Integrated Transcriptomics and Metabolomics Reveal Changes in Cell Homeostasis and Energy Metabolism in <i>Trachinotus ovatus</i> in Response to Acute Hypoxic Stress
<i>Trachinotus ovatus</i> is an economically important mariculture fish, and hypoxia has become a critical threat to this hypoxia-sensitive species. However, the molecular adaptation mechanism of <i>T. ovatus</i> liver to hypoxia remains unclear. In this study, we investigate...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2024-01-01
|
| Series: | International Journal of Molecular Sciences |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1422-0067/25/2/1054 |
| _version_ | 1797339814237831168 |
|---|---|
| author | Qing-Hua Wang Ren-Xie Wu Jiao-Na Ji Jing Zhang Su-Fang Niu Bao-Gui Tang Ben-Ben Miao Zhen-Bang Liang |
| author_facet | Qing-Hua Wang Ren-Xie Wu Jiao-Na Ji Jing Zhang Su-Fang Niu Bao-Gui Tang Ben-Ben Miao Zhen-Bang Liang |
| author_sort | Qing-Hua Wang |
| collection | DOAJ |
| description | <i>Trachinotus ovatus</i> is an economically important mariculture fish, and hypoxia has become a critical threat to this hypoxia-sensitive species. However, the molecular adaptation mechanism of <i>T. ovatus</i> liver to hypoxia remains unclear. In this study, we investigated the effects of acute hypoxic stress (1.5 ± 0.1 mg·L<sup>−1</sup> for 6 h) and re-oxygenation (5.8 ± 0.3 mg·L<sup>−1</sup> for 12 h) in <i>T. ovatus</i> liver at both the transcriptomic and metabolic levels to elucidate hypoxia adaptation mechanism. Integrated transcriptomics and metabolomics analyses identified 36 genes and seven metabolites as key molecules that were highly related to signal transduction, cell growth and death, carbohydrate metabolism, amino acid metabolism, and lipid metabolism, and all played key roles in hypoxia adaptation. Of these, the hub genes <i>FOS</i> and <i>JUN</i> were pivotal hypoxia adaptation biomarkers for regulating cell growth and death. During hypoxia, up-regulation of <i>GADD45B</i> and <i>CDKN1A</i> genes induced cell cycle arrest. Enhancing intrinsic and extrinsic pathways in combination with glutathione metabolism triggered apoptosis; meanwhile, anti-apoptosis mechanism was activated after hypoxia. Expression of genes related to glycolysis, gluconeogenesis, amino acid metabolism, fat mobilization, and fatty acid biosynthesis were up-regulated after acute hypoxic stress, promoting energy supply. After re-oxygenation for 12 h, continuous apoptosis favored cellular function and tissue repair. Shifting from anaerobic metabolism (glycolysis) during hypoxia to aerobic metabolism (fatty acid β-oxidation and TCA cycle) after re-oxygenation was an important energy metabolism adaptation mechanism. Hypoxia 6 h was a critical period for metabolism alteration and cellular homeostasis, and re-oxygenation intervention should be implemented in a timely way. This study thoroughly examined the molecular response mechanism of <i>T. ovatus</i> under acute hypoxic stress, which contributes to the molecular breeding of hypoxia-tolerant cultivars. |
| first_indexed | 2024-03-08T09:52:53Z |
| format | Article |
| id | doaj.art-6fad1bcd88964f5ea1465c6d640c475f |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-08T09:52:53Z |
| publishDate | 2024-01-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-6fad1bcd88964f5ea1465c6d640c475f2024-01-29T13:56:38ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672024-01-01252105410.3390/ijms25021054Integrated Transcriptomics and Metabolomics Reveal Changes in Cell Homeostasis and Energy Metabolism in <i>Trachinotus ovatus</i> in Response to Acute Hypoxic StressQing-Hua Wang0Ren-Xie Wu1Jiao-Na Ji2Jing Zhang3Su-Fang Niu4Bao-Gui Tang5Ben-Ben Miao6Zhen-Bang Liang7College of Fisheries, Guangdong Ocean University, Zhanjiang 524088, ChinaCollege of Fisheries, Guangdong Ocean University, Zhanjiang 524088, ChinaCollege of Fisheries, Guangdong Ocean University, Zhanjiang 524088, ChinaCollege of Fisheries, Guangdong Ocean University, Zhanjiang 524088, ChinaCollege of Fisheries, Guangdong Ocean University, Zhanjiang 524088, ChinaCollege of Fisheries, Guangdong Ocean University, Zhanjiang 524088, ChinaCollege of Fisheries, Guangdong Ocean University, Zhanjiang 524088, ChinaCollege of Fisheries, Guangdong Ocean University, Zhanjiang 524088, China<i>Trachinotus ovatus</i> is an economically important mariculture fish, and hypoxia has become a critical threat to this hypoxia-sensitive species. However, the molecular adaptation mechanism of <i>T. ovatus</i> liver to hypoxia remains unclear. In this study, we investigated the effects of acute hypoxic stress (1.5 ± 0.1 mg·L<sup>−1</sup> for 6 h) and re-oxygenation (5.8 ± 0.3 mg·L<sup>−1</sup> for 12 h) in <i>T. ovatus</i> liver