Pseudogymnoascus destructans

Last updated • 5 min readFrom Wikipedia, The Free Encyclopedia

Pseudogymnoascus destructans
Little Brown Bat with White Nose Syndrome (Greeley Mine, cropped).jpg
In white nose syndrome, Pseudogymnoascus destructans can be found growing on the muzzle, wing, and ear of bats, in this case, a little brown bat.
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Leotiomycetes
Order: Thelebolales
Family: Pseudeurotiaceae
Genus: Pseudogymnoascus
Species:
P. destrucans
Binomial name
Pseudogymnoascus destrucans
Synonyms
  • Geomyces destructansBlehert et al. 2008

Pseudogymnoascus destructans (formerly known as Geomyces destructans) is a psychrophilic (cold-loving) fungus that causes white-nose syndrome (WNS), a fatal disease that has devastated bat populations in parts of the United States and Canada. Unlike species of Geomyces , P. destructans forms asymmetrically curved conidia. [1] Pseudogymnoascus destructans grows very slowly on artificial media and cannot grow at temperatures above 20 °C. [1] [2] [3] It can grow around 4 °C to 20 °C, which encompasses the temperatures found in winter bat hibernacula. [1] [2] Phylogenic evaluation has revealed this organism should be reclassified under the family Pseudeurotiaceae, changing its name to Pseudogymnoascus destructans. [4]

Contents

History

In 2008, Blehert et al. described the fungus associated with white-nose syndrome as a member of the genus Geomyces. [5] In 2009, Gargas et al. were the first to describe the fungus as a unique species; the specific name they chose, "destructans", means "destroying". [1] The fungus was definitively identified as the cause of the syndrome in bats, according to research published in 2011 by scientists at the United States Geological Survey. [6] It was previously unknown whether this fungus was the primary cause of WNS or was an opportunistic pathogen associated with the disease, though strong evidence suggested that the fungus was the etiologic agent. [2] [7] In 2013, an analysis of the phylogenetic relationship indicated that this fungus was more closely related to the genus Pseudogymnoascus than to the genus Geomyces changing its Latin binomial to Pseudogymnoascus destructans. [4]

Distribution

Pseudogymnoascus destructans is believed to originate from Europe. [4] [8] The current P. destructans European distribution includes Austria, Belgium, Czech Republic, Denmark, Estonia, France, Germany, Hungary, the Netherlands, Poland, Romania, Slovakia, Switzerland, Turkey, Ukraine and the United Kingdom. [7] [8] [9] [10]

The North American geographic distribution of P. destructans continues to increase each year since its initial introduction to New York State in 2006. Its current distribution includes 38 states in the U.S.A. and at least 7 Canadian provinces.

Bat species affected by P. destructans

In North America, P. destructans has been found to infect at least eleven species of bats, [11] of which it has caused diagnostic symptoms of white-nose syndrome in the endangered Indiana bat (Myotis sodalis), the endangered gray bat ( Myotis grisescens ), the endangered little brown bat (Myotis lucifugus), the northern long-eared bat (Myotis septentrionalis), the big brown bat (Eptesicus fuscus), the tri-colored bat (Perimyotis subflavus), and the eastern small-footed bat (Myotis leibii). [1] [12] Pseudogymnoascus destructans has been found on four additional North American bat species: the endangered Virginia big-eared bat (Corynorhinus townsendii virginianus), the cave bat (Myotis velifer), the Silver-haired bat (Lasionycteris noctivagans), and the South-eastern bat (Myotis austroriparius). The European bat species that have been shown to harbour P. destructans include Bechstein's bat (Myotis bechsteinii), Lesser mouse-eared bat (Myotis blythii oxygnathus), Brandt's bat (Myotis brandtii), pond bat (Myotis dasycneme), Daubenton's bat (Myotis daubentonii), Greater mouse-eared bat (Myotis myotis), whiskered bat (Myotis mystacinus), Geoffroy's bat (Myotis emarginatus), Northern bat (Eptesicus nilssonii), Lesser horseshoe bat (Rhinolophus hipposideros), Barbastell (Barbastella barbastellus), Brown long-eared bat (Plecotus auritus) and Natterer's bat (Myotis nattereri), although large-scale European bat related fatalities are not reported. [9] [13]

