Abstract
Emerging infectious diseases are a severe conservation threat for a variety of plants and animals. In North America, several bat species are threatened by white-nose disease, which has caused an unprecedented mass mortality of > 6 million bats since 2006. The fungus Pseudogymnoascus (Geomyces) destructans is the causative agent of the disease. Though asexual reproduction is the norm, sexual reproduction is possible as two mating types exist. Sexual reproduction has been implicated in the emergence of virulent strains of fungi but to date no rapid means of mating type characterisation was available for P. destructans. In this study, three mating type-specific primer sets were designed and tested on 80 isolates. The primers were multiplexed with microsatellite loci allowing for rapid and concurrent genotyping and mating type assignment. These markers will have great utility in better understanding and predicting the population dynamics and evolutionary potential of this fungus, including the emergence of virulent strains.
Data availability
Mating type sequences can be found on GenBank (MH360259–MH360269).
References
Arnaud-Haond S, Duarte CM, Alberto F, Serrão EA (2007) Standardizing methods to address clonality in population studies. Mol Ecol 16:5115–5139
Ashu EE, Xu J (2015) The roles of sexual and asexual reproduction in the origin and dissemination of strains causing fungal infectious disease outbreaks. Infect Genet Evol 36:199–209
Chibucos MC, Crabtree J, Nagaraj S, Chaturvedi S, Chaturvedi V (2013) Draft genome sequences of human pathogenic fungus Geomyces pannorumsensu lato and bat white nose syndrome pathogen Geomyces (Pseudogymnoascus) destructans. Genome Announc 1:e01045–13
Dool SE, O’ Donnell CFJ, Monks JM, Puechmaille SJ, Kerth G (2016) Phylogeographic-based conservation implications for the New Zealand long-tailed bat, (Chalinolobus tuberculatus): identification of a single ESU and a candidate population for genetic rescue. Cons Genet 17:1067–1079
Drees KP, Lorch JM, Puechmaille SJ, Parise KL, Wibbelt G, Hoyt JR, Sun K, Jargalsaikhan A, Dalannast M, Palmer JM, Lindner DL, Kilpatrick AM, Pearson T, Keim P, Blehert DS, Foster JT (2017a) Phylogenetics of a fungal invasion: origins and widespread dispersal of white-nose syndrome. mBio 8:e01941–17
Drees KP, Parise KL, Rivas SM, Felton LL, Puechmaille SJ, Keim P, Foster JT (2017b) Characterization of microsatellites in Pseudogymnoascus destructans for white-nose syndrome genetic analysis. J Wild Dis 53:869–874
Farrer RA, Weinert LA, Bielby J, Garner TWJ, Balloux F, Clare F, Bosch J, Cunningham AA, Weldon C, du Preez LH, Anderson L, Pond SLK, Shahar-Golan R, Henk DA, Fisher MC (2011) Multiple emergences of genetically diverse amphibian-infecting chytrids include a globalized hypervirulent recombinant lineage. Proc Natl Acad Sci USA 108:18732–18736
Frick W, Puechmaille SJ, Hoyt JR, Nickel BA, Langwig KE, Foster JT, Horáček I, Bartonička T, Barlow KE, Haarsma A-J, van der Kooij J, Rodrigues L, Mulkens B, Petrov B, Herzog C, Reynolds R, Stihler CW, Turner GG, Feller D, Kilpatrick AM (2015) Disease alters macroecological patterns of North American bats. Glob Ecol Biogeogr 24:741–749
Fritze M, Puechmaille SJ (2018) Identifying unusual mortality events in bats: a baseline for bat hibernation monitoring and white-nose syndrome research. Mammal Rev 48:224–228
Gargas A, Trest MT, Christiensen M, Volk TJ, Blehert DS (2009) Geomyces destructans sp. nov. associated with bat white-nose syndrome. Mycotaxon 108:147–154
