{"title":"Integrated Metabolomics and Transcriptomics Reveals Metabolic Pathway Changes in Common Carp Muscle Under Oxidative Stress.","authors":"Yongxiang Liu, Bing Li, Yiran Hou, Linjun Zhou, Qiqin Yang, Chengfeng Zhang, Hongwei Li, Jian Zhu, Rui Jia","doi":"10.3390/antiox14091115","DOIUrl":null,"url":null,"abstract":"<p><p>Hydrogen peroxide (H<sub>2</sub>O<sub>2</sub>), a ubiquitous reactive oxygen species in aquatic ecosystems, has been shown to induce toxicological effects in aquatic animals. However, the molecular mechanisms underlying H<sub>2</sub>O<sub>2</sub>-mediated alterations in muscle quality and metabolic homeostasis remain largely unexplored. In this study, we performed integrated metabolomic and transcriptomic analyses to characterize the molecular mechanisms underlying H<sub>2</sub>O<sub>2</sub>-induced oxidative stress in fish muscle tissue. Common carp (<i>Cyprinus carpio</i>) were randomized into two groups: a control group (0.0 mM H<sub>2</sub>O<sub>2</sub>) and an H<sub>2</sub>O<sub>2</sub>-treated group (1.0 mM H<sub>2</sub>O<sub>2</sub>) for a 14-day exposure. Following the exposure, comprehensive analyses, including fatty acid composition, amino acid profiles, and multi-omics sequencing, were conducted to elucidate the metabolic responses to oxidative stress. The results showed neither the amino acid nor the fatty acid composition exhibited significant modifications following H<sub>2</sub>O<sub>2</sub> exposure. Metabolomic profiling identified 83 upregulated and 89 downregulated metabolites, predominantly comprising organic acids and derivatives, lipids and lipid-like molecules. These differential metabolites were associated with histidine and purine-derived alkaloid biosynthesis, glyoxylate and dicarboxylate metabolism pathways. Transcriptomic analysis identified 470 upregulated and 451 downregulated differentially expressed genes (DEGs). GO enrichment analysis revealed that these DEGs were significantly enriched in muscle tissue development and transcriptional regulatory activity. KEGG analysis revealed significant enrichment in oxidative phosphorylation, adipocytokine signaling, and PPAR signaling pathways. The elevated oxidative phosphorylation activity and upregulated adipocytokine/PPAR signaling pathways collectively indicate H<sub>2</sub>O<sub>2</sub>-induced metabolic dysregulation in carp muscle. Through the integration of metabolomics and transcriptomics, this study offers novel insights into the toxicity of H<sub>2</sub>O<sub>2</sub> in aquatic environments, elucidates adaptive mechanisms of farmed fish to oxidative stress, and provides a theoretical basis for developing antioxidant strategies.</p>","PeriodicalId":7984,"journal":{"name":"Antioxidants","volume":"14 9","pages":""},"PeriodicalIF":6.6000,"publicationDate":"2025-09-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12466421/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Antioxidants","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.3390/antiox14091115","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Hydrogen peroxide (H2O2), a ubiquitous reactive oxygen species in aquatic ecosystems, has been shown to induce toxicological effects in aquatic animals. However, the molecular mechanisms underlying H2O2-mediated alterations in muscle quality and metabolic homeostasis remain largely unexplored. In this study, we performed integrated metabolomic and transcriptomic analyses to characterize the molecular mechanisms underlying H2O2-induced oxidative stress in fish muscle tissue. Common carp (Cyprinus carpio) were randomized into two groups: a control group (0.0 mM H2O2) and an H2O2-treated group (1.0 mM H2O2) for a 14-day exposure. Following the exposure, comprehensive analyses, including fatty acid composition, amino acid profiles, and multi-omics sequencing, were conducted to elucidate the metabolic responses to oxidative stress. The results showed neither the amino acid nor the fatty acid composition exhibited significant modifications following H2O2 exposure. Metabolomic profiling identified 83 upregulated and 89 downregulated metabolites, predominantly comprising organic acids and derivatives, lipids and lipid-like molecules. These differential metabolites were associated with histidine and purine-derived alkaloid biosynthesis, glyoxylate and dicarboxylate metabolism pathways. Transcriptomic analysis identified 470 upregulated and 451 downregulated differentially expressed genes (DEGs). GO enrichment analysis revealed that these DEGs were significantly enriched in muscle tissue development and transcriptional regulatory activity. KEGG analysis revealed significant enrichment in oxidative phosphorylation, adipocytokine signaling, and PPAR signaling pathways. The elevated oxidative phosphorylation activity and upregulated adipocytokine/PPAR signaling pathways collectively indicate H2O2-induced metabolic dysregulation in carp muscle. Through the integration of metabolomics and transcriptomics, this study offers novel insights into the toxicity of H2O2 in aquatic environments, elucidates adaptive mechanisms of farmed fish to oxidative stress, and provides a theoretical basis for developing antioxidant strategies.
过氧化氢(H2O2)是水生生态系统中普遍存在的一种活性氧,已被证明对水生动物具有毒性作用。然而,h2o2介导的肌肉质量和代谢稳态改变的分子机制在很大程度上仍未被探索。在这项研究中,我们进行了综合代谢组学和转录组学分析,以表征h2o2诱导鱼类肌肉组织氧化应激的分子机制。将鲤鱼(Cyprinus carpio)随机分为两组:对照组(0.0 mM H2O2)和H2O2处理组(1.0 mM H2O2),暴露14 d。暴露后,进行了全面的分析,包括脂肪酸组成,氨基酸谱和多组学测序,以阐明氧化应激的代谢反应。结果表明,H2O2暴露后,氨基酸和脂肪酸组成均未发生显著变化。代谢组学分析鉴定了83种上调代谢物和89种下调代谢物,主要包括有机酸及其衍生物、脂质和类脂分子。这些差异代谢物与组氨酸和嘌呤衍生的生物碱生物合成、乙醛酸盐和二羧酸盐代谢途径有关。转录组学分析鉴定了470个上调和451个下调的差异表达基因(DEGs)。氧化石墨烯富集分析显示,这些deg在肌肉组织发育和转录调控活性中显著富集。KEGG分析显示氧化磷酸化、脂肪细胞因子信号通路和PPAR信号通路显著富集。氧化磷酸化活性升高和脂肪细胞因子/PPAR信号通路上调共同表明h2o2诱导的鲤鱼肌肉代谢失调。通过代谢组学和转录组学的整合,本研究为水生环境中H2O2的毒性提供了新的见解,阐明了养殖鱼类对氧化应激的适应机制,并为制定抗氧化策略提供了理论基础。
AntioxidantsBiochemistry, Genetics and Molecular Biology-Physiology
CiteScore
10.60
自引率
11.40%
发文量
2123
审稿时长
16.3 days
期刊介绍:
Antioxidants (ISSN 2076-3921), provides an advanced forum for studies related to the science and technology of antioxidants. It publishes research papers, reviews and communications. Our aim is to encourage scientists to publish their experimental and theoretical results in as much detail as possible. There is no restriction on the length of the papers. The full experimental details must be provided so that the results can be reproduced. Electronic files and software regarding the full details of the calculation or experimental procedure, if unable to be published in a normal way, can be deposited as supplementary electronic material.