Electric-field dependent decays of two spectroscopically different M-states of photosensory rhodopsin II from Natronobacterium pharaonis

Biophysical Journal

Volumn 84, Issue 6, 2003, Pages 3864-3873

  Rivas, Laura ^a   Hippler Mreyen, Silke ^b   Engelhard, Martin ^b   Hildebrandt, Peter ^a,c  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b MAX PLANCK INSTITUTE OF MOLECULAR PHYSIOLOGY   (Germany)

^c TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIORHODOPSIN; RHODOPSIN; SCHIFF BASE;

ADSORPTION; ARTICLE; BINDING SITE; CHEMICAL REACTION KINETICS; DEGRADATION; ELECTRIC FIELD; HYDROPHOBICITY; NATRONOBACTERIUM PHARAONIS; NONHUMAN; PHOTOCHEMISTRY; PHOTORECEPTOR; PROTEIN STRUCTURE; RAMAN SPECTROMETRY; SURFACE PROPERTY;

BACTERIA (MICROORGANISMS); MUS; NATRONOBACTERIUM; NATRONOBACTERIUM PHARAONIS; NATRONOMONAS PHARAONIS;

EID: 0037763950     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)75114-5     Document Type: Article

References (49)

1. Althaus, T., W. Eisfeld, R. Lohrmann, and M. Stockburger. 1995. Application of Raman spectroscopy to retinal proteins. Isr. J. Chem. 35:227-251.
2. Bamberg, E., and A. Fahr. 1980. Photocurrents induced on black lipid membranes by purple membranes: a method for reconstitution and a kinetic study of the photocurrents. Ann. N. Y. Acad. Sci. 358:324-327.
3. 540 intermediate of sensory rhodopsin II: Asp73 is the Schiff base proton acceptor. Biochemistry. 39:2823-2830.
4. Blanck, A., D. Oesterhelt, E. Ferrando, E. S. Schegk, and F. Lottspeich. 1989. Primary structure of sensory rhodopsin I, a prokaryotic photoreceptor. EMBO J. 8:3963-3971.
5. Braun, D., N. A. Dencher, A. Fahr, M. Lindau, and M. P. Heyn. 1988. Nonlinear voltage dependence of the light-driven proton pump current of bacteriorhodopsin. Biophys. J. 53:617-621.
6. Chizhov, I., D. S. Chernavskii, M. Engelhard, K. H. Müller, B. V. Zubov, and B. Hess. 1996. Spectrally silent transitions in the bacteriorhodopsin photocycle. Biophys. J. 71:2329-2345.
7. Chizhov, I., G. Schmies, R. Seidel, J. R. Sydor, B. Lüttenberg, and M. Engelhard. 1998. The photophobic receptor from Natronobacterium pharaonis: temperature and pH dependencies of the photocycle of sensory rhodopsin II. Biophys. J. 75:999-1009.
8. Dancshazy, Z., S. L. Helgerson, and W. Stoeckenius. 1983. Coupling between the bacteriorhodopsin photocycle kinetics and the protonmotive force. 1. Single flash measurements in Halobacterium halobium cells. Photobiochem. Photobiophys. 5:347-357.
9. Engelhard, M., B. Scharf, and F. Siebert. 1996. Protonation changes during the photocycle of sensory rhodopsin II from Natronobacterium pharaonis. FEBS Lett. 395:195-198.
10. Geibel, S., T. Friedrich, P. Ormos, P. G. Wood, G. Nagel, and E. Bamberg. 2001. The voltage-dependent proton pumping in bacteriorhodopsin is characterized by optoelectric behavior. Biophys. J. 81:2059-2068.
11. Gellini, C., B. Lüttenberg, J. Sydor, M. Engelhard, and P. Hildebrandt. 2000. Resonance Raman spectroscopy of sensory rhodopsin II from Natronobacterium pharaonis. FEBS Lett. 472:263-266.
12. Groma, G. I., S. L. Helgerson, P. K. Wolber, D. Beece, Z. Dancshazy, L. Keszthelyi, and W. Stoeckenius. 1984. Coupling between the bacterio-rhodopsin photocycle kinetics and the protonmotive force in Halobacterium halobium cell envelope vesicles. 2. Quantitation and preliminary modeling of the M → BR reactions. Biophys. J. 45:985-992.
