title: Uncovering the benefits of fluctuating thermal regimes on cold tolerance of drosophila flies by combined metabolomic and lipidomic approach.
abstract: When exposed to constant low temperatures (CLTs), insects often suffer from cumulative physiological injuries that can severely compromise their fitness and survival. Yet, mortality can be considerably lowered when the cold stress period is interrupted by periodic warm interruption(s), referred to as fluctuating thermal regimes, FTRs. In this study, we have shown that FTRs strongly promoted cold tolerance of Drosophila melanogaster adults. We then assessed whether this marked phenotypic shift was associated with detectable physiological changes, such as synthesis of cryoprotectants and/or membrane remodeling. To test these hypotheses, we conducted two different time-series Omics analyzes in adult flies submitted to CLTs vs. FTRs: metabolomics (GC/MS) and lipidomics (LC/ESI/MS) targeting membrane phospholipids. We observed increasing levels in several polyhydric alcohols (arabitol, erythritol, sorbitol, mannitol, glycerol), sugars (fructose, mannose) and amino acids (serine, alanine, glutamine) in flies under CLT. Prolonged exposure to low temperature was also associated with a marked deviation of metabolic homeostasis and warm interruptions as short as 2h were sufficient to periodically return the metabolic system to functionality. Lipidomics revealed an increased relative proportion of phosphatidylethanolamines and a shortening of fatty acyl chains in flies exposed to cold, likely to compensate for the ordering effect of low temperature on membranes. We found a remarkable correspondence in the time-course of changes between the metabolic and phospholipids networks, both suggesting a fast homeostatic regeneration during warm intervals under FTRs. In consequence, we suggest that periodic opportunities to restore system-wide homeostasis contribute to promote cold tolerance under FTRs.
authors.affiliation: Université de Rennes 1, UMR CNRS 6553 ECOBIO, 263 avenue du Général-Leclerc, 35042, Rennes, France. Electronic address: herve.colinet@univ-rennes1.fr.
authors.forename: Hervé
authors.initials: H
authors.lastname: Colinet
authors.affiliation: Université de Rennes 1, UMR CNRS 6553 ECOBIO, 263 avenue du Général-Leclerc, 35042, Rennes, France.
authors.forename: David
authors.initials: D
authors.lastname: Renault
authors.affiliation: URZF, INRA, 45075, Orléans, France.
authors.forename: Marion
authors.initials: M
authors.lastname: Javal
authors.affiliation: Institute of Entomology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05, České Budějovice, Czech Republic.
authors.forename: Petra
authors.initials: P
authors.lastname: Berková
authors.affiliation: Institute of Entomology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05, České Budějovice, Czech Republic.
authors.forename: Petr
authors.initials: P
authors.lastname: Šimek
authors.affiliation: Institute of Entomology, Biology Centre of the Czech Academy of Sciences, Branišovská 31, 370 05, České Budějovice, Czech Republic.
authors.forename: Vladimír
authors.initials: V
authors.lastname: Koštál
mesh_terms: D000222:Adaptation, Physiological; D000818:Animals; D003080:Cold Temperature; D004331:Drosophila melanogaster / Q000378:metabolism*; D005260:Female; D008401:Gas Chromatography-Mass Spectrometry; D016014:Linear Models; D050356:Lipid Metabolism; D055432:Metabolomics / Q000379:methods*; D010743:Phospholipids / Q000378:metabolism; D025341:Principal Component Analysis; D011336:Probability; D021241:Spectrometry, Mass, Electrospray Ionization
chemical_list: D010743:Phospholipids
keywords: Cold stress; Drosophila; Omics; fluctuating thermal regimes; recovery