Nicolas Pichaud , Hichem A. Menail , Kenechukwu C. Ojukwu , Pier Morin , Jantina Toxopeus
{"title":"在抗冻蟋蟀中,类似秋天的驯化改变了线粒体功能和底物的使用","authors":"Nicolas Pichaud , Hichem A. Menail , Kenechukwu C. Ojukwu , Pier Morin , Jantina Toxopeus","doi":"10.1016/j.jtherbio.2025.104253","DOIUrl":null,"url":null,"abstract":"<div><div>Acclimation to low temperatures in insects involves complex metabolic adjustments to ensure survival. Notably, cryoprotectants including glycerol, trehalose and proline can accumulate in insects to promote freeze tolerance. Interestingly, these metabolites can also be converted to metabolic fuels sustaining mitochondrial ATP production. This study investigates the metabolic shifts in the freeze-tolerant cricket <em>Gryllus veletis</em> during fall-like acclimation, focusing on mitochondrial function and its possible link with cryoprotectant accumulation. We hypothesized that fall-like acclimation promotes a shift in mitochondrial substrate utilization within the fat body tissue of crickets, transitioning from a reliance on substrates that donate electrons to complex I (e.g., carbohydrates and fatty acids) toward increased utilization of alternative substrates, such as glycerol-3-phosphate (G3P), which can be derived from glycerol. We demonstrated that acclimation leads to lower glycogen content in the fat body, concomitant with increased pyruvate kinase activity, suggesting increased carbon flux through glycolysis. Moreover, we observed decreased overall mitochondrial oxygen consumption and enzymatic activity of cytochrome <em>c</em> oxidase. Interestingly, while overall mitochondrial capacity decreased, the relative contribution of G3P to mitochondrial metabolism increased, supported by increased enzymatic activity of mitochondrial G3P dehydrogenase. Thus, fall-like acclimation appears to induce a metabolic shift in crickets, redirecting metabolites away from the tricarboxylic acid cycle and towards the production of G3P, which subsequently sustains mitochondrial respiration. This study reveals a key mechanism associated with the development of freeze tolerance in crickets, which could also be important for other cold- and freeze-tolerant insect species.</div></div>","PeriodicalId":17428,"journal":{"name":"Journal of thermal biology","volume":"132 ","pages":"Article 104253"},"PeriodicalIF":2.9000,"publicationDate":"2025-08-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Fall-like acclimation alters mitochondrial function and substrate use in freeze-tolerant crickets\",\"authors\":\"Nicolas Pichaud , Hichem A. Menail , Kenechukwu C. Ojukwu , Pier Morin , Jantina Toxopeus\",\"doi\":\"10.1016/j.jtherbio.2025.104253\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<div><div>Acclimation to low temperatures in insects involves complex metabolic adjustments to ensure survival. Notably, cryoprotectants including glycerol, trehalose and proline can accumulate in insects to promote freeze tolerance. Interestingly, these metabolites can also be converted to metabolic fuels sustaining mitochondrial ATP production. This study investigates the metabolic shifts in the freeze-tolerant cricket <em>Gryllus veletis</em> during fall-like acclimation, focusing on mitochondrial function and its possible link with cryoprotectant accumulation. We hypothesized that fall-like acclimation promotes a shift in mitochondrial substrate utilization within the fat body tissue of crickets, transitioning from a reliance on substrates that donate electrons to complex I (e.g., carbohydrates and fatty acids) toward increased utilization of alternative substrates, such as glycerol-3-phosphate (G3P), which can be derived from glycerol. We demonstrated that acclimation leads to lower glycogen content in the fat body, concomitant with increased pyruvate kinase activity, suggesting increased carbon flux through glycolysis. Moreover, we observed decreased overall mitochondrial oxygen consumption and enzymatic activity of cytochrome <em>c</em> oxidase. Interestingly, while overall mitochondrial capacity decreased, the relative contribution of G3P to mitochondrial metabolism increased, supported by increased enzymatic activity of mitochondrial G3P dehydrogenase. Thus, fall-like acclimation appears to induce a metabolic shift in crickets, redirecting metabolites away from the tricarboxylic acid cycle and towards the production of G3P, which subsequently sustains mitochondrial respiration. This study reveals a key mechanism associated with the development of freeze tolerance in crickets, which could also be important for other cold- and freeze-tolerant insect species.</div></div>\",\"PeriodicalId\":17428,\"journal\":{\"name\":\"Journal of thermal biology\",\"volume\":\"132 \",\"pages\":\"Article 104253\"},\"PeriodicalIF\":2.9000,\"publicationDate\":\"2025-08-01\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Journal of thermal biology\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://www.sciencedirect.com/science/article/pii/S0306456525002104\",\"RegionNum\":2,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of thermal biology","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0306456525002104","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"BIOLOGY","Score":null,"Total":0}
Fall-like acclimation alters mitochondrial function and substrate use in freeze-tolerant crickets
Acclimation to low temperatures in insects involves complex metabolic adjustments to ensure survival. Notably, cryoprotectants including glycerol, trehalose and proline can accumulate in insects to promote freeze tolerance. Interestingly, these metabolites can also be converted to metabolic fuels sustaining mitochondrial ATP production. This study investigates the metabolic shifts in the freeze-tolerant cricket Gryllus veletis during fall-like acclimation, focusing on mitochondrial function and its possible link with cryoprotectant accumulation. We hypothesized that fall-like acclimation promotes a shift in mitochondrial substrate utilization within the fat body tissue of crickets, transitioning from a reliance on substrates that donate electrons to complex I (e.g., carbohydrates and fatty acids) toward increased utilization of alternative substrates, such as glycerol-3-phosphate (G3P), which can be derived from glycerol. We demonstrated that acclimation leads to lower glycogen content in the fat body, concomitant with increased pyruvate kinase activity, suggesting increased carbon flux through glycolysis. Moreover, we observed decreased overall mitochondrial oxygen consumption and enzymatic activity of cytochrome c oxidase. Interestingly, while overall mitochondrial capacity decreased, the relative contribution of G3P to mitochondrial metabolism increased, supported by increased enzymatic activity of mitochondrial G3P dehydrogenase. Thus, fall-like acclimation appears to induce a metabolic shift in crickets, redirecting metabolites away from the tricarboxylic acid cycle and towards the production of G3P, which subsequently sustains mitochondrial respiration. This study reveals a key mechanism associated with the development of freeze tolerance in crickets, which could also be important for other cold- and freeze-tolerant insect species.
期刊介绍:
The Journal of Thermal Biology publishes articles that advance our knowledge on the ways and mechanisms through which temperature affects man and animals. This includes studies of their responses to these effects and on the ecological consequences. Directly relevant to this theme are:
• The mechanisms of thermal limitation, heat and cold injury, and the resistance of organisms to extremes of temperature
• The mechanisms involved in acclimation, acclimatization and evolutionary adaptation to temperature
• Mechanisms underlying the patterns of hibernation, torpor, dormancy, aestivation and diapause
• Effects of temperature on reproduction and development, growth, ageing and life-span
• Studies on modelling heat transfer between organisms and their environment
• The contributions of temperature to effects of climate change on animal species and man
• Studies of conservation biology and physiology related to temperature
• Behavioural and physiological regulation of body temperature including its pathophysiology and fever
• Medical applications of hypo- and hyperthermia
Article types:
• Original articles
• Review articles