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Rhodopsin-Mediated Photoreception in Cryptophyte Flagellates

Oleg A. Sineshchekov ^* , Elena G. Govorunova ^*  , Kwang-Hwan Jung ^*, Stefan Zauner , Uwe-G. Maier  and John L. Spudich ^*

^* Center for Membrane Biology, Department of Biochemistry and Molecular Biology, University of Texas Medical School, Houston, Texas; Biology Department, Moscow State University, Moscow, Russia; and Cell Biology, Philipps-University Marburg, Marburg, Germany

Correspondence: Address reprint requests to Oleg A. Sineshchekov, Chair of Physico-Chemical Biology, Biology Department, Moscow State University, Vorobievy Gory, 119992 Moscow, Russia. Tel.: 7-095-9394374; Fax: 7-095-9394309; E-mail: oleg_sinesh{at}yahoo.com; or to John L. Spudich, Center for Membrane Biology, Dept. of Biochemistry and Molecular Biology, University of Texas Medical School, Houston, TX 77030. Tel.: 713-500-5473; Fax: 713-500-0545; E-mail: John.L.Spudich{at}uth.tmc.edu.

We show that phototaxis in cryptophytes is likely mediated by a two-rhodopsin-based photosensory mechanism similar to that recently demonstrated in the green alga Chlamydomonas reinhardtii, and for the first time, to our knowledge, report spectroscopic and charge movement properties of cryptophyte algal rhodopsins. The marine cryptophyte Guillardia theta exhibits positive phototaxis with maximum sensitivity at 450 nm and a secondary band above 500 nm. Variability of the relative sensitivities at these wavelengths and light-dependent inhibition of phototaxis in both bands by hydroxylamine suggest the involvement of two rhodopsin photoreceptors. In the related freshwater cryptophyte Cryptomonas sp. two photoreceptor currents similar to those mediated by the two sensory rhodopsins in green algae were recorded. Two cDNA sequences from G. theta and one from Cryptomonas encoding proteins homologous to type 1 opsins were identified. The photochemical reaction cycle of one Escherichia-coli-expressed rhodopsin from G. theta (GtR1) involves K-, M-, and O-like intermediates with relatively slow (80 ms) turnover time. GtR1 shows lack of light-driven proton pumping activity in E. coli cells, although carboxylated residues are at the positions of the Schiff base proton acceptor and donor as in proton pumping rhodopsins. The absorption spectrum, corresponding to the long-wavelength band of phototaxis sensitivity, makes this pigment a candidate for one of the G. theta sensory rhodopsins. A second rhodopsin from G. theta (GtR2) and the one from Cryptomonas have noncarboxylated residues at the donor position as in known sensory rhodopsins.

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