13. 380 contains 13-cis retinal bound via an unprotonated Schiff base. FEBS Lett. 356:25-29.
14. Hayashi, S., E. Tajkhorshid, E. Pebay-Peyroula, A. Royant, E. M. Landau, J. Navarro, and K. Schulten. 2001. Structural determinants of spectral tuning in retinal proteins-bacteriorhodopsin vs sensory rhodopsin II. J. Phys. Chem. B. 105:10124-10131.
15. Henglein, A., and J. Lilie. 1981. Storage of electrons in aqueous solution: the rates of chemical charging and discharging the colloidal silver microelectrode. J. Am. Chem. Soc. 103:1059-1066.
16. Heyde, M. E., D. Gill, R. G. Kipponen, and L. Rimai. 1971. Raman spectra of Schiff bases of retinal (models of visual photoreceptors). J. Am. Chem. Soc. 93:6776-6780.
17. Hirayama, J., Y. Imamoto, Y. Shichida, N. Kamo, H. Tomioka, and T. Yoshizawa. 1992. Photocycle of phoborhodopsin from haloalkaliphilic bacterium (Natronobacterium pharaonis) studied by low-temperature spectrophotometry. Biochemistry. 31:2093-2098.
18. Hohenfeld, I. P., A. A. Wegener, and M. Engelhard. 1999. Purification of histidine tagged bacteriorhodopsin, pharaonis halorhodopsin and pharaonis sensory rhodopsin II functionally expressed in Escherichia coli. FEBS Lett. 442:198-202.
19. Imamoto, Y., Y. Shichida, J. Hirayama, H. Tomioka, N. Kamo, and T. Yoshizawa. 1992. Nanosecond laser photolysis of phoborhodopsin: From Natronobacterium pharaonis appearance of KL and L intermediates in the photocycle at room temperature. Photochem. Photobiol. 56:1129-1134.
20. Kandori, H., K. Shimono, Y. Sudo, M. Iwamoto, Y. Shichida, and N. Kamo. 2001. Structural changes of pharaonis phoborhodopsin upon photoisomerization of the retinal chromophore: infrared spectral comparison with bacteriorhodopsin. Biochemistry. 40:9238-9246.
21. Lanyi, J. K., and G. Váró. 1995. The photocycles of bacteriorhodopsin. Isr. J. Chem. 35:365-385.
22. 552 from Thermus thermophilus. A time-resolved surface-enhanced resonance Raman spectroscopic study. J. Phys. Chem. B. 103:10053-10064.
23. 550: biological implications. J. Raman Spectrosc. 23:575-583.
24. Losi, A., A. A. Wegener, M. Engelhard, W. Gärtner, and S. E. Braslavsky. 1999. Time-resolved absorption and photothermal measurements with recombinant sensory rhodopsin II from Natronobacterium pharaonis. Biophys. J. 77:3277-3286.
25. Luecke, H., B. Schobert, J. K. Lanyi, E. N. Spudich, and J. L. Spudich. 2001. Crystal structure of sensory rhodopsin II at 2.4 angstroms: insights into color tuning and transducer interaction. Science. 293:1499-1503.
26. Luecke, H., B. Schobert, H. T. Richter, J. P. Cartailler, and J. K. Lanyi. 1999. Structure of bacteriorhodopsin at 1.55 Å resolution. J. Mol. Biol. 291:899-911.
27. Manor, D., C. A. Hasselbacher, and J. L. Spudich. 1988. Membrane-potential modulates photocycling rates of bacterial rhodopsins. Biochemistry. 27:5843-5848.
28. Miyazaki, M., J. Hirayama, M. Hayakawa, and N. Kamo. 1992. Flash photolysis study on pharaonis phoborhodopsin from a haloalkaliphilic bacterium (Natronobacterium pharaonis). Biochim. Biophys. Acta. 1140:22-29.
29. Murgida, D. H., and P. Hildebrandt. 2001a. Heterogeneous electron transfer of cytochrome c on coated silver electrodes. Electric field effects on structure and redox potential. J. Phys. Chem. B. 105:1578-1586.
