1887

Abstract

Shrews (family ) have already been reported to host microorganisms pathogenic for humans. In an effort to search for additional infectious agents with zoonotic potential, we detected polyomaviruses (PyVs) in common shrew, crowned shrew, and pygmy shrew ( and ). From these, 11 full circular genomes were determined. Phylogenetic analysis based on large T protein sequences showed that these novel PyVs form a separate clade within the genus . Within this clade, the phylogenetic relationships suggest host-virus co-divergence. Surprisingly, one PyV from common shrew showed a genomic sequence nearly identical to that of the human polyomavirus 12 (HPyV12). This indicated that HPyV12 is a variant of a non-human PyV that naturally infects shrews. Whether HPyV12 is a bona fide human-tropic polyomavirus arising from a recent shrew-to-human transmission event or instead reflects a technical artefact, such as consumable contamination with shrew material, needs further investigation.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000948
2017-12-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/98/12/3060.html?itemId=/content/journal/jgv/10.1099/jgv.0.000948&mimeType=html&fmt=ahah

References

  1. 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]
  2. 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]
  3. Sharp PM, Simmonds P. Evaluating the evidence for virus/host co-evolution. Curr Opin Virol 2011; 1:436–441 [View Article][PubMed]
    [Google Scholar]
  4. Madinda NF, Ehlers B, Wertheim JO, Akoua-Koffi C, Bergl RA et al. Assessing host-virus codivergence for close relatives of merkel cell polyomavirus infecting African great apes. J Virol 2016; 90:8531–8541 [View Article][PubMed]
    [Google Scholar]
  5. Geoghegan JL, Duchêne S, Holmes EC. Comparative analysis estimates the relative frequencies of co-divergence and cross-species transmission within viral families. PLoS Pathog 2017; 13:e1006215 [View Article][PubMed]
    [Google Scholar]
  6. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D et al. Global trends in emerging infectious diseases. Nature 2008; 451:990–993 [View Article][PubMed]
    [Google Scholar]
  7. 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]
  8. Madinda NF, Robbins MM, Boesch C, Leendertz FH, Ehlers B et al. Genome sequence of a central chimpanzee-associated polyomavirus related to BK and JC polyomaviruses, Pan troglodytes troglodytes polyomavirus 1. Genome Announc 2015; 3:e00888-15 [View Article][PubMed]
    [Google Scholar]
  9. Leendertz FH, Scuda N, Cameron KN, Kidega T, Zuberbühler K et al. African great apes are naturally infected with polyomaviruses closely related to Merkel cell polyomavirus. J Virol 2011; 85:916–924 [View Article][PubMed]
    [Google Scholar]
  10. Ehlers B, Richter D, Matuschka FR, Ulrich RG. Genome sequences of a rat polyomavirus related to murine polyomavirus, Rattus norvegicus polyomavirus 1. Genome Announc 2015; 3:e00997-15 [View Article][PubMed]
    [Google Scholar]
  11. 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]
  12. 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]
  13. 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]
  14. Nainys J, Timinskas A, Schneider J, Ulrich RG, Gedvilaite A. Identification of two novel members of the tentative genus Wukipolyomavirus in wild rodents. PLoS One 2015; 10:e0140916 [View Article][PubMed]
    [Google Scholar]
  15. 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]
  16. Scuda N, Madinda NF, Akoua-Koffi C, Adjogoua EV, Wevers D et al. Novel polyomaviruses of nonhuman primates: genetic and serological predictors for the existence of multiple unknown polyomaviruses within the human population. PLoS Pathog 2013; 9:e1003429 [View Article][PubMed]
    [Google Scholar]
  17. 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]
  18. Mishra N, Pereira M, Rhodes RH, An P, Pipas JM et al. Identification of a novel polyomavirus in a pancreatic transplant recipient with retinal blindness and vasculitic myopathy. J Infect Dis 2014; 210:1595–1599 [View Article][PubMed]
    [Google Scholar]
  19. Gheit T, Dutta S, Oliver J, Robitaille A, Hampras S et al. Isolation and characterization of a novel putative human polyomavirus. Virology 2017; 506:45–54 [View Article][PubMed]
