1932

Abstract

Oxygenic photosynthesis forms the basis of aerobic life on earth by converting light energy into biologically useful chemical energy and by splitting water to generate molecular oxygen. The water-splitting and oxygen-evolving reaction is catalyzed by photosystem II (PSII), a huge, multisubunit membrane-protein complex located in the thylakoid membranes of organisms ranging from cyanobacteria to higher plants. The structure of PSII has been analyzed at 1.9-Å resolution by X-ray crystallography, revealing a clear picture of the MnCaO cluster, the catalytic center for water oxidation. This article provides an overview of the overall structure of PSII followed by detailed descriptions of the specific structure of the MnCaO cluster and its surrounding protein environment. Based on the geometric organization of the MnCaO cluster revealed by the crystallographic analysis, in combination with the results of a vast number of experimental studies involving spectroscopic and other techniques as well as various theoretical studies, the article also discusses possible mechanisms for water splitting that are currently under consideration.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-050312-120129
2015-04-29
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/arplant/66/1/annurev-arplant-050312-120129.html?itemId=/content/journals/10.1146/annurev-arplant-050312-120129&mimeType=html&fmt=ahah

Literature Cited

  1. Agmon N. 1.  1995. The Grotthuss mechanism. Chem. Phys. Lett. 244:456–62 [Google Scholar]
  2. Ames W, Pantazis DA, Krewald V, Cox N, Messinger J. 2.  et al. 2011. Theoretical evaluation of structural models of the S2 state in the oxygen evolving complex of photosystem II: protonation states and magnetic interactions. J. Am. Chem. Soc. 133:19743–57 [Google Scholar]
  3. Barber J. 3.  2004. Engine of life and big bang of evolution: a personal perspective. Photosynth. Res. 80:137–55 [Google Scholar]
  4. Barber J. 4.  2006. Photosystem II: an enzyme of global significance. Biochem. Soc. Trans. 34:619–31 [Google Scholar]
  5. Barry BA, Babcock GT. 5.  1987. Tyrosine radicals are involved in the photosynthetic oxygen-evolving system. PNAS 84:7099–103 [Google Scholar]
  6. Blomberg MR, Borowski T, Himo F, Liao RZ, Siegbahn PE. 6.  2014. Quantum chemical studies of mechanisms for metalloenzymes. Chem. Rev. 114:3601–58 [Google Scholar]
  7. Boussac A, Rappaport F, Carrier P, Verbavatz JM, Gobin R. 7.  et al. 2004. Biosynthetic Ca2+/Sr2+ exchange in the photosystem II oxygen-evolving enzyme of Thermosynechococcus elongatus. J. Biol. Chem. 279:22809–19 [Google Scholar]
  8. Bovi D, Narzi D, Guidoni L. 8.  2013. The S2 state of the oxygen-evolving complex of photosystem II explored by QM/MM dynamics: spin surfaces and metastable states suggest a reaction path towards the S3 state. Angew. Chem. Int. Ed. 52:11744–49 [Google Scholar]
  9. Bricker TM, Roose JL, Fagerlund RD, Frankel LK, Eaton-Rye JJ. 9.  2012. The extrinsic proteins of Photosystem II. Biochim. Biophys. Acta 1817:121–42 [Google Scholar]
  10. Britt RD, Campbell KA, Peloquin JM, Gilchrist ML, Aznar CP. 10.  et al. 2004. Recent pulsed EPR studies of the Photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms. Biochim. Biophys. Acta 1655:158–71 [Google Scholar]
  11. Brudvig GW. 11.  2008. Water oxidation chemistry of photosystem II. Philos. Trans. R. Soc. B 363:1211–18 [Google Scholar]
  12. Christen G, Seeliger A, Renger G. 12.  1999. P680 reduction kinetics and redox transition probability of the water oxidizing complex as a function of pH and H/D isotope exchange in spinach thylakoids. Biochemistry 38:6082–92 [Google Scholar]
  13. Cox N, Messinger J. 13.  2013. Reflections on substrate water and dioxygen formation. Biochim. Biophys. Acta 1827:1020–30 [Google Scholar]
  14. Cox N, Pantazis DA, Neese F, Lubitz W. 14.  2013. Biological water oxidation. Acc. Chem. Res. 46:1588–96 [Google Scholar]
  15. Cox N, Rapatskiy L, Su JH, Pantazis DA, Sugiura M. 15.  et al. 2011. Effect of Ca2+/Sr2+ substitution on the electronic structure of the oxygen-evolving complex of photosystem II: a combined multifrequency EPR, 55Mn-ENDOR, and DFT study of the S2 state. J. Am. Chem. Soc. 133:3635–48 [Google Scholar]
