Review of the current status and future perspectives on Pseudogymnoascus destructans studies with reference to the species findings in Bulgaria

Автори

DOI :

https://doi.org/10.60066/GSU.BIOFAC.Bot.100.67-99

Ключови думи :

bats, caves , Geomyces destructans, geomycosis , nature conservation , White Nose Disease , White Nose Syndrom

Абстракт

Emerging infectious diseases are a well-known threat to the wildlife and require complex research. There is a rapidly accumulating knowledge on the infectious disease of bats (White Nose Syndrome - WNS/White Nose Disease - WND) and its causative agent - the pathogenic fungus Pseudogymnoascus destructans. Although mass mortality of bats, known since a decade, is currently restricted to North America, the pathogen is of global concern as a potential threat to other hibernating bat populations. Therefore five years after the first comprehensive synthesis on the fungal ecology and relevant knowledge gaps (Foley et al. 2011), we decided to summarize the published information on the pathogen morphology, reproduction, ecological requirements, geographic distribution and systematic position. In addition, the present review compiles the
available data on the affected bat species, mechanisms of WND, on the host response and on the effective treatment strategies with possible methods forfighting the pathogen to reduce the mortality in affected regions as well. Special attention is paid to the finding of the fungus in Bulgarian caves.

 

References:

Amelon S. & Knudsen G. 2010. Evaluation of nonpathogenic bat skin microbes for antagonistic activity to Geomyces destructans. - Progress report, U. S. Forest Service, University of Idaho: 1-2. https://www.whitenosesyndrome.org/resource/evaluation-non-pathogenic-bat-skin-microbes-antagonistic-activity-geomyces-destructans.

Anonymous 2014. News from the world of bats: White-nose news. - The Underground Movement 14 (6): 20-21.

Bandouchova H., Bartonicka T., Berkova H., Brichta J., Cerny J., Kovacova V, Kolarik M., Köllner B., Kulich P., Martinkova N., Rehak Z., Turner G. G., Zukal J. & Pikula J. 2015. Pseudogymnoascus destructans: evidence of virulent skin invasion for bats under natural conditions, Europe. - Transbound. Emerg. Dis. 62 (1): 1-5.

Barlow A., Ford S., Green R., Morris C. & Reaney S 2009. Investigations into suspected white-nose syndrome in two bats in Somerset. - Vet. Rec. 165 (16): 481-482.

Bat Conservation International 2015. http://www.batcon.org.

Ben-Hamo M., Munoz-Garcia A., Williams J. B., Korine C., Pinshow B. 2013. Waking to drink: rates of evaporative water loss determine arousal frequency in hibernating bats. - J. Exp. Biol. 216: 573-577.

Bernard R. F., Foster J. T., Willcox E. V, Parise K. L. & McCracken G. F. 2015. Molecular detection of the causative agent of white-nose syndrome on rafinesque’s big-eared bats (Corynorhinus rafinesquii) and two species of migratory bats in the Southeastern USA. - J. Wildlife Dis. 51 (2): 519-522.

Blehert D. S., Hicks A. C., Behr M., Meteyer C. U., Berlowski-Zier B. M., Buckles E. L., Coleman J. T. H., Darling S. R., Gargas A., Niver R., Okoniewski J. C., Rudd R. J. & Stone W. B. 2009. Bat white-nose syndrome: an emerging fungal pathogen? - Science 323: 227.

Bouma H. R., Henning R. H., Kroese F. G. & Carey H. V. 2012. Hibernation is associated with depression of T-cell independent humoral immune responses in the 13-lined ground squirrel. - Dev. Comp. Immunol. 39 (3): 154-160.

Boyles J. G. & Willis C. K. R. 2010. Could localized warm areas inside cold caves reduce mortality of hibernating bats affected by white-nose syndrome? - Front. Ecol. Environ. 8: 92-98.

Brilhante R. S. N., de Lima R. A. C., Caetano E. P., Leite J. J. G., Castelo-Branco D. de S. M., Ribeiro J. F., Bandeira T. de J. P. G., Cordeiro R. de A., Monteiro A. J., Sidrim J. J. C. & Rocha M. F. G. 2013. Effect of farnesol on growth, ergosterol biosynthesis, and cell permeability in Coccidioidesposadasii. - Antimicrob. Agents Chemother. 57 (5): 2167-2170.

Brock M. 2008. Physiology and metabolic requirements of pathogenic fungi. - In: Brakhafe A. A. & Zipfel P. F. (eds.), The Human and animal relationships, 2nd Edition The Mycota VI, Springer-Verlag Berlin Heidelberg, 63-82.

Brownlee-Bouboulis S. A. & Reeder D. M. 2013. White-nose syndrome-affected little brown myotis (Myotis lucifugus) increase grooming and other active behaviors during arousals from hibernation. - J. Wildl. Dis. 49: 850-859.

Bürger K., Gebhardt O., Wohlfahrt S., Wibbelt G. & Reiter G. 2013. First confirmed records of Geomyces destructans (Blehert & Gargas 2009) in Austria. - Ber. nat.-med. Verein Innsbruck 98: 127-135.

