Infection with Nannizziopsis guarroi and Ophidiomyces ophiodiicola in reptiles in Taiwan

Abstract

Fungal infection is an emerging threat to reptiles. The main pathogens are fungi of the genera Nannizziopsis, Paranannizziopsis and Ophidiomyces. The clinical symptoms range from mild skin lesions to the dissemination of internal organs and even death. Most of the reported cases are from Europe, North America and Australia. In this study, we report the Nannizziopsis guarroi infection in one captive inland bearded dragon (Pogona vitticeps), one captive green iguana (Iguana iguana) and Ophidiomyces ophiodiicola infection in one wild red‐banded snake (Dinodon rufozonatum) and one wild Chinese cobra (Naja atra) in Taiwan. The infections were confirmed by the presence of fungal elements in the tissue. The pathogens were identified based on their morphological and DNA sequence characteristics. The susceptibility profiles of the fungal strains to nine antifungal drugs were obtained using broth microdilution methods. The presence of both fungal species in Asia highlights the urgent need for surveillance and close monitoring of reptile infections to prevent them from spreading and to the possible collapse of reptile populations in the wild.

Population genetic analysis of Ophidiomyces ophidiicola, the causative agent of snake fungal disease, indicates recent introductions to the USA

“…Similar to previous studies that had examined only a small number of loci [26, 27], we identified three major clades among all 82 sampled Oo strains, but all strains originating from wild snakes in the USA belonged to a single clade (Clade II). Within this North American clade, we initially observed what appeared to be high genetic diversity as evidenced by the presence of many long phylogenetic branches (Fig.…”

“…S1). This represented ~81-84% of the annotated protein coding genes for each strain, and the overall topology, which consisted of three, well-supported main clades, was consistent with previously published phylogenies for Oo [26,27]. One of these clades (Clade I) contained all four strains isolated from wild snakes in Europe; a second clade (Clade II) contained all 65 strains isolated from wild snakes in North America as well as 10 strains from captive snakes; and the third clade (Clade III) included three strains, all collected from snakes in captivity.…”

“…Consistent with previous studies, we found that Clade III was an outgroup to Clades I and II; however, our full genome analysis indicated a much higher level of genetic divergence than previously reported. The two protein coding genes used in previous phylogenetic analyses of Oo (actin and translation elongation factor 2L [26, 27]) exhibited average levels of divergence between Clades III and I/II (0.016% and 0% at the amino acid level) that were lower than ∼97-98% of the orthologs we examined (Fig. S1B).…”

“…Under the novel pathogen hypothesis, we would predict that Oo arrived in the USA relatively recently, perhaps in the order of decades prior to the increase in cases of SFD reported during the early 2000s [18, 21]. Indeed, the detection of genetically unique and diverse strains of Oo from wild snakes in Eurasia [26, 27] is consistent with this hypothesis, as it indicates that Oo may have originated from outside North America. In contrast, the endemic pathogen hypothesis would be consistent with a much older arrival of Oo in the USA, with the recent increase in SFD cases linked to greater awareness or environmental changes rather than a new introduction.…”

Genetic mechanisms and biological processes underlying host response to ophidiomycosis (Snake Fungal Disease) inferred from tissue-specific transcriptome analyses

“…O. ophidiicola is a generalist fungus and is known to infect a wide range of snake species with different ecologies irrespective of taxonomy and habitat (33). First reported in the mid-2000s, but likely present as early as the 1940’s (34–36), SFD has since been documented in more than 30 species of wild snakes in the United States and Europe (31) and instances of SFD have also been reported in Australia (37) and South East Asia (38, 39). Clinical signs of ophidiomycosis vary among individuals, from general signs such as lethargy, skin lesions, excessive shedding, to crusts, granulomas, corneal opacity, and ulcers on the head and body in more severe cases (29).…”