Photosynthesis Research

, Volume 92, Issue 3, pp 389–405

Structure of the Mn4–Ca cluster as derived from X-ray diffraction

  • Jan Kern
  • Jacek Biesiadka
  • Bernhard Loll
  • Wolfram Saenger
  • Athina Zouni
Research Article

Abstract

The catalytic centre for light-induced water oxidation in photosystem II (PSII) is a multinuclear metal cluster containing four manganese and one calcium cations. Knowing the structure of this biological catalyst is of utmost importance for unravelling the mechanism of water oxidation in photosynthesis. In this review we describe the current state of the X-ray structure determination at 3.0 Å resolution of the water oxidation complex (WOC) of PSII. The arrangement of metal cations in the cluster, their coordination and protein surroundings are discussed with regard to spectroscopic and mutagenesis studies. Limitations of the presently available structural data are pointed out and possible perspectives for the future are outlined, including the combination of X-ray diffraction and X-ray spectroscopy on single crystals.

Keywords

Mn-cluster Photosystem II Radiation damage Structure Water oxidizing complex X-ray absorption spectroscopy X-ray diffraction 

Abbreviations

Car

Carotenoid

Chla

Chlorophyll a

ETC

Electron transfer chain

EXAFS

Extended X-ray absorption fine structure

FTIR

Fourier transform infrared

PbRC

Purple bacterial reaction centre

Pheo

Pheophytin a

RC

Reaction centre

PSII

Photosystem II

XAS

X-ray absorption spectroscopy

WOC

Water oxidizing complex

References

  1. Adir N, Okamura MY, Feher G (1992) Crystallization of the PSII-reaction center. In: Murata N (ed) Research in photosynthesis. Kluwer Academic Press, DordrechtGoogle Scholar
  2. Allakhverdiev SI, Yruela II, Picorel R, Klimov VV (1997) Bicarbonate is an essential constituent of the water-oxidizing complex of photosystem II. Proc Natl Acad Sci USA 94:5050–5054PubMedCrossRefGoogle Scholar
  3. Baranov SV, Ananyev GM, Klimov VV, Dismukes GC (2000) Bicarbonate accelerates assembly of the inorganic core of the water-oxidizing complex in manganese-depleted photosystem II: a proposed biogeochemical role for atmospheric carbon dioxide in oxygenic photosynthesis. Biochemistry 39:6060–6065PubMedCrossRefGoogle Scholar
  4. Barber J, Nield J, Morris EP, Hankamer B (1999) Subunit positioning in photosystem II revisited. Trends Biochem Sci 24:43–45PubMedCrossRefGoogle Scholar
  5. Barber J, Ferreira KN, Maghlaoui K, Iwata S (2004) Structural model of the oxygen-evolving centre of photosystem II with mechanistic implications. Phys Chem Chem Phys 6:4737–4742CrossRefGoogle Scholar
  6. Baumgarten M, Philo JS, Dismukes GC (1990) Mechanism of photoinhibition of photosynthetic water oxidation by Cl depletion and F substitution: oxidation of a protein residue. Biochemistry 29:10814–10822PubMedCrossRefGoogle Scholar
  7. Biesiadka J, Loll B, Kern J, Irrgang K-D, Zouni A (2004) Crystal structure of cyanobacterial photosystem II at 3.2 Å resolution: a closer look at the Mn-cluster. Phys Chem Chem Phys 6:4733–4736CrossRefGoogle Scholar
  8. Boekema EJ, Hankamer B, Bald D, Kruip J, Nield J, Boonstra AF, Barber J, Rögner M (1995) Supramolecular structure of the photosystem II complex from green plants and cyanobacteria. Proc Natl Acad Sci USA 92:175–179PubMedCrossRefGoogle Scholar
  9. Boekema EJ, van Breemen JF, van Roon H, Dekker JP (2000) Arrangement of photosystem II supercomplexes in crystalline macrodomains within the thylakoid membrane of green plant chloroplasts. J Mol Biol 301:1123–1133PubMedCrossRefGoogle Scholar
  10. Boussac A, Kuhl H, Ghibaudi E, Rögner M, Rutherford AW (1999) Detection of an electron paramagnetic resonance signal in the S0 state of the manganese complex of photosystem II from Synechococcus elongatus. Biochemistry 38:11942–11948PubMedCrossRefGoogle Scholar
  11. Bricker TM, Frankel LK (1998) The structure and function of the 33 kDa extrinsic protein of photosystem II: a critical assessment. Photosynth Res 56:157–173CrossRefGoogle Scholar
  12. Bricker TM, Frankel LK (2002) The structure and function of CP47 and CP43 in Photosystem II. Photosynth Res 72:131–146PubMedCrossRefGoogle Scholar
