Molecular Characterization of Reptile Pathogens Currently Known as Members of the Chrysosporium Anamorph of Nannizziopsis vriesii Complex and Relationship with Some Human-Associated Isolates

Abstract

In recent years, the Chrysosporium anamorph of Nannizziopsis vriesii (CANV), Chrysosporium guarroi, Chrysosporium ophiodiicola, and Chrysosporium species have been reported as the causes of dermal or deep lesions in reptiles. These infections are contagious and often fatal and affect both captive and wild animals. Forty-nine CANV isolates from reptiles and six isolates from human sources were compared with N. vriesii based on their cultural characteristics and DNA sequence data. Analyses of the sequences of the internal transcribed spacer and small subunit of the nuclear ribosomal gene revealed that the reptile pathogens and human isolates belong in well-supported clades corresponding to three lineages that are distinct from all other taxa within the family Onygenaceae of the order Onygenales. One lineage represents the genus Nannizziopsis and comprises N. vriesii, N. guarroi, and six additional species encompassing isolates from chameleons and geckos, crocodiles, agamid and iguanid lizards, and humans. Two other lineages comprise the genus Ophidiomyces, with the species Ophidiomyces ophiodiicola occurring only in snakes, and Paranannizziopsis gen. nov., with three new species infecting squamates and tuataras. The newly described species are Nannizziopsis dermatitidis, Nannizziopsis crocodili, Nannizziopsis barbata, Nannizziopsis infrequens, Nannizziopsis hominis, Nannizziopsis obscura, Paranannizziopsis australasiensis, Paranannizziopsis californiensis, and Paranannizziopsis crustacea. Chrysosporium longisporum has been reclassified as Paranannizziopsis longispora. N. guarroi causes yellow fungus disease, a common infection in bearded dragons and green iguanas, and O. ophiodiicola is an emerging pathogen of captive and wild snakes. Human-associated species were not recovered from reptiles, and reptile-associated species were recovered only from reptiles, thereby mitigating concerns related to zoonosis.

Snake fungal disease: an emerging threat to wild snakes

“…Owing to its association with skin lesions and taxonomic relatedness to other suspected fungal pathogens, O. ophiodiicola has been given 'honorary primary pathogen' status in some literature [8,11]. However, such circumstantial evidence did not preclude that O. ophiodiicola was part of the normal skin flora of snakes, acting merely as a secondary pathogen.…”

“…The initial cases of SFD implicated Chrysosporium ophiodiicola as the possible causative agent [6]. Subsequent genetic studies revealed C. ophiodiicola to be a cryptic member of the Chrysosporium anamorph of Nannizziopsis vriesii (CANV), a complex of morphologically similar fungi associated with skin infections in reptiles [8]. Phylogenetic studies of CANV fungi revealed they were paraphyletic, and this resulted in the transfer of most taxa to other genera, including reassignment of C. ophiodiicola to the monotypic genus Ophidiomyces [8].…”

“…In the USA, isolates have been recovered from captive snakes in California, Georgia, Maryland, New Mexico, New York and Wisconsin (summarized by [8]; figure 1). Some infected snakes were originally collected from the wild [8,14,15] making it unclear where animals were exposed to the fungus.…”

“…In the USA, isolates have been recovered from captive snakes in California, Georgia, Maryland, New Mexico, New York and Wisconsin (summarized by [8]; figure 1). Some infected snakes were originally collected from the wild [8,14,15] making it unclear where animals were exposed to the fungus. Outside North America, O. ophiodiicola has been cultured from lesions of captive snakes in the United Kingdom, Germany and Australia [8,16].…”

“…Subsequent genetic studies revealed C. ophiodiicola to be a cryptic member of the Chrysosporium anamorph of Nannizziopsis vriesii (CANV), a complex of morphologically similar fungi associated with skin infections in reptiles [8]. Phylogenetic studies of CANV fungi revealed they were paraphyletic, and this resulted in the transfer of most taxa to other genera, including reassignment of C. ophiodiicola to the monotypic genus Ophidiomyces [8]. Onygenales includes some of the most medically significant fungal pathogens of animals, including Blastomyces, Histoplasma, Coccidioides, Paracoccidioides, Microsporum and Trichophyton.…”