Photosynthesis Research

, Volume 92, Issue 3, pp 327–343 | Cite as

Time-resolved X-ray spectroscopy leads to an extension of the classical S-state cycle model of photosynthetic oxygen evolution

Original paper

Abstract

In oxygenic photosynthesis, a complete water oxidation cycle requires absorption of four photons by the chlorophylls of photosystem II (PSII). The photons can be provided successively by applying short flashes of light. Already in 1970, Kok and coworkers [Photochem Photobiol 11:457–475, 1970] developed a basic model to explain the flash-number dependence of O2 formation. The third flash applied to dark-adapted PSII induces the S3→S4⇒S0 transition, which is coupled to dioxygen formation at a protein-bound Mn4Ca complex. The sequence of events leading to dioxygen formation and the role of Kok’s enigmatic S4-state are only incompletely understood. Recently we have shown by time-resolved X-ray spectroscopy that in the S3⇒S0 transition an interesting intermediate is formed, prior to the onset of O–O bond formation [Haumann et al. Science 310:1019–1021, 2005]. The experimental results of the time-resolved X-ray experiments are discussed. The identity of the reaction intermediate is considered and the question is addressed how the novel intermediate is related to the S4-state proposed in 1970 by Bessel Kok. This leads us to an extension of the classical S-state cycle towards a basic model which describes sequence and interplay of electron and proton abstraction events at the donor side of PSII [Dau and Haumann, Science 312:1471–1472, 2006].

Keywords

Manganese complex Mechanism of water oxidation Oxygenic photosynthesis Photosynthetic oxygen evolution Photosystem II X-ray absorption spectroscopy 

