Conformational differences between the methoxy groups of QA and QB site ubisemiquinones in bacterial reaction centers: A key role for methoxy group orientation in modulating ubiquinone redox potential

Biochemistry

Volumn 52, Issue 27, 2013, Pages 4648-4655

  Taguchi, Alexander T ^a   O'Malley, Patrick J ^c   Wraight, Colin A ^a   Dikanov, Sergei A ^b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL REACTION; CONFORMATIONAL DIFFERENCES; ELECTRON TRANSPORT; HYPERFINE COUPLING; PHOTOSYNTHETIC REACTION CENTER; PROTEIN COMPLEXES; SECONDARY QUINONE; X RAY CRYSTAL STRUCTURES;

DIHEDRAL ANGLE; PROTEINS; REDOX REACTIONS; SECONDARY BATTERIES;

PLANTS (BOTANY);

QUINONE DERIVATIVE; SEMIQUINONE; UBIQUINONE; PHOTOSYNTHESIS;

ANISOTROPY; ARTICLE; BACTERIAL PHENOMENA AND FUNCTIONS; CHEMICAL REACTION; COMPARATIVE STUDY; CONFORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PHOTOSYNTHESIS; PRIORITY JOURNAL; CHEMISTRY; ELECTRON SPIN RESONANCE; OXIDATION REDUCTION REACTION; RHODOBACTER SPHAEROIDES; X RAY CRYSTALLOGRAPHY;

CRYSTALLOGRAPHY, X-RAY; ELECTRON SPIN RESONANCE SPECTROSCOPY; OXIDATION-REDUCTION; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; RHODOBACTER SPHAEROIDES; UBIQUINONE;

EID: 84880066024     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi400489b     Document Type: Article

References (46)

