Early bacteriopheophytin reduction in charge separation in reaction centers of Rhodobacter sphaeroides

Biophysical Journal

Volumn 104, Issue 11, 2013, Pages 2493-2502

  Zhu, Jingyi ^a   Van Stokkum, Ivo H M ^a   Paparelli, Laura ^a   Jones, Michael R ^b   Groot, Marie Louise ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOPHEOPHYTIN; PHEOPHYTIN;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; ELECTRON TRANSPORT; ENZYMOLOGY; METABOLISM; PHOTOSYNTHESIS; RHODOBACTER SPHAEROIDES;

ELECTRON TRANSPORT; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PHEOPHYTINS; PHOTOSYNTHETIC REACTION CENTER COMPLEX PROTEINS; RHODOBACTER SPHAEROIDES;

BACTERIA (MICROORGANISMS); RHODOBACTER SPHAEROIDES;

EID: 84878819554     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2013.04.026     Document Type: Article

References (68)

1. W. Zinth, and J. Wachtveitl The first picoseconds in bacterial photosynthesis - ultrafast electron transfer for the efficient conversion of light energy ChemPhysChem 6 2005 871 880
2. M.R. Jones The petite purple photosynthetic powerpack Biochem. Soc. Trans. 37 2009 400 407
3. 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
4. H. Lee, Y.C. Cheng, and G.R. Fleming Coherence dynamics in photosynthesis: protein protection of excitonic coherence Science 316 2007 1462 1465
5. E. Collini, and C.Y. Wong G.D. Scholes Coherently wired light-harvesting in photosynthetic marine algae at ambient temperature Nature 463 2010 644 647
6. G.S. Engel, and T.R. Calhoun G.R. Fleming Evidence for wavelike energy transfer through quantum coherence in photosynthetic systems Nature 446 2007 782 786
7. S. Lin, A.K.W. Taguchi, and N.W. Woodbury Excitation wavelength dependence of energy transfer and charge separation in reaction centers from Rhodobacter sphaeroides: evidence for adiabatic electron transfer J. Phys. Chem. 100 1996 17067 17078
8. A.G. Yakovlev, A.Y. Shkuropatov, and V.A. Shuvalov Nuclear wavepacket motion between P and P(+)B(A)(-) potential surfaces with subsequent electron transfer to H(A) in bacterial reaction centers. 1. Room temperature Biochemistry 41 2002 2667 2674
9. A.M. Streltsov, and T.J. Aartsma V.A. Shuvalov Oscillations within the B-L absorption band of Rhodobacter sphaeroides reaction centers upon 30 femtosecond excitation at 865 nm Chem. Phys. Lett. 266 1997 347 352
10. M.H. Vos, and M.R. Jones J.L. Martin Coherent nuclear dynamics at room temperature in bacterial reaction centers Proc. Natl. Acad. Sci. USA 91 1994 12701 12705
11. M.H. Vos, and F. Rappaport J.L. Martin Visualization of coherent nuclear motion in a membrane-protein by femtosecond spectroscopy Nature 363 1993 320 325
12. W. Zinth, and P. Huppmann J. Wachtveitl Ultrafast spectroscopy of the electron transfer in photosynthetic reaction centres: towards a better understanding of electron transfer in biological systems Philos. Trans. A Math. Phys. Eng. Sci 356 1998 465 476
13. M. Bixon, J. Jortner, and M.E. Michelbeyerle A kinetic-analysis of the primary charge separation in bacterial photosynthesis - energy gaps and static heterogeneity Chem. Phys. 197 1995 389 404
14. J. Jortner Temperature-dependent activation energy for electron transfer between biological molecules J. Chem. Phys. 64 1976 4860 4867
15. P. Huppman, and T. Arlt W. Zinth Kinetics, energetics, and electronic coupling of the primary electron transfer reactions in mutated reaction centers of Blastochloris viridis Biophys. J. 82 2002 3186 3197
16. M. Bixon, J. Jortner, and M.E. Michelbeyerle On the mechanism of the primary charge separation in bacterial photosynthesis Biochim. Biophys. Acta 1056 1991 301 315
17. L.M.P. Beekman, and I.H.M. vanStokkum R. vanGrondelle Primary electron transfer in membrane-bound reaction centers with mutations at the M210 position J. Phys. Chem. 100 1996 7256 7268
18. R.A. Marcus, and N. Sutin Electron transfers in chemistry and biology Biochim. Biophys. Acta 811 1985 265 322
19. 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
20. 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
21. N.W. Woodbury, and J.M. Peloquin J.P. Allen Relationship between thermodynamics and mechanism during photoinduced charge separation in reaction centers from Rhodobacter sphaeroides Biochemistry 33 1994 8101 8112
22. R.J. Stanley, and S.G. Boxer Oscillations in the spontaneous fluorescence from photosynthetic reaction centers J. Phys. Chem. 99 1995 859 863
