A unique mode of tissue oxygenation and the adaptive radiation of teleost fishes

Abstract

Teleost fishes constitute 95% of extant aquatic vertebrates, and we suggest that this is related in part to their unique mode of tissue oxygenation. We propose the following sequence of events in the evolution of their oxygen delivery system. First, loss of plasma-accessible carbonic anhydrase (CA) in the gill and venous circulations slowed the Jacobs–Stewart cycle and the transfer of acid between the plasma and the red blood cells (RBCs). This ameliorated the effects of a generalised acidosis (associated with an increased capacity for burst swimming) on haemoglobin (Hb)–O₂ binding. Because RBC pH was uncoupled from plasma pH, the importance of Hb as a buffer was reduced. The decrease in buffering was mediated by a reduction in the number of histidine residues on the Hb molecule and resulted in enhanced coupling of O₂ and CO₂ transfer through the RBCs. In the absence of plasma CA, nearly all plasma bicarbonate ultimately dehydrated to CO₂ occurred via the RBCs, and chloride/bicarbonate exchange was the rate-limiting step in CO₂ excretion. This pattern of CO₂ excretion across the gills resulted in disequilibrium states for CO₂ hydration/dehydration reactions and thus elevated arterial and venous plasma bicarbonate levels. Plasma-accessible CA embedded in arterial endothelia was retained, which eliminated the localized bicarbonate disequilibrium forming CO₂ that then moved into the RBCs. Consequently, RBC pH decreased which, in conjunction with pH-sensitive Bohr/Root Hbs, elevated arterial oxygen tensions and thus enhanced tissue oxygenation. Counter-current arrangement of capillaries (retia) at the eye and later the swim bladder evolved along with the gas gland at the swim bladder. Both arrangements enhanced and magnified CO₂ and acid production and, therefore, oxygen secretion to those specialised tissues. The evolution of β-adrenergically stimulated RBC Na+/H+ exchange protected gill O₂ uptake during stress and further augmented plasma disequilibrium states for CO₂ hydration/dehydration. Finally, RBC organophosphates (e.g. NTP) could be reduced during hypoxia to further increase Hb–O₂ affinity without compromising tissue O₂ delivery because high-affinity Hbs could still adequately deliver O₂ to the tissues via Bohr/Root shifts. We suggest that the evolution of this unique mode of tissue O₂ transfer evolved in the Triassic/Jurassic Period, when O₂ levels were low, ultimately giving rise to the most extensive adaptive radiation of extant vertebrates, the teleost fishes.