  13. Britt RD, Peloquin JM, Campbell KA (2000) Pulsed and parallel-polarization EPR characterization of the photosystem II oxygen-evolving complex. Annu Rev Biophys Biomol Struct 29:463–495PubMedCrossRefGoogle Scholar
  14. Burda K, Bader KP, Schmid GH (2001) An estimation of the size of the water cluster present at the cleavage site of the water splitting enzyme. FEBS Lett 491:81–84PubMedCrossRefGoogle Scholar
  15. Burnap RL (2004) D1 protein processing and Mn cluster assembly in light of the emerging Photosystem II structure. Phys Chem Chem Phys 6:4803–4809CrossRefGoogle Scholar
  16. Campbell KA, Gregor W, Pham DP, Peloquin JM, Debus RJ, Britt RD (1998) The 23 and 17 kDa extrinsic proteins of photosystem II modulate the magnetic properties of the S1-state manganese cluster. Biochemistry 37:5039–5045PubMedCrossRefGoogle Scholar
  17. Campbell KA, Force DA, Nixon PJ, Dole F, Diner BA, Britt RD (2000) Dual-mode EPR detects the initial intermediate in photoassembly of the photosystem II Mn cluster: the influence of amino acid residue 170 of the D1 polypeptide on Mn coordination. J Am Chem Soc 122:3754–3761CrossRefGoogle Scholar
  18. Carrell TG, Tyryshkin AM, Dismukes GC (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
  19. Chu HA, Nguyen AP, Debus RJ (1995a) Amino acid residues that influence the binding of manganese or calcium to photosystem II. 1. The lumenal interhelical domains of the D1 polypeptide. Biochemistry 34:5839–5858PubMedCrossRefGoogle Scholar
  20. Chu HA, Nguyen AP, Debus RJ (1995b) Amino acid residues that influence the binding of manganese or calcium to photosystem II. 2. The carboxy-terminal domain of the D1 polypeptide. Biochemistry 34:5859–5882PubMedCrossRefGoogle Scholar
  21. Chu HA, Hillier W, Debus RJ (2004) Evidence that the C-terminus of the D1 polypeptide of photosystem II is ligated to the manganese ion that undergoes oxidation during the S1 to S2 transition: an isotope-edited FTIR study. Biochemistry 43:3152–3166PubMedCrossRefGoogle Scholar
  22. Cinco RM, Robblee JH, Rompel A, Fernandez C, Yachandra VK, Sauer K, Klein MP (1998) Strontium EXAFS reveals the proximity of calcium to the manganese cluster of oxygen-evolving photosystem II. J Phys Chem B 102:8248–8256CrossRefGoogle Scholar
  23. Cinco RM, McFarlane Holman KL, 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
  24. Cinco RM, Robblee JH, Messinger J, Fernandez C, Holman KL, Sauer K, Yachandra VK (2004) Orientation of calcium in the Mn(4)Ca cluster of the oxygen-evolving complex determined using polarized strontium EXAFS of photosystem II membranes. Biochemistry 43:13271–13282PubMedCrossRefGoogle Scholar
  25. Clausen J, Winkler S, Hays AM, Hundelt M, Debus RJ, Junge W (2001) Photosynthetic water oxidation in Synechocystis sp. PCC6803 mutations D1-E189K, R and Q are without influence on electron transfer at the donor side of photosystem II. Biochim Biophys Acta 1506:224–235PubMedCrossRefGoogle Scholar
  26. Clemens KL, Force DA, Britt RD (2002) Acetate binding at the photosystem II oxygen evolving complex: An S(2)-state multiline signal ESEEM study. J Am Chem Soc 124:10921–10933PubMedCrossRefGoogle Scholar
  27. 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
  28. 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
  29. Debus RJ (2005) The catalytic manganese cluster: protein ligation. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light driven water:plastoquinone oxidoreductase. Springer, DordrechtGoogle Scholar
  30. Debus RJ, Campbell KA, Pham DP, Hays AM, Britt RD (2000) Glutamate 189 of the D1 polypeptide modulates the magnetic and redox properties of the manganese cluster and tyrosine Y(Z) in photosystem II. Biochemistry 39:6275–6287PubMedCrossRefGoogle Scholar
  31. Debus RJ, Campbell KA, Gregor W, Li ZL, Burnap RL, Britt RD (2001) Does histidine 332 of the D1 polypeptide ligate the manganese cluster in photosystem II? An electron spin echo envelope modulation study. Biochemistry 40:3690–3699PubMedCrossRefGoogle Scholar
  32. Debus RJ, Aznar C, Campbell KA, Gregor W, Diner BA, Britt RD (2003) Does aspartate 170 of the D1 polypeptide ligate the manganese cluster in photosystem II? An EPR and ESEEM Study. Biochemistry 42:10600–10608PubMedCrossRefGoogle Scholar
