Pseudogymnoascus Destructans
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''Pseudogymnoascus destructans'' (formerly known as ''Geomyces destructans'') is a
psychrophilic Psychrophiles or cryophiles (adj. ''psychrophilic'' or ''cryophilic'') are extremophilic organisms that are capable of growth and reproduction in low temperatures, ranging from to . They have an optimal growth temperature at . They are found in ...
(cold-loving)
fungus A fungus ( : fungi or funguses) is any member of the group of eukaryotic organisms that includes microorganisms such as yeasts and molds, as well as the more familiar mushrooms. These organisms are classified as a kingdom, separately from th ...
that causes
white-nose syndrome 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 distincti ...
(WNS), a fatal disease that has devastated
bat Bats are mammals of the order Chiroptera.''cheir'', "hand" and πτερόν''pteron'', "wing". 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 ...
populations in parts of the
United States The United States of America (U.S.A. or USA), commonly known as the United States (U.S. or US) or America, is a country primarily located in North America. It consists of 50 states, a federal district, five major unincorporated territorie ...
and
Canada Canada is a country in North America. Its ten provinces and three territories extend from the Atlantic Ocean to the Pacific Ocean and northward into the Arctic Ocean, covering over , making it the world's second-largest country by tot ...
. Unlike species of ''
Geomyces ''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, ...
'', ''P. destructans'' forms asymmetrically curved
conidia A conidium ( ; ), sometimes termed an asexual chlamydospore or chlamydoconidium (), is an asexual, non-motile spore of a fungus. The word ''conidium'' comes from the Ancient Greek word for dust, ('). They are also called mitospores due to the ...
. ''Pseudogymnoascus destructans'' grows very slowly on artificial media and cannot grow at temperatures above 20 °C. It can grow around 4 °C to 20 °C, which encompasses the temperatures found in winter bat hibernacula. Phylogenic evaluation has revealed this organism should be reclassified under the family ''Pseudeurotiaceae'', changing its name to ''Pseudogymnoascus destructans''.


History

In 2008, Blehert ''et al.'' described the fungus associated with white-nose syndrome as a member of the genus ''Geomyces''. In 2009, Gargas ''et al.'' were the first to describe the fungus as a unique species; the specific name they chose, "'", means "destroying". 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 The United States Geological Survey (USGS), formerly simply known as the Geological Survey, is a scientific agency of the United States government. The scientists of the USGS study the landscape of the United States, its natural resources, ...
. It was previously unknown whether this fungus was the primary cause of WNS or was an
opportunistic pathogen An opportunistic infection is an infection caused by pathogens (bacteria, fungi, parasites or viruses) that take advantage of an opportunity not normally available. These opportunities can stem from a variety of sources, such as a weakened immune ...
associated with the disease, though strong evidence suggested that the fungus was the
etiologic agent Cause, also known as etiology () and aetiology, is the Causality, reason or origination of something. The word ''etiology'' is derived from the Ancient Greek, Greek , ''aitiologia'', "giving a reason for" (, ''aitia'', "cause"; and , ''wikt:-logi ...
. 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 ''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, ...
'' changing its
Latin binomial In Taxonomy (biology), taxonomy, binomial nomenclature ("two-term naming system"), also called nomenclature ("two-name naming system") or binary nomenclature, is a formal system of naming species of living things by giving each a name compos ...
to ''Pseudogymnoascus destructans''.