at both the transcriptomic and metabolic levels to elucidate hypoxia adaptation mechanism. Integrated transcriptomics and metabolomics analyses identified 36 genes and seven metabolites as key molecules that were highly related to signal transduction, cell growth and death, carbohydrate metabolism, amino acid metabolism, and lipid metabolism, and all played key roles in hypoxia adaptation. Of these, the hub genes <i>FOS</i> and <i>JUN</i> were pivotal hypoxia adaptation biomarkers for regulating cell growth and death. During hypoxia, up-regulation of <i>GADD45B</i> and <i>CDKN1A</i> genes induced cell cycle arrest. Enhancing intrinsic and extrinsic pathways in combination with glutathione metabolism triggered apoptosis; meanwhile, anti-apoptosis mechanism was activated after hypoxia. Expression of genes related to glycolysis, gluconeogenesis, amino acid metabolism, fat mobilization, and fatty acid biosynthesis were up-regulated after acute hypoxic stress, promoting energy supply. After re-oxygenation for 12 h, continuous apoptosis favored cellular function and tissue repair. Shifting from anaerobic metabolism (glycolysis) during hypoxia to aerobic metabolism (fatty acid β-oxidation and TCA cycle) after re-oxygenation was an important energy metabolism adaptation mechanism. Hypoxia 6 h was a critical period for metabolism alteration and cellular homeostasis, and re-oxygenation intervention should be implemented in a timely way. This study thoroughly examined the molecular response mechanism of <i>T. ovatus</i> under acute hypoxic stress, which contributes to the molecular breeding of hypoxia-tolerant cultivars.https://www.mdpi.com/1422-0067/25/2/1054<i>Trachinotus ovatus</i>acute hypoxic stresstranscriptomicsmetabolomicscell cycle arrestpro-apoptosis |
| spellingShingle | Qing-Hua Wang Ren-Xie Wu Jiao-Na Ji Jing Zhang Su-Fang Niu Bao-Gui Tang Ben-Ben Miao Zhen-Bang Liang Integrated Transcriptomics and Metabolomics Reveal Changes in Cell Homeostasis and Energy Metabolism in <i>Trachinotus ovatus</i> in Response to Acute Hypoxic Stress International Journal of Molecular Sciences <i>Trachinotus ovatus</i> acute hypoxic stress transcriptomics metabolomics cell cycle arrest pro-apoptosis |
| title | Integrated Transcriptomics and Metabolomics Reveal Changes in Cell Homeostasis and Energy Metabolism in <i>Trachinotus ovatus</i> in Response to Acute Hypoxic Stress |
| title_full | Integrated Transcriptomics and Metabolomics Reveal Changes in Cell Homeostasis and Energy Metabolism in <i>Trachinotus ovatus</i> in Response to Acute Hypoxic Stress |
| title_fullStr | Integrated Transcriptomics and Metabolomics Reveal Changes in Cell Homeostasis and Energy Metabolism in <i>Trachinotus ovatus</i> in Response to Acute Hypoxic Stress |
| title_full_unstemmed | Integrated Transcriptomics and Metabolomics Reveal Changes in Cell Homeostasis and Energy Metabolism in <i>Trachinotus ovatus</i> in Response to Acute Hypoxic Stress |
| title_short | Integrated Transcriptomics and Metabolomics Reveal Changes in Cell Homeostasis and Energy Metabolism in <i>Trachinotus ovatus</i> in Response to Acute Hypoxic Stress |
| title_sort | integrated transcriptomics and metabolomics reveal changes in cell homeostasis and energy metabolism in i trachinotus ovatus i in response to acute hypoxic stress |
| topic | <i>Trachinotus ovatus</i> acute hypoxic stress transcriptomics metabolomics cell cycle arrest pro-apoptosis |
| url | https://www.mdpi.com/1422-0067/25/2/1054 |
| work_keys_str_mv | AT qinghuawang integratedtranscriptomicsandmetabolomicsrevealchangesincellhomeostasisandenergymetabolisminitrachinotusovatusiinresponsetoacutehypoxicstress AT renxiewu integratedtranscriptomicsandmetabolomicsrevealchangesincellhomeostasisandenergymetabolisminitrachinotusovatusiinresponsetoacutehypoxicstress AT jiaonaji integratedtranscriptomicsandmetabolomicsrevealchangesincellhomeostasisandenergymetabolisminitrachinotusovatusiinresponsetoacutehypoxicstress AT jingzhang integratedtranscriptomicsandmetabolomicsrevealchangesincellhomeostasisandenergymetabolisminitrachinotusovatusiinresponsetoacutehypoxicstress AT sufangniu integratedtranscriptomicsandmetabolomicsrevealchangesincellhomeostasisandenergymetabolisminitrachinotusovatusiinresponsetoacutehypoxicstress AT baoguitang integratedtranscriptomicsandmetabolomicsrevealchangesincellhomeostasisandenergymetabolisminitrachinotusovatusiinresponsetoacutehypoxicstress AT benbenmiao integratedtranscriptomicsandmetabolomicsrevealchangesincellhomeostasisandenergymetabolisminitrachinotusovatusiinresponsetoacutehypoxicstress AT zhenbangliang integratedtranscriptomicsandmetabolomicsrevealchangesincellhomeostasisandenergymetabolisminitrachinotusovatusiinresponsetoacutehypoxicstress |