The other white‐nose syndrome transcriptome: Tolerant and susceptible hosts respond differently to the pathogen Pseudogymnoascus destructans

Abstract

Mitigation of emerging infectious diseases that threaten global biodiversity requires an understanding of critical host and pathogen responses to infection. For multihost pathogens where pathogen virulence or host susceptibility is variable, host–pathogen interactions in tolerant species may identify potential avenues for adaptive evolution in recently exposed, susceptible hosts. For example, the fungus Pseudogymnoascus destructans causes white‐nose syndrome (WNS) in hibernating bats and is responsible for catastrophic declines in some species in North America, where it was recently introduced. Bats in Europe and Asia, where the pathogen is endemic, are only mildly affected. Different environmental conditions among Nearctic and Palearctic hibernacula have been proposed as an explanation for variable disease outcomes, but this hypothesis has not been experimentally tested. We report the first controlled, experimental investigation of response to P. destructans in a tolerant, European species of bat (the greater mouse‐eared bat, Myotis myotis). We compared body condition, disease outcomes and gene expression in control (sham‐exposed) and exposed M. myotis that hibernated under controlled environmental conditions following treatment. Tolerant M. myotis experienced extremely limited fungal growth and did not exhibit symptoms of WNS. However, we detected no differential expression of genes associated with immune response in exposed bats, indicating that immune response does not drive tolerance of P. destructans in late hibernation. Variable responses to P. destructans among bat species cannot be attributed solely to environmental or ecological factors. Instead, our results implicate coevolution with the pathogen, and highlight the dynamic nature of the “white‐nose syndrome transcriptome.” Interspecific variation in response to exposure by the host (and possibly pathogen) emphasizes the importance of context in studies of the bat‐WNS system, and robust characterization of genetic responses to exposure in various hosts and the pathogen should precede any attempts to use particular bat species as generalizable “model hosts.”

Gene expression response to a nematode parasite in novel and native eel hosts

“…In both frogs and toads suffering from chytridiomycosis, a larger number of genes were differentially expressed in susceptible species and they were involved in a more diverse set of processes, including several immune‐related and metabolic processes (Eskew et al, ; Poorten & Rosenblum, ). Similar patterns were observed in bats exposed to the fungus causing white‐nose syndrome (Davy et al, ; Field et al, ) although the resistant species had cleared the infection at the time of sampling. Finally, more genes were differentially expressed in a more susceptible bee species exposed to Varroa mites (Zhang, Liu, Zhang, & Han, ), although the diversity of processes was not reported.…”

Quantification of pathogen levels is necessary to compare responses to pathogen exposure: Comment on Davy et al. “The other white‐nose syndrome transcriptome”

“…The RNA‐Seq samples from Davy et al. (2017) do not contain detectable Pseudogymnoascus destructans pathogen levels compared to other studies. Future studies will be necessary to determine how hosts resistant to white‐nose syndrome respond differently than susceptible hosts at the whole‐transcriptome level.…”

“…An important question in the disease ecology of WNS is how hosts that are resistant or tolerant to infection respond differently than susceptible hosts. A recent paper in Ecology and Evolution (Davy et al., 2017) attempts to address this question by comparing the transcriptomic responses of the WNS‐resistant Myotis myotis to the WNS‐susceptible M. lucifugus . This study demonstrated that M. myotis are resistant to infection under the same conditions that M. lucifugus are susceptible to infection and under which they develop WNS.…”

“…Because P. destructans is a eukaryotic pathogen, it is possible to use the Poly(A)‐selected RNA‐Seq data to measure pathogen level in each sample. Using the data from this study (Davy et al., 2017) in the Sequence Read Archive, I compared the levels of P. destructans transcripts to other published (Field et al., 2015) and unpublished datasets (Table 1). For this analysis, the RNA‐Seq data were quality trimmed and then the reads were mapped to the combined transcriptomes of M. lucifugus and  P. destructans using Kallisto (Bray, Pimentel, Melsted, & Pachter, 2016).…”

Profiling the immunome of little brown myotis provides a yardstick for measuring the genetic response to white‐nose syndrome

“…While several North America bats are highly susceptible to WNS, European bats do not experience mortality from infection with P. destructans (Puechmaille, Fuller, & Teeling, ; Puechmaille, Wibbelt, et al., ). Controlled experiments with captive bats show that identical strains of P. destructans cause mortality in North American little brown myotis ( Myotis lucifugus ) but not in European greater mouse‐eared bats ( Myotis myotis ; Davy et al., ), suggesting a genetic basis for immunotolerance or immunoprotection.…”