Is Bat Guano a Reservoir of Geomyces destructans?

Janez Mulec, Elizabeth Covington, Julia Walochnik

.
Karst Research Institute, Research Centre of the Slovenian Academy of Sciences and Arts, Postojna, Slovenia.

DOI: 10.4236/ojvm.2013.32025                

Abstract

Bat guano from six different karst caves in Slovenia was screened by PCR for the presence of Geomyces destructans [1]. Two identical DNA sequences from guano heaps in two of the caves with recent bat droppings were retrieved. These sequences were closely related to several unidentified Geomyces clones and to pathogenic G. destructans, but definitive identification remained elusive. Despite the presence of Geomyces species, thus far there has been no report of Whitenose syndrome (WNS) symptoms in bats in Slovenia. Overall physical and chemical conditions in guano, particularly in large guano heaps, offer a suitable environment which might serve as a reservoir for pathogenic Geomyces strains and could represent a permanent reservoir for in situ infection of bats. Screening of guano and analysis of more data related to guano ecology could lend clues to control WNS outbreaks and mortality linked to G. destructans.

Keywords

Geomyces destructans; Bat Guano; Cave; Slovenia

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	J. M. Lorch, A. Gargas, C. U. Meteyer, B. M. Berlowski-Zier, D. E. Green, V. Shearn-Bochsler, N. J. Thomas and D. S. Blehert, “Rapid Polymerase Chain Reaction Diag-nosis of White-Nose Syndrome in Bats,” Journal of Veterinary Diagnostic Investigation, Vol. 22, No. 2, 2010, pp. 224-230. doi:10.1177/104063871002200208
[2]	A. Gargas, M. T. Trest, M. Christensen, T. J. Volk and D. S. Blehert, “Geomyces destructans sp. nov. Associated with Bat White-Nose Syndrome,” Mycotaxon, Vol. 108, No. 8, 2009, pp. 147-154. doi:10.5248/108.147
[3]	V. Chaturvedi, D. J. Springer, M. J. Behr, R. Ramani, X. Li, M. R. Peck, P. Ren, D. J. Bopp, B. Wood, W. A. Samsonoff, C. M. Butchkoski, A. C. Hicks, W. B. Stone, R. J. Rudd and S. Chaturvedi, “Morphological and Molecular Characterizations of Psychrophilic Fungus Geomyces destructans from New York Bats with White Nose Syndrome (WNS),” Plos One, Vol. 5, No. 5, 2010, p. 5. doi:10.1371/journal.pone.0010783
[4]	M. L. Verant, J. G. Boyles, W. Jr. Waldrep, G. Wibbelt and D. S. Blehert, “Temperature-Dependent Growth of Geomyces destructans, the Fungus That Causes Bat White-Nose Syndrome,” Plos One, Vol, 7, No. 9, 2012, p. 9. doi:10.1371/journal.pone.0046280
[5]	D. S. Blehert, A. C. Hicks, M. Behr, C. U. Meteyer, B. M. Berlowski-Zier, E. L. Buckles, J. T. Coleman, S. R. Darling, A. Gargas, R. Niver, J. C. Okoniewski, R. J. Rudd and W. B. Stone, “Bat White-Nose Syndrome: An Emerging Fungal Pathogen?” Science, Vol. 323, No. 5911, 2009, p. 227. doi:10.1126/science.1163874
[6]	L. Warnecke, J. M. Turner, T. K. Bollinger, J. M. Lorch, V. Misra, P. M. Cryan, G. Wibbelt, D. S. Blehert and C. K. Willis, “Inoculation of Bats with European Geomyces destructans Supports the Novel Pathogen Hypothesis for the Origin of White-Nose Syndrome. Proceedings of the National Academy of Sciences of the United States of America, Vol. 109, No. 18, 2012, pp. 6999-7003. doi:10.1073/pnas.1200374109
[7]	G. Wibbelt, A. Kurth, D. Hellmann, M. Weishaar, A. Barlow, M. Veith, J. Prüger, T. Gorfol, L. Grosche, F. Bontadina, U. Zophel, H. P. Seidl, H. P. Seidl and D. S. Blehert, “White-Nose Syndrome Fungus (Geomyces destructans) in Bats, Europe,” Emerging Infectious Diseases, Vol. 16, No. 8, 2010, pp. 1237-1242. doi:10.3201/eid1608.100002
[8]	J. M. Lorch, C. U. Meteyer, M. J. Behr, J. G. Boyles, P. M. Cryan, A. C. Hicks, A. E. Ballmann, J. T. Coleman, D. N. Redell, D. M. Reeder and D. S. Blehert, “Experimental Infection of Bats with Geomyces destructans Causes White-Nose Syndrome,” Nature, Vol. 480, No. 7377, 2011, pp. 376-378. doi:10.1038/nature10590
