1887

Abstract

Polyomaviruses (PyVs) are considered to be highly host-specific in different mammalian species, with no well-supported evidence for host-switching events. We examined the species diversity and host specificity of PyVs in horseshoe bats ( spp.), a broadly distributed and highly speciose mammalian genus. We annotated six PyV genomes, comprising four new PyV species, based on pairwise identity within the large T antigen (LTAg) coding region. Phylogenetic comparisons revealed two instances of highly related PyV species, one in each of the and genera, present in different horseshoe bat host species ( and ), suggestive of short-range host-switching events. The two pairs of PyVs in different horseshoe bat host species were 99.9 and 88.8 % identical with each other over their respective LTAg coding sequences and thus constitute the same virus species. To corroborate the species identification of the bat hosts, we analysed mitochondrial and a large nuclear intron dataset derived from six independent and neutrally evolving loci for bat taxa of interest. Bayesian estimates of the ages of the most recent common ancestors suggested that the near-identical and more distantly related PyV species diverged approximately 9.1E4 (5E3–2.8E5) and 9.9E6 (4E6–18E6) years before the present, respectively, in contrast to the divergence times of the bat host species: 12.4E6 (10.4E6–15.4E6). Our findings provide evidence that short-range host-switching of PyVs is possible in horseshoe bats, suggesting that PyV transmission between closely related mammalian species can occur.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000935
2017-11-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/11/2771.html?itemId=/content/journal/jgv/10.1099/jgv.0.000935&mimeType=html&fmt=ahah

References

  1. DeCaprio J, Imperiale M, Major E. Polyomaviruses. Fields virology, 5th ed. In Knipe DM, Howley PM. (eds) vol. 2 Philadelpha: Lippincott Williams & Wilkins; 2013 pp. 1633–1661
    [Google Scholar]
  2. 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]
  3. Calvignac-Spencer S, Feltkamp MC, Daugherty MD, Moens U, Ramqvist T et al. A taxonomy update for the family Polyomaviridae. Arch Virol 2016; 161:1739–1750 [View Article][PubMed]
    [Google Scholar]
  4. 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]
  5. Pérez-Losada M, Christensen RG, Mcclellan DA, Adams BJ, Viscidi RP et al. Comparing phylogenetic codivergence between polyomaviruses and their hosts. J Virol 2006; 80:5663–5669 [View Article][PubMed]
    [Google Scholar]
  6. Garcea RL, Imperiale MJ. Simian virus 40 infection of humans. J Virol 2003; 77:5039–5045 [View Article][PubMed]
    [Google Scholar]
  7. López-Ríos F, Illei PB, Rusch V, Ladanyi M. Evidence against a role for SV40 infection in human mesotheliomas and high risk of false-positive PCR results owing to presence of SV40 sequences in common laboratory plasmids. Lancet 2004; 364:1157–1166 [View Article][PubMed]
    [Google Scholar]
  8. Delbue S, Tremolada S, Branchetti E, Elia F, Gualco E et al. First identification and molecular characterization of lymphotropic polyomavirus in peripheral blood from patients with leukoencephalopathies. J Clin Microbiol 2008; 46:2461–2462 [View Article][PubMed]
    [Google Scholar]
  9. Guerin JL, Gelfi J, Dubois L, Vuillaume A, Boucraut-Baralon C et al. A novel polyomavirus (goose hemorrhagic polyomavirus) is the agent of hemorrhagic nephritis enteritis of geese. J Virol 2000; 74:4523–4529 [View Article][PubMed]
    [Google Scholar]
  10. Corrand L, Gelfi J, Albaric O, Etievant M, Pingret JL et al. Pathological and epidemiological significance of goose haemorrhagic polyomavirus infection in ducks. Avian Pathol 2011; 40:355–360 [View Article][PubMed]