Cahill J. E., Lewert R. M. & Jaroslow B. N. 1967. Effect of hibernation on course of infection and immune response in Citellus tridecemlineatus infected with Nippostrongylus brasiliensis. - J. Parasitol. 53 (1): 110-115.

Casadevall A., Steenbergen J. N. & Nosanchuk J. D. 2003.‘Ready made’ virulence and ‘dual use’ virulence factors in pathogenic environmental fungi - the Cryptococcus neoformans paradigm. - Curr. Opin. Microbiol. 6: 332-337.

Castle, K. T. & Cryan P. M. 2010. White-nose syndrome in bats: a primer for resource managers. Park Science 27:20-25.

Caven A., Mengak M. T. & Miller K. V 2012. White nose syndrome in the United States. - Wildlife Manadgment Publication Series 12 (15): 2-6.

Chaturvedi V., Springer D. J., Behr M. J., Ramani R., Li X., Peck M. K., Ren P., Bopp D. J., Wood B., Samsonoff W. A., Butchkoski C. M., Hicks A. C., Stone W. B., Rudd R. J. & Chaturvedi S. 2010. Morphological and molecular characterizations of psychrophilic fungus Pseudogymnoascus destructans from New York bats with white nose syndrome (WNS). - PLoS ONE 5 (5): e10783.

Chaturvedi V. & Chaturvedi S. 2011. 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 171: 231-233.

Cohn J. P. 2012. Bats and white-nose still a conundrum. - Bioscience 62 (4): 444. 

Coleman J. 2014. White-nose syndrome. The devastating disease of hibernating bats in North America. - U.S. Fish & WildlifePublications 8: 453.

Coleman J. T. H. & Reichard J. D. 2014. Bat white-nose syndrome in 2014: a brief assessment seven years after discovery of a virulent fungal pathogen in North America. - Outlooks on Pest Management 25 (6): 374-377.

Coleman J., Ballmann 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. 2011. A national plan for assisting states, federal agencies, and tribes in managing white-nose syndrome in bats. - US Fish & Wildlife Publications. Paper 454: 1-18.

Cornelison C. T., Gabriel K., Barlament C. & Crow Jr S. A. 2014a. Inhibition of Pseudogymnoascus destructans growth from conidia and mycelial extension by bacterially produced volatile organic compounds. - Mycopathologia 177 (1-2): 1-10.

Cornelison C. T., Keel M. K., Gabriel K. T., Barlament C. K., Tucker T. A., Pierce G. E. & Crow S. A. 2014b. A preliminary report on the contact-independent antagonism of Pseudogymnoascus destructans by Rhodococcus rhodochrous strain DAP96253. - BMC Microbiology 14: 246.

Cryan P. M., Meteyer C. U., Boyles J. G. & Blehert D. S. 2010. Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology. - BMC Biology 8: 135.

Cryan P. M., Meteyer C. U., Boyles J. G. & Blehert D. S. 2013a. White-nose syndrome in bats: illuminating the darkness. - BMC Biology 11: 47.

Cryan P. M, Meteyer C. U., Blehert D. S., Lorch J. M., Reeder D. M., Turner G. G., Webb J., Behr M., Verant M., Russell R. E. & Castle K. T. 2013b. Electrolyte depletion in white-nose syndrome bats. - J. Wildlife Dis. 49: 398-402.

Cunningham A. A., Daszak P., Rodriguez J. P. 2003. Pathogen pollution: defining a parasitological threat to biodiversity conservation. - J. Parasitol. 89 (Suppl.): S78-S83.

Daszak P., Cunningham A. A. & Hymt A. D. 2000. Emerging infectious diseases of wildlife - threats to biodiversity and human health. - Science 287: 443- 449.

De Castro F. & Bolker B. 2004. Mechanisms of disease-induced extinction. - Ecol. Lett. 8: 117-126.

Dobony C. A., Hicks A. C., Langwig K. E., von Linden R. I., Okoniewski J. C. & Rainbolt R. E. 2011. Little brown myotis persist despite exposure to white-nose syndrome. - Journal of fish and wildlife management 2 (2): 190-195.

Fernando W. G. D., Ramarathnam R., Krishnamoorthy A. S. & Savchuk S. C. 2005. Identification and use of potential bacterial organic antifungal volatiles in biocontrol. - Soil Biol. Biochem. 37 (5): 955-964.

Field K. A., Johnson J. S., Lilley T. M., Reeder S. M., Rogers E. J., Behr M. J. & Reeder D. M. 2015. The white-nose syndrome transcriptome: activation of anti-fungal host responses in wing tissue of hibernating little brown myotis. - PLoS Pathog 11(10): e1005168.

Fisher M. C., Henk D. A., Briggs C. J., Brownstein J. S., Madoff L. C., McCraw S. L. & Gurr S. J. 2012. Emerging fungal threats to animal, plant and ecosystem health. - Nature 484: 186-194. 

Flory A. R., Kumar S., Stohlgren T. J. & Cryan P. M. 2012. Environmental conditions associated with bat white-nose syndrome mortality in the north-eastern United States. - J. Appl. Ecol. 49: 680-689.

