Lipids and Trehalose Actively Cooperate in Heat Stress Management of Schizosaccharomyces pombe

Mária Péter,Attila Glatz,László Vígh,Zoltán Kóta,Gábor Balogh,Péter Gudmann,Zsolt Török

doi:10.3390/ijms222413272

Abstract

Homeostatic maintenance of the physicochemical properties of cellular membranes is essential for life. In yeast, trehalose accumulation and lipid remodeling enable rapid adaptation to perturbations, but their crosstalk was not investigated. Here we report about the first in-depth, mass spectrometry-based lipidomic analysis on heat-stressed Schizosaccharomyces pombe mutants which are unable to synthesize (tps1Δ) or degrade (ntp1Δ) trehalose. Our experiments provide data about the role of trehalose as a membrane protectant in heat stress. We show that under conditions of trehalose deficiency, heat stress induced a comprehensive, distinctively high-degree lipidome reshaping in which structural, signaling and storage lipids acted in concert. In the absence of trehalose, membrane lipid remodeling was more pronounced and increased with increasing stress dose. It could be characterized by decreasing unsaturation and increasing acyl chain length, and required de novo synthesis of stearic acid (18:0) and very long-chain fatty acids to serve membrane rigidification. In addition, we detected enhanced and sustained signaling lipid generation to ensure transient cell cycle arrest as well as more intense triglyceride synthesis to accommodate membrane lipid-derived oleic acid (18:1) and newly synthesized but unused fatty acids. We also demonstrate that these changes were able to partially substitute for the missing role of trehalose and conferred measurable stress tolerance to fission yeast cells.

Highlights

Abrupt temperature fluctuations are able to disturb cellular homeostasis and cause deleterious effects on cellular infrastructure
IPC and DG are known to have versatile signaling properties, all affecting cell growth and viability [42,45,54,55]. We propose that both the defect in membrane protection due to inability to produce trehalose and the defect in membrane remodeling capability due to inability to produce TG [11] contributed to the same physiological outcome, i.e., the transient cell cycle arrest observed upon heat shock (HS) could allow time for cells to recover under suboptimal conditions
We showed that in the absence of trehalose, HS induced a comprehensive, distinctively high-degree lipidome reshaping in which structural, signaling and storage lipids acted in concert, and were able to substitute for the protective role of trehalose at a sizeable extent

Summary

Introduction

Abrupt temperature fluctuations are able to disturb cellular homeostasis and cause deleterious effects on cellular infrastructure. Cellular membranes are the primary sensors to such insults and they represent the most thermally sensitive macromolecular structures [1,2,3]. Disturbances in membrane homeostasis are linked to a number of human diseases, like diabetes or metabolic syndrome. The homeostatic maintenance of the membrane physicochemical state is of utmost importance. The heat stress response (HSR) is a universal defense mechanism to reestablish homeostasis. In the era of global warming, the understanding of HSR is more necessary than ever before for both health [4] and economic reasons

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Discussion

Conclusion