Distribution

''Pseudogymnoascus destructans'' is believed to originate from Europe. The current ''P. destructans'' European distribution includes
Austria Austria, , bar, Östareich officially the Republic of Austria, is a country in the southern part of Central Europe, lying in the Eastern Alps. It is a federation of nine states, one of which is the capital, Vienna, the most populous ...
,
Belgium Belgium, ; french: Belgique ; german: Belgien officially the Kingdom of Belgium, is a country in Northwestern Europe. The country is bordered by the Netherlands to the north, Germany to the east, Luxembourg to the southeast, France to th ...
,
Czech Republic The Czech Republic, or simply Czechia, is a landlocked country in Central Europe. Historically known as Bohemia, it is bordered by Austria to the south, Germany to the west, Poland to the northeast, and Slovakia to the southeast. The ...
,
Denmark ) , song = ( en, "King Christian stood by the lofty mast") , song_type = National and royal anthem , image_map = EU-Denmark.svg , map_caption = , subdivision_type = Sovereign state , subdivision_name = Danish Realm, Kingdom of Denmark ...
,
Estonia Estonia, formally the Republic of Estonia, is a country by the Baltic Sea in Northern Europe. It is bordered to the north by the Gulf of Finland across from Finland, to the west by the sea across from Sweden, to the south by Latvia, a ...
,
France France (), officially the French Republic ( ), is a country primarily located in Western Europe. It also comprises of Overseas France, overseas regions and territories in the Americas and the Atlantic Ocean, Atlantic, Pacific Ocean, Pac ...
,
Germany Germany,, officially the Federal Republic of Germany, is a country in Central Europe. It is the second most populous country in Europe after Russia, and the most populous member state of the European Union. Germany is situated betwe ...
,
Hungary Hungary ( hu, Magyarország ) is a landlocked country in Central Europe. Spanning of the Carpathian Basin, it is bordered by Slovakia to the north, Ukraine to the northeast, Romania to the east and southeast, Serbia to the south, Croatia a ...
, the
Netherlands ) , anthem = ( en, "William of Nassau") , image_map = , map_caption = , subdivision_type = Sovereign state , subdivision_name = Kingdom of the Netherlands , established_title = Before independence , established_date = Spanish Netherl ...
,
Poland Poland, officially the Republic of Poland, is a country in Central Europe. It is divided into 16 administrative provinces called voivodeships, covering an area of . Poland has a population of over 38 million and is the fifth-most populous ...
,
Romania Romania ( ; ro, România ) is a country located at the crossroads of Central Europe, Central, Eastern Europe, Eastern, and Southeast Europe, Southeastern Europe. It borders Bulgaria to the south, Ukraine to the north, Hungary to the west, S ...
,
Slovakia Slovakia (; sk, Slovensko ), officially the Slovak Republic ( sk, Slovenská republika, links=no ), is a landlocked country in Central Europe. It is bordered by Poland to the north, Ukraine to the east, Hungary to the south, Austria to the s ...
,
Switzerland ). Swiss law does not designate a ''capital'' as such, but the federal parliament and government are installed in Bern, while other federal institutions, such as the federal courts, are in other cities (Bellinzona, Lausanne, Luzern, Neuchâtel ...
,
Turkey Turkey ( tr, Türkiye ), officially the Republic of Türkiye ( tr, Türkiye Cumhuriyeti, links=no ), is a list of transcontinental countries, transcontinental country located mainly on the Anatolia, Anatolian Peninsula in Western Asia, with ...
,
Ukraine Ukraine ( uk, Україна, Ukraïna, ) is a country in Eastern Europe. It is the second-largest European country after Russia, which it borders to the east and northeast. Ukraine covers approximately . Prior to the ongoing Russian inv ...
and the
United Kingdom The United Kingdom of Great Britain and Northern Ireland, commonly known as the United Kingdom (UK) or Britain, is a country in Europe, off the north-western coast of the continental mainland. It comprises England, Scotland, Wales and North ...
. The North American geographic distribution of ''P. destructans'' continues to increase each year since its initial introduction to New York State in 2006. It
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, of which it has caused diagnostic symptoms of
white-nose syndrome 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 distincti ...
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''). ''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.