1. Heathcote, P., Fyfe, P. K., and Jones, M. R. (2002) Reaction centers: the structure and evolution of biological solar power Trends Biochem. Sci. 27, 79-86
2. Blankenship, R. (2002) Molecular mechanisms of photosynthesis, Blackwell Science, Ltd, London.
3. Wraight, C. A. (2004) Proton and electron transfer in the acceptor quinone complex of photosynthetic reaction centers from Rhodobacter sphaeroides Front. Biosci. 9, 309-337
4. Wraight, C. A. and Gunner, M. R. (2009) The Acceptor Quinones of Purple Photosynthetic Bacteria-Structure and Spectroscopy. The Purple Phototrophic Bacteria (Hunter, C. N., Daldal, F., Thurnauer, M. C., and Beatty, J. T., Eds.) pp 379, Springer Science + Business Media B.V.
5. + binding coupled to secondary electron transfer in the quinone acceptor complex Biochim. Biophys. Acta 548, 309-327
6. Blankenship, R. E. and Parson, W. W. (1979) The involvement of iron and ubiquinone in electron transfer reactions mediated by reaction centers from photosynthetic bacteria Biochim. Biophys. Acta 545, 429-444
7. - Biochim. Biophys. Acta 766, 126-140
8. - reaction in isolated reaction centers from the photosynthetic bacterium Rhodopseudomonas sphaeroides Biochim. Biophys. Acta 764, 46-54
9. Shinkarev, V. P. and Wraight, C. A. (1997) The interaction of quinone and detergent with reaction centers of purple bacteria. I. Slow quinone exchange between reaction center micelles and pure detergent micelles Biophys. J. 72, 2304-2319
10. Wraight, C. A., Vakkasoglu, A. S., Poluektov, Y., Mattis, A. J., Nihan, D., and Lipshutz, B. H. (2008) The 2-methoxy group of ubiquinone is essential for function of the acceptor quinones in reaction centers from Rba. sphaeroides Biochim. Biophys. Acta 1777, 631-636
11. McComb, J. C., Stein, R. R., and Wraight, C. A. (1990) Investigations on the influence of headgroup substitution and isoprene side-chain length in the function of primary and secondary quinones of bacterial reaction centers Biochim. Biophys. Acta 1015, 156-171
12. Prince, R. C., Dutton, P. L., and Bruce, J. M. (1983) Electrochemistry of ubiquinones, menaquinones and plastoquinones in aprotic solvents FEBS Lett. 160, 273-276
13. Gu, L. Q., Yu, L., and Yu, C. A. (1990) Effect of substituents of the benzoquinone ring on electron-transfer activities of ubiquinone derivatives Biochim. Biophys. Acta 1015, 482-492
14. Nabedryk, E. and Breton, J. (2008) Coupling of electron transfer to proton uptake at the Q(B) site of the bacterial reaction center: a perspective from FTIR difference spectroscopy Biochim. Biophys. Acta 1777, 1229-1248
15. - by EPR and ENDOR Appl. Magn. Reson. 17, 1-48
16. Dikanov, S. A. (2013) Resolving protein-semiquinone interactions by two-dimensional ESEEM spectroscopy Electron Paramagn. Resonan. 23, 103-179
17. Breton, J. and Nabedryk, E. (1996) Protein-quinone interactions in the bacterial photosynthetic reaction center: Light-induced FTIR difference spectroscopy of the quinone vibrations Biochim. Biophys. Acta 1275, 84-90
18. Nonella, M. and Brändli, C. (1996) Density functional investigation of methoxy-substituted p -benzoquinones: Conformational analysis and harmonic force fields of 2-methoxy- and 2,3-dimethoxy-1,4-benzoquinone J. Phys. Chem. 100, 14549-14559
19. Burie, J.-R., Boullais, C., Nonella, M., Mioskowski, C., Nabedryk, E., and Breton, J. (1997) Importance of the conformation of methoxy groups on the vibrational and electrochemical properties of ubiquinones J. Phys. Chem. B 101, 6607-6617
20. Nonella, M. (1997) Structure and vibrational spectra of p -benzoquinone in different oxidation and protonation states: A density functional study J. Phys. Chem. B 101, 1235-1246
21. Nonella, M. (1998) A quantum chemical investigation of structures, vibrational spectra and electron affinities of the radicals of quinone model compounds Photosynth. Res. 55, 253-259
22. Nonella, M., Mathias, G., Eichinger, M., and Tavan, P. (2003) Structures and vibrational frequencies of the quinones of Rb. sphaeroides derived by a combined density functional/molecular mechanics approach J. Phys. Chem. B 107, 316-322
23. Boullais, C., Nabedryk, E., Burie, J.-R., Nonella, M., Mioskowski, C., and Breton, J. (1998) Site-specific isotope labeling demonstrates a large mesomeric resonance effect of the methoxy groups on the carbonyl frequency in ubiquinones Photosynth. Res. 55, 247-252
