Skip to main content
SpringerLink
Log in

First Isolation of Pseudogymnoascus destructans, the Fungal Causative Agent of White-Nose Disease, in Bats from Italy

  • Original Article
  • Published:
Mycopathologia Aims and scope Submit manuscript

Abstract

White-nose disease, caused by the dermatophyte Pseudogymnoascus destructans, is a devastating pathology that has caused a massive decline in the US bat populations. In Europe, this fungus and the related infection in bats have been recorded in several countries and for many bat species, although no mass mortality has been detected. This study reports for the first time the presence of P. destructans in Italy. The fungus was isolated in the Rio Martino cave, a site located in the Western Alps and included in the Natura 2000 network. Twenty bats, belonging to five different species, were analysed. The fungus was retrieved on eight individuals of Myotis emarginatus. The allied keratolytic species P. pannorum was observed on two other individuals, also belonging to M. emarginatus. Strains were isolated in pure culture and characterized morphologically. Results were validated through molecular analyses. Future work should be dedicated to understand the distribution and the effects of the two Pseudogymnoascus species on Italian bats.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Warnecke L, Turner JM, Bollinger TK, Lorch JM, Misra V, Cryan PM, Wibbelt G, Blehert DS, Willis CK. Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc Natl Acad Sci USA. 2012;109(18):6999–7003.

    Article  CAS  Google Scholar 

  2. Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, Buckles EL, Coleman JT, Darling SR, Gargas A, Niver R, Okoniewski JC, Rudd RJ, Stone WB. Bat white-nose syndrome: an emerging fungal pathogen? Science. 2009;323(5911):227–227.

    Article  CAS  Google Scholar 

  3. Gargas A, Trest MT, Christensen M, Volk TJ, Blehert DS. Geomyces destructans sp. nov. associated with bat white-nose syndrome. Mycotaxon. 2009;108(1):147–54.

    Article  Google Scholar 

  4. Verant ML, Boyles JG, Waldrep W Jr, Wibbelt G, Blehert DS. Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome. PLoS ONE. 2012;7(9):e46280.

    Article  CAS  Google Scholar 

  5. Minnis AM, Lindner DL. Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biol. 2013;117(9):638–49.

    Article  Google Scholar 

  6. De Hoog GS, Guarro J, Gené J, Figueras MJ. Atlas of clinical fungi. 2nd ed. Utrecht: Centraalbureau voor Schimmelcultures; 2000.

    Google Scholar 

  7. Martínková N, Pikula J, Zukal J, Kovacova V, Bandouchova H, Bartonička T, Botvinkin AD, Brichta J, Dundarova H, Kokurewicz T, Irwin NR, Linhart P, Orlov OL, Piacek V, Škrabánek P, Tiunov MP, Zahradníková A Jr. Hibernation temperature-dependent Pseudogymnoascus destructans infection intensity in Palearctic bats. Virulence. 2018;9(1):1734–50.

    Article  Google Scholar 

  8. Meteyer CU, Buckles EL, Blehert DS, Hicks AC, Green DE, Shearn-Bochsler V, Thomas NJ, Gargas A, Behr MJ. Histopathologic criteria to confirm white-nose syndrome in bats. J Vet Diagn Invest. 2009;21:411–4.

    Article  Google Scholar 

  9. Reichard JD, Kunz TH. White-nose syndrome inflicts lasting injuries to the wings of little brown myotis (Myotis lucifugus). Acta Chiropterol. 2009;11(2):457–64.

    Article  Google Scholar 

  10. Pikula J, Amelon SK, Bandouchova H, Bartonicka T, Berkova H, Brichta J, Hooper S, Kokurewicz T, Kolarik M, Köllner B, Kovacova V, Linhart P, Piacek V, Turner GG, Zukal J, Martínková N, Swartz S. White-nose syndrome pathology grading in Nearctic and Palearctic bats. PLoS ONE. 2017;12(8):e0180435.

    Article  Google Scholar 

  11. Puechmaille SJ, Verdeyroux P, Fuller H, Gouilh MA, Bekaert M, Teeling EC. White-nose syndrome fungus (Geomyces destructans) in Bat, France. Emerg Infect Dis. 2010;16:290–3.

    Article  CAS  Google Scholar 

  12. Pikula J, Bandouchova H, Novotny L, Meteyer CU, Zukal J, Irwin NR, Zima J, Martínková N. Histopathology confirms white-nose syndrome in bats in Europe. J Wildl Dis. 2012;48(1):207–11.

    Article  Google Scholar 

  13. Voyron S, Lazzari A, Riccucci M, Calvini M, Varese GC. First mycological investigations on Italian bats. Hystrix It J Mamm. 2010;22(1):189–97.

