ABSTRACT
Oxygen supply to the heart of most teleosts, including salmonids, relies in part or in whole on oxygen-depleted venous blood. Given that plasma-accessible carbonic anhydrase (CA) in red muscle of rainbow trout has recently been shown to facilitate oxygen unloading from arterial blood under certain physiological conditions, we tested the hypothesis that plasma-accessible CA is present in the lumen of coho salmon (Oncorhynchus kisutch) hearts, and may therefore assist in the luminal oxygen supply to the spongy myocardium, which has no coronary circulation. We demonstrate a widespread distribution of CA throughout the heart chambers, including lumen-facing cells in the atrium, and confirm that the membrane-bound isoform ca4 is expressed in the atrium and ventricle of the heart. Further, we confirm that CA catalytic activity is available to blood in the atrial lumen using a modified electrometric ΔpH assay in intact atria in combination with either a membrane-impermeable CA inhibitor or specific cleavage of the Ca4 membrane anchor. Combined, these results support our hypothesis of the presence of an enhanced oxygen delivery system in the lumen of a salmonid heart, which could help support oxygen delivery when the oxygen content of venous blood becomes greatly reduced, such as after burst exercise and during environmental hypoxia.
Footnotes
Author contributions
S.L.A., T.S.H., A.P.F. and C.J.B. devised the study. S.L.A. and T.S.H. conducted the experiments. J.M.W. assisted with the enzyme histochemistry. C.T.S. provided the C18. S.L.A. analyzed the data and wrote the manuscript, with intellectual and editorial contributions by all authors throughout. All authors approved the manuscript.
Funding
Financial support for this project was provided by Natural Sciences and Engineering Research Council (NSERC) Discovery grants to C.J.B., A.P.F. and J.M.W. [grant numbers 261924-13, RGPIN-2015-05059 and RGPIN-2014-04289, respectively], and an NSERC Accelerator Supplement to C.J.B. A.P.F. holds a Canada Research Chair. T.S.H. is supported by a UBC Department of Zoology Four-Year Fellowship.