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Broad geographical distribution and high genetic diversity of shrew-borne Seewis hantavirus in Central Europe

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Abstract

For a long time hantaviruses were believed to be exclusively rodent-borne pathogens. Recent findings of numerous shrew- and mole-borne hantaviruses raise important questions on their phylogenetic origin. The objective of our study was to prove the presence and distribution of shrew-associated Seewis virus (SWSV) in different Sorex species in Central Europe. Therefore, a total of 353 Sorex araneus, 59 S. minutus, 27 S. coronatus, and one S. alpinus were collected in Germany, the Czech Republic, and Slovakia. Screening by hantavirus-specific L-segment RT-PCR revealed specific amplification products in tissues of 49 out of 353 S. araneus and four out of 59 S. minutus. S-segment sequences were obtained for 45 of the L-segment positive S. araneus and all four L-segment positive S. minutus. Phylogenetic investigation of these sequences from Germany, the Czech Republic, and Slovakia demonstrated their similarity to SWSV sequences from Hungary, Finland, Austria, and other sites in Germany. The low intra-cluster sequence variability and the high inter-cluster divergence suggest a long-term SWSV evolution in isolated Sorex populations. In 28 of the 49 SWSV S-segment sequences, an additional putative open reading frame (ORF) on the opposite strand to the nucleocapsid protein-encoding ORF was identified. This is the first comprehensive sequence analysis of SWSV strains from Germany, the Czech Republic, and Slovakia, indicating its broad geographical distribution and high genetic divergence. Future studies have to prove whether both S. araneus and S. minutus represent SWSV reservoir hosts or spillover infections are responsible for the parallel molecular detection of SWSV in both species.

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References

  1. D.E. Carey, R. Reuben, K.N. Panicker, R.E. Shope, R.M. Myers, Indian J. Med. Res. 59, 1758–1760 (1971)

    PubMed  CAS  Google Scholar 

  2. J.W. Song, L.J. Baek, C.S. Schmaljohn, R. Yanagihara, Emerg. Infect. Dis. 13, 980–985 (2007)

    Article  PubMed  CAS  Google Scholar 

  3. B. Klempa, E. Fichet-Calvet, E. Lecompte, B. Auste, V. Aniskin, H. Meisel, P. Barriere, L. Koivogui, J. ter Meulen, D.H. Kruger, Emerg. Infect. Dis. 13, 520–522 (2007)

    Article  PubMed  CAS  Google Scholar 

  4. J.W. Song, H.J. Kang, S.H. Gu, S.S. Moon, S.N. Bennett, K.J. Song, L.J. Baek, H.C. Kim, M.L. O’Guinn, S.T. Chong, T.A. Klein, R. Yanagihara, J. Virol. 83, 6184–6191 (2009)

    Article  PubMed  CAS  Google Scholar 

  5. H.J. Kang, B. Kadjo, S. Dubey, F. Jacquet, R. Yanagihara, Virol. J. 8, 373 (2011)

    Article  PubMed  Google Scholar 

  6. J.W. Song, H.J. Kang, K.J. Song, T.T. Truong, S.N. Bennett, S. Arai, N.U. Truong, R. Yanagihara, Emerg. Infect. Dis. 13, 1784–1787 (2007)

    Article  PubMed  CAS  Google Scholar 

  7. S. Arai, J.W. Song, L. Sumibcay, S.N. Bennett, V.R. Nerurkar, C. Parmenter, J.A. Cook, T.L. Yates, R. Yanagihara, Emerg. Infect. Dis. 13, 1420–1423 (2007)

    Article  PubMed  CAS  Google Scholar 

  8. S. Arai, S.N. Bennett, L. Sumibcay, J.A. Cook, J.W. Song, A. Hope, C. Parmenter, V.R. Nerurkar, T.L. Yates, R. Yanagihara, Am. J. Trop. Med. Hyg. 78, 348–351 (2008)

