, Cherpelis B, Giuliano AR, Franceschi S, McKay J, Rollison DE, Tommasino M (2017) Isolation and characterization of a novel putative human polyomavirus. Virology 506:45–54

    Article  CAS  Google Scholar 

  19. Gilchrist CLM, Chooi YH (2021) Clinker & clustermap.js: automatic generation of gene cluster comparison figures. Bioinformatics 37:2473–2475

    Article  CAS  Google Scholar 

  20. Gouy M, Tannier E, Comte N, Parsons DP (2021) Seaview version 5: a multiplatform software for multiple sequence alignment, molecular phylogenetic analyses, and tree reconciliation. Methods Mol Biol 2231:241–260

    Article  CAS  Google Scholar 

  21. 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 

  22. Hirsch HH, Drachenberg CB, Steiger J, Ramos E (2006) Polyomavirus-associated nephropathy in renal transplantation: critical issues of screening and management. Adv Exp Med Biol 577:160–173

    Article  CAS  Google Scholar 

  23. Johne R, Enderlein D, Nieper H, Muller H (2005) Novel polyomavirus detected in the feces of a chimpanzee by nested broad-spectrum PCR. J Virol 79:3883–3887

    Article  CAS  Google Scholar 

  24. Johne R, Buck CB, Allander T, Atwood WJ, Garcea RL, Imperiale MJ, Major EO, Ramqvist T, Norkin LC (2011) Taxonomical developments in the family Polyomaviridae. Arch Virol 156:1627–1634

    Article  CAS  Google Scholar 

  25. Kamminga S, van der Meijden E, Feltkamp MCW, Zaaijer HL (2018) Seroprevalence of fourteen human polyomaviruses determined in blood donors. PLoS One 13:e0206273

    Article  Google Scholar 

  26. Kamminga S, van der Meijden E, Wunderink HF, Touze A, Zaaijer HL, Feltkamp MCW (2018) Development and evaluation of a broad bead-based multiplex immunoassay to measure IgG seroreactivity against human polyomaviruses. J Clin Microbiol 56:e01566-17

    Article  Google Scholar 

  27. Kourieh A, Combes JD, Tommasino M, Dalstein V, Clifford GM, Lacau St Guily J, Clavel C, Franceschi S, Gheit T, For the Split Study Group (2018) Prevalence and risk factors of human polyomavirus infections in non-malignant tonsils and gargles: the SPLIT study. J Gen Virol 99:1686–1698

  28. Kraberger S, Waits K, Ivan J, Newkirk E, VandeWoude S, Varsani A (2018) Identification of circular single-stranded DNA viruses in faecal samples of Canada lynx (Lynx canadensis), moose (Alces alces) and snowshoe hare (Lepus americanus) inhabiting the Colorado San Juan Mountains. Infect Genet Evol 64:1–8

    Article  CAS  Google Scholar 

  29. Kraberger S, Serieys L, Fountain-Jones N, Packer C, Riley S, Varsani A (2019) Novel smacoviruses identified in the faeces of two wild felids: North American bobcat and African lion. Arch Virol 164:2395–2399

    Article  CAS  Google Scholar 

  30. Kraberger S, Serieys LE, Richet C, Fountain-Jones NM, Baele G, Bishop JM, Nehring M, Ivan JS, Newkirk ES, Squires JR, Lund MC, Riley SP, Wilmers CC, van Helden PD, Van Doorslaer K, Culver M, VandeWoude S, Martin DP, Varsani A (2021) Complex evolutionary history of felid anelloviruses. Virology 562:176–189

    Article  CAS  Google Scholar 

  31. Krumbholz A, Bininda-Emonds ORP, Wutzler P, Zell R (2009) Phylogenetics, evolution, and medical importance of polyomaviruses. Infect Genet Evol 9:784–799

    Article  CAS  Google Scholar 

  32. Li D, Liu CM, Luo R, Sadakane K, Lam TW (2015) MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31:1674–1676

    Article  CAS  Google Scholar 

  33. Li Y, Huang H, Lan T, Wang W, Zhang J, Zheng M, Cao L, Sun W, Lu H (2021) First detection and complete genome analysis of the Lyon IARC polyomavirus in China from samples of diarrheic cats. Virus Genes 57:284–288

    Article  CAS  Google Scholar 

  34. Moens U, Calvignac-Spencer S, Lauber C, Ramqvist T, Feltkamp MCW, Daugherty MD, Verschoor EJ, Ehlers B, Ictv Report C (2017) ICTV virus taxonomy profile: Polyomaviridae. J Gen Virol 98:1159–1160

    Article  CAS  Google Scholar 

  35. Momoi Y, Matsuu A (2021) Detection of severe fever with thrombocytopenia syndrome virus and other viruses in cats via unbiased next-generation sequencing. J Vet Diagn Investig 33:279–282

    Article  CAS  Google Scholar 

  36. 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  Google Scholar 

  37. Ng TF, Chen LF, Zhou Y, Shapiro B, Stiller M, Heintzman PD, Varsani A, Kondov NO, Wong W, Deng X, Andrews TD, Moorman BJ, Meulendyk T, MacKay G, Gilbertson RL, Delwart E (2014) Preservation of viral genomes in 700-y-old caribou feces from a subarctic ice patch. Proc Natl Acad Sci USA 111:16842–16847

    Article  Google Scholar 

  38. Oliver-Guimera A, Hejtmankova A, Jackson K, Pesavento PA (2021) A polyomavirus detected in American black bear (Ursus americanus). Arch Virol 166:1521–1524

