Populations of multiple North American bat species have been more than decimated by white-nose syndrome, a fungal disease that spreads within roosting colonies and becomes deadly during hibernation. A paper just released online early at Molecular Ecology adds support to a hypothesis that the reason for the fungus’s virulence is that hibernation puts bats’ immune systems to sleep — and waking up to fight the fungus costs more than they can afford.
Kenneth Field and colleagues captured hibernating, fungus-free little brown bats (Myotis lucifugus, a species susceptible to white nose but not endagered), brought them into the lab, infected them with Pseudogymnoascus destructans, the fungus that causes white nose, and kept them in hibernation for 20 more weeks before rousing them. They took tissue biopsies from infected and fungus-free areas of the bats’ wing membranes at two time points: when the bats were still torpid, with their body temperatures below 6°C, and then when they had roused to the point that their temperatures were normalized. They extracted RNA from the biopsied tissue, reversed-transcribed it, and collected high-throughput short read DNA sequence from the result.
The pairwise comparisons between uninfected and infected wing tissue at torpor and in waking bats were informative. Where the coauthors only detected 49 genes with differences in expression between infected and uninfected tissue from torpid bats, in they found 1,098 genes differentially expressed based on infection status in bats that had warmed up. Perhaps not surprisingly, there were more genes showing differential expression between torpor and arousal in infected tissues than in uninfected tissues, as well.
Functional annotation of the sequenced gene transcripts confirmed that immune response genes were overrepresented among those differentially expressed in response to infection, in both torpid and waking bats — but, again, a longer list of immune components were annotated in the genes showing differential expression in waking bats. Genes with roles in both the innate and adaptive immune system showed increased expression in infected tissue of waking bats relative to torpid ones, suggesting that there isn’t, for this species at least, a significant subset of immune responses to the white nose fungus that persist during torpor.
All of these results are consistent with prior research on hibernating mammals showing, often more directly, that hibernation reduces the responsiveness of at least some elements of the immune system. Like other mammals that hibernate, bats rouse from torpor periodically during the winter, and one function of these brief periods of increased metabolic activity might be immune response — but waking up is energetically costly. Field et al. suggest in their discussion that the fungus kills bats by putting them in a metabolic catch-22: they need to rouse more often to mount an immune response to the fungus, but rousing burns up their energy reserves. Effectively, they starve to death while they sleep.
References
Field KA, BJ Sewall, JM Prokkola, GG Turner, M Gagnon, TM Lilley, JP White, JS Johnson, CL Hauer, and DM Reeder. 2018. Effect of torpor on host transcriptomic responses to a fungal pathogen in hibernating bats. Molecular Ecology. doi: 10.1111/mec.14827
