Molecular characterization of a heterothallic mating system in Pseudogymnoascus destructans, the Fungus causing white-nose syndrome of bats

. 2014 Jul 21 ; 4 (9) : 1755-63. [epub] 20140721

Jazyk angličtina Země Velká Británie, Anglie Médium electronic

Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid25053709

White-nose syndrome (WNS) of bats has devastated bat populations in eastern North America since its discovery in 2006. WNS, caused by the fungus Pseudogymnoascus destructans, has spread quickly in North America and has become one of the most severe wildlife epidemics of our time. While P. destructans is spreading rapidly in North America, nothing is known about the sexual capacity of this fungus. To gain insight into the genes involved in sexual reproduction, we characterized the mating-type locus (MAT) of two Pseudogymnoascus spp. that are closely related to P. destructans and homothallic (self-fertile). As with other homothallic Ascomycota, the MAT locus of these two species encodes a conserved α-box protein (MAT1-1-1) as well as two high-mobility group (HMG) box proteins (MAT1-1-3 and MAT1-2-1). Comparisons with the MAT locus of the North American isolate of P. destructans (the ex-type isolate) revealed that this isolate of P. destructans was missing a clear homolog of the conserved HMG box protein (MAT1-2-1). These data prompted the discovery and molecular characterization of a heterothallic mating system in isolates of P. destructans from the Czech Republic. Both mating types of P. destructans were found to coexist within hibernacula, suggesting the presence of mating populations in Europe. Although populations of P. destructans in North America are thought to be clonal and of one mating type, the potential for sexual recombination indicates that continued vigilance is needed regarding introductions of additional isolates of this pathogen.

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Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., et al. , 1997.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389–3402 PubMed PMC

Amselem J., Cuomo C. A., van Kan J. A., Viaud M., Benito E. P., et al. , 2011.  Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet. 7: e1002230. PubMed PMC

Bayram O., Braus G. H., 2012.  Coordination of secondary metabolism and development in fungi: the velvet family of regulatory proteins. FEMS Microbiol. Rev. 36: 1–24 PubMed

Bayram O., Krappmann S., Ni M., Bok J. W., Helmstaedt K., et al. , 2008.  VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science 320: 1504–1506 PubMed

Champe S. P., el-Zayat A. A., 1989.  Isolation of a sexual sporulation hormone from Aspergillus nidulans. J. Bacteriol. 171: 3982–3988 PubMed PMC

Chaturvedi, V., D. J. Springer, M. J. Behr, R. Ramani, X. Li et al., 2010 Morphological and molecular characterizations of psychrophilic fungus Geomyces destructans from New York bats with white nose syndrome (WNS). PloS One 5:e10783. PubMed PMC

Cheema M. S., Christians J. K., 2011.  Virulence in an insect model differs between mating types in Aspergillus fumigatus. Med. Mycol. 49: 202–207 PubMed

Chibucos M. C., Crabtree J., Nagaraj S., Chaturvedi S., Chaturvedi V., 2013.  Draft genome sequences of human pathogenic fungus Geomyces pannorum sensu lato and bat White Nose Syndrome pathogen Geomyces (Pseudogymnoascus) destructans. Genome Announc 1: e01045–13 PubMed PMC

Christensen M., Whittingham W. F., 1965.  The soil microfungi of open bogs and conifer swamps in Wisconsin. Mycologia 57: 882–896

Dyer P. S., O’Gorman C. M., 2012.  Sexual development and cryptic sexuality in fungi: insights from Aspergillus species. FEMS Microbiol. Rev. 36: 165–192 PubMed

Ferreira A. V., Saupe S., Glass N. L., 1996.  Transcriptional analysis of the mtA idiomorph of Neurospora crassa identifies two genes in addition to mtA-1. Mol. Gen. Genet. 250: 767–774 PubMed

Froschauer A., Coleman J. J., 2012, pp. 1–2 in North American bat death toll exceeds 5.5 million from white-nose syndrome, U.S. Fish & Wildlife Service, http://www.whitenosesyndrome.org/sites/default/files/files/wns_mortality_2012_nr_final_0.pdf Office of Communications, Arlington, VA.