  33. Debus RJ, Strickler MA, Walker LM, Hillier W (2005) No evidence from FTIR difference spectroscopy that aspartate-170 of the D1 polypeptide ligates a manganese ion that undergoes oxidation during the S0 to S1, S1 to S2, or S2 to S3 transitions in photosystem II. Biochemistry 44:1367–1374PubMedCrossRefGoogle Scholar
  34. Deisenhofer J, Epp O, Miki K, Huber R, Michel H (1984) X-ray structure analysis of a membrane protein complex. Electron density map at 3 Å resolution and a model of the chromophores of the photosynthetic reaction center from Rhodopseudomonas viridis. J Mol Biol 180:385–398PubMedCrossRefGoogle Scholar
  35. Deisenhofer J, Epp O, Miki K, Huber R, Michel H (1985) Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution. Nature 318:618–624CrossRefGoogle Scholar
  36. DeLano WL (2002) The PyMOL Molecular Graphics SystemGoogle Scholar
  37. DeRose VJ, Yachandra VK, McDermott AE, Britt RD, Sauer K, Klein MP (1991) Nitrogen ligation to manganese in the photosynthetic oxygen-evolving complex: continuous-wave and pulsed EPR studies of photosystem II particles containing 14N or 15N. Biochemistry 30:1335–1341PubMedCrossRefGoogle Scholar
  38. Diner BA (2001) Amino acid residues involved in the coordination and assembly of the manganese cluster of photosystem II. Proton-coupled electron transport of the redox-active tyrosines and its relationship to water oxidation. Biochim Biophys Acta 1503:147–163PubMedCrossRefGoogle Scholar
  39. Dismukes GC (1988) The spectroscopically derived structure of the manganese site for photosynthetic water oxidization and a proposal for the protein-binding sites for calcium and manganese. Chem Scripta A 28:99–104Google Scholar
  40. Dorlet P, Di Valentin M, Babcock GT, McCracken JL (1998) Interaction of Y-Z(center dot) with its environment in acetate-treated photosystem II membranes and reaction center cores. J Phys Chem B 102:8239–8247CrossRefGoogle Scholar
  41. Eggers B, Vermaas W (1993) Truncation of the D2 protein in Synechocystis sp. PCC 6803 a role of the C-terminal domain of D2 in photosystem II function and stability. Biochemistry 32:11419–11427PubMedCrossRefGoogle Scholar
  42. Erickson JM, Rahire M, Rochaix J-D (1984) Chlamydomonas reinhardii gene for the 32,000 mol. wt. protein of photosystem II contains four large introns and is located entirely within the chloroplast inverted repeat. EMBO J 3:2753–2762PubMedGoogle Scholar
  43. Fernandez C, Cinco RM, Robblee JH, Messinger J, Pizarro SA, Sauer K, Klein MP, Yachandra VK (1998) Calcium and chloride cofactors of the oxygen evolving complex – X-ray absorption spectroscopy evidence for a Mn/Ca/Cl heteronuclear cluster. In: Garab G (ed) Photosynthesis: mechanisms and effects. Kluwer Academic Publishers, DordrechtGoogle Scholar
  44. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838PubMedCrossRefGoogle Scholar
  45. Force DA, Randall DW, Britt RD (1997) Proximity of acetate, manganese, and exchangeable deuterons to tyrosine YZ . in acetate-inhibited photosystem II membranes: implications for the direct involvement of YZ . in water-splitting. Biochemistry 36:12062–12070PubMedCrossRefGoogle Scholar
  46. Fotinou C, Kokkinidis M, Fritzsch G, Haase W, Michel H, Ghanotakis DF (1993) Characterization of a photosystem II core and its three-dimensional crystals. Photosynth Res 37:41–48CrossRefGoogle Scholar
  47. Ghirardi ML, Lutton TW, Seibert M (1998) Effects of carboxyl amino acid modification on the properties of the high-affinity, manganese-binding site in photosystem II. Biochemistry 37:13559–13566PubMedCrossRefGoogle Scholar
  48. Grabolle M, Haumann M, Muller 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
  49. Haag E, Irrgang K-D, Boekema EJ, Renger G (1990) Functional and structural analysis of photosystem II core complexes from spinach with high oxygen evolution capacity. Eur J Biochem 189:47–53PubMedCrossRefGoogle Scholar
  50. Hansson Ö, Andreasson LE, Vänngard T (1986) Oxygen from water is coordinated to manganese in the S2 state of photosystem II. FEBS Lett 195:151–154CrossRefGoogle Scholar
  51. Hasegawa K, Kimura Y, Ono T (2002) Chloride cofactor in the photosynthetic oxygen-evolving complex studied by Fourier transform infrared spectroscopy. Biochemistry 41:13839–13850PubMedCrossRefGoogle Scholar
