1932

Abstract

The structure and mechanism of the water-oxidation chemistry that occurs in photosystem II have been subjects of great interest. The advent of X-ray free electron lasers allowed the determination of structures of the stable intermediate states and of steps in the transitions between these intermediate states, bringing a new perspective to this field. The room-temperature structures collected as the photosynthetic water oxidation reaction proceeds in real time have provided important novel insights into the structural changes and the mechanism of the water oxidation reaction. The time-resolved measurements have also given us a view of how this reaction—which involves multielectron, multiproton processes—is facilitated by the interaction of the ligands and the protein residues in the oxygen-evolving complex. These structures have also provided a picture of the dynamics occurring in the channels within photosystem II that are involved in the transport of the substrate water to the catalytic center and protons to the bulk.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-071723-102519
2024-07-16
2025-02-11
Loading full text...

Full text loading...

/deliver/fulltext/biophys/53/1/annurev-biophys-071723-102519.html?itemId=/content/journals/10.1146/annurev-biophys-071723-102519&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Åhrling KA, Peterson S, Styring S. 1997.. An oscillating manganese electron paramagnetic resonance signal from the S0 state of the oxygen evolving complex in photosystem II. . Biochemistry 36::1314852
    [Crossref] [Google Scholar]
  2. 2.
    Åhrling KA, Peterson S, Styring S. 1998.. The S0 state EPR signal from the Mn cluster arises from an isolated ground state. . In Photosynthesis: Mechanisms and Effects, ed. G Garab , pp. 129194. Dordrecht, Neth:.: Kluwer Acad. Publ.
    [Google Scholar]
  3. 3.
    Allgöwer F, Gamiz-Hernandez AP, Rutherford AW, Kaila VRI. 2022.. Molecular principles of redox-coupled protonation dynamics in photosystem II. . J. Am. Chem. Soc. 144::717180
    [Crossref] [Google Scholar]
  4. 4.
    Ayala I, Kim S, Barry BA. 1999.. A difference Fourier transform infrared study of tyrosyl radical Z center dot decay in photosystem II. . Biophys. J. 77::213744
    [Crossref] [Google Scholar]
  5. 5.
    Bao H, Burnap RL. 2015.. Structural rearrangements preceding dioxygen formation by the water oxidation complex of photosystem II. . PNAS 112::613947
    [Crossref] [Google Scholar]
  6. 6.
    Bhowmick A, Hussein R, Bogacz I, Simon PS, Ibrahim M, et al. 2023.. Structural evidence for intermediates during O2 formation in photosystem II. . Nature 617::62936
    [Crossref] [Google Scholar]
  7. 7.
    Blankenship RE. 2010.. Early evolution of photosynthesis. . Plant Physiol. 154::43438
    [Crossref] [Google Scholar]
  8. 8.
    Boussac A, Kuhl H, Un S, Rögner M, Rutherford AW. 1998.. Effect of near-infrared light on the S2-state of the manganese complex of photosystem II from Synechococcus elongatus. . Biochemistry 37::89959000
    [Crossref] [Google Scholar]
  9. 9.
    Boussac A, Rutherford AW. 1988.. Nature of the inhibition of the oxygen-evolving enzyme of photosystem II induced by NaCl washing and reversed by the addition of Ca2+ or Sr2+. . Biochemistry 27::347683
    [Crossref] [Google Scholar]
  10. 10.
    Boussac A, Rutherford AW, Sugiura M. 2015.. Electron transfer pathways from the S2-states to the S3-states either after a Ca2+/Sr2+ or a Cl/I exchange in photosystem II from Thermosynechococcus elongatus. . Biochim. Biophys. Acta Bioenerg. 1847::57686
    [Crossref] [Google Scholar]
  11. 11.
    Boussac A, Sugiura M, Sellés J. 2022.. Probing the proton release by photosystem II in the S1 to S2 high-spin transition. . Biochim. Biophys. Acta Bioenerg. 1863::148546
    [Crossref] [Google Scholar]
  12. 12.
    Boussac A, Ugur I, Marion A, Sugiura M, Kaila VRI, Rutherford AW. 2018.. The low spin–high spin equilibrium in the S2-state of the water oxidizing enzyme. . Biochim. Biophys. Acta Bioenerg. 1859::34256
    [Crossref] [Google Scholar]
  13. 13.
    Boussac A, Un S, Horner O, Rutherford AW. 1998.. High-spin states (S ≥ 5/2) of the photosystem II manganese complex. . Biochemistry 37::40017
    [Crossref] [Google Scholar]
  14. 14.
    Boussac A, Zimmermann J-L, Rutherford AW. 1990.. Factors influencing the formation of modified S2 EPR signal and the S3 EPR signal in Ca2+-depleted photosystem II. . FEBS Lett. 227::6974
    [Crossref] [Google Scholar]
  15. 15.
    Brändén G, Neutze R. 2021.. Advances and challenges in time-resolved macromolecular crystallography. . Science 373::eaba0954
    [Crossref] [Google Scholar]
  16. 16.
    Bricker TM, Mummadisetti MP, Frankel LK. 2015.. Recent advances in the use of mass spectrometry to examine structure/function relationships in photosystem II. . J. Photochem. Photobiol. B 152::22746
    [Crossref] [Google Scholar]
  17. 17.
    Casey JL, Sauer K. 1984.. EPR detection of a cryogenically photogenerated intermediate in photosynthetic oxygen evolution. . Biochim. Biophys. Acta Bioenerg. 767::2128
    [Crossref] [Google Scholar]
  18. 18.