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

Giles S. S., Dagenais T. R., Botts M. R., Keller N. P., Hull C. M., 2009.  Elucidating the pathogenesis of spores from the human fungal pathogen Cryptococcus neoformans. Infect. Immun. 77: 3491–3500 PubMed PMC

Heitman J., Sun S., James T. Y., 2013.  Evolution of fungal sexual reproduction. Mycologia 105: 1–27 PubMed

Klix V., Nowrousian M., Ringelberg C., Loros J. J., Dunlap J. C., et al. , 2010.  Functional characterization of MAT1–1-specific mating-type genes in the homothallic ascomycete Sordaria macrospora provides new insights into essential and nonessential sexual regulators. Eukaryot. Cell 9: 894–905 PubMed PMC

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

Kwon-Chung K. J., Edman J. C., Wickes B. L., 1992.  Genetic association of mating types and virulence in Cryptococcus neoformans. Infect. Immun. 60: 602–605 PubMed PMC

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

Lorch J. M., Muller L. K., Russell R. E., O’Connor M., Lindner D. L., et al. , 2013.  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: 1293–1301 PubMed PMC

MacHardy W. E., Gadoury D. M., Gessler C., 2001.  Parasitic and biological fitness of Venturia inaequalis: relationship to disease management strategies. Plant Dis. 85: 1036–1051 PubMed

Marchler-Bauer A., Lu S., Anderson J. B., Chitsaz F., Derbyshire M. K., et al. , 2011.  CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res. 39: D225–D229 PubMed PMC

Martin T., Lu S.-W., van Tilbeurgh H., Ripoll D. R., Dixelius C., et al. , 2010.  Tracing the origin of the fungal α1 domain places its ancestor in the HMG-box superfamily: implication for fungal mating-type evolution. PLoS ONE 5: e15199. PubMed PMC

Martínková N., Bačkor P., Bartonička T., Blažková P., Cervený J., et al. , 2010.  Increasing incidence of Geomyces destructans fungus in bats from the Czech Republic and Slovakia. PLoS ONE 5: e13853. PubMed PMC

Meteyer C. U., Buckles E. L., Blehert D. S., Hicks A. C., Green D. E., et al. , 2009.  Histopathologic criteria to confirm white-nose syndrome in bats. J. Vet. Diagn. Invest. 21: 411–414 PubMed

Metzenberg R. L., Glass N. L., 1990.  Mating type and mating strategies in Neurospora. BioEssays 12: 53–59 PubMed

Minnis A. M., Lindner D. L., 2013.  Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America. Fungal Biol. 117: 638–649 PubMed

Muller L. K., Lorch J. M., Lindner D. L., O’Connor M., Gargas A., et al. , 2012.  Bat white-nose syndrome: A real-time TaqMan polymerase chain reaction test targeting the intergenic spacer region of Geomyces destructans. Mycologia 105: 253–259 PubMed

Ni M., Feretzaki M., Sun S., Wang X., Heitman J., 2011.  Sex in fungi. Annu. Rev. Genet. 45: 405–430 PubMed PMC

Nielsen K., Heitman J., 2007.  Sex and virulence of human pathogenic fungi. Adv. Genet. 57: 143–173 PubMed

Nielsen K., Marra R. E., Hagen F., Boekhout T., Mitchell T. G., et al. , 2005.  Interaction between genetic background and the mating-type locus in Cryptococcus neoformans virulence potential. Genetics 171: 975–983 PubMed PMC

O’Gorman C. M., Fuller H. T., Dyer P. S., 2009.  Discovery of a sexual cycle in the opportunistic fungal pathogen Aspergillus fumigatus. Nature 457: 471–474 PubMed

Paoletti M., Rydholm C., Schwier E. U., Anderson M. J., Szakacs G., et al. , 2005.  Evidence for sexuality in the opportunistic fungal pathogen Aspergillus fumigatus. Curr. Biol. 15: 1242–1248 PubMed