Abbreviations

Chl

chlorophyll

EPR

electron paramagnetic resonance

EXAFS

extended X-ray absorption fine-structure

OEC

oxygen-evolving complex

PSII

photosystem II

P680

primary chlorophyll donor in PSII

Pheo

specific pheophytin acting as the primary electron acceptor in PSII

Q

‘quencher’ of PSII fluorescence and electron acceptor in PSII

QA

primary quinone acceptor in PSII

QB

secondary quinone acceptor in PSII

YZ

Tyr 160/161 of the D1 protein of PSII

YZ•+

oxidized form of YZ

XANES

X-ray absorption near-edge structure

XAS

X-ray absorption spectroscopy

References

  1. Ahlbrink R, Haumann M, Cherepanov D, Boegershausen O, Mulkidjanian A, Junge W (1998) Function of tyrosine-Z in water oxidation by photosystem II: electrostatical promotor instead of hydrogen abstractor. Biochemistry 37:1131–1142PubMedCrossRefGoogle Scholar
  2. Ayougou K, Bill E, Charnick JM, Garner CD, Mandon D, Trautwein AX, Weiss R, Winkler H (1995) Characterization of an oxo(porphyrinato)manganese(IV) complex by x-ray absorption spectroscopy. Angew Chem Int Ed 34:343–346CrossRefGoogle Scholar
  3. Babcock GT, Blankenship RE, Sauer K (1976) Reaction kinetics for positive charge accumulation on the water side of chloroplast photosystem II. FEBS Lett 61:286–289PubMedCrossRefGoogle Scholar
  4. Barra M, Haumann M, Loja P, Krivanek R, Grundmeier A, Dau H (2006) Intermediates in assembly by photoactivation after thermally accelerated disassembly of the manganese complex of photosynthetic water oxidation. Biochemistry 45:14523–14532PubMedCrossRefGoogle Scholar
  5. Barry BA, Cooper IB, De Riso A, Brewer SH, Vu DM, Dyer RB (2006) Time-resolved vibrational spectroscopy detects protein-based intermediates in the photosynthetic oxygen-evolving cycle. Proc Natl Acad Sci USA 103:7288–7291PubMedCrossRefGoogle Scholar
  6. Berthomieu C, Hienerwadel R (2005) Vibrational spectroscopy to study the properties of redox-active tyrosines in photosystem II and other proteins. Biochim Biophys Acta 1707:51–66PubMedCrossRefGoogle Scholar
  7. Britt RD, Campbell KA, Peloquin JM, Gilchrist ML, Aznar CP, Dicus MM, Robblee J, Messinger J (2004) Recent pulsed EPR studies of the photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms. Biochim Biophys Acta 1655:158–171PubMedCrossRefGoogle Scholar
  8. Buchta J, Grabolle M, Dau H (2007) Photosynthetic dioxygen formation studied by time-resolved delayed fluorescence measurements – method, rationale, and results on the activation energy of dioxygen formation. Biochim Biophys ActaGoogle Scholar
  9. Carrell G, Tyryshkin M, Dismukes C (2002) An evaluation of structural models for the photosynthetic water-oxidizing complex derived from spectroscopic and X-ray diffraction signatures. J Biol Inorg Chem 7:2–22PubMedCrossRefGoogle Scholar
  10. Christen G, Renger G (1999) The role of hydrogen bonds for the multiphasic P680(+)* reduction by YZ in photosystem II with intact oxygen evolution capacity. Analysis of kinetic H/D isotope exchange effects. Biochemistry 38:2068–2077PubMedCrossRefGoogle Scholar
  11. Chu HA, Hillier W, Law NA, Babcock GT (2001) Vibrational spectroscopy of the oxygen-evolving complex and of manganese model compounds. Biochim Biophys Acta 1503:69–82PubMedCrossRefGoogle Scholar
  12. Cinco RM, Holman KLM, Robblee JH, Yano J, Pizarro SA, Bellacchio E, Sauer K, Yachandra VK (2002) Calcium EXAFS establishes the Mn-Ca cluster in the oxygen-evolving complex of photosystem II. Biochemistry 41:12928–12933PubMedCrossRefGoogle Scholar
  13. Clausen J, Junge W (2004) Detection of an intermediate of photosynthetic water oxidation. Nature 430:480–483PubMedCrossRefGoogle Scholar
  14. Clausen J, Debus RJ, Junge W (2004) Time-resolved oxygen production by PSII: chasing chemical intermediates. Biochim Biophys Acta 1655:184–194PubMedCrossRefGoogle Scholar
