Lipids and Trehalose Actively Cooperate in Heat Stress Management of Schizosaccharomyces pombe
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-...
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| Veröffentlicht in: | International journal of molecular sciences 2021-12, Vol.22 (24), p.13272 |
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| creator | Péter, Mária Gudmann, Péter Kóta, Zoltán Török, Zsolt Vígh, László Glatz, Attila Balogh, Gábor |
| description | 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
mutants which are unable to synthesize (
) or degrade (
) 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. |
| doi_str_mv | 10.3390/ijms222413272 |
| format | Article |
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mutants which are unable to synthesize (
) or degrade (
) 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.</description><identifier>ISSN: 1422-0067</identifier><identifier>ISSN: 1661-6596</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms222413272</identifier><identifier>PMID: 34948069</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>Cell cycle ; Cell membranes ; Crosstalk ; Enzymes ; Glucose ; Glucosyltransferases - genetics ; Glucosyltransferases - metabolism ; Heat ; Heat stress ; Homeostasis ; Hot Temperature ; Lipidomics - methods ; Lipids ; Mass Spectrometry ; Mass spectroscopy ; Metabolism ; Metabolites ; Mutation ; Oleic acid ; Oleic Acid - metabolism ; Phosphoric Monoester Hydrolases - genetics ; Phosphoric Monoester Hydrolases - metabolism ; Physicochemical properties ; Proteins ; Schizosaccharomyces - genetics ; Schizosaccharomyces - growth & development ; Schizosaccharomyces - metabolism ; Schizosaccharomyces pombe ; Schizosaccharomyces pombe Proteins - genetics ; Schizosaccharomyces pombe Proteins - metabolism ; Scientific imaging ; Sensors ; Stearic acid ; Trehalose ; Trehalose - metabolism ; Triglycerides ; Triglycerides - metabolism ; Yeast</subject><ispartof>International journal of molecular sciences, 2021-12, Vol.22 (24), p.13272</ispartof><rights>2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 by the authors. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c415t-c18f280caf71cb62fb3e7b37843dd81e0f0f3e3dee5f6fce3f4629743945ad93</citedby><cites>FETCH-LOGICAL-c415t-c18f280caf71cb62fb3e7b37843dd81e0f0f3e3dee5f6fce3f4629743945ad93</cites><orcidid>0000-0003-0362-6933 ; 0000-0002-4565-6850 ; 0000-0003-0836-3247</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8707580/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8707580/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34948069$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Péter, Mária</creatorcontrib><creatorcontrib>Gudmann, Péter</creatorcontrib><creatorcontrib>Kóta, Zoltán</creatorcontrib><creatorcontrib>Török, Zsolt</creatorcontrib><creatorcontrib>Vígh, László</creatorcontrib><creatorcontrib>Glatz, Attila</creatorcontrib><creatorcontrib>Balogh, Gábor</creatorcontrib><title>Lipids and Trehalose Actively Cooperate in Heat Stress Management of Schizosaccharomyces pombe</title><title>International journal of molecular sciences</title><addtitle>Int J Mol Sci</addtitle><description>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
mutants which are unable to synthesize (
) or degrade (
) 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. 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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
mutants which are unable to synthesize (
) or degrade (
) 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.</abstract><cop>Switzerland</cop><pub>MDPI AG</pub><pmid>34948069</pmid><doi>10.3390/ijms222413272</doi><orcidid>https://orcid.org/0000-0003-0362-6933</orcidid><orcidid>https://orcid.org/0000-0002-4565-6850</orcidid><orcidid>https://orcid.org/0000-0003-0836-3247</orcidid><oa>free_for_read</oa></addata></record> |
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| source | MDPI - Multidisciplinary Digital Publishing Institute; MEDLINE; EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | Cell cycle Cell membranes Crosstalk Enzymes Glucose Glucosyltransferases - genetics Glucosyltransferases - metabolism Heat Heat stress Homeostasis Hot Temperature Lipidomics - methods Lipids Mass Spectrometry Mass spectroscopy Metabolism Metabolites Mutation Oleic acid Oleic Acid - metabolism Phosphoric Monoester Hydrolases - genetics Phosphoric Monoester Hydrolases - metabolism Physicochemical properties Proteins Schizosaccharomyces - genetics Schizosaccharomyces - growth & development Schizosaccharomyces - metabolism Schizosaccharomyces pombe Schizosaccharomyces pombe Proteins - genetics Schizosaccharomyces pombe Proteins - metabolism Scientific imaging Sensors Stearic acid Trehalose Trehalose - metabolism Triglycerides Triglycerides - metabolism Yeast |
| title | Lipids and Trehalose Actively Cooperate in Heat Stress Management of Schizosaccharomyces pombe |
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