Structural changes in the photoactive site of proteorhodopsin during the primary photoreaction

Biochemistry

Volumn 43, Issue 28, 2004, Pages 9075-9083

  Bergo, Vladislav ^a   Amsden, Jason J ^a   Spudich, Elena N ^b   Spudich, John L ^b   Rothschild, Kenneth J ^a  

^a USA   (United States)

^b UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; FOURIER TRANSFORM INFRARED SPECTROSCOPY; MARINE BIOLOGY; PHOTOCHEMICAL REACTIONS; PROTEINS;

PHOTOREACTIONS; PROTEOBACTERIA;

BIOCHEMISTRY;

AMINO ACID; ASPARAGINE; ASPARTIC ACID; BACTERIORHODOPSIN; CARBON; ETHYLENE; HYDROGEN; OXYGEN; PROTEORHODOPSIN; PROTON PUMP; SCHIFF BASE; UNCLASSIFIED DRUG; WATER;

AMINO ACID SUBSTITUTION; ARTICLE; BIOSPHERE; CHROMATOPHORE; CIS ISOMER; COLOR; CONFORMATIONAL TRANSITION; GRAM NEGATIVE BACTERIUM; INFRARED SPECTROSCOPY; ISOMERIZATION; LOW TEMPERATURE; NONHUMAN; PHOTOREACTIVITY; PRIORITY JOURNAL; REACTION ANALYSIS; SITE DIRECTED MUTAGENESIS; SOLAR ENERGY; TRANS ISOMER; VIBRATION;

AMINO ACID SUBSTITUTION; ASPARAGINE; BINDING SITES; ISOMERISM; LIGHT; LIPOSOMES; MOLECULAR STRUCTURE; MUTATION; PROTEOBACTERIA; RHODOPSIN; SCHIFF BASES; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

BACTERIA (MICROORGANISMS); GAMMAPROTEOBACTERIA; NEGIBACTERIA; PROTEOBACTERIA;

EID: 3142779894     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0361968     Document Type: Article

References (54)

