To reveal the regulatory mechanism of the mineralocorticoid aldosterone on basolateral K+ channels, the aldosterone-sensitive lung epithelium of Xenopus laevis was investigated in Ussing chambers under voltage-clamp conditions. Transepithelial measurements were supplemented by current fluctuation analysis of short-circuit current noise in nonstimulated and aldosterone-stimulated lung tissues. The addition of 10(-6) M aldosterone stimulated short-circuit current from 11.3 +/- 2.0 to 27.8 +/- 4.8 microA/cm2 (n = 11) within 4-5 h. In the presence of an alveolar-to-pleural K+ gradient, transepithelial K+ currents were induced by permeabilizing the apical membrane with the pore-forming antibiotic amphotericin B. When the local anesthetic lidocaine (25-1,000 microM) was added to the pleural solution, macroscopic K+ current was dose dependently depressed. Lidocaine induced a Lorentzian component in the power density spectra, and the corner frequency increased linearly with blocker concentration. Aldosterone treatment did not affect mean single K+ channel current, which was 1.5 +/- 0.12 pA corresponding to a 15-pS channel conductance, whereas the number of basolateral K+ channels doubled. We conclude that the basolateral K+ channels in alveolar epithelia are a target site of aldosterone action.