Transcriptome analysis reveals hypoxic response key genes and modules as well as adaptive mechanism of crucian carp (Carassius auratus) gill under hypoxic stress
Fish gill tissue is a primary organ responsive to acute oxygen deprivation or dissolved oxygen (DO) fluctuations in aquatic environments. However, the adaptive mechanism of crucian carp to hypoxic stress remains largely unknown. Here, we investigated gill physiological and transcriptomic changes of...
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Frontiers Media S.A.
2025-02-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2025.1543605/full |
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| author | Mengchao Xing Mengchao Xing Zhen Rong Zhen Rong Xin Zhao Xin Zhao Xiaowei Gao Xiaowei Gao Zhiguang Hou Lihan Zhang Lihan Zhang Waiho Khor Yihuan Xu Yihuan Xu Li Chen Li Chen Chengbin Wu Chengbin Wu |
| author_facet | Mengchao Xing Mengchao Xing Zhen Rong Zhen Rong Xin Zhao Xin Zhao Xiaowei Gao Xiaowei Gao Zhiguang Hou Lihan Zhang Lihan Zhang Waiho Khor Yihuan Xu Yihuan Xu Li Chen Li Chen Chengbin Wu Chengbin Wu |
| author_sort | Mengchao Xing |
| collection | DOAJ |
| description | Fish gill tissue is a primary organ responsive to acute oxygen deprivation or dissolved oxygen (DO) fluctuations in aquatic environments. However, the adaptive mechanism of crucian carp to hypoxic stress remains largely unknown. Here, we investigated gill physiological and transcriptomic changes of crucian carp exposed to hypoxic conditions (dissolved oxygen concentration of 0.6 ± 0.3 mg/L) for different durations (0 d, 1 d, 2d, 3d, 4 d, and 5d). Transcriptomic analysis revealed that the hypoxia group (0.6 ± 0.3 mg/L DO) exhibited a reduction in interlamellar cell mass (ILCM) on the gill filaments, compared with the control group (6.6 ± 0.3 mg/L DO). With prolonged hypoxia stress, the epithelial cells in the gill lamellae became sparse at 3 d to 5 d, and gill vacuoles were increased. A total of 3,502 differentially expressed genes (DEGs) were identified, and 3 hypoxia-specific modules were screened through differential expression analysis, weighted gene co-expression network analysis (WGCNA), and Bayesian network analysis. The apoptosis, necroptosis, efferocytosis and FoxO signaling pathways were significantly enriched based on the KEGG enrichment pathway analysis. The VEGF pathway genes are significantly expressed, enhancing the generation of microvessels in the gill filaments, and improving the capacity to carry oxygen, thus enabling the crucian carp to adapt to hypoxia stress. Hypoxia activated glycolysis, enhanced anaerobic metabolism, promoted β-oxidation of fatty acids, providing energy and maintaining normal physiological metabolism, eventually improving antioxidant and immune capabilities in crucian carp. In summary, this study reveals the molecular mechanism by which crucian carp adapt to hypoxic stress. Our findings provide valuable references for promoting the healthy aquaculture of hypoxic-sensitive fish and breeding hypoxia-tolerant fish varieties. |
| format | Article |
| id | doaj-art-1fd673b42a9541fd9d3f09ac860495bd |
| institution | Kabale University |
| issn | 1664-3224 |
| language | English |
| publishDate | 2025-02-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Immunology |
| spelling | doaj-art-1fd673b42a9541fd9d3f09ac860495bd2025-02-05T07:32:24ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-02-011610.3389/fimmu.2025.15436051543605Transcriptome analysis reveals hypoxic response key genes and modules as well as adaptive mechanism of crucian carp (Carassius auratus) gill under hypoxic stressMengchao Xing0Mengchao Xing1Zhen Rong2Zhen Rong3Xin Zhao4Xin Zhao5Xiaowei Gao6Xiaowei Gao7Zhiguang Hou8Lihan Zhang9Lihan Zhang10Waiho Khor11Yihuan Xu12Yihuan Xu13Li Chen14Li Chen15Chengbin Wu16Chengbin Wu17Ocean College, Hebei Agricultural University, Qinhuangdao, ChinaHebei Key Laboratory of Aquaculture Nutritional Regulation and Disease Control, Hebei Agricultural University, Qinhuangdao, Hebei, ChinaOcean College, Hebei Agricultural University, Qinhuangdao, ChinaHebei Key Laboratory of Aquaculture Nutritional Regulation and Disease Control, Hebei Agricultural University, Qinhuangdao, Hebei, ChinaOcean College, Hebei Agricultural University, Qinhuangdao, ChinaHebei Key Laboratory of Aquaculture Nutritional Regulation and Disease Control, Hebei Agricultural University, Qinhuangdao, Hebei, ChinaOcean College, Hebei Agricultural University, Qinhuangdao, ChinaHebei Key Laboratory of Aquaculture Nutritional Regulation and Disease Control, Hebei Agricultural University, Qinhuangdao, Hebei, ChinaOcean College, Hebei Agricultural University, Qinhuangdao, ChinaOcean College, Hebei Agricultural University, Qinhuangdao, ChinaHebei Key