White adipose tissue remodeling in Little Brown Myotis (Myotis lucifugus) with white-nose syndrome

Abstract

AbstractWhite-nose syndrome (WNS) is a fungal wildlife disease of bats that has caused precipitous declines in certain Nearctic bat species. A key driver of mortality is premature exhaustion of fat reserves, primarily white adipose tissue (WAT), that bats rely on to meet their metabolic needs during winter. However, the pathophysiological and metabolic effects of WNS have remained ill-defined. To elucidate metabolic mechanisms associated with WNS mortality, we infected a WNS susceptible species, the Little Brown Myotis (Myotis lucifugus), withPseudogymnoascus destructans(Pd) and collected WAT biopsies for histology and targeted lipidomics. These results were compared to the WNS-resistant Big Brown Bat (Eptesicus fuscus). A similar distribution in broad lipid class was observed in both species, with ∼60% of total WAT consisting of triacylglycerides (TAGs). We found several baseline differences in WAT chemical composition between species.M. lucifugusWAT had significantly higher levels of measured TAGs (∼30%). Higher lipid levels inE. fuscusWAT were primarily sphingomyelins and glycerophosphoethanolamines (PEs), along with glycerophospholipids (GPs) dominated by unsaturated or monounsaturated moieties and n-6 (18:2, 20:2, 20:3, 20:4) fatty acids. These differences betweenM. lucifugusandE. fuscusmay indicate dietary differences that lead to differential “fuel” reserves that are available during torpor. FollowingPd-infection, we found that perturbation to WAT reserves occurs inM. lucifugus, but not in the resistantE. fuscus. A total of 36 GPs (primarily PEs) were higher inPd-infectedM. lucifugus, indicating perturbation to the WAT structural component. In addition to changes in lipid chemistry, smaller adipocyte sizes and increased extracellular matrix deposition was observed inPd-infectedM. lucifugus. This is the first study to describe WAT lipidomic composition of bats with different susceptibilities to WNS and highlights that recovery from WNS may require repair from adipose remodeling in addition to replenishing depot fat during spring emergence.