Analysis of the kinetics of P+HA- recombination in membrane-embedded wild-type and mutant Rhodobacter sphaeroides reaction centers between 298 and 77 K indicates that the adjacent negatively charged QA ubiquinone modulates the free energy of P +HA- and may influence the rate of the protein dielectric response

Journal of Physical Chemistry B

Volumn 117, Issue 38, 2013, Pages 11112-11123

  Gibasiewicz, Krzysztof ^a   Pajzderska, Maria ^a   Dobek, Andrzej ^a   Brettel, Klaus ^b   Jones, Michael R ^c  

^a ADAM MICKIEWICZ UNIVERSITY   (Poland)

^b INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^c UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOCHLOROPHYLLS; CHARGE RECOMBINATIONS; DIELECTRIC RESPONSE; LIGHT-INDUCED ELECTRON TRANSFER; PHOTOSYNTHETIC REACTION CENTER; RHODOBACTER SPHAEROIDES; TEMPERATURE DEPENDENCE; TIME-RESOLVED SPECTROSCOPIC STUDIES;

DYNAMICS; ELECTRON ENERGY LEVELS; ELECTRON TRANSITIONS; FREE ENERGY; FREE RADICAL REACTIONS; PLANTS (BOTANY); SPECTROSCOPIC ANALYSIS;

PROTEINS;

BACTERIAL PROTEIN; BACTERIOCHLOROPHYLL; BACTERIOPHEOPHYTIN; PHEOPHYTIN; RECOMBINANT PROTEIN; UBIQUINONE;

ARTICLE; BIOSYNTHESIS; CHEMISTRY; ELECTRON TRANSPORT; GENETICS; METABOLISM; MUTATION; PHOTOSYNTHESIS; RHODOBACTER SPHAEROIDES; SPECTROFLUOROMETRY; STATIC ELECTRICITY; TEMPERATURE; TIME;

BACTERIAL PROTEINS; BACTERIOCHLOROPHYLLS; ELECTRON TRANSPORT; MUTATION; PHEOPHYTINS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; RECOMBINANT PROTEINS; RHODOBACTER SPHAEROIDES; SPECTROMETRY, FLUORESCENCE; STATIC ELECTRICITY; TEMPERATURE; TIME FACTORS; UBIQUINONE;

EID: 84884930370     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp4011235     Document Type: Article

References (47)