23. R.J. Stanley, B. King, and S.G. Boxer Excited state energy transfer pathways in photosynthetic reaction centers. 1. Structural symmetry effects J. Phys. Chem. 100 1996 12052 12059
24. M.H. Vos, M.R. Jones, and J.L. Martin Vibrational coherence in bacterial reaction centers: spectroscopic characterisation of motions active during primary electron transfer Chem. Phys. 233 1998 179 190
25. S. Sporlein, W. Zinth, and J. Wachtveitl Vibrational coherence in photosynthetic reaction centers observed in the bacteriochlorophyll anion band J. Phys. Chem. B 102 1998 7492 7496
26. M.H. Vos, and C. Rischel J.L. Martin Electrochromic detection of a coherent component in the formation of the charge pair P(+)H(L)(-) in bacterial reaction centers Biochemistry 39 2000 8353 8361
27. * and BA: Electron-transfer pathways in native and mutant GM203L bacterial reaction centers Chem. Phys. 319 2005 297 307
28. A.M. Streltsov, and S.I.E. Vulto V.A. Shuvalov B-A and B-B absorbance perturbations induced by coherent nuclear motions in reaction centers from Rhodobacter sphaeroides upon 30-fs excitation of the primary donor J. Phys. Chem. B 102 1998 7293 7298
29. M.E. van Brederode, and F. van Mourik R. van Grondelle Multiple pathways for ultrafast transduction of light energy in the photosynthetic reaction center of Rhodobacter sphaeroides Proc. Natl. Acad. Sci. USA 96 1999 2054 2059
30. M.E. Van Brederode, and M.R. Jones R. Van Grondelle A new pathway for transmembrane electron transfer in photosynthetic reaction centers of Rhodobacter sphaeroides not involving the excited special pair Biochemistry 36 1997 6855 6861
31. L.B. Huang, and N. Ponomarenko D.M. Tiede Cofactor-specific photochemical function resolved by ultrafast spectroscopy in photosynthetic reaction center crystals Proc. Natl. Acad. Sci. USA 109 2012 4851 4856
32. M.L. Groot, and N.P. Pawlowicz R. van Grondelle Initial electron donor and acceptor in isolated Photosystem II reaction centers identified with femtosecond mid-IR spectroscopy Proc. Natl. Acad. Sci. USA 102 2005 13087 13092
33. A.R. Holzwarth, and M.G. Müller M. Rögner Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: pheophytin is the primary electron acceptor Proc. Natl. Acad. Sci. USA 103 2006 6895 6900
34. E. Romero, and I.H.M. van Stokkum R. van Grondelle Two different charge separation pathways in photosystem II Biochemistry 49 2010 4300 4307
35. I.V. Shelaev, and F.E. Gostev V.A. Shuvalov P680 (P(D1)P(D2)) and Chl(D1) as alternative electron donors in photosystem II core complexes and isolated reaction centers J. Photochem. Photobiol. B 104 2011 44 50
36. K. Acharya, and V. Zazubovich R. Jankowiak Primary electron donor(s) in isolated reaction center of photosystem II from Chlamydomonas reinhardtii J. Phys. Chem. B 116 2012 4860 4870
37. H.Y. Wang, and S. Lin N.W. Woodbury Protein dynamics control the kinetics of initial electron transfer in photosynthesis Science 316 2007 747 750
38. H.Y. Wang, S. Lin, and N.W. Woodbury Excitation wavelength dependence of primary charge separation in reaction centers from Rhodobacter sphaeroides J. Phys. Chem. B 112 2008 14296 14301
39. H.Y. 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
40. J. Fajer, and D.C. Brune L.D. Spaulding Primary charge separation in bacterial photosynthesis: oxidized chlorophylls and reduced pheophytin Proc. Natl. Acad. Sci. USA 72 1975 4956 4960
41. J.T.M. Kennis, and A.Y. Shkuropatov T.J. Aartsma Formation of a long-lived P+BA- state in plant pheophytin-exchanged reaction centers of Rhodobacter sphaeroides R26 at low temperature Biochemistry 36 1997 16231 16238
42. B. Carter, and S.G. Boxer C. Kirmaier Trapping the P+B(L)- initial intermediate state of charge separation in photosynthetic reaction centers from Rhodobacter capsulatus Biochemistry 48 2009 2571 2573
43. Y. Kakitani, and A. Hou H. Nagae Rates of the initial two steps of electron transfer in reaction centers from Rhodobacter sphaeroides as determined by singular-value decomposition followed by global fitting Chem. Phys. Lett. 492 2010 142 149
44. K.E. McAuley-Hecht, and P.K. Fyfe M.R. Jones 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 37 1998 4740 4750
45. M.L. Groot, L.J. van Wilderen, and M. Di Donato Time-resolved methods in biophysics. 5. Femtosecond time-resolved and dispersed infrared spectroscopy on proteins Photochem. Photobiol. Sci. 6 2007 501 507