  52. Hasegawa K, Kimura Y, Ono TA (2004) Oxidation of the Mn cluster induces structural changes of NO3− functionally bound to the Cl site in the oxygen-evolving complex of photosystem II. Biophys J 86:1042–1050PubMedGoogle Scholar
  53. Haumann M, Müller C, Liebisch P, Iuzzolino L, Dittmer J, Grabolle M, Neisius T, Meyer-Klaucke W, Dau H (2005) 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, and S3,4 → S0) characterized by X-ray absorption spectroscopy at 20 K and room temperature. Biochemistry 44:1894–1908PubMedCrossRefGoogle Scholar
  54. 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
  55. 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
  56. Holzenburg A, Bewly MC, Wilson FH, Nicholson WV, Ford R (1993) Three-dimensional structure of photosystem II. Nature 363:470–472CrossRefGoogle Scholar
  57. Inagaki N, Maitra R, Satoh K, Pakrasi HB (2001) Amino acid residues that are critical for in vivo catalytic activity of CtpA, the carboxyl-terminal processing protease for the D1 protein of photosystem II. J Biol Chem 276:30099–30105PubMedCrossRefGoogle Scholar
  58. Iwata S, Barber J (2004) Structure of photosystem II and molecular architecture of the oxygen-evolving centre. Curr Opin Struct Biol 14:447–453PubMedCrossRefGoogle Scholar
  59. Kamiya N, Shen JR (2003) Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. Proc Natl Acad Sci 100:98–103PubMedCrossRefGoogle Scholar
  60. Kawamori A, Katsuta N, Mino H, Ishii A, Minagawa J, Ono TA (2002) Positions of Q(A) and Chl(Z) relative to tyrosine Y-Z and Y-D in photosystem II studied by pulsed EPR. J Biol Phys 28:413–426CrossRefGoogle Scholar
  61. Keilty AT, Ermakova-Gerdes SY, Vermaas WF (2000) Probing the CD lumenal loop region of the D2 protein of photosystem II in Synechocystis sp. strain PCC 6803 by combinatorial mutagenesis. J Bacteriol 182:2453–2460PubMedCrossRefGoogle Scholar
  62. Keilty AT, Vavilin DV, Vermaas WF (2001) Functional analysis of combinatorial mutants with changes in the C-terminus of the CD loop of the D2 protein in photosystem II of Synechocystis sp. PCC 6803. Biochemistry 40:4131–4139PubMedCrossRefGoogle Scholar
  63. Kern J, Loll B, Lüneberg C, DiFiore D, Biesiadka J, Irrgang KD, Zouni A (2005) Purification, characterisation and crystallisation of photosystem II from Thermosynechococcus elongatus cultivated in a new type of photobioreactor. Biochim Biophys Acta 1706:147–157PubMedCrossRefGoogle Scholar
  64. Kimura Y, Ishii A, Yamanari T, Ono TA (2005a) Water-sensitive low-frequency vibrations of reaction intermediates during S-state cycling in photosynthetic water oxidation. Biochemistry 44:7613–7622PubMedCrossRefGoogle Scholar
  65. Kimura Y, Mizusawa N, Yamanari T, Ishii A, Ono TA (2005b) Structural changes of D1 C-terminal alpha-carboxylate during S-state cycling in photosynthetic oxygen evolution. J Biol Chem 280:2078–2083PubMedCrossRefGoogle Scholar
  66. Klimov VV, Allakhverdiev SI, Feyziev Ya M, Baranov SV (1995) Bicarbonate requirement for the donor side of photosystem II. FEBS Lett 363:251–255PubMedCrossRefGoogle Scholar
  67. Knoepfle N, Bricker TM, Putnam-Evans C (1999) Site-directed mutagenesis of basic arginine residues 305 and 342 in the CP 43 protein of photosystem II affects oxygen-evolving activity in Synechocystis 6803. Biochemistry 38:1582–1588PubMedCrossRefGoogle Scholar
  68. Kodera Y, Hara H, Astashkin YV, Kawamori A, Ono TA (1995) EPR study of trapped tyrosine Z+ in Ca-depleted photosystem II. Biochim Biophys Acta 1232:43–51CrossRefGoogle Scholar
  69. Kuhl H, Kruip J, Seidler A, Krieger-Liszkay A, Bünker M, Bald D, Scheidig AJ, Rögner M (2000) Towards structural determination of the water-splitting enzyme. Purification, crystallization, and preliminary crystallographic studies of photosystem II from a thermophilic cyanobacterium. J Biol Chem 275:20652–20659PubMedCrossRefGoogle Scholar
  70. Kuta Smatanova I, Gavira JA, Rezacova P, Vacha F, Garcia-Ruiz JM (2006) New techniques for membrane protein crystallization tested on photosystem II core complex of Pisum sativum. Photosynth Res 90:255–259PubMedCrossRefGoogle Scholar
