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A novel mechanism for enhancing tissue oxygen delivery in teleost fishes Rummer, Jodie Lynn

Abstract

Teleost fishes represent half of all extant vertebrates and possess a unique Root effect haemoglobin (Hb). The Root effect occurs when a reduction in pH greatly reduces Hb oxygen (O₂) affinity and carrying capacity, and is known to greatly enhance O₂ delivery to specialized structures (retia) at the eye and swimbladder. This phenomenon is thought to be a central component to the most successful adaptive radiation event in the evolutionary history of vertebrates. Here, I propose and demonstrate a role for the Root effect in general O₂ delivery. In Chapter 2, I demonstrated that in rainbow trout blood, which possesses a Root effect, the potential for enhanced O₂ delivery relative to that of an air-breathing vertebrate, such as a human, is an order of magnitude greater for a given arterial-venous blood pH change (ΔpHa-v). However, large ΔpHa-v are generally not thought possible away from retia. In Chapters 3 and 4, I proposed and validated a novel mechanism that induces a large ΔpHa-v at the tissues permitting the Root effect to facilitate general O₂ delivery. During a generalized acidosis, teleosts secure gill O2 uptake by protecting RBC pH via adrenergically-stimulated Na⁺/H⁺ exchange (βNHE). I proposed that short-circuiting βNHE at tissues with plasma-accessible carbonic anhydrase (CA) may create a large ΔpHa-v that could greatly enhance O₂ delivery. In Chapter 3 this was validated in vitro in a closed system. I also validated this mechanism in vivo (Chapter 4), where rainbow trout were implanted with fiber-optic O₂-sensors to monitor red muscle (RM) partial pressure of O₂ (PO₂) in real-time. Resting RMPO increased by 65% following exposure to elevated environmental CO₂ and the associated mild acidosis. This was over 10-times what would be expected in an air-breathing vertebrate, such as a human. Furthermore, the ΔPO₂ was completely abolished in the presence of a CA inhibitor, C18. Thus, in my thesis, I have demonstrated that the Root effect may enhance general tissue O₂ delivery. Given that the Root effect evolved 150-270MY before eye and swimbladder retia, it may be that general O₂ delivery was the initial selection pressure in Root effect evolution.

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