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The Acceptor Quinones of Purple Photosynthetic Bacteria — Structure and Spectroscopy

  • Colin A. WraightEmail author
  • Marilyn R. Gunner
Chapter
Part of the Advances in Photosynthesis and Respiration book series (AIPH, volume 28)

Summary

Type II reaction centers (RCs) have two acceptor quinones that act in series. The primary quinone, QA, cycles between the oxidized quinone and singly reduced semiquinone. QA is tightly bound to the protein as aprosthetic group. The secondary quinone, QB, is reduced by Q A , first to the semiquinone and then to the doubly reduced, fully protonated quinol, QH2. QB freely associates with the protein in the quinone and quinol states. The properties of the two quinones that facilitate this process are largely determined by the nature of the two quinone binding sites. Many reaction center crystal structures show these interactions, although there are significant uncertainties in the conformations of the two quinones, and in the significance of the variable location of QB in the protein. Consequently the influence of structure on quinone function is only very crudely understood. These issues are discussed with emphasis on the quinone reactions in the reaction center from the photosynthetic bacterium, Rhodobacter (Rba.) sphaeroides, which is the best characterized. The structural features of the quinones and their local protein environments are examined in the light of extensive spectroscopic studies, especially by Fourier transform infra-red spectroscopy (FTIR), electron paramagnetic resonance (EPR) and electron nuclear double resonance (ENDOR), on the quinones in their functional redox states.

Keywords

Electron Paramagnetic Resonance Rhodobacter Sphaeroides Photosynthetic Reaction Center Electron Spin Echo Envelope Modulation Acceptor Quinone 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

BChl

bacteriochlorophyll

Bphe

bacteriopheophytin

Blc.

Blastochloris

DFT

density functional theory

ENDOR

Electron Nuclear Double Resonance

EPR

Electron Paramagnetic Resonance

FTIR

Fourier Transform Infrared Spectroscopy

IR

infra-red

NMR

Nuclear Magnetic Resonance

QA,B

primary and secondary quinone acceptors

Rba.

Rhodobacter

RC

reaction center

UQ

ubiquinone (2,3-dimethoxy -5-methyl-6-isoprenyl-1,4-benzoquinone)