    PubMed  CAS  Google Scholar 

  9. H.J. Kang, S. Arai, A.G. Hope, J.A. Cook, R. Yanagihara, Vector Borne Zoonotic Dis. 10, 593–597 (2010)

    Article  PubMed  Google Scholar 

  10. S. Arai, S.D. Ohdachi, M. Asakawa, H.J. Kang, G. Mocz, J. Arikawa, N. Okabe, R. Yanagihara, Proc. Natl. Acad. Sci. USA 105, 16296–16301 (2008)

    Article  PubMed  CAS  Google Scholar 

  11. H.J. Kang, S.N. Bennett, L. Dizney, L. Sumibcay, S. Arai, L.A. Ruedas, J.W. Song, R. Yanagihara, Virology 388, 8–14 (2009)

    Article  PubMed  Google Scholar 

  12. H.J. Kang, S.N. Bennett, L. Sumibcay, S. Arai, A.G. Hope, G. Mocz, J.W. Song, J.A. Cook, R. Yanagihara, PLoS ONE 4, e6149 (2009)

    Article  PubMed  Google Scholar 

  13. H.J. Kang, S.N. Bennett, A.G. Hope, J.A. Cook, R. Yanagihara, J. Virol. 85, 7496 (2011)

    Article  PubMed  CAS  Google Scholar 

  14. S. Weiss, P.T. Witkowski, B. Auste, K. Nowak, N. Weber, J. Fahr, J.V. Mombouli, N.D. Wolfe, J.F. Drexler, C. Drosten, B. Klempa, F.H. Leendertz, D.H. Kruger, Emerg. Infect. Dis. 18, 159–161 (2012)

    Article  PubMed  Google Scholar 

  15. L. Sumibcay, B. Kadjo, S.H. Gu, H.J. Kang, B.K. Lim, J.A. Cook, J.W. Song, R. Yanagihara, Virol. J. 9, 34 (2012)

    Article  PubMed  Google Scholar 

  16. D.H. Kruger, G. Schonrich, B. Klempa, Hum. Vaccin. 7, 685 (2011)

    Article  PubMed  Google Scholar 

  17. J.W. Song, S.H. Gu, S.N. Bennett, S. Arai, M. Puorger, M. Hilbe, R. Yanagihara, Virol. J. 4, 114 (2007)

    Article  PubMed  Google Scholar 

  18. H.J. Kang, S. Arai, A.G. Hope, J.W. Song, J.A. Cook, R. Yanagihara, Virol. J. 6, 208 (2009)

    Article  PubMed  Google Scholar 

  19. L.N. Yashina, S.A. Abramov, V.V. Gutorov, T.A. Dupal, A.V. Krivopalov, V.V. Panov, G.A. Danchinova, V.V. Vinogradov, E.M. Luchnikova, J. Hay, H.J. Kang, R. Yanagihara, Vector Borne Zoonotic Dis. 10, 585–591 (2010)

    Article  PubMed  Google Scholar 

  20. B. Klempa, E. Fichet-Calvet, E. Lecompte, B. Auste, V. Aniskin, H. Meisel, C. Denys, L. Koivogui, J. ter Meulen, D.H. Kruger, Emerg. Infect. Dis. 12, 838–840 (2006)

    Article  PubMed  Google Scholar 

  21. M. Schlegel, E. Kindler, S.S. Essbauer, R. Wolf, J. Thiel, M.H. Groschup, G. Heckel, R.M. Oehme, R.G. Ulrich, Vector Borne Zoonotic Dis. (2012)