Foley J., Clifford D., Castle K., Cryan P. & Ostfeld R. S. 2011. Investigating and managing the rapid emergence of white nose syndrome, a novel, fatal, infectious disease of hibernating bats. - Conserv. Biol. 25 (2): 223-231.

Frick W. F., Pollock J. F., Hicks A. C., Langwig K. E., Reynolds D. S. Turner G. G., Butchkoski C. M. & Kunz T. H. 2010. An emerging disease causes regional population collapse of a common North American bat species. - Science 329: 679-682.

Frick W. F., Puechmaille S. J., Hoyt J. R., Nickel B. A., Langwig K. E., Foster J. T., Barlow K. E., Bartonicka T., Feller D., Haarsma A.-J., Herzog C., Horacek I., Van Der Koou J., Mulkens B., Petrov B., Reynolds R., Rodrigues L., Stihler C. W., Turner G. G. & Kilpatrick A. M. 2015. Disease alters macroecological patterns of North American bats. - Global Ecol. Biogeogr. 24: 741-749.

Frick W. F., Puechmaille S. J. & Willis C. K. R. 2016. White-nose syndrome in bats. - In: Voigt C. C. & Kingston T. (eds), Bats in the Anthropocene: conservation of bats in a changing world, Springer, 245-262.

Fritze M., Pham T. L. H. & Zaspel I. 2012. Effekt des Bodenbacteriums Pseudomonas veronii-like PAZ1 auf das Wachstum des White-Nose Erregers Geomyces destructans in Antagonisten Tests. - Nyctalus 17 (3-4): 104-107.

Gargas A., Trest M. T., Christensen M., Volk T. J. & Blehert D. S. 2009. Geomyces destructans sp. nov. associated with bat white-nose syndrome. - Mycotaxon 108: 147-154.

Gebhardt O. 2010. Erster Hinweis auf Geomyces destructans in Österreich. - Kopf Über 11 (2): 4.

Grieneisen . L. E., Brownlee-Bouboulis S. A., Johnson J. S. & Reeder D. M. 2015. Sex and hibernaculum temperature predict survivorship in white-nose syndrome affected little brown myotis (Myotis lucifugus). - R. Soc. Open Sci. 2 (2): 140470.

Hoyt J. R., Langwig K. E., Okoniewski J., Frick W. F., Stone W. B. & Kilpatrick A. M. 2014. Long-term persistence of Pseudogymnoascus destructans, the causative agent of white-nose syndrome, in the absence of bats. - EcoHealth 12: 330-333.

Hoyt J. R., Cheng T. L., Langwig K. E., Hee M. M., Frick W. F. & Kilpatrick A. M. 2015. bacteria isolated from bats inhibit the growth of Pseudogymnoascus destructans, the causative agent of white-nose syndrome. - PLoS ONE 10 (4): e0121329.

Hoyt J. R., Sun K., Parise K. L., Lu G., Langwig K. E., Jiang T., Yang S., Frick W. F., Kilpatrick A. M., Foster J. T. & Feng J. 2016. Widespread bat white-nose syndrome fungus in North-eastern China [letter]. - Emerg. Infect. Dis. 22 (1): 140-142.

Hung C., Xue J. & Cole G. 2007. Virulence mechanisms of coccidioides. - Ann. N Y Acad. Sci. 1111: 225-235.

Jeon J.-G., Pandit S., Xiao J., Grégoire S., Falsetta M. L., Klein M. I., Koo H. 2011. Influences of trans-trans farnesol, a membrane-targeting sesquiterpenoid, on Streptococcus mutans physiology and survival within mixed-species oral biofilms. - Int. J. Oral Sci. 3: 98-106.

Johnson L. J.A. N., Miller A. N., McCleery R.A., McClanahan R., Kath J.A., Lueschow S. & Porras-Alfaroa A. 2013. Psychrophilic and psychrotolerant fungi on bats and the presence of Geomyces spp. on bat wings prior to the arrival of white nose syndrome. - App. Envir. Micr. 79 (18): 5465-5471. 

Johnson J. S., Reeder D. M., McMichael III J. W., Meierhofer M. B., Stern D. W. F., Lumadue S. S., Sigler L. E., Winters H. D., Vodzak M. E., Kurta A., Kath J. A. & Field K. A. 2014. Host, pathogen, and environmental characteristics predict white-nose syndrome mortality in captive little brown myotis (Myotis lucifugus). - PLoS ONE 9 (11): e112502.

Johnson J. S., Reeder D. A. M., Lilley T. M., Cz ir j a k G. Â., Voigt C. C., McMichael III J. W., Meierhofer M. B., Seery C. W., Lumadue S. S., Altmann A. J., Toro M. O. & Field K. A. 2015. Antibodies to Pseudogymnoascus destructans are not sufficient for protection against white-nose syndrome. - Ecology and evolution 5 (11): 2203-2214.

Kerr J. R. 1999. Bacterial inhibition of fungal growth and pathogenicity. - Microb. Ecol. Health. Dis. 11: 129-142.

