Transepithelial potential in the Magadi tilapia, a fish living in extreme alkalinity

Abstract

We investigated the transepithelial potential (TEP) and its responses to changes in the external medium in Alcolapia grahami, a small cichlid fish living in Lake Magadi, Kenya. Magadi water is extremely alkaline (pH = 9.92) and otherwise unusual: titratable alkalinity (290 mequiv L−1, i.e. HCO3 − and CO3 2−) rather than Cl− (112 mmol L−1) represents the major anion matching Na+ = 356 mmol L−1, with very low concentrations of Ca2+ and Mg2+ (<1 mmol L−1). Immediately after fish capture, TEP was +4 mV (inside positive), but stabilized at +7 mV at 10–30 h post-capture when experiments were performed in Magadi water. Transfer to 250% Magadi water increased the TEP to +9.5 mV, and transfer to fresh water and deionized water decreased the TEP to −13 and −28 mV, respectively, effects which were not due to changes in pH or osmolality. The very negative TEP in deionized water was attenuated in a linear fashion by log elevations in [Ca2+]. Extreme cold (1 vs. 28°C) reduced the positive TEP in Magadi water by 60%, suggesting blockade of an electrogenic component, but did not alter the negative TEP in dilute solution. When fish were transferred to 350 mmol L−1 solutions of NaHCO3, NaCl, NaNO3, or choline Cl, only the 350 mmol L−1 NaHCO3 solution sustained the TEP unchanged at +7 mV; in all others, the TEP fell. Furthermore, after transfer to 50, 10, and 2% dilutions of 350 mmol L−1 NaHCO3, the TEPs remained identical to those in comparable dilutions of Magadi water, whereas this did not occur with comparable dilutions of 350 mmol L−1 NaCl—i.e. the fish behaves electrically as if living in an NaHCO3 solution equimolar to Magadi water. We conclude that the TEP is largely a Na+ diffusion potential attenuated by some permeability to anions. In Magadi water, the net electrochemical forces driving Na+ inwards (+9.9 mV) and Cl− outwards (+3.4 mV) are small relative to the strong gradient driving HCO3 − inwards (−82.7 mV). Estimated permeability ratios are P Cl/P Na = 0.51–0.68 and PHCO3/PNa = 0.10–0.33. The low permeability to HCO3 − is unusual, and reflects a unique adaptation to life in extreme alkalinity. Cl− is distributed close to Nernst equilibrium in Magadi water, so there is no need for lower P Cl. The higher P Na likely facilitates Na+ efflux through the paracellular pathway. The positive electrogenic component is probably due to active HCO3 − excretion.