Protein dielectric environment modulates the electron-transfer pathway in photosynthetic reaction centers

Biophysical Journal

Volumn 103, Issue 9, 2012, Pages 1979-1988

  Guo, Zhi ^a,b   Woodbury, Neal W ^a   Pan, Jie ^a,c   Lin, Su ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPARTIC ACID; BACTERIAL PROTEIN; BACTERIOCHLOROPHYLL; BACTERIOPHEOPHYTIN; PHEOPHYTIN; UBIQUINONE;

AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; ELECTRON TRANSPORT; GENETICS; KINETICS; LIGHT; METABOLISM; MISSENSE MUTATION; MOLECULAR GENETICS; PH; PHOTOSYNTHESIS; RHODOBACTER SPHAEROIDES; STATIC ELECTRICITY;

AMINO ACID SEQUENCE; ASPARTIC ACID; BACTERIAL PROTEINS; BACTERIOCHLOROPHYLLS; ELECTRON TRANSPORT; HYDROGEN-ION CONCENTRATION; KINETICS; LIGHT; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PHEOPHYTINS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; RHODOBACTER SPHAEROIDES; STATIC ELECTRICITY; UBIQUINONE;

RHODOBACTER SPHAEROIDES;

EID: 84868560975     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.09.027     Document Type: Article

References (53)

