1932

Abstract

The investigation of water oxidation in photosynthesis has remained a central topic in biochemical research for the last few decades due to the importance of this catalytic process for technological applications. Significant progress has been made following the 2011 report of a high-resolution X-ray crystallographic structure resolving the site of catalysis, a protein-bound MnCaO complex, which passes through ≥5 intermediate states in the water-splitting cycle. Spectroscopic techniques complemented by quantum chemical calculations aided in understanding the electronic structure of the cofactor in all (detectable) states of the enzymatic process. Together with isotope labeling, these techniques also revealed the binding of the two substrate water molecules to the cluster. These results are described in the context of recent progress using X-ray crystallography with free-electron lasers on these intermediates. The data are instrumental for developing a model for the biological water oxidation cycle.

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2020-06-20
2024-06-24
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Literature Cited

  1. 1. 
    Fischer WW, Hemp J, Johnson JE 2016. Evolution of oxygenic photosynthesis. Annu. Rev. Earth Planet. Sci. 44:647–83
    [Google Scholar]
  2. 2. 
    Hamilton TL, Bryant DA, Macalady JL 2016. The role of biology in planetary evolution: cyanobacterial primary production in low-oxygen Proterozoic oceans. Environ. Microbiol. 18:325–40
    [Google Scholar]
  3. 3. 
    acatech, Nat. Acad. Sci. Eng., Ger. Nat. Acad. Sci. Leopoldina, Union Ger. Acad. Sci. Hum 2018. Artificial photosynthesis: state of research, scientific-technological challenges and perspectives Position Pap., acatech, Nat. Acad. Sci. Eng., Ger. Nat. Acad. Sci. Leopoldina, Union Ger. Acad. Sci. Hum Munich:
    [Google Scholar]
  4. 4. 
    Chabi S, Papadantonakis KM, Lewis NS, Freund MS 2017. Membranes for artificial photosynthesis. Energy Environ. Sci. 10:1320–38
    [Google Scholar]
  5. 5. 
    Collings AF, Critchley C 2005. Artificial Photosynthesis: From Basic Biology to Industrial Application Chichester, UK: Wiley
    [Google Scholar]
  6. 6. 
    Cox N, Lubitz W. 2013. Molecular concepts of water splitting: nature's approach. Chemical Energy Storage R Schlögl 185–224 Berlin: De Gruyter GmbH
    [Google Scholar]
  7. 7. 
    Cox N, Pantazis DA, Neese F, Lubitz W 2015. Artificial photosynthesis: understanding water splitting in nature. Interface Focus 5:20150009
    [Google Scholar]
  8. 8. 
    Faunce TA, Lubitz W, Rutherford AW, MacFarlane DR, Moore GF et al. 2013. Energy and environment policy case for a global project on artificial photosynthesis. Energy Environ. Sci. 6:695–98
    [Google Scholar]
  9. 9. 
    Gratzel M. 2005. Solar energy conversion by dye-sensitized photovoltaic cells. Inorg. Chem. 44:6841–51
    [Google Scholar]
  10. 10. 
    McKone JR, Crans DC, Martin C, Turner J, Duggal AR, Gray HB 2016. Translational science for energy and beyond. Inorg. Chem. 55:9131–43
    [Google Scholar]
  11. 11. 
    Nocera DG. 2012. The artificial leaf. Acc. Chem. Res. 45:767–76
    [Google Scholar]
  12. 12. 
    Nocera DG. 2017. Solar fuels and solar chemicals industry. Acc. Chem. Res. 50:616–19
    [Google Scholar]
  13. 13. 
    Messinger J, Lubitz W, Shen JR 2014. Photosynthesis: from natural to artificial. Special issue. Phys. Chem. Chem. Phys.16
    [Google Scholar]
  14. 14. 
    Junge W. 2019. Oxygenic photosynthesis: history, status and perspective. Q. Rev. Biophys. 52:e11–17
    [Google Scholar]
  15. 15. 
    Pantazis DA. 2018. Missing pieces in the puzzle of biological water oxidation. ACS Catal 8:9477–507
    [Google Scholar]
  16. 16. 