[9]	J. Pikula, H. Bandouchova, L. Novotny, C. U. Meteyer, J. Zukal, N. R. Irwin, J. Zima and N. Martínková, “Histopathology Confirms White-Nose Syndrome in Bats in Europe,” Journal of Wildlife Diseases, Vol. 48, No. 1, 2012, pp. 207-211.
[10]	S. J. Puechmaille, G. Wibbelt, V. Korn, H. Fuller, F. Forget, K. Muhldorfer, A. Kurth, W. Bogdanowicz, C. Borel, T. Bosch, T. Cherezy, M. Drebet, T. Gorfol, A. J. Haarsma, F. Herhaus, G. Hallart, M. Hammer, C. Jungmann, Y. Le Bris, L. Lutsar, M. Masing, B. Mulkens, K. Passior, M. Starrach, A. Wojtaszewski, U. Zophel and E. C. Teeling, “Pan-European Distribution of White-Nose Syndrome Fungus (Geomyces destructans) not Associated with Mass Mortality,” Plos One, Vol. 6, No. 4, 2011, p. 4. doi:10.1371/journal.pone.0019167
[11]	S. J. Puechmaille, P. Verdeyroux, H. Fuller, M. A. Gouilh, M. Bekaert and E. C. Teeling, “White-Nose Syndrome Fungus (Geomyces destructans) in Bat, France,” Emerging Infectious Diseases, Vol. 16, No. 2, 2010, pp. 290-293. doi:10.3201/eid1602.091391
[12]	N. Martínková, P. Backor, T. Bartonicka, P. Blazková, J. Cerveny, L. Falteisek, J. Gaisler, V. Hanzal, D. Horácek, Z. Hubálek, H. Jahelková, M. Kolatik, L. Korytár, A. Kubátová, B. Lehotská, R. Lehotsky, R. K. Lucan, O. Májek, J. Mateju, Z. Rehák, J. Safar, P. Tájek, E. Tkadlec, M. Uhrin, J. Wagner, D. Weinfurtová, J. Zima, J. Zukal and I. Horácek, “Increasing Incidence of Geomyces destructans Fungus in Bats from the Czech Republic and Slovakia,” Plos One, Vol. 5, No. 11, 2010, p. 11. doi:10.1371/journal.pone.0013853
[13]	T. H. Kunz and M. B. Fenton, “Bat Ecology,” University of Chicago Press, Chicago, London, 2003.
[14]	J. M. Lorch, L. K. Muller, R. E. Russell, M. O’Connor, D. L. Lindner and D. S. Blehert, “Distribution and Environmental Persistence of the Causative Agent of White-Nose Syndrome, Geomyces destructans, in Bat Hibernacula of the Eastern United States,” Applied and Environmental Microbiology, 2012, in press.
[15]	J. M. Lorch, D. L. Lindner, A. Gargas, L. K. Muller, A. M. Minnis and D. S. Blehert, “A Culture-Based Survey of Fungi in Soil from Bat Hibernacula in the Eastern United States and its Implications for Detection of Geomyces destructans, yhe Causal Agent of Bat White-Nose Syndrome,” Mycologia, 2012, in press.
[16]	D. L. Lindner, A. Gargas, J. M. Lorch, M. T. Banik, J. Glaeser, T. H. Kunz and D. S. Blehert, “DNA-Based Detection of the Fungal Pathogen Geomyces destructans in Soils From Bat Hibernacula,” Mycologia, Vol. 103, No. 2, 2011, pp. 241-246. doi:10.3852/10-262
[17]	I. Alteras, “First Romanian Isolation of Histoplasma capsulatum from the Soil,” International Journal of Dermatology, Vol. 5, No. 2, 1966, pp. 69-71. doi:10.1111/j.1365-4362.1966.tb05188.x
[18]	B. Julg, J. Elias, A. Zahn, S. Koppen, C. Becker-Gaab and J. R. Bogner, “Bat-Associated Histoplasmosis Can Be Transmitted at Entrances of Bat Caves and Not Only inside the Caves,” Journal of Travel Medicine, Vol. 15, No. 2, pp. 133-136. doi:10.1111/j.1708-8305.2008.00193.x
[19]	V. Kristufek, D. Elhottová, L. Kovác, A. Chronáková, K. Zák and I. Svetlik, “Heap of Old Bat Guano in the Cave Domica (NP Slovak Karst) and Electron Microscopy of Bats Excrements/Stárí kopy netopyrího guana v jeskyni Domica (NP Slovensky Kras) a elektronová mikroskopie exkrementou netopyru,” Acta Carsologica Slovaca, Vol. 46, No. 1, 2008, pp. 165-172.
[20]	A. Novaková, “Microscopic Fungi Isolated from the Domica Cave System (Slovak Karst National Park, Slovakia),” International Journal of Speleology, Vol. 36, No. 1, 2007, pp. 71-82.