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References

  1. Abresch EC, Paddock ML, Stowell MHB, McPhillips TM, Axelrod HL, Soltis SM, Rees DC, Okamura MY and Feher G (1998) Identification of proton transfer pathways in the X-ray crystal structure of the bacterial reaction center from Rhodobacter sphaeroides. Photosynth Res 55: 119–125Google Scholar
  2. Alexov E and Gunner MR (1999) Calculated protein and proton motions coupled to electron transfer: Electron transfer from QA - to QB in bacterial photosynthetic reaction centers. Biochemistry 38: 8254–8270Google Scholar
  3. Alexov E, Miksovska J, Baciou L, Schiffer M, Hanson DK, Sebban P and Gunner MR (2000) Modeling effects of mutations on the free energy of the first electron transfer from QA - to QB in photosynthetic reaction centers. Biochemistry 39: 5940–5952PubMedGoogle Scholar
  4. Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1987a) Structure of the reaction center from Rhodobacter sphaeroides R-26: The cofactors. Proc Natl Acad Sci USA 84: 5730–5734PubMedGoogle Scholar
  5. Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1987b) Structure of the reaction center from Rhodobacter sphaeroides R-26: The protein subunits. Proc Natl Acad Sci USA 84: 6162–6166PubMedGoogle Scholar
  6. Allen JP, Feher G, Yeates TO, Komiya H and Rees DC (1988) Structure of the Reaction Center from Rhodobacter sphaeroides R-26: Protein-cofactor (quinones and Fe2+) Interactions. Proc Natl Acad Sci USA 85: 8487–8491PubMedGoogle Scholar
  7. Allen JP, Williams JC, Graige M, Paddock ML, Labahn A, Feher G and Okamura MY (1998) Free energy dependence of the direct charge recombination from the primary and secondary quinones in reaction centers from Rhodobacter sphaeroides. Photosynth Res 55: 227–233Google Scholar
  8. Arnold W and Clayton RK (1960) The first step in photosynthesis: Evidence for its electronic nature. Proc Natl Acad Sci USA 46: 769–776PubMedGoogle Scholar
  9. Arnoux B, Gaucher JF, Ducruix A and Reiss-Husson F (1995) Structure of the photochemical-reaction center of a spheroidenecontaining purple bacterium, Rhodobacter sphaeroides Y, at 3 Å resolution. Acta Crystallographica D 51: 368–379Google Scholar
  10. Badger RM and Bauer SH (1937) Spectroscopic studies of the hydrogen bond. II. The shift of the O-H vibrational frequency in the formation of the hydrogen bond. J Chem Phys 5: 839–851Google Scholar
  11. Bauscher M and Mäntele W (1992) Electrochemical and infraredspectroscopic characterization of redox reactions of p-quinones. J Phys Chem 96: 11101–11108Google Scholar
  12. Baxter RHG, Ponomarenko N, Srajer V, Pahl R, Moffat K and Norris JR (2004) Time-resolved crystallographic studies of light-induced structural changes in the photosynthetic reaction center. Proc Nat Acad Sci USA 101: 5982–5987PubMedGoogle Scholar
  13. Bellamy LJ (1968) Advances in Infrared Group Frequencies. Methuen & Co. Ltd, LondonGoogle Scholar
  14. Bellamy LJ (1975) The Infrared Spectra of Complex Molecules. Chapman and Hall, London, New YorkGoogle Scholar
  15. Bellamy LJ and Pace RJ (1970) Hydrogen bonding in alcohols and phenols. III. Hydrogen bonds between alcohols and carbonyl groups. Spectrochimica Acta A 27: 705–713Google Scholar
  16. Beroza P, Fredkin DR, Okamura MY and Feher G (1995) Electrostatic calculations of amino acid titration electron transfer, QA -QB → QAQB -, in the reaction center. Biophys J 68: 2233–2250PubMedGoogle Scholar
  17. Blankenship RE and Parson WW (1979) The involvement of iron and ubiquinone in electron transfer reactions mediated by reaction centers from photosynthetic bacteria. Biochim Biophys Acta 545: 429–444PubMedGoogle Scholar
  18. Bloom H, Briggs LH and Cleverley B (1959) Physical properties of anthraquinone and its derivatives. Part I. Infrared spectra. J Chem Soc 1959: 178–185Google Scholar
  19. Boesch SE and Wheeler RA (1997) Structures and properties of ubiquinone-1 and its radical anion predicted from a hybrid Hartree-Fock/density functional method. J Phys Chem A 101: 5799–5804Google Scholar
  20. Bosch MK, Gast P, Hoff AJ, Spoyalov AP and Tsvetkov YD (1995) The primary acceptor quinone QA in reaction centers of Rhodobacter sphaeroides R26 is hydrogen bonded to the Nδ (1)-H of His M219. An electron spin echo study of QA -•. Chem Phys Lett 239: 306–312Google Scholar
  21. 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: 247–252Google Scholar
  22. Breen, DL (1975) Coenzyme Q: A molecular orbital study. J Theor Biol 53: 101–113PubMedGoogle Scholar
  23. Breton J (2004) Absence of large-scale displacement of quinone QB in bacterial photosynthetic reaction centers. Biochemistry 43: 3318–3326PubMedGoogle Scholar
  24. Breton J and Nabedryk E (1995) Protein and bacteriopheophytin response to QA reduction in photosynthetic bacterial reaction centers from Rb. sphaeroides and Rp. viridis investigated by 1H/2H exchange and light-induced FTIR difference spectroscopy. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, Vol I, pp 395–400. Kluwer Academic Publishers, DordrechtGoogle Scholar
  25. 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: 84–90Google Scholar
  26. Breton J, Boullais C, Burie J, Nabedryk E and Mioskowski C (1994a) Binding sites of quinones in photosynthetic bacterial reaction centers investigated by light-induced FTIR difference spectroscopy: Assignment of the interactions of each carbonyl of QA in Rhodobacter sphaeroides using site-specific 13C-labeled ubiquinone. Biochemistry 33: 14378–14386PubMedGoogle Scholar
  27. Breton J, Burie J, Boullais C, Berger G and Nabedryk E (1994b) Binding sites of quinones in photosynthetic bacterial reaction centers investigated by light-induced FTIR difference spectroscopy: Binding of chainless symmetrical quinones to the QA site of Rhodobacter sphaeroides. Biochemistry 33: 12405–12415PubMedGoogle Scholar
  28. Breton J, Burie J-R, Berthomieu C, Berger G and Nabedryk E (1994c) The binding sites of quinones in photosynthetic bacterial reaction centers investigated by light-induced FTIR difference spectroscopy: Assignment of the QA vibrations in Rhodobacter sphaeroides using 18O- or 13C-labeled ubiquinone and vitamin K1. Biochemistry 33: 4953–4965PubMedGoogle Scholar
  29. Breton J, Boullais C, Berger G, Mioskowski C and Nabedryk E (1995) Binding sites of quinones in photosynthetic bacterial reaction centers investigated by light induced FTIR difference spectroscopy: symmetry of the carbonyl interactions and close equivalence of the QB vibrations in Rhodobacter sphaeroides and Rhodopseudomonas viridis probed by isotopic labeling. Biochemistry 34: 11606–11616PubMedGoogle Scholar
