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The Journal of Experimental Biology 206, 949-957 (2003)
doi: 10.1242/jeb.00200

K⁺ transport in Malpighian tubules of Tenebrio molitor L.: a study of electrochemical gradients and basal K⁺ uptake mechanisms

U. I. M. Wiehart¹, S. W. Nicolson¹ and E. Van Kerkhove^2,*

¹ Department of Zoology and Entomology, University of Pretoria, Pretoria 0002, South Africa
² Laboratory of Physiology, Biomed CMK, Limburgs Universitair Centrum, B3590 Diepenbeek, Belgium

^* Author for correspondence (e-mail: emmy.vankerkhove{at}luc.ac.be)

Accepted 10 December 2002

Malpighian tubules of the mealworm Tenebrio molitor were isolated for intracellular measurement of basolateral (V_bl) and, indirectly, apical (V_ap) membrane potentials. In control Ringer (50 mmol l^-1 K⁺, 140 mmol l^-1 Na⁺), V_bl was 24mV, cell negative, and V_ap was 48 mV, cell negative with reference to the lumen. Ion substitution experiments involving K⁺ and Na⁺ indicated that both V_bl and V_ap were sensitive to the bathing K⁺ concentration, with the change in V_ap being 60-77% that of V_bl. A 10-fold drop in bath [K⁺] irreversibly decreased fluid secretion rates from 6.38±0.95 nl min^-1 (mean ± S.E.M.) to 1.48±0.52 nl min^-1 (N=8). In the presence of 6 mmol l^-1 Ba²⁺, a blocker of basal K⁺ channels, fluid secretion rates reversibly decreased and the hyperpolarization of both V_bl and V_ap seen in 50 mmol l^-1 and 140 mmol l^-1 K⁺ indicated a favourable electrochemical gradient for basal K⁺ entry. In 5 mmol l^-1 K⁺, Ba²⁺ induced two different responses: V_bl either hyperpolarized by approximately 10 mV or depolarised by approximately 14mV, according to the electrochemical gradient for K⁺, which was either inward or outward in low bath [K⁺]. Rubidium, a `permeant' potassium substitute, caused a hyperpolarization of V_bl, indicating the specificity of K⁺ channels found in Tenebrio tubule cells. Other possible K⁺ uptake mechanisms located in the basolateral membrane were investigated. Blocking of the putative electroneutral Na⁺/K⁺/2Cl^- cotransporter by 10 µmol l^-1 bumetanide reversibly decreased fluid secretion rates, with no detectable change in membrane potentials. Ouabain (1 mmol l^-1), an Na⁺/K⁺-ATPase inhibitor, irreversibly decreased fluid secretion rates but had no effect on electrical potential differences either in the absence or presence of Ba²⁺. The results implicate K⁺ channels, the Na⁺/K⁺/2Cl^- contransporter and the Na⁺/K⁺-ATPase in basal K⁺ and fluid transport of Tenebrio tubule cells.

Key words: K⁺ transport, K⁺ uptake, Malpighian tubules, Tenebrio molitor, K⁺ channel, Na⁺/K⁺/2Cl^- cotransporter, Na⁺/K⁺-ATPase, basolateral membrane, apical membrane, fluid secretion rate, membrane potential, transepithelial potential

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