1. Wang, W. W., Sineshchekov, O. A., Spudich, E. N., and Spudich, J. L. (2003) Spectroscopic and photochemical characterization of a deep ocean proteorhodopsin, J. Biol. Chem. 278, 33985-33991.
2. Béjà, O., Aravind, L., Koonin, E. V., Suzuki, M. T., Hadd, A., Nguyen, L. P., Jovanovich, S. B., Gates, C. M., Feldman, R. A., Spudich, J. L., Spudich, E. N., and DeLong, E. F. (2000) Bacterial rhodopsin: evidence for a new type of phototrophy in the sea, Science 289, 1902-1906.
3. Béjà, O., Spudich, E. N., Spudich, J. L., Leclerc, M., and DeLong, E. F. (2001) Proteorhodopsin phototrophy in the ocean, Nature 411, 786-789.
4. Krebs, R. A., Dunmire, D., Partha, R., and Braiman, M. S. (2003) Resonance Raman characterization of proteorhodopsin's chromophore environment, J. Phys. Chem. B 107, 7877-7883.
5. Friedrich, T., Geibel, S., Kalmbach, R., Chizhov, I., Ataka, K., Heberle, J., Engelhard, M., and Bamberg, E. (2002) Proteorhodopsin is a light-driven proton pump with variable vectoriality, J. Mol. Biol. 321, 821-838.
6. Dioumaev, A. K., Brown, L. S., Shih, J., Spudich, E. N., Spudich, J. L., and Lanyi, J. K. (2002) Proton transfers in the photochemical reaction cycle of proteorhodopsin, Biochemistry 41, 5348-5358.
7. Alexiev, U., Mollaaghababa, R., Scherrer, P., Khorana, H. G., and Heyn, M. P. (1995) Rapid long-range proton diffusion along the surface of the purple membrane and delayed proton transfer into the bulk, Proc. Natl. Acad. Sci. U.S.A. 92, 372-376.
8. Cao, Y., Brown, L. S., Sasaki, J., Maeda, A., Needleman, R., and Lanyi, J. K. (1995) Relationship of proton release at the extra-cellular surface to deprotonation of the Schiff base in the bacteriorhodopsin photocycle, Biophys. J. 68, 1518-1530.
9. Rothschild, K. J., Zagaeski, M., and Cantore, W. A. (1981) Conformational changes of bacteriorhodopsin detected by Fourier transform infrared difference spectroscopy, Biochem. Biophys. Res. Commun. 103, 483-489.
10. Bagley, K., Dollinger, G., Eisenstein, L., Singh, A. K., and Zimanyi, L. (1982) Fourier transform infrared difference spectroscopy of bacteriorhodopsin and its photoproducts, Proc. Natl. Acad. Sci. U.S.A. 79, 4972-4976.
11. Earnest, T. N., Roepe, P., Braiman, M. S., Gillespie, J., and Rothschild, K. J. (1986) Orientation of the bacteriorhodopsin chromophore probed by polarized Fourier transform infrared difference spectroscopy, Biochemistry 25, 7793-7798.
12. Braiman, M. S., Mogi, T., Marti, T., Stern, L. J., Khorana, H. G., and Rothschild, K. J. (1988) Vibrational spectroscopy of bacteriorhodopsin mutants: light-driven proton transport involves protonation changes of aspartic acid residues 85, 96, and 212, Biochemistry 27, 8516-8520.
13. Siebert, F. (1990) Resonance Raman and infrared difference spectroscopy of retinal proteins, Methods Enzymol. 189, 123-136.
14. Siebert, F., Hein, M., Radu, I., and Engelhard, M. (2002) Time-resolved step-scan FTIR investigations of the photophobic receptor sensory rhodopsin II from Natronobacterium pharaonis, Biophys. J. 82, 1106.
15. Bergo, V., Spudich, E. N., Scott, K. L., Spudich, J. L., and Rothschild, K. J. (2000) FTIR analysis of the SII540 intermediate of sensory rhodopsin II: Asp73 is the Schiff base proton acceptor, Biochemistry 39, 2823-2830.
16. Furutani, Y., Iwamoto, M., Shimono, K., Kamo, N., and Kandori, H. (2002) FTIR Spectroscopy of the M Photointermediate in pharaonis Phoborhodopsin, Biophys. J. 83, 3482-3489.
17. Bergo, V., Spudich, E. N., Spudich, J. L., and Rothschild, K. J. (2002) A Fourier transform infrared study of Neurospora rhodopsin: Similarities with archaeal rhodopsins, Photochem. Photobiol. 76, 341-349.
18. Brown, L. S., Dioumaev, A. K., Lanyi, J. K., Spudich, E. N., and Spudich, J. L. (2001) Photochemical reaction cycle and proton transfers in Neurospora rhodopsin, J. Biol. Chem. 276, 32495-32505.
