UBC Theses and Dissertations

UBC Theses Logo

UBC Theses and Dissertations

The functional significance of plasma-accessible carbonic anhydrase for cardiovascular oxygen transport in teleosts Harter, Till S.


A novel mechanism has recently been discovered in rainbow trout that allows these fish to enhance the partial pressure of O₂ (PO₂) in their muscles. Teleosts have evolved highly pH-sensitive haemoglobins (Hb), where an arterial-venous pH shift (ΔpHa-v) can severely reduce Hb-O₂ binding affinity. Most teleosts create large ΔpHa-v by actively regulating the intracellular (pHi) of their red blood cells (RBC) through adrenergically stimulated sodium-proton exchangers (β-NHE). This creates H⁺ gradients across the RBC membrane that are short-circuited in the presence of plasma-accessible carbonic anhydrase (paCA) at the tissues, to greatly enhance O₂ unloading from pH-sensitive Hb. Thus, I hypothesised that teleosts increase the O₂ capacitance of their blood (βb) by a mechanism of active RBC pHi regulation that is modulated through a heterogeneous distribution of paCA, which has functional significance for O₂ transport in vivo. Mechanistically, I discovered that in rainbow trout, the time-course of β-NHE short-circuiting in the capillaries and the recovery of RBC pHi during venous transit, are consistent with a system that can enhance O₂ unloading at the tissues with every pass through the circulation. Functionally, I discovered that the inhibition of paCA in Atlantic salmon swimming at a low speed or at rest, required a compensatory increase in cardiac output of ~30%, corroborating a role of paCA in O₂ transport over a broad range of conditions. Further, I discovered paCA in the heart lumen of coho salmon; thus, also cardiac O₂ supply in salmonids may rely on β-NHE short-circuiting. In teleosts, the evolution of β-NHE short-circuiting required the loss of paCA at the gills. However, in Antarctic icefish, I propose that the loss of Hb and RBCs released the functional constraint on the expression of paCA at the gills, and allowed for the enzyme to catalyse CO₂ excretion in the absence of RBC CA. Collectively, my findings indicate that an active mechanism at the level of the RBC enhances βb and is an integral part of the salmonid mode of cardiovascular O₂ transport, and perhaps most teleosts, with important implications for the physiology, the conservation and the evolutionary history, of nearly half of all vertebrates.

Item Media

Item Citations and Data


Attribution-NonCommercial-NoDerivatives 4.0 International