  15. Clausen J, Junge W, Dau H, Haumann M (2005) Photosynthetic water oxidation at high O2 backpressure monitored by delayed chlorophyll fluorescence. Biochemistry 44:12775–12779PubMedCrossRefGoogle Scholar
  16. Dau H (1994) Molecular mechanisms and quantitative models of variable photosystem II fluorescence. Photochem Photobiol 60:1–23CrossRefGoogle Scholar
  17. Dau H, Haumann M (2003) X-ray absorption spectroscopy to watch catalysis by metalloenzymes: status and perspectives discussed for the water-splitting manganese complex of photosynthesis. J Synchroton Rad 10:76–85CrossRefGoogle Scholar
  18. Dau H, Haumann M (2005) Considerations on the mechanism of photosynthetic water oxidation – dual role of oxo-bridges between Mn ions in (i) redox-potential maintenance and (ii) proton abstraction from substrate water. Photosynth Res 84:325–331PubMedCrossRefGoogle Scholar
  19. Dau H, Haumann M (2006) Reaction cycle of photosynthetic water oxidation. Science 312:1471–1472Google Scholar
  20. Dau H, Sauer K (1991) Electric field effect on chlorophyll fluorescence and its relation to photosystem II charge separation reactions studied by a salt-jump technique. Biochim Biophys Acta 1098:49–60CrossRefGoogle Scholar
  21. Dau H, Sauer K (1992) Electric field effect on the picosecond fluorescence of photosystem II and its relation to the energetics and kinetics of primary charge separation. Biochim Biophys Acta 1102:91–106CrossRefGoogle Scholar
  22. Dau H, Andrews JC, Roelofs TA, Latimer MJ, Liang W, Yachandra VK, Sauer K, Klein MP (1995) Structural consequences of ammonia binding to the manganese center of the photosynthetic oxygen-evolving complex: an X-ray absorption spectroscopy study of isotropic and oriented photosystem II particles. Biochemistry 34:5274–5287PubMedCrossRefGoogle Scholar
  23. Dau H, Dittmer J, Epple M, Hanss J, Kiss E, Rehder D, Schulzke C, Vilter H (1999) Bromine K-edge EXAFS studies of bromide binding to bromoperoxidase from Ascophyllum nodosum. FEBS Lett 457:237–240PubMedCrossRefGoogle Scholar
  24. Dau H, Iuzzolino L, Dittmer J (2001) The tetra-manganese complex of photosystem II during its redox cycle: X-ray absorption results and mechanistic implications. Biochim Biophys Acta 1503:24–39PubMedCrossRefGoogle Scholar
  25. Dau H, Liebisch P, Haumann M (2003) X-ray absorption spectroscopy to analyze nuclear geometry and electronic structure of biological metal centers – potential and questions examined with special focus on the tetra-nuclear manganese complex of oxygenic photosynthesis. Anal Bioanal Chem 376:562–583PubMedCrossRefGoogle Scholar
  26. Dau H, Liebisch P, Haumann M (2004) The structure of the manganese complex of photosystem II in its dark-stable S1-state: EXAFS results in relation to recent crystallographic data. Phys Chem Chem Phys 6:4781–4792CrossRefGoogle Scholar
  27. Dau H, Liebisch P, Haumann M (2005) The manganese complex of oxygenic photosynthesis: conversion of five-coordinated Mn(III) to six-coordinated Mn(IV) in the S2-S3 transition is implied by XANES simulations. Phys Scripta T115:844–846CrossRefGoogle Scholar
  28. Debus RJ (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102:269–352PubMedCrossRefGoogle Scholar
  29. Debus RJ (2001) Amino acid residues that modulate the properties of tyrosine Y(Z) and the manganese cluster in the water oxidizing complex of photosystem II. Biochim Biophys Acta 1503:164–186PubMedCrossRefGoogle Scholar
  30. Dekker JP, Plijter JJ, Ouwehand L, van Gorkom HJ (1984) Kinetics of manganese redox transitions in the oxygen evolving apparatus of photosynthesis. Biochim Biophys Acta 767:176–179CrossRefGoogle Scholar
  31. De Paula JC, Innes JB, Brudvig GW (1985) Electron transfer in photosystem II at cryogenic temperatures. Biochemistry 24:8114–8120PubMedCrossRefGoogle Scholar