    Chapman HN, Fromme P, Barty A, White TA, Kirian RA, et al. 2011.. Femtosecond X-ray protein nanocrystallography. . Nature 470::7377
    [Crossref] [Google Scholar]
  19. 19.
    Chatterjee R, Han G, Kern J, Gul S, Fuller FD, et al. 2016.. Structural changes correlated with magnetic spin state isomorphism in the S2 state of the Mn4CaO5 cluster in the oxygen-evolving complex of photosystem II. . Chem. Sci. 7::523648
    [Crossref] [Google Scholar]
  20. 20.
    Chatterjee R, Lassalle L, Gul S, Fuller FD, Young ID, et al. 2019.. Structural isomers of the S2 state in photosystem II: Do they exist at room temperature and are they important for function?. Physiol. Plant. 166::6072
    [Crossref] [Google Scholar]
  21. 21.
    Chrysina M, Heyno E, Kutin Y, Reus M, Nilsson H, et al. 2019.. Five-coordinate MnIV intermediate in the activation of nature's water splitting cofactor. . PNAS 116::1684146
    [Crossref] [Google Scholar]
  22. 22.
    Chu HA, Nguyen AP, Debus RJ. 1993.. Residues of the D1 polypeptide that influence the assembly or stability of the manganese cluster or the binding of calcium in photosystem II. . Biophys. J. 64::A216
    [Google Scholar]
  23. 23.
    Cinco RM, Holman KLM, Robblee JH, Yano J, Pizarro SA, et al. 2002.. Calcium EXAFS establishes the Mn-Ca cluster in the oxygen-evolving complex of photosystem II. . Biochemistry 41::1292833
    [Crossref] [Google Scholar]
  24. 24.
    Cinco RM, Robblee JH, Messinger J, Fernandez C, Holman KLM, et al. 2004.. Orientation of calcium in the Mn4Ca cluster of the oxygen-evolving complex determined using polarized strontium EXAFS of photosystem II membranes. . Biochemistry 43::1327182
    [Crossref] [Google Scholar]
  25. 25.
    Cinco RM, Robblee JH, Rompel A, Fernandez C, Yachandra VK, et al. 1998.. Strontium EXAFS reveals the proximity of calcium to the manganese cluster of oxygen-evolving photosystem II. . J. Phys. Chem. B 102::824856
    [Crossref] [Google Scholar]
  26. 26.
    Corry TA, O'Malley PJ. 2019.. Proton isomers rationalize the high- and low-spin forms of the S2 state intermediate in the water-oxidizing reaction of photosystem II. . J. Phys. Chem. Lett. 10::522630
    [Crossref] [Google Scholar]
  27. 27.
    Corry TA, O'Malley PJ. 2020.. Molecular identification of a high-spin deprotonated intermediate during the S2 to S3 transition of nature's water-oxidizing complex. . J. Am. Chem. Soc. 142::1024043
    [Crossref] [Google Scholar]
  28. 28.
    Cox N, Messinger J. 2013.. Reflections on substrate water and dioxygen formation. . Biochim. Biophys. Acta Bioenerg. 1827::102030
    [Crossref] [Google Scholar]
  29. 29.
    Cox N, Pantazis DA, Neese F, Lubitz W. 2013.. Biological water oxidation. . Acc. Chem. Res. 46::158896
    [Crossref] [Google Scholar]
  30. 30.
    Cox N, Retegan M, Neese F, Pantazis DA, Boussac A, Lubitz W. 2014.. Electronic structure of the oxygen-evolving complex in photosystem II prior to O–O bond formation. . Science 345::8048
    [Crossref] [Google Scholar]
  31. 31.
    Dau H, Haumann M. 2007.. Eight steps preceding O–O bond formation in oxygenic photosynthesis—a basic reaction cycle of the photosystem II manganese complex. . Biochim. Biophys. Acta Bioenerg. 1767::47283
    [Crossref] [Google Scholar]
  32. 32.
    Dau H, Haumann M. 2008.. The manganese complex of photosystem II in its reaction cycle—basic framework and possible realization at the atomic level. . Coord. Chem. Rev. 252::27395
    [Crossref] [Google Scholar]
  33. 33.
    Dau H, Liebisch P, Haumann M. 2004.. The structure of the manganese complex of photosystem II in its dark-stable S1-state—EXAFS results in relation to recent crystallographic data. . Phys. Chem. Chem. Phys. 6::478192
    [Crossref] [Google Scholar]
  34. 34.
    Dau H, Liebisch P, Haumann M. 2005.. The manganese complex of oxygenic photosynthesis: conversion of five-coordinated MnIII to six-coordinated MnIV in the S2-S3 transition is implied by XANES simulations. . Phys. Scr. 2005::84446
    [Crossref] [Google Scholar]
  35. 35.
    de Lichtenberg C, Messinger J. 2020.. Substrate water exchange in the S2 state of photosystem II is dependent on the conformation of the Mn4Ca cluster. . Phys. Chem. Chem. Phys. 22::12894908
    [Crossref] [Google Scholar]
  36. 36.
    de Wijn R, van Gorkom HJ. 2001.. Kinetics of electron transfer from QA to QB in photosystem II. . Biochemistry 40::1191222
    [Crossref] [Google Scholar]
  37. 37.
    Deisenhofer J, Epp O, Miki K, Huber R, Michel H. 1985.. Structure of the protein subunits in the photosynthetic reaction center of Rhodopseudomonas viridis at 3 Å resolution. . Nature 318::61824
    [Crossref] [Google Scholar]
  38. 38.
