Ophidiomyces Ophiodiicola
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''Ophidiomyces ophiodiicola'' is the cause of ophidiomycosis also known as snake fungal disease or SFD in some species of snakes. It is a keratinophilic fungus from the family
Onygenaceae The Onygenaceae are a family (biology), family of fungi in the Ascomycota, class Eurotiomycetes. Genera These are the genera that are in the Onygenaceae, according to a 2021 review of fungal classification. Following the genus name is the Author ...
of the order
Onygenales The Onygenales are an order of fungi in the class Eurotiomycetes and division Ascomycota. The order's last common ancestor is estimated to have lived 150 million years ago. Onygenales can consume and break down keratin, the main component of th ...
. ''O. ophiodiicola'' is an emerging pathogen of captive and wild snakes in North America and Europe. 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. ophiodiicola'' is available. ''O. ophiodiicola'' was identified by Sigler, Hambleton & Paré in 2013. ''O. ophiodiicola'' is the only species in the genus ''Ophidiomyces''. It was previously known as ''Chrysosporium ophiodiicola'' and is closely related to ''
Chrysosporium ''Chrysosporium'' is a genus of hyaline hyphomycetes fungi in the family Onygenaceae. ''Chrysosporium'' colonies are moderately fast-growing, flat, white to tan to beige in color; they often have a powdery or granular surface texture. Hyaline, ...
'' anamorph '' Nannizziopsis vriesii'' (CANV).


Taxonomy and naming

''Ophidiomyces ophiodiicola'' 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 The Onygenaceae are a family (biology), family of fungi in the Ascomycota, class Eurotiomycetes. Genera These are the genera that are in the Onygenaceae, according to a 2021 review of fungal classification. Following the genus name is the Author ...
but genetically distinct from members of the genus ''Chrysosporium''.


Culture characteristics

Cultures of ''O. ophiodiicola'' are powdery with whitish mycelium that becomes light yellowish with age. The cultures emit a pungent, skunk like odour. Optimal growth for ''O. ophiodiicola'' occurs at a temperature of . Most isolates fail to grow at . ''O. ophiodiicola'' is able to grow over pH range of 5–11 with optimal growth observed at pH of 9. ''O. ophiodiicola'' 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.


Morphology

No sexual state has been identified in the fungus ''O. ophiodiicola''. Vegetative hyphae of ''O. ophiodiicola'' are narrow, branched and septate. Occasional racquet
mycelia Mycelium (plural mycelia) is a root-like structure of a fungus consisting of a mass of branching, thread-like hyphae. Fungal colonies composed of mycelium are found in and on soil and many other substrates. A typical single spore germinates in ...
are observed. ''O. ophiodiicola'' 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. and are released by rhexolytic dehiscence in which the walls of cell compartments adjacent to conidia erode, freeing the conidia from attached hyphae. The conidia are colourless to pale yellow and smooth-walled.


Ecology

Ecology of ''O. ophiodiicola'' is not well known but it is believed that ''O. ophiodiicola'' persists as an environmental saprobe in soil as well as in living hosts. ''O. ophiodiicola'' 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. ophiodiicola'' physiological characteristics indicate that it is capable of growing in numerous ecosystems.


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 The Crotalinae, commonly known as pit vipers,Mehrtens JM (1987). ''Living Snakes of the World in Color''. New York: Sterling Publishers. 480 pp. . crotaline snakes (from grc, κρόταλον ''krotalon'' castanet), or pit adders, are a subfa ...
species facial swelling, cloudy eyes, improperly shed skin, roughened scales, dermal or subcutaneous granuloma and destruction of venom glands can be seen. In massasaugas ''O. ophiodiicola'' infection infect deep muscle tissue and bone. Also lesions can be observed on the skin of the entire body. In
colubrid Colubridae (, commonly known as colubrids , from la, coluber, 'snake') is a family of snakes. With 249 genera, it is the largest snake family. The earliest species of the family date back to the Oligocene epoch. Colubrid snakes are found on ever ...
species of snake fungal disease is reported to appear as pneumonia, ocular infection and subcutaneous nodules. In
garter snake Garter snake is a common name for generally harmless, small to medium-sized snakes belonging to the genus ''Thamnophis'' in the family Colubridae. Native to North and Central America, species in the genus ''Thamnophis'' can be found from the sub ...
s skin lesions are observed. The infection is reported to be systemic where it affects the lungs, liver and eyes.


Pathogenicity in snakes

Infection begins in the outermost layer of the skin, the ''
stratum corneum The stratum corneum (Latin for 'horny layer') is the outermost layer of the epidermis. The human stratum corneum comprises several levels of flattened corneocytes that are divided into two layers: the ''stratum disjunctum'' and ''stratum compact ...
'', 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. 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. The emergence of ophidiomycosis due to ''O. ophiodiicola'' 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. Multiple species of snakes that are affected including the northern water snake (''
Nerodia sipedon The common watersnake (''Nerodia sipedon'') is a species of large, nonvenomous, common snake in the family Colubridae. The species is native to North America. It is frequently mistaken for the venomous cottonmouth (''Agkistrodon piscivorus''). ...
''), eastern racer ''(
Coluber constrictor The eastern racer (''Coluber constrictor'') is a species of nonvenomous snake in the family Colubridae. The species is endemic to North America and Central America. Eleven subspecies, including the nominotypical subspecies, are recognized, whic ...
''), rat snake (''Pantherophis obsoletus'' species complex), timber rattlesnake ('' Crotalus horridus''), massasauga (''
Sistrurus catenatus The massasauga (''Sistrurus catenatus'') is a rattlesnake species found in midwestern North America from southern Ontario to northern Mexico and parts of the United States in between. Like all rattlesnakes, it is a pit viper and is venomous. Th ...
''), pygmy rattlesnake (''
Sistrurus miliarius :''Common names: pygmy rattlesnake, eastern pygmy rattlesnake, ground rattlesnake, leaf rattler, death rattler, #Common names, more.''Albert Hazen WWright AH, Anna Allen WWright AA (1957). ''Handbook of Snakes of the United States and Canada''. I ...
''), and milk snake ('' Lampropeltis triangulum''). It is reported that population of rattlesnake in New Hampshire reduced to 19 from 40 due to ophidiomycosis caused by ''O. ophiodiicola''. Ophidiomyces ophiodiicola has been successfully treated in captive settings using the antifungal drug terbinafine, which has shown to be effective via both nebulization or subcutaneous implant.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. 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. The National Wildlife Health Center along with other organizations and researchers are working together to develop management strategies to mitigate disease impact.


References

{{Taxonbar, from=Q28405719 Onygenales