Biology

''P. destructans'' is a psychrophilic fungus, able to grow below and with an upper limit near . 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 Arthroconidia are a type of fungal spore typically produced by segmentation of pre-existing fungal hyphae. Background These spores are asexual and are generally not as durable and environmentally persistent as, for instance, bacterial endospores ...
can be present and undergo rhexolytic separation. Research has shown that ''P. destructans'' grows optimally between , with an upper growth limit of about . 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. ''P. destructans'' grows as an opportunistic pathogen on bats, causing white-nose syndrome, but it can also persist in the cave environment, as a saprotroph. ''P. destructans'' can grow and sporulate ( reproduce asexually via
conidiation Conidiation is a biological process in which filamentous fungi reproduce asexually from spores. Rhythmic conidiation is the most obvious output of fungal circadian rhythms. ''Neurospora'' species are most often used to study this rhythmic conidiat ...
) on
keratin Keratin () is one of a family of structural fibrous proteins also known as ''scleroproteins''. Alpha-keratin (α-keratin) is a type of keratin found in vertebrates. It is the key structural material making up scales, hair, nails, feathers, ho ...
aceous,
chitin Chitin ( C8 H13 O5 N)n ( ) is a long-chain polymer of ''N''-acetylglucosamine, an amide derivative of glucose. Chitin is probably the second most abundant polysaccharide in nature (behind only cellulose); an estimated 1 billion tons of chit ...
aceous,
cellulosic Cellulose is an organic compound with the formula , a polysaccharide consisting of a linear chain of several hundred to many thousands of β(1→4) linked D-glucose units. Cellulose is an important structural component of the primary cell wa ...
, and lipid/protein rich substrates including dead fish, mushroom fruit bodies and dead insects. ''P. destructans'' has been shown to utilize many nitrogen sources: nitrate, nitrite, ammonium, urea, and uric acid. Although ''P. destructans'' can penetrate senescing moss cells, cellulosic debris may not be a long term substrate for colonization. ''P. destructans'' can tolerate elevated levels of environmental inhibitory sulfur compounds (
cysteine Cysteine (symbol Cys or C; ) is a semiessential proteinogenic amino acid with the formula . The thiol side chain in cysteine often participates in enzymatic reactions as a nucleophile. When present as a deprotonated catalytic residue, sometime ...
,
sulfite Sulfites or sulphites are compounds that contain the sulfite ion (or the sulfate(IV) ion, from its correct systematic name), . The sulfite ion is the conjugate base of bisulfite. Although its acid ( sulfurous acid) is elusive, its salts are wide ...
, and
sulfide Sulfide (British English also sulphide) is an inorganic anion of sulfur with the chemical formula S2− or a compound containing one or more S2− ions. Solutions of sulfide salts are corrosive. ''Sulfide'' also refers to chemical compounds lar ...
), 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

