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First published online July 20, 2006
Journal of Experimental Biology 209, 2813-2827 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02345

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Intestinal anion exchange in marine fish osmoregulation

Martin Grosell

RSMAS, University of Miami, 4600 Rickenbacker Causeway, Miami, FL 33149-1098, USA

View larger version (29K): [in a new window]   Fig. 1. Schematic cellular model of transport processes in the intestinal epithelium of marine teleost fish. Transcellular and/or paracellular fluid absorption is driven by active NaCl transport fueled primarily by the basolateral Na+-K+-ATPase (), which provides the electrochemical Na+ gradient allowing for Na+, Cl- and K+ entry across the apical membrane. Two parallel systems, the Na+, Cl- and the Na+,K+,2Cl- cotransporters account for Na+, K+ and a portion of Cl- absorption, with the remaining Cl- uptake occurring via anion exchange (AE). The apical AE performs active transport of not only Cl- but also HCO3-, resulting in high luminal HCO3- concentrations and highly alkaline intestinal fluids. Endogenous metabolic CO provides cellular HCO-23 via carbonic anhydrase for the apical anion exchange process, with the resulting H+ being extruded across the basolateral membrane via an NHE-like transporter. The H+ extrusion across the basolateral membrane is critical for apical HCO3- secretion and ultimately relies on the activity of the basolateral Na+-K+-ATPase. A physical association of AE and carbonic anhydrase II (CAII) might explain how local HCO3- concentrations on the luminal side of the apical membrane can reach levels satisfying the thermodynamical conditions necessary for anion exchange. Exchange of a metabolic waste product (CO2), which exerts limited osmotic pressure, in exchange for an electrolyte provides an osmotic drivingforce for cellular water uptake. Basolateral import of HCO3- from extracellular fluids appears to also contribute to luminal HCO-33 secretion and may occur via Na+:HCO3- cotransport (NBC). Based on previous studies summarized in Table 2, fluid absorbed by the intestinal epithelium is hyper-osmotic and highly acidic (values represent means of all studies listed in Table 2). See text for further details.

View larger version (13K): [in a new window]   Fig. 2. Total CO2 concentrations in fluids obtained from the anterior (Ant), mid, posterior (Post) intestine and the rectum (Rect) of freshwater (FW) and seawater (SW) acclimated Tilapia auratus. Values are mean ± s.e.m. N=10. Samples were obtained as outlined previously (Grosell et al., 1999; Grosell et al., 2001; Grosell and Jensen, 2000).

View larger version (15K): [in a new window]   Fig. 3. (A) The amount of Na+ and Cl- ingested by a marine teleost fish assuming a drinking rate of 2 ml kg-1h-1 (Marshall and Grosell, 2005) and the amount of Na+ and Cl- present in fluids passing through the esophagus, the anterior (Ant), the mid, the posterior (Post) and the rectal segment (Rect) of the intestine. The amount of Na+ and Cl- passing through the esophagus was calculated from concentrations of Na+ and Cl- in stomach fluids from starved fish (Kirsch and Meister, 1982; Parmelee and Renfro, 1983; Smith, 1930; Wilson et al., 1996), assuming that no water absorption occur across the esophagus (Hirano and Mayer-Gostan, 1976; Parmelee and Renfro, 1983). Amounts of Na+ and Cl- present in the intestinal segments were calculated from concentrations of Na+ and Cl- found in unfed toadfish intestinal fluids (Taylor and Grosell, 2006a) and a fractional water absorption of 20% in each intestinal segment, yielding a total fractional water absorption of 80% (Marshall and Grosell, 2005). Note that the concentrations of Cl- exceed corresponding Na+ concentrations in all gastro-intestinal segments but that the absolute concentration difference between the two ions diminishes as fluids are passing along the intestine. (B) Net Na+ and Cl- uptake rates (mmol kg-1 h-1) occurring across different segments of the gastro-intestinal tract calculated from the different amounts of Na+ and Cl- presented in A. Note the equal molar Na+ and Cl- absorption in the esophagus and the substantial excess Cl- absorption in the anterior intestine. See text for further details.

View larger version (18K): [in a new window]   Fig. 4. Intestinal HCO3- secretion rates (bars, means + s.e.m., N=8) of isolated anterior (Ant), mid and posterior (Post) segments of toadfish intestine and total CO2 concentrations of luminal fluids (circles; means ± s.e.m., N=8) obtained from the anterior, mid, posterior and rectal portion (Rect) of the toadfish intestine. Flux rates in isolated intestinal segments were measured using the same luminal saline (identical HCO3- and Cl- concentrations for all segments) and serosal saline for all three segments (Grosell and Genz, 2006). Total CO2 values are from a recent study on unfed toadfish (Taylor and Grosell, 2006a).

View larger version (15K): [in a new window]   Fig. 5. Electrochemical potential for the apical anion exchange (AE) process calculated assuming intracellular Cl- concentration and apical membrane potential of 30 mmol l-1 and -100 mV, respectively, and using luminal Cl- and HCO3- concentrations from unfed gulf toadfish (Taylor and Grosell, 2006a) and different intracellular HCO3- concentrations ranging from 1.5 to 40 mmol l-1 (indicated by different symbols). Absorption of Cl- and HCO3- secretion via 1:1 anion exchange can only occur when the AE electrochemical potential is >0, which requires intracellular HCO3- concentrations of >10 mmol l-1 in the anterior intestine and close to 40 mmol l-1 in the mid intestine. See text for further details.