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The Biophysics of Photosynthesis pp 299–320Cite as

The Radical Intermediates of Photosystem II

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Part of the book series: Biophysics for the Life Sciences ((BIOPHYS,volume 11))

Abstract

The solar water-splitting protein complex, photosystem II (PSII), catalyzes one of the most energetically demanding reactions in nature by using light energy to drive the catalytic oxidation of water to dioxygen. Light-driven electron and proton-coupled electron transfer (PCET) reactions, which are exquisitely tuned by smart protein matrix effects, are central to this water-splitting chemistry. PSII contains a series of charge-transfer cofactors, such as the special chlorophylls, pheophytin, primary and secondary plastoquinones, tetranuclear manganese-calcium-oxo cluster, and two symmetrically placed redox-active tyrosine residues, YD and YZ, that participate in the charge-transfer reactions. These cofactors are functionally very distinct and the versatility is provided by their distinct local environments in PSII. This chapter focuses on providing the reader with an outline of the primary electron transfer reactions of PSII and a description of the structure and function of the charge-transfer cofactors that participate in the primary electron transfer pathway.

This study is supported by the Photosynthetic Systems Program, Office of Basic Energy Sciences, the United States Department of Energy (DE-FG02-07ER15903).

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References

  1. Blankenship RE. Molecular mechanisms of photosynthesis. Oxford: Blackwell; 2002.

    Google Scholar 

  2. McEvoy JP, Brudvig GW. Water-splitting chemistry of photosystem II. Chem Rev. 2006;106:4455–83.

    Google Scholar 

  3. Nicholls DG, Ferguson SJ. Bioenergetics 3. New York: Academic Press; 2002.

    Google Scholar 

  4. Blankenship RE. Origin and early evolution of photosynthesis. Photosynth Res. 1992;33:91–111.

    Google Scholar 

  5. Debus RJ. The manganese and calcium-ions of photosynthetic oxygen evolution. Biochim Biophys Acta. 1992;1102:269–352.

    Google Scholar 

  6. Tommos C, Babcock GT. Oxygen production in nature: a light-driven metalloradical enzyme process. Acc Chem Res. 1998;31:18–25.

    Google Scholar 

  7. Iverson TM. Evolution and unique bioenergetic mechanisms in oxygenic photosynthesis. Curr Opin Chem Biol. 2006;10:91–100.

    Google Scholar 

  8. Barber J, Anderson JM. Photosystem II: molecular structure and function—introduction. Philos Trans R Soc Lond B Biol Sci. 2002;357:1325–8.

    Google Scholar 

  9. Hansson O, Wydrzynski T. Current perceptions of photosystem-II. Photosynth Res. 1990;23:131–62.

    Google Scholar 

  10. Yachandra VK, Sauer K, Klein MP. Manganese cluster in photosynthesis: where plants oxidize water to dioxygen. Chem Rev. 1996;96:2927–50.

    Google Scholar 

  11. Miller AF, Brudvig GW. A guide to electron-paramagnetic resonance spectroscopy of photosystem II membranes. Biochim Biophys Acta. 1991;1056:1–18.

    Google Scholar 

  12. Schlodder E. Introduction to optical methods in photosynthesis. Photosynth Res. 2009;101:93–104.

    Google Scholar 

  13. Novoderezhkin V, Romero E, Dekker J, van Grondelle R. Multiple charge-separation pathways in photosystem II: modeling of transient absorption kinetics. Chemphyschem. 2011;12:681–8.

    Google Scholar 

  14. van Mieghem F, Brettel K, Hillmann B, Kamlowski A, Rutherford A, Schlodder E. Charge recombination reactions in photosystem II. 1. Yields, recombination pathways, and kinetics of the primary pair. Biochemistry. 1995;34:4798–813.

    Google Scholar 

  15. Hillmann B, Brettel K, Van Mieghem F, Kamlowski A, Rutherford A, Schlodder E. Charge recombination reactions in photosystem-II. 2. Transient absorbency difference spectra and their temperature dependence. Biochemistry. 1995;34:4814–27.

