Environmental factors responsible for switching on the SO42−excretory system in the kidney of seawater eels

Abstract

Eels are unique in that they maintain lower plasma SO(4)(2-) concentration in SO(4)(2-)-rich (∼30 mM) seawater (SW) than in SO(4)(2-)-poor (<0.3 mM) freshwater (FW), showing drastic changes in SO(4)(2-) regulation between FW and SW. We previously showed that the expression of renal SO(4)(2-) transporter genes, FW-specific Slc13a1 and SW-specific Slc26a6a, changes profoundly after transfer of FW eels to SW, which results in the decrease in plasma SO(4)(2-) concentration after 3 days in SW. In this study, we attempted to identify the environmental factor(s) that trigger the switching of SO(4)(2-) regulation using changes in plasma and urine SO(4)(2-) concentrations and expression of the transporter genes as markers. Transfer of FW eels to 30 mM SO(4)(2-) or transfer of SW eels to SO(4)(2-)-free SW did not change the SO(4)(2-) regulation. Major divalent cations in SW, Mg(2+) (50 mM) and Ca(2+) (10 mM), were also ineffective, but 50 mM NaCl was effective for switching the SO(4)(2-) regulation. Further analyses using choline-Cl and Na-gluconate showed that Cl(-) is a primary factor and Na(+) is permissive for the Cl(-) effect. Since plasma SO(4)(2-) and Cl(-) concentrations were inversely correlated, we injected various solutions into the blood and found that Cl(-) alone triggered the switching from FW to SW-type regulation. Furthermore, the inhibitor of Na-Cl cotransporter (NCC) added to media significantly impaired the expression of SW-specific Slc26a6a in 150 mM NaCl. In summary, it appears that Cl(-) ions in SW are taken up into the circulation via the NCC together with Na(+), and the resultant increase in plasma Cl(-) concentration enhances SO(4)(2-) excretion by the kidney through downregulation of absorptive Slc13a1 and upregulation of excretory Slc26a6a, resulting in low plasma SO(4)(2-) concentration in SW.