Khankhet J. 2014. Clonal expansion of the Pseudogymnoascus destructans genotype in North America is accompanied by significant variation in phenotypic expression. M. Sc. Thesis. McMaster University, Hamilton, Ontario (Supervisor: Prof. Dr. Jianping Xu), 88 pp.

Knudsen G. R., Dixon R. D. & Amelon S. K. 2013. Potential spread of white-nose syndrome of bats to the northwest: epidemiological considerations. - Northwest Sci. 87 (4): 292-306.

Kooser A., Kimble J. C., Young J. M., Buecher D. C., Valdez E. W., Porras-Alfaro A. & Northup D. E. 2015. External microbiota of western united states bats: does it matter where you are from? - BioRxive. The preprint server for biology. doi: http://dx.doi.org/10.1101/017319.

Kubatova A., Koukol O. & Novakova A. 2011. Geomyces destructans, phenotypic features of some Czech isolates. - Czech. Mycol. 63: 65-75.

Langwig K. E., Frick W. F., Bried J. T., Hicks A. C., Kunzand T. H., Kilpatrick A. M. 2012. Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. - Ecol. Lett. 15 (9): 1050-1057.

Langwig K., Frick W. F., Rick R., Parise K. L., Drees K. P., Hoyt J. R., Cheng T. L., Kunz T. H., Foster J. T. & Kilpatrick A. M. 2015a. Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome. - Proc. R. Soc. B. 282: 20142335.

Langwig K. E., Hoyt J. R., Parise K. L., Kath J., Kirk D., Frick W. F., Foster J. T. & Kilpatrick A. M. 2015b. Invasion dynamics of white-nose syndrome fungus, Midwestern United States, 2012-2014. - Emerg. Infect. Dis. 21 (6): 1023-1026.

Leibundgut-Landmann S., Wüthrich M. & Hohl T. M. 2012. Immunity to fungi. - Curr. Opin. Immunol. 24 (4): 449-458.

Leopardi S., Blake D. & Puechmaille S. 2015. White-nose syndrome fungus introduced from Europe to North America. - Current Biology 25 (6): R217-R219.

Lindner D. L., Gargas A., Lorch J. M., Banik M. T., Glaeser J., Kunz T. H. & Blehert D. S. 2011. DNA-based detection of the fungal pathogen Geomyces destructans in soils from bat hibernacula. - Mycologia 103: 241-246.

Lorch J. M., Meteyer C. U., Behr M. J., Boyles J. G., Cryan P. M. & Hicks A. C. 2011. Experimental infection of bats with Geomyces destructans causes white-nose syndrome. - Nature 480: 376-378. 

Lorch J. M., Lindner D. L., Gargas A., Muller L. K., Minnis A. M. & Blehert D. S. 2013a. 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 105: 237-252.

Lorch J. M., Muller L. K., Russell R. E., O'Connor M., Lindner D. L., Blehert D. S. 2013b. Distribution and environmental persistence of the causative agent of white-nose syndrome, Geomyces destructans, in bat hibernacula of the eastern United States. - Appl. Environ. Microbiol. 79 (4): 1293-1301.

Lorch J. M., Minnis A. M., Meteyer C. U., Redell J. A., White J. P., Kaarakka H. M., Muller L. K., Lindner D. L., Verant M. L., Shearn Bochsler V & Blehert D. S. 2015. The fungus Trichophyton redellii sp. nov. causes skin infections that resemble white-nose syndrome of hibernating bats. - J. Wildlife Dis. 51 (1): 36-47.

Lucan R. K., Bandouchova H., Bartonicka T., Pikula J., Zahradnikova Jr A., Zukal J. & Martinkova N. 2016. Ectoparasites may serve as vectors for the white-nose syndrome fungus. - Parasites & Vectors 9: 16. DOI 10.1186/s13071-016-1302-2

Maniero G. D. 2000. The influence of temperature and season on mitogen-induced proliferation of ground squirrel lymphocytes. - In: Heldmaier G. & Klingenspor M. (eds), Life in the cold: eleventh international hibernation symposium, Springer, 493–503.

Martinkova N., Backor P., Bartonicka T., Blazkova, P., Cerveny J., Falteisek L., Gaisler J., V. Hanzal, Horacek D., Hubalek Z., Jahelkova H., Kolarik M., Korytar L., Kubatova A., Lehotska B., Lehotsky R., Lucan R. K., Majek O., Mateju J., Rehak Z., Safar J., Tajek P., Tkadlec E., Uhrin M., Wagner J., Weinfurtova D., Zima J., Zukal J. & Horacek I. 2010. Increasing incidence of Geomyces destructans fungus in bats from the Czech Republic and Slovakia. - PLoS ONE 5: e13853.

Mestdagh X., Baltus L., Hoffman L. & Titeux N. 2012. Découverte de chauves-souris au nez blanc au Luxembourg. - Bull. Soc. Nat. Luxemb. 113: 141-149.

Meteyer C., Barber D. & Mandl J. N. 2012. Pathology in euthermic bats with white nose syndrome suggests a natural manifestation of immune reconstitution inflammatory syndrome. - Virulence 3 (7): 583-588.

