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<p>Hypoxia is a critical environmental stressor for aquatic organisms; it regulates gill remodeling and apoptosis in fish. Despite the commercial importance of the Japanese flounder (<i>Paralichthys olivaceus</i>), the molecular mechanisms underlying its hypoxic adaptability, particularly those involving epigenetic regulation and gene networks, remain poorly characterized. To address this issue, we subjected Japanese flounder to acute hypoxia ((2.39±0.84) mg/L DO) for 0 (control), 1, 6, and 24 h, which was followed by an integrated multi-omics analysis of gill tissue comprising RNA-seq and MethylRAD. We identified 319 CG-type and 969 CWG-type differentially methylated genes (DMGs) enriched in energy metabolism, immune signaling, and oxidative homeostasis. Transcriptomics revealed 6410 differentially expressed genes (DEGs) associated with apoptosis, ion transport, and metabolic reprogramming. Cross-omics integration pinpointed 59 consensus genes, with comparative analysis identifying four hypoxia-responsive ones: <i>gpx1b, ero1a, rps23</i>, and <i>OTU domain-containing protein 4-like</i>. Notably, promoter hypomethylation in <i>gpx1b</i> correlated with increased transcription. Dual-luciferase assays confirmed its HIF-1α-mediated transcriptional activation. Overexpression of <i>gpx1b</i> could partially attenuate apoptosis in gill cells. In summary, this study systematically delineated the epigenetic–transcriptional interplay that drives hypoxia adaptation in Japanese flounder, providing mechanistic insights into hypoxia response pathways and a molecular framework for breeding stress-resilient strains for aquaculture.</p>

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Epigenetic Regulation of Gill Function in Japanese Flounder Under Hypoxic Stress Analyzed via Genome-Wide Methylome and Transcriptome Dynamics

  • 期刊论文

  • 发表日期：

    2026年8月4日

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  • Hengtai Tang,
  • Chengnan Ding,
  • Tianyang Cai,
  • Guangling Li,
  • Pingping Liu,
  • Zhirui Zhang,
  • Feng He

摘要

Hypoxia is a critical environmental stressor for aquatic organisms; it regulates gill remodeling and apoptosis in fish. Despite the commercial importance of the Japanese flounder (Paralichthys olivaceus), the molecular mechanisms underlying its hypoxic adaptability, particularly those involving epigenetic regulation and gene networks, remain poorly characterized. To address this issue, we subjected Japanese flounder to acute hypoxia ((2.39±0.84) mg/L DO) for 0 (control), 1, 6, and 24 h, which was followed by an integrated multi-omics analysis of gill tissue comprising RNA-seq and MethylRAD. We identified 319 CG-type and 969 CWG-type differentially methylated genes (DMGs) enriched in energy metabolism, immune signaling, and oxidative homeostasis. Transcriptomics revealed 6410 differentially expressed genes (DEGs) associated with apoptosis, ion transport, and metabolic reprogramming. Cross-omics integration pinpointed 59 consensus genes, with comparative analysis identifying four hypoxia-responsive ones: gpx1b, ero1a, rps23, and OTU domain-containing protein 4-like. Notably, promoter hypomethylation in gpx1b correlated with increased transcription. Dual-luciferase assays confirmed its HIF-1α-mediated transcriptional activation. Overexpression of gpx1b could partially attenuate apoptosis in gill cells. In summary, this study systematically delineated the epigenetic–transcriptional interplay that drives hypoxia adaptation in Japanese flounder, providing mechanistic insights into hypoxia response pathways and a molecular framework for breeding stress-resilient strains for aquaculture.