Ophidiomyces

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Ophidiomyces
Ophidiomyces ophiodiicola.jpg
Hyphae
Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Fungi
Division: Ascomycota
Class: Eurotiomycetes
Order: Onygenales
Family: Onygenaceae
Genus: Ophidiomyces
Sigler, Hambl. & Paré (2013)
Species:
O. ophidiicola
Binomial name
Ophidiomyces ophidiicola
(Guarro, Sutton, Wickes & Rajeev) Sigler, Hambleton & Paré (2013)
Synonyms

Chrysosporium ophiodiicolaGuarro, Sutton, Wickes & Rajeev (2009)

Contents

Ophidiomyces ophidiicola (formerly Ophidiomyces ophiodiicola) is the cause of ophidiomycosis also known as snake fungal disease or SFD in some species of snakes. [1] It is a keratinophilic fungus from the family Onygenaceae of the order Onygenales. O. ophidiicola is an emerging pathogen of captive and wild snakes in North America and Europe. [2] Clinical signs include skin swelling, crusts, and nodules of the skin. The mode of transmission is unknown, but is speculated to occur with direct contact between snakes or with the contaminated environment. Currently no treatment for O. ophidiicola is available. O. ophidiicola was identified by Sigler, Hambleton & Paré in 2013. O. ophidiicola is the only species in the genus Ophidiomyces. It was previously known as Chrysosporium ophiodiicola and is closely related to Chrysosporium anamorph Nannizziopsis vriesii (CANV). [2]

Taxonomy and naming

Ophidiomyces ophidiicola was first described as Chrysosporium ophiodiicola by Josef Guarro and colleagues in 2009 from infected snakes. Morphologically, the fungus resembled members of the genus Chrysosporium, and was thought to be closely related to the reptile pathogen that had been referred to as the Chrysosporium anamorph Nannizziopsis vriesii (CANV). The genus Ophidiomyces was erected to accommodate this fungus in 2013 when DNA sequencing confirmed it to be a member of the family Onygenaceae but genetically distinct from members of the genus Chrysosporium. [2]

Culture characteristics

Isolates from Nerodia clarkii O. ophiodiicola colony.jpg
Isolates from Nerodia clarkii

Cultures of O. ophidiicola are powdery with whitish mycelium that becomes light yellowish with age. The cultures emit a pungent, skunk like odour. Optimal growth for O. ophidiicola occurs at a temperature of 25 °C (77 °F). Most isolates fail to grow at 35 °C (95 °F). O. ophidiicola is able to grow over pH range of 5–11 with optimal growth observed at pH of 9. O. ophidiicola is able tolerate matric induced water stress below −5 MPa. The fungus exhibits strong urease activity and produces robust growth on ammonium sulfate, sulfite and thiosulfate. [3]

Morphology

No sexual state has been identified in the fungus O. ophidiicola. Vegetative hyphae of O. ophidiicola are narrow, branched and septate. Occasional racquet mycelia are observed. O. ophidiicola reproduces asexually by the production of conidia. The conidia are produces at the end of short stalks ranging from 2.5 to 7.5 μm in length and 1.5 to 2.5 μm in width. The conidia range from 3 to 12.5 μm long and 1.3 to 3.5 μm wide. [4] and are released by rhexolytic dehiscence in which the walls of cell compartments adjacent to conidia erode, freeing the conidia from attached hyphae. [4] The conidia are colourless to pale yellow and smooth-walled. [3]

Ecology

Ecology of O. ophidiicola is not well known but it is believed that O. ophidiicola persists as an environmental saprobe in soil as well as in living hosts. O. ophidiicola is able to utilize multiple carbon and nitrogen sources, and tolerates a range of pH, naturally occurring sulfur compounds and low matric potential. These are mostly characteristics required to live in soil. Good growth on dead fish, insect, mushroom tissue and demineralized shrimp exoskeleton is observed. O. ophidiicola physiological characteristics indicate that it is capable of growing in numerous ecosystems. [3]