Biology

Typical grey colony of Pseudogymnoascus destructans on Sabouraud dextrose agar. Pseudogymnoascus destructans grey culture.jpg
Typical grey colony of Pseudogymnoascus destructans on Sabouraud dextrose agar.
Pseudogymnoascus destructans in culture demonstrating characteristic curved conidia in blue/purple. (false color SEM image) Geomyces destructans in culture.png
Pseudogymnoascus destructans in culture demonstrating characteristic curved conidia in blue/purple. (false color SEM image)

P. destructans is a psychrophilic fungus, able to grow below 10 °C (50 °F) and with an upper limit near 20 °C (68 °F). This fungus produces brown and grey colonies, secretes a brownish pigment and reproduces asexually via characteristically curved conidia when cultured on Sabaouraud dextrose agar. The asymmetrically curved conidia are produced at the tips or sides singly or in short chains. Arthroconidia can be present and undergo rhexolytic separation. [1] Research has shown that P. destructans grows optimally between 12.5 and 15.8 °C (54.5 and 60.4 °F), with an upper growth limit of about 20 °C (68 °F). [3] The in vitro growth rate of P. destructans is reported to be very slow; however, several studies have shown that not all P. destructans isolates grow at the same rate. [3] [14] P. destructans grows as an opportunistic pathogen on bats, causing white-nose syndrome, [1] but it can also persist in the cave environment, [15] as a saprotroph. [16] [17] P. destructans can grow and sporulate (reproduce asexually via conidiation) on keratinaceous, chitinaceous, cellulosic, and lipid/protein rich substrates including dead fish, mushroom fruit bodies and dead insects. [16] P. destructans has been shown to utilize many nitrogen sources: nitrate, nitrite, ammonium, urea, and uric acid. [16] Although P. destructans can penetrate senescing moss cells, [18] cellulosic debris may not be a long term substrate for colonization. [16] P. destructans can tolerate elevated levels of environmental inhibitory sulfur compounds (cysteine, sulfite, and sulfide), grow over a wide pH range (pH 5-11), tolerate elevated environmental levels of calcium; however, P. destructans was found to be intolerant to matric-induced water stress.

Enzymatic activity

Pseudogymnoascus destructans demonstrating lipase activity on Rhodamine B agar. Pseudogymnoascus destructans on Rhodamine B agar.jpg
Pseudogymnoascus destructans demonstrating lipase activity on Rhodamine B agar.

Under laboratory conditions, P. destructans has been shown to produce numerous enzymes including β-glucosidase, esterase/esterase lipase/lipase, leucine and valine arylamidase, N-acetyl-β-glucosaminidase, naphthol-AS-B1-phosphohydrolase, both acid and alkaline phosphatases, various proteinase, and urease, while testing negative for cystine arylamidase, α-chymotrypsin, alpha/beta-galactosidase, β-glucuronidase, α-fucosidase, α-mannosidase, and trypsin. [2] Important dual virulence factors found in P. destructans and many other pathogenic fungi include urease, proteinase (aspartyll) and superoxide dismutase. [18] [19]

Control agents

In 2011, several compounds (antifungals, fungicides, and biocides) were shown to effectively inhibit the growth of P. destructans including benzalkonium chloride, chloroacetoxyquinoline, chloroxine, ciclopirox olamine, econazole, phenylmercuric acetate, pyrithione zinc and sulconazole. [20] The same study showed that P. destructans was sensitive to Amphotericin B, itraconazole, ketoconazole, posaconazole and voriconazole, while the fungus had some resistance to anidulafungin, caspofungin, flucytosine and micafungin. A recent study (2014) identified several volatile organic compounds (benzaldehyde, benzothiazole, decanal, nonanal, N,N-dimethyloctylamine, and 2-ethyl-1-hexanol) that were previously identified from fungistatic soils, which demonstrated inhibition of both mycelial extension and growth from conidia. [21]

A 2015 study showed that Rhodococcus rhodochrous could inhibit the growth of P. destructans. [22]

A positive breakthrough may have come while utilizing competitive genetics to investigate the evolutionary history of P. destructans compared to six closely related nonpathogenic species. The study published in the journal Nature Communications in 2018 discovered that due to a lost enzyme, P. destructans lacks an ability to repair DNA which has been damaged by ultraviolet (UV) light. [23] Ongoing research is taking place to see if there is a practical method to have bats activate a UV system as they enter and leave a hibernaculum and treat their infection. Not a long term solution, it may be enough to avoid population collapse allowing the species to evolve its own defenses to the fungus as Eurasian bats have.

