Biochemical, Histological, and Multi-Omics Analyses Reveal the Molecular and Metabolic Mechanisms of Cold Stress Response in the Chinese Soft-Shelled Turtle (<i>Pelodiscus sinensis</i>)

The Chinese soft-shelled turtle (<i>Pelodiscus sinensis</i>), a type of warm-water reptile, is frequently chosen as the model animal to understand how organisms respond to environmental stressors. However, the responsive mechanism of <i>P. sinensis</i> to natural cold stress...

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Main Authors: Liqin Ji, Qing Shi, Chen Chen, Xiaoli Liu, Junxian Zhu, Xiaoyou Hong, Chengqing Wei, Xinping Zhu, Wei Li
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Language:English
Published: MDPI AG 2025-01-01
Series:Biology
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Online Access:https://www.mdpi.com/2079-7737/14/1/55
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author Liqin Ji
Qing Shi
Chen Chen
Xiaoli Liu
Junxian Zhu
Xiaoyou Hong
Chengqing Wei
Xinping Zhu
Wei Li
author_facet Liqin Ji
Qing Shi
Chen Chen
Xiaoli Liu
Junxian Zhu
Xiaoyou Hong
Chengqing Wei
Xinping Zhu
Wei Li
author_sort Liqin Ji
collection DOAJ
description The Chinese soft-shelled turtle (<i>Pelodiscus sinensis</i>), a type of warm-water reptile, is frequently chosen as the model animal to understand how organisms respond to environmental stressors. However, the responsive mechanism of <i>P. sinensis</i> to natural cold stress is unclear, especially in terms of metabolic pattern and molecular pathways. Herein, plasma biochemical, hepatic morphological, apoptotic, transcriptomic, and metabolomic detection methods were performed to investigate the response of <i>P. sinensis</i> to acute cold stress. A consistent increase in plasma AST and ALT activities with a decline in ALP activity was found following 14 °C and 7 °C cold stress compared with the control group. Plasma GLU, TG, CHO, and HDL contents, reflecting energy metabolism, were decreased to lower levels from 2 to 16 days post cold stress (dps). Histological and TUNEL detection in the liver demonstrated that the 14 °C and 7 °C cold stress caused severe morphological damage and cell apoptosis in a time-dependent manner. DEGs in the biosynthesis of fatty acids (<i>Acsbg2, Acsl3, Acsl4, Acsl5, Mcat,</i> and <i>Acacb</i>), as well as unsaturated fatty acids (<i>Hsd17b12</i>, <i>Elovl7</i>, <i>Scd</i>, and <i>Baat</i>), starch and sucrose metabolism (<i>Pgm1</i>, <i>Pgm2</i>, and <i>Treh</i>), and apoptosis (<i>Ddit3</i>, <i>Gadd45a</i>, <i>Lmnb1</i>, <i>Tuba1c</i>, <i>Tnf</i>, <i>Tnfsf10</i>, <i>Fos</i>, <i>Itpr1</i>, and <i>Ctso</i>) were discovered in the transcriptome under cold stress. The metabolomic data showed that metabolites, including chenodeoxycholic acid, oleoylethanolamide, uric acid, fructose 1,6-bisphosphate, CMP, and S-(Hydroxymethyl)-glutathione, were remarkably altered in the cold stress groups. Combined transcriptomic and metabolomic data revealed that pyrimidine metabolism, amino acid metabolism, and pyruvate metabolism were the most significant pathways regulated by the low-temperature exposure. Overall, this work suggests that 14 °C and 7 °C cold stress could induce obvious morphological damage and apoptosis in the liver at 4 dps. Moreover, energy metabolism and amino acid metabolism were the main signaling pathways in response to cold stress for <i>P. sinensis</i>.
