Temperature‐mediated shifts in salamander transcriptomic responses to the amphibian‐killing fungus

Abstract

Life processes of ectothermic vertebrates are intimately linked to the temperature of their environment, influencing their metabolism, reproduction, behaviour and immune responses. In amphibians infected by the generalist chytrid pathogen Batrachochytrium dendrobatidis (Bd), host survival, infection prevalence and infection intensity are often temperature‐ and/or seasonally dependent. However, the transcriptional underpinnings of thermal differences in infection responses remain unknown. Measuring the impact of temperature on host responses to infection is a key component for understanding climatic influences on chytrid disease dynamics. The Bd‐responsive gene pathways in frogs are well documented, but our understanding of salamander immune expression profiles during infection with chytrids remains limited. Here we characterize the transcriptomic responses of Plethodon cinereus using RNA sequencing by comparing skin and splenic gene expression of individuals uninfected, succumbing to Bd infection and naturally cleared of Bd infection at three temperatures. We suggest that amphibian temperature‐dependent susceptibility to Bd is probably driven by shifts in expression of the innate and adaptive immune axes. Our study shows increased expression of transcripts associated with inflammation at lower temperatures and a shift towards increased expression of adaptive immune genes, including MHC (major histocompatibility complex), at higher temperatures. In the face of climate change, and as concerns for the spread of emergent chytrid pathogens increase, our results provide important functional genomic resources to help understand how these pathogenic fungi may continue to affect amphibian communities globally in the future.

Preparing for invasion: Assessing risk of infection by chytrid fungi in southeastern plethodontid salamanders

“…In our study several individuals carried natural Bd infections that were not detected by field swabbing, but emerged during the experiment (Figure 5 and Figure S2, as has been reported in other species (Byrne et al, 2018; Mendoza‐Almeralla et al, 2016). This result is likely a combination of low detection probability at low intensity infections (e.g., DiRenzo et al, 2018) as well as within‐host processes such as symbiont recruitment and immunity that can change with translocation to the lab and constant temperatures (Ellison et al, 2020; Loudon et al, 2013). In addition, many plethodontid species harbor skin bacteria that can kill Bd in culture, and these symbionts can be lost with the transfer from the field to the lab (Harris et al, 2006; Harris et al, 2009; 2009; Loudon et al, 2013; Muletz Wolz et al, 2018).…”

“…This result is likely a combination of low detection probability at low intensity infections (e.g., DiRenzo et al, 2018) as well as within-host processes such as symbiont recruitment and immunity that can change with translocation to the lab and constant temperatures (Ellison et al, 2020;Loudon et al, 2013). In addition, many plethodontid species harbor skin bacteria that can kill Bd in culture, and these symbionts can be lost with the transfer from the field to the lab (Harris et al, 2006;Loudon et al, 2013;Muletz Wolz et al, 2018).…”

“…Many Appalachian plethodontid salamanders in the United States have experienced enigmatic declines since the 1980s without a clear link to the emergence of Bd or Bsal (Adams et al, 2013; Caruso & Lips, 2013; Highton, 2005; Muletz et al, 2014). Laboratory susceptibility trials have shown high variation in disease development in plethodontids (Carter et al, 2019; Martel et al, 2014), which could be related to species traits, microbial associations, and/or immune complexity (Ellison et al, 2020; Muletz‐Wolz et al, 2017; Woodhams et al, 2020).…”

Cross-Disciplinary Genomics Approaches to Studying Emerging Fungal Infections

“…Meanwhile, transcriptomics has revealed how host responses to infection vary depending on the host species but also the lineage of fungus infecting [64,65], and that the fungus itself exhibits host-specific gene expression [66]. Further emphasising how -omics reveals the extreme complexity of fungal host-pathogen systems, recent research has shown that environmental conditions such as temperature also mediate the transcriptional host response to infection [67]. The most recent advances have also addressed the microbiome of the host, drawing correlations between the microbiome, the metabolome and the transcriptome of the microbiome with disease status [68][69][70][71], with the hope of using this information to target mitigation strategies [72].…”

Immunological Aspects of Chytridiomycosis

“…As with all physiological processes in ectotherms, the immune function in amphibians is strongly influenced by temperature [72]. Numerous studies have found that the performance of both innate [73][74][75] and adaptive [76] immune responses are reduced at low temperatures. Rapid changes in temperature have also been found to have a detrimental effect on immune function [74,77].…”