1887

Abstract

Polyomaviruses (PyVs) are small, circular dsDNA viruses carried by diverse vertebrates, including bats. Although previous studies have reported several horseshoe bat PyVs collected in Zambia and China, it is still unclear how PyVs evolved in this group of widely dispersed mammals. Horseshoe bats (genus ) are distributed across the Old World and are natural reservoirs of numerous pathogenic viruses. Herein, non-invasive bat samples from European horseshoe bat species were collected in Hungary for PyV identification and novel PyVs with complete genomes were successfully recovered from two different European horseshoe bat species. Genomic and phylogenetic analysis of the Hungarian horseshoe bat PyVs supported their classification into the genera and . Notably, despite the significant geographical distances between the corresponding sampling locations, Hungarian PyVs exhibited high genetic relatedness with previously described Zambian and Chinese horseshoe bat PyVs, and phylogenetically clustered with these viruses in each PyV genus. Correlation and virus–host relationship analysis suggested that these PyVs co-diverged with their European, African and Asian horseshoe bat hosts distributed on different continents during their evolutionary history. Additionally, assessment of selective pressures over the major capsid protein (VP1) of horseshoe bat PyVs showed sites under positive selection located in motifs exposed to the exterior of the capsid. In summary, our findings revealed a pattern of stable intrahost divergence of horseshoe bat PyVs with their mammalian hosts on the African and Eurasian continents over evolutionary time.

Funding
This study was supported by the:
  • Japan Agency for Medical Research and Development (Award JP18fm0108008)
    • Principle Award Recipient: Gabriel Gonzalez
  • Hungarian Scientific Research Fund (HU) (Award OTKA NN128309)
    • Principle Award Recipient: Márton Z. Vidovszky
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2020-07-09
2024-04-19
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References

  1. DeCaprio JA, Garcea RL. A cornucopia of human polyomaviruses. Nat Rev Microbiol 2013; 11:264–276 [View Article][PubMed]
    [Google Scholar]
  2. Moens U, Calvignac-Spencer S, Lauber C, Ramqvist T, Feltkamp MCW et al. ICTV Virus Taxonomy Profile: Polyomaviridae . J Gen Virol 2017; 98:1159–1160 [View Article][PubMed]
    [Google Scholar]
  3. Polyomaviridae Study Group of the International Committee on Taxonomy of Viruses Calvignac-Spencer S, Feltkamp MCW, Daugherty MD, Moens U et al. A taxonomy update for the family Polyomaviridae . Arch Virol 2016; 161:1739–1750 [View Article][PubMed]
    [Google Scholar]
  4. van der Meijden E, Feltkamp M. The human polyomavirus middle and alternative T-antigens; thoughts on roles and relevance to cancer. Front Microbiol 2018; 9:398 [View Article][PubMed]
    [Google Scholar]
  5. van der Meijden E, Kazem S, Dargel CA, van Vuren N, Hensbergen PJ et al. Characterization of T antigens, including middle T and alternative T, expressed by the human polyomavirus associated with Trichodysplasia Spinulosa. J Virol 2015; 89:9427–9439 [View Article][PubMed]
    [Google Scholar]
  6. Moens U, Krumbholz A, Ehlers B, Zell R, Johne R et al. Biology, evolution, and medical importance of polyomaviruses: an update. Infect Genet Evol 2017; 54:18–38 [View Article][PubMed]
    [Google Scholar]