  30. Breton J, Boullais C, Mioskowski C, Sebban P, Baciou L and Nabedryk E (2002) Vibrational spectroscopy favors a unique QB binding site at the proximal position in wild-type reaction centers and in the Pro-L209→Tyr mutant from Rhodobacter sphaeroides. Biochemistry 41: 12921–12927PubMedGoogle Scholar
  31. Breton J, Wakeham MC, Fyfe PK, Jones MR and Nabedryk E (2004) Characterization of the bonding interactions of QB upon photoreduction via A-branch or B-branch electron transfer in mutant reaction centers from Rhodobacter sphaeroides. Biochim Biophys Acta 1656: 127–138PubMedGoogle Scholar
  32. Breton J, Lavergne J, Wakeham MC, Nabedryk E and Jones MR (2007) The unusually strong hydrogen bond between the carbonyl of QA and His M219 in the Rhodobacter sphaeroides reaction center is not essential for efficient electron transfer from QA - to QB. Biochemistry 46: 6468–6476PubMedGoogle Scholar
  33. Bruce BD, Fuller RC and Blankenship RE (1982) Primary photosynthesis in the facultative aerobic green photosynthetic bacterium Chloroflexus aurantiacus. Proc Natl Acad Sci USA 79: 6532–6536PubMedGoogle Scholar
  34. Brudler R, de Groot HJM, van Liemt WBS, Steggerda WF, Esmeijer R, Gast P, Hoff AJ, Lugtenburg J and Gerwert K (1994) Asymmetric binding of the 1- and 4-C=O groups of QA in Rhodobacter sphaeroides R26 reaction centers monitored by Fourier transform infra-red spectroscopy using site-specific isotopically labelled ubiquinone-10. EMBO J 13: 5523–5530PubMedGoogle Scholar
  35. Brudler R, de Groot HJM, van Liemt WBS, Hoff AJ, Lugtenburg JL and Gerwert K (1995) FTIR spectroscopy shows weak symmetric hydrogen bonding of the QB carbonyl groups in Rhodobacter sphaeroides R26 reaction centres. FEBS Lett 370: 2–14Google Scholar
  36. Burie J-R, Boussac A, Boullas C, Berger G, Mattioli T, Mioskowski C, Nabedryk E and Breton J (1995) FTIR spectroscopy of UV-generated quinone radicals: Evidence for an intramolecular hydrogen atom transfer in ubiquinone, naphthoquinone, and plastoquinone. J Phys Chem B 99: 4059–4070Google Scholar
  37. 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: 6607–6617Google Scholar
  38. Burley SK and Petsko GA (1985) Aromatic-aromatic interaction: A mechanism of protein structure stabilization. Science 229: 23–28PubMedGoogle Scholar
  39. Butler WF, Johnston DC, Shore HB, Fredkin DR, Okamura MY and Feher G (1980) The electronic structure of Fe2+ in reaction centers from Rhodopseudomonas sphaeroides I. Static magnetization measurements. Biophys J 32: 967–992PubMedGoogle Scholar
  40. Butler WF, Calvo R, Fredkin DR, Isaacson RA, Okamura MY and Feher G (1984) The electronic structure of Fe2+ in reaction centers from Rhodopseudomonas sphaeroides III. EPR measurements of the reduced acceptor complex. Biophys J 45: 947–973PubMedGoogle Scholar
  41. Chang C-H, El-Kabbani O, Tiede D, Norris J and Schiffer M (1991) Structure of the membrane-bound protein photosynthetic reaction center from Rhodobacter sphaeroides. Biochemistry 30: 5352–5360PubMedGoogle Scholar
  42. Chirino AJ, Lous EJ, Huber M, Allen JP, Schenck CC, Paddock ML, Feher G and Rees DC (1994) Crystallographic analyses of site-directedmutants of the photosynthetic reaction center from Rhodobacter sphaeroides. Biochemistry 33: 4584–4593PubMedGoogle Scholar
  43. Coleman WJ, Bylina EJ and Youvan DC (1990a) Reconstitution of photochemical activity in Rhodobacter capsulatus reaction centers containing mutations at trytophan M-250 in the primary quinone binding site. In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol 1, pp 149–152. Kluwer Academic Publishers, DordrechtGoogle Scholar
  44. Coleman WJ, Youvan DC, Aumeier W, Eberl U, Volk M, Lang E, Siegl J, Heckmann R, Lersch W, Ogrodnik A and Michel-Beyerle ME (1990b) How conclusive is mutagenic replacement of Trp M250 in photosynthetic reaction centers? In: Baltscheffsky M (ed) Current Research in Photosynthesis, Vol 1, pp 153–156. Kluwer Academic Publishers, DordrechtGoogle Scholar
  45. De Groot HJM (1995) Asymmetric primary quinone hydrogen bonding in Rhodobacter sphaeroides reaction centers. In: Mathis P (ed) Photosynthesis: From Light to Biosphere, I, pp 401–406. Kluwer Academic Publishers, DordrechtGoogle Scholar
  46. Deisenhofer J and Michel H (1989a) The photosynthetic reaction center from the purple bacterium Rhodopseudomonas viridis. Science 245: 1463–1473PubMedGoogle Scholar
  47. Deisenhofer J and Michel H (1989b) The photosynthetic reaction centre from the purple bacterium Rhodopseudomonas viridis. EMBO J 8: 2149–2170PubMedGoogle Scholar
  48. Deisenhofer J and Michel H (1991) High-resolution structures of photosynthetic reaction centers. Annu Rev Biophys Chem 20: 247–266Google Scholar
  49. Deisenhofer J, Epp O, Miki R, Huber R and Michel H (1985) Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3 Å resolution. Nature 318: 618–624Google Scholar
  50. Deng H and Callender R (1999) Raman spectroscopic studies of the structure, energetics, and bond distortions of substrates bound to enzymes. Methods Enzymol 308: 176–201PubMedGoogle Scholar
  51. DeVault D (1980) Quantum-mechanical tunneling in biological systems. Q Rev Biophys 13: 387–564PubMedGoogle Scholar
  52. El-Kabbani O, Chang C-H, Tiede D, Norris J and Schiffer M (1991) Comparison of reaction centers from Rhodobacter sphaeroides and Rhodopseudomonas viridis: Overall architecture and protein-pigment interactions. Biochemistry 30: 5361–5369PubMedGoogle Scholar
  53. Ermler U, Fritzsch G, Buchanan SK and Michel H (1994) Structure of the photosynthetic reaction center from Rhodobacter sphaeroides at 2.65 Å resolution: Cofactors and protein-cofactor interactions. Structure 2: 925–936PubMedGoogle Scholar
  54. Feher G, Okamura MY and McElroy JD (1972) Identification of an electron acceptor in reaction centers of Rhodopseudomonas spheroides by EPR spectroscopy. Biochim Biophys Acta 267: 222–226PubMedGoogle Scholar
  55. Feher G, Isaacson RA, Okamura MY and Lubitz W (1985) ENDOR of semiquinones in reaction centers from Rhodopseudomonas sphaeroides. In: Michel-Beyerle ME (ed) Antennas and Reaction Centers of Photosynthetic Bacteria—Structure, Interactions and Dynamics, pp 174–189. Springer-Verlag, BerlinGoogle Scholar
  56. Feher G, Isaacson RA, Okamura MY and Lubitz W (1988). ENDOR of exchangeable protons of the reduced intermediate acceptor in reaction centers from Rhodobacter sphaeroides R-26. In: Breton J and Verméglio A (eds) The Photosynthetic Bacterial Reaction Center, Cadarache, France, Plenum PressGoogle Scholar
  57. Ferreira KN, Iverson TM, Maghlaoui K, Barber J and Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303: 1831–1838PubMedGoogle Scholar
  58. Fisher N and Rich PR (2000) A motif for quinone binding sites in respiratory and photosynthetic systems. J Mol Biol 296: 1153–1162PubMedGoogle Scholar
  59. Flett MSC (1948) The application of infra-red spectroscopy to structural problems in the anthraquinone field. J Chem Soc 1948: 1441–1448Google Scholar