  16. Dau H, Grundmeier A, Loja P, Haumann M. 16.  2008. On the structure of the manganese complex of photosystem II: extended-range EXAFS data and specific atomic resolution models for four S-states. Philos. Trans. R. Soc. B 363:1237–44 [Google Scholar]
  17. Dau H, Haumann M. 17.  2008. The manganese complex of photosystem II in its reaction cycle—basic framework and possible realization at the atomic level. Coord. Chem. Rev. 252:273–95 [Google Scholar]
  18. Dau H, Liebisch P, Haumann M. 18.  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. 6:4781–92 [Google Scholar]
  19. Debus RJ. 19.  2008. Protein ligation of the photosynthetic oxygen-evolving center. Coord. Chem. Rev. 252:244–58 [Google Scholar]
  20. Debus RJ, Barry BA, Sithole I, Babcock GT, McIntosh L. 20.  1988. Directed mutagenesis indicates that the donor to P+680in photosystem II is tyrosine-161 of the D1 polypeptide. Biochemistry 27:9071–74 [Google Scholar]
  21. Diner BA, Rappaport F. 21.  2002. Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu. Rev. Plant. Biol. 53:551–80 [Google Scholar]
  22. Enami I, Okumura A, Nagao R, Suzuki T, Iwai M, Shen JR. 22.  2008. Structures and functions of the extrinsic proteins of photosystem II from different species. Photosynth. Res. 98:349–63 [Google Scholar]
  23. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S. 23.  2004. Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–38 [Google Scholar]
  24. Gabdulkhakov A, Guskov A, Broser M, Kern J, Müh F. 24.  et al. 2009. Probing the accessibility of the Mn4Ca cluster in photosystem II: channels calculation, noble gas derivatization, and cocrystallization with DMSO. Structure 17:1223–34 [Google Scholar]
  25. Galstyan A, Robertazzi A, Knapp EW. 25.  2012. Oxygen-evolving Mn cluster in photosystem II: the protonation pattern and oxidation state in the high-resolution crystal structure. J. Am. Chem. Soc. 134:7442–49 [Google Scholar]
  26. Gatt P, Petrie S, Stranger R, Pace RJ. 26.  2012. Rationalizing the 1.9 Å crystal structure of photosystem II—a remarkable Jahn–Teller balancing act induced by a single proton transfer. Angew. Chem. Int. Ed. 51:12025–28 [Google Scholar]
  27. Gatt P, Stranger R, Pace RJ. 27.  2011. Application of computational chemistry to understanding the structure and mechanism of the Mn catalytic site in photosystem II—a review. J. Photochem. Photobiol. B 104:80–93 [Google Scholar]
  28. Glöckner C, Kern J, Broser M, Zouni A, Yachandra V, Yano J. 28.  2013. Structural changes of the oxygen-evolving complex in Photosystem II during the catalytic cycle. J. Biol. Chem. 288:22607–20 [Google Scholar]
  29. Grabolle M, Haumann M, Müller C, Liebisch P, Dau H. 29.  2006. Rapid loss of structural motifs in the manganese complex of oxygenic photosynthesis by X-ray irradiation at 10–300 K. J. Biol. Chem. 281:4580–88 [Google Scholar]
  30. Grundmeier A, Dau H. 30.  2012. Structural models of the manganese complex of photosystem II and mechanistic implications. Biochim. Biophys. Acta 1817:88–105 [Google Scholar]
  31. Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W. 31.  2009. Cyanobacterial photosystem II at 2.9 Å resolution and role of quinones, lipids, channels and chloride. Nat. Struct. Mol. Biol. 16:334–42 [Google Scholar]
  32. Haddy A. 32.  2007. EPR spectroscopy of the manganese cluster of photosystem II. Photosynth. Res. 92:357–68 [Google Scholar]
  33. Haumann M, Müller C, Liebisch P, Iuzzolino L, Dittmer J. 33.  et al. 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 44:1894–908 [Google Scholar]
  34. Hays AMA, Vassiliev IR, Golbeck JH, Debus RJ. 34.  1998. Role of D1-His190 in proton coupled electron transfer reactions in photosystem II: a chemical complementation study. Biochemistry 37:11352–65 [Google Scholar]
  35. Hays AMA, Vassiliev IR, Golbeck JH, Debus RJ. 35.  1999. Role of D1-His190 in the proton-coupled oxidation of tyrosine YZ in manganese-depleted photosystem II. Biochemistry 38:11851–65 [Google Scholar]
  36. Hillier W, Wydrzynski T. 36.  2004. Substrate water interactions within the photosystem II oxygen evolving complex. Phys. Chem. Chem. Phys. 6:4882–89 [Google Scholar]
  37. Hillier W, Wydrzynski T. 37.  2008. 18O-water exchange in photosystem II: substrate binding and intermediates of the water splitting cycle. Coord. Chem. Rev. 252:306–17 [Google Scholar]
