Fat Body Metabolome Revealed Glutamine Metabolism Pathway Involved in Prepupal <i>Apis mellifera</i> Responding to Cold Stress

Thermal condition affects the development and growth of ectotherms. The stenothermic honeybee brood, particularly the prepupae, are sensitive to low rearing temperature. The fat body plays important roles in energy reserve and metabolism during the honeybee brood development. To date, the fat body m...

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Main Authors: Xinjian Xu, Mingjie Cao, Chenyu Zhu, Lingqing Mo, Huajiao Huang, Jiaying Xie, Bingfeng Zhou, Shujing Zhou, Xiangjie Zhu
Format: Article
Language:English
Published: MDPI AG 2025-01-01
Series:Insects
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Online Access:https://www.mdpi.com/2075-4450/16/1/37
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author Xinjian Xu
Mingjie Cao
Chenyu Zhu
Lingqing Mo
Huajiao Huang
Jiaying Xie
Bingfeng Zhou
Shujing Zhou
Xiangjie Zhu
author_facet Xinjian Xu
Mingjie Cao
Chenyu Zhu
Lingqing Mo
Huajiao Huang
Jiaying Xie
Bingfeng Zhou
Shujing Zhou
Xiangjie Zhu
author_sort Xinjian Xu
collection DOAJ
description Thermal condition affects the development and growth of ectotherms. The stenothermic honeybee brood, particularly the prepupae, are sensitive to low rearing temperature. The fat body plays important roles in energy reserve and metabolism during the honeybee brood development. To date, the fat body metabolic changes in prepupae responding to cold stress have not been completely understood. In this study, the ultra-performance liquid chromatography coupled with tandem mass spectrometry (UPLC-MS/MS)-based non-target metabolome was analyzed between the cold-treated (CT, 20 °C, 36 h) and control (CK, 35 °C) fat body in prepupal honeybees. The fat body metabolomic data showed that the levels of 1860 and 254 metabolites were significantly increased and decreased, respectively, in cold-stressed prepupae. These altered metabolites, glutamine, glutamic acid, pyroglutamic acid, and oxidized glutathione, were significantly enriched into glutamine metabolism and glutathione metabolism pathways. Furthermore, the expression levels of glutamine metabolism-related genes, <i>glutaminase</i> (<i>GLS</i>), <i>glutamate dehydrogenase</i> (<i>GDH</i>), and <i>gamma-glutamyl transferase</i> (<i>GGT-1</i> and <i>GGT-7</i>), were significantly decreased in cold-exposed prepupae compared with the control groups. Meanwhile, the oxidized glutathione (GSSG), but not the reduced glutathione (GSH) content, was increased in the cold-exposed group compared with controls. Collectively, our data revealed the fat body metabolomic changes in larva-to-pupa transition when exposed to cold stress. Our data provided new insights into stenothermic honeybee sensitivity to cold, characterized by perturbation of glutamine metabolism and oxidative stress.
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spelling doaj-art-bf6596e61a4c4099a5d2fee2f03538992025-01-24T13:35:40ZengMDPI AGInsects2075-44502025-01-011613710.3390/insects16010037Fat Body Metabolome Revealed Glutamine Metabolism Pathway Involved in Prepupal <i>Apis mellifera</i> Responding to Cold StressXinjian Xu0Mingjie Cao1Chenyu Zhu2Lingqing Mo3Huajiao Huang4Jiaying Xie5Bingfeng Zhou6Shujing Zhou7Xiangjie Zhu8College of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaThermal condition affects the development and growth of ectotherms. The stenothermic honeybee brood, particularly the prepupae, are sensitive to low rearing temperature. The fat body plays important roles in energy reserve and metabolism during the honeybee brood development. To date, the fat body metabolic changes in prepupae responding to cold stress have not been completely understood. In this study, the ultra-performance liquid chromatography coupled with tandem mass spectrometry (UPLC-MS/MS)-based non-target metabolome was analyzed between the cold-treated (CT, 20 °C, 36 h) and control (CK, 35 °C) fat body in prepupal honeybees. The fat body metabolomic data showed that the levels of 1860 and 254 metabolites were significantly increased and decreased, respectively, in cold-stressed prepupae. These altered metabolites, glutamine, glutamic acid, pyroglutamic acid, and oxidized glutathione, were significantly enriched into glutamine metabolism and glutathione metabolism pathways. Furthermore, the expression levels of glutamine metabolism-related genes, <i>glutaminase</i> (<i>GLS</i>), <i>glutamate dehydrogenase</i> (<i>GDH</i>), and <i>gamma-glutamyl transferase</i> (<i>GGT-1</i> and <i>GGT-7</i>), were significantly decreased in cold-exposed prepupae compared with the control groups. Meanwhile, the oxidized glutathione (GSSG), but not the reduced glutathione (GSH) content, was increased in the cold-exposed group compared with controls. Collectively, our data revealed the fat body metabolomic changes in larva-to-pupa transition when exposed to cold stress. Our data provided new insights into stenothermic honeybee sensitivity to cold, characterized by perturbation of glutamine metabolism and oxidative stress.https://www.mdpi.com/2075-4450/16/1/37honeybeesfat bodymetabolomicsoxidative stresscold stress
spellingShingle Xinjian Xu
Mingjie Cao
Chenyu Zhu
Lingqing Mo
Huajiao Huang
Jiaying Xie
Bingfeng Zhou
Shujing Zhou
Xiangjie Zhu
Fat Body Metabolome Revealed Glutamine Metabolism Pathway Involved in Prepupal <i>Apis mellifera</i> Responding to Cold Stress
Insects
honeybees
fat body
metabolomics
oxidative stress
cold stress
title Fat Body Metabolome Revealed Glutamine Metabolism Pathway Involved in Prepupal <i>Apis mellifera</i> Responding to Cold Stress
title_full Fat Body Metabolome Revealed Glutamine Metabolism Pathway Involved in Prepupal <i>Apis mellifera</i> Responding to Cold Stress
title_fullStr Fat Body Metabolome Revealed Glutamine Metabolism Pathway Involved in Prepupal <i>Apis mellifera</i> Responding to Cold Stress
title_full_unstemmed Fat Body Metabolome Revealed Glutamine Metabolism Pathway Involved in Prepupal <i>Apis mellifera</i> Responding to Cold Stress
title_short Fat Body Metabolome Revealed Glutamine Metabolism Pathway Involved in Prepupal <i>Apis mellifera</i> Responding to Cold Stress
title_sort fat body metabolome revealed glutamine metabolism pathway involved in prepupal i apis mellifera i responding to cold stress
topic honeybees
fat body
metabolomics
oxidative stress
cold stress
url https://www.mdpi.com/2075-4450/16/1/37
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