    Shen J-R. 2015. The structure of photosystem II and the mechanism of water oxidation in photosynthesis. Annu. Rev. Plant Biol. 66:23–48
    [Google Scholar]
  17. 17. 
    Vinyard DJ, Brudvig GW. 2017. Progress toward a molecular mechanism of water oxidation in photosystem II. Annu. Rev. Phys. Chem. 68:101–16
    [Google Scholar]
  18. 18. 
    Yano J, Yachandra V. 2014. Mn4Ca cluster in photosynthesis: where and how water is oxidized to dioxygen. Chem. Rev. 114:4175–205
    [Google Scholar]
  19. 19. 
    Barber J. 2017. A mechanism for water splitting and oxygen production in photosynthesis. Nat. Plants 3:17041
    [Google Scholar]
  20. 20. 
    Lubitz W, Chrysina M, Cox N 2019. Water oxidation in photosystem II. Photosynth. Res. 142:105–25
    [Google Scholar]
  21. 21. 
    Wydrzynski T, Satoh K 2005. Photosystem II, The Light-Driven Water: Plastoquinone Oxidoreductase Netherlands: Springer
    [Google Scholar]
  22. 22. 
    Joliot P, Barbieri G, Chabaud R 1969. A new model of photochemical centers in system 2. Photochem. Photobiol. 10:309–29
    [Google Scholar]
  23. 23. 
    Kok B, Forbush B, McGloin M 1970. Cooperation of charges in photosynthetic O2 evolution—1. A linear four step mechanism. Photochem. Photobiol. 11:457–75
    [Google Scholar]
  24. 24. 
    Nilsson H, Cournac L, Rappaport F, Messinger J, Lavergne J 2016. Estimation of the driving force for dioxygen formation in photosynthesis. Biochim. Biophys. Acta 1857:23–33
    [Google Scholar]
  25. 25. 
    Klauss A, Haumann M, Dau H 2012. Alternating electron and proton transfer steps in photosynthetic water oxidation. PNAS 109:16035–40
    [Google Scholar]
  26. 26. 
    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 119:2677–89
    [Google Scholar]
  27. 27. 
    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. 131:7849–57
    [Google Scholar]
  28. 28. 
    Dau H, Haumann M. 2007. Eight steps preceding O-O bond formation in oxygenic photo synthesis—a basic reaction cycle of the photosystem II manganese complex. Biochim. Biophys. Acta 1767:472–83
    [Google Scholar]
  29. 29. 
    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. 274:30387–92
    [Google Scholar]
  30. 30. 
    Nixon PJ, Michoux F, Yu JF, Boehm M, Komenda J 2010. Recent advances in understanding the assembly and repair of photosystem II. Ann. Bot. 106:1–16
    [Google Scholar]
  31. 31. 
    Järvi S, Suorsa M, Aro E-M 2015. Photosystem II repair in plant chloroplasts—regulation, assisting proteins and shared components with photosystem II biogenesis. Biochim. Biophys. Acta Bioenerget. 1847:900–9
    [Google Scholar]
  32. 32. 
    Vass I, Aro E-M. 2008. Photoinhibition of photosynthetic electron transport. Primary Processes of Photosynthesis, Part 1: Basic Principles and Apparatus G Renger 393–425 Cambridge: Royal Soc. Chem.
    [Google Scholar]
  33. 33. 
    van Wijk KJ, Nilsson LO, Styring S 1994. Synthesis of reaction center proteins and reactivation of redox components during repair of photosystem II after light-induced inactivation. J. Biol. Chem. 269:28382–92
    [Google Scholar]
  34. 34. 
    Messinger J, Renger G. 2008. Photosynthetic water splitting. Primary Processes of Photosynthesis, Part 2: Principles and Apparatus G Renger 291–349 Cambridge: Royal Soc. Chem.
    [Google Scholar]
  35. 35. 
    Krieger-Liszkay A, Fufezan C, Trebst A 2008. Singlet oxygen production in photosystem II and related protection mechanism. Photosynth. Res. 98:551–64
    [Google Scholar]
  36. 36. 
    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 318:618–24
    [Google Scholar]
  37. 37. 