  38. Ho FM, Styring S. 38.  2008. Access channels and methanol binding site to the CaMn4 cluster in Photosystem II based on solvent accessibility simulations, with implications for substrate water access. Biochim. Biophys. Acta 1777:140–53 [Google Scholar]
  39. Hoganson CW, Babcock GT. 39.  1997. A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277:1953–56 [Google Scholar]
  40. Ifuku K. 40.  2014. The PsbP and PsbQ family proteins in the photosynthetic machinery of chloroplasts. Plant Physiol. Biochem. 81:108–14 [Google Scholar]
  41. Ishida N, Sugiura M, Rappaport F, Lai TL, Rutherford AW, Boussac A. 41.  2008. Biosynthetic exchange of bromide for chloride and strontium for calcium in the photosystem II oxygen-evolving enzymes. J. Biol. Chem. 283:13330–40 [Google Scholar]
  42. Isobe H, Shoji M, Yamanaka S, Umena Y, Kawakami K. 42.  et al. 2012. Theoretical illumination of water-inserted structures of the CaMn4O5 cluster in the S2 and S3 states of oxygen-evolving complex of photosystem II: full geometry optimizations by B3LYP hybrid density functional. Dalton Trans. 41:13727–40 [Google Scholar]
  43. Joliot P. 43.  2003. Period-four oscillations of the flash-induced oxygen formation in photosynthesis. Photosynth. Res. 76:65–72 [Google Scholar]
  44. Joliot P, Barbieri G, Chabaud R. 44.  1969. Un nouveau modèle des centres photochimiques du système II. Photochem. Photobiol. 10:309–31 [Google Scholar]
  45. Junge W, Haumann M, Ahlbrink R, Mulkidjanian A, Clausen J. 45.  2002. Electrostatics and proton transfer in photosynthetic water oxidation. Philos. Trans. R. Soc. B 357:1407–18 [Google Scholar]
  46. Kamiya N, Shen JR. 46.  2003. Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. PNAS 100:98–103 [Google Scholar]
  47. Kanady JS, Mendoza-Cortes JL, Tsui EY, Nielsen RJ, Goddard WA, Agapie T. 47.  2013. Oxygen atom transfer and oxidative water incorporation in cuboidal Mn3MOn complexes based on synthetic, isotopic labeling, and computational studies. J. Am. Chem. Soc. 135:1073–82 [Google Scholar]
  48. Kanady JS, Tsui EY, Day MW, Agapie T. 48.  2011. A synthetic model of the Mn3Ca subsite of the oxygen-evolving complex in photosystem II. Science 333:733–36 [Google Scholar]
  49. Kanda K, Yamanaka S, Saito T, Umena Y, Kawakami K. 49.  et al. 2011. Labile electronic and spin states of the CaMn4O5 cluster in the PSII system refined to the 1.9 Å X-ray resolution. UB3LYP computational results. Chem. Phys. Lett. 506:98–103 [Google Scholar]
  50. Kawakami K, Iwai M, Ikeuchi M, Kamiya N, Shen JR. 50.  2007. Location of PsbY in oxygen-evolving photosystem II revealed by mutagenesis and X-ray crystallography. FEBS Lett. 581:4983–87 [Google Scholar]
  51. Kawakami K, Umena Y, Kamiya N, Shen JR. 51.  2009. Location of chloride and its possible functions in oxygen-evolving photosystem II revealed by X-ray crystallography. PNAS 106:8567–72 [Google Scholar]
  52. Kawakami K, Umena Y, Kamiya N, Shen JR. 52.  2011. Structure of the catalytic, inorganic core of oxygen-evolving photosystem II at 1.9 Å resolution. J. Photochem. Photobiol. B 104:9–18 [Google Scholar]
  53. Kern J, Alonso-Mori R, Hellmich J, Tran R, Hattne J. 53.  et al. 2012. Room temperature femtosecond X-ray diffraction of photosystem II microcrystals. PNAS 109:9721–26 [Google Scholar]
  54. Kern J, Loll B, Lüneberg C, DiFiore D, Biesiadka J. 54.  et al. 2005. Purification, characterisation and crystallisation of photosystem II from Thermosynechococcus elongatus cultivated in a new type of photobioreactor. Biochim. Biophys. Acta 1706:147–57 [Google Scholar]
  55. Kern J, Tran R, Alonso-Mori R, Koroidov S, Echols N. 55.  et al. 2014. Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy. Nat. Commun. 5:4371 [Google Scholar]
  56. Kok B, Forbush B, McGloin M. 56.  1970. Cooperation of charges in photosynthetic oxygen evolution. I. A linear four step mechanism. Photochem. Photobiol. 11:457–75 [Google Scholar]
  57. Kolling DR, Cox N, Ananyev GM, Pace RJ, Dismukes GC. 57.  2012. What are the oxidation states of manganese required to catalyze photosynthetic water oxidation?. Biophys. J. 103:313–22 [Google Scholar]
  58. Koua FH, Umena Y, Kawakami K, Shen JR. 58.  2013. Structure of Sr-substituted photosystem II at 2.1 Å resolution and its implications in the mechanism of water oxidation. PNAS 110:3889–94 [Google Scholar]