  60. Flores M, Isaacson RA, Calvo R, Feher G and Lubitz W (2003) Probing hydrogen bonding to quinone anion radicals by 1H and 2H ENDOR spectroscopy at 35 GHz. Chem Phys 294: 401–413Google Scholar
  61. Flores M, Isaacson R, Abresch E, Calvo R, Lubitz W and Feher G (2006) Protein-cofactor interactions in bacterial reaction centers from Rhodobacter sphaeroides R-26: I. Identification of the ENDOR lines associated with the hydrogen bonds to the primary quinone QA -. Biophys J 90: 3356–3362PubMedGoogle Scholar
  62. Flores M, Isaacson R, Abresch E, Calvo R, Lubitz W and Feher G (2007) Protein-cofactor interactions in bacterial reaction centers from Rhodobacter sphaeroides R-26: II. Geometry of the hydrogen bonds to the primary quinone QA •- by 1H and 2H ENDOR spectroscopy. Biophys J 92: 671–682PubMedGoogle Scholar
  63. Franzen S, Goldstein RF and Boxer SG (1990) Electric field modulation of electron transfer reaction rates in isotropic systems: Long distance charge recombination in photosynthetic reaction centers. J Phys Chem 94: 5135–5149Google Scholar
  64. Fritscher J, Prisner TF and MacMillan F (2006) Theoretical investigation of QA -ligand interactions in bacterial reaction centers of Rhodobacter sphaeroides. Appl Mag Res 30: 251–268CrossRefGoogle Scholar
  65. Fritzsch G, Koepke J, Diem R, Kuglstatter A and Baciou L (2002) Charge separation induces conformational changes in the photosynthetic reaction centre of purple bacteria. Acta Cryst D 58: 1660–1663Google Scholar
  66. Gast P, Michalski,TJ, Hunt JE and Norris JR (1985) Determination of the amount and the type of quinones present in single crystals from reaction center protein from the photosynthetic bacterium Rhodopseudomonas viridis. FEBS Lett 179: 325–328Google Scholar
  67. Giangiacomo KM and Dutton PL (1989) In photosynthetic reaction centers, the free energy difference for electron transfer between quinones bound at the primary and secondary quinonebinding sites governs the observed secondary site specificity. Proc Natl Acad Sci USA 86: 2658–2662PubMedGoogle Scholar
  68. Gordy W (1940) Spectroscopic evidence for hydrogen bonds: Effects of chelation on the carbonyl frequency. J Chem Phys 8: 516–519Google Scholar
  69. Grafton AK and Wheeler RA (1999) Amino acid protonation states determine binding sites of the secondary ubiquinone and its anion in the Rhodobacter sphaeroides photosynthetic reaction center. J Phys Chem B 103: 5380–5387Google Scholar
  70. Graige MS, Paddock ML, Bruce JM, Feher G and Okamura MY (1996) Mechanism of proton-coupled electron transfer for quinone (QB) reduction in reaction centers of Rb. sphaeroides. J Am Chem Soc 118: 9005–9016Google Scholar
  71. Graige MS, Feher G and Okamura MY (1998) 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: 11679–11684PubMedGoogle Scholar
  72. Graige MS, Paddock ML, Feher G and Okamura MY (1999) Observation of the protonated semiquinone intermediate in isolated reaction centers from Rhodobacter sphaeroides: Implications for the mechanism of electron and proton transfer in proteins. Biochemistry 38: 11465–11473PubMedGoogle Scholar
  73. Gunner MR and Dutton PL (1989) Temperature and -ΔG dependence of the electron transfer from BPh•- to QA in reaction center protein from Rhodobacter sphaeroides with different quinones as QA. J Am Chem Soc 111: 3400–3412.Google Scholar
  74. Gunner MR, Braun BS, Bruce JM and Dutton PL (1985) The characterization of the QA binding site of the reaction center of Rhodopseudomonas sphaeroides. In: Michel-Beyerle ME (ed) Antennas and Reaction Centers of Photosynthetic Bacteria: Structure, Interactions and Dynamics, pp 298–304. Springer-Verlag, BerlinGoogle Scholar
  75. Gunner MR, Robertson DE and Dutton PL (1986) Kinetic studies on the reaction center protein from Rhodopseudomonas sphaeroides: The temperature and free energy dependence of electron transfer between various quinones in the QA site and the oxidized bacteriochlorophyll dimer. J Phys Chem 90: 3783–3795Google Scholar
  76. Gunner MR, Saleh MA, Cross E, ud-Doula A and Wise M (2000) Backbone dipoles generate positive potential in all proteins: Origins and implications of the effect. Biophys J 78: 1126–1144PubMedGoogle Scholar
  77. Heathcote P, Fyfe PK and Jones MR (2002) Reaction centres: The structure and evolution of biological solar power. Trends Biochem Sci 27: 79–87PubMedGoogle Scholar
  78. Heinen U, Utschig LM, Poluektov OG, Link G, Ohmes E and Kothe G (2007) Structure of the charge separated state P865+QA - in the phootosynthetic reaction centers of Rhodobacter sphaeroides by quantum beat oscillations and high-field electron paramagnetic resonance: Evidence for light-induced QA - reorientation. J Am Chem Soc 129: 15935–15946PubMedGoogle Scholar
  79. Hucke O, Schmid R and Labahn A (2002) Exploring the primary electron acceptor (QA)-site of the bacterial reaction center from Rhodobacter sphaeroides. Binding mode of vitamin K derivatives. Eur J Biochem 269: 1096–1108PubMedGoogle Scholar
  80. Isaacson RA, Lendzian F, Abresch C, Lubitz W and Feher G (1995) Electronic structure of QA - in reaction centers from Rhodobacter sphaeroides. I. Electron paramagnetic resonance in single crystals. Biophys J 69: 311–322PubMedGoogle Scholar
  81. Isaacson RA, Abresch EC, Lendzian F, Boullais C, Paddock ML, Mioskowski C, Lubitz W and Feher G (1996). Asymmetry of the binding sites of QA - and QB - in reaction centers of Rb. sphaeroides probed by Q-Band EPR with 13C-labeled quinones. In: Michel-Beyerle ME (ed) The Reaction Center of Photosynthetic Bacteria: Structure and Dynamics, pp 353–368. Springer-Verlag, BerlinGoogle Scholar
  82. Ishikita H, Morra G and Knapp E-W (2003) Redox potential of quinones in photosynthetic reaction centers from Rhodobacter sphaeroides: Dependence on protonation of Glu-L212 and Asp-L213. Biochemistry 42: 3882–3892PubMedGoogle Scholar
  83. Kacprzak S and Kaupp M (2004) Electronic g-tensors of semiquinones in photosynthetic reaction centers. A density functional study. J Phys Chem B 108: 2464–2469Google Scholar
  84. Katona G, Snijder A, Gourdon P, Andréasson U, Hansson Ö, Andréasson L-E and Neutze R (2005) Conformational regulation of charge recombination in a photosynthetic bacterial reaction center. Nature Struct Mol Biol 12: 630–631Google Scholar
  85. Kaupp M (2002) The function of Photosystem I. Quantum chemical insight into the role of tryptophan-quinone interactions. Biochemistry 41: 2895–2900PubMedGoogle Scholar
  86. Kim J, Mao J and Gunner MR (2005) Are acidic and basic groups in buried proteins predicted to be ionized? J Mol Biol 348: 1283–1298PubMedGoogle Scholar
