The Antifungal Properties of Epidermal Fatty Acid Esters: Insights from White-Nose Syndrome (WNS) in Bats

Abstract

Numerous free fatty acids (FFAs) are known to have potent antifungal effects. The mammalian epidermis contains both FFAs and multiple classes of fatty acid esters, including 1-monoacylglycerols and wax esters. We thus hypothesized that wax esters and 1-monoacylglycerols composed of antifungal fatty acids would also have antifungal properties. We tested this hypothesis by examining the effects of 1-monoacylglycerols, 1,3-diacylglycerols, and wax esters on the growth of Pseudogymnoascus destructans (Pd), the fungus that causes White-nose Syndrome (WNS) in North American bats by invading their epidermis. Laboratory experiments with Pd cultures demonstrated that: (a) three 1-monoacylglycerols (1-monopalmitolein, 1-monoolein, and 1-monolinolein), as well as, (b) two wax esters, behenyl oleate and behenyl palmitoleate, profoundly inhibit Pd growth. The normal growth cycle of Pd was interrupted by addition of two cholesterol esters to the media as well. A bat species resistant to cutaneous Pd infections has these 1-monoacylglycerols in the epidermis, and another Pd resistant bat species has these wax esters in the sebum, thus cutaneous lipid composition is one factor which enables some bats to avoid WNS. Our experiments also revealed that the fatty acid esters which inhibit Pd growth are not hydrolyzed by the lipases secreted by this fungus, whereas the esters that do not inhibit Pd growth are hydrolyzed.

When are extinctions simply bad luck? Rarefaction as a framework for disentangling selective and stochastic extinctions

“…Importantly, our results also suggest the potential susceptibility of Corynorhinus townsendii virginianus , which is not generally recognized as vulnerable to the pathogen (Coleman & Reichard, ; Silvis, Perry, & Ford, ). Further, these results confirm recent findings that E. fuscus may have species‐specific, trait‐based resistance to WNS (Frank et al, ; Frank, Sitler‐Elbel, Hudson, & Ingala, ), as its abundance was greater than expected post‐decline.…”

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

“…Although the transcriptional activity of the fungus was comparable between the species within the lesions themselves, M. myotis had fewer total lesions than M. lucifugus , suggesting the growth of P. destructans in M. myotis could be controlled by other factors not associated with transcriptional host responses during arousals. These factors may include abiotic environmental conditions (Johnson et al 2014), microbial competition (Cornelison et al 2014; Micalizzi et al 2017), and the antifungal properties of epidermal fatty acid esters (Frank et al 2018).…”

Antifungal Potential of the Skin Microbiota of Hibernating Big Brown Bats (Eptesicus fuscus) Infected With the Causal Agent of White-Nose Syndrome

“…We recommend that future studies try to better characterize post- Pd colonization patterns and, especially, characterize functional changes resulting from these patterns. WNS resistance and tolerance may reflect a range of mechanisms, from storage of extra body fat in fall ( Cheng et al, 2019 ), endogenous fat in epidermis composition ( Frank et al, 2016 , 2018 ), variation in individual behavior ( Frick et al, 2016 ) to variation in immune response ( Maslo and Fefferman, 2015 ). Our results suggest that the skin microbiota could be another mechanism helping some bats survive infection with Pd .…”

“…One underexplored factor that could affect resistance to WNS is the skin microbiota. Differences in lipid profiles affecting WNS-resistance ( Frank et al, 2016 , 2018 ) may contribute to different microbial profiles by providing different nutritional substrates. Hundreds of microorganisms isolated from wild bats and their corresponding habitats have been tested in controlled laboratory conditions for their inhibitory effects on Pd , by focusing on the actions of secreted compounds, contact inhibition or volatile molecules ( Hamm et al, 2017 ; Micalizzi et al, 2017 ).…”