Membrane lipid physiology and toxin catabolism underlie ethanol and acetic acid tolerance inDrosophila melanogaster

Abstract

SUMMARY Drosophila melanogaster has evolved the ability to tolerate and utilize high levels of ethanol and acetic acid encountered in its rotting-fruit niche. Investigation of this phenomenon has focused on ethanol catabolism, particularly by the enzyme alcohol dehydrogenase. Here we report that survival under ethanol and acetic acid stress in D. melanogasterfrom high- and low-latitude populations is an integrated consequence of toxin catabolism and alteration of physical properties of cellular membranes by ethanol. Metabolic detoxification contributed to differences in ethanol tolerance between populations and acclimation temperatures viachanges in both alcohol dehydrogenase and acetyl-CoA synthetase mRNA expression and enzyme activity. Independent of changes in ethanol catabolism,rapid thermal shifts that change membrane fluidity had dramatic effects on ethanol tolerance. Cold temperature treatments upregulated phospholipid metabolism genes and enhanced acetic acid tolerance, consistent with the predicted effects of restoring membrane fluidity. Phospholipase D was expressed at high levels in all treatments that conferred enhanced ethanol tolerance, suggesting that this lipid-mediated signaling enzyme may enhance tolerance by sequestering ethanol in membranes as phophatidylethanol. These results reveal new candidate genes underlying toxin tolerance and membrane adaptation to temperature in Drosophila and provide insight into how interactions between these phenotypes may underlie the maintenance of latitudinal clines in ethanol tolerance.

Modeling trade‐offs between plant fiber and toxins: a framework for quantifying risks perceived by foraging herbivores

“…1). Individuals may differ physiologically (e.g., detoxification capacity, stress hormones, metabolism; Maltby 1999, Montooth et al 2006 or behaviorally (e.g., boldness; Mella et al 2014). For example, individual brushtail possums (Trichosurus vulpecula) varied in measures of boldness, and boldness influenced foraging at patches with high predation risk and patches with low predation risk only when food toxins were low (Mella et al 2014).…”

Reduction in the cumulative effect of stress-induced inbreeding depression due to intragenerational purging in Drosophila melanogaster

“…We propose that this pattern seen with the two abiotic stresses could arise from a combination of purging and a general stress-induced physiological weakening. Extensive work in a variety of animals shows longterm protein damage and impaired cellular functioning can result from heat and ethanol stress (Hoffmann and Parsons, 1991;Sorensen et al, 2003;Montooth et al, 2006). Studies in Drosophila found exposure to high heat and sublethal concentrations of ethanol alters membrane lipid composition and energy reserves (Sorensen et al, 2003;Montooth et al, 2006), which could have enduring negative effects on later life history traits such as female fecundity and male fertility (Krebs and Loeschcke, 1994;Bokor and Pecsenye, 2000).…”

Mechanisms of naturally evolved ethanol resistance inDrosophila melanogaster

“…In addition to its well-known advantages as a model organism, D. melanogaster shows marked geographic variation in ethanol resistance, with populations from temperate latitudes being consistently more resistant than those from the tropics or subtropics (David and Bocquet, 1975;Cohan and Graf, 1985;David et al, 1986;Parkash et al, 1999;Montooth et al, 2006). This variation is correlated with allele frequency variation in the well-studied enzyme gene Alcohol dehydrogenase (Adh), whose product converts ethanol to acetaldehyde ( Fig.…”

“…Another relevant observation is that, both among D. melanogaster strains and among Drosophila species, resistance to ethanol is strongly correlated with resistance to acetic acid (Chakir et al, 1993;Eisses and Den Boer, 1995;Montooth et al, 2006). This could be explained in at least three ways.…”