  87. Kirmaier C and Holten D (1990) Evidence that a distribution of bacterial reaction centers underlies the temperature and detection-wavelength dependence of the rates of the primary electrontransfer reactions. Proc Natl Acad Sci USA 87: 3552–3556PubMedGoogle Scholar
  88. Kleinfeld D, Okamura MY and Feher G (1984a) Electron-transfer kinetics in photosynthetic reaction centers cooled to cryogenic temperatures in the charge separated state: Evidence for lightinduced structural changes. Biochemistry 23: 5780–5786PubMedGoogle Scholar
  89. Kleinfeld D, Okamura MY and Feher G (1984b) Electron transfer in reaction centers of Rhodopseudomonas sphaeroides: I. Determination of the charge recombination pathway of D+QAQB - and free energy and kinetic relations between QA -QB and QAQB -. Biochim Biophys Acta 766: 126–140PubMedGoogle Scholar
  90. Koepke J, Krammer EM, Klingen AR, Sebban P, Ullmann GM and Fritzsch G (2007) pH modulates the quinone position in the photosynthetic reaction center from Rhodobacter sphaeroides in the neutral and charge separated states. J Mol Biol 371: 396–409PubMedGoogle Scholar
  91. Krivanek R, Kern J, Zouni A, Dau H and Haumann M (2007) Spare quinones in the QB cavity of crystallized Photosystem II from Thermosynechocoecus elongatus. Biochim Biophys Acta 1767: 520–527PubMedGoogle Scholar
  92. Kruk J, Strzalka K and Leblanc RM (1993) Fourier transform infrared studies on charge-transfer interactions of plastoquinones and α-tocopherol quinone with their hydroquinone forms and monogalactosyldiacylglycerol. Biophysical Chemistry 45: 235–244Google Scholar
  93. Kuglstatter A, Ermler U, Michel H, Baciou L and Fritzsch G (2001) X-ray structure analysis of photosynthetic reaction center variants from Rhodobacter sphaeroides: Structural changes induced by point mutations at position L209 modulate electron and proton transfer. Biochemistry 40: 4253–4260PubMedGoogle Scholar
  94. Labahn A, Bruce JM, Okamura MY and Feher G (1995) Direct charge recombination from D+QAQB - to DQAQB in bacterial reaction centers from Rhodobacter sphaeroides containing low potential quinone in the QA site. Chem Phys 197: 355–366Google Scholar
  95. Laible PD, Kirmaier C, Udawatte CS, Hofman SJ, Holten D and Hanson DK (2003) Quinone reduction via secondary B-branch electron transfer in mutant bacterial reaction centers. Biochemistry 42: 1718–1730PubMedGoogle Scholar
  96. Lancaster CRD (1998) Ubiquinone reduction and protonation in photosynthetic reaction centres from Rhodopseudomonas viridis — X-ray structures and their functional implications. Biochim Biophys Acta 1365: 143–150Google Scholar
  97. Lancaster CRD and Michel H (1996a) New Insights into the X-ray structure of the reaction center of Rhodopseudomonas viridis. In: Michel-Beyerle ME (ed) The Reaction Center of Photosynthetic Bacteria: Structure and Dynamics, pp 23–35. Springer-Verlag, BerlinGoogle Scholar
  98. Lancaster CRD and Michel H (1996b) Three-dimensional structures of photosynthetic reaction centers. Photosynth Res 48: 65–74Google Scholar
  99. Lancaster CRD and Michel H (1997) The coupling of light-induced electron transfer and proton uptake as derived from crystal structures of reaction centres from Rhodopseudomonas viridis modified at the binding site of the secondary quinone, QB. Structure 5: 1339–1359PubMedGoogle Scholar
  100. Lancaster CRD, Michel H, Honig B and Gunner MR (1996) Calculated coupling of electron and proton transfer in the photosynthetic reaction center of Rhodopseudomonas viridis. Biophys J 70: 2469–2492PubMedGoogle Scholar
  101. Lavergne J, Matthews C and Ginet N (1999) Electron and proton transfer on the acceptor side of the reaction center in chromatophores of Rhodobacter capsulatus: Evidence for direct protonation of the semiquinone state of QB. Biochemistry 38: 4542–4552PubMedGoogle Scholar
  102. Leigh JS and Dutton PL (1972) The primary electron acceptor in photosynthesis. Biochem Biophys Res Comm 46: 414–421PubMedGoogle Scholar
  103. Lendzian F, Rautter J, Käß H, Gardiner A and Lubitz W (1996) ENDOR and pulsed EPR studies of photosynthetic reaction centers: Protein-cofactor interactions. Ber Bunsenges Phys Chem 100: 2036–2040Google Scholar
  104. Li J, Gilroy D, Tiede DM and Gunner MR (1998) 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: 2818–2829PubMedGoogle Scholar
  105. Li J, Takahashi E and Gunner MR (2000) -ΔG AB o and pH dependence of the electron transfer from P+QA -QB to P+QAQB - in Rhodobacter sphaeroides reaction centers. Biochemistry 39: 7445–7454PubMedGoogle Scholar
  106. Lin X, Murchison HA, Nagarajan V, Parson WW, Allen JP and Williams JC (1994) Specific alterations of the oxidation potential of the electron donor in reaction centers from Rhodobacter sphaeroides. Proc Natl Acad Sci USA 91: 10265–10269PubMedGoogle Scholar
  107. Loll B, Kern J, Saenger W, Zouni A and Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438: 1040–1044PubMedGoogle Scholar
  108. Lubitz W and Feher G (1999) The primary and secondary acceptors in bacterial photosynthesis III. Characterization of the quinone radicals QA -• and QB -• by EPR and ENDOR. Appl Magn Res 17: 1–48Google Scholar
  109. Lubitz W, Abresch EC, Debus RJ, Isaacson RA, Okamura MY and Feher G (1985) Electron nuclear double resonance of semiquinones in reaction centers of Rhodopseudomonas sphaeroides. Biochim Biophys Acta 808: 464–469PubMedGoogle Scholar
  110. Mancino LJ, Dean DP and Blankenship RE (1984) Kinetics and thermodynamics of the P870+QA - → P870+QB - reaction in isolated reaction centers from the photosynthetic bacterium Rhodopseudomonas sphaeroides. Biochim Biophys Acta 764: 46–54Google Scholar
  111. Marcus RA (1964) Chemical and electrochemical electron-transfer theory. Ann Rev Phys Chem 15: 155–196Google Scholar
  112. Marcus RA and Sutin N (1985) Electron transfers in chemistry and biology. Biochim Biophys Acta 811: 265–322Google Scholar
  113. McComb JC, Stein RR and Wraight CA (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: 156–171PubMedGoogle Scholar
  114. McMahon BH, Müller JD, Wraight CA and Nienhaus GU (1998) Electron transfer and protein dynamics in the photosynthetic reaction center. Biophys J 74: 2567–2587PubMedGoogle Scholar
  115. Meyerson ML (1985) A quantitative model for carbonyl infrared frequencies of substituted quinones. Spectrochim Acta A 41: 1263–1267Google Scholar
  116. Mezzetti A, Leibl W, Breton J and Nabedryk E (2003) Photoreduction of the quinone pool in the bacterial photosynthetic membrane: Identification of infrared marker bands for quinol formation. FEBS Lett 537: 161–165PubMedGoogle Scholar
  117. Moser CC, Keske JM, Warncke K, Farid RS and Dutton PL (1992) Nature of biological electron transfer. Nature 355: 796–802PubMedGoogle Scholar
  118. Moser CC, Page CC, Farid R and Dutton PL (1995) Biological electron transfer. J Bioenerg Biomemb 27: 263–274Google Scholar