Clinical symptoms

The mode of transmission is unknown, but is speculated to occur with direct contact between individuals or with the contaminated environment. Different symptoms can be seen in different species of snakes. In pit viper species facial swelling, cloudy eyes, improperly shed skin, roughened scales, dermal or subcutaneous granuloma and destruction of venom glands can be seen. [5] In massasaugas O. ophidiicola infection infect deep muscle tissue and bone. Also lesions can be observed on the skin of the entire body. [3] In colubrid species of snake fungal disease is reported to appear as pneumonia, ocular infection and subcutaneous nodules. [3] In garter snakes skin lesions are observed. The infection is reported to be systemic where it affects the lungs, liver and eyes. [3]

Pathogenicity in snakes

Lesions on Hoplocephalus bungaroides Lesions on Hoplocephalus bungaroides.jpg
Lesions on Hoplocephalus bungaroides

Infection begins in the outermost layer of the skin, the stratum corneum , and progresses into the epidermis. Once the infection reaches epidermis, the snake's immune response becomes activated and immune cells are recruited at the site of infection, causing the epidermis to become necrotic and thickened after a few days. [6]

Lesions begin at the edge of individual scales and progress to adjacent scales. As lesions progress scales became rough and hyperpigmented. Lesions progressively become larger and more severe until the snake sheds its skin. Fluid-filled vesicles form between the new and old skin resulting in improper shedding of the skin: fragments of the old skin remain on the snake. Histological studies show skin lesions with areas of necrosis and granulocytic inflammation in the superficial to midepidermis. Mild chronic lymphoplasmacytic to lymphohistiocytic inflammation in the liver, lungs, heart, stomach and colon can be observed as well. [1]

The emergence of ophidiomycosis due to O. ophidiicola has caused great concern for the conservation of snake populations in the Eastern United States. Confirmed cases of ophidiomycosis have been reported in 23 states in USA though the disease is believed to be more widespread than has been documented. [7] Multiple species of snakes that are affected including the northern water snake ( Nerodia sipedon ), eastern racer (Coluber constrictor ), rat snake (Pantherophis obsoletus species complex), timber rattlesnake ( Crotalus horridus ), massasauga ( Sistrurus catenatus ), pygmy rattlesnake ( Sistrurus miliarius ), and milk snake ( Lampropeltis triangulum ). [8] It is reported that population of rattlesnake in New Hampshire reduced to 19 from 40 due to ophidiomycosis caused by O. ophidiicola. [3]

Ophidiomyces ophidiicola has been successfully treated in captive settings using the antifungal drug terbinafine, which has shown to be effective via both nebulization or subcutaneous implant. [9] Such a strategy is impractical for many snake populations because it can be difficult to locate the majority of individuals within the population, is resource intensive, and fails to prevent reinfection. [6] The National Wildlife Health Center along with other organizations and researchers are working together to develop management strategies to mitigate disease impact. [8]

Related Research Articles

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<i>Chlamydosauromyces</i> Genus of fungi

Chlamydosauromyces punctatus is the sole species in the monotypic genus of fungi, Chlamydosauromyces in the family, Onygenaceae. It was found in the skin shed from frilled lizard. This fungus is mesophilic and digests hair. It reproduces both sexually and asexually. The fungus has so far not been reported to be pathogenic.

<i>Uncinocarpus</i> Genus of fungi

Uncinocarpus is a genus of fungi within the Onygenaceae family. The name is derived from the Latin word uncinus, meaning "hook" and the Greek word karpos (καρπός), meaning "fruit". It was distinguished from the genus Gymnoascus based on keratinolytic capacity, ascospore morphology and the development of hooked, occasionally spiraling appendages. Alternatively, Uncinocarpus species may possess helically coiled or smooth, wavy appendages, or lack appendages altogether, an example of such species being U. orissi.