19. Rothschild, K. J., and Marrero, H. (1982) Infrared evidence that the Schiff base of bacteriorhodopsin is protonated: BR570 and K intermediates, Proc. Natl. Acad. Sci. U.S.A. 79, 4045-4049.
20. Siebert, F., and Mäntele, W. (1983) Investigation of the primary photochemistry of bacteriorhodopsin by low-temperature Fourier transform infrared spectroscopy, Eur. J. Biochem. 130, 565-573.
21. DeGrip, W. J., and Rothschild, K. J. (2000) in Molecular Mechanisms in Visual Transduction (Stravenga, D. G., de Grip, W. J., and Pugh, E. N., Eds.) pp 1-54, Elsevier Science B.V., Amsterdam.
22. Rothschild, K. J., Cantore, W. A., and Marrero, H. (1983) Fourier transform infrared difference spectra of intermediates in rhodopsin bleaching, Science 219, 1333-1335.
23. Siebert, F., Mantele, W., and Gerwert, K. (1983) Fourier transform infrared spectroscopy applied to rhodopsin. The problem of the protonation state of the retinylidene Schiff base re-investigated, Eur. J. Biochem. 136, 119-127.
24. Kandori, H., Shimono, K., Sudo, Y., Iwamoto, M., Shichida, Y., and Kamo, N. (2001) Structural changes of pharaonis phoborhodopsin upon photoisomerization of the retinal chromophore: infrared spectral comparison with bacteriorhodopsin, Biochemistry 40, 9238-9246.
25. Rothschild, K. J., Marrero, H., Braiman, M., and Mathies, R. (1984) Primary photochemistry of bacteriorhodopsin: comparison of Fourier transform infrared difference spectra with resonance Raman spectra, Photochem. Photobiol. 40, 675-679.
26. Aton, B., Doukas, A. G., Callender, R. H., Becher, B., and Ebrey, T. G. (1977) Resonance Raman studies of the purple membrane, Biochemistry 16, 2995-2999.
27. Bergo, V., Spudich, E. N., Spudich, J. L., and Rothschild, K. J. (2003) Conformational changes detected in a sensory rhodopsin II-transducer complex, J. Biol. Chem. 278, 36556-36562.
28. Smith, S. O., Myers, A. B., Mathies, R. A., Pardoen, J. A., Winkel, C., Van den Berg, E. M. M., and Lugtenburg, J. (1985) Vibrational analysis of the all-trans retinal protonated Schiff base, Biophys. J. 47, 653-664.
29. Roepe, P. D., Ahl, P. L., Herzfeld, J., Lugtenburg, J., and Rothschild, K. J. (1988) Tyrosine protonation changes in bacteriorhodopsin. A Fourier transform infrared study of bR548 and its primary photoproduct, J. Biol. Chem. 263, 5110-5117.
30. Roepe, P., Ahl, P. L., Das Gupta, S. K., Herzfeld, J., and Rothschild, K. J. (1987) Tyrosine and carboxyl protonation changes in the bacteriorhodopsin photocycle. 1. M412 and L550 intermediates, Biochemistry 26, 6696-6707.
31. Mathies, R. A., Lin, S. W., Ames, J. B., and Pollard, W. T. (1991) From femtoseconds to biology: Mechanism of bacteriorhodopsin's light-driven proton pump, Annu. Rev. Biophys. Biophys. Chem. 20, 491-518.
32. Rothschild, K. J. (1992) FTIR difference spectroscopy of bacteriorhodopsin: Toward a molecular model, J. Bioenerg. Biomembr. 24, 147-167.
33. Rothschild, K. J., Roepe, P., Lugtenburg, J., and Pardoen, J. A. (1984) Fourier transform infrared evidence for Schiff base alteration in the first step of the bacteriorhodopsin photocycle, Biochemistry 23, 6103-6109.
34. Neutze, R., Pebay-Peyroula, E., Edman, K., Royant, A., Navarro, J., and Landau, E. M. (2002) Bacteriorhodopsin: a high-resolution structural view of vectorial proton transport, Biochim. Biophys. Acta 1565, 144-167.
35. Aton, B., Doukas, A. G., Narva, D., Callender, R. H., Dinur, U., and Honig, B. (1980) Resonance Raman studies of the primary photochemical event in visual pigments, Biophys. J. 29, 79-94.