  22. P. Taberlet, L. Fumagalli, A.G. Wust-Saucy, J.F. Cosson, Mol. Ecol. 7, 453–464 (1998)

    Article  PubMed  CAS  Google Scholar 

  23. G. Yannic, P. Basset, J. Hausser, Mol. Phylogenet. Evol. 47, 237–250 (2008)

    Article  PubMed  CAS  Google Scholar 

  24. M. Schlegel, H.S. Ali, N. Stieger, M.H. Groschup, R. Wolf, R.G. Ulrich, Biochem. Genet. (2011)

  25. F. Spitzenberger, H.M. Steiner, Bonn Zool Beitr 18, 258–296 (1967)

    Google Scholar 

  26. S. Churchfield, L. Rychlik, J. Zool. 269, 381–390 (2006)

    Article  Google Scholar 

  27. M. Stanko, L. Mošanský, Lynx 30, 101–111 (1999)

    Google Scholar 

  28. J. Schmidt-Chanasit, S. Essbauer, R. Petraityte, K. Yoshimatsu, K. Tackmann, F.J. Conraths, K. Sasnauskas, J. Arikawa, A. Thomas, M. Pfeffer, J.J. Scharninghausen, W. Splettstoesser, M. Wenk, G. Heckel, R.G. Ulrich, J. Virol. 84, 459–474 (2010)

    Article  PubMed  CAS  Google Scholar 

  29. M. Schlegel, B. Klempa, B. Auste, M. Bemmann, J. Schmidt-Chanasit, T. Buchner, M.H. Groschup, M. Meier, A. Balkema-Buschmann, H. Zoller, D.H. Kruger, R.G. Ulrich, Emerg. Infect. Dis. 15, 2017–2020 (2009)

    Article  PubMed  Google Scholar 

  30. M. Weidmann, P. Schmidt, M. Vackova, K. Krivanec, P. Munclinger, F.T. Hufert, J. Clin. Microbiol. 43, 808–812 (2005)

    Article  PubMed  CAS  Google Scholar 

  31. B. Hjelle, T. Yates, Curr. Top. Microbiol. Immunol. 256, 77–90 (2001)

    Article  PubMed  CAS  Google Scholar 

  32. C. Ramsden, F.L. Melo, L.M. Figueiredo, E.C. Holmes, P.M. Zanotto, Mol. Biol. Evol. 25, 1488–1492 (2008)

    Article  PubMed  CAS  Google Scholar 

  33. A. Plyusnin, S.P. Morzunov, Curr. Top. Microbiol. Immunol. 256, 47–75 (2001)

    Article  PubMed  CAS  Google Scholar 

  34. K.M. Jaaskelainen, P. Kaukinen, E.S. Minskaya, A. Plyusnina, O. Vapalahti, R.M. Elliott, F. Weber, A. Vaheri, A. Plyusnin, J. Med. Virol. 79, 1527–1536 (2007)

