Morphological and molecular characterizations of psychrophilic fungus Geomyces destructans from New York bats with white nose syndrome (WNS)

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  Chaturvedi, Vishnu ^a,b   Springer, Deborah J ^a,b,e   Behr, Melissa J ^a,f   Ramani, Rama ^a,b   Li, Xiaojiang ^a   Peck, Marcia K ^a   Ren, Ping ^a   Bopp, Dianna J ^a   Wood, Britta ^a,g   Samsonoff, William A ^a   Butchkoski, Calvin M ^c   Hicks, Alan C ^d   Stone, Ward B ^d   Rudd, Robert J ^a   Chaturvedi, Sudha ^a,b  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c Pennsylvania Game Commission   (United States)

^d NEW YORK STATE DEPARTMENT OF ENVIRONMENTAL CONSERVATION   (United States)

^e DUKE UNIVERSITY MEDICAL CENTER   (United States)

^f UNIVERSITY OF WISCONSIN MADISON   (United States)

^g Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL DNA;

ANIMAL DISEASE; ANIMAL TISSUE; ARTICLE; BAT; CONTROLLED STUDY; DNA DETERMINATION; FEMALE; FUNGAL EXAMINATION; FUNGAL MORPHOLOGY; FUNGAL VIRULENCE; FUNGUS; FUNGUS CULTURE; FUNGUS IDENTIFICATION; FUNGUS ISOLATION; GEOMYCES DESTRUCTANS; IN VITRO STUDY; MALE; MOLECULAR DYNAMICS; MOLECULAR PHYLOGENY; MORPHOLOGICAL TRAIT; MYCOSIS; NONHUMAN; NOSE SMEAR; NUCLEOTIDE SEQUENCE; PERIODIC ACID SCHIFF STAIN; PROTEIN DEGRADATION; PSYCHROPHILE; RANDOM AMPLIFIED POLYMORPHIC DNA; SCANNING ELECTRON MICROSCOPY; TISSUE SECTION; UNINDEXED SEQUENCE; WHITE NOSE SYNDROME; ANIMAL; ANTIBODY SPECIFICITY; ASCOMYCETES; CLASSIFICATION; DNA SEQUENCE; GENETICS; ISOLATION AND PURIFICATION; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; PATHOLOGY; PHYLOGENY; SYNDROME; ULTRASTRUCTURE; UNITED STATES;

ANIMALIA; FUNGI; GEOMYCES; MYOTIS LUCIFUGUS;

ANIMALS; ASCOMYCOTA; CHIROPTERA; DNA, FUNGAL; MYCOLOGICAL TYPING TECHNIQUES; MYCOSES; NEW YORK; ORGAN SPECIFICITY; PHYLOGENY; RANDOM AMPLIFIED POLYMORPHIC DNA TECHNIQUE; SEQUENCE ANALYSIS, DNA; SYNDROME;

EID: 77956278404     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010783     Document Type: Article

References (57)

