Root Effect Haemoglobins in Fish May Greatly Enhance General Oxygen Delivery Relative to Other Vertebrates

The teleost fishes represent over half of all extant vertebrates; they occupy nearly every body of water and in doing so, occupy a diverse array of environmental conditions. We propose that their success is related to a unique oxygen (O(2)) transport system involving their extremely pH-sensitive haemoglobin (Hb). A reduction in pH reduces both Hb-O(2) affinity (Bohr effect) and carrying capacity (Root effect). This, combined with a large arterial-venous pH change (ΔpH(a-v)) relative to other vertebrates, may greatly enhance tissue oxygen delivery in teleosts (e.g., rainbow trout) during stress, beyond that in mammals (e.g., human). We generated oxygen equilibrium curves (OECs) at five different CO(2) tensions for rainbow trout and determined that, when Hb-O(2) saturation is 50% or greater, the change in oxygen partial pressure (ΔPO(2)) associated with ΔpH(a-v) can exceed that of the mammalian Bohr effect by at least 3-fold, but as much as 21-fold. Using known ΔpH(a-v) and assuming a constant arterial-venous PO(2) difference (P(a-v)O(2)), Root effect Hbs can enhance O(2) release to the tissues by 73.5% in trout; whereas, the Bohr effect alone is responsible for enhancing O(2) release by only 1.3% in humans. Disequilibrium states are likely operational in teleosts in vivo, and therefore the ΔpH(a-v), and thus enhancement of O(2) delivery, could be even larger. Modeling with known P(a-v)O(2) in fish during exercise and hypoxia indicates that O(2) release from the Hb and therefore potentially tissue O(2) delivery may double during exercise and triple during some levels of hypoxia. These characteristics may be central to performance of athletic fish species such as salmonids, but may indicate that general tissue oxygen delivery may have been the incipient function of Root effect Hbs in fish, a trait strongly associated with the adaptive radiation of teleosts.