Leopardi S, Blake D, Puechmaille SJ (2015) White-nose syndrome fungus introduced from Europe to North America. Curr Biol 25:R217–R219
O’Hanlon SJ, Rieux A, Farrer RA, Rosa GM, Waldman B, Bataille A, Kosch TA, Murray KA, Brankovics B, Fumagalli M, Martin MD, Wales N, Alvarado-Rybak M, Bates KA, Berger L, Böll S, Brookes L, Clare F, Courtois EA, Cunningham AA, Doherty-Bone TM, Ghosh P, Gower DJ, Hintz WE, Höglund J, Jenkinson TS, Lin C-F, Laurila A, Loyau A, Martel A, Meurling S, Miaud C, Minting P, Pasmans F, Schmeller DS, Schmidt BR, Shelton JMG, Skerratt LF, Smith F, Soto-Azat C, Spagnoletti M, Tessa G, Toledo LF, Valenzuela-Sánchez A, Verster R, Vörös J, Webb RJ, Wierzbicki C, Wombwell E, Zamudio KR, Aanensen DM, James TY, Gilbert MTP, Weldon C, Bosch J, Balloux F, Garner TWJ, Fisher MC (2018) Recent Asian origin of chytrid fungi causing global amphibian declines. Science 360:621–627
Palmer JM, Kubatova A, Novakova A, Minnis AM, Kolarik M, Lindner DL (2014) Molecular characterization of a heterothallic mating system in Pseudogymnoascus destructans, the fungus causing white-nose syndrome of bats. G3 Genes Genom Genet 4:1755–1763
Puechmaille SJ, Verdeyroux P, Fuller H, Ar Gouilh M, Bekaert M, Teeling EC (2010) White-nose syndrome fungus (Geomyces destructans) in bat, France. Emerg Infect Dis 16:290–293
Puechmaille SJ, Frick W, Kunz TH, Racey PA, Voigt CC, Wibbelt G, Teeling EC (2011a) White-nose syndrome: is this emerging disease a threat to European bats? Trends Ecol Evol 26:570–576
Puechmaille SJ, Wibbelt G, Korn V, Fuller H, Forget F, Mühldorfer K, Kurth A, Bogdanowicz W, Borel C, Bosch T, Cherezy T, Drebet M, Görföl T, Haarsma A-J, Herhaus F, Hallart G, Hammer M, Jungmann C, Le Bris Y, Lutsar L, Masing M, Mulkens B, Passior K, Starrach M, Wojtaszewski A, Zöphel U, Teeling EC (2011b) Pan-European distribution of White-Nose Syndrome fungus (Geomyces destructans) not associated with mass mortality. PLoS One 6:e19167
Stukenbrock EH (2016a) Hybridization speeds up the emergence and evolution of a new pathogen species. Nat Genet 48:113–115
Stukenbrock EH (2016b) The role of hybridization in the evolution and emergence of new fungal plant pathogens. Phytopathology 106:104–112
Zhan J, Kema GHJ, Waalwijk C, McDonald BA (2002) Distribution of mating type alleles in the wheat pathogen Mycosphaerella graminicola over spatial scales from lesions to continents. Fungal Genet Biol 36:128–136
Acknowledgements
We kindly thank Jens Berg of NABU Mecklenburg Vorpommern bat conservation group for facilitating access to the sampling site and Gerald Kerth for providing access to lab facilities. This work was funded by a Bat Conservation International grant awarded to SJP.
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12686_2018_1064_MOESM1_ESM.xlsx
Supplementary material 1: Table S1 contains the genotypic and mating type data, as well as clonal richness (R) calculated per bat and per swab, as recommended in Arnaud-Haond et al. (2007). (XLSX 22 KB)
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Dool, S., Altewischer, A., Fischer, N.M. et al. Mating type determination within a microsatellite multiplex for the fungal pathogen Pseudogymnoascus destructans, the causative agent of white-nose disease in bats. Conservation Genet Resour 12, 45–48 (2020). https://doi.org/10.1007/s12686-018-1064-6
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DOI: https://doi.org/10.1007/s12686-018-1064-6