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Differential effects of bicarbonate on severe hypoxia- and hypercapnia-induced cardiac malfunctions in diverse fish species

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Abstract

We tested in six fish species [Pacific lamprey (Lampetra richardsoni), Pacific spiny dogfish (Squalus suckleyi), Asian swamp eel (Monopterus albus), white sturgeon (Acipenser transmontanus), zebrafish (Danio rerio), and starry flounder (Platichthys stellatus)] the hypothesis that elevated extracellular [HCO3−] protects spontaneous heart rate and cardiac force development from the known impairments that severe hypoxia and hypercapnic acidosis can induce. Hearts were exposed in vitro to either severe hypoxia (~ 3% of air saturation), or severe hypercapnic acidosis (either 7.5% CO2 or 15% CO2), which reduced heart rate (in six test species) and net force development (in three test species). During hypoxia, heart rate was restored by [HCO3−] in a dose-dependent fashion in lamprey, dogfish and eel (EC50 = 5, 25 and 30 mM, respectively), but not in sturgeon, zebrafish or flounder. During hypercapnia, elevated [HCO3−] completely restored heart rate in dogfish, eel and sturgeon (EC50 = 5, 25 and 30 mM, respectively), had a partial effect in lamprey and zebrafish, and had no effect in flounder. Elevated [HCO3−], however, had no significant effect on net force of electrically paced ventricular strips from dogfish, eel and flounder during hypoxia and hypercapnia. Only in lamprey hearts did a specific soluble adenylyl cyclase (sAC) inhibitor, KH7, block the HCO3−-mediated rescue of heart rate during both hypoxia and hypercapnia, and was the only species where we conclusively demonstrated sAC activity was involved in the protective effects of HCO3− on cardiac function. Our results suggest a common HCO3−-dependent, sAC-dependent transduction pathway for heart rate recovery exists in cyclostomes and a HCO3−-dependent, sAC-independent pathway exists in other fish species.

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Acknowledgements

Gratitude is given to the staff at the Department of Fisheries and Oceans’ Centre for Aquaculture and Environmental Research for assistance with animal care. We also thank Mike Sackville for providing the lampreys used in this study.

Funding

M.L. was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Canada Graduate Scholarships-Master’s (CGS M) scholarship. J.N.R. was supported by the William Townsend Porter Predoctoral Fellowship from the American Physiological Society. M.T. was supported by the National Science Foundation (IOS #1754994). A.P.F. was supported by a Discovery Grant from NSERC, and he holds a Canada Research Chair.

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Authors and Affiliations

  1. Department of Zoology, University of British Columbia, 6270 University Boulevard, Vancouver, BC, V6T 1Z4, Canada

    Mandy Lo, Arash Shahriari & Anthony P. Farrell

  2. Marine Biology Research Division, Scripps Institution of Oceanography, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093, USA

    Jinae N. Roa & Martin Tresguerres

  3. Faculty of Land and Food Systems, University of British Columbia, 2357 Main Mall, Vancouver, BC, V6T 1Z4, Canada

    Anthony P. Farrell

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  1. Mandy Lo
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  2. Arash Shahriari
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Contributions

ML was involved in study conception and design, carried out all isolated heart experiments, data analysis, and produced the first draft. AS assisted with the lamprey isolated heart experiments. JNR performed the microscopy work. MT designed and contributed to the microscopy work, data analysis, and manuscript editing. APF was involved in the study conception and design. All the authors reviewed and revised the manuscript, and gave final approval for publication.

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Correspondence to Mandy Lo.

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Lo, M., Shahriari, A., Roa, J.N. et al. Differential effects of bicarbonate on severe hypoxia- and hypercapnia-induced cardiac malfunctions in diverse fish species. J Comp Physiol B 191, 113–125 (2021). https://doi.org/10.1007/s00360-020-01324-y

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