  71. Lakshmi KV, Eaton SS, Eaton GR, Brudvig GW (1999) Orientation of the tetranuclear manganese cluster and tyrosine Z in the O2-evolving complex of photosystem II: an EPR study of the S2YZ* state in oriented acetate-inhibited photosystem II membranes. Biochemistry 38:12758–12767PubMedCrossRefGoogle Scholar
  72. Lakshmi KV, Reifler MJ, Chisholm DA, Wang JY, Diner BA, Brudvig GW (2002) Correlation of the cytochrome c(550) content of cyanobacterial Photosystem II with the EPR properties of the oxygen-evolving complex. Photosynth Res 72:175–189PubMedCrossRefGoogle Scholar
  73. Latimer MJ, DeRose VJ, Mukerji I, Yachandra VK, Sauer K, Klein MP (1995) Evidence for the proximity of calcium to the manganese cluster of photosystem II: determination by X-ray absorption spectroscopy. Biochemistry 34:10898–10909PubMedCrossRefGoogle Scholar
  74. Li ZL, Burnap RL (2001) Mutations of arginine 64 within the putative Ca2+-binding lumenal interhelical a-b loop of the photosystem II D1 protein disrupt binding of the manganese stabilizing protein and cytochrome c(550) in Synechocystis sp. PCC6803. Biochemistry 40:10350–10359PubMedCrossRefGoogle Scholar
  75. Li Z, Andrews H, Eaton-Rye JJ, Burnap RL (2004) In situ effects of mutations of the extrinsic cytochrome c550 of photosystem II in Synechocystis sp. PCC6803. Biochemistry 43:14161–14170PubMedCrossRefGoogle Scholar
  76. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044PubMedCrossRefGoogle Scholar
  77. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2007) Lipids in Photosystem II: interactions with protein and cofactors. Biochim Biophys Acta doi:10.1016/j.bbabio.2006.12.009Google Scholar
  78. Magnuson A, Andreasson LE (1997) Different manganese binding sites in photosystem II probed by selective chemical modification of histidyl and carboxylic acid residues. Biochemistry 36:3254–3261PubMedCrossRefGoogle Scholar
  79. Metz JG, Bishop NI (1980) Identification of a chloroplast membrane polypeptide associated with the oxidizing side of photosystem-II by the use of select low-fluorescent mutants of Scenedesmus. Biochem Biophys Res Commun 94:560–566PubMedCrossRefGoogle Scholar
  80. Michel H, Deisenhofer J (1986) X-ray diffraction studies on a crystalline bacterial reaction center: A progress report and conclusions on the structure of photosystem II reaction centers. In: Staehelin LA, Arntzen CJ (eds) Encyclopedia of plant physiology – photosynthesis III. Springer, Berlin, pp 371–381Google Scholar
  81. Michel H, Deisenhofer J (1988) Relevance of the photosynthetic reaction center from purple bacteria to the structure of photosystem II. Biochemistry 27:1–7CrossRefGoogle Scholar
  82. Miyao M, Murata N (1984) Role of the 33-Kda polypeptide in preserving Mn in the photosynthetic oxygen-evolution system and its replacement by Chloride-ions. FEBS Lett 170:350–354CrossRefGoogle Scholar
  83. Mizusawa N, Kimura Y, Ishii A, Yamanari T, Nakazawa S, Teramoto H, Ono TA (2004) Impact of replacement of D1 C-terminal alanine with glycine on structure and function of photosynthetic oxygen evolving complex. J Biol Chem 279:29622–29627PubMedCrossRefGoogle Scholar
  84. Morris EP, Hankamer B, Zheleva D, Friso G, Barber J (1997) The three-dimensional structure of a photosystem II core complex determined by electron crystallography. Structure 5:837–849PubMedCrossRefGoogle Scholar
  85. Mulkidjanian AY, Cherepanov DA, Haumann M, Junge W (1996) Photosystem II of green plants: topology of core pigments and redox cofactors as inferred from electrochromic difference spectra. Biochemistry 35:3093–3107PubMedCrossRefGoogle Scholar
  86. Nakazato K, Toyoshima C, Enami I, Inoue Y (1996) Two-dimensional crystallization and cryo-electron microscopy of photosystem II. J Mol Biol 257:225–232PubMedCrossRefGoogle Scholar
  87. Nield J, Orlova EV, Morris EP, Gowen B, van Heel M, Barber J (2000) 3D map of the plant photosystem II supercomplex obtained by cryoelectron microscopy and single particle analysis. Nat Struct Biol 7:44–47PubMedCrossRefGoogle Scholar
  88. Nixon PJ, Diner BA (1994) Analysis of water-oxidation mutants constructed in the cyanobacterium Synechocystis sp. PCC 6803. Biochem Soc Trans 22:338–343PubMedGoogle Scholar