Related Research Articles

<span class="mw-page-title-main">Tricolored bat</span> Species of bat

The tricolored bat or American perimyotis is a species of microbat native to eastern North America. Formerly known as the eastern pipistrelle, based on the incorrect belief that it was closely related to European Pipistrellus species, the closest known relative of the tricolored bat is now recognized as the canyon bat. Its common name "tricolored bat" derives from the coloration of the hairs on its back, which have three distinct color bands. It is the smallest bat species in the eastern and midwestern US, with individuals weighing only 4.6–7.9 g (0.16–0.28 oz). This species mates in the fall before hibernation, though due to sperm storage, females do not become pregnant until the spring. Young are born helpless, though rapidly develop, flying and foraging for themselves by four weeks old. It has a relatively long lifespan, and can live nearly fifteen years.

<span class="mw-page-title-main">Mexican free-tailed bat</span> Species of bat native to the Americas

The Mexican free-tailed bat or Brazilian free-tailed bat is a medium-sized bat native to North, Central, and South America and the Caribbean, so named because its tail can be almost half its total length and is not attached to its uropatagium. It has been claimed to have the fastest horizontal speed of any animal, reaching top ground speeds over 99 mph (160 km/h). It also flies the highest among bats, at altitudes around 3,300 m (10,800 ft).

<span class="mw-page-title-main">Big brown bat</span> Species of vesper bat

The big brown bat is a species of vesper bat distributed widely throughout North America, the Caribbean, and the northern portion of South America. It was first described as a species in 1796. Compared to other microbats, the big brown bat is relatively large, weighing 15–26 g (0.53–0.92 oz) and possessing a wingspan of 32.5–35 cm (12.8–13.8 in).

<span class="mw-page-title-main">Indiana bat</span> Species of bat

The Indiana bat is a medium-sized mouse-eared bat native to North America. It lives primarily in Southern and Midwestern U.S. states and is listed as an endangered species. The Indiana bat is grey, black, or chestnut in color and is 1.2–2.0 in long and weighs 4.5–9.5 g (0.16–0.34 oz). It is similar in appearance to the more common little brown bat, but is distinguished by its feet size, toe hair length, pink lips, and a keel on the calcar.

Rhodococcus rhodochrous is a bacterium used as a soil inoculant in agriculture and horticulture.

<span class="mw-page-title-main">Eastern red bat</span> Species of bat

The eastern red bat is a species of microbat in the family Vespertilionidae. Eastern red bats are widespread across eastern North America, with additional records in Bermuda.

A panzootic is an epizootic that spreads across a large region, or even worldwide. The equivalent in human populations is called a pandemic.

<span class="mw-page-title-main">Rafinesque's big-eared bat</span> Species of bat

Rafinesque's big-eared bat, sometimes known as the southeastern big-eared bat, is a species of vesper bat native to the southeastern United States.

<span class="mw-page-title-main">Ussuri tube-nosed bat</span> Species of bat

The Ussuri tube-nosed bat is a species of vesper bat in the family Vespertilionidae. It is threatened by habitat loss. It is the only species of bat that hibernates in snowbanks.

<span class="mw-page-title-main">Eastern small-footed myotis</span> Species of bat

The eastern small-footed bat is a species of vesper bat. It can be found in southern Ontario and Quebec in Canada and in mountainous portions of the eastern United States from New England to northern Georgia, and westward to northern Arkansas. It is among the smallest bats in eastern North America and is known for its small feet and black face-mask. Until recently, all North American small-footed Myotis were considered to be "Myotis leibii". The western population is now considered to be a separate species, Myotis ciliolabrum. The eastern small-footed bat is rare throughout its range, although the species may be locally abundant where suitable habitat exists. Studies suggest white-nose syndrome has caused declines in their populations. However, most occurrences of this species have only been counted within the past decade or two and are not revisited regularly, making their population status difficult to assess. Additionally, most bat populations in the eastern U.S. have been monitored using surveys conducted in caves and mines in the winter, but eastern small-footed bats hibernate in places that make them unlikely to be encountered during these surveys. Perhaps as a result, the numbers of eastern small-footed bats counted in winter tend to be low and they are relatively variable compared to other species of bats. Many biologists believe the species is stable, having declined little in recent times, but that it is vulnerable due to its relatively restricted geographic range and habitat needs.