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spelling doaj-art-fcd71ecb5ca84e94ab526718067d7c8b2025-01-24T13:23:27ZengMDPI AGBiology2079-77372025-01-011415510.3390/biology14010055Biochemical, Histological, and Multi-Omics Analyses Reveal the Molecular and Metabolic Mechanisms of Cold Stress Response in the Chinese Soft-Shelled Turtle (<i>Pelodiscus sinensis</i>)Liqin Ji0Qing Shi1Chen Chen2Xiaoli Liu3Junxian Zhu4Xiaoyou Hong5Chengqing Wei6Xinping Zhu7Wei Li8Key Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510380, ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510380, ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510380, ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510380, ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510380, ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510380, ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510380, ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510380, ChinaKey Laboratory of Tropical and Subtropical Fishery Resources Application and Cultivation, Ministry of Agriculture and Rural Affairs, Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510380, ChinaThe Chinese soft-shelled turtle (<i>Pelodiscus sinensis</i>), a type of warm-water reptile, is frequently chosen as the model animal to understand how organisms respond to environmental stressors. However, the responsive mechanism of <i>P. sinensis</i> to natural cold stress is unclear, especially in terms of metabolic pattern and molecular pathways. Herein, plasma biochemical, hepatic morphological, apoptotic, transcriptomic, and metabolomic detection methods were performed to investigate the response of <i>P. sinensis</i> to acute cold stress. A consistent increase in plasma AST and ALT activities with a decline in ALP activity was found following 14 °C and 7 °C cold stress compared with the control group. Plasma GLU, TG, CHO, and HDL contents, reflecting energy metabolism, were decreased to lower levels from 2 to 16 days post cold stress (dps). Histological and TUNEL detection in the liver demonstrated that the 14 °C and 7 °C cold stress caused severe morphological damage and cell apoptosis in a time-dependent manner. DEGs in the biosynthesis of fatty acids (<i>Acsbg2, Acsl3, Acsl4, Acsl5, Mcat,</i> and <i>Acacb</i>), as well as unsaturated fatty acids (<i>Hsd17b12</i>, <i>Elovl7</i>, <i>Scd</i>, and <i>Baat</i>), starch and sucrose metabolism (<i>Pgm1</i>, <i>Pgm2</i>, and <i>Treh</i>), and apoptosis (<i>Ddit3</i>, <i>Gadd45a</i>, <i>Lmnb1</i>, <i>Tuba1c</i>, <i>Tnf</i>, <i>Tnfsf10</i>, <i>Fos</i>, <i>Itpr1</i>, and <i>Ctso</i>) were discovered in the transcriptome under cold stress. The metabolomic data showed that metabolites, including chenodeoxycholic acid, oleoylethanolamide, uric acid, fructose 1,6-bisphosphate, CMP, and S-(Hydroxymethyl)-glutathione, were remarkably altered in the cold stress groups. Combined transcriptomic and metabolomic data revealed that pyrimidine metabolism, amino acid metabolism, and pyruvate metabolism were the most significant pathways regulated by the low-temperature exposure. Overall, this work suggests that 14 °C and 7 °C cold stress could induce obvious morphological damage and apoptosis in the liver at 4 dps. Moreover, energy metabolism and amino acid metabolism were the main signaling pathways in response to cold stress for <i>P. sinensis</i>.https://www.mdpi.com/2079-7737/14/1/55Chinese soft-shelled turtlecold stressapoptosismorphologytranscriptomemetabolism
spellingShingle Liqin Ji
Qing Shi
Chen Chen
Xiaoli Liu
Junxian Zhu
Xiaoyou Hong
Chengqing Wei
Xinping Zhu
Wei Li
Biochemical, Histological, and Multi-Omics Analyses Reveal the Molecular and Metabolic Mechanisms of Cold Stress Response in the Chinese Soft-Shelled Turtle (<i>Pelodiscus sinensis</i>)
Biology
Chinese soft-shelled turtle
cold stress
apoptosis
morphology
transcriptome
metabolism
title Biochemical, Histological, and Multi-Omics Analyses Reveal the Molecular and Metabolic Mechanisms of Cold Stress Response in the Chinese Soft-Shelled Turtle (<i>Pelodiscus sinensis</i>)
title_full Biochemical, Histological, and Multi-Omics Analyses Reveal the Molecular and Metabolic Mechanisms of Cold Stress Response in the Chinese Soft-Shelled Turtle (<i>Pelodiscus sinensis</i>)
title_fullStr Biochemical, Histological, and Multi-Omics Analyses Reveal the Molecular and Metabolic Mechanisms of Cold Stress Response in the Chinese Soft-Shelled Turtle (<i>Pelodiscus sinensis</i>)
title_full_unstemmed Biochemical, Histological, and Multi-Omics Analyses Reveal the Molecular and Metabolic Mechanisms of Cold Stress Response in the Chinese Soft-Shelled Turtle (<i>Pelodiscus sinensis</i>)
title_short Biochemical, Histological, and Multi-Omics Analyses Reveal the Molecular and Metabolic Mechanisms of Cold Stress Response in the Chinese Soft-Shelled Turtle (<i>Pelodiscus sinensis</i>)
title_sort biochemical histological and multi omics analyses reveal the molecular and metabolic mechanisms of cold stress response in the chinese soft shelled turtle i pelodiscus sinensis i
topic Chinese soft-shelled turtle
cold stress
apoptosis
morphology
transcriptome
metabolism
url https://www.mdpi.com/2079-7737/14/1/55
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