Abstract
Teleost fishes are diverse and successful, comprising almost half of all extant vertebrate species. It has been suggested that their success as a group is related, in part, to their unique O2 transport system, which includes pH-sensitive hemoglobin, a red blood cell β-adrenergic Na+/H+ exchanger (RBC β-NHE) that protects red blood cell pH, and plasma accessible carbonic anhydrase which is absent at the gills but present in some tissues, that short-circuits the β-NHE to enhance O2 unloading during periods of stress. However, direct support for this has only been examined in a few species of salmonids. Here, we expand the knowledge of this system to two warm-water, highly active marine percomorph fish, cobia (Rachycentron canadum) and mahi-mahi (Coryphaena hippurus). We show evidence for RBC β-NHE activity in both species, and characterize the Hb-O2 transport system in one of those species, cobia. We found significant RBC swelling following β-adrenergic stimulation in both species, providing evidence for the presence of a rapid, active RBC β-NHE in both cobia and mahi-mahi, with a time-course similar to that of salmonids. We generated oxygen equilibrium curves (OECs) for cobia blood and determined the P50, Hill, and Bohr coefficients, and used these data to model the potential for enhanced O2 unloading. We determined that there was potential for up to a 61% increase in O2 unloading associated with RBC β-NHE short-circuiting, assuming a − 0.2 ∆pHa-v in the blood. Thus, despite phylogenetic and life history differences between cobia and the salmonids, we found few differences between their Hb-O2 transport systems, suggesting conservation of this physiological trait across diverse teleost taxa.
At the gills, under stress, catecholamines (1) stimulate β-NHE activity, extruding excess H+ from the red blood cell (2) to maintain intracellular pH (3) and hemoglobin (Hb)-O2 binding (4). Cell increases in volume (5) due to osmosis from β-NHE activity.
At the tissues, plasma-accessible carbonic anhydrase (CA) catalyzes dehydration of extruded H+ into CO2 (6), which rapidly diffuses back into the red blood cell (7), decreasing intracellular pH (8) and increasing O2 unloading to the tissues (9). [Display omitted]
•Enhanced O2 unloading due to RBC β-NHE short-circuiting has previously been shown in three salmonids•Cobia and mahi-mahi both possess rapidly activated red blood cell β-NHE, which is abolished by propranolol•A decrease in blood pH by 0.2 units may enhance O2 unloading in cobia by over 60% in cobia•These data provide further support for the hypothesis that enhanced O2 unloading may be a general trait among teleosts