  89. Nixon PJ, Trost JT, Diner BA (1992) Role of the carboxy terminus of polypeptide D1 in the assembly of a functional water-oxidizing manganese cluster in photosystem II of the cyanobacterium Synechocystis sp. PCC 6803: assembly requires a free carboxyl group at C-terminal position 344. Biochemistry 31:10859–10871PubMedCrossRefGoogle Scholar
  90. Noguchi T, Ono T, Inoue Y (1995) Direct detection of a carboxylate bridge between Mn and Ca2+ in the photosynthetic oxygen-evolving center by means of Fourier transform infrared spectroscopy. Biochim Biophys Acta 1228:189–200CrossRefGoogle Scholar
  91. Noguchi T, Inoue Y, Tang XS (1999) Structure of a histidine ligand in the photosynthetic oxygen-evolving complex as studied by light-induced Fourier transform infrared difference spectroscopy. Biochemistry 38:10187–10195PubMedCrossRefGoogle Scholar
  92. Oishi KK, Shapiro DR, Tewari KK (1984) Sequence organization of a pea chloroplast DNA gene coding for a 34,500-dalton protein. Mol Cell Biol 4:2556–2563PubMedGoogle Scholar
  93. Olesen K, Andreasson LE (2003) The function of the chloride ion in photosynthetic oxygen evolution. Biochemistry 42:2025–2035PubMedCrossRefGoogle Scholar
  94. Ono TA, Mino H (1999) Unique binding site for Mn2+ ion responsible for reducing an oxidized YZ tyrosine in manganese-depleted photosystem II membranes. Biochemistry 38:8778–8785PubMedCrossRefGoogle Scholar
  95. Peloquin JM, Campbell KA, Britt RD (1998) 55Mn pulsed ENDOR demonstrates that the photosystem II “split” EPR signal arises from a magnetically-coupled mangano-tyrosyl complex. J Am Chem Soc 120:6840–6841CrossRefGoogle Scholar
  96. Pizarro SA, Visser H, Cinco RM, Robblee JH, Pal S, Mukhopadhyay S, Mok HJ, Sauer K, Wieghardt K, Armstrong WH, Yachandra VK (2004) Chloride ligation in inorganic manganese model compounds relevant to photosystem II studied using X-ray absorption spectroscopy. J Biol Inorg Chem 9:247–255PubMedCrossRefGoogle Scholar
  97. Renger G, Christen G, Karge M, Eckert H-J, Irrgang K-D (1998) Application of the Marcus theory for analysis of the temperature dependence of the reactions leading to photosynthetic water oxidation – results and implications. Bioinorg Chem 3:360–366Google Scholar
  98. Rhee KH (2001) Photosystem II: the solid structural era. Annu Rev Biophys Biomol Struct 30:307–328PubMedCrossRefGoogle Scholar
  99. Rhee K-H, Morris EP, Zheleva D, Hankamer B, Kühlbrandt W, Barber J (1997) Two-dimensional structure of plant photosystem II at 8-Å resolution. Nature 389:522–526CrossRefGoogle Scholar
  100. Rhee KH, Morris EP, Barber J, Kühlbrandt W (1998) Three-dimensional structure of the plant photosystem II reaction centre at 8 Å resolution. Nature 396:283–286PubMedCrossRefGoogle Scholar
  101. Rögner M, Dekker JP, Boekema EJ, Witt HT (1987) Size, Shape and mass of the oxygen-evolving photosystem II complex from the thermophilic cyanobacterium Synechococcus sp FEBS Lett 219:207–211CrossRefGoogle Scholar
  102. Roffey RA, Kramer DM, Govindjee, Sayre RT (1994) Lumenal side histidine mutations in the D1 protein of photosystem II affect donor side electron transfer in Chlamydomonas reinhardtii. Biochim Biophys Acta 1185:257–270PubMedCrossRefGoogle Scholar
  103. Rosenberg C, Christian J, Bricker TM, Putnam-Evans C (1999) Site-directed mutagenesis of glutamate residues in the large extrinsic loop of the photosystem II protein CP 43 affects oxygen-evolving activity and PS II assembly. Biochemistry 38:15994–16000PubMedCrossRefGoogle Scholar
  104. Sachs RK, Halverson KM, Barry BA (2003) Specific isotopic labeling and photooxidation-linked structural changes in the manganese-stabilizing subunit of photosystem II. J Biol Chem 278:44222–44229PubMedCrossRefGoogle Scholar
  105. Santini C, Tidu V, Tognon G, Ghiretti Magaldi A, Bassi R (1994) Three-dimensional structure of the higher-plant photosystem II reaction centre and evidence for its dimeric organization in vivo. Eur J Biochem 221:307–315PubMedCrossRefGoogle Scholar
  106. Shen JR, Kamiya N (2000) Crystallization and the crystal properties of the oxygen-evolving photosystem II from Synechococcus vulcanus. Biochemistry 39:14739–14744PubMedCrossRefGoogle Scholar