    Google Scholar 

  16. Lewis K, Oglivie J. Probing photosynthetic energy and charge transfer with two dimensional electronic spectroscopy. J Phys Chem Lett. 2012;3:503–10.

    ADS  Google Scholar 

  17. Berthomieu C, Hienerwadel R. Fourier transform infrared (FTIR) spectroscopy. Photosynth Res. 2009;101:157–70.

    Google Scholar 

  18. Sproviero EM, Gascon JA, McEvoy JP, Brudvig GW, Batista VS. Computational studies of the O2-evolving complex of photosystem II and biomimetic oxomanganese complexes. Coord Chem Rev. 2008;252:395–415.

    Google Scholar 

  19. Yano J, Yachandra VK. X-ray absorption spectroscopy. Photosynth Res. 2009;102:241–54.

    Google Scholar 

  20. Lakshmi KV, Brudvig GW. Pulsed electron paramagnetic resonance methods for macromolecular structure determination. Curr Opin Struct Biol. 2001;11:523–31.

    Google Scholar 

  21. Lakshmi KV, Brudvig GW. Electron paramagnetic resonance distance measurements in photosynthetic reaction centers. In: Berliner LJ, Eaton SS, Eaton GR, editors. Biological magnetic resonance: distance measurements in biological systems by EPR. New York: Kluwer Academic/Plenum Publishers; 2000. p. 513–67.

    Google Scholar 

  22. Stehlik D, Mobius K. New EPR methods for investigating photoprocesses with paramagnetic intermediates. Annu Rev Phys Chem. 1997;48:745–84.

    ADS  Google Scholar 

  23. Prisner T, Rohrer M, MacMillan F. Pulsed EPR spectroscopy: biological applications. Annu Rev Phys Chem. 2001;52:279–313.

    ADS  Google Scholar 

  24. Bovet JM, Park EJ, Sharp RR. NMR paramagnetic relaxation enhancements due to manganese in the S0 and S2 states of photosystem II-enriched membrane-fragments and in the detergent-solubilized photosystem II complex. Photosynth Res. 1993;38:347–54.

    Google Scholar 

  25. Chu HA, Hillier W, Law NA, Babcock GT. Vibrational spectroscopy of the oxygenevolving complex and of manganese model compounds. Biochim Biophys Acta. 2001;1503:69–82.

    Google Scholar 

  26. Zouni A, Witt HT, Kern J, Fromme P, Krauss N, Saenger W, Orth P. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 angstrom resolution. Nature. 2001;409:739–43.

    ADS  Google Scholar 

  27. Kamiya N, Shen JR. Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7 angstrom resolution. Proc Natl Acad Sci U S A. 2003;100:98–103.

    ADS  Google Scholar 

  28. Umena Y, Kawakami K, Shen JR, Kamiya N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 angstrom. Nature. 2011;473:55–60.

    ADS  Google Scholar 

  29. Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S. Architecture of the photosynthetic oxygen-evolving center. Science. 2004;303:1831–8.

    ADS  Google Scholar 

  30. Loll B, Kern J, Saenger W, Zouni A, Biesiadka J. Towards complete cofactor arrangement in the 3.0 angstrom resolution structure of photosystem II. Nature. 2005;438:1040–4.

    ADS  Google Scholar 

  31. Diner BA, Rappaport F. Structure, dynamics, and energetics of the primary photochemistry of photosystem II of oxygenic photosynthesis. Annu Rev Plant Biol. 2002;53:551–80.

    Google Scholar 

  32. Rutherford AW, Faller P. Photosystem II: evolutionary perspectives. Philos Trans R Soc Lond B Biol Sci. 2003;358:245–53.

    Google Scholar 

  33. Lubitz W, Lendzian F, Bittl R. Radicals, radical pairs and triplet states in photosynthesis. Acc Chem Res. 2002;35:313–20.

    Google Scholar 

  34. Renger G, Holzwarth AR. Primary electron transfer. In: Wydrzynski TJ, Satoh K, editors. The light-driven water/plastoquinone oxidoreductase. Dordrecht, The Netherlands: Kluwer; 2005. p. 139–75.