    [Google Scholar]
  20. Carey DE, Reuben R, Panicker KN, Shope RE, Myers RM. Thottapalayam virus: a presumptive arbovirus isolated from a shrew in India. Indian J Med Res 1971; 59:1758–1760[PubMed]
    [Google Scholar]
  21. Klempa B, Fichet-Calvet E, Lecompte E, Auste B, Aniskin V et al. Novel hantavirus sequences in Shrew, Guinea. Emerg Infect Dis 2007; 13:520–522 [View Article][PubMed]
    [Google Scholar]
  22. Radosa L, Schlegel M, Gebauer P, Ansorge H, Heroldová M et al. Detection of shrew-borne hantavirus in Eurasian pygmy shrew (Sorex minutus) in Central Europe. Infect Genet Evol 2013; 19:403–410 [View Article][PubMed]
    [Google Scholar]
  23. Schlegel M, Radosa L, Rosenfeld UM, Schmidt S, Triebenbacher C et al. Broad geographical distribution and high genetic diversity of shrew-borne Seewis hantavirus in Central Europe. Virus Genes 2012; 45:48–55 [View Article][PubMed]
    [Google Scholar]
  24. Hilbe M, Herrsche R, Kolodziejek J, Nowotny N, Zlinszky K et al. Shrews as reservoir hosts of borna disease virus. Emerg Infect Dis 2006; 12:675–677 [View Article][PubMed]
    [Google Scholar]
  25. Chae JS, Yu DH, Shringi S, Klein TA, Kim HC et al. Microbial pathogens in ticks, rodents and a shrew in northern Gyeonggi-do near the DMZ, Korea. J Vet Sci 2008; 9:285–293 [View Article][PubMed]
    [Google Scholar]
  26. Engbaek K, Lawson PA. Identification of Bartonella species in rodents, shrews and cats in Denmark: detection of two B. henselae variants, one in cats and the other in the long-tailed field mouse. APMIS 2004; 112:336–341 [View Article][PubMed]
    [Google Scholar]
  27. Brisson D, Dykhuizen DE, Ostfeld RS. Conspicuous impacts of inconspicuous hosts on the Lyme disease epidemic. Proc Biol Sci 2008; 275:227–235 [View Article][PubMed]
    [Google Scholar]
  28. Mayer-Scholl A, Hammerl JA, Schmidt S, Ulrich RG, Pfeffer M et al. Leptospira spp. in rodents and Shrews in Germany. Int J Environ Res Public Health 2014; 11:7562–7574 [View Article][PubMed]
    [Google Scholar]
  29. Vaughan JA, Azad AF. Acquisition of murine typhus rickettsiae by fleas. Ann N Y Acad Sci 1990; 590:70–75 [View Article][PubMed]
    [Google Scholar]
  30. Ehlers B, Dural G, Yasmum N, Lembo T, de Thoisy B et al. Novel mammalian herpesviruses and lineages within the Gammaherpesvirinae: cospeciation and interspecies transfer. J Virol 2008; 82:3509–3516 [View Article][PubMed]
    [Google Scholar]
  31. Drexler JF, Corman VM, Lukashev AN, van den Brand JM, Gmyl AP et al. Evolutionary origins of hepatitis A virus in small mammals. Proc Natl Acad Sci USA 2015; 112:15190–15195 [View Article][PubMed]
    [Google Scholar]
  32. Tsoleridis T, Onianwa O, Horncastle E, Dayman E, Zhu M et al. Discovery of novel alphacoronaviruses in European rodents and shrews. Viruses 2016; 8:84 [View Article][PubMed]
    [Google Scholar]
  33. Obiegala A, Albrecht C, Dafalla M, Drewes S, Oltersdorf C et al. Leptospira spp. in small mammals from areas with low and high human hantavirus incidences in South-West Germany. Vector Borne Zoonotic Dis 2017; 17:312–318 [View Article][PubMed]
    [Google Scholar]
  34. Carter JJ, Daugherty MD, Qi X, Bheda-Malge A, Wipf GC et al. Identification of an overprinting gene in Merkel cell polyomavirus provides evolutionary insight into the birth of viral genes. Proc Natl Acad Sci USA 2013; 110:12744–12749 [View Article][PubMed]
    [Google Scholar]
  35. Gottlieb KA, Villarreal LP. Natural biology of polyomavirus middle T antigen. Microbiol Mol Biol Rev 2001; 65:288–318 [View Article][PubMed]
    [Google Scholar]
  36. van Ghelue M, Khan MT, Ehlers B, Moens U. Genome analysis of the new human polyomaviruses. Rev Med Virol 2012; 22:354–377 [View Article][PubMed]
    [Google Scholar]
  37. Harrison C, Jiang T, Banerjee P, Meinke G, D'Abramo CM et al. Polyomavirus large T antigen binds symmetrical repeats at the viral origin in an asymmetrical manner. J Virol 2013; 87:13751–13759 [View Article][PubMed]
    [Google Scholar]
  38. Oshchepkov DY, Levitsky VG. In silico prediction of transcriptional factor-binding sites. Methods Mol Biol 2011; 760:251–267 [View Article][PubMed]
    [Google Scholar]