  7. Buck CB, Van Doorslaer K, Peretti A, Geoghegan EM, Tisza MJ et al. The ancient evolutionary history of polyomaviruses. PLoS Pathog 2016; 12:e1005574 [View Article][PubMed]
    [Google Scholar]
  8. Amador LI, Moyers Arévalo RL, Almeida FC, Catalano SA, Giannini NP. Bat Systematics in the light of unconstrained analyses of a comprehensive molecular supermatrix. J Mamm Evol 2018; 25:37–70 [View Article]
    [Google Scholar]
  9. Elliott P. Bat Migrations in Europe–A Review of Banding Data and Literature. In Hutterer R, Ivanova T, Meyer-Cords C, Rodrigues L. (editors) Elsevier; 2006
  10. Rossiter SJ, Jones G, Ransome RD, Barratt EM. Parentage, reproductive success and breeding behaviour in the greater horseshoe bat (Rhinolophus ferrumequinum). Proc Biol Sci 2000; 267:545–551 [View Article][PubMed]
    [Google Scholar]
  11. Maas B, Clough Y, Tscharntke T. Bats and birds increase crop yield in tropical agroforestry landscapes. Ecol Lett 2013; 16:1480–1487 [View Article][PubMed]
    [Google Scholar]
  12. Carr MJ, Gonzalez G, Teeling EC, Sawa H. Bat Polyomaviruses: A challenge to the strict host-restriction paradigm within the mammalian Polyomaviridae . In Corrales-Aguilar E, Schwemmle M. (editors) Bats and Viruses: Current Research and Future Trends Caister Academic Press; 2020 pp 87–118
    [Google Scholar]
  13. Schneeberger K, Voigt CC. Zoonotic viruses and conservation of bats. In Voigt CC, Kingston T. (editors) Bats in the Anthropocene: Conservation of Bats in a Changing World Cham: Springer International Publishing; 2016 pp 263–292
    [Google Scholar]
  14. Tao Y, Shi M, Conrardy C, Kuzmin IV, Recuenco S et al. Discovery of diverse polyomaviruses in bats and the evolutionary history of the Polyomaviridae. J Gen Virol 2013; 94:738–748 [View Article][PubMed]
    [Google Scholar]
  15. Fagrouch Z, Sarwari R, Lavergne A, Delaval M, de Thoisy B et al. Novel polyomaviruses in South American bats and their relationship to other members of the family Polyomaviridae. J Gen Virol 2012; 93:2652–2657 [View Article][PubMed]
    [Google Scholar]
  16. Kobayashi S, Sasaki M, Nakao R, Setiyono A, Handharyani E et al. Detection of novel polyomaviruses in fruit bats in Indonesia. Arch Virol 2015; 160:1075–1082 [View Article][PubMed]
    [Google Scholar]
  17. de Sales Lima FE, Cibulski SP, Witt AA, Franco AC, Roehe PM. Genomic characterization of two novel polyomaviruses in Brazilian insectivorous bats. Arch Virol 2015; 160:1831–1836 [View Article][PubMed]
    [Google Scholar]
  18. Wang LF, Cowled C. Bats and Viruses: A New Frontier of Emerging Infectious Diseases Wiley; 2015
    [Google Scholar]
  19. Misra V, Dumonceaux T, Dubois J, Willis C, Nadin-Davis S et al. Detection of polyoma and corona viruses in bats of Canada. J Gen Virol 2009; 90:2015–2022 [View Article][PubMed]
    [Google Scholar]
  20. Carr M, Gonzalez G, Sasaki M, Dool SE, Ito K et al. Identification of the same polyomavirus species in different African horseshoe bat species is indicative of short-range host-switching events. J Gen Virol 2017; 98:2771–2785 [View Article][PubMed]
    [Google Scholar]
  21. Carr M, Gonzalez G, Sasaki M, Ito K, Ishii A et al. Discovery of African bat polyomaviruses and infrequent recombination in the large T antigen in the Polyomaviridae. J Gen Virol 2017; 98:726–738 [View Article][PubMed]
    [Google Scholar]
  22. Hutson AM, Rossiter SJ, Csorba G. Family Rhinolophidae (horseshoe bats). In Wilson DE, Mittermeier RA. (editors) Handbook of the Mammals of the World Barcelona, Spain: Lynx Edicions; 2019 pp 260–279