  59. Kuhl H, Kruip J, Seidler A, Krieger-Liszkay A, Bunker M. 59.  et al. 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. 275:20652–59 [Google Scholar]
  60. Kulik LV, Epel B, Lubitz W, Messinger J. 60.  2005. 55Mn pulse ENDOR at 34 GHz of the S0 and S2 states of the oxygen-evolving complex in photosystem II. J. Am. Chem. Soc. 127:2392–93 [Google Scholar]
  61. Kulik LV, Epel B, Lubitz W, Messinger J. 61.  2007. Electronic structure of the Mn4OxCa cluster in the S0 and S2 states of the oxygen-evolving complex of photosystem II based on pulse 55Mn-ENDOR and EPR spectroscopy. J. Am. Chem. Soc. 129:13421–35 [Google Scholar]
  62. Kupitz C, Basu S, Grotjohann I, Fromme R, Zatsepin NA. 62.  et al. 2014. Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature 513:261–65 [Google Scholar]
  63. Kurashige Y, Chan GKL, Yanai T. 63.  2013. Entangled quantum electronic wavefunctions of the Mn4CaO5 cluster in photosystem II. Nat. Chem. 5:660–66 [Google Scholar]
  64. Kusunoki M. 64.  2011. S1-state Mn4Ca complex of Photosystem II exists in equilibrium between the two most-stable isomeric substates: XRD and EXAFS evidence. J. Photochem. Photobiol. B 104:100–10 [Google Scholar]
  65. Lee CI, Lakshmi KV, Brudvig GW. 65.  2007. Probing the functional role of Ca2+ in the oxygen-evolving complex of photosystem II by metal ion inhibition. Biochemistry 46:3211–23 [Google Scholar]
  66. Linke K, Ho FM. 66.  2014. Water in Photosystem II: structural, functional and mechanistic considerations. Biochim. Biophys. Acta 1837:14–32 [Google Scholar]
  67. Lohmiller T, Cox N, Su JH, Messinger J, Lubitz W. 67.  2012. The basic properties of the electronic structure of the oxygen-evolving complex of photosystem II are not perturbed by Ca2+ removal. J. Biol. Chem. 287:24721–33 [Google Scholar]
  68. Lohmiller T, Krewald V, Navarro MP, Retegan M, Rapatskiy L. 68.  et al. 2014. Structure, ligands and substrate coordination of the oxygen-evolving complex of photosystem II in the S2 state: a combined EPR and DFT study. Phys. Chem. Chem. Phys. 16:11877–92 [Google Scholar]
  69. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J. 69.  2005. Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–44 [Google Scholar]
  70. Loll B, Kern J, Zouni A, Saenger W, Biesiadka J, Irrgang KD. 70.  2005. The antenna system of photosystem II from Thermosynechococcus elongatus at 3.2 Å resolution. Photosynth. Res. 86:175–84 [Google Scholar]
  71. Luber S, Rivalta I, Umena Y, Kawakami K, Shen JR. 71.  et al. 2011. S1-state model of the O2-evolving complex of photosystem II. Biochemistry 50:6308–11 [Google Scholar]
  72. Mamedov F, Sayre RT, Styring S. 72.  1998. Involvement of histidine 190 on the D1 protein in electron/proton transfer reactions on the donor side of photosystem II. Biochemistry 37:14245–56 [Google Scholar]
  73. McEvoy JP, Brudvig GW. 73.  2006. Water-splitting chemistry of photosystem II. Chem. Rev. 106:4455–83 [Google Scholar]
  74. McEvoy JP, Gascon JA, Batista VS, Brudvig GW. 74.  2005. The mechanism of photosynthetic water splitting. Photochem. Photobiol. Sci. 4:940–49 [Google Scholar]
  75. Müh F, Renger T, Zouni A. 75.  2008. Crystal structure of cyanobacterial photosystem II at 3.0 Å resolution: a closer look at the antenna system and the small membrane-intrinsic subunits. Plant Physiol. Biochem. 46:238–64 [Google Scholar]
  76. Mukherjee S, Stull JA, Yano J, Stamatatos TC, Pringouri K. 76.  et al. 2012. Synthetic model of the asymmetric [Mn3CaO4] cubane core of the oxygen-evolving complex of photosystem II. PNAS 109:2257–62 [Google Scholar]
  77. Murray JW, Barber J. 77.  2007. Structural characteristics of channels and pathways in photosystem II including the identification of an oxygen channel. J. Struct. Biol. 159:228–37 [Google Scholar]
  78. Murray JW, Maghlaoui K, Kargul J, Ishida N, Lai TL. 78.  et al. 2008. X-ray crystallography identifies two chloride binding sites in the oxygen evolving centre of Photosystem II. Energy Environ. Sci. 1:161–66 [Google Scholar]
  79. Nakamura S, Nagao R, Takahashi R, Noguchi T. 79.  2014. Fourier transform infrared detection of a polarizable proton trapped between photooxidized tyrosine YZ and a coupled histidine in photosystem II: relevance to the proton transfer mechanism of water oxidation. Biochemistry 53:3131–44 [Google Scholar]
