Winter is coming–Temperature affects immune defenses and susceptibility to Batrachochytrium salamandrivorans

Abstract

Environmental temperature is a key factor driving various biological processes, including immune defenses and host-pathogen interactions. Here, we evaluated the effects of environmental temperature on the pathogenicity of the emerging fungal pathogen, Batrachochytrium salamandrivorans ( Bsal), using controlled laboratory experiments, and measured components of host immune defense to identify regulating mechanisms. We found that adult and juvenile Notophthalmus viridescens died faster due to Bsal chytridiomycosis at 14°C than at 6 and 22°C. Pathogen replication rates, total available proteins on the skin, and microbiome composition likely drove these relationships. Temperature-dependent skin microbiome composition in our laboratory experiments matched seasonal trends in wild N. viridescens, adding validity to these results. We also found that hydrophobic peptide production after two months post-exposure to Bsal was reduced in infected animals compared to controls, perhaps due to peptide release earlier in infection or impaired granular gland function in diseased animals. Using our temperature-dependent susceptibility results, we performed a geographic analysis that revealed N. viridescens populations in the northeastern United States and southeastern Canada are at greatest risk for Bsal invasion, which shifted risk north compared to previous assessments. Our results indicate that environmental temperature will play a key role in the epidemiology of Bsal and provide evidence that temperature manipulations may be a viable disease management strategy.

Author summary

In 2010, a new skin-eating fungus, Batrachochytrium salamandrivorans ( Bsal), was discovered killing salamanders in the Netherlands. Since then, the pathogen has spread to other European countries. Bsal is believed to be from Asia and is being translocated through the international trade of amphibians. To our knowledge, Bsal has not arrived to North America. As a proactive strategy for disease control, we evaluated how a range of environmental temperatures in North America could affect invasion risk of Bsal into a widely distributed salamander species, the eastern newt ( Notophthalmus viridescens). Our results show that northeastern USA, southeastern Canada, and the higher elevations of the Appalachian Mountains have the greatest likelihood of Bsal invasion, when temperature-dependent susceptibility is included in risk analyses. Changes in eastern newt susceptibility to Bsal infection associated with temperature are likely an interaction between pathogen replication rate and host immune defenses, including changes in skin microbiome composition and the host’s ability to produce Bsal-killing proteins on the skin. Our study provides new insights into how latitude, elevation and season can impact the epidemiology of Bsal, and suggests that strategies that manipulate microclimate of newt habitats could be useful in managing Bsal outbreaks and that climate change will impact Bsal invasion probability.