    Google Scholar 

  14. Wibbelt G, Kurth A, Hellmann D, Weishaar M, Barlow A, Veith M, Prüger J, Görföl T, Grosche L, Bontadina F, Zöphel U, Seidl HP, Cryan PM, Blehert D. White-nose syndrome fungus (Geomyces destructans) in bats, Europe. Emerg Infect Dis. 2010;16(8):1237.

    Article  Google Scholar 

  15. Puechmaille SJ, Wibbelt G, Korn V, Fuller H, Forget F, Mühldorfer K, Kurth A, Bogdanowicz W, Borel C, Bosch T, Cherezy T, Drebet M, Görföl T, Haarsma AJ, Herhaus F, Hallart G, Hammer M, Jungmann C, Le Bris Y, Lutsar L, Masing M, Mulkens B, Passior K, Starrach M, Wojtaszewski A, Zöphel U, Teeling EC. Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality. PLoS ONE. 2011;6(4):e19167.

    Article  CAS  Google Scholar 

  16. Šimonovičov A, Pangallo D, Chovanová K, Lehotská B. Geomyces destructans associated with bat disease WNS detected in Slovakia. Biologia. 2011;66(3):562–4.

    Article  Google Scholar 

  17. Paiva-Cardoso MDN, Morinha F, Barros P, Vale-Gonçalves H, Coelho AC, Fernandes L, Travassos P, Faria AS, Bastos E, Santos M, Cabral JA. First isolation of Pseudogymnoascus destructans in bats from Portugal. Eur J Wildlife Res. 2014;60:645–9.

    Article  Google Scholar 

  18. Pavlinić I, Đaković M, Lojkić I. Pseudogymnoascus destructans in Croatia confirmed. Eur J Wildlife Res. 2015;61(2):325–8.

    Article  Google Scholar 

  19. Leopardi S, Blake D, Puechmaille SJ. White-nose syndrome fungus introduced from Europe to North America. Curr Biol. 2015;25(6):R217–9.

    Article  CAS  Google Scholar 

  20. Barlow AM, Worledge L, Miller H, Drees KP, Wright P, Foster JT, Sobek C, Borman AM, Fraser M. First confirmation of Pseudogymnoascus destructans in British bats and hibernacula. Vet Rec. 2015;177(3):73.

    Article  CAS  Google Scholar 

  21. Zukal J, Bandouchova H, Bartonička T, Berkova H, Brack V, Brichta J, Dolinay M, Jaron KS, Kovacova V, Kovarik M, Martínková N, Ondracek K, Rehák Z, Turner GG, Pikula J. White-nose syndrome fungus: a generalist pathogen of hibernating bats. PLoS ONE. 2014;9:e97224.

    Article  Google Scholar 

  22. La Magrì F. Grotta di Rio Marino (valle del Po–Piemonte). Regione Piemonte, Torino: Associazione Gruppi Speleologici Piemontesi; 2007.

    Google Scholar 

  23. Associazione Gruppi Speleologici Piemontesi, Atlante delle Aree Carsiche Piemontesi -vol. 1. Regione Piemonte, Torino, 2010.

  24. Badino G. Models of temperature, entropy production and convective airflow in caves. J Geol Soc. 2018;466:359–79.

    Google Scholar 

  25. Remoto A. I risultati delle misure di temperatura dell’aria. In: Magrì F, editor. La Grotta di Rio Martino (Valle Po–Piemonte). Regione Piemonte, Torino: Associazione Gruppi Speleologici Piemontesi; 2007. p. 53–7.

    Google Scholar 

  26. Patriarca E, Debernardi P, Grazioli F, Garzoli L, Magagnoli S. Attività finalizzate alla conoscenza, conservazione e valorizzazione sostenibile della chirotterofauna della ZSC IT1160037 Grotta di Rio Martino. Ente di gestione delle Aree protette del Monviso. 2019; pp. 43.

  27. Garzoli L, Poli A, Prigione V, Gnavi G, Varese GC. Peacock’s tail with a fungal cocktail: first assessment of the mycobiota associated with the brown alga Padina pavonica. Fungal Ecol. 2018;35:87–97.

    Article  Google Scholar 

  28. White TJ, Bruns T, Lee S, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innin SA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications. London: Academic Press; 1990. p. 315–32.

    Google Scholar 

  29. Dietz C, Kiefer A. Bats of Britain and Europe. London: Bloomsbury Publishing; 2016.

    Google Scholar 

  30. Zukal J, Bandouchova H, Brichta J, Cmokova A, Jaron KS, Kolarik M, Kovacova V, Kubátová A, Nováková A, Orlov O, Pikula J, Presetnik P, Šuba J, Zahradníková A, Martínková N. White-nose syndrome without borders: Pseudogymnoascus destructans infection tolerated in Europe and Palearctic Asia but not in North America. Sci Rep. 2016;6:19829.