<span class="mw-page-title-main">Little brown bat</span> Species of mammal found in North America

The little brown bat or little brown myotis is an endangered species of mouse-eared microbat found in North America. It has a small body size and glossy brown fur. It is similar in appearance to several other mouse-eared bats, including the Indiana bat, northern long-eared bat, and Arizona myotis, to which it is closely related. Despite its name, the little brown bat is not closely related to the big brown bat, which belongs to a different genus.

<span class="mw-page-title-main">White-nose syndrome</span> Fungal disease of bats

White-nose syndrome (WNS) is a fungal disease in North American bats which has resulted in the dramatic decrease of the bat population in the United States and Canada, reportedly killing millions as of 2018. The condition is named for a distinctive fungal growth around the muzzles and on the wings of hibernating bats. It was first identified from a February 2006 photo taken in a cave located in Schoharie County, New York. The syndrome has rapidly spread since then. In early 2018, it was identified in 33 U.S. states and seven Canadian provinces; plus the fungus, albeit sans syndrome, had been found in three additional states. Most cases are in the eastern half of both countries, but in March 2016, it was confirmed in a little brown bat in Washington state. In 2019, evidence of the fungus was detected in California for the first time, although no affected bats were found.

<span class="mw-page-title-main">Virginia big-eared bat</span> Subspecies of bat

The Virginia big-eared bat is one of two endangered subspecies of the Townsend's big-eared bat. It is found in Virginia, West Virginia, North Carolina, and Kentucky. In 1979, the US Fish and Wildlife Service categorized this as an endangered species. There are about 20,000 left and most of them can be found in West Virginia. The Virginia big-eared bat is the state bat of Virginia.

Geomyces is a genus of filamentous fungi in the family Myxotrichaceae. Members of the genus are widespread in distribution, especially in northern temperate regions. Known to be psychrotolerant and associated with Arctic permafrost soils, they are equally prevalent in the air of domestic dwellings, and children's sandpits. Species of Geomyces have previously been placed in the genus Chrysosporium.

<span class="mw-page-title-main">Bat</span> Order of flying mammals

Bats are flying mammals of the order Chiroptera. With their forelimbs adapted as wings, they are the only mammals capable of true and sustained flight. Bats are more agile in flight than most birds, flying with their very long spread-out digits covered with a thin membrane or patagium. The smallest bat, and arguably the smallest extant mammal, is Kitti's hog-nosed bat, which is 29–34 mm (1.1–1.3 in) in length, 150 mm (5.9 in) across the wings and 2–2.6 g (0.071–0.092 oz) in mass. The largest bats are the flying foxes, with the giant golden-crowned flying fox reaching a weight of 1.6 kg (3.5 lb) and having a wingspan of 1.7 m.

<i>Myotis septentrionalis</i> Species of mammal

Myotis septentrionalis, known as the northern long-eared bat or northern myotis, is a species of bat native to North America. There are no recognized subspecies. The northern long-eared bat is about 3–3.7 inches in length, with a wingspan of 9–10 inches. It is distinguishable by its long ears when comparing it to other bats in its genus. This species is commonly found in the northern United States and Southern Canada east of British Columbia. The geographic range includes 37 states.

There are eighteen indigenous species of bats in Canada, which are found in many parts of the country. They are insectivores, and are prey to falcons, hawks, owls, snakes, cats, and raccoons.

<i>Pseudogymnoascus</i> Genus of fungi

Pseudogymnoascus is a genus of fungi in the family Pseudeurotiaceae.

<span class="mw-page-title-main">Australasian bent-wing bat</span> Species of vesper bat

The Australasian bent-wing bat is a species of vesper bat in the family Miniopteridae. It is found in Australia and in Southeast Asia.

Malassezia vespertilionis is a species of yeast-like fungus that grows on the skin of bats. It was described as a new species in 2018. The holotype was obtained from a swab of wing skin of a hibernating northern long-eared bat collected in Wisconsin. The species epithet vespertilionis uses the Latin vespertilio (bat) to refer to the host.

