Thermal plasticity of adrenaline-mediated, frequency-dependent calcium homeostasis, in rainbow trout ventricular cardiomyocytes

The effect of global warming on rising aquatic temperatures is producing ever-steeper thermoclines. Fish encountering these sharp changes in water temperature might experience an acute-warming stress. Temperature is the most dominant environmental factor affecting heart function in fish, and without compensatory mechanisms as temperatures rise (e.g., higher heart rate), it could imperil cardiovascular performance. To enhance heart function during acute warming, fish release adrenaline to boost Ca2+ influx in heart cells (cardiomyocytes). However, the relationship between acute warming, elevated heart rate, adrenergic stimulation, and intracellular Ca2+ handling is not well understood at the cellular level. In this study, we investigated the interplay between these key functional drivers in isolated ventricular cardiomyocytes of rainbow trout, at either their acclimation temperature of 10°C or following acute warming (22°C). A subset of cardiomyocytes from each group was treated with either adrenaline, sarcoplasmic-reticulum (SR) inhibitors (that inhibit intracellular Ca2+ cycling via the SR), or both, while pacing frequency was simultaneously increased (simulating faster heart rate). Using epifluorescent microscopy, we measured intracellular Ca2+ transients (Δ[Ca2+]i) and Ca2+-cycling kinetics. Across all pacing frequencies, we found no differences in Δ[Ca2+]i between control (untreated) 10°C and 22°C cardiomyocytes, and that adrenaline had a positive inotropic effect at both temperatures, but was less effective at 22°C. SR inhibition had no effect on Δ[Ca2+]i, but was associated with a greater incidence of irregular Δ[Ca2+]i. Our data suggest that acute thermal stress can disrupt Ca2+-homeostatic mechanisms in trout cardiomyocytes, potentially disrupting whole-heart contractility as global temperatures rise.