Globally, fungal pathogens are increasingly associated with widespread wildlife epidemics that threaten sensitive populations. The Eastern Massasauga rattlesnake (Sistrurus catenatus) is listed as threatened under the federal endangered species act, and in Illinois few extant populations remain. In the eastern US, the Eastern Massasauga is vulnerable to snake fungal disease (SFD) caused by Ophidiomyces ophiodiicola infections, which are associated with > 90% mortality. To determine the nature of this species’ sensitivity, a comprehensive health assessment program investigated animal health and disease epidemiology before and after the emergence of this pathogen in Illinois. A healthy and diverse skin microbiome has been linked to a reduction in skin diseases in people, and disruption of the natural skin microbiome is associated with pathogens and overall decreased health in wildlife. The goals of this study were to assess the micro- and mycobiome of Eastern Massasaugas from a population with a persistent occurrence of SFD. The specific hypotheses were: 1) microbial composition on the skin of Eastern Massasaugas will be altered in individuals with SFD, 2) disease state would have a greater impact on microbial composition than demographic factors, and 3) the presence of co-pathogens may be identified in individuals with Ophidiomyces.
144 skin swabs were collected from 48 Eastern Massasaugas in 2015 and 62 in 2016 across 3 sites in Illinois. Ophidiomyces DNA was detected at all sites, with no significant difference among sites, years, or sex. Presence of dermatitis was significantly associated with presence of Ophidiomyces (93.8%, p<0.001). There was no clear pattern of alpha diversity associated with Ophidiomyces status. For both fungal and bacterial communities, distinct assemblages of microbes were observed between SFD–positive and –negative samples (bacteria: ANOSIM R = 0.3633, p<0.001; fungi: ANOSIM R = 0.1573, p < 0.001). SFD status explained 6.8% of bacterial community variance and 5.4% of variance in the fungal community.
Relative abundance of bacterial and fungal taxa differed by SFD status. Dominant bacterial taxa included Pseudomonas, and taxa within the Burkholderiales, Actinomycetales, and Enterobacteriaceae. Actinomycetales were reduced in relative abundance in SFD-positive samples, while Xanthomondales, Sphingobacteriales, and Burkholderiales increased in relative abundance. The fungal microbiome of SFD-positive samples was dominated by Ophidiomyces ophiodiicola, and fungi within the order Pleosporales were reduced in SFD-positive samples. Understanding drivers of SFD status will aid in forming conservation goals, developing recovery strategies to minimize population level disease threats, and targeting interventions supporting a microbiome without Ophidiomyces.