    Article  CAS  Google Scholar 

  39. Phan TG, Kapusinszky B, Wang C, Rose RK, Lipton HL, Delwart EL (2011) The fecal viral flora of wild rodents. PLoS Pathog 7:e1002218

    Article  CAS  Google Scholar 

  40. Polyomaviridae Study Group of the International Committee on Taxonomy of Viruses, Calvignac-Spencer S, Feltkamp MC, Daugherty MD, Moens U, Ramqvist T, Johne R, Ehlers B (2016) A taxonomy update for the family Polyomaviridae. Arch Virol 161:1739–1750

    Article  Google Scholar 

  41. Prado JCM, Monezi TA, Amorim AT, Lino V, Paladino A, Boccardo E (2018) Human polyomaviruses and cancer: an overview. Clinics (Sao Paulo) 73:e558s

    Article  Google Scholar 

  42. Qi D, Shan T, Liu Z, Deng X, Zhang Z, Bi W, Owens JR, Feng F, Zheng L, Huang F, Delwart E, Hou R, Zhang W (2017) A novel polyomavirus from the nasal cavity of a giant panda (Ailuropoda melanoleuca). Virol J 14:207

    Article  Google Scholar 

  43. Ruggiero LF, Aubry KB, Buskirk SW, Lyon LJ, Zielinski WJ (1994) The scientific basis for conserving forest carnivores: American marten, fisher, lynx, and wolverine in the western United States. https://doi.org/10.2737/RM-GTR-254

  44. Schmidlin K, Kraberger S, Cook C, DeNardo DF, Fontenele RS, Van Doorslaer K, Martin DP, Buck CB, Varsani A (2021) A novel lineage of polyomaviruses identified in bark scorpions. Virology 563:58–63

    Article  CAS  Google Scholar 

  45. Siebrasse EA, Reyes A, Lim ES, Zhao G, Mkakosya RS, Manary MJ, Gordon JI, Wang D (2012) Identification of MW polyomavirus, a novel polyomavirus in human stool. J Virol 86:10321–10326

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  47. Tan Z, Gonzalez G, Sheng J, Wu J, Zhang F, Xu L, Zhang P, Zhu A, Qu Y, Tu C, Carr MJ, He B (2020) Extensive genetic diversity of polyomaviruses in sympatric bat communities: host switching versus coevolution. J Virol 94:e02101-19

    Article  Google Scholar 

  48. Tao Y, Shi M, Conrardy C, Kuzmin IV, Recuenco S, Agwanda B, Alvarez DA, Ellison JA, Gilbert AT, Moran D, Niezgoda M, Lindblade KA, Holmes EC, Breiman RF, Rupprecht CE, Tong S (2013) Discovery of diverse polyomaviruses in bats and the evolutionary history of the Polyomaviridae. J Gen Virol 94:738–748

    Article  CAS  Google Scholar 

  49. Tisza MJ, Belford AK, Dominguez-Huerta G, Bolduc B, Buck CB (2021) Cenote-Taker 2 democratizes virus discovery and sequence annotation. Virus Evol 7:veaa100

  50. 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

  51. 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  CAS  Google Scholar 

  52. 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 Adelie penguins (Pygoscelis adeliae). J Gen Virol 96:851–857

    Article  CAS  Google Scholar 

  53. Wang Y, Keinonen A, Koskenmies S, Pitkanen S, Fyhrquist N, Sadeghi M, Makisalo H, Soderlund-Venermo M, Hedman K (2019) Occurrence of newly discovered human polyomaviruses in skin of liver transplant recipients and their relation with squamous cell carcinoma in situ and actinic keratosis—a single-center cohort study. Transpl Int 32:516–522

    Article  CAS  Google Scholar 

  54. Wiederspahn A (2021) Montana on high alert for invasion of feral swine from Canada; Wyoming not concerned yet.

  55. Williams SH, Che X, Garcia JA, Klena JD, Lee B, Muller D, Ulrich W, Corrigan RM, Nichol S, Jain K, Lipkin WI (2018) Viral diversity of house mice in New York City. mBio 9:e01354-17

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Acknowledgements

We would like to thank Daniel Thompson and Kent Schmidlin at the Wyoming Game and Fish Department (Lander, Wyoming, USA) and the team at Trophy Game, for collecting bear fecal samples that contributed to this study.

Funding

The work described here was supported by startup funds awarded to AV from the Arizona State University.

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Authors and Affiliations

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

    Simona Kraberger, Kara Schmidlin & Arvind Varsani

  2. Panthera, 8 W 40th St, 18th Floor, New York, NY, 10018, USA

    Laurel E. K. Serieys

  3. Santa Monica Mountains National Recreation Area, National Park Service, Thousand Oaks, CA, 91360, USA

    Laurel E. K. Serieys & Seth P. D. Riley

  4. Speedgoat Wildlife Solutions, Missoula, MT, 59801, USA

    Eric S. Newkirk

  5. U.S. Forest Service, Rocky Mountain Research Station, 800 East Beckwith Avenue, Missoula, MT, 59801, USA

    John R. Squires

  6. Lab of Cellular Oncology, National Cancer Institute, National Institutes of Health, Bethesda, MD, 20892, USA

    Christopher B. Buck

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

    Arvind Varsani

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  1. Simona Kraberger
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  2. Laurel E. K. Serieys
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Correspondence to Simona Kraberger or Arvind Varsani.

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GenBank accession numbers: OM338640-OM338645.

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Kraberger, S., Serieys, L.E.K., Riley, S.P.D. et al. Novel polyomaviruses identified in fecal samples from four carnivore species. Arch Virol 168, 18 (2023). https://doi.org/10.1007/s00705-022-05675-5

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