Meteyer C. Ü., Buckles E. L., Blehert D. S., Hicks A. C., Green D. E., Shearn-Bochsler V., Thomas N. J., Gargas A. & Behr M. J. 2009. Histopathologic criteria to confirm white-nose syndrome in bats. - J. Vet. Diagn. Invest. 21: 411-414.

Meteyer C. U., Valent M., Kashmer J., Buckles E. L., Lorch J. M., Blehert D. S., Lollar A., Berndt D., Wheeler, E., White C. L. & Ballmann A. E. 2011. Recovery of little brown bats (Myotis lucifugus) from natural infection with Geomyces destructans, white-nose syndrome. - J. Wildlife Dis. 47: 618-626.

Minnis A. M., Lindner D. L. 2013. Phylogenetic evaluation of Pseudogymnoascus and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov. in bat hibernacula of eastern North America. - Fungal biology 117 (9): 638-649.

Moore M. S., Reichard J. D., Murtha T. D., Zahedi B., Fallier R. M. & Kunz T. H. 2011. Specific alterations in complement protein activity of little brown myotis (Myotis lucifugus) hibernating in white-nose syndrome affected sites. - PLoS ONE 6 (11): e27430.

Moore M. S., Reichard J. D., Murtha T. D., Nabhan M. L., Pian R. E., Ferreira J. S. & Kunz T. H. 2013. Hibernating little brown myotis (Myotis lucifugus) show variable immunological responses to white-nose syndrome. - PloS ONE 8: e58976. 

Muhldorfer K. 2012. Bats and bacterial pathogens: A review. - Zoonoses Public Health 60: 93-103.

Mulec J., Covington E. & Walochnik J. 2013. Is bat guano a reservoir of Geomyces destructans? - Open J. Vet. Med. 3: 161-167.

Muller L. K., Lorch J. M., Lindner D. L., O’Connor M., Gargas A. & Blehert D. S. 2013. Bat white-nose syndrome: a real-time TaqMan polymerase chain reaction test targeting the intergenic spacer region of Geomyces destructans. - Mycologia 105 (2): 253-259.

Naglik J., Albrecht A., Bader O. & Hube B. 2004. Candida albicans proteinases and host/pathogen interactions. - Cell Microbiol. 6 (10): 915-926.

Netea M. G., Brown G. D., Kullberg B. J. & Gow N. A. 2008. An integrated model of the recognition of Candida albicans by the innate immune system. - Nat. Rev. Microbiol. 6 (1): 67-78.

Nilsson S. 2012. Surveillance of Geomyces destructans in Swedish bats and bat hibernacula. SLU, Department of Biomedical Sciences and Veterinary Public Health, Upsalla, Sweden. Examensarbete 2012: 40, 31 pp. ISSN 1652-8697 (http://epsilon.slu.se).

O’Donoghue A. J., Knudsen G. M., Beekman C., Perry J. A., Johnson A. D., DeRisi J. L., Craik C. S. & Bennett R. J. 2015. Destructin-1 is a collagen-degrading endopeptidase secreted by Pseudogymnoascus destructans, the causative agent of white-nose syndrome. - Proc. Natl. Acad. Sci. U. S. A. 112 (24): 7478-7483.

Paiva-Cardoso Md. N., Morinha F., Barros P., Vale-Gonçalves H., Coelho A. C., Fernandes L., Travassos P., Faria A. S., Bastos E., Santos M. & Cabral J. A. 2014. First isolation of Pseudogymnoascus destructans in bats from Portugal. - Eur. J. Wildl. Res. 60: 645-649.

Palmer J. M., Kubátova A., Novakova A., Minnis A. M., Kolarik M. & Lindner D. L. 2014. Molecular characterization of a heterothallic mating system in Pseudogymnoascus destructans, the fungus causing white-nose syndrome of bats. - G3 (Bethesda) 4 (9): 1755-63.

Pavlinic I., Bakovic M.& Lojkic I. 2014. Pseudogymnoascus destructans in Croatia confirmed. - Eur. J. Wildl. Res. 61 (2): 325-328.

PhillipsC.D., Phelan G., Dowd S.E., McDonough M.M., Ferguson A.W., Delton Hanson J., Siles L., Ordonez-Garza N., San Francisco M. & Baker R. J. 2012. Microbiome analysis among bats describes influences of host phylogeny, life history, physiology and geography. - Mol. Ecol. 21 (11): 2617-2627.

Pierce G. E., Drago G. K., Ganguly S., Tucker T. A., Hooker J. W., Jones S. & Crow S. A. Jr. 2011. Preliminary report on a catalyst derived from induced cells of Rhodococcus rhodochrous DAP 96253 that delays the ripening of selected climacteric fruit: bananas, avocados, and peaches. - J. Ind. Microbiol. Biotechnol. 38 (9): 1567-1573.

Pikula J., Bandouchova H., Novotny L., Meteyer C. U., Zukal J., Irwin N. R., Zima J. & Martinkova N. 2012. Histopathology confirms White-Nose Syndrome in bats in Europe. - J. Wildlife Dis. 48 (1): 207-211.