    Dexheimer SL, Klein MP. 1992.. Detection of a paramagnetic intermediate in the S1 state of the photosynthetic oxygen-evolving complex. . J. Am. Chem. Soc. 114::282126
    [Crossref] [Google Scholar]
  39. 39.
    Dismukes GC, Ferris K, Watnick P. 1982.. EPR spectroscopic evidence for a tetranuclear manganese cluster as the site for photosynthetic oxygen evolution. . Photobiochem. Photobiophys. 3::24356
    [Google Scholar]
  40. 40.
    Dismukes GC, Siderer Y. 1980.. EPR spectroscopic observations of a manganese center associated with water oxidation in spinach chloroplasts. . FEBS Lett. 121::7880
    [Crossref] [Google Scholar]
  41. 41.
    Dismukes GC, Siderer Y. 1981.. Intermediates of a polynuclear manganese cluster involved in photosynthetic oxidation of water. . PNAS 78::27478
    [Crossref] [Google Scholar]
  42. 42.
    Doyle MD, Bhowmick A, Wych DC, Lassalle L, Simon PS, et al. 2023.. Water networks in photosystem II using crystalline molecular dynamics simulations and room-temperature XFEL serial crystallography. . J. Am. Chem. Soc. 145:(27):1462135
    [Crossref] [Google Scholar]
  43. 43.
    Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S. 2004.. Architecture of the photosynthetic oxygen-evolving center. . Science 303::183138
    [Crossref] [Google Scholar]
  44. 44.
    Frankel LK, Sallans L, Bellamy H, Goettert JS, Limbach PA, Bricker TM. 2013.. Radiolytic mapping of solvent-contact surfaces in photosystem II of higher plants: experimental identification of putative water channels within the photosystem. . J. Biol. Chem. 288::2356572
    [Crossref] [Google Scholar]
  45. 45.
    Gabdulkhakov A, Guskov A, Broser M, Kern J, Muh F, et al. 2009.. Probing the accessibility of the Mn4Ca cluster in photosystem II: channels calculation, noble gas derivatization, and cocrystallization with DMSO. . Structure 17::122334
    [Crossref] [Google Scholar]
  46. 46.
    Geijer P, Peterson S, Åhrling KA, Deák Z, Styring S. 2001.. Comparative studies of the S0 and S2 multiline electron paramagnetic resonance signals from the manganese cluster in photosystem II. . Biochim. Biophys. Acta Bioenerg. 1503::8395
    [Crossref] [Google Scholar]
  47. 47.
    George GN, Prince RC, Cramer SP. 1989.. The manganese site of the photosynthetic water-splitting enzyme. . Science 243::78991
    [Crossref] [Google Scholar]
  48. 48.
    Glatzel P, Bergmann U, Yano J, Visser H, Robblee JH, et al. 2004.. The electronic structure of Mn in oxides, coordination complexes, and the oxygen-evolving complex of photosystem II studied by resonant inelastic X-ray scattering. . J. Am. Chem. Soc. 126::994659
    [Crossref] [Google Scholar]
  49. 49.
    Glatzel P, Schroeder H, Pushkar Y, Boron T III, Mukherjee S, et al. 2013.. Electronic structural changes of Mn in the oxygen-evolving complex of photosystem II during the catalytic cycle. . Inorg. Chem. 52::564244
    [Crossref] [Google Scholar]
  50. 50.
    Greife P, Schönborn M, Capone M, Assunção R, Narzi D, et al. 2023.. The electron–proton bottleneck of photosynthetic oxygen evolution. . Nature 617::62328
    [Crossref] [Google Scholar]
  51. 51.
    Guiles RD, Yachandra VK, McDermott AE, Cole JL, Dexheimer SL, et al. 1990.. The S0 state of photosystem II induced by hydroxylamine: differences between the structure of the manganese complex in the S0 and S1 states determined by X-ray absorption spectroscopy. . Biochemistry 29::48696
    [Crossref] [Google Scholar]
  52. 52.
    Guiles RD, Zimmermann J-L, McDermott AE, Yachandra VK, Cole JL, et al. 1990.. The S3 state of photosystem II: differences between the structure of the manganese complex in the S2 and S3 states determined by X-ray absorption spectroscopy. . Biochemistry 29::47185
    [Crossref] [Google Scholar]
  53. 53.
    Guo Y, Messinger J, Kloo L, Sun L. 2023.. Alternative mechanism for O2 formation in natural photosynthesis via nucleophilic oxo-oxo coupling. . J. Am. Chem. Soc. 145::412941
    [Crossref] [Google Scholar]
  54. 54.
    Gupta R, Taguchi T, Lassalle-Kaiser B, Bominaar EL, Yano J, et al. 2015.. High-spin Mn-oxo complexes and their relevance to the oxygen-evolving complex within photosystem II. . PNAS 112::531924
    [Crossref] [Google Scholar]
  55. 55.
    Guskov A, Kern J, Gabdulkhakov A, Broser M, Zouni A, Saenger W. 2009.. Cyanobacterial photosystem II at 2.9-Å resolution and the role of quinones, lipids, channels and chloride. . Nat. Struct. Mol. Biol. 16::33442
    [Crossref] [Google Scholar]
  56. 56.
    Haddy A. 2007.. EPR spectroscopy of the manganese cluster of photosystem II. . Photosynth. Res. 92::35768
    [Crossref] [Google Scholar]
  57. 57.
