Resistance is futile: RNA-sequencing reveals differing responses to bat fungal pathogen in Nearctic Myotis lucifugus and Palearctic Myotis myotis

Thomas M Lilley,Steve Paterson,Kenneth A Field,Erik Bachorec,Tomáš Bartonička,Anna S Blomberg,Gregory G Turner,Deeann M Reeder,Joseph S Johnson,Jenni M Prokkola

doi:10.1007/s00442-019-04499-6

Abstract

Resistance and tolerance allow organisms to cope with potentially life-threatening pathogens. Recently introduced pathogens initially induce resistance responses, but natural selection favors the development of tolerance, allowing for a commensal relationship to evolve. Mycosis by Pseudogymnoascus destructans, causing white-nose syndrome (WNS) in Nearctic hibernating bats, has resulted in population declines since 2006. The pathogen, which spread from Europe, has infected species of Palearctic Myotis for a longer period. We compared ecologically relevant responses to the fungal infection in the susceptible Nearctic M. lucifugus and less susceptible Palearctic M. myotis, to uncover factors contributing to survival differences in the two species. Samples were collected from euthermic bats during arousal from hibernation, a naturally occurring phenomenon, during which transcriptional responses are activated. We compared the whole-transcriptome responses in wild bats infected with P. destructans hibernating in their natural habitat. Our results show dramatically different local transcriptional responses to the pathogen between uninfected and infected samples from the two species. Whereas we found 1526 significantly upregulated or downregulated transcripts in infected M. lucifugus, only one transcript was downregulated in M. myotis. The upregulated response pathways in M. lucifugus include immune cell activation and migration, and inflammatory pathways, indicative of an unsuccessful attempt to resist the infection. In contrast, M. myotis appears to tolerate P. destructans infection by not activating a transcriptional response. These host-microbe interactions determine pathology, contributing to WNS susceptibility, or commensalism, promoting tolerance to fungal colonization during hibernation that favors survival.Graphic abstract

Highlights

Exposure to novel pathogens in naive wildlife populations has increased over the last decades (Daszak et al 2000)
This study set out to test the hypothesis that M. myotis exhibits similar whole-transcriptome responses to P. destructans infection as the M. lucifugus from remnant populations that are more recently exposed to the pathogen
We found that UV-positive M. lucifugus contained 1475 ± 1010 P. destructans transcripts per million mapped reads (TPM) and UV-positive M. myotis 3817 ± 1965 TPM (Welch twosample t test, p = 0.0557)

Summary

Introduction

Exposure to novel pathogens in naive wildlife populations has increased over the last decades (Daszak et al 2000). Many of these introductions are caused by humans inadvertently transporting microbes with pathogenic potential to new geographic locations, where they emerge as a major concern for native species (Tompkins et al 2015). White-nose syndrome (WNS), a bat fungal disease, has been linked to varied host responses rather than increased pathogen virulence (Field et al 2015; Leopardi et al 2015; Bandouchova et al 2018). WNS is caused by Pseudogymnoascus destructans, and has resulted in extensive declines in populations of several bat species since arriving in North America likely from Eurasia in 2006 (Blehert et al 2009; Frick et al 2010; Leopardi et al 2015; Campana et al 2017)

Methods

Results

Conclusion