  80. Nelson DL, Cox MM. 80.  2008. Lehninger Principles of Biochemistry Basingstoke, UK: Palgrave Macmillan, 5th ed..
  81. Nilsson H, Rappaport F, Boussac A, Messinger J. 81.  2014. Substrate-water exchange in photosystem II is arrested before dioxygen formation. Nat. Commun. 5:4305 [Google Scholar]
  82. Noguchi T. 82.  2008. Fourier transform infrared analysis of the photosynthetic oxygen-evolving center. Coord. Chem. Rev. 252:336–46 [Google Scholar]
  83. Noguchi T. 83.  2008. FTIR detection of water reactions in the oxygen-evolving centre of photosystem II. Philos. Trans. R. Soc. B 363:1189–94 [Google Scholar]
  84. Noguchi T. 84.  2015. Fourier transform infrared difference and time-resolved infrared detection of the electron and proton transfer dynamics in photosynthetic water oxidation. Biochim. Biophys. Acta 184735–45
  85. Pace RJ, Jin L, Stranger R. 85.  2012. What spectroscopy reveals concerning the Mn oxidation levels in the oxygen evolving complex of photosystem II: X-ray to near infra-red. Dalton Trans. 41:11145–60 [Google Scholar]
  86. Pantazis DA, Ames W, Cox N, Lubitz W, Neese F. 86.  2012. Two interconvertible structures that explain the spectroscopic properties of the oxygen-evolving complex of photosystem II in the S2 state. Angew. Chem. Int. Ed. 51:9935–40 [Google Scholar]
  87. Peloquin JM, Campbell KA, Randall DW, Evanchik MA, Pecoraro VL. 87.  et al. 2000. 55Mn ENDOR of the S2-state multiline EPR signal of photosystem II: implications on the structure of the tetranuclear Mn cluster. J. Am. Chem. Soc. 122:10926–42 [Google Scholar]
  88. Pérez Navarro M, Ames WM, Nilsson H, Lohmiller T, Pantazis DA. 88.  et al. 2013. Ammonia binding to the oxygen-evolving complex of photosystem II identifies the solvent-exchangeable oxygen bridge (μ-oxo) of the manganese tetramer. PNAS 110:15561–66 [Google Scholar]
  89. Petrie S, Gatt P, Stranger R, Pace RJ. 89.  2012. Modelling the metal atom positions of the Photosystem II water oxidising complex: a density functional theory appraisal of the 1.9 Å resolution crystal structure. Phys. Chem. Chem. Phys. 14:11333–43 [Google Scholar]
  90. Popelková H, Yocum CF. 90.  2007. Current status of the role of Cl ion in the oxygen-evolving complex. Photosynth. Res. 93:111–21 [Google Scholar]
  91. Pushkar Y, Yano J, Glatzel P, Messinger J, Lewis A. 91.  et al. 2007. Structure and orientation of the Mn4Ca cluster in plant photosystem II membranes studied by polarized range-extended X-ray absorption spectroscopy. J. Biol. Chem. 282:7198–208 [Google Scholar]
  92. Pushkar Y, Yano J, Sauer K, Boussac A, Yachandra VK. 92.  2008. Structural changes in the Mn4Ca cluster and the mechanism of photosynthetic water splitting. PNAS 105:1879–84 [Google Scholar]
  93. Rapatskiy L, Cox N, Savitsky A, Ames WM, Sander J. 93.  et al. 2012. Detection of the water-binding sites of the oxygen-evolving complex of Photosystem II using W-band 17O electron-electron double resonance-detected NMR spectroscopy. J. Am. Chem. Soc. 134:16619–34 [Google Scholar]
  94. Rappaport F, Ishida N, Sugiura M, Boussac A. 94.  2011. Ca2+ determines the entropy changes associated with the formation of transition states during water oxidation by Photosystem II. Energy Environ. Sci. 4:2520–24 [Google Scholar]
  95. Raszewski G, Diner BA, Schlodder E, Renger T. 95.  2008. Spectroscopic properties of reaction center pigments in photosystem II core complexes: revision of the multimer model. Biophys. J. 95:105–19 [Google Scholar]
  96. Renger G, Kühn P. 96.  2007. Reaction pattern and mechanism of light induced oxidative water splitting in photosynthesis. Biochim. Biophys. Acta 1767:458–71 [Google Scholar]
  97. Renger G, Renger T. 97.  2008. Photosystem II: the machinery of photosynthetic water splitting. Photosynth. Res. 98:53–80 [Google Scholar]