    Google Scholar 

  35. Seely GR. Energetics of electron-transfer reactions of chlorophyll and other compounds. Photochem Photobiol. 1978;27:639–54.

    Google Scholar 

  36. Watanabe T, Kobayashi M. Electrochemistry of chlorophylls. In: Scheer H, editor. Chlorophylls. Boca Raton, FL: CRC Press; 1991. p. 287–315.

    Google Scholar 

  37. Moenneloccoz P, Robert B, Lutz M. A resonance Raman characterization of the primary electron-acceptor in photosystem II. Biochemistry. 1989;28:3641–5.

    Google Scholar 

  38. Noguchi T, Tomo T, Inoue Y. Fourier transform infrared study of the cation radical of P680 in the photosystem II reaction center: evidence for charge delocalization on the chlorophyll dimer. Biochemistry. 1998;37:13614–25.

    Google Scholar 

  39. Sarcina M, Breton J, Nabedryk E, Diner BA, Nixon PJ. FTIR studies on the P680 cation and triplet states in WT and mutant PSII reaction centres of Synechocystis 6803. In: Garab G, editor. XIth international congress on photosynthesis—mechanisms and effects. Budapest, Hungary, Vol I–V. 1998;1053–56.

    Google Scholar 

  40. Raszewski G, Saenger W, Renger T. Theory of optical spectra of photosystem II reaction centers: location of the triplet state and the identity of the primary electron donor. Biophys J. 2005;88:986–98.

    Google Scholar 

  41. Diner BA, Schlodder E, Nixon PJ, Coleman WJ, Rappaport F, Lavergne J, Vermaas WFJ, Chisholm DA. Site-directed mutations at D1-His198 and D2-His97 of photosystem II in Synechocystis PCC 6803: sites of primary charge separation and cation and triplet stabilization. Biochemistry. 2001;40:9265–81.

    Google Scholar 

  42. Noguchi T, Inoue Y, Satoh K. FT-IR studies on the triplet-state of P680 in the photosystem II reaction center: triplet equilibrium within a chlorophyll dimer. Biochemistry. 1993;32:7186–95.

    Google Scholar 

  43. Okubo T, Tomo T, Sugiura M, Noguchi T. Perturbation of the structure of P680 and the charge distribution on its radical cation in isolated reaction center complexes of photosystem II as revealed by Fourier transform infrared spectroscopy. Biochemistry. 2007;46:4390–7.

    Google Scholar 

  44. Kamlowski A, Frankemoller L, van der Est A, Stehlik D, Holzwarth L. Evidence for delocalization of the triplet state 3P680 in the D1-D2-Cyt b559 complex of photosystem II. Phys Chem Chem Phys. 1996;100:2045–51.

    Google Scholar 

  45. Zech SG, Kurreck J, Eckert HJ, Renger G, Lubitz W, Bittl R. Pulsed EPR measurement of the distance between P680 + ·and QA – ·in photosystem II. FEBS Lett. 1997;414:454–6.

    Google Scholar 

  46. Takahashi R, Hasegawa K, Noguchi T. Effect of charge distribution over a chlorophyll dimer on the redox potential of P680 in photosystem II as studied by density functional theory calculations. Biochemistry. 2008;47:6289–91.

    Google Scholar 

  47. Mimuro M, Tomo T, Nishimura Y, Yamazaki I, Satoh K. Identification of a photochemically inactive pheophytin molecule in the spinach D1-D2-Cyt b559 complex. Biochim Biophys Acta. 1995;1232:81–8.

    Google Scholar 

  48. Shkuropatov AY, Khatypov RA, Volshchukova TS, Shkuropatova VA, Owens TG, Shuvalov VA. Spectral and photochemical properties of borohydride-treated D1-D2-Cyt b559 complex of photosystem II. FEBS Lett. 1997;420:171–4.