Laboratory of Aquaculture Nutritional Regulation and Disease Control, Hebei Agricultural University, Qinhuangdao, Hebei, ChinaHigher Institution Centre of Excellence (HICoE), Institute of Tropical Aquaculture and Fisheries, Universiti Malaysia Terengganu, Kuala Terengganu, MalaysiaOcean College, Hebei Agricultural University, Qinhuangdao, ChinaHebei Key Laboratory of Aquaculture Nutritional Regulation and Disease Control, Hebei Agricultural University, Qinhuangdao, Hebei, ChinaOcean and Fisheries Science Research Institute of Hebei Province, Department of Science and Technology of Hebei Province, Qinhuangdao, ChinaHebei Key Laboratory of Marine Biological Resources and Environment, Department of Science and Technology of Hebei Province, Qinhuangdao, ChinaOcean College, Hebei Agricultural University, Qinhuangdao, ChinaHebei Key Laboratory of Aquaculture Nutritional Regulation and Disease Control, Hebei Agricultural University, Qinhuangdao, Hebei, ChinaFish gill tissue is a primary organ responsive to acute oxygen deprivation or dissolved oxygen (DO) fluctuations in aquatic environments. However, the adaptive mechanism of crucian carp to hypoxic stress remains largely unknown. Here, we investigated gill physiological and transcriptomic changes of crucian carp exposed to hypoxic conditions (dissolved oxygen concentration of 0.6 ± 0.3 mg/L) for different durations (0 d, 1 d, 2d, 3d, 4 d, and 5d). Transcriptomic analysis revealed that the hypoxia group (0.6 ± 0.3 mg/L DO) exhibited a reduction in interlamellar cell mass (ILCM) on the gill filaments, compared with the control group (6.6 ± 0.3 mg/L DO). With prolonged hypoxia stress, the epithelial cells in the gill lamellae became sparse at 3 d to 5 d, and gill vacuoles were increased. A total of 3,502 differentially expressed genes (DEGs) were identified, and 3 hypoxia-specific modules were screened through differential expression analysis, weighted gene co-expression network analysis (WGCNA), and Bayesian network analysis. The apoptosis, necroptosis, efferocytosis and FoxO signaling pathways were significantly enriched based on the KEGG enrichment pathway analysis. The VEGF pathway genes are significantly expressed, enhancing the generation of microvessels in the gill filaments, and improving the capacity to carry oxygen, thus enabling the crucian carp to adapt to hypoxia stress. Hypoxia activated glycolysis, enhanced anaerobic metabolism, promoted β-oxidation of fatty acids, providing energy and maintaining normal physiological metabolism, eventually improving antioxidant and immune capabilities in crucian carp. In summary, this study reveals the molecular mechanism by which crucian carp adapt to hypoxic stress. Our findings provide valuable references for promoting the healthy aquaculture of hypoxic-sensitive fish and breeding hypoxia-tolerant fish varieties.https://www.frontiersin.org/articles/10.3389/fimmu.2025.1543605/fullCarassius auratushypoxia-tolerantadaptive mechanismRNA-SeqBayesian networks |
| spellingShingle | Mengchao Xing Mengchao Xing Zhen Rong Zhen Rong Xin Zhao Xin Zhao Xiaowei Gao Xiaowei Gao Zhiguang Hou Lihan Zhang Lihan Zhang Waiho Khor Yihuan Xu Yihuan Xu Li Chen Li Chen Chengbin Wu Chengbin Wu Transcriptome analysis reveals hypoxic response key genes and modules as well as adaptive mechanism of crucian carp (Carassius auratus) gill under hypoxic stress Frontiers in Immunology Carassius auratus hypoxia-tolerant adaptive mechanism RNA-Seq Bayesian networks |
| title | Transcriptome analysis reveals hypoxic response key genes and modules as well as adaptive mechanism of crucian carp (Carassius auratus) gill under hypoxic stress |
| title_full | Transcriptome analysis reveals hypoxic response key genes and modules as well as adaptive mechanism of crucian carp (Carassius auratus) gill under hypoxic stress |
| title_fullStr | Transcriptome analysis reveals hypoxic response key genes and modules as well as adaptive mechanism of crucian carp (Carassius auratus) gill under hypoxic stress |
| title_full_unstemmed | Transcriptome analysis reveals hypoxic response key genes and modules as well as adaptive mechanism of crucian carp (Carassius auratus) gill under hypoxic stress |
| title_short | Transcriptome analysis reveals hypoxic response key genes and modules as well as adaptive mechanism of crucian carp (Carassius auratus) gill under hypoxic stress |
| title_sort | transcriptome analysis reveals hypoxic response key genes and modules as well as adaptive mechanism of crucian carp carassius auratus gill under hypoxic stress |
| topic | Carassius auratus hypoxia-tolerant adaptive mechanism RNA-Seq Bayesian networks |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2025.1543605/full |
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