<i>Aphanoascus fulvescens</i> Species of fungus

Aphanoascus fulvescens is a mould fungus that behaves as a keratinophilic saprotroph and belongs to the Ascomycota. It is readily isolated from soil and dung containing keratin-rich tissues that have been separated from their animal hosts. This organism, distributed worldwide, is most commonly found in areas of temperate climate, in keeping with its optimal growth temperature of 28 °C (82 °F). While A. fulvescens is recognized as a geophilic fungal species, it is also a facultative opportunistic pathogen. Although it is not a dermatophyte, A. fulvescens has occasionally been shown to cause onychomycosis infections in humans. Its recognition in the laboratory is clinically important for correct diagnosis and treatment of human dermal infections.

Nannizziopsis vreisii is a keratinophilic microfungus in the Family Onygenaceae of the order Onygenales. Also included in this family are dematophytes and saprophytic species. While the ecology of N. vriessi is not well known, there has been several studies which identifies the Chrysosporium anamorph of N. vriesii as a causal agent of skin lesions in reptiles across several regions. This species is usually identified under a microscope by its white ascomata, and hyaline and globose ascospores. Like many other fungi, N. vreisii has a sexual and asexual state, the asexual states are classified as the genus Chryososporium, Malbranchea or Sporendonema.

<i>Microascus brevicaulis</i> Species of fungus

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<i>Chrysosporium keratinophilum</i> Species of fungus

Chrysosporium keratinophilum is a mold that is closely related to the dermatophytic fungi and is mainly found in soil and the coats of wild animals to break down keratin. Chrysosporium keratinophilum is one of the more commonly occurring species of the genus Chrysosporium in nature. It is easily detected due to its characteristic "light-bulb" shape and flat base. Chrysosporium keratinophilum is most commonly found in keratin-rich, dead materials such as feathers, skin scales, hair, and hooves. Although not identified as pathogenic, it is a regular contaminant of cutaneous specimens which leads to the common misinterpretation that this fungus is pathogenic.

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Chrysosporium longisporum is a keratinophilic microfungus in the family Onygenaceae that causes skin infections in reptiles, producing hyaline, thin-walled, small, sessile conidia and colonies with a strong skunk-like odour.

Nannizziopsis pluriseptata is a keratinophilic microfungus in the family Onygenaceae that causes skin infections in reptiles, producing hyaline, thin-walled, small, sessile conidia and colonies with a strong skunk-like odour. It is distinguished by its production of 1- to 5-celled sessile conidia.

Nannizziopsis arthrosporioides is a keratinophilic microfungus in the family Onygenaceae that causes skin infections in reptiles, producing hyaline, thin-walled, small, sessile conidia and colonies with a strong skunk-like odour. It is distinguished by the production of long arthroconidia.

Nannizziopsis draconii is a keratinophilic microfungus in the family Onygenaceae that causes skin infections in reptiles, producing hyaline, thin-walled, small, sessile conidia and colonies with a strong skunk-like odour.

Nannizziopsis chlamydospora is a keratinophilic microfungus in the family Onygenaceae that causes skin infections in reptiles, producing hyaline, thin-walled, small, sessile conidia and colonies with a strong skunk-like odour. This species is distinguished by producing chlamydospores and its ability to grow at 5 °C.

Nannizziopsis guarroi was first documented in 2006 on a variety of lizards then described in Spain in 2010 and was classified as Chrysosporium guarroi, a member of the anamorphic genus Chrysosporium in the family Onygenaceae. Etymologically, the species epithet "guarroi" honours Professor Josep Guarro in recognition of his extensive mycological work including on the genus Chrysosporium. Skin samples taken from pet green iguanas suffering from dermatomycosis were sent to a laboratory for analysis. Five species were isolated and morphologic studies identified the fungus causing the mycoses as a member of the anamorphic species of Chrysosporium. Further investigation of these species using a combination of morphological, cultural and molecular studies showed that they were not identical to any previously described species within the genus Chrysosporium so they were classified as a new species Chrysosporium guarroisp. nov. The delineation of species in the genus Chrysosporium and their assignment to higher taxonomic levels can be challenging due to the marked morphological simplicity of these fungi. Increased scrutiny of strains of these fungi using molecular genetic tools has revealed numerous hidden species and unexpected relationships.