    Google Scholar 

  49. Germano M, Shkuropatov AY, Permentier H, de Wijn R, Hoff AJ, Shuvalov VA, van Gorkom HJ. Pigment organization and their interactions in reaction centers of photosystem II: optical spectroscopy at 6 K of reaction centers with modified pheophytin composition. Biochemistry. 2001;40:11472–82.

    Google Scholar 

  50. Germano M, Shkuropatov AY, Permentier H, Khatypov RA, Shuvalov VA, Hoff AJ, Van Gorkom HJ. Selective replacement of the active and inactive pheophytin in reaction centres of Photosystem II by 131-deoxo-131-hydroxy-pheophytin a and comparison of their 6 K absorption spectra. Photosynth Res. 2000;64:189–98.

    Google Scholar 

  51. Shkuropatov AY, Khatypov RA, Shkuropatova VA, Zvereva MG, Owens TG, Shuvalov VA. Reaction centers of photosystem II with a chemically-modified pigment composition: exchange of pheophytins with 131-deoxo-131-hydroxy-pheophytin a. FEBS Lett. 1999;450:163–7.

    Google Scholar 

  52. Giorgi LB, Nixon PJ, Merry SAP, Joseph DM, Durrant JR, Rivas JD, Barber J, Porter G, Klug DR. Comparison of primary charge separation in the photosystem II reaction center complex isolated from wild-type and D1-E130 mutants of the cyanobacterium Synechocystis PCC 6803. J Biol Chem. 1996;271:2093–101.

    Google Scholar 

  53. Dorlet P, Xiong L, Sayre RT, Un S. High field EPR study of the pheophytin anion radical in wild type and D1-E130 mutants of photosystem II in Chlamydomonas reinhardtii. J Biol Chem. 2001;276:22313–6.

    Google Scholar 

  54. Germano M, Pascal A, Shkuropatov AY, Robert B, Hoff AJ, van Gorkom HJ. Pheophytin-protein interactions in photosystem II studied by resonance Raman spectroscopy of modified reaction centers. Biochemistry. 2002;41:11449–55.

    Google Scholar 

  55. Lancaster CRD, Michel H. Refined crystal structures of reaction centres from Rhodopseudomonas viridis in complexes with the herbicide atrazine and two chiral atrazine derivatives also lead to a new model of the bound carotenoid. J Mol Biol. 1999;286:883–98.

    Google Scholar 

  56. Allen JP, Feher G, Yeates TO, Rees DC, Deisenhofer J, Michel H, Huber R. Structural homology of reaction centers from Rhodopseudomonas sphaeroides and Rhodopseudomonas viridis as determined by X-ray diffraction. Proc Natl Acad Sci U S A. 1986;83:8589–93.

    ADS  Google Scholar 

  57. Feher G, Allen JP, Okamura MY, Rees DC. Structure and function of bacterial photosynthetic reaction centers. Nature. 1989;339:111–6.

    ADS  Google Scholar 

  58. Deisenhofer J, Epp O, Miki K, Huber R, Michel H. Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3 angstrom resolution. Nature. 1985;318:618–24.

    ADS  Google Scholar 

  59. Krauss N, Schubert WD, Klukas O, Fromme P, Witt HT, Saenger W. Photosystem I at 4 angstrom resolution represents the first structural model of a joint photosynthetic reaction centre and core antenna system. Nat Struct Biol. 1996;3:965–73.

    Google Scholar 

  60. Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauss N. Three-dimensional structure of cyanobacterial photosystem I at 2.5 angstrom resolution. Nature. 2001;411:909–17.

    ADS  Google Scholar 

  61. Brettel K, Leibl W. Electron transfer in photosystem I. Biochim Biophys Acta. 2001;1507:100–14.

    Google Scholar 

  62. Ptushenko VV, Cherepanov DA, Krishtalik LI, Semenov AY. Semi-continuum electrostatic calculations of redox potentials in photosystem I. Photosynth Res. 2008;97:55–74.

    Google Scholar 

  63. Srinivasan N, Golbeck JH. Protein-cofactor interactions in bioenergetic complexes: the role of the A1A and A1B phylloquinones in Photosystem I. Biochim Biophys Acta. 2009;1787:1057–88.

