title: 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 Ca(2+) 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 the model. 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.
authors.affiliation: Department of Chemistry, Wilfrid Laurier University, 75 University Ave. West, Waterloo, ON, N2L 3C5, Canada, ccooper@wlu.ca.
authors.forename: C A
authors.initials: CA
authors.lastname: Cooper
authors.forename: M D
authors.initials: MD
authors.lastname: Regan
authors.forename: C J
authors.initials: CJ
authors.lastname: Brauner
authors.forename: E S R
authors.initials: ES
authors.lastname: De Bastos
authors.forename: R W
authors.initials: RW
authors.lastname: Wilson
mesh_terms: D000138:Acidosis; D000818:Animals; D001639:Bicarbonates / Q000378:metabolism*; D005432:Flounder / Q000378:metabolism*; D005618:Fresh Water; D006454:Hemoglobins / Q000378:metabolism; D006859:Hydrogen; D007413:Intestinal Mucosa / Q000378:metabolism*; D017686:Oncorhynchus mykiss / Q000378:metabolism*; D064587:Osmoregulation; D010100:Oxygen / Q000378:metabolism*; D054712:Salinity; D012623:Seawater
chemical_list: D001639:Bicarbonates; D006454:Hemoglobins; D006859:Hydrogen; D010100:Oxygen