46. 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
47. K.M. Mullen, and I.H.M. van Stokkum TIMP: an R package for modeling multi-way spectroscopic measurements J. Stat. Softw. 18 2007 1 46
48. K. Gibasiewicz, and M. Pajzderska A. Dobek Excitation and electron transfer in reaction centers from Rhodobacter sphaeroides probed and analyzed globally in the 1-nanosecond temporal window from 330 to 700 nm Phys. Chem. Chem. Phys. 11 2009 10484 10493
49. C. Kirmaier, and D. Gaul C.C. Schenck Charge separation in a reaction center incorporating bacteriochlorophyll for photoactive bacteriopheophytin Science 251 1991 922 927
50. I.H. van Stokkum, and L.M. 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
51. A. Ogrodnik, and W. Keupp M.E. Michelbeyerle Inhomogeneity of radical pair energies in photosynthetic reaction centers revealed by differences in recombination dynamics of P+H(A-) when detected in delayed emission and in absorption J. Phys. Chem. 98 1994 3432 3439
52. D.C. Arnett, and C.C. Moser N.F. Scherer The first events in photosynthesis: electronic coupling and energy transfer dynamics in the photosynthetic reaction center from Rhodobacter sphaeroides J. Phys. Chem. B 103 1999 2014 2032
53. A. de la Lande, and J. Řezáč D.R. Salahub Transmission coefficients for chemical reactions with multiple states: role of quantum decoherence J. Am. Chem. Soc. 133 2011 3883 3894
54. M.L. Groot, and J.Y. Yu G.R. Fleming Three-pulse photon echo measurements on the accessory pigments in the reaction center of Rhodobacter sphaeroides J. Phys. Chem. B 102 1998 5923 5931
55. J.A. Jackson, and S. Lin N.W. Woodbury Energy transfer in Rhodobacter sphaeroides reaction centers with the initial electron donor oxidized or missing J. Phys. Chem. B 101 1997 5747 5754
56. M.H. Vos, J. Breton, and J.L. Martin Electronic energy transfer within the hexamer cofactor system of bacterial reaction centers J. Phys. Chem. B 101 1997 9820 9832
57. K.M. Pelzer, and G.B. Griffin G.S. Engel Inhomogeneous dephasing masks coherence lifetimes in ensemble measurements J. Chem. Phys. 136 2012 164508
58. D.V. Matyushov, and G.A. Voth Reorganization parameters of electronic transitions in electronically delocalized systems. 1. Charge transfer reactions J. Phys. Chem. A 104 2000 6470 6484
59. D.V. Matyushov, and G.A. Voth Reorganization parameters of electronic transitions in electronically delocalized systems. 2. Optical spectra J. Phys. Chem. A 104 2000 6485 6494
60. J. Linnanto, A. Freiberg, and J. Korppi-Tommola Quantum chemical simulations of excited-state absorption spectra of photosynthetic bacterial reaction center and antenna complexes J. Phys. Chem. B 115 2011 5536 5544
61. C. Kirmaier, and D. Holten Evidence that a distribution of bacterial reaction centers underlies the temperature and detection-wavelength dependence of the rates of the primary electron-transfer reactions Proc. Natl. Acad. Sci. USA 87 1990 3552 3556
62. M.S. Graige, G. Feher, and M.Y. Okamura Conformational gating of the electron transfer reaction QA-×QB-> QAQB-× in bacterial reaction centers of Rhodobacter sphaeroides determined by a driving force assay Proc. Natl. Acad. Sci. USA 95 1998 11679 11684
63. J.L. Li, and D. Gilroy M.R. Gunner Kinetic phases in the electron transfer from P+QA-QB to P+QAQB- and the associated processes in Rhodobacter sphaeroides R-26 reaction centers Biochemistry 37 1998 2818 2829
64. D. Kleinfeld, M.Y. Okamura, and G. Feher Electron-transfer kinetics in photosynthetic reaction centers cooled to cryogenic temperatures in the charge-separated state: evidence for light-induced structural changes Biochemistry 23 1984 5780 5786
65. N. Ginet, and J. Lavergne Conformational control of the Q(A) to Q(B) electron transfer in bacterial reaction centers: evidence for a frozen conformational landscape below -25 degrees C J. Am. Chem. Soc. 130 2008 9318 9331
66. M.Y. Okamura, and M.L. Paddock G. Feher Proton and electron transfer in bacterial reaction centers Biochim. Biophys. Acta. 1458 2000 148 163
67. A.B. Wöhri, and G. Katona R. Neutze Light-induced structural changes in a photosynthetic reaction center caught by Laue diffraction Science 328 2010 630 633
68. F. van Mourik, M. Reus, and A.R. Holzwarth Long-lived charge-separated states in bacterial reaction centers isolated from Rhodobacter sphaeroides Biochim. Biophys. Acta. 1504 2001 311 318