<i>Epidermophyton floccosum</i> Species of fungus

Epidermophyton floccosum is a filamentous fungus that causes skin and nail infections in humans. This anthropophilic dermatophyte can lead to diseases such as tinea pedis, tinea cruris, tinea corporis and onychomycosis. Diagnostic approaches of the fungal infection include physical examination, culture testing, and molecular detection. Topical antifungal treatment, such as the use of terbinafine, itraconazole, voriconazole, and ketoconazole, is often effective.

<i>Phialophora verrucosa</i> Species of fungus

Phialophora verrucosa is a pathogenic, dematiaceous fungus that is a common cause of chromoblastomycosis. It has also been reported to cause subcutaneous phaeohyphomycosis and mycetoma in very rare cases. In the natural environment, it can be found in rotting wood, soil, wasp nests, and plant debris. P. verrucosa is sometimes referred to as Phialophora americana, a closely related environmental species which, along with P. verrucosa, is also categorized in the P. carrionii clade.

<i>Metarhizium granulomatis</i> Species of fungus

Metarhizium granulomatis is a fungus in the family Clavicipitaceae associated with systemic mycosis in veiled chameleons. The genus Metarhizium is known to infect arthropods, and collectively are referred to green-spored asexual pathogenic fungi. This species grows near the roots of plants and has been reported as an agent of disease in captive veiled chameleons. The etymology of the species epithet, "granulomatis" refers to the ability of the fungus to cause granulomatous disease in susceptible reptiles.

<i>Ctenomyces serratus</i> Species of fungus

Ctenomyces serratus is a keratinophilic fungal soil saprotroph classified by the German mycologist, Michael Emil Eduard Eidam in 1880, who found it growing on an old decayed feather. Many accounts have shown that it has a global distribution, having been isolated in select soils as well as on feathers and other substrates with high keratin content. It has also been found in indoor dust of hospitals and houses in Kanpur, Northern India and as a common keratinophilic soil fungus in urban Berlin. This species has been associated with nail infections in humans as well as skin lesions and slower hair growth in guinea pigs.

