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

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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 \( P_{{{\text{HCO}}_{3} }} /P_{\text{Na}} \) = 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.

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Acknowledgments

We are extremely grateful for the kindness, hospitality, and support of the Magadi Soda Company, and particularly the help of John Ndonga and John Kabera. Dishon Muthee and George Muthee provided invaluable logistical assistance. Three anonymous reviewers provided constructive comments. CMW is supported by the Canada Research Chair Program. AB is a Research Fellow from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil) and supported by the International Canada Research Chair Program from the International Development Research Centre (IDRC, Ottawa, Canada). Funded by an NSERC (Canada) Discovery grant to CMW, a grant from the Brazilian CNPq to AB, and a grant from the National Research Foundation of South Africa to JM.

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Correspondence to Chris M. Wood.

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Communicated by G. Heldmaier.

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Wood, C.M., Bergman, H.L., Bianchini, A. et al. Transepithelial potential in the Magadi tilapia, a fish living in extreme alkalinity. J Comp Physiol B 182, 247–258 (2012). https://doi.org/10.1007/s00360-011-0614-y

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  • DOI: https://doi.org/10.1007/s00360-011-0614-y

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