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Osmoregulatory bicarbonate secretion exploits H(+)-sensitive haemoglobins to autoregulate intestinal O(2) delivery in euryhaline teleosts

Marine teleost fish secrete bicarbonate (HCO(3) (−)) into the intestine to aid osmoregulation and limit Ca(2+) uptake by carbonate precipitation. Intestinal HCO(3) (−) secretion is associated with an equimolar transport of protons (H(+)) into the blood, both being proportional to environmental salin...

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Autores principales: Cooper, C. A., Regan, M. D., Brauner, C. J., De Bastos, E. S. R., Wilson, R. W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4171588/
https://www.ncbi.nlm.nih.gov/pubmed/25160040
http://dx.doi.org/10.1007/s00360-014-0844-x
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author Cooper, C. A.
Regan, M. D.
Brauner, C. J.
De Bastos, E. S. R.
Wilson, R. W.
author_facet Cooper, C. A.
Regan, M. D.
Brauner, C. J.
De Bastos, E. S. R.
Wilson, R. W.
author_sort Cooper, C. A.
collection PubMed
description Marine teleost fish secrete bicarbonate (HCO(3) (−)) into the intestine to aid osmoregulation and limit Ca(2+) uptake by carbonate precipitation. Intestinal HCO(3) (−) 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-O(2) affinity and/or capacity with decreasing pH) to improve O(2) 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 (pH(i)) 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 O(2) 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 pH(i)). 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 HCO(3) (−) secretion) increases at higher environmental salinity, so does the enhancement of O(2) delivery to the intestine via a localized acidosis and the Bohr (and possibly Root) effect.
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spelling pubmed-41715882014-09-24 Osmoregulatory bicarbonate secretion exploits H(+)-sensitive haemoglobins to autoregulate intestinal O(2) delivery in euryhaline teleosts Cooper, C. A. Regan, M. D. Brauner, C. J. De Bastos, E. S. R. Wilson, R. W. J Comp Physiol B Original Paper Marine teleost fish secrete bicarbonate (HCO(3) (−)) into the intestine to aid osmoregulation and limit Ca(2+) uptake by carbonate precipitation. Intestinal HCO(3) (−) 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-O(2) affinity and/or capacity with decreasing pH) to improve O(2) 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 (pH(i)) 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 O(2) 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 pH(i)). 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 HCO(3) (−) secretion) increases at higher environmental salinity, so does the enhancement of O(2) delivery to the intestine via a localized acidosis and the Bohr (and possibly Root) effect. Springer Berlin Heidelberg 2014-08-27 2014 /pmc/articles/PMC4171588/ /pubmed/25160040 http://dx.doi.org/10.1007/s00360-014-0844-x Text en © The Author(s) 2014 https://creativecommons.org/licenses/by/4.0/ Open AccessThis article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.
spellingShingle Original Paper
Cooper, C. A.
Regan, M. D.
Brauner, C. J.
De Bastos, E. S. R.
Wilson, R. W.
Osmoregulatory bicarbonate secretion exploits H(+)-sensitive haemoglobins to autoregulate intestinal O(2) delivery in euryhaline teleosts
title Osmoregulatory bicarbonate secretion exploits H(+)-sensitive haemoglobins to autoregulate intestinal O(2) delivery in euryhaline teleosts
title_full Osmoregulatory bicarbonate secretion exploits H(+)-sensitive haemoglobins to autoregulate intestinal O(2) delivery in euryhaline teleosts
title_fullStr Osmoregulatory bicarbonate secretion exploits H(+)-sensitive haemoglobins to autoregulate intestinal O(2) delivery in euryhaline teleosts
title_full_unstemmed Osmoregulatory bicarbonate secretion exploits H(+)-sensitive haemoglobins to autoregulate intestinal O(2) delivery in euryhaline teleosts
title_short Osmoregulatory bicarbonate secretion exploits H(+)-sensitive haemoglobins to autoregulate intestinal O(2) delivery in euryhaline teleosts
title_sort osmoregulatory bicarbonate secretion exploits h(+)-sensitive haemoglobins to autoregulate intestinal o(2) delivery in euryhaline teleosts
topic Original Paper
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4171588/
https://www.ncbi.nlm.nih.gov/pubmed/25160040
http://dx.doi.org/10.1007/s00360-014-0844-x
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