Rhodopsin-mediated photoreceptor currents, I(P), of the unicellular alga Chlamydomonas reinhardtii were studied under neutral and acidic conditions. We characterized the kinetically overlapping components of the first, flash-induced inward current recorded from the eye, I(P1), as a low- and high-intensity component, I(P1a) and I(P1b), respectively. They peak between 1 and 10 ms after the light-flash and are both likely to be carried by Ca(2+). I(P1a) and I(P1b) exhibit half-maximal photon flux densities, Q(1/2), of approximately 0.14 and 58 microE m(-2), and maximal amplitudes of approximately 4.9 and 38 pA, respectively. At acidic extracellular pH values (pH 3-5), both I(P1) currents are followed by distinct H(+) currents, I(P2a) and I(P2b), with maxima after approximately 5 and 100 ms, respectively. Because the Q(1/2) values of I(P1b) and I(P2b) virtually coincide with Q(1/2) of rhodopsin bleaching, we suggest that the respective conductances G(1b) and G(2b) are closely coupled to the rhodopsin, whereas the low light-saturating conductances G(1a) and G(2a) reflect transducer-activated states of a second rhodopsin photoreceptor system.