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

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.

References

  1. Oesterhelt, D. & Stoeckenius, W. Rhodopsin-like protein from the purple membrane of Halobacterium halobium. Nature 233, 149–152 (1971)

    CAS  Google Scholar 

  2. Bieszke, J. A. et al. A eukaryotic protein, NOP-1, binds retinal to form an archaeal rhodopsin-like photochemically reactive pigment. Biochemistry 38, 14138–14145 (1999)

    CAS  Article  Google Scholar 

  3. Béjà, O. et al. Bacterial rhodopsin: evidence for a new type of phototrophy in the sea. Science 289, 1902–1906 (2000)

    ADS  Article  Google Scholar 

  4. Rudolph, J. & Oesterhelt, D. Deletion analysis of the che operon in the archaeon Halobacterium salinarium. J. Mol. Biol. 258, 548–554 (1996)

    CAS  Article  Google Scholar 

  5. Zhang, X. N., Zhu, J. & Spudich, J. L. The specificity of interaction of archaeal transducers with their cognate sensory rhodopsins is determined by their transmembrane helices. Proc. Natl Acad. Sci. USA 96, 857–862 (1999)

    ADS  CAS  Article  Google Scholar 

  6. Wegener, A. A., Chizhov, I., Engelhard, M. & Steinhoff, H. J. Time-resolved detection of transient movement of helix F in spin- labelled pharaonis sensory rhodopsin II. J. Mol. Biol. 301, 881–891 (2000)

    CAS  Article  Google Scholar 

  7. Wegener, A. A., Klare, J. P., Engelhard, M. & Steinhoff, H. J. Structural insights into the early steps of receptor-transducer signal transfer in archaeal phototaxis. EMBO J. 20, 5312–5319 (2001)

    CAS  Article  Google Scholar 

  8. Schmies, G. et al. Electrophysiological characterization of specific interactions between bacterial sensory rhodopsins and their transducers. Proc. Natl Acad. Sci. USA 98, 1555–1559 (2001)

    ADS  CAS  Article  Google Scholar 

  9. Sasaki, J. & Spudich, J. L. Proton circulation during the photocycle of sensory rhodopsin II. Biophys. J. 77, 2145–2152 (1999)

    ADS  CAS  Article  Google Scholar 

  10. Landau, E. M. & Rosenbusch, J. P. Lipidic cubic phases—a novel concept for the crystallization of membrane proteins. Proc. Natl Acad. Sci. USA 93, 14532–14535 (1996)

    ADS  CAS  Article  Google Scholar 

  11. Royant, A. et al. X-ray structure of sensory rhodopsin II at 2.1-Å resolution. Proc. Natl Acad. Sci. USA 98, 10131–10136 (2001)

    ADS  CAS  Article  Google Scholar 

  12. Luecke, H. et al. Crystal structure of sensory rhodopsin II at 2.4 Å: insights into colour tuning and transducer interaction. Science 293, 1499–1503 (2001)

    ADS  CAS  Article  Google Scholar 

  13. Zhang, W. S., Brooun, A., Mueller, M. M. & Alam, M. The primary structures of the archaeon halobacterium salinarium blue light receptor sensory rhodopsin II and its transducer, a methyl-accepting protein. Proc. Natl Acad. Sci. USA 93, 8230–8235 (1996)

    ADS  CAS  Article  Google Scholar 

  14. Hou, S. B. et al. Sensory rhodopsin II transducer HtrII is also responsible for serine chemotaxis in the archaeon halobacterium salinarum. J. Bacteriol. 180, 1600–1602 (1998)

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Yeh, J. I. et al. High-resolution structures of the ligand binding domain of the wild-type bacterial aspartate receptor. J. Mol. Biol. 262, 186–201 (1996)

    CAS  Article  Google Scholar 

  16. Ihara, K. et al. Evolution of the archaeal rhodopsins: evolution rate changes by gene duplication and functional differentiation. J. Mol. Biol. 285, 163–174 (1999)

    CAS  Article  Google Scholar 

  17. Koch, M. H. J. et al. Time-resolved X-ray diffraction study of structural changes associated with the photocycle of bacteriorhodopsin. EMBO J. 10, 521–526 (1991)

    CAS  Article  Google Scholar 

  18. Subramaniam, S., Gerstein, M., Oesterhelt, D. & Henderson, R. Electron diffraction analysis of structural changes in the photocycle of bacteriorhodopsin. EMBO J. 12, 1–8 (1993)

    CAS  Article  Google Scholar 

  19. Lynch, B. A. & Koshland, D. E. Jr Structural similarities between the aspartate receptor of bacterial chemotaxis and the trp repressor of E. coli. Implications for transmembrane signaling. FEBS Lett. 307, 3–9 (1992)

    CAS  Article  Google Scholar 

  20. Falke, J. J. & Hazelbauer, G. L. Transmembrane signaling in bacterial chemoreceptors. Trends Biochem. Sci. 26, 257–265 (2001)

    CAS  Article  Google Scholar 

  21. Gerwert, K., Hess, B. & Engelhard, M. Proline residues undergo structural changes during proton pumping in bacteriorhodopsin. FEBS Lett. 261, 449–454 (1990)

    CAS  Article  Google Scholar 

  22. Abrahams, J. P., Leslie, A. G. W., Lutter, R. & Walker, J. E. Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria. Nature 370, 621–628 (1994)

    ADS  CAS  Article  Google Scholar 

  23. Koshland, D. E. Jr The structural basis of negative cooperativity: receptors and enzymes. Curr. Opin. Struct. Biol. 6, 757–761 (1996)

    CAS  Article  Google Scholar 

  24. Klostermeier, D., Seidel, R. & Reinstein, J. Functional properties of the molecular chaperone DnaK from Thermus thermophilus. J. Mol. Biol. 279, 841–853 (1998)

    CAS  Article  Google Scholar 

  25. Hohenfeld, I. P., Wegener, A. A. & Engelhard, M. Purification of histidine tagged bacteriorhodopsin, pharaonis halorhodopsin and pharaonis sensory rhodopsin II functionally expressed in Escherichia coli. FEBS Lett. 442, 198–202 (1999)

    CAS  Article  Google Scholar 

  26. Shimono, K., Iwamoto, M., Sumi, M. & Kamo, N. Functional expression of pharaonis phoborhodopsin in Escherichia coli. FEBS Lett. 420, 54–56 (1997)

    CAS  Article  Google Scholar 

  27. Leslie, A. G. W. Recent changes to the MOSFLM package for processing film and image data. CCP4 ESF-EACMB Newslett. Protein Crystallogr. 26 (2002)

  28. Collaborative Computational Project The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D 50, 760–763 (1994)

    Article  Google Scholar 

  29. Brunger, A. T. et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D 54, 905–921 (1998)

    CAS  Article  Google Scholar 

  30. Jones, T. A., Zou, J. Y., Cowan, S. W. & Kjeldgaard, M. Improved methods for building protein models in electron-density maps and the location of errors in these models. Acta Crystallogr. A 47, 110–119 (1991)

    Article  Google Scholar 

  31. Kim, K. K., Yokota, H. & Kim, S. H. Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400, 787–792 (1999)

    ADS  CAS  Article  Google Scholar 

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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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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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