    [Google Scholar]
  11. Johne R, Müller H. Polyomaviruses of birds: etiologic agents of inflammatory diseases in a tumor virus family. J Virol 2007; 81:11554–11559 [View Article][PubMed]
    [Google Scholar]
  12. Wang LF, Walker PJ, Poon LL. Mass extinctions, biodiversity and mitochondrial function: are bats 'special' as reservoirs for emerging viruses?. Curr Opin Virol 2011; 1:649–657 [View Article][PubMed]
    [Google Scholar]
  13. O'Shea TJ, Cryan PM, Cunningham AA, Fooks AR, Hayman DT et al. Bat flight and zoonotic viruses. Emerg Infect Dis 2014; 20:741–745 [View Article][PubMed]
    [Google Scholar]
  14. Luis AD, Hayman DT, O'Shea TJ, Cryan PM, Gilbert AT et al. A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special?. Proc Biol Sci 2013; 280:20122753 [View Article][PubMed]
    [Google Scholar]
  15. 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]
  16. 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]
  17. 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]
  18. 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]
  19. Wang J, Moore NE, Murray ZL, Mcinnes K, White DJ et al. Discovery of novel virus sequences in an isolated and threatened bat species, the New Zealand lesser short-tailed bat (Mystacina tuberculata). J Gen Virol 2015; 96:2442–2452 [View Article][PubMed]
    [Google Scholar]
  20. 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]
  21. 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]
  22. Wilson DE, Reeder DM. Mammal Species of the World: A Taxonomic and Geographic Reference Baltimore, Maryland: JHU Press; 2005
    [Google Scholar]
  23. Csorba G, Ujhelyi P, Thomas N. Horseshoe Bats of the World: (Chiroptera: Rhinolophidae) Shropshire: Alana Books; 2003
    [Google Scholar]
  24. 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]
  25. Stoffberg S, Jacobs DS, Mackie IJ, Matthee CA. Molecular phylogenetics and historical biogeography of Rhinolophus bats. Mol Phylogenet Evol 2010; 54:1–9 [View Article][PubMed]
    [Google Scholar]
  26. Foley NM, Thong VD, Soisook P, Goodman SM, Armstrong KN et al. How and why overcome the impediments to resolution: lessons from rhinolophid and hipposiderid bats. Mol Biol Evol 2015; 32:313–333 [View Article][PubMed]
    [Google Scholar]
  27. Yamaguchi H, Kobayashi S, Ishii A, Ogawa H, Nakamura I et al. Identification of a novel polyomavirus from vervet monkeys in Zambia. J Gen Virol 2013; 94:1357–1364 [View Article][PubMed]
    [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. Orba Y, Kobayashi S, Nakamura I, Ishii A, Hang'ombe BM et al. Detection and characterization of a novel polyomavirus in wild rodents. J Gen Virol 2011; 92:789–795 [View Article][PubMed]
    [Google Scholar]
  30. Gerits N, Moens U. Agnoprotein of mammalian polyomaviruses. Virology 2012; 432:316–326 [View Article][PubMed]
    [Google Scholar]
  31. Nieva JL, Madan V, Carrasco L. Viroporins: structure and biological functions. Nat Rev Microbiol 2012; 10:563–574 [View Article][PubMed]
    [Google Scholar]
  32. Suzuki T, Orba Y, Makino Y, Okada Y, Sunden Y et al. Viroporin activity of the JC polyomavirus is regulated by interactions with the adaptor protein complex 3. Proc Natl Acad Sci USA 2013; 110:18668–18673 [View Article][PubMed]
    [Google Scholar]
  33. Conow C, Fielder D, Ovadia Y, Libeskind-Hadas R. Jane: a new tool for the cophylogeny reconstruction problem. Algorithms Mol Biol 2010; 5:16 [View Article][PubMed]
    [Google Scholar]
  34. Legendre P, Desdevises Y, Bazin E. A statistical test for host-parasite coevolution. Syst Biol 2002; 51:217–234 [View Article][PubMed]
    [Google Scholar]
