The air-breathing Alaska blackfish ( Dallia pectoralis ) remodels ventricular Ca 2+ cycling with chronic hypoxic submergence to maintain ventricular contractility.

The Alaska blackfish ( Dallia pectoralis ) is a facultative air-breather endemic to northern latitudes where it remains active in winter under ice cover in cold hypoxic waters. To understand the changes in cellular Ca ²⁺ cycling that allow the heart to function in cold hypoxic water, we acclimated Alaska blackfish to cold (5 °C) normoxia or cold hypoxia (2.1-4.2 kPa; no air access) for 5-8 weeks. We then assessed the impact of the acclimation conditions on intracellular Ca ²⁺ transients (Δ[Ca ²⁺ ] _i ) of isolated ventricular myocytes and contractile performance of isometrically-contracting ventricular strips. Measurements were obtained at various contractile frequencies (0.2-0.6 Hz) in normoxia, during acute exposure to hypoxia, and reoxygenation at 5 °C. The results show that hypoxia-acclimated Alaska blackfish compensate against the depressive effects of hypoxia on excitation-contraction coupling by remodelling cellular Δ[Ca ²⁺ ] _i to maintain ventricular contractility. When measured at 0.2 Hz in normoxia, hypoxia-acclimated ventricular myocytes had a 3.8-fold larger Δ[Ca ²⁺ ] _i peak amplitude with a 4.1-fold faster rate of rise, compared to normoxia-acclimated ventricular myocytes. At the tissue level, maximal developed force was 2.1-fold greater in preparations from hypoxia-acclimated animals. However, maximal attainable contraction frequencies in hypoxia were lower in hypoxia-acclimated myocytes and strips than preparations from normoxic animals. Moreover, the inability of hypoxia-acclimated ventricular myocytes and strips to contract at high frequency persisted upon reoxygenation. Overall, the findings indicate that hypoxia alters aspects of Alaska blackfish cardiac myocyte Ca ²⁺ cycling, and that there may be consequences for heart rate elevation during hypoxia, which may impact cardiac output in vivo .
Competing Interests: The authors declare the following financial interests/personal relationships which may be considered as potential competing interests: Jonathan Stecyk reports financial support was provided by 10.13039/100000001National Science Foundation. Diarmid Hall, Shannon Royal reports financial support was provided by 10.13039/100000002National Institutes of Health.
(© 2022 The Authors.)