    Haumann M, Liebisch P, Muller C, Barra M, Grabolle M, Dau H. 2005.. Photosynthetic O2 formation tracked by time-resolved X-ray experiments. . Science 310::101921
    [Crossref] [Google Scholar]
  58. 58.
    Haumann M, Muller C, Liebisch P, Iuzzolino L, Dittmer J, 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, S4 → S0) characterized by X-ray absorption spectroscopy at 20 K and room temperature. . Biochemistry 44::1894908
    [Crossref] [Google Scholar]
  59. 59.
    Havelius KGV, Sjoholm J, Ho FM, Mamedov F, Styring S. 2010.. Metalloradical EPR signals from the YZ· S-state intermediates in photosystem II. . Appl. Magn. Reson. 37::15176
    [Crossref] [Google Scholar]
  60. 60.
    Hillier W, Wydrzynski T. 2008.. 18O-water exchange in photosystem II: substrate binding and intermediates of the water splitting cycle. . Coord. Chem. Rev. 252::30617
    [Crossref] [Google Scholar]
  61. 61.
    Ho FM, Styring S. 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 Bioenerg. 1777::14053
    [Crossref] [Google Scholar]
  62. 62.
    Hussein R, Ibrahim M, Bhowmick A, Simon PS, Bogacz I, et al. 2023.. Evolutionary diversity of proton and water channels on the oxidizing side of photosystem II and their relevance to function. . Photosynth. Res. 158::91107
    [Crossref] [Google Scholar]
  63. 63.
    Hussein R, Ibrahim M, Bhowmick A, Simon PS, Chatterjee R, et al. 2021.. Structural dynamics in the water and proton channels of photosystem II during the S2 to S3 transition. . Nat. Commun. 12::6531
    [Crossref] [Google Scholar]
  64. 64.
    Ibrahim M, Fransson T, Chatterjee R, Cheah MH, Hussein R, et al. 2020.. Untangling the sequence of events during the S2→S3 transition in photosystem II and implications for the water oxidation mechanism. . PNAS 117::1262435
    [Crossref] [Google Scholar]
  65. 65.
    Ifuku K, Nagao R. 2021.. Evolution and function of the extrinsic subunits of photosystem II. . In Photosynthesis: Molecular Approaches to Solar Energy Conversion, ed. J-R Shen, K Satoh, SI Allakhverdiev , pp. 42946. Berlin:: Springer
    [Google Scholar]
  66. 66.
    Ishikita H, Saenger W, Loll B, Biesiadka J, Knapp EW. 2006.. Energetics of a possible proton exit pathway for water oxidation in photosystem II. . Biochemistry 45::206371
    [Crossref] [Google Scholar]
  67. 67.
    Isobe H, Shoji M, Suzuki T, Shen J-R, Yamaguchi K. 2021.. Exploring reaction pathways for the structural rearrangements of the Mn cluster induced by water binding in the S3 state of the oxygen evolving complex of photosystem II. . J. Photochem. Photobiol. A 405::112905
    [Crossref] [Google Scholar]
  68. 68.
    Joliot P, Barbieri G, Chabaud R. 1969.. A new model of photochemical centers in system II. . Photochem. Photobiol. 10::30929
    [Crossref] [Google Scholar]
  69. 69.
    Kamiya N, Shen JR. 2003.. Crystal structure of oxygen-evolving photosystem II from Thermosynechococcus vulcanus at 3.7-Å resolution. . PNAS 100::98103
    [Crossref] [Google Scholar]
  70. 70.
    Kashino Y, Koike H, Yoshio M, Egashira H, Ikeuchi M, et al. 2002.. Low-molecular-mass polypeptide components of a photosystem II preparation from the thermophilic cyanobacterium Thermosynechococcus vulcanus. . Plant Cell Physiol. 43::136673
    [Crossref] [Google Scholar]
  71. 71.
    Kern J, Alonso-Mori R, Hellmich J, Rosalie T, Hattne J, et al. 2012.. Room temperature femtosecond X-ray diffraction of photosystem II microcrystals. . PNAS 109::972126
    [Crossref] [Google Scholar]
  72. 72.
    Kern J, Alonso-Mori R, Tran R, Hattne J, Gildea RJ, et al. 2013.. Simultaneous femtosecond X-ray spectroscopy and diffraction of photosystem II at room temperature. . Science 340::49195
    [Crossref] [Google Scholar]
  73. 73.
    Kern J, Chatterjee R, Young ID, Fuller FD, Lassalle L, et al. 2018.. Structures of the intermediates of Kok's photosynthetic water oxidation clock. . Nature 563::42125
    [Crossref] [Google Scholar]
  74. 74.
    Kern J, Tran R, Alonso-Mori R, Koroidov S, Echols N, et al. 2014.. Taking snapshots of photosynthetic water oxidation using femtosecond X-ray diffraction and spectroscopy. . Nat. Commun. 5::4371
    [Crossref] [Google Scholar]
  75. 75.
    Kern J, Yachandra VK, Yano J. 2015.. Metalloprotein structures at ambient conditions and in real-time: biological crystallography and spectroscopy using X-ray free electron lasers. . Curr. Opin. Struct. Biol. 34::8798
    [Crossref] [Google Scholar]
  76. 76.
    Kim CJ, Debus RJ. 2019.. One of the substrate waters for O2 formation in photosystem II is provided by the water-splitting Mn4CaO5 cluster's Ca2+ ion. . Biochemistry 58::318592
    [Crossref] [Google Scholar]
  77. 77.