  119. Moser CC, Page CC, Cogdell RJ, Barber J, Wraight CA and Dutton PI, (2003) Length, time and energy scales of photosystems. Advances Protein Chem 63: 71–109PubMedGoogle Scholar
  120. Nabedryk E and Breton J (2008) Coupling of electron transfer to proton uptake at the QB site of the bacterial reaction center: A perspective from FTIR difference spectroscopy. Biochim Biophys Acta, in pressGoogle Scholar
  121. Nogi T, Fathir I, Kobayashi M, Nozawa T and Miki K (2000) Crystal structures of photosynthetic reaction center and highpotential iron-sulfur protein from Thermochromatium tepidum: Thermostability and electron transfer. Proc Nat Acad Sci USA 97: 13561–13566PubMedGoogle Scholar
  122. Nonella M (1997) Structure and vibrational spectra of p-benzo-quinone in different oxidation and protonation states: A density functional study. J Phys Chem B 101: 1235–1246Google Scholar
  123. Nonella M (1998) A quantum chemical investigation of structures, vibrational spectra and electron affinities of the radicals of quinone model compounds. Photosynth Res 55: 253–259Google Scholar
  124. 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: 14549–14559Google Scholar
  125. 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: 316–322Google Scholar
  126. Okamura MY and Feher G (1986) Isotope effect on electron transfer in reaction centers from Rhodopseudomonas sphaeroides. Proc Natl Acad Sci USA 83: 8152–8156PubMedGoogle Scholar
  127. Okamura MY and Feher G (1992) Proton transfer in reaction centers from photosynthetic bacteria. Annu Rev Biochem 61: 861–896PubMedGoogle Scholar
  128. Okamura MY and Feher G (1995) Proton-coupled electron transfer reactions of QB in reaction centers from photosynthetic bacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria (Advances in Photosynthesis and Respiration, Vol 2, pp 577–593. Kluwer Academic PublishersGoogle Scholar
  129. Okamura MY, Isaacson RA and Feher G (1975) The primary acceptor in bacterial photosynthesis: Obligatory role of ubiquinone in photoactive reaction centers of Rhodopseudomonas sphaeroides. Proc Natl Acad Sci USA 72: 3492–3496Google Scholar
  130. Okamura MY, Paddock ML, Graige MS and Feher G (2000) Proton and electron transfer in bacterial reaction centers. Biochim Biophys Acta 1458: 148–163PubMedGoogle Scholar
  131. O’Malley PJ (1997a) A density functional study of the effect of reduction on the geometry and electron affinity of hydrogen bonded 1,4-benzoquinone. Implications for quinone reduction and protonation in photosynthetic reaction centers. Chem Phys Lett 274: 251–254Google Scholar
  132. O’Malley PJ (1997b) Hybrid density functional study of the p-benzosemiquinone anion radical: The influence of hydrogen bonding on geometry and hyperfine couplings. J Phys Chem A 101: 6334–6338Google Scholar
  133. O’Malley PJ (2001) Electronic structure studies of quinones and semiquinones: Accurate calculation of spin densities and electron paramagnetic resonance parameters. Antioxid Redox Signal 3: 825–838PubMedGoogle Scholar
  134. O’Malley PJ (2003) The origin of the spin density asymmetry at the QA binding site of type II photosynthetic reaction centres. Chem Phys Lett 379: 277–281Google Scholar
  135. Paddock ML, Abresch EC, Isaacson RA, Lubitz W, Okamura MY and Feher G (1999) Identification of hydrogen bonds to QA in RCs of Rb. sphaeroides by ENDOR spectroscopy. Biophys J 76: A141Google Scholar
  136. Paddock ML, Feher G and Okamura MY (2003) Proton transfer pathways and mechanism in bacterial reaction centers. FEBS Lett 555: 45–50PubMedGoogle Scholar
  137. Paddock ML, Flores M, Isaacson R, Chang C, Selvaduray P, Feher G and Okamura MY (2005) Hydrogen bond reorientation upon QB reduction revealed by ENDOR spectroscopy in reaction centers from Rhodobacter sphaeroides. Biophys J 88: 204aGoogle Scholar
  138. Paddock ML, Flores M, Isaacson R, Chang C, Abresch EC, Selvaduray P and Okamura MY (2006) Trapped conformational states of semiquinone (D+•QB -•) formed by B-branch electron transfer at low temperature in Rhodobacter sphaeroides reaction centers. Biochemistry 45: 14032–14042PubMedGoogle Scholar
  139. Paddock ML, Flores M, Isaacson R, Chang C, Abresch EC and Okamura MY (2007) ENDOR spectroscopy reveals light induced movement of the H-bond from Ser-L223 upon forming the semiquinone (QB -•) in reaction centers from Rhodobacter sphaeroides. Biochemistry 46: 8234–8243PubMedGoogle Scholar
  140. Parson WW (1978) Quinones as secondary electron acceptors. In: Clayton RK and Sistrom WR (eds) The Photosynthetic Bacteria, pp 455–469. Plenum, New YorkGoogle Scholar
  141. Plato M, Michel-Beyerle ME, Bixon M and Jortner J (1989) On the role of tryptophan as a superexchange mediator for quinone reduction in photosynthetic reaction centers. FEBS Lett 249: 70–74Google Scholar
  142. Pokkuluri PR, Laible PD, Deng Y-L, Wong TN, Hanson DK and Schiffer M (2002) The structure of amutantphotosynthetic reaction center shows unexpected changes in main chain orientations and quinone position. Biochemistry 41: 5998–6007PubMedGoogle Scholar
  143. Pokkuluri PR, Laible PD, Crawford AE, Mayfield JF, Yousef MA, Ginell SL, Hanson DK and Schiffer M (2004) Temperature and cryoprotectant influence secondary quinone binding position in bacterial reaction centers. FEBS Lett 570: 171–174PubMedGoogle Scholar
  144. Prince RC, Dutton PL and Bruce JM (1983) Electrochemistry of ubiquinones, menaquinones and plastoquinones in aprotic solvents. FEBS Lett 160: 273–276Google Scholar
  145. Prince RC, Halbert TR and Upton TH (1988) Structural influences on the electrochemistry of ubiquinone. In: Kim CH, Tedeschi H, Diwan JJ and Salerno JC (eds) Advances in Membrane Biochemistry and Bioenergetics, pp 469–478. Plenum Press, New YorkGoogle Scholar
  146. Rabenstein B, Ullmann GM and Knapp E-W (2000) Electron transfer between the quinones in the photosynthetic reaction center and its coupling to conformational changes. Biochemistry 39: 10487–10496PubMedGoogle Scholar
  147. Rao CNR, Dwivedi PC, Ratajczak H and Orville-Thomas WJ (1975) Relation between O-H stretching frequency and hydrogen bond energy: Re-examination of the Badger-Bauer rule. J Chem Soc Faraday Trans II 71: 955–966Google Scholar
  148. Rasmussen RS, Tunnicliff DD and Brattain RR (1949) Infrared and ultraviolet spectroscopic studies on ketones. J Am Chem Soc 71: 1068–1072Google Scholar
  149. Remy A, Boers RB, Egorova-Zachernyuk T, Gast P, Lugtenberg J and Gerwert K (2003) Does different orientation of the methoxy groups of ubiquinone-10 in the reaction center of Rhodobacter sphaeroides cause different binding at QA and QB? Eur J Biochem 270: 3603–3609PubMedGoogle Scholar
