Osmoregulatory bicarbonate secretion exploits H+-sensitive haemoglobins to autoregulate intestinal O2 delivery in euryhaline teleosts

Abstract

Marine teleost fish secrete bicarbonate (HCO3−) into the intestine to aid osmoregulation and limit Ca2+ uptake by carbonate precipitation. Intestinal HCO3− secretion is associated with an equimolar transport of protons (H+) into the blood, both being proportional to environmental salinity. We hypothesized that the H+-sensitive haemoglobin (Hb) system of seawater teleosts could be exploited via the Bohr and/or Root effects (reduced Hb-O2 affinity and/or capacity with decreasing pH) to improve O2 delivery to intestinal cells during high metabolic demand associated with osmoregulation. To test this, we characterized H+ equilibria and gas exchange properties of European flounder (Platichthys flesus)haemoglobin and constructed a model incorporating these values, intestinal blood flow rates and arterial–venous acidification at three different environmental salinities (33, 60 and 90). The model suggested red blood cell pH (pHi) during passage through intestinal capillaries could be reduced by 0.14–0.33 units (depending on external salinity) which is sufficient to activate the Bohr effect (Bohr coefficient of −0.63), and perhaps even the Root effect, and enhance tissue O2 delivery by up to 42 % without changing blood flow. In vivo measurements of intestinal venous blood pH were not possible in flounder but were in seawater-acclimated rainbow trout which confirmed a blood acidification of no less than 0.2 units (equivalent to −0.12 for pHi). When using trout-specific values for the model variables, predicted values were consistent with measured in vivo values, further supporting themodel. Thus this system is an elegant example of autoregulation: as the need for costly osmoregulatory processes (including HCO3− secretion) increases at higher environmental salinity, so does the enhancement of O2 delivery to the intestine via a localized acidosis and the Bohr (and possibly Root) effect.