  39. Darriba D, Taboada GL, Doallo R, Posada D. ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 2011; 27:1164–1165 [View Article][PubMed]
    [Google Scholar]
  40. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 2010; 59:307–321 [View Article][PubMed]
    [Google Scholar]
  41. Notredame C, Higgins DG, Heringa J. T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 2000; 302:205–217 [View Article][PubMed]
    [Google Scholar]
  42. Darriba D, Taboada GL, Doallo R, Posada D. jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 2012; 9:772 [View Article][PubMed]
    [Google Scholar]
  43. Dubey S, Salamin N, Ohdachi SD, Barrière P, Vogel P. Molecular phylogenetics of shrews (Mammalia: Soricidae) reveal timing of transcontinental colonizations. Mol Phylogenet Evol 2007; 44:126–137 [View Article][PubMed]
    [Google Scholar]
  44. Yannic G, Dubey S, Hausser J, Basset P. Additional data for nuclear DNA give new insights into the phylogenetic position of Sorex granarius within the Sorex araneus group. Mol Phylogenet Evol 2010; 57:1062–1071 [View Article][PubMed]
    [Google Scholar]
  45. 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]
  46. Krumbholz A, Bininda-Emonds OR, Wutzler P, Zell R. Phylogenetics, evolution, and medical importance of polyomaviruses. Infect Genet Evol 2009; 9:784–799 [View Article][PubMed]
    [Google Scholar]
  47. 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]
  48. Erlwein O, Robinson MJ, Dustan S, Weber J, Kaye S et al. DNA extraction columns contaminated with murine sequences. PLoS One 2011; 6:e23484 [View Article][PubMed]
    [Google Scholar]
  49. Smuts H, Kew M, Khan A, Korsman S. Novel hybrid parvovirus-like virus, NIH-CQV/PHV, contaminants in silica column-based nucleic acid extraction kits. J Virol 2014; 88:1398 [View Article][PubMed]
    [Google Scholar]
  50. Naccache SN, Greninger AL, Lee D, Coffey LL, Phan T et al. The perils of pathogen discovery: origin of a novel parvovirus-like hybrid genome traced to nucleic acid extraction spin columns. J Virol 2013; 87:11966–11977 [View Article][PubMed]
    [Google Scholar]
  51. Evans GE, Murdoch DR, Anderson TP, Potter HC, George PM et al. Contamination of Qiagen DNA extraction kits with Legionella DNA. J Clin Microbiol 2003; 41:3452–3453 [View Article][PubMed]
    [Google Scholar]
  52. Korup-Schulz SV, Lucke C, Moens U, Schmuck R, Ehlers B. Large T antigen variants of human polyomaviruses 9 and 12 and seroreactivity against their N terminus. J Gen Virol 2017; 98:704–714 [View Article][PubMed]
    [Google Scholar]
  53. Scuda N, Hofmann J, Calvignac-Spencer S, Ruprecht K, Liman P et al. A novel human polyomavirus closely related to the african green monkey-derived lymphotropic polyomavirus. J Virol 2011; 85:4586–4590 [View Article][PubMed]
    [Google Scholar]
  54. ribero S, Costa C, Sidoti F, Osella‐abate S, Senetta R et al. No evidence of association of HpyV6, HpyV7, St. Louis HpyV and HpyV12 with squamous cell carcinoma. Br J Dermatol 2017; 177:e112e113 [Crossref]
    [Google Scholar]
  55. Bialasiewicz S, Rockett RJ, Barraclough KA, Leary D, Dudley KJ et al. Detection of recently discovered human polyomaviruses in a longitudinal kidney transplant cohort. Am J Transplant 2016; 16:2734–2740 [View Article][PubMed]
    [Google Scholar]
  56. Herberhold S, Hellmich M, Panning M, Bartok E, Silling S et al. Human polyomavirus and human papillomavirus prevalence and viral load in non-malignant tonsillar tissue and tonsillar carcinoma. Med Microbiol Immunol 2017; 206:93–103 [View Article][PubMed]
    [Google Scholar]
  57. Anisimova M, Gil M, Dufayard JF, Dessimoz C, Gascuel O. Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Syst Biol 2011; 60:685–699 [View Article][PubMed]
    [Google Scholar]
  58. Yannic G, Basset P, Hausser J. A new perspective on the evolutionary history of western European Sorex araneus group revealed by paternal and maternal molecular markers. Mol Phylogenet Evol 2008; 47:237–250 [View Article][PubMed]
    [Google Scholar]
  59. Rambaut A, Lam TT, Max Carvalho L, Pybus OG. Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen). Virus Evol 2016; 2:vew007 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000948
Loading
/content/journal/jgv/10.1099/jgv.0.000948
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