30. Murgida, D. H., and P. Hildebrandt. 2001b. Proton-coupled electron transfer of cytochrome c. J. Am. Chem. Soc. 123:4062-4068.
31. Murgida, D. H., and P. Hildebrandt. 2002. Electrostatic-field dependent activation energies control biological electron transfer. J. Phys. Chem. B. 106:12814-12819.
32. 2. Biophys. J. 74:403-412.
33. Oellerich, S., H. Wackerbarth, and P. Hildebrandt. 2002. Spectroscopic characterization of nonnative conformational states of cytochrome c. J. Phys. Chem. B. 106:6566-6580.
34. Ormos, P. 1991. Infrared spectroscopic demonstration of a conformational change in bacteriorhodopsin involved in proton pumping. Proc. Natl. Acad. Sci. USA. 88:473-477.
35. Ren, L., C. H. Martin, K. J. Wise, N. B. Gillespie, H. Luecke, J. K. Lanyi, J. L. Spudich, and R. R. Birge. 2001. Molecular mechanism of spectral tuning in sensory rhodopsin II. Biochemistry. 40:13906-13914.
36. Royant, A., P. Nollert, R. Neutze, E. M. Landau, E. Pebay-Peyroula, and J. Navarro. 2001. X-ray structure of sensory rhodopsin II at 2.1-Å resolution. Proc. Natl. Acad. Sci. USA. 98:10131-10136.
37. Schäfer, G., M. Engelhard, and V. Müller. 1999. Bioenergetics of the archaea. Microbiol. Mol. Biol. Rev. 63:570-620.
38. Scharf, B., B. Pevec, B. Hess, and M. Engelhard. 1992. Biochemical and photochemical properties of the photophobic receptors from Halobacterium halobium and Natronobacterium pharaonis. Eur. J. Biochem. 206:359-366.
39. Schmies, G., M. Engelhard, P. G. Wood, G. Nagel, and E. Bamberg. 2001. Electrophysiological characterization of specific interactions between bacterial sensory rhodopsins and their transducers. Proc. Natl. Acad. Sci. USA. 98:1555-1559.
40. Seidel, R., B. Scharf, M. Gautel, K. Kleine, D. Oesterhelt, and M. Engelhard. 1995. The primary structure of sensory rhodopsin II: a member of an additional retinal protein subgroup is coexpressed with its transducer, the halobacterial transducer of rhodopsin II. Proc. Natl. Acad. Sci. USA. 92:3036-3040.
41. Shimono, K., M. Iwamoto, M. Sumi, and N. Kamo. 1997. Functional expression of pharaonis phoborhodopsin in Escherichia coli. FEBS Lett. 420:54-56.
42. 3 from Desulfovibrio gigas immobilized on electrodes. Biopolymers. 67:331-334.
43. Spudich, J. L. 1998. Variations on a molecular switch: transport and sensory signalling by archaeal rhodopsins. Mol. Microbiol. 28:1051-1058.
44. Spudich, J. L., and H. Luecke. 2002. Sensory rhodopsin II: functional insights from structure. Curr. Opin. Struct. Biol. 12:540-546.
45. Váró, G., and J. K. Lanyi. 1990. Protonation and deprotonation of the M, N, and O intermediates during the bacteriorhodopsin photocycle. Biochemistry. 29:6858-6865.
46. Wegener, A. A., I. Chizhov, M. Engelhard, and H. J. Steinhoff. 2000. Time-resolved detection of transient movement of helix F in spin-labelled pharaonis sensory rhodopsin II. J. Mol. Biol. 301:881-891.
47. Westerhoff, H. V., and Z. Dancshazy. 1984. Keeping a light-driven proton pump under control. Trends Biochem. Sci. 9:112-117.
48. Wittenberg, R. 1995. Charakterisierung der Elektronentransportkette und Untersuchungen zur Bioenergetik in Natronobacterium pharaonis. Ruhr-Universität, Bochum, Germany.
49. Zhang, W. S., A. Brooun, M. M. Mueller, and M. Alam. 1996. 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.