The recently identified causative agent of white-nose syndrome (WNS), Pseudogymnoascus destructans, has been implicated in the mortality of an estimated 5.5 million North American bats since its initial documentation in 2006 (Frick et al. in Science 329:679–682, 2010). In an effort to identify potential biological and chemical control options for WNS, 6 previously described bacterially produced volatile organic compounds (VOCs) were screened for anti-P. destructans activity. The compounds include decanal; 2-ethyl-1-hexanol; nonanal; benzothiazole; benzaldehyde; andN,N-dimethyloctylamine. P. destructans conidia and mycelial plugs were exposed to the VOCs in a closed air space at 15 and 4 °C and then evaluated for growth inhibition. All VOCs inhibited growth from conidia as well as inhibiting radial mycelial extension, with the greatest effect at 4 °C. Studies of the ecology of fungistatic soils and the natural abundance of the fungistatic VOCs present in these environments suggest a synergistic activity of select VOCs may occur. The evaluation of formulations of two or three VOCs at equivalent concentrations was supportive of synergistic activity in several cases. The identification of bacterially produced VOCs with anti-P. destructans activity indicates disease-suppressive and fungistatic soils as a potentially significant reservoir of biological and chemical control options for WNS and provides wildlife management personnel with tools to combat this devastating disease.
This is a preview of subscription content, access via your institution.
Buy single article
Instant access to the full article PDF.
Tax calculation will be finalised during checkout.
Ballman A, Benedict L, Britzke E, Castle K, Cottrell W, Cryan P, DeLiberto T, Elliot A, Ewing R, Hicks A, Reynolds R, Rubado J, Slack B, Williams L, Coleman J. A national plan for assisting states, federal agencies, and tribes in managing white-nose syndrome in bats. 2011: whitenosesyndrom.org.
Blehert DS, Hicks AC, Behr M. Bat white-nose syndrome: an emerging fungal pathogen? Science. 2008;323:227.
Boyles JG, Willis C. Could localized warm areas inside cold caves reduce mortality of hibernating bats affected by white-nose syndrome? Front Ecol Environ. 2010;8:92–8.
Boyles JG, Cryan PM, McCracken GF, Kunz TH. Economic importance of bats in agriculture. Science. 2011;332:41–2.
Casadevall A. Fungal virulence, vertebrate endothermy, and dinosaur extinction: is there a connection? Fungal Genet Biol. 2005;42:98–106.
Chaturvedi S, Rajkumar SS, Li X, Hurteau GJ, Shtutman M, Chaturvedi V. Antifungal testing and high-throughput screening of compound library against Geomyces destructans, the etiologic agent of Geomycosis (WNS) in bats. PLoS ONE. 2011;6:e17032. doi:10.1371/journal.pone.0017032.
Chuankun X, Minghe M, Leming Z, Keqin Z. Soil volatile fungistasis and volatile fungistatic compounds. Soil Biol Biochem. 2004;36:1997–2004.
Cryan P, Meteyer CU, Boyles J, Blehert DS. Wing pathology of white-nose syndrome in bats suggests life threatening disruption of physiology. BMC Biol. 2010;8:135.
Cryan P. White-nose syndrome threatens the survival of hibernating bats in North America. In: USGS Fort Collins Science Center. 2011. Retrieved 21 Apr 2012.
Ezra D, Strobel GA. Effect of substrate on the bioactivity of volatile antimicrobials produced by Muscodor albus. Plant Sci. 2003;165:1229–38.
Fernando WGD, Ramarathnam R, Krishnamoorthy AS, Savchuk SC. Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem. 2005;37:955–64.
Frick WF, Pollock JF, Hicks AC, Langwig KE, Reynolds DS, Turner GG, Butchkoski CM, Kunz TH. An emerging disease causes regional population collapse of a common North American bat species. Science. 2010;329:679–82.
Froschauer A, Coleman J. North American bat death toll exceeds 5.5 million from white-nose syndrome. U.S. Fish and Wildlife Service; 2012. http://www.batcon.org/pdfs/USFWS_WNS_Mortality_2012_NR_FINAL.pdf
Garbeva P, Hol WHG, Termorshuizen AJ, Kowalchuk GA, Boer WD. Fungistasis and general soil biostasis—a new synthesis. Soil Biol Biochem. 2001;43:469–77.
Gargas A, Trest MT, Christensen M, Volk TJ, Blehert DS. Geomyces destructans sp. nov., associated with bat white-nose syndrome. Mycotaxon. 2009;108:147–54.
Kerr JR. Bacterial inhibition of fungal growth and pathogenicity. Microb Ecol Health Dis. 1999;11:129–42.
Liu W, Mu W, Zhu B, Liu F. Antifungal activities and components of VOCs produced by Bacillus subtilis G8. Curr Res Bacteriol. 2008;1:128–34.
Lorch JM, Meteyer CU, Boyles JG, Cryan P, Hicks AC, Ballman AE, Coleman JTH, Redell DN, Reeder DM, Blehert DS. Experimental infection of bats with Geomyces destructans causes white-nose syndrome. Nature. 2011;480:376–8.
Lorch JM, Lindner DL, Gargas A, Muller LK, Minnis AM, Blehert DS. A culture-based survey of fungi in soil from bat hibernacula in the eastern United States and its implications for detection of Geomyces destructans, the causal agent of bat white-nose syndrome. Mycologia. 2013;105:237–52.
Minnis AM, Linder 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. http://dx.doi.org/10.1016/j.funbio.2013.07.001.
Stebbing ARD. Hormesis: the stimulation of growth by low levels of inhibitors. Sci Total Environ. 1982;22:213–34.
Strobel GA, Kluck K, Hess WM, Sears J, Ezra D, Vargas PN. Muscodor albus E-6, an endophyte of Guazuma ulmifolia making volatile antibiotics: isolation, characterization and experimental establishment in the host plant. Microbiology. 2007;153:2613–20.
Turner GG, Reeder DM, Coleman JTH. A five-year assessment of mortality and geographic spread of white-nose syndrome in North American bats and a look to the future. Bat Res News. 2011;52:13–27.
Verant ML, Boyles JG, Waldrep W, Wibbelt G, Blehert DS. Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome. PLoS ONE. 2012;7:e46280. doi:10.1371/journal.pone.0046280.
Zou CS, Mo ME, Gu YQ, Zhou JP, Zhang KQ. Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol Biochem. 2007;39:2371–9.
This work was funded by the Georgia State University Department of Biology, as well as the Georgia State University Environmental Research Program. The authors would like to thank Kevin Keel for providing the fungal cultures used in this study. The authors would also like to thank Ian Sarad, Blake Cherney, and Ben Poodiak for their contributions to this effort.
About this article
Cite this article
Cornelison, C.T., Gabriel, K.T., Barlament, C. et al. Inhibition of Pseudogymnoascus destructans Growth from Conidia and Mycelial Extension by Bacterially Produced Volatile Organic Compounds. Mycopathologia 177, 1–10 (2014). https://doi.org/10.1007/s11046-013-9716-2
- Pseudogymnoascus destructans
- White-nose syndrome