Puechmaille S. J., Fuller H. & Teeling E. C. 2011a. Effect of sample preservation methods on the viability of Geomyces destructans, the fungus associated with white-nose syndrome in bats. - Acta Chiropterologica 13 (1): 217-221. 

Puechmaille S. J., Verdeyroux P., Fuller H., Ar Gouilh M., Bekaert M. & Teeling E. C. 2010. White-nose syndrome fungus (Geomyces destructans) in bat, France. - Emerg. Infect. Dis. 16 (2): 290-293.

Puechmaille S. J., Frick W. F., Kunz T. H., Racey P. A., Voigt C. C., Wibbelt G. & Teeling E. C. 2011b. White-nose syndrome: is this emerging disease a threat to European bats? - Trends Ecol. Evol. 26 (11): 570-576.

Puechmaille S. J., Wibbelt G., Korn V, Fuller H., Forget F., MühlDorfer K., Kurth A., Bogdanowicz W., Borel C., Bosch T., Cherezy T., Drebet M., Goerfoel T., Haarsma A., Herhaus F., Hallart G., Hammer M., Jungmann C., LeBris Y., Lutsar L., Masing M., Mulkens B., Passior K., Starrach M., Wojtaszewski A., Zö phel U. & Teeling E. C. 2011c. Pan-European distribution of white-nose syndrome fungus (Pseudogymnoascus destructans) not associated with mass mortality. - PLoS ONE 6 (4): e19167.

Rapin N., Johns K., Martin L., Warnecke L., Turner J. M., Bollinger T. K., Willis C. K., Voyles J. & Misra V. 2014. Activation of innate immune-response genes in little brown bats (Myotis lucifugus) infected with the fungus Pseudogymnoascus destructans. - PLoS ONE 9 (11): e112285.

Raudabaugh D. B. & Miller A. N. 2013. Nutritional capability of and substrate suitability for Pseudogymnoascus destructans, the causal agent of bat white-nose syndrome. - PLoS ONE 8: e78300.

Raudabaugh D. B. & Miller A. N. 2015. Effect of Trans, Trans-Farnesol on Pseudogymnoascus destructans and Several Closely Related Species. - Mycopathologia 180 (5): 325-332.

Reeder D. M. & Moore M. S. 2013. White-Nose Syndrome: A Deadly Emerging Infectious Disease of Hibernating Bats. - In: Adams R. A. & S. C. Pedersen (eds), Bat Evolution, Ecology, and Conservation, Springer Science+Business Media New York, 413-434.

Reeder D. M. & Turner G. R. 2008. Working together to combat white-nose syndrome: a report of a meeting on 9-11 June 2008, in Albany, New York. - Bat Research News 49 (3): 75-78.

Reeder D. M., Frank C. L., Turner G. G., Meteyer C. U., Kurta A., Britzke E. R., Vodzak M. E., Darling S. R., Stihler C.W., HicksA. C., Jacob R., Grieneisen L. E., Brownlee S. A., Muller L. K. & Blehert D. S. 2012. Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. - PLoS ONE 7 (6): e38920.

Reynolds H. T., Barton H. A. 2014. Comparison of the white-nose syndrome agent Pseudogymnoascus destructans to cave-dwelling relatives suggests reduced saprotrophic enzyme activity. - PloS ONE 9 (1): e86437.

Reynolds H. T., Ingersoll T. & Barton H. A. 2015. Modeling the environmental growth of Pseudogymnoascus destructans and its impact on the white-nose syndrome epidemic. - J. Wildlife Dis. 51: 318-331.

Romani L. 2011. Immunity to fungal infections. - Nat. Rev. Immunol. 11 (4): 275-288.

Sachanowicz K., Stępień A. & Ciechanowski M. 2014. Prevalence and phenology of white-nose syndrome fungus Pseudogymnoascus destructans in bats from Poland. - Cent. Eur. J. Biol. 9 (4): 437-443.

Santos A. L. S. & Braga-Silva L. A. 2013. Aspartic protease inhibitors: effective drugs against the human fungal pathogen Candida albicans. - Mini Rev. Med. Chem. 13 (1): 155-162.

Semighini C. P. Hornby, J. M. Dumitru R. Nickerson K. & Harris S. D. 2006. Farnesol-induced apoptosis in Aspergillus nidulans reveals a possible mechanism for antagonistic interactions between fungi. - Mol. Microbiol. 59 (3): 753-764.

Shelley V., Kaiser S., Shelley E., Williams T., Kramer M., Haman K., Keel K., Barton H. A. 2013. Evaluation of strategies for the decontamination of equipment for Geomyces destructans, the causative agent of white-nose syndrome (WNS). - Journal of cave and karst studies 75 (1): 1-10.

Sieckmann D. G., Jaffe H., Golech S., Cai D., Hallenbeck J. M. & McCarron R. M. 2014. Anti-lymphoproliferative activity of alpha-2-macroglobulin in the plasma of hibernating 13-lined ground squirrels and woodchucks. - Vet. Immunol. Immunopathol. 161: 1-11.

