Temperature effects on Ca2+ cycling in scombrid cardiomyocytes: a phylogenetic comparison

Abstract

SUMMARYSpecialisations in excitation-contraction coupling may have played an important role in the evolution of endothermy and high cardiac performance in scombrid fishes. We examined aspects of Ca 2+ handling in cardiomyocytes from Pacific bonito (Sarda chiliensis), Pacific mackerel (Scomber japonicus), yellowfin tuna (Thunnus albacares) and Pacific bluefin tuna (Thunnus orientalis). The whole-cell voltage-clamp technique was used to measure the temperature sensitivity of the L-type Ca 2+ channel current (I Ca ), density, and steady-state and maximal sarcoplasmic reticulum (SR) Ca 2+ content (ssSR load and maxSR load ). Current-voltage relations, peak I Ca density and charge density of I Ca were greatest in mackerel and yellowfin at all temperatures tested. I Ca density and kinetics were temperature sensitive in all species studied, and the magnitude of this response was not related to the thermal preference of the species. SR load was greater in atrial than in ventricular myocytes in the Pacific bluefin tuna, and in species that are more cold tolerant (bluefin tuna and mackerel). I Ca and SR load were particularly small in bonito, suggesting the Na + /Ca 2+ exchanger plays a more pivotal role in Ca 2+ entry into cardiomyocytes of this species. Our comparative approach reveals that the SR of cold-tolerant scombrid fishes has a greater capacity for Ca 2+ storage. This specialisation may contribute to the temperature tolerance and thermal niche expansion of the bluefin tuna and mackerel.

Heart rate responses to temperature in free-swimming Pacific bluefin tuna (Thunnus orientalis)

“…Notably, it has been documented that the in vitro metabolism of slow-and fast-twitch muscle from skipjack and bigeye tunas is independent of temperature between 5 and 35°C (Gordon, 1968), yet slow-twitch muscle power output is highly temperature dependent in yellowfin and thus force and frequency benefit from countercurrent heat exchangers (Altringham and Block, 1997). Cardiac studies indicate that Pacific bluefin tunas outperform yellowfin tunas at cooler temperatures because of their capacity to maintain heart function, which at the cellular level has been linked to enrichment of sarcoplasmic reticulum calcium stores, enhanced calcium ATPase activity and a short action potential duration (Galli et al, 2009;Galli et al, 2011;Landeira-Fernandez et al, 2012).…”

“…In contrast, other research indicates that the cardiac function of Pacific bluefin tunas is more tolerant of cold temperatures such that they can routinely dive into waters less than 10°C and maintain a consistent presence in the mixed layer of the cool but productive California Current waters (14-21°C) Blank et al, 2004;Kitagawa et al, 2007;Galli et al, 2009;Boustany et al, 2010;Galli et al, 2011).…”

Satellite telemetry reveals physical processes driving billfish behavior

“…how long the fish retains the heat gained from occupying the mixed layer) influence the variation in dive depths and ambient temperatures that is often observed among individuals and between species [41,48,120]. In contrast, deeper dwelling pelagic fishes, such as swordfish and some tunas, forage extensively below the mixed layer by maintaining cardiac function via greater capacity for cardiac calcium cycling at reduced temperatures [118,121]. Selective heating of the neural infrastructure of the brain and eyes in billfishes and tunas also contribute to their ability to conduct sustained forays into cold water [78,89,122] and provide superior vision for deep foraging [79].…”

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

“…The cellular proteins that cycle Ca 2þ and develop force during excitation-contraction coupling are all known to be acutely temperature-sensitive (e.g. the L-type Ca 2þ current (I Ca ) [24,25], the ryanodine receptor [26][27][28][29], the SR Ca 2þ ATPase (SERCA) [30][31][32], the Na þ -Ca 2þ exchanger [33,34] and the myofilaments [35,36]). However, changes in the shape of the rainbow trout AP have been shown to offset the acute effect of temperature on I Ca [22], suggesting compensatory interplay between thermal sensitivity of the different components of excitation-contraction coupling in fish.…”