1. Woodbury, N. W. T.; Parson, W. W. Nanosecond Fluorescence from Isolated Photosynthetic Reaction Centers of Rhodopseudomonas sphaeroides Biochim. Biophys. Acta 1984, 767, 345-361 (Pubitemid 15218680)
2. Peloquin, J. M.; Williams, J. A. C.; Lin, X.; Alden, R. G.; Taguchi, A. K. W.; Allen, J. P.; Woodbury, N. W. Time-Dependent Thermodynamics During Early Electron-Transfer in Reaction Centers from Rhodobacter sphaeroides Biochemistry 1994, 33, 8089-8100 (Pubitemid 24223831)
3. Wang, H.; Lin, S.; Allen, J. P.; Williams, J. A. C.; Blankert, S.; Laser, C.; Woodbury, N. W. Protein Dynamics Controls the Kinetics of Initial Electron Transfer in Photosynthesis Science 2007, 316, 747-750 (Pubitemid 46717683)
4. Wang, H.; Lin, S.; Katilius, E.; Laser, C.; Allen, J. P.; Williams, J. A. C.; Woodbury, N. W. Unusual Temperature Dependence of Photosynthetic Electron Transfer due to Protein Dynamics J. Phys. Chem. B 2009, 113, 818-824
5. Wang, H.; Hao, Y.; Jiang, Y.; Lin, S.; Woodbury, N. W. The Role of Protein Dynamics in Guiding Electron Transfer Pathways in Reaction Centers from Rhodobacter sphaeroides J. Phys. Chem. B 2012, 116, 711-717
6. Guo, Z.; Woodbury, N. W.; Pan, J.; Lin, S. Protein Dielectric Environment Modulates the Electron-Transfer Pathway in Photosynthetic Reaction Centers Biophys. J. 2012, 103, 1979-1988
7. Frauenfelder, H.; Sligar, S. G.; Wolynes, P. G. The Energy Landscapes and Motions of Proteins Science 1991, 254, 1598-1603 (Pubitemid 21917496)
8. Frauenfelder, H. The Physics of Proteins: An Introduction to Biological Physics and Molecular Biophysics; Chan, S. S.; Chan, W. S., Eds.; Biological and Medical Physics, Biomedical Engineering; Springer Verlag: New York, 2011.
9. Anoxygenic Photosynthetic Bacteria; Blankenship, R. E.; Madigan, M. T.; Bauer, C. E., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands/Boston, MA/London, 1995.
10. Zinth, W.; Wachtveitl, J. The First Picoseconds in Bacterial Photosynthesis-Ultrafast Electron Transfer for the Efficient Conversion of Light Energy ChemPhysChem 2005, 6, 871-880 (Pubitemid 40669550)
11. Shuvalov, V. A.; Parson, W. W. Energies and Kinetics of Radical Pairs Involving Bacteriochlorophyll and Bacteriopheophytin in Bacterial Reaction Centers Proc. Natl. Acad. Sci. U.S.A. 1981, 78, 957-961 (Pubitemid 11100750)
12. Schenck, C. C.; Blankenship, R. E.; Parson, W. W. Radical-Pair Decay Kinetics, Triplet Yields and Delayed Fluorescence from Bacterial Reaction Centers Biochim. Biophys. Acta 1982, 680, 44-59
13. Chidsey, C. E. D.; Kirmaier, C.; Holten, D.; Boxer, S. G. Magnetic Field Dependence of Radical Pair Decay Kinetics and Molecular Triplet Quantum Yield in Quinone-Depleted Bacterial Reaction Centers Biochim. Biophys. Acta 1984, 766, 424-437
14. Ogrodnik, A.; Volk, M.; Letterer, R.; Feick, R.; Michel-Beyerle, M. E. Determination of Free Energies in Reaction Centers of Rb. sphaeroides Biochim. Biophys. Acta 1988, 936, 361-371
15. Tang, C. K.; Williams, J. C.; Taguchi, A. K. W.; Allen, J. P.; Woodbury, N. W. P+HA- Charge Recombination Reaction Rate Constant in Rhodobacter sphaeroides Reaction Centers is Independent of the P/P+ Midpoint Potential Biochemistry 1999, 38, 8794-8799
16. Gibasiewicz, K.; Pajzderska, M. Primary Radical Pair P+H- Lifetime in Rhodobacter sphaeroides with Blocked Electron Transfer to QA. Effect of o-Phenanthroline J. Phys. Chem. B 2008, 112 (6) 1858-1865 (Pubitemid 351316391)
17. Gibasiewicz, K.; Pajzderska, M.; Ziółek, M.; Karolczak, J.; Dobek, A. Internal Electrostatic Control of the Primary Charge Separation and Recombination in Reaction Centers from Rhodobacter sphaeroides Revealed by Femtosecond Transient Absorption J. Phys. Chem. B 2009, 113 (31) 11023-11031