  35. Wertheim JO, Kosakovsky Pond SL. Purifying selection can obscure the ancient age of viral lineages. Mol Biol Evol 2011; 28:3355–3365 [View Article][PubMed]
    [Google Scholar]
  36. Anthony SJ, Islam A, Johnson C, Navarrete-Macias I, Liang E et al. Non-random patterns in viral diversity. Nat Commun 2015; 6:8147 [View Article][PubMed]
    [Google Scholar]
  37. Antonsson A, Hansson BG. Healthy skin of many animal species harbors papillomaviruses which are closely related to their human counterparts. J Virol 2002; 76:12537–12542 [View Article][PubMed]
    [Google Scholar]
  38. Pimenoff VN, de Oliveira CM, Bravo IG. Transmission between archaic and modern human ancestors during the evolution of the oncogenic human Papillomavirus 16. Mol Biol Evol 2017; 34:4–19 [View Article][PubMed]
    [Google Scholar]
  39. García-Pérez R, Ibáñez C, Godínez JM, Aréchiga N, Garin I et al. Novel papillomaviruses in free-ranging Iberian bats: no virus-host co-evolution, no strict host specificity, and hints for recombination. Genome Biol Evol 2014; 6:94–104 [View Article][PubMed]
    [Google Scholar]
  40. Decaprio JA, Garcea RL. A cornucopia of human polyomaviruses. Nat Rev Microbiol 2013; 11:264–276 [View Article][PubMed]
    [Google Scholar]
  41. De Gascun CF, Carr MJ. Human polyomavirus reactivation: disease pathogenesis and treatment approaches. Clin Dev Immunol 2013; 2013:1–27 [View Article][PubMed]
    [Google Scholar]
  42. Hahn BH, Shaw GM, de Cock KM, Sharp PM. AIDS as a zoonosis: scientific and public health implications. Science 2000; 287:607–614 [View Article][PubMed]
    [Google Scholar]
  43. Webby RJ, Webster RG. Emergence of influenza A viruses. Philos T R Soc B 2001; 356:1817–1828 [Crossref]
    [Google Scholar]
  44. Woolhouse ME, Gowtage-Sequeria S. Host range and emerging and reemerging pathogens. Emerg Infect Dis 2005; 11:1842–1847 [View Article][PubMed]
    [Google Scholar]
  45. Woolhouse ME, Haydon DT, Antia R. Emerging pathogens: the epidemiology and evolution of species jumps. Trends Ecol Evol 2005; 20:238–244 [View Article][PubMed]
    [Google Scholar]
  46. Longdon B, Hadfield JD, Webster CL, Obbard DJ, Jiggins FM. Host phylogeny determines viral persistence and replication in novel hosts. PLoS Pathog 2011; 7:e1002260 [View Article][PubMed]
    [Google Scholar]
  47. Baer GM, Shaddock JH, Quirion R, Dam TV, Lentz TL. Rabies susceptibility and acetylcholine receptor. Lancet 1990; 335:664–665 [View Article][PubMed]
    [Google Scholar]
  48. Rota PA, Oberste MS, Monroe SS, Nix WA, Campagnoli R et al. Characterization of a novel coronavirus associated with severe acute respiratory syndrome. Science 2003; 300:1394–1399 [View Article][PubMed]
    [Google Scholar]
  49. Guan Y, Zheng BJ, He YQ, Liu XL, Zhuang ZX et al. Isolation and characterization of viruses related to the SARS coronavirus from animals in southern China. Science 2003; 302:276–278 [View Article][PubMed]
    [Google Scholar]
  50. Kan B, Wang M, Jing H, Xu H, Jiang X et al. Molecular evolution analysis and geographic investigation of severe acute respiratory syndrome coronavirus-like virus in palm civets at an animal market and on farms. J Virol 2005; 79:11892–11900 [View Article][PubMed]
    [Google Scholar]
  51. Lau SK, Woo PC, Li KS, Huang Y, Tsoi HW et al. Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci USA 2005; 102:14040–14045 [View Article][PubMed]
    [Google Scholar]
  52. Li W, Shi Z, Yu M, Ren W, Smith C et al. Bats are natural reservoirs of SARS-like coronaviruses. Science 2005; 310:676–679 [View Article][PubMed]
    [Google Scholar]
  53. Yuan J, Hon CC, Li Y, Wang D, Xu G et al. Intraspecies diversity of SARS-like coronaviruses in Rhinolophus sinicus and its implications for the origin of SARS coronaviruses in humans. J Gen Virol 2010; 91:1058–1062 [View Article][PubMed]