    Jordan P, Fromme P, Witt HT, Klukas O, Saenger W, Krauß N 2001. Three-dimensional structure of cyanobacterial photosystem I at 2.5Å resolution. Nature 411:909–17
    [Google Scholar]
  38. 38. 
    Zouni A, Witt HT, Kern J, Fromme P, Krauss N et al. 2001. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409:739–43
    [Google Scholar]
  39. 39. 
    Hoganson CW, Babcock GT. 1997. A metalloradical mechanism for the generation of oxygen from water in photosynthesis. Science 277:1953–56
    [Google Scholar]
  40. 40. 
    Yano J, Kern J, Irrgang KD, Latimer MJ, Bergmann U 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]
  41. 41. 
    Grabolle M, Haumann M, Müller C, Liebisch P, Dau H 2006. Rapid loss of structural motifs in the manganese complex of oxygenic photosynthesis by X-ray irradiation at 10–300 K. J. Biol. Chem. 281:4580–88
    [Google Scholar]
  42. 42. 
    Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S 2004. Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–38
    [Google Scholar]
  43. 43. 
    Robblee JH, Cinco RM, Yachandra VK 2001. X-ray spectroscopy-based structure of the Mn cluster and mechanism of photosynthetic oxygen evolution. Biochim. Biophys. Acta Bioenerget. 1503:7–23
    [Google Scholar]
  44. 44. 
    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 Mn cluster. J. Am. Chem. Soc. 122:10926–42
    [Google Scholar]
  45. 45. 
    Peloquin JM, Britt RD. 2001. EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn cluster. Biochim. Biophys. Acta Bioenerget. 1503:96–111
    [Google Scholar]
  46. 46. 
    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 473:55–60
    [Google Scholar]
  47. 47. 
    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. 127:14974–75
    [Google Scholar]
  48. 48. 
    Dau H, Grundmeier A, Loja P, Haumann M 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 363:1237–43
    [Google Scholar]
  49. 49. 
    Luber S, Rivalta I, Umena Y, Kawakami K, Shen J-R et al. 2011. S1-state model of the O2-evolving complex of photosystem II. Biochemistry 50:6308–11
    [Google Scholar]
  50. 50. 
    Ames W, Pantazis DA, Krewald V, Cox N, Messinger J 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]
  51. 51. 
    Galstyan A, Robertazzi A, Knapp EW 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]
  52. 52. 
    Hirata K, Shinzawa-Itoh K, Yano N, Takemura S, Kato K et al. 2014. Determination of damage-free crystal structure of an X-ray–sensitive protein using an XFEL. Nat. Methods 11:734–36
    [Google Scholar]
  53. 53. 
    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 517:99–103
    [Google Scholar]
  54. 54. 
    Perez-Navarro M, Neese F, Lubitz W, Pantazis DA, Cox N 2016. Recent developments in biological water oxidation. Curr. Opin. Chem. Biol. 31:113–19
    [Google Scholar]
  55. 55. 
    Neutze R, Wouts R, van der Spoel D, Weckert E, Hajdu J 2000. Potential for biomolecular imaging with femtosecond X-ray pulses. Nature 406:752–57
    [Google Scholar]
  56. 56. 
    Chapman HN, Fromme P, Barty A, White TA, Kirian RA et al. 2011. Femtosecond X-ray protein nanocrystallography. Nature 470:73–77
    [Google Scholar]
  57. 57. 
    Johansson LC, Arnlund D, White TA, Katona G, DePonte DP et al. 2012. Lipidic phase membrane protein serial femtosecond crystallography. Nat. Methods 9:263–65
    [Google Scholar]
  58. 58. 
    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 340:491–95
    [Google Scholar]
  59. 59. 
    Kern J, Hattne J, Tran R, Alonso-Mori R, Laksmono H et al. 2014. Methods development for diffraction and spectroscopy studies of metalloenzymes at X-ray free-electron lasers. Philos. Trans. R. Soc. B 369:20130590
    [Google Scholar]
  60. 60. 
    Kern J, Alonso-Mori R, Hellmich J, Tran R, Hattne J et al. 2012. Room temperature femtosecond X-ray diffraction of photosystem II microcrystals. PNAS 109:9721–26
    [Google Scholar]
  61. 61. 
