Ionic Transport in the Fish Gill Epithelium

The gill of fishes is modified for gas exchange, thereby providing a site for net movement of salts and water down their respective gradients. Specialized cells in the gill epithelium are joined by tight junctions of variable depth and express a variety of transporters and channels. These cells mediate NaCl extrusion in marine fishes and NaCl uptake in freshwater fishes. These transport steps also provide pathways for the extrusion of ammonia and acid vs. base equivalents. J. Exp. Zool. 283:641–652, 1999. © 1999 Wiley-Liss, Inc. The fish gill, like any gas exchanger, is modified to: (1) maximize the surface area available for diffusion of O2 and CO2; (2) minimize the diffusion distance between the external medium and the blood; and (3) maximize the perfusion of the tissue. The gill evolved from the surface epithelium of the branchial basket of protovertebrates, which was used in filter feeding, and probably appeared about 550 million years ago in the Pteraspid agnathans (Gilbert, ’93). Evolutionary modification of a surface epithelium to facilitate gas exchange is not without physiological cost: in an aquatic environment it exacerbates any diffusional movements of solutes or water into or out of an organism that is not iso-osmotic to the medium. Ancestors to the vertebrates were iso-osmotic/ionic to their marine habitats, but, for reasons that are still debated (e.g., Griffith, ’87; Evans, ’93), the vertebrates (except the hagfishes) are not. So aquatic gas exchange presents osmoregulatory problems to fishes. Although osmoregulation in fishes is mediated by a suite of structures including the gastrointestinal epithelium and kidney, the gill is the major site of ion movements to balance diffusional gains or losses. The marine elasmobranchs have evolved a rectal gland that provides for ion extrusion (see Shuttleworth, this volume), but there also is evidence that gill ionic extrusion mechanisms exist (see below). This review examines current models for these transport steps in the gill epithelium in fishes and shows how they are pivotal in acidbase regulation and nitrogen excretion. For recent reviews of these subjects, see Perry (’97); Claiborne (’98); Karnaky (’98); Marshall and Bryson (’98); Walsh (’98). For the purpose of this review, we will focus on teleost fishes, with some references to the elasmobranchs, and do not include gill transport steps for Ca regulation, which have been reviewed recently by Flik and his coworkers (’95, ’96). For a discussion of what little is known about gill function in the agnatha (hagfishes and lampreys), see reviews by Evans (’93) and Karnaky (’98).