    Google Scholar 

  64. Ishikita H, Knapp EW. Oxidation of the non-heme iron complex in photosystem II. Biochemistry. 2005;44:14772–83.

    Google Scholar 

  65. Ishikita H, Knapp EW. Redox potential of quinones in both electron transfer branches of photosystem I. J Biol Chem. 2003;278:52002–11.

    Google Scholar 

  66. Kern J, Renger G. Photosystem II: structure and mechanism of the water:plastoquinone oxidoreductase. Photosynth Res. 2007;94:183–202.

    Google Scholar 

  67. Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W. Cyanobacterial photosystem II at 2.9 angstrom resolution and the role of quinones, lipids, channels and chloride. Nat Struct Mol Biol. 2009;16:334–42.

    Google Scholar 

  68. Deligiannakis Y, Hanley J, Rutherford AW. 1D- and 2D ESEEM study of the semiquinone radical QA – of photosystem II. J Am Chem Soc. 1999;121:7653–64.

    Google Scholar 

  69. Zheng M, Dismukes GC. The conformation of the isoprenyl chain relative to the semiquinone head in the primary electron acceptor QA of higher plant PSII (plastosemiquinone) differs from that in bacterial reaction centers (ubisemiquinone or menasemiquinone) by ca 90 degrees. Biochemistry. 1996;35:8955–63.

    Google Scholar 

  70. Debus RJ, Feher G, Okamura MY. Iron-depleted reaction centers from Rhodopseudomonas sphaeroides r-26.1—characterization and reconstitution with Fe2+, Mn2+, Co2+, Ni2+, Cu2+ and Zn2+. Biochemistry. 1986;25:2276–87.

    Google Scholar 

  71. Chatterjee R, Milikisiyants S, Coates CS, Lakshmi KV. High-resolution two-dimensional 1H and 14N hyperfine sublevel correlation spectroscopy of the primary quinone of photosystem II. Biochemistry. 2011;50:491–501.

    Google Scholar 

  72. Moser CC, Page CC, Dutton PL. Tunneling in PSII. Photochem Photobiol Sci. 2005;4:933–9.

    Google Scholar 

  73. de Wijn R, van Gorkom HJ. Kinetics of electron transfer from QA to QB in photosystem II. Biochemistry. 2001;40:11912–22.

    Google Scholar 

  74. Vrettos JS, Limburg J, Brudvig GW. Mechanism of photosynthetic water oxidation: combining biophysical studies of photosystem II with inorganic model chemistry. Biochim Biophys Acta. 2001;1503:229–45.

    Google Scholar 

  75. Hoganson CW, Babcock GT. A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science. 1997;277:1953–6.

    Google Scholar 

  76. Styring S, Rutherford AW. In the oxygen-evolving complex of photosystem II the S0 state is oxidized to the S1 state by D+ signal-II slow. Biochemistry. 1987;26:2401–5.

    Google Scholar 

  77. Tracewell CA, Brudvig GW. Two redox-active β carotene molecules in Photosystem II. Biochemistry. 2003;42:9127–36.

    Google Scholar 

  78. Tommos C, Babcock GT. Proton and hydrogen currents in photosynthetic water oxidation. Biochim Biophys Acta. 2000;1458:199–219.

    Google Scholar 

  79. Ahlbrink R, Haumann M, Cherepanov D, Bogershausen O, Mulkidjanian A, Junge W. Function of tyrosine-Z in water oxidation by photosystem II: electrostatical promotor instead of hydrogen abstractor. Biochemistry. 1998;37:1131–42.

    Google Scholar 

  80. Diner BA, Force DA, Randall DW, Britt RD. Hydrogen bonding, solvent exchange, and coupled proton and electron transfer in the oxidation and reduction of redox-active tyrosine YZ in Mn-depleted core complexes of Photosystem II. Biochemistry. 1998;37:17931–43.