    Article  PubMed  CAS  Google Scholar 

  35. F. Ronquist, J.P. Huelsenbeck, Bioinformatics 19, 1572–1574 (2003)

    Article  PubMed  CAS  Google Scholar 

  36. K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, S. Kumar, Mol. Biol. Evol. (2011)

  37. D. Posada, Mol. Biol. Evol. 25, 1253–1256 (2008)

    Article  PubMed  CAS  Google Scholar 

  38. D.P. Martin, P. Lemey, M. Lott, V. Moulton, D. Posada, P. Lefeuvre, Bioinformatics 26, 2462–2463 (2010)

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors kindly acknowledge the support of Andreas Gehrke, Anne Balkema-Buschmann, Daniel Balkema, Christian Imholt, Christian Kiffner, Daniel Masur, Daniela Reil, Dietmar Haschenz, Dietrich Heidecke, Dörte Kaufmann, Ferdinand Rühe, Hans-Joachim Pelz, Hermann Ansorge, Hinrich Zoller, Ingolf Stodian, Jana Eccard, Jens Jacob, Jörg Thiel, Jona Freise, Jonas Schmidt-Chanasit, Kati Sevke, Margrit Bemmann, Matthias Tzschoppe, Matthias Wenk, Mechthild Budde, Michael Stubbe, Peter Jork, Peter Liesegang, Ronny Wolf, Sandra Blome, Thilo Liesenjohann, Thomas Büchner, Torsten Heidecke, Wolfgang Wegener for animal trapping, Bärbel Hammerschmidt, Christian Kretzschmar, Christina Maresch, Daniel Windolph, Denny Maaz, Hanan Sheikh Ali, Henrike Gregersen, Josephine Schlosser, Josephine Schröter, Julie Elkins, Konrad Wanka, Lena Buschke, Marc Mertens, Nicole Stieger, Paul Dremsek, Ramona Spließ, Theres Wollny, Ulrike Duve, Ute Wessels for animal necropsy and Franziska Thomas and Nicole Schmidt for technical assistance. This work was supported by the German Federal Ministry of Food, Agriculture and Consumer Protection (BMELV) through the Federal Institute for Agriculture and Nutrition (BLE), Grant number 07HS027 (contract no.: 506122), the Robert Koch-Institut with funds of the German Ministry of Public Health (grant no. 1362/1-924, 1362/1-980,1369-382, 1369-435), the Federal Environment Agency (Grant No. 3710 63 401), the Slovak Research and Development Agency (under the contract No. APVV-0267-10). In addition, this study was partially funded by EU Grant FP7-261504 EDENext and is cataloged by the EDENext Steering Committee as EDENext016 (http://www.edenext.eu). The contents of this publication are the sole responsibility of the authors and don’t necessarily reflect the views of the European Commission.

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Authors and Affiliations

  1. Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, OIE Collaborating Centre for Zoonoses in Europe, Institute for Novel and Emerging Infectious Diseases, Südufer 10, 17493, Greifswald-Insel Riems, Germany

    Mathias Schlegel, Ulrike M. Rosenfeld, Sabrina Schmidt, Martin H. Groschup & Rainer G. Ulrich

  2. Institute of Medical Virology, Helmut-Ruska-Haus, Charité University Hospital, Berlin, Germany

    Lukáš Radosa, Detlev H. Krüger & Boris Klempa

  3. Bayerische Landesanstalt für Wald und Forstwirtschaft, Freising, Germany

    Cornelia Triebenbacher

  4. Mücke-Merlau, Vogelsbergkreis, Germany

    Paul-Walter Löhr

  5. Landesbetrieb Forst Brandenburg, Oberförsterei Neustadt, Revier Dreetz, Germany

    Dieter Fuchs

  6. Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Brno, Czech Republic

    Marta Heroldová & Eva Jánová

  7. Institute of Zoology, Slovak Academy of Sciences, Bratislava, Slovakia

    Michal Stanko

  8. Institute of Parasitology, Slovak Academy of Sciences, Košice, Slovakia

    Michal Stanko, Ladislav Mošanský & Jana Fričová

  9. National Institute of Public Health, Prague and National Reference Laboratory for Monitoring of Environmental Biotic Factors, Brno, Czech Republic

    Milan Pejčoch

  10. Institute of Forest Ecology, Mendel University, Brno, Czech Republic

    Josef Suchomel & Luboš Purchart

  11. Institute of Virology, Slovak Academy of Sciences, Bratislava, Slovakia

    Lukáš Radosa & Boris Klempa

Authors
  1. Mathias Schlegel
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  2. Lukáš Radosa
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  3. Ulrike M. Rosenfeld
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  4. Sabrina Schmidt
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  5. Cornelia Triebenbacher
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  6. Paul-Walter Löhr
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  7. Dieter Fuchs
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  11. Ladislav Mošanský
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  13. Milan Pejčoch
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  14. Josef Suchomel
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  16. Martin H. Groschup
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  17. Detlev H. Krüger
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  18. Boris Klempa
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  19. Rainer G. Ulrich
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Correspondence to Rainer G. Ulrich.

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Schlegel, M., Radosa, L., Rosenfeld, U.M. et al. Broad geographical distribution and high genetic diversity of shrew-borne Seewis hantavirus in Central Europe. Virus Genes 45, 48–55 (2012). https://doi.org/10.1007/s11262-012-0736-7

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  • DOI: https://doi.org/10.1007/s11262-012-0736-7

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