References

  1. 1 2 3 4 5 6 7 Gargas A, Trest MT, Christensen M, Volk TJ, Blehert DS (April–June 2009). "Geomyces destructans sp. nov. associated with bat white-nose syndrome" (PDF). Mycotaxon . 108: 147–154. doi:10.5248/108.147. Archived from the original (PDF) on 2012-09-15. Retrieved 2010-12-30.
  2. 1 2 3 4 Chaturvedi V, Springer DJ, Behr MJ, Ramani R, Li X, Peck MK, Ren P, Bopp DJ, Wood B, Samsonoff WA, Butchkoski CM, Hicks AC, Stone WB, Rudd RJ, Chaturvedi S (May 2010). "Morphological and Molecular Characterizations of Psychrophilic Fungus Geomyces destructans from New York Bats with White Nose Syndrome (WNS)". PLOS ONE. 5 (5): e10783. Bibcode:2010PLoSO...510783C. doi: 10.1371/journal.pone.0010783 . PMC   2875398 . PMID   20520731.
  3. 1 2 3 Verant ML, Boyles JG, Waldrop W, Wibbelt G, Blehart DS (September 2012). "Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome". PLOS ONE. 7 (9): e46280. Bibcode:2012PLoSO...746280V. doi: 10.1371/journal.pone.0046280 . PMC   3460873 . PMID   23029462.
  4. 1 2 3 Minnis AM, Lindner DL (July 2013). "Phylogenetic evaluation of Geomyces and allies reveals no close relatives of Pseudogymnoascus destructans, comb. nov., in bat hibernacula of eastern North America". Fungal Biology. 117 (9): 638–49. doi:10.1016/j.funbio.2013.07.001. PMID   24012303.
  5. ↑ Blehert DS, Hicks AC, Behr M, et al. (October 2008). "Bat White-Nose Syndrome: An Emerging Fungal Pathogen?". Science. 323 (5911): 227. doi:10.1126/science.1163874. PMID   18974316. S2CID   23869393.
  6. ↑ Lorch, Jeffrey M.; Meteyer, Behr; Boyles, Cryan; Hicks, Ballman; Coleman, Redell; Reeder, Blehert (2011-10-26). "Experimental infection of bats with Geomyces destructans causes white-nose syndrome". Nature. advanced online publication (7377): 376–378. Bibcode:2011Natur.480..376L. doi:10.1038/nature10590. PMID   22031324. S2CID   4381156.
  7. 1 2 Puechmaille, Sébastien J.; Verdeyroux, Pascal; Fuller, Hubert; Ar Gouilh, Meriadeg; Bekaert, Michaël; Teeling, Emma C (February 2010). "White-nose syndrome fungus (Geomyces destructans) in bat, France". Emerging Infectious Diseases. 16 (2). Atlanta: Centers for Disease Control and Prevention: 290–293. doi:10.3201/eid1602.091391. ISSN   1080-6059. PMC   2958029 . PMID   20113562.
  8. 1 2 Puechmaille, SJ; Wibbelt G; Korn V; Fuller H; Forget F.; et al. (2011). "Pan-European distribution of white-nose syndrome fungus (Geomyces destructans) not associated with mass mortality". PLOS ONE. 6 (4): e19167. Bibcode:2011PLoSO...619167P. doi: 10.1371/journal.pone.0019167 . PMC   3083413 . PMID   21556356.
  9. 1 2 Martinkova, N; Backer P; Bartonicka T; Blazkova P; Cerveny J; et al. (2010). "Increasing incidence of Geomyces destructans fungus in bats from Czech Republic and Slovakia". PLOS ONE. 5 (11): e13853. Bibcode:2010PLoSO...513853M. doi: 10.1371/journal.pone.0013853 . PMC   2974652 . PMID   21079781.
  10. ↑ Wibbelt G, Kurth A, Hellmann D, Weishaar M, Barlow A, et al. (2010). "White-nose syndrome fungus (Geomyces destructans) in bats, Europe". Emerging Infectious Diseases. 16 (8): 1237–1242. doi:10.3201/eid1608.100002. PMC   3298319 . PMID   20678317.
  11. ↑ "Bats affected by WNS / White Nose Syndrome". whitenosesyndrome.org. U.S. Fish and Wildlife Service . Retrieved February 17, 2018.
  12. ↑ Blehart, DS; Hicks AC; Behr M; et al. (October 2008). "Bat white-nose syndrome: an emerging fungal Pathogen?". Science. 323 (5911): 227. doi:10.1126/science.1163874. PMID   18974316. S2CID   23869393.