1. R.A. Marcus Electrostatic free energy and other properties of states having nonequilibrium polarization. I J. Chem. Phys. 24 1956 979 989
2. R.D.L. Kronig On the theory of dispersion of x-rays J. Opt. Soc. Am. 12 1926 547 556
3. D.N. LeBard, and D.V. Matyushov Protein-water electrostatics and principles of bioenergetics Phys. Chem. Chem. Phys. 12 2010 15335 15348
4. -. in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay Proc. Natl. Acad. Sci. USA 95 1998 11679 11684
5. B.H. McMahon, and J.D. Müller G.U. Nienhaus Electron transfer and protein dynamics in the photosynthetic reaction center Biophys. J. 74 1998 2567 2587
6. H. Wang, and S. Lin N.W. Woodbury Protein dynamics control the kinetics of initial electron transfer in photosynthesis Science 316 2007 747 750
7. H. Wang, and S. Lin N.W. Woodbury Unusual temperature dependence of photosynthetic electron transfer due to protein dynamics J. Phys. Chem. B 113 2009 818 824
8. - lifetime in Rhodobacter sphaeroides with blocked electron transfer to Q(A). Effect of o-phenanthroline J. Phys. Chem. B 112 2008 1858 1865
9. H. Wang, and Y. Hao N.W. Woodbury The role of protein dynamics in guiding electron transfer pathways in reaction centers from Rhodobacter sphaeroides J. Phys. Chem. B 116 2011 711 717
10. A.L.M. Haffa, and S. Lin N.W. Woodbury The dependence of the initial electron-transfer rate on driving force in Rhodobacter sphaeroides reaction centers J. Phys. Chem. B 106 2002 7376 7384
11. V. Nagarajan, and W.W. Parson C. Schenck Effect of specific mutations of tyrosine-(M)210 on the primary photosynthetic electron-transfer process in Rhodobacter sphaeroides Proc. Natl. Acad. Sci. USA 87 1990 7888 7892
12. V. Nagarajan, and W.W. Parson C.C. Schenck Kinetics and free energy gaps of electron-transfer reactions in Rhodobacter sphaeroides reaction centers Biochemistry 32 1993 12324 12336
13. J.O. Goldsmith, and S.G. Boxer Rapid isolation of bacterial photosynthetic reaction centers with an engineered poly-histidine tag Biochim. Biophys. Acta 1276 1996 171 175
14. A.L.M. Haffa, and S. Lin N.W. Woodbury Controlling the pathway of photosynthetic charge separation in bacterial reaction centers J. Phys. Chem. B 108 2003 4 7
15. M.Y. Okamura, R.A. Isaacson, and G. Feher Primary acceptor in bacterial photosynthesis: obligatory role of ubiquinone in photoactive reaction centers of Rhodopseudomonas spheroides Proc. Natl. Acad. Sci. USA 72 1975 3491 3495
16. J. Pan, and S. Lin N.W. Woodbury Carotenoid excited-state properties in photosynthetic purple bacterial reaction centers: effects of the protein environment J. Phys. Chem. B 115 2011 7058 7068
17. I.H.M. van Stokkum, D.S. Larsen, and R. van Grondelle Global and target analysis of time-resolved spectra Biochim. Biophys. Acta 1657 2004 82 104
18. R.E. Georgescu, E.G. Alexov, and M.R. Gunner Combining conformational flexibility and continuum electrostatics for calculating pK(a)s in proteins Biophys. J. 83 2002 1731 1748
19. Y. Song, J. Mao, and M.R. Gunner MCCE2: improving protein pKa calculations with extensive side chain rotamer sampling J. Comput. Chem. 30 2009 2231 2247
20. L.L.C. Schrodinger The PyMOL Molecular Graphics System, version 1.3r1 2010 Schrodinger New York
21. A. Nicholls, and B. Honig A rapid finite difference algorithm, utilizing successive over-relaxation to solve the Poisson-Boltzmann equation J. Comput. Chem. 12 1991 435 445
22. C. Kirmaier, and D. Holten D.C. Youvan Electron transfer in a genetically modified bacterial reaction center containing a heterodimer Proc. Natl. Acad. Sci. USA 85 1988 7562 7566
23. C. Kirmaier, and L. Laporte D. Holten The nature and dynamics of the charge-separated intermediate in reaction centers in which bacteriochlorophyll replaces the photoactive bacteriopheophytin. 2. The rates and yields of charge separation and recombination J. Phys. Chem. 99 1995 8910 8917
24. M.H. Vos, and M.R. Jones J.L. Martin Vibrational dephasing of long- and short-lived primary donor excited states in mutant reaction centers of Rhodobacter sphaeroides Biochemistry 35 1996 2687 2692
25. J. Breton, and J. Martin D. Youvan Ground state and femtosecond transient absorption spectroscopy of a mutant of Rhodobacter capsulatus which lacks the initial electron acceptor bacteriopheophytin M.-E. Michel-Beyerle, Reaction Centers of Photosynthetic Bacteria 1990 Springer-Verlag Berlin 293 302
26. L.M. McDowell, and D. Gaul C.C. Schenck Investigation into the source of electron transfer asymmetry in bacterial reaction centers Biochemistry 30 1991 8315 8322
27. M. Volk, and G. Aumeier M.-E. Michel-Beyerle Energetics and mechanism of primary charge separation in bacterial photosynthesis. A comparative study on reaction centers of Rhodobacter sphaeroides and Chloroflexus aurantiacus J. Phys. Chem. B 102 1998 735 751
