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Effects of hypoxic acclimation on contractile properties of the spongy and compact ventricular myocardium of steelhead trout (Oncorhynchus mykiss)

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Abstract

The trout ventricle has an outer compact layer supplied with well-oxygenated arterial blood from the coronary circulation, and an inner spongy myocardium supplied with oxygen poor venous blood. It was hypothesized that: (1) the spongy myocardium of steelhead trout (Oncorhynchus mykiss), given its routine exposure to low partial pressures of oxygen (PO2), would be better able to maintain contractile performance (work) when exposed to acute hypoxia (100 to 10% air saturation) relative to the compact myocardium, and would show little benefit from hypoxic acclimation; and (2) the compact myocardium from hypoxia-acclimated (40% air saturation) fish would be better able to maintain work during acute exposure to hypoxia relative to normoxia-acclimated individuals. Consistent with our expectations, when PO2 was acutely lowered, net work from the compact myocardium of normoxia-acclimated fish declined more (by ~ 73%) than the spongy myocardium (~ 50%), and more than the compact myocardium of hypoxia-acclimated fish (~ 55%), and hypoxic acclimation did not benefit the spongy myocardium in the face of reduced PO2. Further, while hypoxic acclimation resulted in a 25% (but not significant) decrease in net work of the spongy myocardium, the performance of the compact myocardium almost doubled. This research suggests that, in contrast to the spongy myocardium, performance of the compact myocardium is improved by hypoxic acclimation; and supports previous research suggesting that the decreased contractile performance of the myocardium upon exposure to lowered PO2 may be adaptive and mediated by mechanisms within the muscle itself.

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Acknowledgements

We thank Mr. Danny Boyce and the staff of the Dr. Joe Brown Aquatic Research Building for assistance with fish care. This research was supported by Natural Sciences and Engineering Research Council of Canada Discovery grants to AKG (249926-2011) and DAS (201190-2012), and an NSERC Accelerator grant to AKG (412325-2011). During these studies CC was supported by a Memorial University School of Graduate Studies fellowship.

Funding

This research was supported by Natural Sciences and Engineering Research Council of Canada Discovery grants to AKG (249926-2011) and DAS (201190-2012), and an NSERC Accelerator grant to AKG (412325-2011). During these studies CC was supported by a Memorial University School of Graduate Studies fellowship.

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Authors and Affiliations

  1. Department of Biological Sciences, University of Calgary, 2500 University Drive NW, Calgary, AB, T2N 1N4, Canada

    Jordan C. Roberts & Douglas A. Syme

  2. Departments of Ocean Sciences and Biology, Memorial University of Newfoundland, St. John’s, NL, A1C 5S7, Canada

    Christian Carnevale & A. Kurt Gamperl

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  1. Jordan C. Roberts
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  2. Christian Carnevale
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  4. Douglas A. Syme
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Contributions

AKG and DAS contributed to the study conception and design. Material preparation, data collection and analysis were performed by AKG, DAS, CC and JCR. The first draft of the manuscript was written by JCR and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Douglas A. Syme.

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All applicable international, national, and institutional guidelines for the care and use of animals were followed. All animal care and handling procedures were approved by the animal care committees of both the University of Calgary (Protocol #AC14-0214) and Memorial University of Newfoundland (Protocol #15-89-KG), and followed guidelines of the Canadian Council on Animal Care.

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All authors attest that all data and materials as well as software application or custom code support their published claims and comply with field standards. All data generated or analysed during this study are included in this published article.

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Communicated by B. Pelster.

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Roberts, J.C., Carnevale, C., Gamperl, A.K. et al. Effects of hypoxic acclimation on contractile properties of the spongy and compact ventricular myocardium of steelhead trout (Oncorhynchus mykiss). J Comp Physiol B 191, 99–111 (2021). https://doi.org/10.1007/s00360-020-01318-w

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