18. - in External Magnetic and Electric Fields. In Anoxygenic Photosynthetic Bacteria; Blankenship, R. E.; Madigan, M. T.; Bauer, C. E., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands/Boston, MA/London, 1995; p 595.
19. Woodbury, N. W. T.; Parson, W. W.; Gunner, M. R; Prince, R. C.; Dutton, P. L. Radical-Pair Energetics and Decay Mechanisms in Reaction Centers Containing Anthraquinones, Naphthoquinones or Benzoquinones in Place of Ubiquinone Biochim. Biophys. Acta 1986, 851, 6-22
20. Woodbury, N. W. T.; Allen, J. P. Electron Transfer in Purple Nonsulfur Bacteria. In Anoxygenic Photosynthetic Bacteria; Blankenship, R. E.; Madigan, M. T.; Bauer, C. E., Eds.; Kluwer Academic Publishers: Dordrecht, The Netherlands/Boston, MA/London, 1995; p 527.
21. Holzapfel, W.; Finkele, U.; Kaiser, W.; Oesterhelt, D.; Scheer, H.; Stilz, H. U.; Zinth, W. Observation of a Bacteriochlorophyll Anion Radical during the Primary Charge Separation in a Reaction Center Chem. Phys. Lett. 1989, 160, 1-7
22. Holzapfel, W.; Finkele, U.; Kaiser, W.; Oesterhelt, D.; Scheer, H.; Stilz, H. U.; Zinth, W. Initial Electron-Transfer in the Reaction Center from Rhodobacter sphaeroides Proc. Natl. Acad. Sci. U.S.A. 1990, 87, 5168-5172
23. Kirmaier, C.; Holten, D. Subpicosecond Characterization of the Optical Properties of the Primary Electron Donor and the Mechanism of the Initial Electron Transfer in Rhodobacter Capsulatus Reaction Centers FEBS Lett. 1988, 239, 211-218
24. Kirmaier, C.; Holten, D. An Assessment of the Mechanism of Initial Electron Transfer in Bacterial Reaction Centers Biochemistry 1991, 30, 609-613
25. Lockhart, D. J.; Kirmaier, C.; Holten, D.; Boxer, S. G. Electric Field Effects on the Initial Electron Transfer Kinetics in Bacterial Photosynthetic Reaction Centers J. Phys. Chem. 1990, 94, 6987-6995
26. Rodriguez, J.; Kirmaier, C.; Johnson, M. R.; Friesner, R. A.; Holten, D.; Sessler, J. L. Picosecond Studies of Electron Transfer in Quinone Substituted Monometalated Porphyrin Dimers: Evidence for Superexchange Mediated Electron Transfer in a Photosynthetic Model System J. Am. Chem. Soc. 1991, 113, 1652-1659
27. Chan, C. K.; DiMagno, T. J.; Chen, L. X.; Norris, J. R.; Fleming, G. R. Mechanism of the Initial Charge Separation in Bacterial Photosynthetic Reaction Centers Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 11202-11206 (Pubitemid 21916008)
28. Deisenhofer, J.; Epp, O.; Miki, K.; Huber, R.; Michel, H. X-ray Structure Analysis of a Membrane Protein Complex. Electron Density Map at 3 A Resolution and a Model of the Chromophores of the Photosynthetic Reaction Center from Rhodopseudomonas viridis J. Mol. Biol. 1984, 180, 385-398
29. Allen, J. P.; Feher, G.; Yeates, T. O.; Komiya, H.; Rees, D. C. Structure of the Reaction Center from Rhodobacter sphaeroides R-26: The Cofactors Proc. Natl. Acad. Sci. U.S.A. 1987, 84, 5730-5734
30. Warren, J. J.; Winkler, J. R.; Gray, H. B. Hopping Maps for Photosynthetic Reaction Centers Coord. Chem. Rev. 2013, 257, 165-170
31. Gibasiewicz, K.; Pajzderska, M.; Potter, J. A.; Fyfe, P. K.; Dobek, A.; Brettel, K.; M. R. Jones, M. R. Mechanism of Recombination of the P+HA- Radical Pair in Mutant Rhodobacter sphaeroides Reaction Centers with Modified Free Energy Gaps between P+BA- and P+HA- J. Phys. Chem. B 2011, 115, 13037
32. Gibasiewicz, K.; Pajzderska, M.; Dobek, A.; Karolczak, J.; Burdziński, G.; Brettel, K.; Jones, M. R. Submitted for publication.