    Kupitz C, Basu S, Grotjohann I, Fromme R, Zatsepin NA et al. 2014. Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature 513:261–65
    [Google Scholar]
  62. 62. 
    Askerka M, Wang J, Vinyard DJ, Brudvig GW, Batista VS 2016. S3 state of the O2-evolving complex of photosystem II: insights from QM/MM, EXAFS, and femtosecond X-ray diffraction. Biochemistry 55:981–84
    [Google Scholar]
  63. 63. 
    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
    [Google Scholar]
  64. 64. 
    Young ID, Ibrahim M, Chatterjee R, Gul S, Fuller FD et al. 2016. Structure of photosystem II and substrate binding at room temperature. Nature 540:453–57
    [Google Scholar]
  65. 65. 
    Sauter NK, Echols N, Adams PD, Zwart PH, Kern J et al. 2016. No observable conformational changes in PSII. Nature 533:E1–2
    [Google Scholar]
  66. 66. 
    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 543:131–35
    [Google Scholar]
  67. 67. 
    Pantazis DA. 2019. The S3 state of the oxygen-evolving complex: overview of spectroscopy and XFEL crystallography with a critical evaluation of early-onset models for O–O bond formation. Inorganics 7:55
    [Google Scholar]
  68. 68. 
    Messinger J, Badger M, Wydrzynski T 1995. Detection of one slowly exchanging substrate water molecule in the S3 state of photosystem II. PNAS 92:3209–13
    [Google Scholar]
  69. 69. 
    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 345:804–8
    [Google Scholar]
  70. 70. 
    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 563:421–25
    [Google Scholar]
  71. 71. 
    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 366:334–38
    [Google Scholar]
  72. 72. 
    Mukherjee S, Stull JA, Yano J, Stamatatos TC, Pringouri K 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]
  73. 73. 
    Kanady JS, Tsui EY, Day MW, Agapie T 2011. A synthetic model of the Mn3Ca subsite of the oxygen-evolving complex in photosystem II. Science 333:733–36
    [Google Scholar]
  74. 74. 
    Spatzal T, Aksoyoglu M, Zhang L, Andrade SLA, Schleicher E et al. 2011. Evidence for interstitial carbon in nitrogenase FeMo cofactor. Science 334:940
    [Google Scholar]
  75. 75. 
    Tanaka A, Fukushima Y, Kamiya N 2017. Two different structures of the oxygen-evolving complex in the same polypeptide frameworks of photosystem II. J. Am. Chem. Soc. 139:1718–21
    [Google Scholar]
  76. 76. 
    Dismukes GC, Siderer Y. 1981. Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water. PNAS 78:274–78
    [Google Scholar]
  77. 77. 
    Messinger J, Robblee JH, Bergmann U, Fernandez C, Glatzel P et al. 2001. Absence of Mn-centered oxidation in the S2 → S3 transition: implications for the mechanism of photosynthetic water oxidation. J. Am. Chem. Soc. 123:7804–20
    [Google Scholar]
  78. 78. 
    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 44:1894–908
    [Google Scholar]
  79. 79. 
    Kulik LV, Epel B, Lubitz W, Messinger J 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]
  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. 129:13421–35
    [Google Scholar]
  81. 81. 
    Dau H, Liebisch P, Haumann M 2005. The manganese complex of oxygenic photosynthesis conversion of five-coordinated Mn(III) to six-coordinated Mn(IV) in the S2-S3 transition is implied by XANES simulations. Phys. Scr. T115:844–46
    [Google Scholar]
  82. 82. 
    Krewald V, Retegan M, Cox N, Messinger J, Lubitz W et al. 2015. Metal oxidation states in biological water splitting. Chem. Sci. 6:1676–95
    [Google Scholar]
  83. 83. 
    Krewald V, Retegan M, Neese F, Lubitz W, Pantazis DA, Cox N 2016. Spin state as a marker for the structural evolution of nature's water splitting catalyst. Inorg. Chem. 55:488–501
    [Google Scholar]
  84. 84. 
