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Experimental infection of snakes with Ophidiomyces ophiodiicola causes pathological changes that typify snake fungal disease

Jeffrey M. Lorch·Julia S. Lankton·Katrien Werner·Elizabeth A. Falendysz·Kevin McCurley·David S. Blehert
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Abstract

Snake fungal disease (SFD) is an emerging skin infection of wild snakes in eastern North America. The fungus Ophidiomyces ophiodiicola is frequently associated with the skin lesions that are characteristic of SFD, but a causal relationship between the fungus and the disease has not been established. We experimentally infected captive-bred corn snakes ( Pantherophis guttatus ) in the laboratory with pure cultures of O. ophiodiicola . All snakes in the infected group ( n = 8) developed gross and microscopic lesions identical to those observed in wild snakes with SFD; snakes in the control group ( n = 7) did not develop skin infections. Furthermore, the same strain of O. ophiodiicola used to inoculate snakes was recovered from lesions of all animals in the infected group, but no fungi were isolated from individuals in the control group. Monitoring progression of lesions throughout the experiment captured a range of presentations of SFD that have been described in wild snakes. The host response to the infection included marked recruitment of granulocytes to sites of fungal invasion, increased frequency of molting, and abnormal behaviors, such as anorexia and resting in conspicuous areas of enclosures. While these responses may help snakes to fight infection, they could also impact host fitness and may contribute to mortality in wild snakes with chronic O. ophiodiicola infection. This work provides a basis for understanding the pathogenicity of O. ophiodiicola and the ecology of SFD by using a model system that incorporates a host species that is easy to procure and maintain in the laboratory. IMPORTANCE Skin infections in snakes, referred to as snake fungal disease (SFD), have been reported with increasing frequency in wild snakes in the eastern United States. While most of these infections are associated with the fungus Ophidiomyces ophiodiicola , there has been no conclusive evidence to implicate this fungus as a primary pathogen. Furthermore, it is not understood why the infections affect different host populations differently. Our experiment demonstrates that O. ophiodiicola is the causative agent of SFD and can elicit pathological changes that likely impact fitness of wild snakes. This information, and the laboratory model we describe, will be essential in addressing unresolved questions regarding disease ecology and outcomes of O. ophiodiicola infection and helping to conserve snake populations threatened by the disease. The SFD model of infection also offers utility for exploring larger concepts related to comparative fungal virulence, host response, and host-pathogen evolution.

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Jeffrey M. Lorch, Julia S. Lankton, Katrien Werner, Elizabeth A. Falendysz, Kevin McCurley, David S. Blehert. 2015. Experimental infection of snakes with Ophidiomyces ophiodiicola causes pathological changes that typify snake fungal disease. https://doi.org/10.1128/mbio.01534-15

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