  98. Robblee JH, Messinger J, Cinco RM, McFarlane KL, Fernandez C. 98.  et al. 2002. The Mn cluster in the S0 state of the oxygen-evolving complex of photosystem II studied by EXAFS spectroscopy: Are there three di-μ-oxo-bridged Mn2 moieties in the tetranuclear Mn complex?. J. Am. Chem. Soc. 124:7459–71 [Google Scholar]
  99. Robertazzi A, Galstyan A, Knapp EW. 99.  2011. Can oxidation states and the protonation pattern of oxomanganese complexes be recognized from their structures?. CrystEngComm 13:6369–72 [Google Scholar]
  100. Robertazzi A, Galstyan A, Knapp EW. 100.  2014. PSII manganese cluster: protonation of W2, O5, O4 and His337 in the S1 state explored by combined quantum chemical and electrostatic energy computations. Biochim. Biophys. Acta 1837:1316–21 [Google Scholar]
  101. Roose JL, Wegener KM, Pakrasi HB. 101.  2007. The extrinsic proteins of Photosystem II. Photosynth. Res. 92:369–87 [Google Scholar]
  102. Saito K, Ishikita H. 102.  2014. Influence of the Ca2+ ion on the Mn4Ca conformation and the H-bond network arrangement in Photosystem II. Biochim. Biophys. Acta 1837:159–66 [Google Scholar]
  103. Saito K, Shen JR, Ishida T, Ishikita H. 103.  2011. Short hydrogen bond between redox-active tyrosine YZ and D1-His190 in the photosystem II crystal structure. Biochemistry 50:9836–44 [Google Scholar]
  104. Saito T, Yamanaka S, Kanda K, Isobe H, Takano Y. 104.  et al. 2012. Possible mechanisms of water splitting reaction based on proton and electron release pathways revealed for CaMn4O5 cluster of PSII refined to 1.9 Å X-ray resolution. Int. J. Quantum Chem. 112:253–76 [Google Scholar]
  105. Sauer K, Yano J, Yachandra VK. 105.  2008. X-ray spectroscopy of the photosynthetic oxygen-evolving complex. Coord. Chem. Rev. 252:318–35 [Google Scholar]
  106. Schinzel S, Schraut J, Arbuznikov AV, Siegbahn PE, Kaupp M. 106.  2010. Density functional calculations of 55Mn, 14N and 13C electron paramagnetic resonance parameters support an energetically feasible model system for the S2 state of the oxygen-evolving complex of photosystem II. Chem. Eur. J. 16:10424–38 [Google Scholar]
  107. Shen JR. 107.  2014. Structure-function relationships in the Mn4CaO5 water-splitting cluster. The Biophysics of Photosynthesis J Golbeck, A van der Est 321–49 New York: Springer [Google Scholar]
  108. Shen JR, Henmi T, Kamiya N. 108.  2008. Structure and function of photosystem II. Photosynthetic Protein Complexes: A Structural Approach P Fromme 83–106 Weinheim, Ger.: Wiley-Blackwell [Google Scholar]
  109. Shen JR, Ikeuchi M, Inoue Y. 109.  1992. Stoichiometric association of extrinsic cytochrome c550 and 12 kDa protein with a highly purified oxygen-evolving photosystem II core complex from Synechococcus vulcanus. FEBS Lett. 301:145–49 [Google Scholar]
  110. Shen JR, Inoue Y. 110.  1993. Binding and functional properties of two new extrinsic components, cytochrome c550 and a 12 kDa protein, in cyanobacterial photosystem II. Biochemistry 32:1825–32 [Google Scholar]
  111. Shen JR, Kamiya N. 111.  2000. Crystallization and the crystal properties of the oxygen-evolving photosystem II from Synechococcus vulcanus. Biochemistry 39:14739–44 [Google Scholar]
  112. Shen JR, Qian M, Inoue Y, Burnap RL. 112.  1998. Functional characterization of Synechocystis sp. PCC 6803 ΔpsbU and ΔpsbV mutants reveals important roles of cytochrome c-550 in cyanobacterial oxygen evolution. Biochemistry 37:1551–58 [Google Scholar]
  113. Shoji M, Isobe H, Yamanaka S, Umena Y, Kawakami K. 113.  et al. 2013. Theoretical insight into hydrogen-bonding networks and proton wire for the CaMn4O5 cluster of photosystem II. Elongation of Mn–Mn distances with hydrogen bonds. Catal. Sci. Technol. 3:1831–48 [Google Scholar]