1. Kunz TH, Fenton MB (2003) Bat Ecology. Chicago, IL: University of Chicago Press. 779 p.
2. Williams-Guillen K, Perfecto I, Vandermeer J (2008) Bats limit insects in a neotropical agroforestry system. Science 320: 70.
3. Jülg B, Elias J, Zahn A, Köppen S, Becker-Gaab C, et al. (2008) Bat-associated histoplasmosis can be transmitted at entrances of bat caves and not only inside the caves. J Travel Med 15: 133-136.
4. Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T (2006) Bats: Important reservoir hosts of emerging viruses. Clin Microbiol Rev 19: 531-545.
5. Chaturvedi VP, Randhawa HS, Khan ZU, Singh N, Kini S (1984) Prevalence of Basidiobolus ranarum Eidam in the intestinal tract of an insectivorous bat, Rhinopoma hardwickei hardwickei Gray, in Delhi. Sabouraudia 22: 185-189.
6. Trimarchi CV, Debbie JG (1977) Naturally occurring rabies virus and neutralizing antibody in two species of insectivorous bats of New York State. J Wildl Dis 13: 366-369.
7. Lampo M, Feliciangeli MD, Marquez LM, Bastidas C, Lau P (2000) A possible role of bats as a blood source for the Leishmania vector Lutzomyia longipalpis (Diptera: Psychodidae). Am J Trop Med Hyg 62: 718-719.
8. Wilkinson GS, South JM (2002) Life history, ecology and longevity in bats. Aging Cell 1: 124-131.
9. Griffin DR (1940) Notes on the life history of New England cave bats. J Mammal 21: 181-187.
10. Hicks AC, Novak PG (2002) History, status, and behaviour of hibernating populations in the Northeast; Kurta A, Kennedy J, eds. Austin, TX: Bat Conservation International. pp 35-47.
11. Johnson SA, Brack V, Rolley RE (1998) Overwinter weight loss of Indiana bats (Myotis sodalis) from hibernacula subject to human visitation. Am Mid Nat 139: 255-261.
12. DeBlase AF, Humphrey SR, Drury KS (1965) Cave flooding and mortality in bats in Wind Cave, Kentucky. J Mammal 46: 96.
13. Kelly T (2008) Bats perish, and no one knows why. The New York Times. New York, NY. 1 p.
14. Blehert DS, Hicks AC, Behr M, Meteyer CU, Berlowski-Zier BM, et al. (2009) Bat white-nose syndrome: an emerging fungal pathogen? Science 323: 227.
15. Gargas A, Trest MT, Christensen M, Volk TJ, Blehert DS (2009) Geomyces destructans sp.nov. associated with bat white-nose syndrome. Mycotaxon 108: 147-154.
16. Rice AV, Currah RS (2006) Two new species of Pseudogymnoascus with Geomyces anamorphs and their phylogenetic relationship with Gymnostellatospora. Mycologia 98: 307-318.
17. Courtin F, Stone WB, Risatti G, Gilbert K, Van Kruiningen HJ (2010) Pathologic findings and liver elements in hibernating bats with White-Nose Syndrome. Vet Pathol: 47(2): 214-219.
18. Puechmaille SJ, Verdeyroux P, Fuller H, Gouilh MA, Bekaert M, et al. (2010) White-nose syndrome fungus (Geomyces destructans) in bat, France. Emerg Infect Dis 16: 290-293.
19. Meteyer CU, Buckles EL, Blehert DS, Hicks AC, Green DE, et al. (2009) Histopathologic criteria to confirm white-nose syndrome in bats. J Vet Diagn Invest 21: 411-414.
20. de Hoog GS, Guarro J, Gene J, Figueras MJ (2000) Atlas of Clinical Fungi. Utrecht: Centraalbureau voor Schimmelcultures/Universitat Rovira i Virgili. 1126 p.
21. Christen-Zaech S, Patel S, Mancini AJ (2008) Recurrent cutaneous Geomyces pannorum infection in three brothers with ichthyosis. J Am Acad Dermatol 58: S112-113.
22. Erne JB, Walker MC, Strik N, Alleman AR (2007) Systemic infection with Geomyces organisms in a dog with lytic bone lesions. J Am Vet Med Assoc 230: 537-540.
23. Gianni C, Caretta G, Romano C (2003) Skin infection due to Geomyces pannorum var. pannorum. Mycoses 46: 430-432.
24. Zelenkova H (2006) Geomyces pannorum as a possible causative agent of dermatomycosis and onychomycosis in two patients. Acta Dermatovenerol Croat 14: 21-25.
25. Carvajal Zamora JR (1977) Isolation of Histoplasma capsulatum from soil in the Aguas Buenos Caves, Aguas Buenos, Puerto Rico. I. An ecological approach. Mycopathologia 60: 157-161.
26. Baptista-Rosas RC, Hinojosa A, Riquelme M (2007) Ecological niche modeling of Coccidioides spp. in western North American deserts. Ann N Y Acad Sci 1111: 35-46.
27. Klein BS, Vergeront JM, Weeks RJ, Kumar UN, Mathai G, et al. (1986) Isolation of Blastomyces dermatitidis in soil associated with a large outbreak of blastomycosis in Wisconsin. N Engl J Med 314: 529-534.
28. Franco M, Bagagli E, Scapolio S, da Silva Lacaz C (2000) A critical analysis of isolation of Paracoccidioides brasiliensis from soil. Med Mycol 38: 185-191.
29. Ruisi S, Barreca D, Selbmann L, Zucconi L, Onofri S (2007) Fungi in Antarctica. Rev Environ Sci Biotechnol 6: 127-141.
30. Möller C, Weber G, Dreyfuss MM (1996) Intraspecific diversity in the fungal species Chaunopycnis alba: Implications for microbial screening programs. J Ind Microbiol Biotechnol 17: 359-372.