    Google Scholar 

  81. Mamedov F, Sayre RT, Styring S. Involvement of histidine 190 on the D1 protein in electron/proton transfer reactions on the donor side of photosystem II. Biochemistry. 1998;37:14245–56.

    Google Scholar 

  82. Hays AMA, Vassiliev IR, Golbeck JH, Debus RJ. Role of D1-His190 in proton-coupled electron transfer reactions in photosystem II: a chemical complementation study. Biochemistry. 1998;37:11352–65.

    Google Scholar 

  83. Kuhne H, Brudvig GW. Proton-coupled electron transfer involving Tyrosine-Z in photosystem II. J Phys Chem B. 2002;106:8189–96.

    Google Scholar 

  84. Nugent JHA, Rich AM, Evans MCW. Photosynthetic water oxidation: towards a mechanism. Biochim Biophys Acta. 2001;1503:138–46.

    Google Scholar 

  85. Haumann M, Bogershausen O, Cherepanov D, Ahlbrink R, Junge W. 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. 1997;51:193–208.

    Google Scholar 

  86. Christen G, Seeliger A, Renger G. 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. 1999;38:6082–92.

    Google Scholar 

  87. Haumann M, Mulkidjanian A, Junge W. Tyrosine-Z in oxygen-evolving photosystem II: a hydrogen-bonded tyrosinate. Biochemistry. 1999;38:1258–67.

    Google Scholar 

  88. Berthomieu C, Hienerwadel R, Boussac A, Breton J, Diner BA. Hydrogen bonding of redox-active tyrosine Z of photosystem II probed by FTIR difference spectroscopy. Biochemistry. 1998;37:10547–54.

    Google Scholar 

  89. Jeans C, Schilstra MJ, Ray N, Husain S, Minagawa J, Nugent JHA, Klug DR. Replacement of tyrosine D with phenylalanine affects the normal proton transfer pathways for the reduction of P680 + in oxygen-evolving Photosystem II particles from Chlamydomonas. Biochemistry. 2002;41:15754–61.

    Google Scholar 

  90. Noguchi T, Inoue Y, Tang XS. Structural coupling between the oxygen-evolving Mn cluster and a tyrosine residue in photosystem II as revealed by Fourier transform infrared spectroscopy. Biochemistry. 1997;36:14705–11.

    Google Scholar 

  91. Berthomieu C, Hienerwadel R. Vibrational spectroscopy to study the properties of redoxactive tyrosines in photosystem II and other proteins. Biochim Biophys Acta. 2005;1707:51–66.

    Google Scholar 

  92. Zhang CX, Boussac A, Rutherford AW. Low-temperature electron transfer in photosystem II: a tyrosyl radical and semiquinone charge pair. Biochemistry. 2004;43:13787–95.

    Google Scholar 

  93. Zhang CX, Styring S. Formation of split electron paramagnetic resonance signals in photosystem II suggests that Tyrosine-Z can be photooxidized at 5 K in the S0 and S1 states of the oxygen-evolving complex. Biochemistry. 2003;42:8066–76.

    Google Scholar 

  94. Faller P, Goussias C, Rutherford AW, Un S. Resolving intermediates in biological proton-coupled electron transfer: a tyrosyl radical prior to proton movement. Proc Natl Acad Sci U S A. 2003;100:8732–5.

    ADS  Google Scholar 

  95. Faller P, Rutherford AW, Debus RJ. Tyrosine D oxidation at cryogenic temperature in photosystem II. Biochemistry. 2002;41:12914–20.

    Google Scholar 

  96. Babcock GT, Barry BA, Debus RJ, Hoganson CW, Atamian M, McIntosh L, Sithole I, Yocum CF. Water oxidation in photosystem II from radical chemistry to multi-electron chemistry. Biochemistry. 1989;28:9557–65.

    Google Scholar 

  97. Tang XS, Chisholm DA, Dismukes GC, Brudvig GW, Diner BA. Spectroscopic evidence from site-directed mutants of Synechocystis PCC 6803 in favor of a close interaction between histidine-189 and redox-active tyrosine-160 both of polypeptide D2 of the photosystem II reaction center. Biochemistry. 1993;32:13742–8.

