Thermal acclimation and seasonal acclimatization: a comparative study of cardiac response to prolonged temperature change in shorthorn sculpin

Abstract

Seasonal thermal remodelling (acclimatization) and laboratory thermal remodelling (acclimation) can induce different physiological changes in ectothermic animals. As global temperatures are changing at an increasing rate, there is urgency to understand the compensatory abilities of key organs such as the heart to adjust under natural conditions. Thus, the aim of the present study was to directly compare the acclimatization and acclimatory response within a single eurythermal fish species, the European shorthorn sculpin (Myoxocephalus scorpio). We used current-and voltage-clamp to measure ionic current densities in both isolated atrial and ventricular myocytes from three groups of fish: (1) summer-caught fish kept at 12°C ('summer-acclimated'); (2) summer-caught fish kept at 3°C ('cold acclimated'); and (3) fish caught in March ('winteracclimatized'). At a common test temperature of 7.5°C, action potential (AP) was shortened by both winter acclimatization and cold acclimation compared with summer acclimation; however, winter acclimatization caused a greater shortening than did cold acclimation. Shortening of AP was achieved mostly by a significant increase in repolarizing current density (I Kr and I K1 ) following winter acclimatization, with cold acclimation having only minor effects. Compared with summer acclimation, the depolarizing L-type calcium current (I Ca ) was larger following winter acclimatization, but again, there was no effect of cold acclimation on I Ca . Interestingly, the other depolarizing current, I Na , was downregulated at low temperatures. Our further analysis shows that ionic current remodelling is primarily due to changes in ion channel density rather than current kinetics. In summary, acclimatization profoundly modified the electrical activity of the sculpin heart while acclimation to the same temperature for >1.5 months produced very limited remodelling effects.

A rapid intrinsic heart rate resetting response with thermal acclimation in rainbow trout, Oncorhynchus mykiss

“…This means that the lack of pacemaker resetting responses in fishes cannot be attributed solely to species differences, as suggested previously (Matikainen and Vornanen, 1992). Indeed, differences in both intrinsic heart rate, and in the electrophysiology of cardiac myocytes have been previously observed in a number of fish species, although not in salmonids (Filatova et al, 2019;Harri and Talo, 1975;Matikainen and Vornanen, 1992). What might turn off pacemaker resetting awaits further study, but the present results suggest seasonal acclimatisation could be a factor given that the two experiments were performed at different times of the year.…”

Warmer, faster, stronger: Ca2+ cycling in avian myocardium

“…The sarcolemmal Ca 2+ current registered in quail cardiomyocytes had conventional current-voltage configurations and the observed difference in current density between atrial and ventricular myocytes is a common phenomenon for vertebrate hearts (Badr et al, 2018;Filatova et al, 2019;Hatano et al, 2006). Of note is the large amplitude of I Ca in quail ventricular myocytes.…”

Cardiophysiological responses of the air-breathing Alaska blackfish to cold acclimation and chronic hypoxic submergence at 5°C

“…N (cells/animals)=10/6 (15N), 12/6 (5N) and 11/6 (5H) for I K1 , and N (cells/animals)=13/6 (15N), 15/6 (5N) and 11/6 (5H) for I Kr . Filatova et al, 2019;Hassinen et al, 2014). Indeed, paradoxically, Alaska blackfish can be caught by baited hook and line from waters covered with more than a metre of ice, with temperatures of between 2 and 4°C and with P O2 lower (ranging from 0.8 kPa at depth to 3.6 kPa in the water column) than their laboratory-measured critical O 2 level (Lefevre et al, 2014).…”

“…Nevertheless, some cardiophysiological responses to cold are not mutually exclusive to an overwintering strategy. For instance, a pronounced and shared response between cold-active and colddormant species with cold acclimation and acclimatization is a prominent shortening of action potential duration (APD) Vornanen, 2015, 2017;Filatova et al, 2019;Galli et al, 2009;Hassinen et al, 2014Hassinen et al, , 2008bHaverinen and Vornanen, 2009;Shiels et al, 2006;Vornanen, 2016Vornanen, , 2017Vornanen et al, 2002). The mechanism underlying the shortening of APD is an upregulation of the main cardiac K + currents I K1 and I Kr , especially I Kr , which is considered to play the most important role in the control of APD in fish myocardium (Hassinen et al, 2008a).…”