  107. Shestakov SV, Anbudurai PR, Stanbekova GE, Gadzhiev A, Lind LK, Pakrasi HB (1994) Molecular cloning and characterization of the ctpA gene encoding a carboxyl-terminal processing protease. Analysis of a spontaneous photosystem II-deficient mutant strain of the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem 269:19354–19359PubMedGoogle Scholar
  108. Shevela DN, Khorobrykh AA, Klimov VV (2006) Effect of bicarbonate on the water-oxidizing complex of photosystem II in the super-reduced S-states. Biochim Biophys Acta 1757:253–261PubMedCrossRefGoogle Scholar
  109. Sproviero EM, Gascon JA, McEvoy JP, Brudvig GW, Batista VS (2006) Characterization of synthetic oxomanganese complexes and the inorganic core of the O2-evolving complex in photosystem II: evaluation of the DFT/B3LYP level of theory. J Inorg Biochem 100:786–800PubMedCrossRefGoogle Scholar
  110. Steffen R, Kelly AA, Huyer J, Doermann P, Renger G (2005) Investigations on the reaction pattern of photosystem II in leaves from Arabidopsis thaliana wild type plants and mutants with genetically modified lipid content. Biochemistry 44:3134–3142PubMedCrossRefGoogle Scholar
  111. Strickler MA, Walker LM, Hillier W, Debus RJ (2005) Evidence from biosynthetically incorporated strontium and FTIR difference spectroscopy that the C-terminus of the D1 polypeptide of photosystem II does not ligate calcium. Biochemistry 44:8571–8577PubMedCrossRefGoogle Scholar
  112. Suzuki H, Taguchi Y, Sugiura M, Boussac A, Noguchi T (2006) Structural perturbation of the carboxylate ligands to the manganese cluster upon Ca2+/Sr2+ exchange in the S-state cycle of photosynthetic oxygen evolution as studied by flash-induced FTIR difference spectroscopy. Biochemistry 45:13454–13464PubMedCrossRefGoogle Scholar
  113. Svensson B, Vass I, Cendergren E, Styring S (1990) Structure of donor side components in photosystem II predicted by computer modelling. EMBO J 9:2051–2059PubMedGoogle Scholar
  114. Svensson B, Etchebest C, Tuffery P, van Kan P, Smith J, Styring S (1996) A model for the photosystem II reaction center core including the structure of the primary donor P680. Biochemistry 35:14486–14502PubMedCrossRefGoogle Scholar
  115. Taguchi F, Yamamoto Y, Satoh K (1995) Recognition of the structure around the site of cleavage by the carboxyl-terminal processing protease for D1 precursor protein of the photosystem II reaction center. J Biol Chem 270:10711–10716PubMedCrossRefGoogle Scholar
  116. Tang XS, Diner BA, Larsen BS, Gilchrist ML Jr, Lorigan GA, Britt RD (1994) Identification of histidine at the catalytic site of the photosynthetic oxygen-evolving complex. Proc Natl Acad Sci 91:704–708PubMedCrossRefGoogle Scholar
  117. Taylor MA, Packer JR, Bowyer JR (1988) Processing of the D1 polypeptide of the photosystem-II reaction center and photoactivation of a low fluorescence mutant (Lf-1) of Scenedesmus Obliquus. FEBS Lett 237:229–233CrossRefGoogle Scholar
  118. Trebst A (1986) The topology of the plastoquinone and herbicide binding peptides of photosystem II in the thylakoid membrane. Z Naturforsch 41c:240–245Google Scholar
  119. Trost JT, Chisholm DA, Jordan DB, Diner BA (1997) The D1 C-terminal processing protease of photosystem II from Scenedesmus obliquus. Protein purification and gene characterization in wild type and processing mutants. J Biol Chem 272:20348–20356PubMedCrossRefGoogle Scholar
  120. Tsiotis G, McDermott G, Ghanotakis D (1996) Progress towards structural elucidation of photosystem II. Photosynth Res 50:93–101CrossRefGoogle Scholar
  121. van Gorkom HJ, Yocum CF (2005) The calcium and chloride cofactors. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light driven water:plastoquinone oxidoreductase. Springer, DordrechtGoogle Scholar
  122. van Rensen JJ, Klimov V (2005) Bicarbonate interactions. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light driven water:plastoquinone oxidoreductase. Springer, DordrechtGoogle Scholar
  123. Xiong J, Subramaniam S, Govindjee (1996) Modeling of the D1/D2 proteins and cofactors of the photosystem II reaction center: implications for herbicide and bicarbonate binding. Protein Sci 5:2054–2073PubMedCrossRefGoogle Scholar
  124. Xiong J, Subramaniam S, Govindjee (1998) A knowledge-based three dimensional model of the photosystem II reaction center of Chlamydomonas reinhardti. Photosynth Res 56:229–254CrossRefGoogle Scholar