    Klauss A, Haumann M, Dau H. 2012.. Alternating electron and proton transfer steps in photosynthetic water oxidation. . PNAS 109::1603540
    [Crossref] [Google Scholar]
  78. 78.
    Klauss A, Haumann M, Dau H. 2015.. Seven steps of alternating electron and proton transfer in photosystem II water oxidation traced by time-resolved photothermal beam deflection at improved sensitivity. . J. Phys. Chem. B 119::267789
    [Crossref] [Google Scholar]
  79. 79.
    Kok B, Forbush B, McGloin M. 1970.. Cooperation of charges in photosynthetic oxygen evolution. A linear four step mechanism. . Photochem. Photobiol. 11::45775
    [Crossref] [Google Scholar]
  80. 80.
    Kulik LV, Epel B, Lubitz W, Messinger J. 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::1342135
    [Crossref] [Google Scholar]
  81. 81.
    Kuroda H, Kawashima K, Ueda K, Ikeda T, Saito K, et al. 2021.. Proton transfer pathway from the oxygen-evolving complex in photosystem II substantiated by extensive mutagenesis. . Biochim. Biophys. Acta Bioenerg. 1862::148329
    [Crossref] [Google Scholar]
  82. 82.
    Kusunoki M. 2007.. Mono-manganese mechanism of the photosytem II water splitting reaction by a unique Mn4Ca cluster. . Biochim. Biophys. Acta Bioenerg. 1767::48492
    [Crossref] [Google Scholar]
  83. 83.
    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::10898909
    [Crossref] [Google Scholar]
  84. 84.
    Liang WC, Roelofs TA, Cinco RM, Rompel A, Latimer MJ, et al. 2000.. Structural change of the Mn cluster during the S2 → S3 state transition of the oxygen-evolving complex of photosystem II. Does it reflect the onset of water/substrate oxidation? Determination by Mn X-ray absorption spectroscopy. . J. Am. Chem. Soc. 122::3399412
    [Crossref] [Google Scholar]
  85. 85.
    Liao R-Z, Masaoka S, Siegbahn PEM. 2018.. Metal oxidation states for the O–O bond formation in the water oxidation catalyzed by a pentanuclear iron complex. . ACS Catal. 8::1167178
    [Crossref] [Google Scholar]
  86. 86.
    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::104044
    [Crossref] [Google Scholar]
  87. 87.
    Lubitz W, Pantazis DA, Cox N. 2023.. Water oxidation in oxygenic photosynthesis studied by magnetic resonance techniques. . FEBS Lett. 597::629
    [Crossref] [Google Scholar]
  88. 88.
    Malone LA, Proctor MS, Hitchcock A, Hunter CN, Johnson MP. 2021.. Cytochrome b6f—orchestrator of photosynthetic electron transfer. . Biochim. Biophys. Acta Bioenerg. 1862::148380
    [Crossref] [Google Scholar]
  89. 89.
    Mamedov M, Govindjee, Nadtochenko V, Semenov A. 2015.. Primary electron transfer processes in photosynthetic reaction centers from oxygenic organisms. . Photosynth. Res. 125::5163
    [Crossref] [Google Scholar]
  90. 90.
    McDermott AE, Yachandra VK, Guiles RD, Cole JL, Dexheimer SL, et al. 1988.. Characterization of the manganese O2-evolving complex and the iron-quinone acceptor complex in photosystem II from a thermophilic cyanobacterium by electron paramagnetic resonance and X-ray absorption spectroscopy. . Biochemistry 27::402131
    [Crossref] [Google Scholar]
  91. 91.
    Messinger J, Nugent JHA, Evans MCW. 1997.. Detection of an EPR multiline signal for the S0* state in photosystem II. . Biochemistry 36::1105560
    [Crossref] [Google Scholar]
  92. 92.
    Messinger J, Robblee JH, Bergmann U, Fernandez C, Glatzel P, et al. 2001.. Absence of Mn-centered oxidation in the S2 to S3 transition: implications for the mechanism of photosynthetic water oxidation. . J. Am. Chem. Soc. 123::780420
    [Crossref] [Google Scholar]
  93. 93.
    Messinger J, Robblee JH, Yu WO, Sauer K, Yachandra VK, Klein MP. 1997.. The S0 state of the oxygen-evolving complex in photosystem II is paramagnetic: detection of an EPR multiline signal. . J. Am. Chem. Soc. 119::1134950
    [Crossref] [Google Scholar]
  94. 94.
    Mukerji I, Andrews JC, DeRose VJ, Latimer MJ, Yachandra VK, et al. 1994.. Orientation of the oxygen-evolving manganese complex in a photosystem II membrane preparation: an X-ray absorption spectroscopy study. . Biochemistry 33::971221
    [Crossref] [Google Scholar]
  95. 95.
    Murray J, Barber J. 2008.. Oxygen, water, proton and quinone channels in PSII. . In Photosynthesis. Energy from the Sun, , 46770. Dordrecht, Neth.:: Springer
    [Crossref] [Google Scholar]
  96. 96.
    Murray JW, Barber J. 2007.. Structural characteristics of channels and pathways in photosystem II including the identification of an oxygen channel. . J. Struct. Biol. 159::22837
    [Crossref] [Google Scholar]
  97. 97.
    Nakamura S, Ota K, Shibuya Y, Noguchi T. 2016.. Role of a water network around the Mn4CaO5 cluster in photosynthetic water oxidation: a Fourier transform infrared spectroscopy and quantum mechanics/molecular mechanics calculation study. . Biochemistry 55::597607
    [Crossref] [Google Scholar]
  98. 98.
