Responses of Action Potential and K+ Currents to Temperature Acclimation in Fish Hearts: Phylogeny or Thermal Preferences?

Electrical activity of the heart is assumed to be one of the key factors that set thermal tolerance limits for ectothermic vertebrates. Therefore, we hypothesized that in thermal acclimation-the duration of cardiac action potential and the repolarizing K+ currents that regulate action potential duration (APD)-the rapid component of the delayed rectifier K+ current (I-Kr) and the inward rectifier K+ current (I-K1) are more plastic in eurythermal than in stenothermal fish species. The hypothesis was tested in six freshwater teleosts representing four different fish orders (Cadiformes, Cypriniformes, Perciformes, Salmoniformes) acclimated at +4 degrees C (cold acclimation) or +18 degrees C (warm acclimation). In cold acclimation, a compensatory shortening of APD occurred in all species regardless of thermal tolerances, life styles, or phylogenies of the fish, suggesting that this response is a common characteristic of the teleost heart. The strength of the response did not, however, obey simple eurythermy-stenothermy gradation but differed among the phylogenetic groups. Salmoniformes fish showed the greatest acclimation capacity of cardiac electrical activity, whereas the weakest response appeared in the perch (Perciformes) heart. The underlying ionic mechanisms were also partly phylogeny dependent. Modification of the I-Kr current was almost ubiquitously involved in acclimation response of fish cardiac myocytes to temperature, while the ability to change the I-K1 current under chronic thermal stress was absent or showed inverse compensation in Salmoniformes species. Thus, in Salmoniformes fish, the thermal plasticity of APD is strongly based on I-Kr, while other fish groups rely on both I-Kr and I-K1.