Warm fish with cold hearts: thermal plasticity of excitation–contraction coupling in bluefin tuna

Abstract

Bluefin tuna have a unique physiology. Elevated metabolic rates coupled with heat exchangers enable bluefin tunas to conserve heat in their locomotory muscle, viscera, eyes and brain, yet their hearts operate at ambient water temperature. This arrangement of a warm fish with a cold heart is unique among vertebrates and can result in a reduction in cardiac function in the cold despite the elevated metabolic demands of endothermic tissues. In this study, we used laser scanning confocal microscopy and electron microscopy to investigate how acute and chronic temperature change affects tuna cardiac function. We examined the temporal and spatial properties of the intracellular Ca ] i , indicating that temperature change limits cardiac myocyte performance. Importantly, we show that thermal acclimation offered partial compensation for these direct effects of temperature. Prolonged cold exposure (more than four weeks) increased the amplitude and kinetics of D[Ca 2þ ] i by increasing intracellular Ca 2þ cycling through the sarcoplasmic reticulum (SR). These functional findings are supported by electron microscopy, which revealed a greater volume fraction of ventricular SR in cold-acclimated tuna myocytes. The results indicate that SR function is crucial to the performance of the bluefin tuna heart in the cold. We suggest that SR Ca 2þ cycling is the malleable unit of cellular Ca 2þ flux, offering a mechanism for thermal plasticity in fish hearts. These findings have implications beyond endothermic fish and may help to delineate the key steps required to protect vertebrate cardiac function in the cold.

Cardiac function in an endothermic fish: cellular mechanisms for overcoming acute thermal challenges during diving

“…Vertebrate heart function [25,48], including that of tunas [14,32,41], is acutely temperature dependent. Thus, diving into cooler waters could be a challenge for cardiac function, especially given the unique arrangement of bluefin tunas having a warm core and a cardiac system at ambient water temperature.…”

“…However, we show that D[Ca 2þ ] i is reduced during cooling from 14 to 88C (figure 4), which cannot be explained by Ca 2þ influx on I Ca (figure 5). The reduction in D[Ca 2þ ] i may be due to a reduction in Ca 2þ release from the intracellular stores of the SR. Release of SR Ca 2þ is triggered by the rate and amplitude of I Ca [41,43], and thus may fail at acutely cooler temperatures (figure 4). Earlier work by the authors has shown that tuna use SR Ca 2þ stores for excitation-contraction coupling [41], so the reduction in D[Ca 2þ ] i may be due to a reduction in Ca 2þ -induced Ca 2þ release.…”

“…Pacific bluefin tuna, T. orientalis (mean mass 8.6 + 0.8 kg, mean fork length 76.1 + 2.3 cm, n ¼ 5, males and females), were captured off the coast of southern California or in Mexican waters off northern Baja as previously described [41]. Fish were held at the Tuna Research and Conservation Centre in Pacific Grove, CA, USA, in 109 m 3 circular tanks acclimated to 148C.…”

“…The Kd of Fluo-4 was adjusted for in vivo temperature dependence [44]: 829 nM at 288C, 1594 at 148C and 1922 nM at 88C. Kinetic analyses of Ca 2þ transients are described in detail in [41] and in the electronic supplementary material.…”

“…Briefly, myocytes were loaded with 4 mM Fluo-4-AM [41], perfused with the same solution used for the electrophysiology and imaged (excitation at 488 nm, detection more than 505 nm) with an Olympus Fluoview confocal microscope. Repetitive line scans (1000 lines of 512 pixels) were taken every 2-4 ms across the width of the cell.…”