    Neutze R, Wouts R, van der Spoel D, Weckert E, Hajdu J. 2000.. Potential for biomolecular imaging with femtosecond X-ray pulses. . Nature 406::75257
    [Crossref] [Google Scholar]
  99. 99.
    Nixon PJ, Diner BA. 1994.. Analysis of water-oxidation mutants constructed in the cyanobacterium Synechocystis sp. PCC 6803. . Biochem. Soc. Trans. 22::33843
    [Crossref] [Google Scholar]
  100. 100.
    Noguchi T. 2007.. Light-induced FTIR difference spectroscopy as a powerful tool toward understanding the molecular mechanism of photosynthetic oxygen evolution. . Photosynth. Res. 91::5969
    [Crossref] [Google Scholar]
  101. 101.
    Noguchi T. 2008.. Fourier transform infrared analysis of the photosynthetic oxygen-evolving center. . Coord. Chem. Rev. 252::33646
    [Crossref] [Google Scholar]
  102. 102.
    Noguchi T, Suzuki H, Tsuno M, Sugiura M, Kato C. 2012.. Time-resolved infrared detection of the proton and protein dynamics during photosynthetic oxygen evolution. . Biochemistry 51::320514
    [Crossref] [Google Scholar]
  103. 103.
    Ono T, Inoue Y. 1988.. Discrete extraction of the Ca atom functional for O2 evolution in higher-plant photosystem II by a simple low pH treatment. . FEBS Lett. 227::14752
    [Crossref] [Google Scholar]
  104. 104.
    Pantazis DA, Ames W, Cox N, Lubitz W, Neese F. 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::993540
    [Crossref] [Google Scholar]
  105. 105.
    Peloquin JM, Campbell KA, Randall DW, Evanchik MA, Pecoraro VL, et al. 2000.. 55Mn ENDOR of the S2-state multiline EPR signal of photosystem II: implications on the structure of the tetranuclear cluster. . J. Am. Chem. Soc. 122::1092642
    [Crossref] [Google Scholar]
  106. 106.
    Penner-Hahn JE. 1998.. Structural characterization of the Mn site in the photosynthetic oxygen-evolving complex. . In Metal Sites in Proteins and Models: Redox Centres, , 136. Berlin:: Springer
    [Google Scholar]
  107. 107.
    Penner-Hahn JE, Fronko RM, Pecoraro VL, Yocum CF, Betts SD, Bowlby NR. 1990.. Structural characterization of the manganese sites in the photosynthetic oxygen-evolving complex using X-ray absorption spectroscopy. . J. Am. Chem. Soc. 112::254957
    [Crossref] [Google Scholar]
  108. 108.
    Pirson A. 1937.. Ernährungs- und stoffwechselphysiologische Untersuchungen an Fontinalis und Chlorella. . Z. Bot. 31::193267
    [Google Scholar]
  109. 109.
    Pokhrel R, Brudvig GW. 2014.. Oxygen-evolving complex of photosystem II: correlating structure with spectroscopy. . Phys. Chem. Chem. Phys. 16::1181221
    [Crossref] [Google Scholar]
  110. 110.
    Pushkar Y, Ravari AK, Jensen SC, Palenik M. 2019.. Early binding of substrate oxygen is responsible for a spectroscopically distinct S2 state in photosystem II. . J. Phys. Chem. Lett. 10::528491
    [Crossref] [Google Scholar]
  111. 111.
    Pushkar Y, Yano J, Sauer K, Boussac A, Yachandra VK. 2008.. Structural changes in the Mn4Ca cluster and the mechanism of photosynthetic water splitting. . PNAS 105::187984
    [Crossref] [Google Scholar]
  112. 112.
    Rappaport F, Blancharddesce M, Lavergne J. 1994.. Kinetics of electron-transfer and electrochromic change during the redox transitions of the photosynthetic oxygen-evolving complex. . Biochim. Biophys. Acta Bioenerg. 1184::17892
    [Crossref] [Google Scholar]
  113. 113.
    Renger G. 2012.. Mechanism of light induced water splitting in photosystem II of oxygen evolving photosynthetic organisms. . Biochim. Biophys. Acta Bioenerg. 1817::116476
    [Crossref] [Google Scholar]
  114. 114.
    Riggs-Gelasco PJ, Mei R, Yocum CF, Penner-Hahn JE. 1996.. Reduced derivatives of the Mn cluster in the oxygen-evolving complex of photosystem II: an EXAFS study. . J. Am. Chem. Soc. 118::238799
    [Crossref] [Google Scholar]
  115. 115.
    Robblee JH, Messinger J, Cinco RM, McFarlane KL, Fernandez C, 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::745971
    [Crossref] [Google Scholar]
  116. 116.
    Roelofs TA, Liang MC, Latimer MJ, Cinco RM, Rompel A, et al. 1996.. Oxidation states of the manganese cluster during the flash-induced S-state cycle of the photosynthetic oxygen-evolving complex. . PNAS 93::333540
    [Crossref] [Google Scholar]
  117. 117.
    Romero E, Novoderezhkin VI, van Grondelle R. 2017.. Quantum design of photosynthesis for bio-inspired solar-energy conversion. . Nature 543::35565
    [Crossref] [Google Scholar]
  118. 118.
    Rutherford AW, Osyczka A, Rappaport F. 2012.. Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: redox tuning to survive life in O2. . FEBS Lett. 586::60316
    [Crossref] [Google Scholar]
  119. 119.