    Google Scholar 

  98. Junge W, Haumann M, Ahlbrink R, Mulkidjanian A, Clausen J. Electrostatics and proton transfer in photosynthetic water oxidation. Philos Trans R Soc Lond B Biol Sci. 2002;357:1407–17.

    Google Scholar 

  99. Rappaport F, Lavergne J. Charge recombination and proton transfer in manganesedepleted photosystem II. Biochemistry. 1997;36:15294–302.

    Google Scholar 

  100. Rappaport F, Blancharddesce M, Lavergne J. Kinetics of electron transfer and electrochromic change during the redox transitions of the photosynthetic oxygenevolving complex. Biochim Biophys Acta. 1994;1184:178–92.

    Google Scholar 

  101. Eckert HJ, Renger G. Temperature-dependence of P680 + reduction in O2-evolving PSII membrane fragments at different redox states Si of the water oxidizing system. FEBS Lett. 1988;236:425–31.

    Google Scholar 

  102. Renger G. Coupling of electron and proton transfer in oxidative water cleavage in photosynthesis. Biochim Biophys Acta. 2004;1655:195–204.

    Google Scholar 

  103. Kok B, Forbush B, McGloin M. Cooperation of charges in photosynthetic O2 evolution 1. A linear 4-step mechanism. Photochem Photobiol. 1970;11:457.

    Google Scholar 

  104. Peloquin JM, Britt RD. EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster. Biochim Biophys Acta. 2001;1503:96–111.

    Google Scholar 

  105. Messinger J, Nugent JHA, Evans MCW. Detection of an EPR multiline signal for the S0 state in photosystem II. Biochemistry. 1997;36:11055–60.

    Google Scholar 

  106. Ahrling KA, Peterson S, Styring S. The S0 state EPR signal from the Mn cluster in photosystem II arises from an isolated S = 1/2 ground state. Biochemistry. 1998;37:8115–20.

    Google Scholar 

  107. Kulik LV, Epel B, Lubitz W, Messinger J. 55Mn pulse ENDOR at 34 GHz of the S0 and S2 states of the oxygen-evolving complex in photosystem II. J Am Chem Soc. 2005;127:2392–3.

    Google Scholar 

  108. Debus RJ. Protein ligation of the photosynthetic oxygen-evolving center. Coord Chem Rev. 2008;252:244–58.

    Google Scholar 

  109. Yano J, Pushkar Y, Glatzel P, Lewis A, Sauer K, Messinger J, Bergmann U, Yachandra V. High-resolution Mn EXAFS of the oxygen-evolving complex in photosystem II: structural implications for the Mn4Ca cluster. J Am Chem Soc. 2005;127:14974–5.

    Google Scholar 

  110. Sproviero EM, Gascon JA, McEvoy JP, Brudvig GW, Batista VS. Quantum mechanics/molecular mechanics structural models of the oxygen-evolving complex of photosystem II. Curr Opin Struct Biol. 2007;17:173–80.

    Google Scholar 

  111. Yano J, Kern J, Sauer K, Latimer MJ, Pushkar Y, Biesiadka J, Loll B, Saenger W, Messinger J, Zouni A, Yachandra VK. Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster. Science. 2006;314:821–5.

    ADS  Google Scholar 

  112. Luber S, Rivalta I, Umena Y, Kawakami K, Shen J-R, Kamiya N, Brudvig GW, Batista VS. S1-state model of the O2-evolving complex of photosystem II. Biochemistry. 2011;50:6308–11.

    Google Scholar 

  113. Pushkar YL, Yano J, Sauer K, Boussac A, Yachandra VK. Structural changes in the Mn4Ca cluster and the mechanism of photosynthetic water splitting. Proc Natl Acad Sci U S A. 2008;105:1879–84.

    ADS  Google Scholar 

  114. Chu HA, Hillier W, Debus RJ. 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. 2004;43:3152–66.

    Google Scholar 

  115. Noguchi T, Ono T, Inoue Y. Detection of structural-changes upon S1-to-S2 transition in the oxygen-evolving manganese cluster in photosystem II by light-induced Fourier transform infrared difference spectroscopy. Biochemistry. 1992;31:5953–6.