    [Google Scholar]
  23. Csorba G, Ujhelyi P, Thomas N. Horseshoe Bats of the World:(Chiroptera: Rhinolophidae) Alana books; 2003
    [Google Scholar]
  24. Tan Z, Gonzalez G, Sheng J, Wu J, Zhang F et al. Extensive genetic diversity of polyomaviruses in sympatric bat communities: host switching versus coevolution. J Virol 2020; 94: [View Article]
    [Google Scholar]
  25. Wu Z, Yang L, Ren X, He G, Zhang J et al. Deciphering the bat virome catalog to better understand the ecological diversity of bat viruses and the bat origin of emerging infectious diseases. ISME J 2016; 10:609–620 [View Article][PubMed]
    [Google Scholar]
  26. Vidovszky M, Kohl C, Boldogh S, Görföl T, Wibbelt G et al. Random sampling of the central European bat fauna reveals the existence of numerous hitherto unknown adenoviruses. Acta Vet Hung 2015; 63:508–525 [View Article][PubMed]
    [Google Scholar]
  27. Boldogh S. The bat fauna of the Aggtelek National Park and its surroundings (Hungary). Vespertilio 2006; 9:33–56
    [Google Scholar]
  28. Johne R, Enderlein D, Nieper H, Müller H. Novel polyomavirus detected in the feces of a chimpanzee by nested broad-spectrum PCR. J Virol 2005; 79:3883–3887 [View Article][PubMed]
    [Google Scholar]
  29. Muhire BM, Varsani A, Martin DP. SDT: a virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 2014; 9:e108277 [View Article][PubMed]
    [Google Scholar]
  30. Katoh K, Standley DM. A simple method to control over-alignment in the MAFFT multiple sequence alignment program. Bioinformatics 2016; 32:1933–1942 [View Article][PubMed]
    [Google Scholar]
  31. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 2012; 61:539–542 [View Article][PubMed]
    [Google Scholar]
  32. Carr M, Kawaguchi A, Sasaki M, Gonzalez G, Ito K et al. Isolation of a simian immunodeficiency virus from a malbrouck (Chlorocebus cynosuros). Arch Virol 2017; 162:543–548 [View Article][PubMed]
    [Google Scholar]
  33. Team RC R: A language and environment for statistical computing Vienna, Austria: R Foundation for Statistical Computing; 2014
  34. Kumar S, Stecher G, Suleski M, Hedges SB. TimeTree: a resource for timelines, timetrees, and divergence times. Mol Biol Evol 2017; 34:1812–1819 [View Article][PubMed]
    [Google Scholar]
  35. Dool SE, Puechmaille SJ, Foley NM, Allegrini B, Bastian A et al. Nuclear introns outperform mitochondrial DNA in inter-specific phylogenetic reconstruction: lessons from horseshoe bats (Rhinolophidae: Chiroptera). Mol Phylogenet Evol 2016; 97:196–212 [View Article][PubMed]
    [Google Scholar]
  36. Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res 2018; 46:W296–W303 [View Article][PubMed]
    [Google Scholar]
  37. Weaver S, Shank SD, Spielman SJ, Li M, Muse SV et al. Datamonkey 2.0: a modern web application for characterizing selective and other evolutionary processes. Mol Biol Evol 2018; 35:773–777 [View Article][PubMed]
    [Google Scholar]
  38. Smith MD, Wertheim JO, Weaver S, Murrell B, Scheffler K et al. Less is more: an adaptive branch-site random effects model for efficient detection of episodic diversifying selection. Mol Biol Evol 2015; 32:1342–1353 [View Article][PubMed]
    [Google Scholar]
  39. Gerits N, Moens U. Agnoprotein of mammalian polyomaviruses. Virology 2012; 432:316–326 [View Article][PubMed]
    [Google Scholar]
  40. Stehle T, Yan Y, Benjamin TL, Harrison SC. Structure of murine polyomavirus complexed with an oligosaccharide receptor fragment. Nature 1994; 369:160–163 [View Article][PubMed]
