Skin sloughing in susceptible and resistant amphibians regulates infection with a fungal pathogen

Abstract

The fungal pathogen Batrachochytrium dendrobatidis (Bd) has been implicated in amphibian population declines globally. Given that Bd infection is limited to the skin in post-metamorphic amphibians, routine skin sloughing may regulate infection. Skin sloughing has been shown to reduce the number of cultivatable microbes on amphibian skin, and Bd infection increases skin sloughing rates at high loads. However, it is unclear whether species specific differences in skin sloughing patterns could regulate Bd population growth on the skin, and influence subsequent infection dynamics. We exposed five Australian frog species to Bd, and monitored sloughing rates and infection loads over time. Sloughing reduced Bd load on the ventral skin surface, in all five species, despite wide variation in susceptibility to disease. In the least susceptible species, an increase in sloughing rate occurred at lower infection loads, and sloughing reduced Bd load up to 100%, leading to infection clearance. Conversely, the drop in Bd load with sloughing was only temporary in the more susceptible species. These findings indicate that the ability of sloughing to act as an effective immune defence is species specific, and they have implications for understanding the pattern of Bd population growth on individual hosts, as well as population-level effects.

Diverse genotypes of the amphibian‐killing fungus produce distinct phenotypes through plastic responses to temperature

“…We found that Bd genotypes displayed similar growth pat- (Berger et al, 2005). During this time, Bd is interacting with host skin tissue, host immune molecules and host skin microbiomes, all of which can vary in composition among host species and environments (Ellison et al, 2014;Muletz Wolz, Yarwood, Campbell Grant, Fleischer, & Lips, 2018;Ohmer, Cramp, Russo, White, & Franklin, 2017 We found preliminary evidence that functional traits and their plasticity evolved independently of Bd phylogenetic relationships. Tests of phylogenetic signal are not without shortcomings and the short evolutionary divergence time of Bd-GPL and our limited sample size for taxa may have influenced the chances of detecting a phylogenetic signal (Blomberg et al, 2003;Freckleton et al, 2002;Revell et al, 2008).…”

“…Bd completes its life cycle within keratinized tissue, initially invading as zoospores a few layers deep, and then maturing into zoosporangia as the epidermal cells move outwards and keratinize (Berger et al., ). During this time, Bd is interacting with host skin tissue, host immune molecules and host skin microbiomes, all of which can vary in composition among host species and environments (Ellison et al., ; Muletz Wolz, Yarwood, Campbell Grant, Fleischer, & Lips, ; Ohmer, Cramp, Russo, White, & Franklin, ). The more variable growth patterns we observed at lower temperatures may result from variation in these host and environmental pressures on Bd genotypes.…”

Phylogenetic investigation of skin sloughing rates in frogs: relationships with skin characteristics and disease-driven declines

“…It is assumed that this process transpires in most amphibians, and it is thought to occur anywhere from daily [25] to once a week or fortnightly [26,27]. Sloughing primarily acts in skin renewal, but may also play a role in controlling cutaneous microbial populations [27,28], and even regulating Bd load on the skin [29]. It has thus been suggested that sloughing rate, or the rate of epidermal turnover, could contribute to the susceptibility of amphibians to chytridiomycosis [29][30][31].…”

“…Sloughing primarily acts in skin renewal, but may also play a role in controlling cutaneous microbial populations [27,28], and even regulating Bd load on the skin [29]. It has thus been suggested that sloughing rate, or the rate of epidermal turnover, could contribute to the susceptibility of amphibians to chytridiomycosis [29][30][31]. However, most of the research on amphibian sloughing occurred prior to the discovery of Bd, and only with a limited number of common laboratory species [24].…”

Xela DS2 and Xela VS2: two novel skin epithelial-like cell lines from adult African clawed frog (Xenopus laevis) and their response to an extracellular viral dsRNA analogue

“…Nonetheless, the establishment and characterization of Xela DS2 and Xela 691 VS2 represent a key advancement in the generation of in vitro model systems for future 692 investigations in amphibian skin epithelial cell biology, including environmental parameters that 693 may impact epithelial cell characteristics such as cellular junctions and transepithelial resistance 694 as a means of determining skin barrier integrity. 695 may be linked to the increased skin sloughing observed in some frog species in response to 714 pathogens (Ohmer et al, 2017). However, given the limited studies on amphibian skin tissue and 715 epithelial cell responses to extracellular viral dsRNA, pathogens in general, and the mechanisms 716 that drive skin sloughing in response to pathogens, further investigation is required to ascertain 717 whether our in vitro observations in Xela DS2 and Xela VS2 following poly(I:C) treatment are 718 reflective of in vivo skin sloughing responses.…”