Unraveling the metabolic gene expression and energetic patterns of the seasonally acclimatized gilthead seabream

The aim of the present study was to investigate how seasonal changes in the oxidation of biological energy substrates contribute to the thermal tolerance of farmed fish, as well as to explore the potential relationship between seasonality, metabolic pathways, and the energy reserves of a highly important aquaculture species, i.e., the gilthead sea bream Sparus aurata. In a monthly basis collected tissue samples from a fish farm in Evoikos Gulf in Greece, RNA/DNA ratio was measured, representing a highly informative index of the nutritional condition and growth of fish. Additionally, seasonal variations in glucose and lipid metabolism were assessed through relative gene expressions of key metabolic enzymes and proteins such as glucose transporter (Glu), lactate dehydrogenase (L-LDH), citrate synthase (CS), 3-hydroxyacyl-CoA dehydrogenase (HOAD), pyruvate kinase (PK), AMP-activated protein kinase (AMPK), and peroxisome proliferator-activated receptors (PPARα/γ). Furthermore, the expression of uncoupling proteins, NADH dehydrogenase (NDH-2), hypoxia-inducible factor-1 alpha (Hif-1a), electron transport system activity (ETS), and its components (complex I + III) was also employed as indicators of the respiratory chain activity. The findings reveal two distinct metabolic periods affecting productivity: a cold acclimatization phase marked by significant lipid accumulation and a warm acclimatization phase characterized by elevated carbohydrate metabolic pathways and enhanced corresponding enzymatic activities. However, the decreasing CS enzymatic activity during warm acclimatization may reflect the initiation of mitochondrial dysfunction. These metabolic adjustments underscore the fish adaptive responses to seasonal temperature fluctuations, highlighting their mechanisms of thermal tolerance and energy utilization. This understanding is particularly relevant for sustainability practices under varying thermal conditions.