    [Google Scholar]
  54. Wang L, Fu S, Cao Y, Zhang H, Feng Y et al. Discovery and genetic analysis of novel coronaviruses in least horseshoe bats in southwestern China. Emerg Microbes Infect 2017; 6:e14 [View Article][PubMed]
    [Google Scholar]
  55. Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P et al. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 2014; 346:1320–1331 [View Article][PubMed]
    [Google Scholar]
  56. Zhong S, Randhawa PS, Ikegaya H, Chen Q, Zheng HY et al. Distribution patterns of BK polyomavirus (BKV) subtypes and subgroups in American, European and Asian populations suggest co-migration of BKV and the human race. J Gen Virol 2009; 90:144–152 [View Article][PubMed]
    [Google Scholar]
  57. Ikegaya H, Saukko PJ, Tertti R, Metsärinne KP, Carr MJ et al. Identification of a genomic subgroup of BK polyomavirus spread in European populations. J Gen Virol 2006; 87:3201–3208 [View Article][PubMed]
    [Google Scholar]
  58. Yogo Y, Sugimoto C, Zheng HY, Ikegaya H, Takasaka T et al. JC virus genotyping offers a new paradigm in the study of human populations. Rev Med Virol 2004; 14:179–191 [View Article][PubMed]
    [Google Scholar]
  59. Agostini HT, Deckhut A, Jobes DV, Girones R, Schlunck G et al. Genotypes of JC virus in East, Central and Southwest Europe. J Gen Virol 2001; 82:1221–1331 [View Article][PubMed]
    [Google Scholar]
  60. Shackelton LA, Rambaut A, Pybus OG, Holmes EC. JC virus evolution and its association with human populations. J Virol 2006; 80:9928–9933 [View Article][PubMed]
    [Google Scholar]
  61. Francis CM, Borisenko AV, Ivanova NV, Eger JL, Lim BK et al. The role of DNA barcodes in understanding and conservation of mammal diversity in southeast Asia. PLoS One 2010; 5:e12575 [View Article][PubMed]
    [Google Scholar]
  62. Taylor PJ, Stoffberg S, Monadjem A, Schoeman MC, Bayliss J et al. Four new bat species (Rhinolophus hildebrandtii complex) reflect plio-pleistocene divergence of dwarfs and giants across an Afromontane archipelago. PLoS One 2012; 7:e41744 [View Article][PubMed]
    [Google Scholar]
  63. Olival KJ, Hayman DT. Filoviruses in bats: current knowledge and future directions. Viruses 2014; 6:1759–1788 [View Article][PubMed]
    [Google Scholar]
  64. Ishii A, Ueno K, Orba Y, Sasaki M, Moonga L et al. A nairovirus isolated from African bats causes haemorrhagic gastroenteritis and severe hepatic disease in mice. Nat Commun 2014; 5:5651 [View Article][PubMed]
    [Google Scholar]
  65. Korup S, Rietscher J, Calvignac-Spencer S, Trusch F, Hofmann J et al. Identification of a novel human polyomavirus in organs of the gastrointestinal tract. PLoS One 2013; 8:e58021 [View Article][PubMed]
    [Google Scholar]
  66. The Zambia Wildlife Act, 1998 (No. 12 of 1998), 12 (1998) (URL accessed 14 June 2017). Database: FAOLEX, LEX-FAOC050734
  67. 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]
  68. Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 2013; 30:772–780 [View Article][PubMed]
    [Google Scholar]
  69. 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]
  70. 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]
  71. Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014; 30:1312–1313 [View Article][PubMed]
    [Google Scholar]
  72. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 2012; 29:1969–1973 [View Article][PubMed]
    [Google Scholar]
  73. Perelman P, Johnson WE, Roos C, Seuánez HN, Horvath JE et al. A molecular phylogeny of living primates. PLoS Genet 2011; 7:e1001342 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000935
Loading
/content/journal/jgv/10.1099/jgv.0.000935
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error