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WATER AND ELECTROLYTE HOMEOSTASIS

Identification of intestinal bicarbonate transporters involved in formation of carbonate precipitates to stimulate water absorption in marine teleost fish

¹Department of Biological Sciences, Tokyo Institute of Technology, Yokohama; ²Shimonoseki Marine Science Museum "Kaikyokan," Shimonoseki Academy of Marine Science, Shimonoseki, Japan; and ³Physiology and Biomedical Engineering, Mayo Clinic College of Medicine, Rochester, Minnesota

Submitted 18 October 2007 ; accepted in final form 19 January 2008

Marine teleost fish precipitate divalent cations as carbonate deposits in the intestine to minimize the potential for excessive Ca²⁺ entry and to stimulate water absorption by reducing luminal osmotic pressure. This carbonate deposit formation, therefore, helps maintain osmoregulation in the seawater (SW) environment and requires controlled secretion of HCO₃^– to match the amount of Ca²⁺ entering the intestinal lumen. Despite its physiological importance, the process of HCO₃^– secretion has not been characterized at the molecular level. We analyzed the expression of two families of HCO₃^– transporters, Slc4 and Slc26, in fresh-water- and SW-acclimated euryhaline pufferfish, mefugu (Takifugu obscurus), and obtained the following candidate clones: NBCe1 (an Na⁺-HCO₃^– cotransporter) and Slc26a6A and Slc26a6B (putative Cl^–/HCO₃^– exchangers). Heterologous expression in Xenopus oocytes showed that Slc26a6A and Slc26a6B have potent HCO₃^–-transporting activity as electrogenic Cl^–/nHCO₃^– exchangers, whereas mefugu NBCe1 functions as an electrogenic Na⁺-nHCO₃^– cotransporter. Expression of NBCe1 and Slc26a6A was highly induced in the intestine in SW and expression of Slc26a6B was high in the intestine in SW and fresh water, suggesting their involvement in HCO₃^– secretion and carbonate precipitate formation. Immunohistochemistry showed staining on the apical (Slc26a6A and Slc26a6B) and basolateral (NBCe1) membranes of the intestinal epithelial cells in SW. We therefore propose a mechanism for HCO₃^– transport across the intestinal epithelial cells of marine fish that includes basolateral HCO₃^– uptake (NBCe1) and apical HCO₃^– secretion (Slc26a6A and Slc26a6B).

osmoregulation; NBC; Slc26; intestine; calcium carbonate