36. Otto, H., Marti, T., Holz, M., Mogi, T., Stern, L. J., Engel, F., Khorana, H. G., and Heyn, M. P. (1990) Substitution of amino acids Asp-85, Asp-212, and Arg-82 in bacteriorhodopsin affects the proton release phase of the pump and the pK of the Schiff base, Proc. Natl. Acad. Sci. U.S.A. 87, 1018-1022.
37. Fahmy, K., Weidlich, O., Engelhard, M., Tittor, J., Oesterhelt, D., and Siebert, F. (1992) Identification of the proton acceptor of Schiff base deprotonation in bacteriorhodopsin: a Fourier-transform-infrared study of the mutant Asp85→Glu in its natural lipid environment, Photochem. Photobiol. 56, 1073-1083.
38. Honig, B., Dinur, U., Nakanishi, K., Balogh-Nair, V., Gawinowicz, M. A., Arnaboldi, M., and Motto, M. G. (1979) An external point-charge model for wavelength regulation in visual pigments, J. Am. Chem. Soc. 101, 7084-7086.
39. Barth, A., and Zscherp, C. (2000) Substrate binding and enzyme function investigated by infrared spectroscopy, FEBS Lett. 477, 151-156.
40. Fischer, W., Sonar, S., Marti, T., Khorana, H. G., and Rothschild, K. J. (1994) Detection of a water molecule in the active site of bacteriorhodopsin: hydrogen bonding changes during the primary photoreaction, Biochemistry 33, 12757-12762.
41. Maeda, A., Sasaki, J., Shichida, Y., and Yoshizawa, T. (1992) Water structural changes in the bacteriorhodopsin photocycle: analysis by Fourier transform infrared spectroscopy, Biochemistry 31, 462-467.
42. Kandori, H., Furutani, Y., Shimono, K., Shichida, Y., and Kamo, N. (2001) Internal water molecules of pharaonis phoborhodopsin studied by low-temperature infrared spectroscopy, Biochemistry 40, 15693-15698.
43. Shibata, M., Tanimoto, T., and Kandori, H. (2003) Water molecules in the Schiff base region of bacteriorhodopsin, J. Am. Chem. Soc. 125, 13312-13313.
44. Maeda, A., Sasaki, J., Yamazaki, Y., Needleman, R., and Lanyi, J. K. (1994) Interaction of aspartate-85 with a water molecule and the protonated Schiff base in the L intermediate of bacteriorhodopsin: a Fourier-transform infrared spectroscopic study, Biochemistry 33, 1713-1717.
45. Kandori, H., and Shichida, Y. (2000) Direct observation of the bridged water stretching vibrations inside a protein, J. Am. Chem. Soc. 122, 11745-11746.
46. Barth, A. (2000) The infrared absorption of amino acid side chains, Prog. Biophys. Mol. Biol. 74, 141-173.
47. Song, L., Yang, D. F., Elsayed, M. A., and Lanyi, J. K. (1995) Retinal isomer composition in some bacteriorhodopsin mutants under light and dark-adaptation conditions, J. Phys. Chem. 99, 10052-10055.
48. Brown, L. S., Kamikubo, H., Zimanyi, L., Kataoka, M., Tokunaga, F., Verdegem, P., Lugtenburg, J., and Lanyi, J. K. (1997) A local electrostatic change is the cause of the large-scale protein conformation shift in bacteriorhodopsin, Proc. Natl. Acad. Sci. U.S.A. 94, 5040-5044.
49. Luecke, H., Schobert, B., Richter, H. T., Cartailler, J. P., and Lanyi, J. K. (1999) Structure of bacteriorhodopsin at 1.55 Å resolution, J. Mol. Biol. 291, 899-911.
50. Luecke, H., Schobert, B., Lanyi, J. K., Spudich, E. N., and Spudich, J. L. (2001) Crystal structure of sensory rhodopsin II at 2.4 angstroms: insights into color tuning and transducer interaction, Science 293, 1499-1503.
51. Royant, A., Nollert, P., Edman, K., Neutze, R., Landau, E. M., Pebay-Peyroula, E., and Navarro, J. (2001) X-ray structure of sensory rhodopsin II at 2.1 Å resolution, Proc. Natl. Acad. Sci. U.S.A. 98, 10131-10136.
52. Pebay-Peyroula, E., Royant, A., Landau, E. M., and Navarro, J. (2002) Structural basis for sensory rhodopsin function, Biochim. Biophys. Acta 1565, 196-205.
53. DeLano, W. L. (2003) DeLano Scientific LLC, South San Francisco, CA 94080.
54. Man, D., Wang, W., Sabehi, G., Aravind, L., Post, A. F., Massana, R., Spudich, E. N., Spudich, J. L., and Béjà, O. (2003) Diversification and spectral tuning in marine proteorhodopsins, EMBO J. 8 1725-1731.