  32. de Wijn R, van Gorkom HJ (2001) Kinetics of electron transfer from Q(a) to Q(b) in photosystem II. Biochemistry 40:11912–11922PubMedCrossRefGoogle Scholar
  33. de Wijn R, Schrama T, van Gorkom HJ (2001) Secondary stabilization reactions and proton-coupled electron transport in photosystem II investigated by electroluminescence and fluorescence spectroscopy. Biochemistry 40:5821–5834PubMedCrossRefGoogle Scholar
  34. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838PubMedCrossRefGoogle Scholar
  35. Geijer P, Peterson S, Ahrling KA, Deak Z, Styring S (2001) Comparative studies of the S0 and S2 multiline electron paramagnetic resonance signals from the manganese cluster in Photosystem II. Biochim Biophys Acta 1503:83–95PubMedCrossRefGoogle Scholar
  36. Grabolle M (2005) Die Donorseite des Photosystems II: Rekombinationsfluoreszenz- und Röntgenabsorptionsstudien. Thesis, FB Physik, Freie Univ. BerlinGoogle Scholar
  37. Grabolle M, Dau H (2005) Energetics of primary and secondary electron transfer in photosystem II membrane particles of spinach revisited on basis of recombination-fluorescence measurements. Biochim Biophys Acta 1708:209–218PubMedCrossRefGoogle Scholar
  38. Grabolle M, Haumann M, Müller C, Liebisch P, Dau H (2006) Rapid loss of structural motifs in the manganese complex of oxygenic photosynthesis by X-ray irradiation at 10–300 K. J Biol Chem 281:4580–4588PubMedCrossRefGoogle Scholar
  39. Haumann M, Junge W (1994a) Extent and rate of proton release by photosynthetic water oxidation in thylakoids: electrostatic relaxation versus chemical production. Biochemistry 33:864–872CrossRefGoogle Scholar
  40. Haumann M, Junge W (1994b) The rates of proton uptake and electron transfer at the reducing side of photosystem II in thylakoids. FEBS Lett 347:45–50CrossRefGoogle Scholar
  41. Haumann M, Junge W (1996) Protons and charge indicators in oxygen evolution. In: Ort D, Yocum CF (eds) Oxygenic photosynthesis – the light reactions. Kluwer Academic Publ., Dordrecht, pp 165–192Google Scholar
  42. Haumann M, Bögershausen O, Cherepanov D, Ahlbrink R, Junge W (1997) Photosynthetic oxygen evolution: H/D isotope effects and the coupling between electron and proton transfer during the redox reactions at the oxidizing side of Photosystem II. Photosynth Res 51:193–208CrossRefGoogle Scholar
  43. Haumann M, Grabolle M, Neisius T, Dau H (2002a) The first room-temperature X-ray absorption spectra of higher oxidation states of the tetra-manganese complex of photosystem II. FEBS Lett 512:116–120CrossRefGoogle Scholar
  44. Haumann M, Pospisil P, Grabolle M, Müller C, Liebisch P, Sole VA, Neisius T, Dittmer J, Iuzzolino L, Dau H (2002b) First steps towards time-resolved BioXAS at room temperature: state transitions of the manganese complex of oxygenic photosynthesis. J Synchrotron Rad 9:304–308CrossRefGoogle Scholar
  45. Haumann M, Liebisch P, Müller C, Barra M, Grabolle M, Dau H (2005a) Photosynthetic O2 formation tracked by time-resolved X-ray experiments. Science 310:1019–1021CrossRefGoogle Scholar
  46. Haumann M, Müller C, Liebisch P, Iuzzolino L, Dittmer J, Grabolle M, Neisius T, Meyer-Klaucke W, Dau H (2005b) Structural and oxidation state changes of the photosystem II manganese complex in four transitions of the water oxidation cycle (S0→S1, S1→S2, S2→S3, S3,4→S0) characterized by X-ray absorption spectroscopy at 20 K as well as at room temperature. Biochemistry 44:1894–1908CrossRefGoogle Scholar
  47. Haumann M, Müller C, Liebisch P, Neisius T, Dau H (2005c) A novel BioXAS technique with sub-millisecond time resolution to track oxidation state and structural changes at biological metal centers. J Synchrotron Rad 12:35–44CrossRefGoogle Scholar
