Intestinal anion exchange in marine fish osmoregulation

Abstract

Osmoregulation in marine fishThree 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 (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 Cl -through 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 2-concentrations while at the same time contributing substantially to intestinal Cl -and 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 ...

Feeding ratio and frequency affects cadmium bioaccumulation in black sea bream Acanthopagrus schlegeli

“…Since most marine fish drink seawater continuously to maintain osmotic homeostasis (Grosell 2006) and intestines are the major sites for the uptake of dissolved metals (Zhang & Wang 2007a), feeding and digestion can alter the waterdrinking rate (Wood et al 2010) and physico-chemical environment of fish intestines (e.g. pH and acid−base levels [Taylor et al 2007, Bucking et al 2009] and major ion concentrations [Bucking et al 2011]).…”

The distribution and expression of CFTR restricts electrogenic anion secretion to the ileum of the brushtail possum, Trichosurus vulpecula

“…In eutherian mammals, the SLC26 transporters associated with HCO 3 -secretion are expressed primarily in the villi (Simpson et al, 2007;Wang et al, 2002). Furthermore, HCO 3 -secretion through Cl --HCO 3 -exchange also occurs in the ileum and proximal colon of eutherian mammals (Knickelbein et al, 1985;Mugharbil et al, 1990;Rajendran and Binder, 1993) and is an important mechanism of HCO 3 -secretion in other vertebrates, particularly marine teleosts (Grosell, 2006). Therefore, it is possible that ileal HCO 3 -secretion involves both CFTR-dependent and SLC26-dependent secretion.…”

Mechanisms of transepithelial ammonia excretion and luminal alkalinization in the gut of an intestinal air-breathing fish, Misgurnus anguilliacaudatus

“…Gut lumen surface alkalinization in the loach is probably accomplished through HCO 3 -excretion in exchange for Cl -as has been reported in marine fishes (Grosell et al, 2009b). Although intestinal base excretion has been reported in freshwater trout (Genz et al, 2011), the mechanism of luminal alkalinizaton has only been well characterized in marine fishes, which imbibe water for osmoregulation (Grosell, 2006). The intestinal anion exchanger responsible for alkalinization in marine teleosts has been determined to be Slc26a6 (Kurita et al, 2008;Grosell et al, 2009b) although in freshwater trout gut expression is generally absent (Genz et al, 2011).…”