Cardiac taurine deficiency impairs physiological performance and mitochondrial function in brook trout (Salvelinus fontinalis)

Abstract

Taurine is a nonessential amino acid abundant in skeletal and cardiac muscle tissues. Taurine plays a critical role in many physiological processes, such as osmoregulation, cardioprotection, and oxidative stress mediation. Studies in other animal models have shown that taurine deficiency is associated with the progression of cardiovascular and mitochondrial diseases, as well as interruptions in energy metabolism. This study evaluated the effects of taurine on the physiological performance and mitochondrial function in brook trout, Salvelinus fontinalis. Dietary supplementation of 𝛽-alanine, a competitive inhibitor of the taurine transporter, was administered over a minimum time frame of four weeks to decrease intracellular taurine concentrations. Two treatment groups were used in this study, a group of fish fed a control diet and a taurine-deficient (TD) group fed the same diet infused with 5% 𝛽-alanine. The physiological impacts of taurine deficiency were assessed through evaluating the critical thermal maximum (CTmax) and tolerance to acute hypoxia through time-to-loss of equilibrium (LOE) tests. CTmax was evaluated by increasing tank water temperature at a set ramp rate until fish could no longer maintain equilibrium. CTmax was found to be significantly higher in (p=0.017), while tolerance to acute hypoxia was observed to be significantly lower (p=0.015) in TD trout than in the control group. FluoRespirometry evaluated mitochondrial efficiency at different points along the electron transport chain. Increased mitochondrial leak rates were observed in TD trout, indicating a greater degree of proton leak into the intermembrane space (p=0.0056). Activities of mitochondrial complexes I and II were not affected by TD. The average respiratory control ratio (RCR) of the TD trout was significantly decreased in comparison to the control group, indicating that a greater portion of oxygen consumption in TD mitochondria is not coupled with ADP phosphorylation and is instead dissipated as heat energy (p=0.0051). Respirometry also revealed that maximum oxygen consumption of complex IV of the electron transport chain was significantly decreased by TD (p=0.0216). Expression of complex IV protein COX3 was significantly downregulated in TD cardiac muscle tissue, indicating potential defects in protein synthesis correlated with TD (p=0.007). Our findings provide further insight into the roles of taurine, and pathology of taurine deficiency in the cardiovascular system of fish. This understanding can enable us to further gauge the effects of environmental fluctuations on this species.