  48. Haumann M, Barra M, Loja P, Löscher S, Krivanek R, Grundmeier A, Andreasson LE, Dau H (2006) Bromide does not bind to the Mn4Ca complex in its S1 state in Cl-depleted and Br-reconstituted oxygen-evolving photosystem II: evidence from X-ray absorption spectroscopy at the Br K-edge. Biochemistry 45:13101–13107PubMedCrossRefGoogle Scholar
  49. Hays AM, Vassiliev IR, Golbeck JH, Debus RJ (1998) Role of D1-His190 in proton-coupled electron transfer reactions in photosystem II: a chemical complementation study. Biochemistry 37:11352–11365PubMedCrossRefGoogle Scholar
  50. Hays AM, Vassiliev IR, Golbeck JH, Debus RJ (1999) Role of D1-His190 in the proton-coupled oxidation of tyrosine YZ in manganese-depleted photosystem II. Biochemistry 38:11851–11865PubMedCrossRefGoogle Scholar
  51. Hillier W, Wydrzynski T (2004) Substrate water interactions within the photosystem II oxygen evolving complex. Phys Chem Chem Phys 6:4882–4889CrossRefGoogle Scholar
  52. Ishikita H, Saenger W, Loll B, Biesiadka J, Knapp EW (2006) Energetics of a possible proton exit pathway for water oxidation in photosystem II. Biochemistry 45:2063–2071PubMedCrossRefGoogle Scholar
  53. Iuzzolino L, Dittmer J, Dörner W, Meyer-Klaucke W, Dau H (1998) X-ray absorption spectroscopy on layered photosystem II membrane particles suggests manganese-centered oxidation of the oxygen-evolving complex for the S0–S1, S1–S2, and S2–S3 transitions of the water oxidation cycle. Biochemistry 37:17112–17119PubMedCrossRefGoogle Scholar
  54. Joliot P, Joliot A (1968a) Analysis of the interactions between the two photosystems in isolated chloroplasts. Biochim Biophys Acta 153:635–652CrossRefGoogle Scholar
  55. Joliot P, Joliot A (1968b) A polarographic method for detection of oxygen production and reduction of Hill reagent by isolated chloroplasts. Biochim Biophys Acta 153:625–634CrossRefGoogle Scholar
  56. Junge W (1976) Flash kinetic spectrophotometry in the study of plant pigments. In: Goodwin TW (ed) Chemistry and biochemistry of plant pigments 2. Academic Press, London, pp 233–333Google Scholar
  57. Junge W, Clausen J (2006) Photosynthetic oxygen production. Science 312:1470PubMedCrossRefGoogle Scholar
  58. Junge W, Haumann M, Ahlbrink R, Mulkidjanian A, Clausen J (2002) Electrostatics and proton transfer in photosynthetic water oxidation. Phil Trans R Soc London Ser B 357:1407–1418CrossRefGoogle Scholar
  59. Kamiya N, Shen J-R (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc Natl Acad Sci USA 100:98–103PubMedCrossRefGoogle Scholar
  60. Kern J, Loll B, Zouni A, Saenger W, Irrgang KD, Biesiadka J (2005) Cyanobacterial photosystem II at 3.2 A resolution – the plastoquinone binding pockets. Photosynth Res 84:153–159PubMedCrossRefGoogle Scholar
  61. Kok B, Forbush B, McGloin M (1970) Cooperation of charges in photosynthetic O2 evolution – I. A linear four-step mechanism. Photochem Photobiol 11:457–475PubMedGoogle Scholar
  62. Koningsberger DC, Mojet BL, van Dorssen GE, Ramaker DE (2000) XAFS spectroscopy; fundamental principles and data analysis. Top Catal 10:143–155CrossRefGoogle Scholar
  63. Krivanek R, Kern J, Zouni A, Dau H, Haumann M (2007) Spare quinones in the QB cavity of crystallized potosystem II from Thermosynechococcus elongatus, Biochim Biophys Acta (submitted)Google Scholar
  64. Lavergne J (1987) Optical-difference spectra of the S-state transitions in the photosynthetic oxygen-evolving complex. Biochim Biophys Acta 894:91–107CrossRefGoogle Scholar
  65. Lavergne J, Junge W (1993) Proton release during the redox cycle of the water oxidase. Photosynth Res 38:279–296CrossRefGoogle Scholar