24. Breen, D. L. (1975) Coenzyme Q: A molecular orbital study J. Theor. Biol. 53, 101-113
25. Robinson, H. and Kahn, S. (1990) Interplay of substitutent conformation and electron affinity in quinone models of quinone reductases J. Am. Chem. Soc. 112, 4728-4731
26. Prince, R. C., Halbert, T. R., and Upton, T. H. (1988) Structural influences on the electrochemistry of ubiquinone. Advances in Membrane Biochemistry and Bioenergetics (Kim, C. H., Tedeschi, H., Diwan, J. J., and Salerno, J. C., Eds.) pp 469-478, Plenum Press, New York.
27. B? Eur. J. Biochem. 270, 3603-3609
28. 13C-labeled methyl and methoxy substituents J. Biol. Chem. 286, 10105-10114
29. Lin, M. T., Sperling, L. J., Frericks Schmidt, H. L., Tang, M., Samoilova, R. I., Kumasaka, T., Iwasaki, T., Dikanov, S. A., Rienstra, Ch. M., and Gennis, R. B. (2011) A rapid and robust method for selective isotope labeling of proteins Methods 55, 370-378
30. Goldsmith, J. O. and Boxer, S. G. (1996) Rapid isolation of bacterial photosynthetic reaction center with an engineered poly-histidine tag Biochim. Biophys. Acta 1276, 171-175
31. Stoll, S., Calle, C., Mitrikas, G., and Schweiger, A. (2005) Peak suppression in ESEEM spectra of multinuclear spin systems J. Magn. Reson. 177, 93-101
32. B-site of bacterial reaction centers J. Am. Chem. Soc. 132, 11671-11677
33. Okamura, M., Isaacson, R., and Feher, G. (1975) Primary acceptor in Bacterial Photosynthesis: Obligatory role of Ubiquinone in Photoactive Reaction Centers of Rhodopseudomonas spheroides Proc. Nat. Acad. Sci. U.S.A. 72, 3491-3495
34. Höfer, P., Grupp, A., Nebenführ, H., and Mehring, M. (1986) Hyperfine sublevel correlation (HYSCORE) spectrocopy: A 2D ESR investigation of the squaric acid radical Chem. Phys. Lett. 132, 279-282
35. Stoll, S. and Britt, R. D. (2009) General and efficient simulation of pulse EPR spectra Phys. Chem. Chem. Phys. 11, 6614-6625
36. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Scalmani, G., Barone, V., Mennucci, B., Petersson, G. A., Nakatsuji, H., Caricato, M., Li, X., Hratchian, H. P., Izmaylov, A. F., Bloino, J., Zheng, G., Sonnenberg, J. L., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Vreven, T., Montgomery, J. A., Jr., Peralta, J. E., Ogliaro, F., Bearpark, M., Heyd, J. J., Brothers, E., Kudin, K. N., Staroverov, V. N., Kobayashi, R., Normand, J., Raghavachari, K., Rendell, A., Burant, J. C., Iyengar, S. S., Tomasi, J., Cossi, M., Rega, N., Millam, J. M., Klene, M., Knox, J. E., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C., Ochterski, J. W., Martin, R. L., Morokuma, K., Zakrzewski, V. G., Voth, G. A., Salvador, P., Dannenberg, J. J., Dapprich, S., Daniels, A. D., Farkas, Ö, Foresman, J. B., Ortiz, J. V., Cioslowski, J., and Fox, D. J. (2009) Gaussian 09, revision A.1, Gaussian, Inc., Wallingford, CT.
37. Lin, T.-J. and O'Malley, P. J. (2008) An ONIOM study of the QA site semiquinone in the Rhodobacter sphaeroides photosynthetic reaction centre J. Mol. Struct.: THEOCHEM 870, 31-35
38. A Site J. Am. Chem. Soc. 133, 5525-5537
39. B Site Ubisemiquinone and Ser-L223 in the Bacterial Reaction Center: A Combined Spectroscopic and Computational Perspective Biochemistry 51, 9086-9093
40. Dikanov, S. A. and Bowman, M. K. (1995) Cross-peak lineshape of two-dimensional ESEEM spectra in disordered S=1/2, I=1/2 spin system J. Magn. Reson., Ser. A 116, 125-128
41. Dikanov, S. A., Tyryshkin, A. M., and Bowman, M. K. (2000) Intensity of cross-peaks in HYSCORE spectra of S=1/2, I=1/2 spin systems J. Magn. Reson. 144, 228-242
42. Das, M. R., Connor, H. D., Leniart, D. S., and Freed, J. H. (1970) An Electron Nuclear Double Resonance and Electron Spin Resonance Study of Semiquinones Related to Vitamins K and E J. Am. Chem. Soc. 92, 2258-2268
43. Kirste, B. (1987) ENDOR studies of semiquinone radical ions in liquid crystalline solutions Magn. Reson. Chem. 25, 166-175
44. 13C-enriched ubiquinone radicals. Part 2 J. Chem. Soc., Perkin. Trans. 2 2063-2068
45. O'Malley, P. J. (1998) B3LYP, Hybrid Density Functional Studies of the Durosemiquinone Radical: The Effect of Symmetrical and Asymmetrical Hydrogen Bonding on Spin Densities and Hyperfine Couplings J. Phys. Chem. A 102, 248-253
46. 3 from Escherichia coli Biochemistry 51, 3827-3838 Division