    Zaharieva I, Chernev P, Berggren G, Anderlund M, Styring S et al. 2016. Room-temperature energy-sampling Kβ X-ray emission spectroscopy of the Mn4Ca complex of photosynthesis reveals three manganese-centered oxidation steps and suggests a coordination change prior to O2 formation. Biochemistry 55:4197–211
    [Google Scholar]
  85. 85. 
    Zaharieva I, Dau H, Haumann M 2016. Sequential and coupled proton and electron transfer events in the S2 → S3 transition of photosynthetic water oxidation revealed by time-resolved X-ray absorption spectroscopy. Biochemistry 55:6996–7004
    [Google Scholar]
  86. 86. 
    Davis KM, Pushkar YN. 2015. Structure of the oxygen evolving complex of photosystem II at room temperature. J. Phys. Chem. B 119:3492–98
    [Google Scholar]
  87. 87. 
    Haumann M, Liebisch P, Müller C, Barra M, Grabolle M, Dau H 2005. Photosynthetic O2 formation tracked by time-resolved X-ray experiments. Science 310:1019–21
    [Google Scholar]
  88. 88. 
    Haumann M, Grundmeier A, Zaharieva I, Dau H 2008. Photosynthetic water oxidation at elevated dioxygen partial pressure monitored by time-resolved X-ray absorption measurements. PNAS 105:17384–89
    [Google Scholar]
  89. 89. 
    Kolling DRJ, Brown TS, Ananyev G, Dismukes GC 2009. Photosynthetic oxygen evolution is not reversed at high oxygen pressures: mechanistic consequences for the water-oxidizing complex. Biochemistry 48:1381–89
    [Google Scholar]
  90. 90. 
    Pushkar Y, Davis KM, Palenik MC 2018. Model of the oxygen evolving complex which is highly predisposed to O–O bond formation. J. Phys. Chem. Lett. 9:3525–31
    [Google Scholar]
  91. 91. 
    Narzi D, Bovi D, Guidoni L 2014. Pathway for Mn-cluster oxidation by tyrosine-Z in the S2 state of photosystem II. PNAS 111:8723–28
    [Google Scholar]
  92. 92. 
    Rivalta I, Amin M, Luber S, Vassiliev S, Pokhrel R et al. 2011. Structural-functional role of chloride in photosystem II. Biochemistry 50:6312–15
    [Google Scholar]
  93. 93. 
    Debus RJ. 2014. Evidence from FTIR difference spectroscopy that D1-Asp61 influences the water reactions of the oxygen-evolving Mn4CaO5 cluster of photosystem II. Biochemistry 53:2941–55
    [Google Scholar]
  94. 94. 
    Retegan M, Cox N, Lubitz W, Neese F, Pantazis DA 2014. The first tyrosyl radical intermediate formed in the S2-S3 transition of photosystem II. Phys. Chem. Chem. Phys. 16:11901–10
    [Google Scholar]
  95. 95. 
    Takemoto H, Sugiura M, Noguchi T 2019. Proton release process during the S2-to-S3 transition of photosynthetic water oxidation as revealed by the pH dependence of kinetics monitored by time-resolved infrared spectroscopy. Biochemistry 58:4276–83
    [Google Scholar]
  96. 96. 
    Chrysina M, de Mendonça Silva JC, Zahariou G, Pantazis DA, Ionnidis N 2019. Proton translocation via tautomerization of Asn298 during the S2-S3 state transition in the oxygen evolving complex of photosystem II. J. Phys. Chem. B 123:3068–78
    [Google Scholar]
  97. 97. 
    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. 51:9935–40
    [Google Scholar]
  98. 98. 
    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 Å X-ray resolution. Int. J. Quantum Chem. 112:253–76
    [Google Scholar]
  99. 99. 
    Bovi D, Narzi D, Guidoni L 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]
  100. 100. 
    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. 166:60–72
    [Google Scholar]
  101. 101. 
    Boussac A, Girerd JJ, Rutherford AW 1996. Conversion of the spin state of the manganese complex in photosystem II induced by near-infrared light. Biochemistry 35:6984–89
    [Google Scholar]
  102. 102. 
    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 1859:342–56
    [Google Scholar]
  103. 103. 
