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

TY - JOUR

T1 - Transepithelial potential in the Magadi tilapia, a fish living in extreme alkalinity

AU - Wood, Chris M.

AU - Bergman, Harold L.

AU - Bianchini, Adalto

AU - Laurent, Pierre

AU - Maina, John

AU - Johannsson, Ora E.

AU - Bianchini, Lucas F.

AU - Chevalier, Claudine

AU - Kavembe, Geraldine D.

AU - Papah, Michael B.

AU - Ojoo, Rodi O.

PY - 2012/2/1

Y1 - 2012/2/1

N2 - 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. HCO 3 - and CO 3 2-) rather than Cl - (112 mmol L -1) represents the major anion matching Na + = 356 mmol L -1, with very low concentrations of Ca 2+ and Mg 2+ (<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 [Ca 2+]. 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 NaHCO 3, NaCl, NaNO 3, or choline Cl, only the 350 mmol L -1 NaHCO 3 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 NaHCO 3, 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 NaHCO 3 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 HCO 3 - inwards (-82.7 mV). Estimated permeability ratios are P Cl/P Na = 0.51-0.68 and P HCO3 = 0.10-0.33. The low permeability to HCO 3 - 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 HCO 3 - excretion.

AB - 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. HCO 3 - and CO 3 2-) rather than Cl - (112 mmol L -1) represents the major anion matching Na + = 356 mmol L -1, with very low concentrations of Ca 2+ and Mg 2+ (<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 [Ca 2+]. 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 NaHCO 3, NaCl, NaNO 3, or choline Cl, only the 350 mmol L -1 NaHCO 3 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 NaHCO 3, 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 NaHCO 3 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 HCO 3 - inwards (-82.7 mV). Estimated permeability ratios are P Cl/P Na = 0.51-0.68 and P HCO3 = 0.10-0.33. The low permeability to HCO 3 - 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 HCO 3 - excretion.

KW - Alcolapia grahami

KW - Calcium-dependent potential

KW - Electrogenic potential

KW - Gill permeability

KW - Na diffusion potential

KW - P /P ratio

KW - P ratio

KW - TEP

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UR - http://www.scopus.com/inward/citedby.url?scp=84856022442&partnerID=8YFLogxK

U2 - 10.1007/s00360-011-0614-y

DO - 10.1007/s00360-011-0614-y

M3 - Article

C2 - 21912898

AN - SCOPUS:84856022442

VL - 182

SP - 247

EP - 258

JO - Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

JF - Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

SN - 0174-1578

IS - 2

ER -