Nutritional status modulates mitochondrial bioenergetic and redox responses to zinc exposure in rainbow trout

Fish frequently face fluctuations in food availability and elevated metals levels, which can independently or interactively affect physiological functions. This study examined how nutritional status and zinc (Zn) exposure influence mitochondrial bioenergetics and redox balance in rainbow trout (Oncorhynchus mykiss). Fish were subjected to three nutritional regimes: seven-day satiation, seven-day starvation, or seven-day starvation followed by a 24-h refeeding. Liver and heart mitochondria were isolated and assessed for respiration and H₂O₂ emission during oxidation of glutamate-malate (complex I, CxI) and succinate (complex II; CxII), with and without Zn (0, 25, or 50 μM). Starvation decreased body and organ mass and suppressed CxI- and CxII-linked oxidative phosphorylation (OXPHOS), LEAK respiration, and respiratory control ratio (RCR) in both organs. Refeeding restored liver mitochondrial function but only partially recovered heart function. Zn effects were tissue-, substrate-, and concentration-dependent, with heart more sensitive than liver. In liver, low Zn mitigated starvation-induced OXPHOS suppression, while high Zn impaired respiration across all conditions. Zn elevated H₂O₂ emission in satiated liver mitochondria but reduced it in starved and refed fish. In contrast, heart mitochondria showed Zn-induced respiratory inhibition and a 4-5-fold increase in H₂O₂ emission regardless of nutritional state. Starvation and refeeding alone reduced H₂O₂ emission in heart but not liver. Succinate-supported mitochondria emitted more H₂O₂ than glutamate-malate, likely via enhanced reverse electron transport. Overall, nutritional status and Zn independently and interactively shape mitochondrial function in a tissue-specific manner, highlighting the importance of considering metabolic state in metals toxicity assessments and ecological risk evaluation.