Under laboratory conditions, ''P. destructans'' has been shown to produce numerous enzymes including
β-glucosidase β-Glucosidase (EC 3.2.1.21; systematic name β-D-glucoside glucohydrolase) is an enzyme that catalyses the following reaction: : Hydrolysis of terminal, non-reducing β-D-glucosyl residues with release of β-D-glucose Structure β-Glucosidase ...
,
esterase An esterase is a hydrolase enzyme that splits esters into an acid and an alcohol in a chemical reaction with water called hydrolysis. A wide range of different esterases exist that differ in their substrate specificity, their protein structure, ...
/esterase lipase/
lipase Lipase ( ) is a family of enzymes that catalyzes the hydrolysis of fats. Some lipases display broad substrate scope including esters of cholesterol, phospholipids, and of lipid-soluble vitamins and sphingomyelinases; however, these are usually tr ...
, leucine and valine arylamidase, N-acetyl-β-glucosaminidase, naphthol-AS-B1-phosphohydrolase, both acid and alkaline
phosphatase In biochemistry, a phosphatase is an enzyme that uses water to cleave a phosphoric acid Ester, monoester into a phosphate ion and an Alcohol (chemistry), alcohol. Because a phosphatase enzyme catalysis, catalyzes the hydrolysis of its Substrate ...
s, various
proteinase A protease (also called a peptidase, proteinase, or proteolytic enzyme) is an enzyme that catalysis, catalyzes (increases reaction rate or "speeds up") proteolysis, breaking down proteins into smaller polypeptides or single amino acids, and spurri ...
, and
urease Ureases (), functionally, belong to the superfamily of amidohydrolases and phosphotriesterases. Ureases are found in numerous bacteria, fungi, algae, plants, and some invertebrates, as well as in soils, as a soil enzyme. They are nickel-containin ...
, while testing negative for cystine arylamidase, α-chymotrypsin,
alpha Alpha (uppercase , lowercase ; grc, ἄλφα, ''álpha'', or ell, άλφα, álfa) is the first letter of the Greek alphabet. In the system of Greek numerals, it has a value of one. Alpha is derived from the Phoenician letter aleph , whic ...
/
beta Beta (, ; uppercase , lowercase , or cursive ; grc, βῆτα, bē̂ta or ell, βήτα, víta) is the second letter of the Greek alphabet. In the system of Greek numerals, it has a value of 2. In Modern Greek, it represents the voiced labiod ...
-galactosidase,
β-glucuronidase Beta-glucuronidases are members of the glycosidase family of enzymes that catalyze breakdown of complex carbohydrates. Human β-glucuronidase is a type of glucuronidase (a member of glycosidase Family 2) that catalyzes hydrolysis of β-D-glucur ...
, α-fucosidase, α-mannosidase, and
trypsin Trypsin is an enzyme in the first section of the small intestine that starts the digestion of protein molecules by cutting these long chains of amino acids into smaller pieces. It is a serine protease from the PA clan superfamily, found in the dig ...
. Important dual
virulence factors Virulence factors (preferably known as pathogenicity factors or effectors in plant science) are cellular structures, molecules and regulatory systems that enable microbial pathogens (bacteria, viruses, fungi, and protozoa) to achieve the followin ...
found in ''P. destructans'' and many other pathogenic fungi include urease, proteinase (aspartyll) and
superoxide dismutase Superoxide dismutase (SOD, ) is an enzyme that alternately catalyzes the dismutation (or partitioning) of the superoxide () radical into ordinary molecular oxygen (O2) and hydrogen peroxide (). Superoxide is produced as a by-product of oxygen me ...
.


