Multi-omics analysis revealed the dysfunction of ovary and testis induced by chronic hypoxia in Pelteobagrus fulvidraco

Hypoxia is a global problem that not only impairs parental fish reproductive functions and fertility but can also decrease offspring fertility through the transgenerational effect, further resulting in the degradation of fish germplasm resources in aquaculture. However, an in-depth exploration of the comprehensive mechanisms of hypoxia-induced gonadal impairment in teleosts is lacking. In this study, the juvenile yellow catfish (Pelteobagrus fulvidraco) were continuously exposed to hypoxic conditions (1.9 ± 0.3 mg/L dissolved oxygen) for one month. The transcriptome, proteome, and metabolome were integrated to study the gonadal response to hypoxia in yellow catfish comprehensively. Hypoxia altered gonadal biological processes involved in angiogenesis, energy metabolism, apoptosis, and steroidogenesis. The testes and ovaries exhibited different adaptive mechanisms in response to chronic hypoxia. Angiogenesis was activated in the testes to increase oxygen delivery. Angiogenesis was inhibited in the ovaries when ovarian hemoglobin levels increased. Activated glycolysis and catabolism of glycogenic amino acids were observed in the testes. The energy metabolism in the ovaries was disrupted by hypoxia, as reflected by disordered glycolysis and suppressed synthesis of amino acids and fatty acids. Gonadal dysfunction and suppression of germ cell development by hypoxia were observed. The decrease in synaptonemal complex protein 1 (SYCP1), SYCP3, Piwi like RNA-mediated gene silencing 2 (PIWIL2), and Nanos C2HC-type zinc finger 3 (Nanos3) in the testes reflected suppressed meiosis and spermatogenesis. The downregulation of vitellogenin 1 (VTG1), zona pellucida (ZP), growth differentiation factor 9 (GDF9), inhibin subunit beta B (Inhbb), and insulin-like growth factor (IGF) signaling inhibited folliculogenesis and vitellogenesis in the ovaries. Our results provide insight into the molecular mechanisms underlying hypoxia-induced reproductive impairment in teleosts.