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

Edward Davis Carter,Brandon Labumbard,Douglas C Woodhams,Louise A Rollins-Smith,Matthew J Gray,Molly C Bletz,Debra L Miller,Mitchell Le Sage,Chengshu Wang

doi:10.1371/journal.ppat.1009234

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.

Highlights

The environment and interactions among organisms under local abiotic conditions are key factors underpinning the functional ecology and distribution of organisms [1]
Our results show that northeastern USA, southeastern Canada, and the higher elevations of the Appalachian Mountains have the greatest likelihood of Batrachochytrium salamandrivorans (Bsal) invasion, when temperaturedependent susceptibility is included in risk analyses
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

Summary

Introduction

The environment and interactions among organisms under local abiotic conditions are key factors underpinning the functional ecology and distribution of organisms [1]. Temperature drives many ecophysiological processes that manifest in organismal vital rates (of both hosts and pathogens), and can influence population persistence and species distributions. Temperature influences organisms through various mechanisms, including metabolic and immunological pathways [2] It can drive interactions among organisms and microparasites [3]. Environmental temperature is expected to affect host susceptibility to pathogens and epidemiological processes. By their nature, the ecophysiology of ectothermic vertebrate species is strongly coupled with environmental temperature [2,4]. Environmental temperature affects many physiological processes in amphibians including immune function [5,6]. Temperature is considered a primary factor influencing invasion probability of pathogens in ectothermic vertebrate populations [9,10]

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Conclusion