Functional expression of Δ12 fatty acid desaturase modulates thermoregulatory behaviour in Drosophila

Abstract

polyunsaturated fatty acids (pUfAs) play crucial roles in adaptation to cold environments in a wide variety of animals and plants. However, the mechanisms by which PUFAs affect thermoregulatory behaviour remain elusive. Thus, we investigated the roles of PUFAs in thermoregulatory behaviour of Drosophila melanogaster. To this end, we generated transgenic flies expressing Caenorhabditis elegans Δ12 fatty acid desaturase (FAT-2), which converts mono-unsaturated fatty acids to PUFAs such as linoleic acid [C18:2 (n-6)] and linolenic acid [C18:3 (n-3)]. Neuron-specific expression of FAT-2 using the GAL4/UAS expression system led to increased contents of C18:2 (n-6)-containing phospholipids in central nerve system (CNS) and caused significant decreases in preferred temperature of third instar larvae. In genetic screening and calcium imaging analyses of thermoreceptor-expressing neurons, we demonstrated that ectopic expression of FAT-2 in TRPA1-expressing neurons led to decreases in preferred temperature by modulating neuronal activity. We conclude that functional expression of FAT-2 in a subset of neurons changes the thermoregulatory behaviour of D. melanogaster, likely by modulating quantities of PUFA-containing phospholipids in neuronal cell membranes. Polyunsaturated fatty acids (PUFAs) contain multiple double bonds in their hydrocarbon chains and, as bioactive lipids, regulate various animal physiological functions, such as those relating to immunity, reproduction and energy metabolism 1,2. PUFAs have also been implicated in thermal adaptation, particularly cold adaptation, because the cis double bonds in PUFAs create the "kinks" in hydrocarbon chain structures that reduce the packing of phospholipids, thus increasing membrane fluidity at low temperatures 3,4. For instance, ectothermic fish that live in low temperatures have high PUFA contents in phospholipids 5,6 , facilitating membrane fluidity 7 and modulating the activities of membrane proteins, such as Na +-K + ATPase 8 , in cold environments. Most organisms produce mono-unsaturated fatty acids from saturated fatty acids through the actions of Δ9 fatty acid desaturases 9-13. In mammals, PUFAs such as arachidonic acid [C20:4 (n-6)] and eicosapentaenoic acid [C20:5 (n-3)] are produced from linoleic acid [C18:2 (n-6)] and α-linolenic acid [C18:3 (n-3)], respectively, by Δ5 and Δ6 fatty acid desaturases. In contrast, Δ12 fatty acid desaturases that convert oleic acid [C18:1 (n-9)] to C18:2 (n-6), such as those in nematode Caenorhabditis elegans 14 , American cockroach 15 and cricket 16 , are found in few animals. Therefore, most animals have to obtain PUFAs, such as C18:2 (n-6) and C18:3 (n-3), from their diet. In bacteria 17 , protozoa 18 , algae 19,20 and plants 21,22 , Δ12 fatty acid desaturase can be reportedly induced following exposures to low temperatures. Hence, its biosynthetic product C18:2 (n-6) is thought to play crucial roles in low-temperature acclimation. C. elegans synthesises PUFAs using seven desaturases (FAT-1, FAT-2, FAT-3, FAT-4, FAT-5, FAT-6, ...

Adipose triglyceride lipase promotes prostaglandin-dependent actin remodeling by regulating substrate release from lipid droplets

“…It seems likely that LDs also buffer AA released from endogenous sources. Because Drosophila lacks the enzymes to synthesize AA (Shen et al ., 2010; Suito et al ., 2020), AA present in the ovary must be derived from food and be transported, like other FAs, through the hemolymph via lipoprotein particles. These lipoproteins are captured by lipophorin receptors at the surface of nurse cells which deliver FAs to the germ line (Parra-Peralbo and Culi, 2011).…”

Nutritional Enhancement of Health Beneficial Omega-3 Long-Chain Polyunsaturated Fatty Acids in the Muscle, Liver, Kidney, and Heart of Tattykeel Australian White MARGRA Lambs Fed Pellets Fortified with Omega-3 Oil in a Feedlot System

“…EPA + DPA + DHA are known to promote intellectual development in infancy, relieve inflammation, boost the immune system, reduce incidences of cardiovascular diseases, some cancers, diabetes, allergies, behavioral disorders, and sustain retinal functions [9][10][11][12]. However, humans, like all mammals, cannot synthesize n-3 LC-PUFA because they are unable to produce ∆12 and ∆15-desaturase enzymes [13], hence, rely on dietary sources like leafy vegetables, oilseeds, nuts, eggs, and seafood, especially fish and crustaceans [10,14], edible marine algae, bacteria, fungi, diatoms, fruits, and herbs [15], to meet their daily n-3 LC-PUFA requirements. Oilseeds commonly used in human diets include rapeseed [16] and soybean [17], while seed oils from waste food by-products such as tomato [18] and citrus [19] are cheap animal feed sources that can enhance healthy fatty acid composition.…”

Limited introgression from non‐native commercial strains and signatures of adaptation in the key pollinator Bombus terrestris

“…Such gustatory systems are key mechanisms for animals, from mammals to insects, for sensing amino acids in the environment (Lim et al, 2019). In addition, we find enrichment for one KEGG pathway, the biosynthesis of unsaturated fatty acids, which has been shown to have a role in thermoregulation in Drosophila (Suito et al, 2020).…”