28. K. Gibasiewicz, and M. Pajzderska A. Dobek 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 113 2009 11023 11031
29. T. Arlt, and S. Schmidt W. Zinth The accessory bacteriochlorophyll: a real electron carrier in primary photosynthesis Proc. Natl. Acad. Sci. USA 90 1993 11757 11761
30. A.R. Holzwarth, and M.G. Müller Energetics and kinetics of radical pairs in reaction centers from Rhodobacter sphaeroides. A femtosecond transient absorption study Biochemistry 35 1996 11820 11831
31. C. Kirmaier, D. Holten, and W.W. Parson Temperature and detection-wavelength dependence of the picosecond electron-transfer kinetics measured in Rhodopseudomonas sphaeroides reaction centers. Resolution of new spectral and kinetic components in the primary charge-separation process Biochim. Biophys. Acta 810 1985 33 48
32. + midpoint potential Biochemistry 38 1999 8794 8799
33. C. Kirmaier, and D. Gaul C.C. Schenck Charge separation in a reaction center incorporating bacteriochlorophyll for photoactive bacteriopheophytin Science 251 1991 922 927
34. T. Arlt, and B. Dohse D. Oesterhelt Electron transfer dynamics of Rhodopseudomonas viridis reaction centers with a modified binding site for the accessory bacteriochlorophyll Biochemistry 35 1996 9235 9244
35. V.A. Shuvalov, and W.W. Parson Energies and kinetics of radical pairs involving bacteriochlorophyll and bacteriopheophytin in bacterial reaction centers Proc. Natl. Acad. Sci. USA 78 1981 957 961
36. C.C. Schenck, R.E. Blankenship, and W.W. Parson Radical-pair decay kinetics, triplet yields and delayed fluorescence from bacterial reaction centers Biochim. Biophys. Acta 680 1982 44 59
37. - J. Phys. Chem. B 115 2011 13037 13050
38. - when detected in delayed emission and in absorption J. Phys. Chem. 98 1994 3432 3439
39. J.M. Peloquin, and J.C. Williams N.W. Woodbury Time-dependent thermodynamics during early electron transfer in reaction centers from Rhodobacter sphaeroides Biochemistry 33 1994 8089 8100
40. W. Holzapfel, and U. Finkele W. Zinth Observation of a bacteriochlorophyll anion radical during the primary charge separation in a reaction center Chem. Phys. Lett. 160 1989 1 7
41. A.G. Yakovlev, A.Y. Shkuropatov, and V.A. Shuvalov Nuclear wavepacket motion producing a reversible charge separation in bacterial reaction centers FEBS Lett. 466 2000 209 212
42. K. Wynne, and G. Haran R.M. Hochstrasser Femtosecond infrared spectroscopy of low-lying excited states in reaction centers of Rhodobacter sphaeroides J. Phys. Chem. 100 1996 5140 5148
43. N.W.T. Woodbury, and W.W. Parson Nanosecond fluorescence from isolated photosynthetic reaction centers of Rhodopseudomonas sphaeroides Biochim. Biophys. Acta 767 1984 345 361
44. M. Du, and S.J. Rosenthal G.R. Fleming Femtosecond spontaneous-emission studies of reaction centers from photosynthetic bacteria Proc. Natl. Acad. Sci. USA 89 1992 8517 8521
45. Y. Jia, and T.J. DiMagno G.R. Fleming Primary charge separation in mutant reaction centers of Rhodobacter capsulatus J. Phys. Chem. 97 1993 13180 13191
46. I.H.M. van Stokkum, and L.M.P. Beekman R. van Grondelle Primary electron transfer kinetics in membrane-bound Rhodobacter sphaeroides reaction centers: a global and target analysis Biochemistry 36 1997 11360 11368
47. L. Laporte, and C. Kirmaier D. Holten Free-energy dependence of the rate of electron transfer to the primary quinone in beta-type reaction centers Chem. Phys. 197 1995 225 237
48. G.R. Grimsley, J.M. Scholtz, and C.N. Pace A summary of the measured pK values of the ionizable groups in folded proteins Protein Sci. 18 2009 247 251
49. C. Zscherp, and R. Schlesinger J. Heberle In situ determination of transient pKa changes of internal amino acids of bacteriorhodopsin by using time-resolved attenuated total reflection Fourier-transform infrared spectroscopy Proc. Natl. Acad. Sci. USA 96 1999 5498 5503
50. M.H.M. Olsson, and C.R. Sondergaard J.H. Jensen PROPKA3: consistent treatment of internal and surface residues in empirical pKa predictions J. Chem. Theory Comput. 7 2011 525 537
51. C.R. Sondergaard, and M.H.M. Olsson J.H. Jensen Improved treatment of ligands and coupling effects in empirical calculation and rationalization of pKa values J. Chem. Theory Comput. 7 2011 2284 2295
52. M.R. Gunner, A. Nicholls, and B. Honig Electrostatic potentials in Rhodopseudomonas viridis reaction centers: implications for the driving force and directionality of electron transfer J. Phys. Chem. 100 1996 4277 4291
53. N.P. Pawlowicz, and R. van Grondelle M.L. Groot 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. 95 2008 1268 1284