Integrated biochemical and transcriptomic analyses elucidate the physiological mechanisms in rainbow trout (Oncorhynchus mykiss) head kidney under hypoxia stress

Hypoxia has emerged as a critical threat to the stability of aquatic ecosystems and the sustainability of aquaculture industries. Rainbow trout (Oncorhynchus mykiss), a globally significant economic fish species, exhibits remarkable sensitivity to hypoxia. However, the physiological mechanisms of head kidney in rainbow trout under hypoxia stress, especially under acute and severe hypoxia conditions, remain largely unexplored. This research explored the transcriptomic responses of rainbow trout head kidney to moderate hypoxia (4.5 ± 0.1 mg/L) and severe hypoxia (3.0 ± 0.1 mg/L) for 12 h, alongside dynamic changes in biochemical parameters during hypoxia exposure (0, 4, 8, 12, 24 h, and 1 month) and reoxygenation (R12 h and R24 h). The results showed that compared with the control group, the activities of T-AOC, CAT, T-SOD, GOT, GPT, and ACP were decreased under moderate and severe hypoxia conditions, while the content of MDA and the activity of AKP were increased. In RNA-seq analysis, we identified several hypoxia-related, immune-related and metabolism-related genes (hif-1α, fih1, vhl, ddit4, egln1/2/3, cxcr1/3/4/5, ccr5/7, clec4e/m, tlr2, socs2/3, ighv3–43, ighv3–53, g6pc3, pk, ldha, hk2, and foxo1a) from 20,399 significantly differentially expressed genes, which were enriched in insulin signaling pathway, glycolysis/gluconeogenesis, FcγR-mediated phagocytosis, hematopoietic cell lineage and B cell receptor signaling pathway. Additionally, the expression levels of cxcr1, ddit4, egln2, egln3, fih1 and foxo1a in rainbow trout were significantly up-regulated under hypoxia stress and returned to normal after reoxygenation. These findings provide new insights into the physiological and molecular responses of rainbow trout under hypoxia stress and contribute to developing effective strategies for fish to cope with environmental hypoxia.