    [Google Scholar]
  41. Neu U, Woellner K, Gauglitz G, Stehle T. Structural basis of GM1 ganglioside recognition by simian virus 40. Proc Natl Acad Sci U S A 2008; 105:5219–5224 [View Article][PubMed]
    [Google Scholar]
  42. Neu U, Maginnis MS, Palma AS, Ströh LJ, Nelson CDS et al. Structure-Function analysis of the human JC polyomavirus establishes the LSTc pentasaccharide as a functional receptor motif. Cell Host Microbe 2010; 8:309–319 [View Article][PubMed]
    [Google Scholar]
  43. Neu U, Hengel H, Blaum BS, Schowalter RM, Macejak D et al. Structures of Merkel cell polyomavirus VP1 complexes define a sialic acid binding site required for infection. PLoS Pathog 2012; 8:e1002738 [View Article][PubMed]
    [Google Scholar]
  44. Hurdiss DL, Frank M, Snowden JS, Macdonald A, Ranson NA. The structure of an infectious human polyomavirus and its interactions with cellular receptors. Structure 2018; 26:839–847 [View Article][PubMed]
    [Google Scholar]
  45. Neu U, Wang J, Macejak D, Garcea RL, Stehle T. Structures of the major capsid proteins of the human Karolinska Institutet and Washington University polyomaviruses. J Virol 2011; 85:7384–7392 [View Article][PubMed]
    [Google Scholar]
  46. Verhalen B, Starrett GJ, Harris RS, Jiang M. Functional upregulation of the DNA cytosine deaminase APOBEC3B by polyomaviruses. J Virol 2016; 90:6379–6386 [View Article][PubMed]
    [Google Scholar]
  47. Baroja U, Garin I, Aihartza J, Arrizabalaga-Escudero A, Vallejo N et al. Pest consumption in a vineyard system by the lesser horseshoe bat (Rhinolophus hipposideros). PLoS One 2019; 14:e0219265 [View Article][PubMed]
    [Google Scholar]
  48. Mello MAR, Marquitti FMD, Kalko EKV, Kalko EKV, Jordano P et al. The missing part of seed dispersal networks: structure and robustness of bat-fruit interactions. PLoS One 2011; 6:e17395 [View Article][PubMed]
    [Google Scholar]
  49. Campanero-Rhodes MA, Smith A, Chai W, Sonnino S, Mauri L et al. N-Glycolyl GM1 ganglioside as a receptor for simian virus 40. J Virol 2007; 81:12846–12858 [View Article][PubMed]
    [Google Scholar]
  50. O'Hara SD, Stehle T, Garcea R. Glycan receptors of the Polyomaviridae: structure, function, and pathogenesis. Curr Opin Virol 2014; 7:73–78 [View Article][PubMed]
    [Google Scholar]
  51. Jin L, Gibson PE, Knowles WA, Clewley JP. BK virus antigenic variants: sequence analysis within the capsid VP1 epitope. J Med Virol 1993; 39:50–56 [View Article][PubMed]
    [Google Scholar]
  52. Erickson KD, Garcea RL, Tsai B. Ganglioside GT1b is a putative host cell receptor for the Merkel cell polyomavirus. J Virol 2009; 83:10275–10279 [View Article][PubMed]
    [Google Scholar]
  53. Murata H, Teferedegne B, Sheng L, Lewis AM, Peden K. Identification of a neutralization epitope in the VP1 capsid protein of SV40. Virology 2008; 381:116–122 [View Article][PubMed]
    [Google Scholar]
  54. Fleury MJJ, Nicol JTJ, Samimi M, Arnold F, Cazal R et al. Identification of the neutralizing epitopes of Merkel cell polyomavirus major capsid protein within the BC and EF surface loops. PLoS One 2015; 10:e0121751 [View Article][PubMed]
    [Google Scholar]
  55. Ströh LJ, Neu U, Blaum BS, Buch MHC, Garcea RL et al. Structure analysis of the major capsid proteins of human polyomaviruses 6 and 7 reveals an obstructed sialic acid binding site. J Virol 2014; 88:10831–10839 [View Article][PubMed]
    [Google Scholar]
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