    Saito T, Yamanaka S, Kanda K, Isobe H, Takano Y, 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 angstrom X-ray resolution. . Int. J. Quantum Chem. 112::25376
    [Crossref] [Google Scholar]
  120. 120.
    Sakashita N, Ishikita H, Saito K. 2020.. Rigidly hydrogen-bonded water molecules facilitate proton transfer in photosystem II. . Phys. Chem. Chem. Phys. 22::1583141
    [Crossref] [Google Scholar]
  121. 121.
    Sanchez-Baracaldo P, Cardona T. 2020.. On the origin of oxygenic photosynthesis and cyanobacteria. . New Phytol. 225::144046
    [Crossref] [Google Scholar]
  122. 122.
    Schlodder E, Witt HT. 1999.. Stoichiometry of proton release from the catalytic center in photosynthetic water oxidation. Reexamination by a glass electrode study at pH 5.5–7.2. . J. Biol. Chem. 274::3038792
    [Crossref] [Google Scholar]
  123. 123.
    Schuth N, Zaharieva I, Chernev P, Berggren G, Anderlund M, et al. 2018.. Kα X-ray emission spectroscopy on the photosynthetic oxygen-evolving complex supports manganese oxidation and water binding in the S3 state. . Inorg. Chem. 57::1042430
    [Crossref] [Google Scholar]
  124. 124.
    Shevela D, Kern JF, Govindjee G, Messinger J. 2023.. Solar energy conversion by photosystem II: principles and structures. . Photosynth. Res. 156::279307
    [Crossref] [Google Scholar]
  125. 125.
    Shevela D, Messinger J. 2013.. Studying the oxidation of water to molecular oxygen in photosynthetic and artificial systems by time-resolved membrane-inlet mass spectrometry. . Front. Plant Sci. 4::473
    [Crossref] [Google Scholar]
  126. 126.
    Shimizu T, Sugiura M, Noguchi T. 2018.. Mechanism of proton-coupled electron transfer in the S0-to-S1 transition of photosynthetic water oxidation as revealed by time-resolved infrared spectroscopy. . J. Phys. Chem. B 122::946070
    [Crossref] [Google Scholar]
  127. 127.
    Siegbahn PE. 2009.. Structures and energetics for O2 formation in photosystem II. . Acc. Chem. Res. 42::187180
    [Crossref] [Google Scholar]
  128. 128.
    Simon PS, Makita H, Bogacz I, Fuller F, Bhowmick A, et al. 2023.. Capturing the sequence of events during the water oxidation reaction in photosynthesis using XFELs. . FEBS Lett. 597::3037
    [Crossref] [Google Scholar]
  129. 129.
    Solomon EI, Hedman B, Hodgson KO, Dey A, Szilagyi RK. 2005.. Ligand K-edge X-ray absorption spectroscopy: covalency of ligand-metal bonds. . Coord. Chem. Rev. 249::97129
    [Crossref] [Google Scholar]
  130. 130.
    Soo RM, Hemp J, Parks DH, Fischer WW, Hugenholtz P. 2017.. On the origins of oxygenic photosynthesis and aerobic respiration in cyanobacteria. . Science 355::143639
    [Crossref] [Google Scholar]
  131. 131.
    Spence JCH. 2017.. XFELs for structure and dynamics in biology. . IUCrJ 4::32239
    [Crossref] [Google Scholar]
  132. 132.
    Sproviero EM, Gascon JA, McEvoy JP, Brudvig GW, Batista VS. 2008.. Quantum mechanics/molecular mechanics study of the catalytic cycle of water splitting in photosystem II. . J. Am. Chem. Soc. 130::342842
    [Crossref] [Google Scholar]
  133. 133.
    Suga M, Akita F, Hirata K, Ueno G, Murakami H, et al. 2015.. Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. . Nature 517::99103
    [Crossref] [Google Scholar]
  134. 134.
    Suga M, Akita F, Sugahara M, Kubo M, Nakajima Y, et al. 2017.. Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL. . Nature 543::13135
    [Crossref] [Google Scholar]
  135. 135.
    Suga M, Akita F, Yamashita K, Nakajima Y, Ueno G, et al. 2019.. An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an X-ray free-electron laser. . Science 366::33438
    [Crossref] [Google Scholar]
  136. 136.
    Suzuki H, Sugiura M, Noguchi T. 2009.. Monitoring proton release during photosynthetic water oxidation in photosystem II by means of isotope-edited infrared spectroscopy. . J. Am. Chem. Soc. 131::784957
    [Crossref] [Google Scholar]
  137. 137.
    Takaoka T, Sakashita N, Saito K, Ishikita H. 2016.. pKa of a proton-conducting water chain in photosystem II. . J. Phys. Chem. Lett. 7::192532
    [Crossref] [Google Scholar]
  138. 138.
    Tommos C, Hoganson CW, Valentin MD, Lydakis-Simantiris N, Dorlet P, et al. 1998.. Manganese and tyrosyl radical function in photosynthetic oxygen evolution. . Curr. Opin. Chem. Biol. 2::24452
    [Crossref] [Google Scholar]
  139. 139.
    Tso J, Sivaraja M, Dismukes GC. 1991.. Calcium limits substrate accessibility or reactivity at the manganese cluster in photosynthetic water oxidation. . Biochemistry 30::473439
    [Crossref] [Google Scholar]
  140. 140.
    Ugur I, Rutherford AW, Kaila VR. 2016.. Redox-coupled substrate water reorganization in the active site of photosystem II—the role of calcium in substrate water delivery. . Biochim. Biophys. Acta Bioenerg. 1857::74048
    [Crossref] [Google Scholar]
  141. 141.
