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Molecular basis of transmembrane signalling by sensory rhodopsin II–transducer complex

Nature volume 419, pages 484–487 (2002)Cite this article

Abstract

Microbial rhodopsins, which constitute a family of seven-helix membrane proteins with retinal as a prosthetic group, are distributed throughout the Bacteria, Archaea and Eukaryota1,2,3. This family of photoactive proteins uses a common structural design for two distinct functions: light-driven ion transport and phototaxis. The sensors activate a signal transduction chain similar to that of the two-component system of eubacterial chemotaxis4. The link between the photoreceptor and the following cytoplasmic signal cascade is formed by a transducer molecule that binds tightly and specifically5 to its cognate receptor by means of two transmembrane helices (TM1 and TM2). It is thought that light excitation of sensory rhodopsin II from Natronobacterium pharaonis (SRII) in complex with its transducer (HtrII) induces an outward movement of its helix F (ref. 6), which in turn triggers a rotation of TM2 (ref. 7). It is unclear how this TM2 transition is converted into a cellular signal. Here we present the X-ray structure of the complex between N. pharaonis SRII and the receptor-binding domain of HtrII at 1.94 Å resolution, which provides an atomic picture of the first signal transduction step. Our results provide evidence for a common mechanism for this process in phototaxis and chemotaxis.

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Figure 1: Two-component signalling cascade.
Figure 2: Fold of the receptor–transducer complex a, Ribbon diagram of the top view from the cytoplasmic side.
Figure 3: Stereo view of the hydrogen bonds and van der Waals contacts between receptor (α-helices in red) and transducer (α-helices in green).
Figure 4: Interactions between SRII and HtrII.

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Acknowledgements

We thank C. Baeken, I. Ritter and M. Schumacher for technical help, and B. Gehrmann for secretarial assistance. Discussions with R. G. Goody are gratefully acknowledged. We also thank the support by the staff of beamline ID14-1, and in particular E. Mitchell, ESRF, Grenoble, France; H. J. Brandt and C. Wandrey (IBT-Jülich) for a high yield fermentation of SRII containing E. coli cells; A. K. Islamov, A. I. Kuklin and G.N. Bobarikina for help in investigations on mechanisms of membrane protein crystallization in lipidic phases; and I. N. Groznov and V. B. Kireev for their support of this work. This study was supported by the Deutsche Forschungsgemeinschaft, the Max-Planck-Gesellschaft, and the Alexander von Humboldt Foundation.

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  1. Tudor Savopol

    Present address: Carol Davila Medical and Pharmaceutical University, POB15-205, Bucharest, Romania

Authors and Affiliations

  1. Research Centre Jülich, Institute of Structural Biology (IBI-2), 52425, Jülich, Germany

    Valentin I. Gordeliy, Jörg Labahn, Rouslan Moukhametzianov, Rouslan Efremov, Joachim Granzin, Ramona Schlesinger & Georg Büldt

  2. Centre for Biophysics and Physical Chemistry of Supramolecular Structures, MIPT, 141700, Moscow District, Russia

    Valentin I. Gordeliy, Rouslan Moukhametzianov & Rouslan Efremov

  3. Max-Planck-Institut für Molekulare Physiologie, Otto Hahn Str. 11, 44227, Dortmund, Germany

    Tudor Savopol, Axel J. Scheidig, Johann P. Klare & Martin Engelhard

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Correspondence to Georg Büldt or Martin Engelhard.

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Gordeliy, V., Labahn, J., Moukhametzianov, R. et al. Molecular basis of transmembrane signalling by sensory rhodopsin II–transducer complex. Nature 419, 484–487 (2002). https://doi.org/10.1038/nature01109

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