  66. Liang W, Latimer MJ, Dau H, Roelofs TA, Yachandra VK, Sauer K, Klein MP (1994) Correlation between structure and magnetic spin state of the manganese cluster in the oxygen-evolving complex of photosystem II in the S2 state: determination by x-ray absorption spectroscopy. Biochemistry 33:4923–4932PubMedCrossRefGoogle Scholar
  67. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 A resolution structure of photosystem II. Nature 438:1040–1044PubMedCrossRefGoogle Scholar
  68. Mamedov F, Sayre RT, Styring S (1998) Involvement of histidine 190 on the D1 protein in electron/proton transfer reactions on the donor side of photosystem II. Biochemistry 37:14245–14256PubMedCrossRefGoogle Scholar
  69. McEvoy JP, Brudvig GW (2004) Structure-based mechanism of photosynthetic water oxidation. Phys Chem Chem Phys 6:4754–4763CrossRefGoogle Scholar
  70. McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106:4455–4483PubMedCrossRefGoogle Scholar
  71. Meinke C, Sole VA, Pospisil P, Dau H (2000) Does the structure of the water-oxidizing photosystem II-manganese complex at room temperature differ from its low-temperature structure? A comparative X-ray absorption study. Biochemistry 39:7033–7040PubMedCrossRefGoogle Scholar
  72. Messinger J, Schroder WP, Renger G (1993) Structure-function relations in photosystem II. Effects of temperature and chaotropic agents on the period four oscillation of flash-induced oxygen evolution. Biochemistry 32:7658–7668PubMedCrossRefGoogle Scholar
  73. Messinger J, Robblee JH, Bergmann U, Fernandez C, Glatzel P, Visser H, Cinco RM, McFarlane KL, Bellacchio E, Pizarro SA, Cramer SP, Sauer K, Klein MP, Yachandra VK (2001) Absence of Mn-centered oxidation in the S2->S3 transition: implications for the mechanism of photosynthetic water oxidation. J Am Chem Soc 123:7804–7820PubMedCrossRefGoogle Scholar
  74. Müller C, Liebisch P, Barra M, Dau H, Haumann M (2005) The location of calcium in the manganese complex of oxygenic photosynthesis studied by X-ray absorption spectroscopy at the Ca K-edge. Phys Scripta T115:847–850CrossRefGoogle Scholar
  75. Nugent JHA (2001) Photosynthetic water oxidation (special issue). Biochim Biophys Acta 1503:1–259PubMedCrossRefGoogle Scholar
  76. Ono T, Noguchi T, Inoue Y, Kusunoki M, Matsushita T, Oyanagi H (1992) X-ray-detection of the period-4 cycling of the manganese cluster in photosynthetic water oxidizing enzyme. Science 258:1335–1337CrossRefPubMedGoogle Scholar
  77. Ort D, Yocum CF (1996) Oxygenic photosynthesis – the light reactions. Kluwer Academic Publ., DordrechtGoogle Scholar
  78. Peloquin JM, Britt RD (2001) EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster. Biochim Biophys Acta 1503:96–111PubMedCrossRefGoogle Scholar
  79. Penner-Hahn JE (1999a) Structural characterization of the Mn site in the photosynthetic oxygen-evolving complex. In: Hill HAO, Sadler PJ, Thomson AJ (eds) Metal sites in proteins and models: redox centers. Springer, Berlin, pp 1–36Google Scholar
  80. Penner-Hahn JE (1999b) X-ray absorption spectroscopy in coordination chemistry. Coord Chem Rev 190–192:1101–1123CrossRefGoogle Scholar
  81. Penner-Hahn JE, Yocum CF (2006) Photosynthetic oxygen production – response. Science 312:1470–1471Google Scholar
  82. Pospisil P, Haumann M, Dittmer J, Sole VA, Dau H (2003) Stepwise transition of the tetra-manganese complex of photosystem II to a binuclear Mn2(m-O)2 complex in response to a temperature jump: a time-resolved structural investigation eEmploying X-ray absorption spectroscopy. Biophys J 84:1370–1386PubMedCrossRefGoogle Scholar
  83. Rappaport F, Blanchard-Desce M, Lavergne J (1994) Kinetics of electron transfer and electrochromic change during the redox transition of the photosynthetic oxygen-evolving complex. Biochim Biophys Acta 1184:178–192CrossRefGoogle Scholar
  84. Razeghifard MR, Pace RJ (1997) Electron paramagnetic resonance kinetic studies of the S states in spinach PSII membranes. Biochim Biophys Acta 1322:141–150CrossRefGoogle Scholar