Simonovicova A., Pangallo D., Chovanova K. & Lehotska B. 2011. Geomyces destructans associated with bat disease WNS detected in Slovakia. - Biologia 66 (3): 562-564.

Smyth C., Schlesinger S., Overton B. E. & Butchkoski C. 2013. The alternative host hypothesis and potential virulence genes in Geomyces destructans. - Bat Research News 54: 17-24.

Storm J. J. & Boyles J. G. 2011. Body temperature and bodymass of hibernating little brown bats Myotis lucifugus in hibernacula affected by white-nose syndrome. - Acta Theriol. 56: 123-127.

Thogmartin W. E., Sanders-Reed C.A., Szymanski J.A., McKann P. C., Pruitt L., King R. A., Runge M. C., Russell R. E. 2013. White-nose syndrome is likely to extirpate the endangered Indiana bat over large parts of its range. - Biol. Conserv. 160: 162-172.

Toshkova N. 2014. Distribution in Bulgaria of the causative agent of WNS - Pseudogymnoascus destructans Master Thesis, Sofia University, Faculty of Biology, Department of Ecology and Environmental Protection (Supervisor: Assoc. Prof. Dr. D. Zlatanova, Consultant: Main Asist. Dr. B. Uzunov ), 76 pp. (In Bulgarian).

Toshkova N. & Zhelyvkova V. 2014. To the bottom of Bulgaria: first report of Geomyces destructans from the deepest Bulgarian caves. - In: Lina P. H. C. & Hutson A. M. (eds), Book of Abstracts, XlIIth European Bat Research Symposium, September 01–05, 2014 Sibenik, Croatia, printed by Denona, Zagreb, p.178. http://www.hbsd.hr/Publikacije/13EBRS_Croatia2014_Abstracts_HBSD_fin_web.pdf

Turner G. G. & Reeder D. M. 2009. Update of white nose syndrome in bats, September 2009. - Bat Research News 50: 47-53.

Turner G. G., Reeder D. M. & Coleman J. T. H. 2011. A fife-year assessment of mortality and geographic spread of white-nose syndrome in North American bats and a look to the future. - Bat Research News 52 (2): 13-27.

Turner G. G., Meteyer C. U., Barton H., Gumbs J. F., Reeder D. M., Overton B., Bandouchova H., Bartonicka T., Martinkova N., Pikula J., Zukal J. & Blehert D. S. 2014. Nonlethal screening of bat-wing skin with the use of ultraviolet fluorescence to detect lesions indicative of white-nose syndrome. - J. Wildlife Dis. 50 (3): 566-573.

U.S. Fish and Wildlife Service 2016. White-nose syndrome: the devastating disease of hibernating bats in North America. https://www.whitenosesyndrome.org/sites/default/files/resource/white-nose_fact_sheet_5-2016_2.pdf.

USGS 2010. Geomyces destructans detected in Oklahoma cave Myotis and listed Missouri gray bats. - USGS National Wildlife Health Center - Wildlife Health Bulletin, 2010-97.

Vanderwolf K., Malloch D. & McAlpine D. F. 2015. Fungi associated with overwintering tricolored bats, Perimyotis subflavus, in a White-nose syndrome region of Eastern Canada. - J. Cave Karst Stud. 77: 145-151.

Vanderwolf K., McAlpine D. F., Malloch D. & Forbes G. J. 2013. Ectomycota associated with hybernating bats in Eastern Canadian caves prior to the emergence of White-nose syndrome. - Northeastern Naturalist 20: 115-130.

Veilleux J. P. 2008. Current status of white-nose syndrome in the Northeastern United States. - Bat Research News 49: 15-17.

Verant M. L., Boyles J. G., Waldrep Jr. W., Wibbelt G. & Blehert D. S. 2012. Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome. - PLoS ONE 7 (9): e46280.

Verant M. L., Meteyer C. U., Speakman J. R., Cryan P. M., Lorch J. M. & Blehert D. S. 2014. White-nose syndrome initiates a cascade of physiologic disturbances in the hibernating bat host. - BMC Physiol 14: 10.

Voigt C. C. & Kingston T. (eds) 2016. Bats in the Anthropocene: conservation of bats in a changing world. Springer Open, 606 pp.

Voyron S., Lazzari A., Riccucci M., Calvini M. & Varese G. C. 2010. First mycological investigations on Italian bats. - Hystrix Italian J. Mammal. 22:189-197.

Warmink J. A., Nazir R., Corten B. & van Elsas J. D. 2011. Hitchhikers on the fungal highway: the helper effect for bacterial migration via fungal hyphae. - Soil Biol. Biochem 43 (4): 760-765.

Warnecke L., Turner J. & Bollinger T. 2013. Pathophysiology of white-nose syndrome in bats: a mechanistic model linking wing damage to mortality. - Biol. Lett. 9 (4): 20130177.

Webb P. I., Speakman J. R. & Racey P. A. 1996. How hot is a hibernaculum? A review of the temperatures at which bats hibernate. - Canadian Journal of Zoology 74 (4): 761-765.