31. Murtagh GJ, Dyer PS, Furneaux PA, Crittenden PD (2002) Molecular and physiological diversity in the bipolar lichen-forming fungus Xanthoria elegans. Mycolo Res 106: 1277-1286.
32. Gilichinsky D, Rivkina E, Bakermans C, Shcherbakova V, Petrovskaya L, et al. (2005) Biodiversity of cryopegs in permafrost. FEMS Microbiol Ecol 53: 117-128.
33. Connell L, Redman R, Craig S, Scorzetti G, Iszard M, et al. (2008) Diversity of Soil Yeasts Isolated from South Victoria Land, Antarctica. Microb Ecol 56: 448-459.
34. Malosso E, Waite I, English L, Hopkins D, O'Donnell A (2006) Fungal diversity in maritime Antarctic soils determined using a combination of culture isolation, molecular fingerprinting and cloning techniques. Polar Biol 29: 552-561.
35. Schmidt S, Wilson K, Meyer A, Gebauer M, King A (2008) Phylogeny and ecophysiology of opportunistic "Snow Molds" from a subalpine forest ecosystem. Microb Ecol 56: 681-687.
36. Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151: 341-353.
37. Marshall WA (1998) Aerial transport of keratinaceous substrate and distribution of the fungus Geomyces pannorum in Antarctic soils. Microb Ecol 36: 212-219.
38. Schonborn C, Schmoranzer H (1970) [Mold infections of the toe nails] Untersuchungen uber Schimmelpilzinfektionen der Zehennagel. Mykosen 13: 253-272.
39. Kerth G, Almasi B, Ribi N, Thiel D, Lüpold S (2003) Social interactions among wild female Bechstein's bats (Myotis bechsteinii) living in a maternity colony. Acta Ethologica 5: 107-114.
40. Lopez-Otan C, Bond JS (2008) Proteases: Multifunctional enzymes in life and disease. J Biol Chem 283: 30433-30437.
41. Scott DW, Miller WH, Griffin CE (2000) Muller and Kirk's Small Animal Dermatology. Philadelphia: W.B. Saunders Company. 1528 p.
42. Hatten BA, Allen R, Sulkin SE (1970) Studies on the immune capabilities of Chiroptera: I. Quantitative and Qualitative Nature of the Immune Responses in Bats to Bacteriophage {varphi}X174. J Immunol 105: 872-878.
43. Carey HV, Andrews MT, Martin SL (2003) Mammalian hibernation: Cellular and molecular responses to depressed metabolism and low temperature. Physiol Rev 83: 1153-1181.
44. Kurtz CC, Carey HV (2007) Seasonal changes in the intestinal immune system of hibernating ground squirrels. Dev Comp Immunol 31: 415-428.
45. ter Hofsted HM, Fenton MB (2005) Relationships between roost preferences, ectoparasite density, and grooming behaviour of neotropical bats. J Zool 266: 333-340.
46. Giorgi MS, Arlettaz R, Christe P, Vogel P (2001) The energetic grooming costs imposed by a parasitic mite (Spinturnix myoti) upon its bat host (Myotis myotis). Proc Biol Sci 268: 2071-2075.
47. Samson RA, Hoekstra ES, Frisvad JC (2004) Introduction to Food- and Airborne Fungi. Utrecht: Centraalbureau voor Schimmelcultures. 389 p.
48. Kwon-Chung KJ, Bennett JA (1992) Medical Mycology. Philadelphia: Lea & Febiger. 866 p.
49. Symonds EP, Trott DJ, Bird PS, Mills P (2008) Growth characteristics and enzyme activity in Batrachochytrium dendrobatidis isolates. Mycopathologia 166: 143-147.
50. De Bernardis F, Mondello F, San Millan R, Ponton J, Cassone A (1999) Biotyping and virulence properties of skin isolates of Candida parapsilosis. J Clin Microbiol 37: 3481-3486.
51. Price MF, Wilkinson ID, Gentry LO (1982) Plate method for detection of phospholipase activity in Candida albicans. Sabouraudia 20: 7-14.
52. Chaturvedi V, Fan J, Stein B, Behr MJ, Samsonoff WA, et al. (2002) Molecular genetic analyses of mating pheromones reveal intervariety mating or hybridization in Cryptococcus neoformans. Infect Immun 70: 5225-5235.
53. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, diagnostics and forensics. In: Innis MA, Gelfand D.H, Sninsky J.J, White T.J, eds. PCR Protocols:A guide to methods and applications. San Diego: Academic Press.
54. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0. Mol Biol Evol 24: 1596-1599.
55. Dyavaiah M, Ramani R, Chu D, Ritterband D, Shah M, et al. (2007) Molecular characterization, biofilm analysis and experimental biofouling study of Fusarium isolates from recent cases of fungal keratitis in New York State. BMC Ophthalmol 7: 1.
56. Meyer W, Marszewska K, Amirmostofian M, Igreja RP, Hardtke C, et al. (1999) Molecular typing of global isolates of Cryptococcus neoformans var. neoformans by polymerase chain reaction fingerprinting and randomly amplified polymorphic DNA-a pilot study to standardize techniques on which to base a detailed epidemiological survey. Electrophoresis 20: 1790-1799.
57. Gente S, Sohier D, Coton E, Duhamel C, Gueguen M (2006) Identification of Geotrichum candidum at the species and strain level: proposal for a standardized protocol. J Ind Microbiol Biotechnol 33: 1019-1031.