  125. Yachandra V (2005) The catalytic manganese cluster: organization of the metal ions. In: Wydrzynski T, Satoh K (eds) Photosystem II: the light driven water:plastoquinone oxidoreductase. Springer, DordrechtGoogle Scholar
  126. Yachandra VK, Sauer K, Klein MP (1996) Manganese cluster in photosynthesis: where plants oxidize water to dioxygen. Chem Rev 96:2927–2950PubMedCrossRefGoogle Scholar
  127. Yakushevska AE, Keegstra W, Boekema EJ, Dekker JP, Andersson J, Jansson S, Ruban AV, Horton P (2003) The structure of photosystem II in Arabidopsis: localization of the CP26 and CP29 antenna complexes. Biochemistry 42:608–613PubMedCrossRefGoogle Scholar
  128. Yano J, Kern J, Irrgang KD, Latimer MJ, Bergmann U, Glatzel P, Pushkar Y, Biesiadka J, Loll B, Sauer K, Messinger J, Zouni A, Yachandra VK (2005a) X-ray damage to the Mn4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography. Proc Natl Acad Sci 102:12047–12052PubMedCrossRefGoogle Scholar
  129. Yano J, Pushkar Y, Glatzel P, Lewis A, Sauer K, Messinger J, Bergmann U, Yachandra V (2005b) High-resolution Mn EXAFS of the oxygen-evolving complex in photosystem II: structural implications for the Mn4Ca cluster. J Am Chem Soc 127:14974–14975PubMedCrossRefGoogle Scholar
  130. Yano J, Kern J, Sauer K, Latimer MJ, Pushkar Y, Biesiadka J, Loll B, Saenger W, Messinger J, Zouni A, Yachandra VK (2006) Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster. Science 314:821–825PubMedCrossRefGoogle Scholar
  131. Yi X, McChargue M, Laborde S, Frankel LK, Bricker TM (2005) The manganese-stabilizing protein is required for photosystem II assembly/stability and photoautotrophy in higher plants. J Biol Chem 280:16170–16174PubMedCrossRefGoogle Scholar
  132. Zech SG, Kurreck J, Eckert HJ, Renger G, Lubitz W, Bittl R (1997) Pulsed EPR measurement of the distance between P680and Q(A) in photosystem II. FEBS Lett 414:454–456PubMedCrossRefGoogle Scholar
  133. Zech SG, Kurreck J, Renger G, Lubitz W, Bittl R (1999) Determination of the distance between Y(Z)ox* and QA -* in photosystem II by pulsed EPR spectroscopy on light-induced radical pairs. FEBS Lett 442:79–82PubMedCrossRefGoogle Scholar
  134. Zimmermann K, Heck M, Frank J, Kern J, Vass I, Zouni A (2006) Herbicide binding and thermal stability of photosystem II isolated from Thermosynechococcus elongatus. Biochim Biophys Acta 1757:106–114PubMedCrossRefGoogle Scholar
  135. Zouni A, Lüneberg C, Fromme P, Schubert WD, Saenger W, Witt HT (1998) Characterization of single crystals of photosystem II from the thermophilic cyanobacterium Synechococcus elongatus In: Garab G (ed) Photosynthesis: mechanisms and effects. Kluwer Academic, DordrechtGoogle Scholar
  136. Zouni A, Jordan R, Schlodder E, Fromme P, Witt HT (2000) First photosystem II crystals capable of water oxidation. Biochim Biophys Acta 1457:103–105PubMedCrossRefGoogle Scholar
  137. Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001a) Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–743PubMedCrossRefGoogle Scholar
  138. Zouni A, Kern J, Loll B, Fromme P, Witt HT, Orth P, Krauss N, Saenger W, Biesiadka J (2001b) Biochemical characterization and crystal structure of water oxidizing photosystem II from Synechococcus elongatus. In: Proceedings of the 12th international congress on photosynthesis. CSIRO Publishing, Colingwood, S05-003Google Scholar
  139. Zouni A, Kern J, Frank J, Hellweg T, Behlke J, Saenger W, Irrgang KD (2005) Size determination of cyanobacterial and higher plant photosystem II by gel permeation chromatography, light scattering, and ultracentrifugation. Biochemistry 44:4572–4581PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Jan Kern
    • 1
  • Jacek Biesiadka
    • 2
  • Bernhard Loll
    • 2
    • 3
  • Wolfram Saenger
    • 2
  • Athina Zouni
    • 1
  1. 1.Institut für Chemie, Max Volmer Laboratorium für Biophysikalische Chemie, Sekr. PC 14Technische Universität BerlinBerlinGermany
  2. 2.Institut für Chemie und Biochemie/KristallographieFreie Universität BerlinBerlinGermany
  3. 3.Max-Planck-Institut für Medizinische Forschung, Abteilung für Biomolekulare MechanismenHeidelbergGermany

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