  13. ↑ Zukal J, Bandouchova H, Bartonicka T, Berkova H, Brack V, Brichta J, Dolinay M, Jaron KS, Kovacova V, Kovarik M, Martínková N, Ondracek K, Rehak Z, Turner GG, Pikula J (May 2014). "White-nose syndrome fungus: a generalist pathogen of hibernating bats". PLOS ONE. 9 (5): e97224. Bibcode:2014PLoSO...997224Z. doi: 10.1371/journal.pone.0097224 . PMC   4018256 . PMID   24820101.
  14. ↑ Johnson L, Miller AN, McCleery RA, McClanahan R, Kath JA, Lueschow S, Porras-Alfaro A (June 2013). "Psychrophilic and psychrotolerant fungi on bats and the presence of Geomyces spp. on bat wings prior to the arrival of white nose syndrome". Applied and Environmental Microbiology. 79 (18): 5465–5471. Bibcode:2013ApEnM..79.5465J. doi:10.1128/AEM.01429-13. PMC   3754168 . PMID   23811520.
  15. ↑ Lorch, JM; Muller LK; Russell RF; O'Connor M; Lindner DL; Blehert DS (2013). "Distribution and environmental persistence of the causative agent of white-nose syndrome, Geomyces destructans, in bat hibernacula of the eastern United states". Applied and Environmental Microbiology. 79 (4): 1293–1301. Bibcode:2013ApEnM..79.1293L. doi:10.1128/AEM.02939-12. PMC   3568617 . PMID   23241985.
  16. 1 2 3 4 Raudabaugh, DB; Miller AN (2013). "Nutritional capability of and substrate suitability for Pseudogymnoascus destructans, the causal agent of bat white nose syndrome". PLOS ONE. 8 (10): e78300. Bibcode:2013PLoSO...878300R. doi: 10.1371/journal.pone.0078300 . PMC   3804546 . PMID   24205191.
  17. ↑ Reynolds, HT; Barton HA (2014). "Comparison of the white-nose syndrome agent Pseudogymnoascus destructans to cave dwelling relatives suggests reduced saprotrophic enzyme activity". PLOS ONE. 9 (1): e86437. Bibcode:2014PLoSO...986437R. doi: 10.1371/journal.pone.0086437 . PMC   3899275 . PMID   24466096.
  18. 1 2 Smyth, CS; Schlesinger SC; Overton BE; Butchkoshi C (2013). "The alternative host hypothesis and potential virulence genes in Geomyces destructans". Bat Research News. 54: 17–24.
  19. ↑ Casadevall, A; Steenbergen JN; Nosanchuk JD (2003). "'Ready made' virulence and 'dual use' virulence factors in pathogenic environmental fungi-the Cryptococcus neoformans paradigm". Current Opinion in Microbiology. 6 (4): 332–337. doi:10.1016/s1369-5274(03)00082-1. PMID   12941400.
  20. ↑ Chaturvedi, S; Rajkumar SS; Li X; Hurteau GJ; Shtutman M; Chaturvedi V (2011). "Anti fungal testing and high-throughput screening of compound library against Geomyces destructans, the etiologic agent of geomycosis (WNS) in bats". PLOS ONE. 6 (3): e17032. Bibcode:2011PLoSO...617032C. doi: 10.1371/journal.pone.0017032 . PMC   3047530 . PMID   21399675.
  21. ↑ Cornelison, CT; Gabriel KT; Barlament C; Crow SA (2014). "Inhibition of Pseudogymnoascus destructans growth from conidia and mycelial extension by bacterially produced volatile organic compounds". Mycopathologia. 177 (1–2): 1–10. doi:10.1007/s11046-013-9716-2. PMID   24190516. S2CID   15726620.
  22. ↑ "Bats Successfully Treated for White-Nose Syndrome Released Back into the Wild". The Nature Conservancy. 2015-05-20. Archived from the original on 2015-05-25. Retrieved 2015-05-26.
  23. ↑ Lindner, Daniel L.; Foster, Jeffrey T.; Drees, Kevin P.; Palmer, Jonathan M. (2018-01-02). "Extreme sensitivity to ultraviolet light in the fungal pathogen causing white-nose syndrome of bats". Nature Communications. 9 (1): 35. Bibcode:2018NatCo...9...35P. doi:10.1038/s41467-017-02441-z. ISSN   2041-1723. PMC   5750222 . PMID   29295979.
This page is based on this Wikipedia article
Text is available under the CC BY-SA 4.0 license; additional terms may apply.
Images, videos and audio are available under their respective licenses.