  114. Siegbahn PE. 114.  2008. A structure-consistent mechanism for dioxygen formation in photosystem II. Chem. Eur. J. 14:8290–302 [Google Scholar]
  115. Siegbahn PE. 115.  2009. Structures and energetics for O2 formation in photosystem II. Acc. Chem. Res. 42:1871–80 [Google Scholar]
  116. Siegbahn PE. 116.  2011. The effect of backbone constraints: the case of water oxidation by the oxygen evolving complex in photosystem II. ChemPhysChem 12:3274–80 [Google Scholar]
  117. Siegbahn PE. 117.  2013. Water oxidation mechanism in photosystem II, including oxidations, proton release pathways, O–O bond formation and O2 release. Biochim. Biophys. Acta 1827:1003–19 [Google Scholar]
  118. Siegbahn PE. 118.  2014. Water oxidation energy diagrams for photosystem II for different protonation states, and the effect of removing calcium. Phys. Chem. Chem. Phys. 16:11893–900 [Google Scholar]
  119. Styring S, Rutherford AW. 119.  1987. In the oxygen-evolving complex of photosystem II the S0 state is oxidized to the S1 state by D+ (signal IIslow). Biochemistry 26:2401–5 [Google Scholar]
  120. Styring S, Sjöholm J, Mamedov F. 120.  2012. Two tyrosines that changed the world: interfacing the oxidizing power of photochemistry to water splitting in photosystem II. Biochim. Biophys. Acta 1817:76–87 [Google Scholar]
  121. Sugiura M, Inoue Y. 121.  1999. Highly purified thermo-stable oxygen-evolving photosystem II core complex from the thermophilic cyanobacterium Synechococcus elongatus having His-tagged CP43. Plant Cell Physiol. 40:1219–31 [Google Scholar]
  122. Suzuki H, Sugiura M, Noguchi T. 122.  2008. Monitoring water reactions during the S-state cycle of the photosynthetic water-oxidizing center: detection of the DOD bending vibrations by means of Fourier transform infrared spectroscopy. Biochemistry 47:11024–30 [Google Scholar]
  123. Suzuki H, Sugiura M, Noguchi T. 123.  2009. Monitoring proton release during photosynthetic water oxidation in photosystem II by means of isotope-edited infrared spectroscopy. J. Am. Chem. Soc. 131:7849–57 [Google Scholar]
  124. Suzuki H, Taguchi Y, Sugiura M, Boussac A, Noguchi T. 124.  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 45:13454–64 [Google Scholar]
  125. Tommos C, Babcock GT. 125.  2000. Proton and hydrogen currents in photosynthetic water oxidation. Biochim. Biophys. Acta 1458:199–219 [Google Scholar]
  126. Tsui EY, Kanady JS, Agapie T. 126.  2013. Synthetic cluster models of biological and heterogeneous manganese catalysts for O2 evolution. Inorg. Chem. 52:13833–48 [Google Scholar]
  127. Umena Y, Kawakami K, Shen JR, Kamiya N. 127.  2011. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60 [Google Scholar]
  128. Vass I, Styring S. 128.  1991. pH-dependent charge equilibria between tyrosine-D and the S states in photosystem II. Estimation of relative midpoint redox potentials. Biochemistry 30:830–39 [Google Scholar]
  129. Vassiliev S, Zaraiskaya T, Bruce D. 129.  2013. Molecular dynamics simulations reveal highly permeable oxygen exit channels shared with water uptake channels in photosystem II. Biochim. Biophys. Acta 1827:1148–55 [Google Scholar]
  130. Wincencjusz H, van Gorkom HJ, Yocum CF. 130.  1997. The photosynthetic oxygen evolving complex requires chloride for its redox state S2→S3 and S3→S0 transitions but not for S0→S1 or S1→S2 transitions. Biochemistry 36:3663–70 [Google Scholar]
  131. Wydrzynski TJ, Satoh K. 131.  2005. Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase. Dordrecht, Neth: Springer
  132. Yachandra VK, Yano J. 132.  2011. Calcium in the oxygen-evolving complex: structural and mechanistic role determined by X-ray spectroscopy. J. Photochem. Photobiol. B 104:51–59 [Google Scholar]