[21]	C. A. Dobony, K. E. Langwig, R. L. von Linden, J. C. Okoniewski, M. L. Verant, R. E. Rainbolt and A. C. Hicks, “White-Nose Syndrome: Lessons Learned at Fort Drum Military Installation, NY,” 5th Annual White-Nose Syndrome Symposium, Madison, 4-7 June 2012, p. 8.
[22]	L. K. Muller, J. M. Lorch, D. L. Lindner, M. O’Connor, A. Gargas and D. S. Blehert, “Bat White-Nose Syndrome: A Real-Time TaqMan Polymerase Chain Reaction Test Targeting the Intergenic Spacer Region of Geomyces destructans,” Mycologia, 2012, in press.
[23]	S. Chaturvedi, R. J. Rudd, A. Davis, T. R. Victor, X. Li, K. A. Appler, S. S. Rajkumar and V. Chaturvedi, “Rapid Real-Time PCR Assay for Culture and Tissue Identification of Geomyces destructans: The Etiologic Agent of Bat Geomycosis (White Nose Syndrome),” Mycopathologia, Vol. 172, No. 4, 2011, pp. 247-256. doi:10.1007/s11046-011-9435-5
[24]	P. Presetnik, K. Koselj, M. Zagmajster, N. Aupic, K. Jazbec, U. Zibrat, A. Petrinjak and A. Hudoklin, “Atlas Netopirjev (Chiroptera) Slovenije,” Center za kartografijo favne in flore, Miklavz na Dravskem polju, 2009.
[25]	A. Hudoklin and P. Presetnik, “The Cave Spodnja klevevska jama—Important Bat Roost and Newly Recorded Site of Schreiber’s Bat (Miniopterus schreibersii) in Dolenjska (South-Eastern Slovenia),” Natura Sloveniae, Vol. 7, No. 1, 2005, pp. 31-35.
[26]	J. Mulec, V. Kristufek and A. Chronáková, “Comparative Microbial Sampling From Eutrophic Caves in Slovenia and Slovakia Using RIDACOUNT Test Kits,” International Journal of Speleology, Vol. 41, No. 1, 2012, pp. 1-8. doi:10.5038/1827-806X.41.1.1
[27]	J. Mulec, V. Kristufek and A. Chroňáková, “Monitoring of Microbial Indicator Groups in Caves through the Use of RIDA COUNT Kits,” Acta Carsologica, Vol. 42, No. 2-3, 2012, pp. 287-296.
[28]	G. A. Kochkina, N. E. Ivanushkina, V. N. Akimov, D. A. Gilichinski and S. M. Ozerskaia, “Halo- and Psychrotolerant Geomyces Fungi from Arctic Cryopegs and Marine Deposits,” Mikrobiology, Vol. 76, No. 1, 2007, pp. 39-47.
[29]	L. J. Maher, “Environmental Information from Guano Palynology of Insectivorous Bats of the Central Part of the United States of America,” Palaeogeography Palaeoclimatology Palaeoecology, Vol. 237, No. 1, 2006, pp. 19-31. doi:10.1016/j.palaeo.2005.11.026
[30]	J. Mulec, J. Vaupotic and J. Walochnik, “Prokaryotic and Eukaryotic Airborne Microorganisms as Tracers of Microclimatic Changes in the Underground (Postojna Cave, Slovenia),” Microbial Ecology, Vol. 64, No. 3, 2012, pp. 654-667. doi:10.1007/s00248-012-0059-1
[31]	C. H. Robinson, “Cold Adaptation in Arctic and Antarctic Fungi,” New Phytologist, Vol. 151, No. 2, 2001, pp. 341-353. doi:10.1007/s00248-008-9387-6
[32]	S. K. Schmidt, K. L. Wilson, A. F. Meyer, M. M. Gebauer and A. J. King, “Phylogeny and Ecophysiology of Opportunistic ‘Snow Molds’ from a Subalpine Forest Ecosystem,” Microbial Ecology, Vol. 56, No. 4, 2008, pp. 681-687. doi: 10.1007/s00248-008-9387-6
[33]	A. Chronáková, A. Horák, D. Elhottová and V. Kristufek, “Diverse Archaeal Community of a Bat Guano Pile in Domica Cave (Slovak Karst, Slovakia),” Folia Microbiologica, Vol. 54, No. 5, 2009, pp. 436-446. doi:10.1007/s12223-009-0061-2
[34]	R. Shahack-Gross, F. Berna, P. Karkanas and S. Weiner, “Bat Guano and Preservation of Archaeological Remains in Cave Sites,” Journal of Archaeological Science, Vol. 31, No. 9, 2004, pp. 1259-1272. doi:10.1016/j.jas.2004.02.004
[35]	L. A. Walker, V. R. Simpson, L. Rockett, C. L. Wienburg and R. F. Shore, “Heavy Metal Contamination in Bats in Britain,” Environmental Pollution, Vol. 148, No. 2, 2007, pp. 483-490.
[36]	V. Kristufek, A. Chronáková and J. Mulec, “The Heavy Metal Content in Bat Guano Heaps in Karst Caves,” Abstract Book: 20th International Conference on Subterranean Biology, Postojna, 29 August-3 September 2010, pp. 101-102.