Weber, K. Sohr R., Schulz B., Fleischhacker M. & Ruhnke M. 2008. Secretion of E, E-farnesol and biofilm formation in eight different Candida species. - Antimicrob. Agents Chemother. 52 (5): 1859-1861.

Wibbelt G., Kurth A., Hellmann D., Weishaar M., Barlow A., Veith M., Prüger J., Görföl T., Grosche L., Bontadina F., Zöpfel U., Seidl H.-P., Cryvn P. M. & Blehert D. S. 2010. White-nose syndrome fungus (Geomyces destructans) in bats, Europe. - Emerg. Infect. Dis. 16 (8): 1237-1242.

Wibbelt G., Puechmaille S. J., Ohlendorf B., Mühldorfer K., Bosch T., Görfol T., Passior K., Kurth A., Lacremans D. & Forget F. 2013. Skin lesions in european hibernating bats associated with Geomyces destructans, the etiologic agent of White-Nose Syndrome. - PLoS ONE 8 (9): e74105.

Wilcox A., Warnecke L., Turner J. M., McGuire L. P., Jameson J. W., Misra V., Bollinger T. C. & Willis C. K. R. 2014. Behaviour of hibernating little brown bats experimentally inoculated with the pathogen that causes white-nose syndrome. - Anim. Behav. 88: 157-164.

Willis C. K. R., Menzies A. K., Boyles J. G. & Wojciechowski M. S. 2011. Evaporative water loss is a plausible explanation for mortality of bats from white-nose syndrome. - Integr. Comp. Biol. 51: 364-373.

Willis C. & Wilcox A. 2014. Hormones and hibernation: possible links between hormone systems, winter energy balance and white-nose syndrome in bats. - Horm. Behav. 66 (1): 66-73.

Xu C., Mo M., Zhang L. & Zhang K. 2004. Soil volatile fungistasis and volatile fungistatic compounds. - Soil Biology & Biochemistry 36 (12): 1997-2004.

Yang J., Li J., Liang L., Tian B., Zhang Y., Cheng C., & Zhang K. Q. 2007a. Cloning and characterization of an extracellular serine protease from the nematode-trapping fungus Arthrobotrys conoides. - Arch. Microbiol. 188 (2): 167-174.

Yang J., Liang L., Zhang Y., Li J., Zhang L., Ye F., Gan Z. & Zhang K. Q. 2007b. Purification and cloning of a novel serine protease from the nematode-trapping fungus Dactylellina varietas and its potential roles in infection against nematodes. - Appl. Microbiol. Biotechnol. 75 (3): 557-565.

Zanowiak D. J., Harrison T. P. &, Caire W. 1993. External bacteria of hibernating Myotis velifer (Chiroptera: Vespertilionidae). - The Southwestern naturalist 38 (1): 73-76.

Zhang T., Victor T. R., Rajkumar S. S., Li X., Okoniewski J. C., Hicks A. C., Davis A. D., Broussard K., LaDeau S. L., Chaturvedi S. & Chaturvedi V 2014. Mycobiome of the bat white nose syndrome affected caves and mines reveals diversity of fungi and local adaptation by the fungal pathogen Pseudogymnoascus (Geomyces) destructans. - PLoS One 9 (9): e108714.

Zhelyazkova V. 2014. Pseudogymnoascus destructans (Syn. Geomyces destructans) in Stara Planina Mts, Bulgaria. Master Thesis, Sofia University, Faculty of Biology, Department of Botany (Supervisor: Prof. Dr. M. P. Stoyneva), 87 pp. (In Bulgarian).

Zou C. S., Mo M. E., Gu Y. Q., Zhou J. P., Zhang K. Q. 2007. Possible contributions of volatile-producing bacteria to soil fungistasis. - Soil. Biol. Biochem. 39: 2371-2379.

Zukal J., Bandouchova H., Bartonicka T., Berkova H., Brack V., J. Brichta, Dolinay M., Jaron K. S., Kovacova V., Kovarík M., Martinkova. N., Ondracek K., Rehak Z., Turner G. G. & Pikula J. 2014. White-nose syndrome fungus: a generalist pathogen of hibernating bats. - PloS ONE 9 (5): e97224.

Zukal J., Bandouchova H., Brichta J., Cmokova A., Jaron K. S., Kolarík M., Kovacova V, KuBârovâ A., Novakova A., Orlov O., Pikula J., Presetnik P., Suba J., Zahradnikova Jr. A. & Martinkova N. 2016. White-nose syndrome without borders: Pseudogymnoascus destructans infection tolerated in Europe and Palearctic Asia but not in North America. - Scientific Reports 6: 19829.

Файлове за сваляне

Публикуван

2016-01-01

Как да цитирате

Review of the current status and future perspectives on Pseudogymnoascus destructans studies with reference to the species findings in Bulgaria. (2016). Годишник на Софийския Университет „Св. Климент Охридски“, Биологически факултет, Книга 2 – Ботаника, 100, 67-99. https://doi.org/10.60066/GSU.BIOFAC.Bot.100.67-99