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Physiological, metabolomic, and transcriptomic reveal metabolic pathway alterations in Gymnocypris przewalskii due to cold exposure

Teleost fish have evolved various adaptations that allow them to tolerate cold water conditions. However, the underlying mechanism of this adaptation is poorly understood in Tibetan Plateau fish. RNA-seq combined with liquid chromatography‒mass spectrometry (LC‒MS/MS) metabolomics was used to invest...

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Autores principales: Liu, Sijia, Tian, Fei, Qi, Delin, Qi, Hongfang, Wang, Yang, Xu, Shixiao, Zhao, Kai
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10500822/
https://www.ncbi.nlm.nih.gov/pubmed/37710165
http://dx.doi.org/10.1186/s12864-023-09587-9
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author Liu, Sijia
Tian, Fei
Qi, Delin
Qi, Hongfang
Wang, Yang
Xu, Shixiao
Zhao, Kai
author_facet Liu, Sijia
Tian, Fei
Qi, Delin
Qi, Hongfang
Wang, Yang
Xu, Shixiao
Zhao, Kai
author_sort Liu, Sijia
collection PubMed
description Teleost fish have evolved various adaptations that allow them to tolerate cold water conditions. However, the underlying mechanism of this adaptation is poorly understood in Tibetan Plateau fish. RNA-seq combined with liquid chromatography‒mass spectrometry (LC‒MS/MS) metabolomics was used to investigate the physiological responses of a Tibetan Plateau-specific teleost, Gymnocypris przewalskii, under cold conditions. The 8-month G. przewalskii juvenile fish were exposed to cold (4 ℃, cold acclimation, CA) and warm (17 ℃, normal temperature, NT) temperature water for 15 days. Then, the transcript profiles of eight tissues, including the brain, gill, heart, intestine, hepatopancreas, kidney, muscle, and skin, were evaluated by transcriptome sequencing. The metabolites of the intestine, hepatopancreas, and muscle were identified by LC‒MS/MS. A total of 5,745 differentially expressed genes (DEGs) were obtained in the CA group. The key DEGs were annotated using Gene Ontology and Kyoto Encyclopedia of Genes and Genomes analysis. The DEGs from the eight tissues were significantly enriched in spliceosome pathways, indicating that activated alternative splicing is a critical biological process that occurs in the tissues to help fish cope with cold stress. Additionally, 82, 97, and 66 differentially expressed metabolites were identified in the intestine, hepatopancreas, and muscle, respectively. Glutathione metabolism was the only overlapping significant pathway between the transcriptome and metabolome analyses in these three tissues, indicating that an activated antioxidative process was triggered during cold stress. In combination with the multitissue transcriptome and metabolome, we established a physiology-gene‒metabolite interaction network related to energy metabolism during cold stress and found that gluconeogenesis and long-chain fatty acid metabolism played critical roles in glucose homeostasis and energy supply. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09587-9.
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spelling pubmed-105008222023-09-15 Physiological, metabolomic, and transcriptomic reveal metabolic pathway alterations in Gymnocypris przewalskii due to cold exposure Liu, Sijia Tian, Fei Qi, Delin Qi, Hongfang Wang, Yang Xu, Shixiao Zhao, Kai BMC Genomics Research Teleost fish have evolved various adaptations that allow them to tolerate cold water conditions. However, the underlying mechanism of this adaptation is poorly understood in Tibetan Plateau fish. RNA-seq combined with liquid chromatography‒mass spectrometry (LC‒MS/MS) metabolomics was used to investigate the physiological responses of a Tibetan Plateau-specific teleost, Gymnocypris przewalskii, under cold conditions. The 8-month G. przewalskii juvenile fish were exposed to cold (4 ℃, cold acclimation, CA) and warm (17 ℃, normal temperature, NT) temperature water for 15 days. Then, the transcript profiles of eight tissues, including the brain, gill, heart, intestine, hepatopancreas, kidney, muscle, and skin, were evaluated by transcriptome sequencing. The metabolites of the intestine, hepatopancreas, and muscle were identified by LC‒MS/MS. A total of 5,745 differentially expressed genes (DEGs) were obtained in the CA group. The key DEGs were annotated using Gene Ontology and Kyoto Encyclopedia of Genes and Genomes analysis. The DEGs from the eight tissues were significantly enriched in spliceosome pathways, indicating that activated alternative splicing is a critical biological process that occurs in the tissues to help fish cope with cold stress. Additionally, 82, 97, and 66 differentially expressed metabolites were identified in the intestine, hepatopancreas, and muscle, respectively. Glutathione metabolism was the only overlapping significant pathway between the transcriptome and metabolome analyses in these three tissues, indicating that an activated antioxidative process was triggered during cold stress. In combination with the multitissue transcriptome and metabolome, we established a physiology-gene‒metabolite interaction network related to energy metabolism during cold stress and found that gluconeogenesis and long-chain fatty acid metabolism played critical roles in glucose homeostasis and energy supply. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09587-9. BioMed Central 2023-09-14 /pmc/articles/PMC10500822/ /pubmed/37710165 http://dx.doi.org/10.1186/s12864-023-09587-9 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Liu, Sijia
Tian, Fei
Qi, Delin
Qi, Hongfang
Wang, Yang
Xu, Shixiao
Zhao, Kai
Physiological, metabolomic, and transcriptomic reveal metabolic pathway alterations in Gymnocypris przewalskii due to cold exposure
title Physiological, metabolomic, and transcriptomic reveal metabolic pathway alterations in Gymnocypris przewalskii due to cold exposure
title_full Physiological, metabolomic, and transcriptomic reveal metabolic pathway alterations in Gymnocypris przewalskii due to cold exposure
title_fullStr Physiological, metabolomic, and transcriptomic reveal metabolic pathway alterations in Gymnocypris przewalskii due to cold exposure
title_full_unstemmed Physiological, metabolomic, and transcriptomic reveal metabolic pathway alterations in Gymnocypris przewalskii due to cold exposure
title_short Physiological, metabolomic, and transcriptomic reveal metabolic pathway alterations in Gymnocypris przewalskii due to cold exposure
title_sort physiological, metabolomic, and transcriptomic reveal metabolic pathway alterations in gymnocypris przewalskii due to cold exposure
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10500822/
https://www.ncbi.nlm.nih.gov/pubmed/37710165
http://dx.doi.org/10.1186/s12864-023-09587-9
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