  133. Yamaguchi K, Isobe H, Yamanaka S, Saito T, Kanda K. 133.  et al. 2013. Full geometry optimizations of the mixed-valence CaMn4O4X(H2O)4 (X=OH or O) cluster in OEC of PS II: degree of symmetry breaking of the labile Mn-X-Mn bond revealed by several hybrid DFT calculations. Int. J. Quantum Chem. 113:525–41 [Google Scholar]
  134. Yamaguchi K, Yamanaka S, Isobe H, Saito T, Kanda K. 134.  et al. 2013. The nature of chemical bonds of the CaMn4O5 cluster in oxygen evolving complex of photosystem II: Jahn-Teller distortion and its suppression by Ca doping in cubane structures. Int. J. Quantum Chem. 113:453–73 [Google Scholar]
  135. Yamanaka S, Isobe H, Kanda K, Saito T, Umena Y. 135.  et al. 2011. Possible mechanisms for the O-O bond formation in oxygen evolution reaction at the CaMn4O5(H2O)4 cluster of PSII refined to 1.9 Å X-ray resolution. Chem. Phys. Lett. 511:138–45 [Google Scholar]
  136. Yamanaka S, Kanda K, Saito T, Umena Y, Kawakami K. 136.  et al. 2012. Electronic and spin structures of the CaMn4O5(H2O)4 cluster in OEC of PSII refined to 1.9 Å X-ray resolution. Adv. Quantum Chem. 64:121–87 [Google Scholar]
  137. Yamanaka S, Saito T, Kanda K, Isobe H, Umena Y. 137.  et al. 2012. Structure and reactivity of the mixed-valence CaMn4O5(H2O)4 and CaMn4O4(OH)(H2O)4 clusters at oxygen evolution complex of photosystem II. Hybrid DFT (UB3LYP and UBHANDHLYP) calculations. Int. J. Quantum Chem. 112:321–43 [Google Scholar]
  138. Yano J, Kern J, Irrgang KD, Latimer MJ, Bergmann U. 138.  et al. 2005. X-ray damage to the Mn4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography. PNAS 102:12047–52 [Google Scholar]
  139. Yano J, Kern J, Sauer K, Latimer MJ, Pushkar Y. 139.  et al. 2006. Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster. Science 314:821–25 [Google Scholar]
  140. Yano J, Pushkar Y, Glatzel P, Lewis A, Sauer K. 140.  et al. 2005. High-resolution Mn EXAFS of the oxygen-evolving complex in photosystem II: structural implications for the Mn4Ca cluster. J. Am. Chem. Soc. 127:14974–75 [Google Scholar]
  141. Yano J, Yachandra VK. 141.  2008. Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster from X-ray spectroscopy. Inorg. Chem. 47:1711–26 [Google Scholar]
  142. Yano J, Yachandra VK. 142.  2014. Mn4Ca cluster in photosynthesis: where and how water is oxidized to dioxygen. Chem. Rev. 114:4175–205 [Google Scholar]
  143. Yeagle GJ, Gilchrist ML, McCarrick RM, Britt RD. 143.  2008. Multifrequency pulsed electron paramagnetic resonance study of the S2 state of the photosystem II manganese cluster. Inorg. Chem. 47:1803–14 [Google Scholar]
  144. Yeagle GJ, Gilchrist ML, Walker LM, Debus RJ, Britt RD. 144.  2008. Multifrequency electron spin-echo envelope modulation studies of nitrogen ligation to the manganese cluster of photosystem II. Philos. Trans. R. Soc. B 363:1157–66 [Google Scholar]
  145. Yocum CF. 145.  2008. The calcium and chloride requirements of the O2 evolving complex. Coord. Chem. Rev. 252:296–305 [Google Scholar]
  146. Zein S, Kulik LV, Yano J, Kern J, Pushkar Y. 146.  et al. 2008. Focusing the view on nature's water-splitting catalyst. Philos. Trans. R. Soc. B 363:1167–77 [Google Scholar]
  147. Zhang C. 147.  2007. Low-barrier hydrogen bond plays key role in active photosystem II—a new model for photosynthetic water oxidation. Biochim. Biophys. Acta 1767:493–99 [Google Scholar]
  148. Zouni A, Jordan R, Schlodder E, Fromme P, Witt HT. 148.  2000. First photosystem II crystals capable of water oxidation. Biochim. Biophys. Acta 1457:103–5 [Google Scholar]
  149. Zouni A, Witt HT, Kern J, Fromme P, Krauß N. 149.  et al. 2001. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–43 [Google Scholar]
/content/journals/10.1146/annurev-arplant-050312-120129
Loading
/content/journals/10.1146/annurev-arplant-050312-120129
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error