  150. Robinson HH and Kahn SD (1990) Interplay of substituted conformation and electron affinity in quinone models of quinone reductases. J Am Chem Soc 112: 4728–4731Google Scholar
  151. Savitsky A, Dubinskii AA, Flores M, Lubitz W and Möbius K (2007) Orientation-resolving pulsed electron dipolar high-field EPR spectroscopy on disordered solids: I. Structure of spincorrelated radical pairs in bacterial photosynthetic reaction centers. J Phys Chem B 111: 6245–6262PubMedGoogle Scholar
  152. Schenck CC, Parson WW, Holten D, Windsor MW and Sarai A (1981) Temperature dependence of electron transfer between bacteriopheophytin and ubiquinone in protonated and deuterated reaction centers of Rhodopseudomonas sphaeroides. Biophys J 36: 479–489PubMedGoogle Scholar
  153. Schmid R and Labahn A (2000) Temperature and free energy dependence of the direct charge recombination rate from the secondary quinone in bacterial reaction centers from Rhodobacter sphaeroides. J Phys Chem B 104: 2928–2936Google Scholar
  154. Schmid R, Goebel F, Warnecke A and Labahn A (1999) Synthesis and redox potentials of methylated vitamin K derivatives. J Chem Soc, Perkin Trans 2 1199–1202Google Scholar
  155. Schüler RH, Tripathi GNR, Prebenda MF and Chipman DM (1983) Resonance Raman and molecular orbital studies of the effects of deuteration on the vibrational structure of the p-benzoquinone radical anion. J Phys Chem 87: 5357–5361Google Scholar
  156. Sebban P, Maróti P, Schiffer M and Hanson DK (1995) Electrostatic dominoes: Long distance propagation of mutational effects in photosynthetic reaction centers of Rhodobacter capsulatus. Biochemistry 34: 8390–8397PubMedGoogle Scholar
  157. Shinkarev VP and Wraight CA (1993) Electron and proton transfer in the acceptor quinone complex of reaction centers of phototrophic bacteria. In: Deisenhofer J and Norris JR (eds) The Photosynthetic Reaction Center, 1, pp 193–255. Academic Press, San DiegoGoogle Scholar
  158. Shinkarev VP and Wraight CA (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: 2304–2319PubMedGoogle Scholar
  159. Shopes RJ and Wraight CA (1985) The acceptor quinone complex of Rhodopseudomonas viridis reaction centers. Biochim Biophys Acta 806: 348–356PubMedGoogle Scholar
  160. Sinnecker S, Flores M and Lubitz W (2006) Protein-cofactor interactions in bacterial reaction centers from Rhodobacter sphaeroides R-26: Effect of hydrogen bonding on the electronic and geometric structure of the primary quinone. A density functional theory study. Phys Chem Chem Phys 8: 5659–5670PubMedGoogle Scholar
  161. Slifkin MA and Walmsley RH (1969) Infra-red studies of quinhydrone type complexes. Spectrochim Acta A 26: 1237–1242Google Scholar
  162. Spoyalov AP, Hulsebosch RJ, Shochat S, Gast P and Hoff AJ (1996) Evidence that Ala M260 is hydrogen-bonded to the reduced primary acceptor quinone QA -• in reaction centers of Rb. sphaeroides. Chem Phys Lett 263: 715–720Google Scholar
  163. Stilz HU, Finkele U, Holzapfel W, Lauterwasser C, Zinth W and Oesterhelt D (1994) Influence of M subunit Thr222 and Trp252 on quinone binding and electron transfer in Rhodobacter sphaeroides reaction centres. Eur J Biochem 223: 233–242PubMedGoogle Scholar
  164. Stowell MHB, McPhillips TM, Rees DC, Soltis SM, Abresch E and Feher G (1997) Light-induced structural changes in photosynthetic reaction center: Implications for mechanism of electron-proton transfer. Science 276: 812–816PubMedGoogle Scholar
  165. Sundberg RJ and Martin RB (1974) Interactions of histidine and other imidazole derivatives with transition metal ions in chemical and biological systems. Chem Rev 74: 471–517Google Scholar
  166. Taly A, Sebban P, Smith JC and Ullmann GM (2003) The position of QB in the photosynthetic reaction center depends on pH: A theoretical analysis of the proton uptake upon QB reduction. Biophys J 84: 2090–2098.PubMedGoogle Scholar
  167. Tandori J, Sebban P, Michel H and Baciou L (1999) In Rhodobacter sphaeroides reaction centers, mutation of proline L209 to aromatic residues in the vicinity of a water channel alters the dynamic coupling between electron and proton transfer processes. Biochemistry 38: 13179–13187PubMedGoogle Scholar
  168. Tandori J, Maróti P, Alexov E, Sebban P and Baciou L (2002) Key role of proline L209 in connecting the distant quinone pockets in the reaction center of Rhodobacter sphaeroides. Proc Natl Acad Sci USA 99: 6702–6706PubMedGoogle Scholar
  169. Thijs R and Zeegers-Huyskens T (1984) Infrared and Raman studies of hydrogen bonded complexes involving acetone, acetophenone and benzophenone. I. Thermodynamic constants and frequency shifts of the vOH and vC=O stretching vibrations. Spectrochim Acta 40A: 307–313Google Scholar
  170. Tiede DM, Vazquez J, Cordova J and Marone PA (1996) Timeresolved electrochromism associated with the formation of quinone anions in the Rhodobacter sphaeroides R26 reaction center. Biochemistry 35: 10763–10775PubMedGoogle Scholar
  171. Utschig LM, Thurnauer MC, Tiede DM and Poluektov OG (2005) Low-temperature interquinone electron transfer in photosynthetic reaction centers from Rhodobacter sphaeroides and Blastochloris viridis: Characterization of QB - states by high-frequency electron paramagnetic resonance (EPR) and electron-nuclear double resonance (ENDOR). Biochemistry 44: 14131–14142PubMedGoogle Scholar
  172. Van den Brink JS, Hulsebosch RJ, Gast P, Hore PJ and Hoff AJ (1994) QA binding in reaction in reaction centers of the photosynthetic purple bacterium Rhodobacter sphaeroides R26: Investigation with electron spin polarization spectroscopy. Biochemistry 33: 13668–13677PubMedGoogle Scholar
  173. Van der Est A, Prisner T, Bittl R, Fromme P, Lubitz W, Möbius K and Stehlik D (1997) Time resolved X-, K- and W- band EPR of the radical pair state P700 •+A1 •- of photosystem I in comparison with P865 •+QA •- of bacterial reaction center. J Phys Chem B 101: 1437–1443Google Scholar
  174. Van Liemt BS, Boender GJ, Gast P, Hoff AJ, Lugtenburg J and De Groot HJM (1995) 13C Magic angle spinning NMR characterization of the functionally asymmetric QA binding in Rhodobacter sphaeroides R26 photosynthetic reaction centers using site-specific 13C-labeled ubiquinone-10. Biochemistry 34: 10229–10236PubMedGoogle Scholar
  175. Wakeham MC, Breton J, Nabedryk E and Jones MR (2004) Formation of a semiquinone at the QB site by A- or B-branch electron transfer in the reaction center from Rhodobacter sphaeroides. Biochemistry 43: 4755–4763PubMedGoogle Scholar
  176. Waiden SE and Wheeler RA (2002) Protein conformational gate controlling binding site preference and migration for ubiquinone-B in the photosynthetic reaction center of Rhodobacter sphaeroides. J Phys Chem B 106: 3001–3006Google Scholar