References

  1. 1 2
    Lopes, Patricia C.; French, Susannah S.; Woodhams, Douglas C.; Binning, Sandra A. (2021). "Sickness behaviors across vertebrate taxa: proximate and ultimate mechanisms". Journal of Experimental Biology . 224 (9). The Company of Biologists. doi: 10.1242/jeb.225847 . ISSN   0022-0949. S2CID   233719623.
    This review is cited by Di Nicola et al., 2022, Aguilar et al., 2023 and others — Davy, Christina M.; Shirose, Leonard; Campbell, Doug; Dillon, Rachel; McKenzie, Christina; Nemeth, Nicole; Braithwaite, Tony; Cai, Hugh; Degazio, Tarra; Dobbie, Tammy; Egan, Sean; Fotherby, Heather; Litzgus, Jacqueline D.; Manorome, Pilar; Marks, Steve; Paterson, James E.; Sigler, Lynne; Slavic, Durda; Slavik, Emily; Urquhart, John; Jardine, Claire (2021). "Revisiting Ophidiomycosis (Snake Fungal Disease) After a Decade of Targeted Research". Frontiers in Veterinary Science . 8. Frontiers Media SA. doi: 10.3389/fvets.2021.665805 . ISSN   2297-1769. PMC   8200636 . PMID   34136555. S2CID   235249427.
    These reviews cite this research.
    Lorch, Jeffrey M.; Lankton, Julia; Werner, Katrien; Falendysz, Elizabeth A.; McCurley, Kevin; Blehert, David S. (2015). "Experimental Infection of Snakes with Ophidiomyces ophiodiicola Causes Pathological Changes That Typify Snake Fungal Disease". mBio . 6 (6). American Society for Microbiology (ASM). doi: 10.1128/mbio.01534-15 . ISSN   2161-2129. PMC   4659463 . S2CID   11404838.
  2. 1 2 3 Rajeev, S.; Sutton, D. A.; Wickes, B. L.; Miller, D. L.; Giri, D.; Van Meter, M.; Thompson, E. H.; Rinaldi, M. G.; Romanelli, A. M.; Cano, J. F.; Guarro, J. (24 December 2008). "Isolation and Characterization of a New Fungal Species, Chrysosporium ophiodiicola, from a Mycotic Granuloma of a Black Rat Snake (Elaphe obsoleta obsoleta)". Journal of Clinical Microbiology. 47 (4): 1264–1268. doi:10.1128/JCM.01751-08. PMC   2668353 . PMID   19109465.
  3. 1 2 3 4 5 6 7 Allender, Matthew C.; Raudabaugh, Daniel B.; Gleason, Frank H.; Miller, Andrew N. (October 2015). "The natural history, ecology, and epidemiology of Ophidiomyces ophiodiicola and its potential impact on free-ranging snake populations". Fungal Ecology. 17: 187–196. doi:10.1016/j.funeco.2015.05.003.
  4. 1 2 Sigler, L.; Hambleton, S.; Pare, J. A. (7 August 2013). "Molecular Characterization of Reptile Pathogens Currently Known as Members of the Chrysosporium Anamorph of Nannizziopsis vriesii Complex and Relationship with Some Human-Associated Isolates". Journal of Clinical Microbiology. 51 (10): 3338–3357. doi:10.1128/JCM.01465-13. PMC   3811641 . PMID   23926168.
  5. ↑ Allender, M. C.; Bunick, D.; Dzhaman, E.; Burrus, L.; Maddox, C. (16 March 2015). "Development and use of a real-time polymerase chain reaction assay for the detection of Ophidiomyces ophiodiicola in snakes". Journal of Veterinary Diagnostic Investigation. 27 (2): 217–220. doi: 10.1177/1040638715573983 .
  6. 1 2 Lorch, Jeffrey M.; Knowles, Susan; Lankton, Julia S.; Michell, Kathy; Edwards, Jaime L.; Kapfer, Joshua M.; Staffen, Richard A.; Wild, Erik R.; Schmidt, Katie Z.; Ballmann, Anne E.; Blodgett, Doug; Farrell, Terence M.; Glorioso, Brad M.; Last, Lisa A.; Price, Steven J.; Schuler, Krysten L.; Smith, Christopher E.; Wellehan, James F. X.; Blehert, David S. (24 October 2016). "Snake fungal disease: an emerging threat to wild snakes". Philosophical Transactions of the Royal Society B: Biological Sciences. 371 (1709): 20150457. doi:10.1098/rstb.2015.0457. PMC   5095536 . PMID   28080983.
  7. ↑ Thompson, Noelle E.; Lankau, Emily W.; Rogall, Gail Moede (2018). "Snake Fungal Disease in North America: U.S. Geological Survey Updates" (PDF). USGS Publications. U.S. Department of the Interior & U.S. Geological Survey. Retrieved 23 April 2020.
  8. 1 2 "Snake Fungal Disease". National Wildlife Health Center. U.S. Geological Survey. 19 May 2016. Archived from the original on 24 December 2017.
  9. ↑ Kane LP, Allender MC, Archer G, Leister K, Rzadkowska M, Boers K, Souza M, Cox S. Pharmacokinetics of nebulized and subcutaneously implanted terbinafine in cottonmouths (Agkistrodon piscivorus). J Vet Pharmacol Ther. 2017 Oct;40(5):575–579. doi: 10.1111/jvp.12406. Epub 2017 Apr 6. PMID 28382637.
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