Paoletti M., Seymour F. A., Alcocer M. J. C., Kaur N., Calvo A. M., et al. , 2007.  Mating type and the genetic basis of self-fertility in the model fungus Aspergillus nidulans. Curr. Biol. 17: 1384–1389 PubMed

Pikula J., Bandouchova H., Novotny L., Meteyer C. U., Zukal J., et al. , 2012.  Histopathology confirms white-nose syndrome in bats in Europe. J. Wildl. Dis. 48: 207–211 PubMed

Puechmaille S. J., Frick W. F., Kunz T. H., Racey P. A., Voigt C. C., et al. , 2011.  White-nose syndrome: is this emerging disease a threat to European bats? Trends Ecol. Evol. 26: 570–576 PubMed

Puechmaille S. J., Verdeyroux P., Fuller H., Gouilh M. A., Bekaert M., et al. , 2010.  White-nose syndrome fungus (Geomyces destructans) in bat, France. Emerg. Infect. Dis. 16: 290–293 PubMed PMC

Quevillon E., Silventoinen V., Pillai S., Harte N., Mulder N., et al. , 2005.  InterProScan: protein domains identifier. Nucleic Acids Res. 33: W116–120. PubMed PMC

Rajkumar S. S., Li X., Rudd R. J., Okoniewski J. C., Xu J., et al. , 2011.  Clonal genotype of Geomyces destructans among bats with White Nose Syndrome, New York, USA. Emerg. Infect. Dis. 17: 1273–1276 PubMed PMC

Ren P., Haman K. H., Last L. A., Rajkumar S. S., Keel M. K., et al. , 2012.  Clonal spread of Geomyces destructans among bats, midwestern and southern United States. Emerg. Infect. Dis. 18: 883–885 PubMed PMC

Rice A. V., Currah R. S., 2006.  Two new species of Pseudogymnoascus with Geomyces anamorphs and their phylogenetic relationship with Gymnostellatospora. Mycologia 98: 307–318 PubMed

Sambrook J., Russell D. W., 2001.  Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY

Shimizu K., Keller N. P., 2001.  Genetic involvement of a cAMP-dependent protein kinase in a G protein signaling pathway regulating morphological and chemical transitions in Aspergillus nidulans. Genetics 157: 591–600 PubMed PMC

Solovyev V., Kosarev P., Seledsov I., Vorobyev D., 2006.  Automatic annotation of eukaryotic genes, pseudogenes and promoters. Genome Biol. 7: S10–S12 PubMed PMC

Stanke, M., R. Steinkamp, S. Waack, and B. Morgenstern, 2004 AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res. 32: W309–312. PubMed PMC

Tsuneda A., 1982.  Scanning electron microscopy of Pseudogymnoascus roseus. Mycologia 74: 844–847

Velagapudi R., Hsueh Y.-P., Geunes-Boyer S., Wright J. R., Heitman J., 2009.  Spores as infectious propagules of Cryptococcus neoformans. Infect. Immun. 77: 4345–4355 PubMed PMC

Wang Z., Ye S., Li J., Zheng B., Bao M., et al. , 2011.  Fusion primer and nested integrated PCR (FPNI-PCR): a new high-efficiency strategy for rapid chromosome walking or flanking sequence cloning. BMC Biotechnol. 11: 109. PubMed PMC

Warnecke L., Turner J. M., Bollinger T. K., Lorch J. M., Misra V., et al. , 2012.  Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc. Natl. Acad. Sci. USA 109: 6999–7003 PubMed PMC

Wibbelt G., Kurth A., Hellmann D., Weishaar M., Barlow A., et al. , 2010.  White-nose syndrome fungus (Geomyces destructans) in bats, Europe. Emerg. Infect. Dis. 16: 1237–1243 PubMed PMC

Yun S. H., Arie T., Kaneko I., Yoder O. C., Turgeon B. G., 2000.  Molecular organization of mating type loci in heterothallic, homothallic, and asexual Gibberella/Fusarium species. Fungal Genet. Biol. 31: 7–20 PubMed

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