  177. Warncke K and Dutton PL (1992) Both carbonyl groups are necessary for strong interaction of the semiquinone at the QA site of photosynthetic reaction center protein. Biophys J 57: 571aGoogle Scholar
  178. Warncke K and Dutton PL (1993a) Experimental resolution of the free energies of aqueous solvation contributions to ligand-protein binding: quinone-QA site interactions in the photosynthetic reaction center protein. Proc Natl Acad Sci USA 90: 2920–2924PubMedGoogle Scholar
  179. Warncke K and Dutton PL (1993b) Influence of QA site cofactor structure on equilibrium binding, in situ electrochemistry, and electron-transfer performance in the photosynthetic reaction center protein. Biochemistry 32: 4769–4779PubMedGoogle Scholar
  180. Warncke K, Gunner MR and Dutton PL (1987) Effect of hydrocarbon tail structure on the affinity of substituted quinones for the QA site in reaction centers of Rhodopseudomonas sphaeroides R-26. In: Biggins J (ed) Progress in Photosynthesis Research, pp 217–220. Martinus Nijhoff, DordrechtGoogle Scholar
  181. Warncke K, Gunner MR, Braun BS, Gu L, Yu C-A, Bruce JM and Dutton PL (1994) Influence of hydrocarbon tail structure on quinone binding and electron-transfer performance at the QA and QB sites of the photosynthetic reaction center protein. Biochemistry 33: 7830–7841PubMedGoogle Scholar
  182. Wells TA, Takahashi E and Wraight CA (2003) Protein control of the redox potential of the primary quinone acceptor in reaction centers from Rhodobacter sphaeroides. Biochemistry 42: 4064–4074PubMedGoogle Scholar
  183. Wheeler RA (2001) Quinones and quinoidal radicals in photosynthesis. In: Eriksson LA (ed) Theoretical Biochemistry — Processes and Properties, pp 655–690. Elsevier, AmsterdamGoogle Scholar
  184. Williams JC, Steiner LA and Feher G (1986) Primary structure of the reaction center from Rhodopseudomonas sphaeroides. Proteins 1: 312–325PubMedGoogle Scholar
  185. Williams JC, Paddock ML, Feher G and Allen JP (1991) Effects of iron ligand substitutions in reaction centers from Rhodobacter sphaeroides. Biophys J 59: 142aCrossRefGoogle Scholar
  186. Woodbury NW and Allen JP (1995) The pathway, kinetics and thermodynamics of electron transfer in wild type and mutant reaction centers of purple nonsulfur bacteria. In: Blankenship RE, Madigan MT and Bauer CE (eds) Anoxygenic Photosynthetic Bacteria, pp 527–557. Kluwer Academic Publishers, DordrechtGoogle Scholar
  187. Woodbury NW, Becker M, Middendorf D and Parson WW (1985) Picosecond kinetics of the initial photochemical electrontransfer reaction in bacterial photosynthetic reaction centers. Biochemistry 24: 7516–7521PubMedGoogle Scholar
  188. Woodbury NW, Parson WW, Gunner MR, Prince RC and Dutton PL (1986) Radical-pair energetics and decay mechanisms in reaction center containing anthraquinones or benzoquinones in place of ubiquinone. Biochim Biophys Acta 851: 6–22PubMedGoogle Scholar
  189. Wraight CA (1978) Iron-quinone interactions in the electron acceptor region of bacterial photosynthetic reaction centers. FEBS Lett 93: 283–288Google Scholar
  190. Wraight CA (1979) Electron acceptors of bacterial photosynthetic reaction centers II. H+ binding coupled to secondary electron transfer in the quinone acceptor complex. Biochim Biophys Acta 548: 309–327PubMedGoogle Scholar
  191. Wraight CA (1982) The involvement of stable semiquinones in the two-electron gates of plant and bacterial photosystems. In: Trumpower BL (ed) Function of Quinones in Energy Conserving Systems, pp 181–197. Academic Press, New YorkGoogle Scholar
  192. Wraight CA (2004) Proton and electron transfer in the acceptor quinone complex of bacterial photosynthetic reaction centers. Frontiers Biosci 9: 309–327Google Scholar
  193. Wraight CA (2005) Intraprotein proton transfer — Concepts and realities from the bacterial photosynthetic reaction center. In: Wikström M (ed) Biophysical and Structural Aspects of Bioenergetics, pp 273–313. Royal Society of Chemistry, Cambridge, U.K.Google Scholar
  194. Xu Q and Gunner MR (2000) Temperature dependence of the free energy, enthalpy, and entropy of P+QA - charge recombination in Rhodobacter sphaeroides R-26 reaction centers. J Phys Chem B 104: 8035–8043Google Scholar
  195. Xu Q and Gunner MR (2001) Trapping conformational intermediate states in the reaction center protein from photosynthetic bacteria. Biochemistry 40: 3232–3241PubMedGoogle Scholar
  196. Xu Q and Gunner MR (2002) Exploring the energy profile of the QA - to QB electron transfer reaction in bacterial photosynthetic reaction centers: pH dependence of the conformational gating step. Biochemistry 41: 2694–2701PubMedGoogle Scholar
  197. Xu Q, Baciou L, Sebban P and Gunner MR (2002) Exporing the energy landscape for QA - to QB electron transfer in bacterial photosynthetic reaction centers: Effect of substrate position and tail length on the conformational gating step. Biochemistry 41: 10021–10025PubMedGoogle Scholar
  198. Zachariae U and Lancaster CRD (2001) Proton uptake associated with the reduction of the primary quinone QA influences the binding site of the secondary quinone QB in Rhodopseudomonas viridis photosynthetic reaction centres. Biochim Biophys Acta 1505: 280–290PubMedGoogle Scholar
  199. Zadorozhnyi BA and Ishchenko IK (1965) Hydrogen bond energies and shifts of the stretching vibration bands of C=O groups. Optics & spectroscopy (Eng Translation) 19: 306–308Google Scholar
  200. Zhao X and Kitagawa T (1998) Solvent effects of 1,4-benzoquinone and its anion radicals probed by resonance Raman and absorption spectra and their correlation with redox potentials. J Raman Spectrosc 29: 773–780Google Scholar
  201. Zhao X, Imahori H, Zhan C-G, Sakata Y, Iwata S and Kitagawa T (1997a) Resonance Raman and FTIR spectra of isotope-labeled reduced 1,4-benzoquinone and its protonated forms in solution. J Phys Chem A 101: 622–631Google Scholar
  202. Zhao X, Ogura T, Okamura M and Kitagawa T (1997b) Observation of the resonance Raman spectra of the semiquinones QA •- and QB •- in photosynthetic reaction centers from Rhodobacter sphaeroides R26. J Am Chem Soc 119: 5263–5264Google Scholar
  203. Zhu Z and Gunner MR (2005) The energetics of quinone dependent electron and proton transfers in Rhodobacter sphaeroides photosynthetic reaction centers. Biochemistry 44: 82–96PubMedGoogle Scholar
  204. Zhu Z-Y and Karlin S (1996) Clusters of charged residues in protein three-dimensional structures. Proc Natl Acad Sci USA 93: 8350–8355PubMedGoogle Scholar

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© Springer Science + Business Media B.V 2009

Authors and Affiliations

  1. 1.Department of Biochemistry, and Center for Biophysics & Computational BiologyUniversity of IllinoisUrbanaUSA
  2. 2.Department of PhysicsCity College of New YorkNew YorkUSA

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