    Google Scholar 

  116. Noguchi T, Sugiura M. Flash-induced Fourier transform infrared detection of the structural changes during the S-state cycle of the oxygen-evolving complex in photosystem II. Biochemistry. 2001;40:1497–502.

    Google Scholar 

  117. Yamada H, Mino H, Itoh S. Protons bound to the Mn cluster in photosystem II oxygenevolving complex detected by proton matrix ENDOR. Biochim Biophys Acta. 2007;1767:197–203.

    Google Scholar 

  118. Britt RD, Campbell KA, Peloquin JM, Gilchrist ML, Aznar CP, Dicus MM, Robblee J, Messinger J. Recent pulsed EPR studies of the Photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms. Biochim Biophys Acta. 2004;1655:158–71.

    Google Scholar 

  119. Su JH, Messinger J. Is Mn-bound substrate water protonated in the S2 state of photosystem II? Appl Magn Reson. 2010;37:123–36.

    Google Scholar 

  120. Sproviero EM, Gascon JA, McEvoy JP, Brudvig GW, Batista VS. Quantum mechanics/molecular mechanics study of the catalytic cycle of water splitting in photosystem II. J Am Chem Soc. 2008;130:3428–42.

    Google Scholar 

  121. Siegbahn PEM. Quantum chemical studies of manganese centers in biology. Curr Opin Chem Biol. 2002;6:227–35.

    Google Scholar 

  122. Siegbahn PEM. Structures and energetics for O2 formation in photosystem II. Acc Chem Res. 2009;42:1871–80.

    Google Scholar 

  123. Chatterjee R, Milikisiyants S, Lakshmi KV. Two-dimensional 14N HYSCORE spectroscopy of the coordination geometry of ligands in dimanganese di-μ-oxo mimics of the oxygen-evolving complex of photosystem II. Phys Chem Chem Phys. 2012;14:7090–7.

    Google Scholar 

  124. Milikisiyants S, Chatterjee R, Coates CS, Koua FHM, Shen JR, Lakshmi KV. The structure and activation of substrate water molecules in the S2 state of photosystem II studied by hyperfine sublevel correlation spectroscopy. Energy Environ Sci. 2012;5:7747–56.

    Google Scholar 

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Authors and Affiliations

  1. Department of Chemistry and Chemical Biology, Rensselaer Polytechnic Institute, 110 8th Street, 12180, Troy, NY, USA

    K. V. Lakshmi, Christopher S. Coates & Ruchira Chatterjee

  2. The Baruch ’60 Center for Biochemical Solar Energy Research, Rensselaer Polytechnic Institute, 110 8th Street, 12180, Troy, NY, USA

    K. V. Lakshmi, Christopher S. Coates, Stuart Smith & Ruchira Chatterjee

  3. Department of Physics, Rensselaer Polytechnic Institute, 12180, Troy, NY, USA

    Stuart Smith

  4. Physical Biosciences Division, Lawrence Berkeley National Laboratory, 94720, Berkeley, CA, USA

    Ruchira Chatterjee

Authors
  1. K. V. Lakshmi
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  2. Christopher S. Coates
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  3. Stuart Smith
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  4. Ruchira Chatterjee
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Correspondence to K. V. Lakshmi .

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Editors and Affiliations

  1. Dept of Biochemistry & Molecular Biology, Department of Chemistry, The Pennsylvania State University, University Park, Pennsylvania, USA

    John Golbeck

  2. Dept of Chemistry, Brock University, St. Catharines, Ontario, Canada

    Art van der Est

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Lakshmi, K.V., Coates, C.S., Smith, S., Chatterjee, R. (2014). The Radical Intermediates of Photosystem II. In: Golbeck, J., van der Est, A. (eds) The Biophysics of Photosynthesis. Biophysics for the Life Sciences, vol 11. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1148-6_10

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