  85. Razeghifard MR, Pace RJ (1999) EPR kinetic studies of oxygen release in thylakoids and PSII membranes: an intermediate in the S3 to S0 transition. Biochemistry 38:1252–1257PubMedCrossRefGoogle Scholar
  86. Rehder D, Schulzke C, Dau H, Meinke C, Hanss J, Epple M (2000) Water and bromide in the active center of vanadate-dependent haloperoxidases. J Inorg Biochem 80:115–121PubMedCrossRefGoogle Scholar
  87. Renger G (2001) Photosynthetic water oxidation to molecular oxygen: apparatus and mechanism. Biochim Biophys Acta 1503:210–228PubMedCrossRefGoogle Scholar
  88. Renger G, Hanssum B (1992) Studies on the reaction coordinates of the water oxidase in PS II membrane fragments from spinach. FEBS Lett 299:28–32PubMedCrossRefGoogle Scholar
  89. Renger G, Weiss W (1982) The detection of intrinsic 320 nm absorption changes reflecting the turnover of the water-splitting enzyme system Y which leads to oxygen formation in trypsinized chloroplasts. FEBS Lett 137(2):217–221CrossRefGoogle Scholar
  90. Riggs-Gelasco PJ, Mei R, Yocum CF, Penner-Hahn JE (1996) Reduced derivatives of the Mn cluster in the oxygen-evolving complex of photosystem II: an EXAFS study. J Am Chem Soc 118:2387–2399CrossRefGoogle Scholar
  91. Robblee JH, Cinco RM, Yachandra VK (2001) X-ray spectroscopy-based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution. Biochim Biophys Acta 1503:7–23PubMedCrossRefGoogle Scholar
  92. Schiller H, Dau H (2000) Preparation protocols for high-activity Photosystem II membrane particles of green algae and higher plants, pH dependence of oxygen evolution and comparison of the S2-state multiline signal by X-band EPR spectroscopy. J Photochem Photobiol B 55:138–144PubMedCrossRefGoogle Scholar
  93. Schiller H, Dittmer J, Iuzzolino L, Dörner W, Meyer-Klaucke W, Sole VA, Nolting H-F, Dau H (1998) Structure and orientation of the oxygen-evolving manganese complex of green algae and higher plants investigated by X-ray absorption linear dichroism spectroscopy on oriented photosystem II membrane particles. Biochemistry 37:7340–7350PubMedCrossRefGoogle Scholar
  94. Teo B (1986) EXAFS: basic principles and data analysis. Springer Verlag, Berlin, GermanyGoogle Scholar
  95. Weng T-C, Hsieh W-Y, Uffelman ES, Gordon-Wylie SW, Collins TJ, Pecoraro VL, Penner-Hahn JE (2004) XANES evidence against a manganyl species in the S3 state of the oxygen-evolving complex. J Am Chem Soc 126:8070–8071PubMedCrossRefGoogle Scholar
  96. Westphal KL, Lydakis-Simantiris N, Cukier RI, Babcock GT (2000) Effects of Sr2+-substitution on the reduction rates of Yz* in PSII membranes – evidence for concerted hydrogen-atom transfer in oxygen evolution. Biochemistry 39:16220–16229PubMedCrossRefGoogle Scholar
  97. Witt HT, Rumberg B, Schmidt-Mende P, Siggel U, Skerra B, Vater J, Weikard J (1965) On the analysis of photosynthesis by flashlight techniques. Angew Chem In Ed 4:799–819CrossRefGoogle Scholar
  98. Yamanari T, Kimura Y, Mizusawa N, Ishii A, Ono T-A (2004) Mid- to low-frequency Fourier transform infrared spectra of S-state cycle for photosynthetic water oxidation in Synechocystis sp. PCC 6803. Biochemistry 43:7479–7490PubMedCrossRefGoogle Scholar
  99. Yano J, Kern J, Irrgang K-D, Latimer MJ, Bergmann U, Glatzel P, Pushkar Y, Biesiadka J, Loll B, Sauer K, Messinger J, Zouni A, Yachandra VK (2005) X-ray damage to the Mn4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography. Proc Natl Acad Sci USA 102:12047–12052PubMedCrossRefGoogle Scholar
  100. Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–743PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.FB PhysikFreie Universität BerlinBerlinGermany

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