Blood-Based Characterization of Hypoxia-Tolerant and Hypoxia-Susceptible Atlantic Salmon (Salmo salar) Under Acute Hypoxic Stress

Hypoxia is a significant environmental and production-related stressor in Atlantic salmon aquaculture, yet the blood-based mechanisms underlying differential hypoxia tolerance remain poorly characterized. In this study, we examined hematological, biochemical, and transcriptional responses in Atlantic salmon parr classified as hypoxia-tolerant or hypoxia-susceptible following an acute progressive hypoxia challenge. Time to loss of equilibrium and dissolved oxygen concentration at loss of equilibrium were recorded. Blood samples were analyzed for hematological parameters, serum metabolites, and the expression of genes related to hypoxia signaling, glycolysis, oxidative stress, and immune regulation. Hypoxia-tolerant fish maintained equilibrium significantly longer than susceptible fish (Tolerant: 224 ± 18 min; Susceptible: 115 ± 24 min) and tolerated lower dissolved oxygen concentrations (Tolerant: 1.89 ± 0.09 mg L−1; Susceptible: 2.55 ± 0.34 mg L−1) before losing their ability to maintain equilibrium. Tolerance varied among families, while body weight was not significantly associated with time to loss of equilibrium. Acute hypoxia altered erythrocyte-related parameters, increased serum lactate (p < 0.0001), and reduced total protein (p = 0.0148) in both phenotypes. At the transcriptional level, tolerant fish exhibited higher expression of hif1α (p = 0.0012), k6pp (p = 0.0045) and il15 (p = 0.0159), along with reduced phd3 (p = 0.0317) expression, whereas susceptible fish showed increased anx1 expression. Taken together, our results showed that hypoxia tolerance in Atlantic salmon is associated with a coordinated blood response involving metabolic compensation and hypoxia-responsive signaling, supporting the use of blood as a practical tool for identifying resilient fish.