    Umena Y, Kawakami K, Shen J-R, Kamiya N. 2011.. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. . Nature 473::5560
    [Crossref] [Google Scholar]
  142. 142.
    Vassiliev S, Zaraiskaya T, Bruce D. 2012.. Exploring the energetics of water permeation in photosystem II by multiple steered molecular dynamics simulations. . Biochim. Biophys. Acta Bioenerg. 1817::167178
    [Crossref] [Google Scholar]
  143. 143.
    Ward LM, Kirschvink JL, Fischer WW. 2016.. Timescales of oxygenation following the evolution of oxygenic photosynthesis. . Orig. Evol. Biosph. 46::5165
    [Crossref] [Google Scholar]
  144. 144.
    Weisz DA, Gross ML, Pakrasi HB. 2017.. Reactive oxygen species leave a damage trail that reveals water channels in photosystem II. . Sci. Adv. 3::eaao3013
    [Crossref] [Google Scholar]
  145. 145.
    Wydrzynski T, Satoh S, eds. 2005.. Photosystem II: The Light-Driven Water:Plastoquinone Oxidoreductase. Berlin:: Springer
    [Google Scholar]
  146. 146.
    Yachandra VK, DeRose VJ, Latimer MJ, Mukerji I, Sauer K, Klein MP. 1993.. Where plants make oxygen: a structural model for the photosynthetic oxygen-evolving manganese cluster. . Science 260::67579
    [Crossref] [Google Scholar]
  147. 147.
    Yachandra VK, Guiles RD, McDermott A, Britt RD, Dexheimer SL, et al. 1986.. The state of manganese in the photosynthetic apparatus: 4. Structure of the manganese complex in photosystem II studied using EXAFS spectroscopy. The S1 state of the O2-evolving photosystem II complex from spinach. . Biochim. Biophys. Acta Bioenerg. 850::32432
    [Crossref] [Google Scholar]
  148. 148.
    Yachandra VK, Guiles RD, McDermott AE, Cole JL, Britt RD, et al. 1987.. Comparison of the structure of the manganese complex in the S1 and S2 states of the photosynthetic O2-evolving complex: an X-ray absorption spectroscopy study. . Biochemistry 26::597481
    [Crossref] [Google Scholar]
  149. 149.
    Yachandra VK, Sauer K, Klein MP. 1996.. Manganese cluster in photosynthesis: where plants oxidize water to dioxygen. . Chem. Rev. 96::292750
    [Crossref] [Google Scholar]
  150. 150.
    Yachandra VK, Yano J. 2011.. Calcium in the oxygen-evolving complex: structural and mechanistic role determined by X-ray spectroscopy. . J. Photochem. Photobiol. B 104::5159
    [Crossref] [Google Scholar]
  151. 151.
    Yamaguchi K, Shoji M, Isobe H, Miyagawa K, Nakatani K. 2019.. Theory of chemical bonds in metalloenzymes XXII: a concerted bond-switching mechanism for the oxygen-oxygen bond formation coupled with one electron transfer for water oxidation in the oxygen-evolving complex of photosystem II. . Mol. Phys. 117::232054
    [Crossref] [Google Scholar]
  152. 152.
    Yano J, Kern J, Irrgang K-D, Latimer MJ, Bergmann U, et al. 2005.. X-ray damage to the Mn4Ca complex in photosystem II crystals: a case study for metallo-protein X-ray crystallography. . PNAS 102::1204752
    [Crossref] [Google Scholar]
  153. 153.
    Yano J, Kern J, Sauer K, Latimer M, Pushkar Y, et al. 2006.. Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster. . Science 314::82125
    [Crossref] [Google Scholar]
  154. 154.
    Yano J, Pushkar Y, Glatzel P, Lewis A, Sauer K, 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::1497475
    [Crossref] [Google Scholar]
  155. 155.
    Yano J, Yachandra VK. 2007.. Oxidation state changes of the Mn4Ca cluster in photosystem II. . Photosynth. Res. 92::289303
    [Crossref] [Google Scholar]
  156. 156.
    Yano J, Yachandra VK. 2008.. Where water is oxidized to dioxygen: structure of the photosynthetic Mn4Ca cluster from X-ray spectroscopy. . Inorg. Chem. 47::171126
    [Crossref] [Google Scholar]
  157. 157.
    Yano J, Yachandra VK. 2014.. Mn4Ca cluster in photosynthesis: where and how water is oxidized to dioxygen. . Chem. Rev. 114::4175205
    [Crossref] [Google Scholar]
  158. 158.
    Yoneda Y, Arsenault EA, Yang S-J, Orcutt K, Iwai M, Fleming GR. 2022.. The initial charge separation step in oxygenic photosynthesis. . Nat. Commun. 13::2275
    [Crossref] [Google Scholar]
  159. 159.
    Young ID, Ibrahim M, Chatterjee R, Gul S, Fuller FD, et al. 2016.. Structure of photosystem II and substrate binding at room temperature. . Nature 540::45357
    [Crossref] [Google Scholar]
  160. 160.
    Zimmermann J-L, Rutherford AW. 1984.. EPR studies of the oxygen-evolving enzyme of photosystem II. . Biochim. Biophys. Acta Bioenerg. 767::16067
    [Crossref] [Google Scholar]
  161. 161.
    Zouni A, Witt H-T, Kern J, Fromme P, Krauß N, et al. 2001.. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. . Nature 409::73943
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-biophys-071723-102519
Loading
/content/journals/10.1146/annurev-biophys-071723-102519
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