    Article  CAS  Google Scholar 

  31. Wibbelt G, Puechmaille SJ, Ohlendorf B, Mühldorfer K, Bosch T, Görföl T, Passior K, Kurth A, Lacremans D, Forget F. Skin lesions in European hibernating bats associated with Geomyces destructans, the etiologic agent of white-nose syndrome. PLoS ONE. 2013;8(9):e74105.

    Article  CAS  Google Scholar 

  32. Langwig KE, Frick WF, Reynolds R, Parise KL, Drees KP, Hoyt JR, Cheng TL, Kunz TH, Foster JT, Kilpatrick AM. Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome. Proc R Soc Lond [Biol]. 2015;282:20142335.

    Article  Google Scholar 

  33. Gianni C, Caretta G, Romano C. Skin infection due to Geomyces pannorum var. pannorum. Fallbericht. Hautinfektion durch Geomyces pannorum var. pannorum. Mycoses. 2003;46(9–10):430–2.

    Article  Google Scholar 

  34. Dorland W. Dorland’s illustrated medical dictionary. 32nd ed. Philadelphia: Elsevier Health Sciences; 2011.

    Google Scholar 

  35. Venes D. Taber’s cyclopedic medical dictionary. 21st ed. West Trenton: Davis Company; 2017.

    Google Scholar 

  36. Frick WF, Puechmaille S, Jand C, Willis KR. White-nose syndrome in bats. In: Voigt CC, Kingston T, editors. Bats in the anthropocene: conservation of bats in a changing world. Heidelberg: Springer Cham; 2016. p. 245–62.

    Chapter  Google Scholar 

  37. Chaturvedi V, Chaturvedi S. Editorial: what is in a name? A proposal to use geomycosis instead of White Nose syndrome (WNS) to describe bat infection caused by Geomyces destructans. Mycopathologia. 2011;171:231–3.

    Article  Google Scholar 

  38. Kováčová V, Zukal J, Banďouchová H, Botvinkin AD, Harazim M, Martínková N, Orlov OL, Piaček V, Shumkina AP, Tiunov MP, Pikula J. White-nose syndrome detected in bats over an extensive area of Russia. BMC Vet Res. 2018;14:192.

    Article  Google Scholar 

Download references

Acknowledgements

Captures of bats were performed in the framework of bat surveys promoted and funded by the Ente di gestione delle aree protette del Monviso. Authors are grateful to Dr. Carolina Girometta and Dr. Carlo Cusaro for their support in the molecular analyses. Authors are thankful to Dr. Vishnu Chaturvedi and the anonymous reviewer, whose sound comments helped to improve the final version of the manuscript.

Author information

Authors and Affiliations

  1. Department of Earth and Environmental Sciences, University of Pavia, Via S. Epifanio 14, 27100, Pavia, PV, Italy

    L. Garzoli & A. M. Picco

  2. Zoological Section «La Specola», Museum of Natural History of the University of Florence, c/o via Maccatella 26/B, 56124, Pisa, PI, Italy

    M. Riccucci

  3. S.Te.P. c/o Museo Civ. St. Nat., via S. Francesco di Sales, 188, 10022, Carmagnola, TO, Italy

    L. Garzoli, E. Patriarca & P. Debernardi

  4. CNR-Water Research Institute (IRSA), Corso Tonolli 50, 28922, Verbania, VB, Italy

    L. Garzoli & A. Boggero

  5. School of Pharmaceutical Science and Technology, Health Sciences Platform, Tianjin University, Nankai District, Building 24, 92, Weijin Road, Tianjin, 300072, China

    L. Pecoraro

Authors
  1. L. Garzoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Riccucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. Patriarca
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. Debernardi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. Boggero
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. L. Pecoraro
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. A. M. Picco
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to L. Garzoli.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. Captures of bats were carried out under licence (Italian Environment Ministry m_amte.PNM.REGISTRO UFFICIALE.U.0007303.07-04-2017; Province of Cuneo prot. 2017/11.12/000009).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Handling editor: Vishnu Chaturvedi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Garzoli, L., Riccucci, M., Patriarca, E. et al. First Isolation of Pseudogymnoascus destructans, the Fungal Causative Agent of White-Nose Disease, in Bats from Italy. Mycopathologia 184, 637–644 (2019). https://doi.org/10.1007/s11046-019-00371-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11046-019-00371-6

Keywords

Search

Navigation