Intestinal anion exchange in marine fish osmoregulation
Journal of Experimental Biology
Osmoregulation in marine fish Three distinct strategies for maintaining salt and water balance have evolved in fishes inhabiting the marine environments. (1) Osmoconformity/ionoconformity is found in the strictly marine agnathan hagfishes, which do not appear to regulate osmotic pressure and concentrations of main osmolytes to a great extent in seawater (Morris, 1958) . (2) Osmoconformity and ionoregulation are seen in marine elasmobranchs (Hazon et al., 2003) and in the lobe-finned coelacanth
... -finned coelacanth (Griffith et al., 1974) , which maintains plasma osmolality at or slightly above that of the surrounding seawater but NaCl concentrations at approximately d of ambient levels. (3) The most common strategy is osmoregulation, found in all teleosts (Marshall and Grosell, 2005) and marine lampreys (Morris, 1958) , achieved by the regulation of the main extracellular electrolyte (Na + and Cl -) levels at approximately d of full strength seawater. Under steady state conditions at constant salinities, hagfish, elasmobranchs and coelacanths presumably do not need to drink to maintain water balance. It was shown, however, that the unavoidable renal and extra-renal fluid loss to the hypertonic marine environment in hypo-osmoregulating fish was compensated for by ingestion of seawater with subsequent water absorption across the gastro-intestinal tract (Smith, 1930) . More recently, it was demonstrated that even the osmoconforming elasmobranchs display transient drinking when exposed to elevated ambient salinity, and evidence for components of the rennin-angiotensin system (RAS), even in the elasmobranchs (Anderson et al., 2002; Hazon et al., 2003) and hagfish (Cobb et al., 2004) as well as in lamprey (Brown et al., 2005) , continues to accumulate. The drinking reflex is at least in part controlled by RAS and it thus appears that the ability to regulate ingestion of seawater and thereby the magnitude of intestinal fluid absorption is an ancestral osmoregulatory trait among fishes. The ingestion and processing of the imbibed seawater for osmoregulatory purposes have, at least in teleost fish, received much attention for three quarters of a century since the first classic studies by Smith published in 1930 (Smith, 1930 . It is now well established that an initial desalinization of the ingested seawater occurs in the esophagus, which absorbs Na + and Clthrough both passive and active transport pathways, Despite early reports, dating back three quarters of a century, of high total CO 2 concentrations in the intestinal fluids of marine teleost fishes, only the past decade has provided some insight into the functional significance of this phenomenon. It is now being recognized that intestinal anion exchange is responsible for high luminal HCO 3 and CO 3 2concentrations while at the same time contributing substantially to intestinal Cland thereby water absorption, which is vital for marine fish osmoregulation. In species examined to date, the majority of HCO 3 secreted by the apical anion exchange process is derived from hydration of metabolic CO 2 with the resulting H + being extruded via a Na + :H + exchange mechanism in the basolateral membrane. The basolateral H + extrusion is critical for the apical anion exchange and relies on the Na + gradient established by the Na + -K + -ATPase. This enzyme thereby ultimately fuels the secondary active transport of HCO 3 and Clby the apical anion exchanger. High cellular HCO 3 concentrations (>10·mmol·l -1 ) are required for the anion exchange process and could be the result of both a high metabolic activity of the intestinal epithelium and a close association of the anion exchange protein and the enzyme carbonic anhydrase. The anion exchange activity in vivo is likely most pronounced in the anterior segment and results in net intestinal acid absorption. In contrast to other water absorbing vertebrate epithelia, the marine teleost intestine absorbs what appears to be a hypertonic fluid to displace diffusive fluid loss to the marine environment.