Control agents

In 2011, several compounds (antifungals, fungicides, and biocides) where shown to effectively inhibit the growth of ''P. destructans'' including
benzalkonium chloride Benzalkonium chloride (BZK, BKC, BAK, BAC), also known as alkyldimethylbenzylammonium chloride (ADBAC) and by the trade name Zephiran, is a type of cationic surfactant. It is an organic salt classified as a quaternary ammonium compound. ADBACs hav ...
, chloroacetoxyquinoline, chloroxine, ciclopirox olamine,
econazole Econazole is an antifungal medication of the imidazole class. It was patented in 1968, and approved for medical use in 1974. Medical uses Econazole is used as a cream to treat skin infections such as athlete's foot, tinea, pityriasis versicol ...
,
phenylmercuric acetate Phenylmercuric acetate is an organomercury compound used as a preservative, disinfectant, and antitranspirant. Properties Phenylmercuric acetate forms colorless, lustrous crystals, and is soluble in ethanol, benzene, acetic acid, and sparingly ...
,
pyrithione zinc Zinc pyrithione (or pyrithione zinc) is a coordination complex of zinc. It has fungistatic (inhibiting the division of fungal cells) and bacteriostatic (inhibiting bacterial cell division) properties and is used in the treatment of seborrhoeic d ...
and sulconazole. The same study showed that ''P. destructans'' was sensitive to
Amphotericin B Amphotericin B is an antifungal medication used for serious mycosis, fungal infections and leishmaniasis. The fungal infections it is used to treat include mucormycosis, aspergillosis, blastomycosis, candida infections, candidiasis, coccidioidomy ...
,
itraconazole Itraconazole, sometimes abbreviated ITZ, is an antifungal medication used to treat a number of fungal infections. This includes aspergillosis, blastomycosis, coccidioidomycosis, histoplasmosis, and paracoccidioidomycosis. It may be given by mouth ...
,
ketoconazole Ketoconazole, sold under the brand name Nizoral among others, is an antiandrogen and antifungal medication used to treat a number of fungal infections. Applied to the skin it is used for fungal skin infections such as tinea, cutaneous candid ...
,
posaconazole Posaconazole, sold under the brand name Noxafil among others, is a triazole antifungal medication. It was approved for medical use in the United States in September 2006, and is available as a generic medication. Medical uses Posaconazole is u ...
and
voriconazole Voriconazole, sold under the brand name Vfend among others, is an antifungal medication used to treat a number of fungal infections. This includes aspergillosis, candidiasis, coccidioidomycosis, histoplasmosis, penicilliosis, and infections by '' ...
, while the fungus had some resistance to
anidulafungin Anidulafungin (International nonproprietary name, INN) (trade names Eraxis, Ecalta) is a Semisynthesis, semisynthetic echinocandin used as an antifungal medication, antifungal drug. It was previously known as LY303366. It may also have applicatio ...
,
caspofungin Caspofungin (INN) (brand name Cancidas) is a lipopeptide antifungal drug from Merck & Co., Inc. discovered by James Balkovec, Regina Black and Frances A. Bouffard. It is a member of a new class of antifungals termed the echinocandins. It wor ...
,
flucytosine Flucytosine, also known as 5-fluorocytosine (5-FC), is an antifungal medication. It is specifically used, together with amphotericin B, for serious ''Candida'' infections and cryptococcosis. It may be used by itself or with other antifungals for ...
and
micafungin Micafungin, sold under the brand name Mycamine, is an echinochandin antifungal medication used to treat and prevent invasive fungal infections including candidemia, abscesses, and esophageal candidiasis. It inhibits the production of beta-1,3- ...
. A recent study (2014) identified several
volatile organic compounds Volatile organic compounds (VOCs) are organic compounds that have a high vapour pressure at room temperature Colloquially, "room temperature" is a range of air temperatures that most people prefer for indoor settings. It feels comfortable to a ...
(
benzaldehyde Benzaldehyde (C6H5CHO) is an organic compound consisting of a benzene ring with a formyl substituent. It is the simplest aromatic aldehyde and one of the most industrially useful. It is a colorless liquid with a characteristic almond-like odor. ...
,
benzothiazole Benzothiazole is an aromatic heterocyclic compound with the chemical formula . It is colorless, slightly viscous liquid. Although the parent compound, benzothiazole is not widely used, many of its derivatives are found in commercial products or ...
,
decanal Decanal is an organic compound classified as an aldehyde with the chemical formula C10H20O. Occurrence Decanal occurs naturally in citrus, along with octanal, citral, and sinensal, in buckwheat Buckwheat (''Fagopyrum esculentum''), or com ...
,
nonanal Nonanal, also called nonanaldehyde, pelargonaldehyde or Aldehyde C-9, is an aldehyde. A colourless, oily liquid, nonanal is a component of perfumes. Although it occurs in several natural oils, it is produced commercially by hydroformylation of 1- ...
, 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. A 2015 study showed that ''
Rhodococcus rhodochrous ''Rhodococcus rhodochrous'' is a bacterium used as a soil inoculant in agriculture and horticulture. It is gram positive, in the shape of rods/ cocci, oxidase negative, and catalase positive. It is industrially produced to catalyse acryloni ...
'' could inhibit the growth of ''P. destructans''. 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 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. 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.


References


External links

* * {{Taxonbar, from=Q5535539 Fungi described in 2009 Fungi of Europe Dothideomycetes enigmatic taxa Parasitic fungi