33. Ridge, J. P.; van Brederode, M. E.; Goodwin, M. G.; van Grondelle, R.; Jones, M. R. Mutations That Modify or Exclude Binding of the Q(A) Ubiquinone and Carotenoid in the Reaction Center from Rhodobacter sphaeroides Photosynth. Res. 1999, 59, 9-26 (Pubitemid 29221123)
34. McAuley, K. E.; Fyfe, P. K.; Ridge, J. P.; Cogdell, R. J.; Isaacs, N. W.; Jones, M. R. Ubiquinone Binding, Ubiquinone Exclusion, and Detailed Cofactor Conformation in a Mutant Bacterial Reaction Center Biochemistry 2000, 39, 15032-15043
35. Pawlowicz, N. P.; van Grondelle, R.; van Stokkum, I. H. M.; Jones, M. R.; Breton, J.; Groot, M. L. Identification of the First Steps in Charge Separation in Bacterial Photosynthetic Reaction Centers of Rhodobacter sphaeroides by Ultrafast Mid-Infrared Spectroscopy: Electron Transfer and Protein Dynamics Biophys. J. 2008, 95, 1268-1284
36. Jones, M. R.; Visschers, R. W.; van Grondelle, R.; Hunter, C. N. Construction and Characterization of a Mutant of Rhodobacter Sphaeroides with the Reaction Center as the Sole Pigment-Protein Complex Biochemistry 1992, 31, 4458-4465
37. Jones, M. R.; Fowler, G. J. S.; Gibson, L. C. D.; Grief, G. G.; Olsen, J. D.; Crielaard, W.; Hunter, C. N. Mutants of Rhodobacter Sphaeroides Lacking One or More Pigment-Protein Complexes and Complementation with Reaction-Centre, LH1, and LH2 Genes Mol. Microbiol. 1992, 6, 1173-1184
38. Jones, M. R.; Heer-Dawson, M.; Mattioli, T. A.; Hunter, C. N.; Robert, B. Site-Specific Mutagenesis of the Reaction Centre from Rhodobacter Sphaeroides Studied by Fourier Transform Raman Spectroscopy: Mutations at Tyrosine M210 Do Not Affect the Electronic Structure of the Primary Donor FEBS Lett. 1994, 339, 18-24
39. McAuley-Hecht, K. E.; Fyfe, P. K.; Ridge, J. P.; Prince, S. M.; Hunter, C. N.; Isaacs, N. W.; Cogdell, R. J.; Jones, M. R. Structural Studies of Wild-Type and Mutant Reaction Centers from an Antenna-Deficient Strain of Rhodobacter Sphaeroides: Monitoring the Optical Properties of the Complex from Bacterial Cell to Crystal Biochemistry 1998, 37, 4740-4750 (Pubitemid 28175953)
40. Okamura, M. Y.; Isaacson, R. A.; Feher, G. Primary Acceptor in Bacterial Photosynthesis: Obligatory Role of Ubiquinone in Photoactive Reaction Centers of Rhodopseudomonas spheroides Proc. Natl. Acad. Sci. U.S.A. 1975, 79, 3491-3495
41. Michel, H.; Epp, O.; Deisenhofer, J. Pigment-Protein Interactions in the Photosynthetic Reaction Centre from Rhodopseudomonas Viridis EMBO J. 1986, 5, 2445-2451
42. Byrdin, M.; Thiagarajan, V.; Villette, S.; Espagne, A.; Brettel, K. Use of Ruthenium Dyes for Subnanosecond Detector Fidelity Testing in Real Time Transient Absorption Rev. Sci. Instrum. 2009, 80, 043102
43. Gibasiewicz, K.; Pajzderska, M.; Karolczak, J.; Burdziński, G.; Dobek, A.; Jones, M. R. Primary Electron Transfer Reactions in Membrane-Bound Open and Closed Reaction Centers from Purple Bacterium Rb. Sphaeroides Acta Phys. Pol., A 2012, 122, 263-268
44. Parson, W. W.; Clayton, R. K.; Cogdell, R. J. Excited States of Photosynthetic Reaction Centers at Low Redox Potentials Biochim. Biophys. Acta 1975, 387, 265-278
45. Michel-Beyerle, M. E.; Scheer, H.; Seidlitz, H.; Tempus, D. Magnetic Field Effect on Triplets and Radical Ions in Reaction Centers of Photosynthetic Bacteria FEBS Lett. 1980, 110, 129-132 (Pubitemid 10136618)
46. Heller, B. A.; Holten, D.; Kirmaier, C. Effects of Asp Residues near the L-Side Pigments in Bacterial Reaction Centers Biochemistry 1996, 35, 15418-15427 (Pubitemid 26408878)
47. Katilius, E.; Turanchik, T.; Lin, S.; Taguchi, A. K. W.; Woodbury, N. W. B-Side Electron Transfer in a Rhodobacter Sphaeroides Reaction Center Mutant in Which the B-Side Monomer Bacteriochlorophyll Is Replaced with Bacteriopheophytin J. Phys. Chem. B 1999, 103, 7386-7389