    Ahrling 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 36:13148–52
    [Google Scholar]
  104. 104. 
    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 EPR multiline signal. J. Am. Chem. Soc. 119:11349–50
    [Google Scholar]
  105. 105. 
    Hillier W, Messinger J, Wydrzynski T 1998. Kinetic determination of the fast exchanging substrate water molecule in the S3 state of photosystem II. Biochemistry 37:16908–14
    [Google Scholar]
  106. 106. 
    Hillier W, Wydrzynski T. 2000. The affinities for the two substrate water binding sites in the O2 evolving complex of photosystem II vary independently during S-state turnover. Biochemistry 39:4399–405
    [Google Scholar]
  107. 107. 
    Hillier W, Wydrzynski T. 2004. Substrate water interactions within the photosystem II oxygen evolving complex. Phys. Chem. Chem. Phys. 6:4882–89
    [Google Scholar]
  108. 108. 
    Cox N, Messinger J. 2013. Reflections on substrate water and dioxygen formation. Biochim. Biophys. Acta 1827:1020–30
    [Google Scholar]
  109. 109. 
    Tagore R, Chen HY, Crabtree RH, Brudvig GW 2006. Determination of μ-oxo exchange rates in di-μ-oxo dimanganese complexes by electrospray ionization mass spectrometry. J. Am. Chem. Soc. 128:9457–65
    [Google Scholar]
  110. 110. 
    McConnell IL, Grigoryants VM, Scholes CP, Myers WK, Chen P-Y et al. 2012. EPR-ENDOR characterization of (17O, 1H, 2H) water in manganese catalase and its relevance to the oxygen-evolving complex of photosystem II. J. Am. Chem. Soc. 134:1504–12
    [Google Scholar]
  111. 111. 
    Rapatskiy L, Cox N, Savitsky A, Ames WM, Sander J 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]
  112. 112. 
    Navarro MP, Ames WM, Nilsson H, Lohmiller T, Pantazis DA 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]
  113. 113. 
    Lohmiller T, Krewald V, Navarro MP, Retegan M, Rapatskiy L 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]
  114. 114. 
    Rapatskiy L, Ames WM, Perez-Navarro M, Savitsky A, Griese JJ et al. 2015. Characterization of oxygen bridged manganese model complexes using multifrequency 17O-hyperfine EPR spectroscopies and density functional theory. J. Phys. Chem. Lett. B 119:13904–21
    [Google Scholar]
  115. 115. 
    Lohmiller T, Krewald V, Sedoud A, Rutherford AW, Neese F et al. 2017. The first state in the catalytic cycle of the water-oxidizing enzyme: identification of a water-derived μ-hydroxo bridge. J. Am. Chem. Soc. 139:14412–24
    [Google Scholar]
  116. 116. 
    Klauss A, Sikora T, Suss B, Dau H 2012. Fast structural changes (200–900 ns) may prepare the photosynthetic manganese complex for oxidation by the adjacent tyrosine radical. Biochim. Biophys. Acta 1817:1196–207
    [Google Scholar]
  117. 117. 
    Sakamoto H, Shimizu T, Nagao R, Noguchi T 2017. Monitoring the reaction process during the S2 → S3 transition in photosynthetic water oxidation using time-resolved infrared spectroscopy. J. Am. Chem. Soc. 139:2022–29
    [Google Scholar]
  118. 118. 
    Siegbahn PEM. 2009. Structures and energetics for O2 formation in photosystem II. Acc. Chem. Res. 42:1871–80
    [Google Scholar]
  119. 119. 
    Siegbahn PEM. 2012. Mechanisms for proton release during water oxidation in the S2 to S3 and S3 to S4 transitions in photosystem II. Phys. Chem. Chem. Phys. 14:4849–56
    [Google Scholar]
  120. 120. 
    Ugur I, Rutherford AW, Kaila VRI 2016. Redox-coupled substrate water reorganization in the active site of photosystem II—the role of calcium in substrate water delivery. Biochim. Biophys. Acta 1857:740–48
    [Google Scholar]
  121. 121. 
    Retegan M, Krewald V, Mamedov F, Neese F, Lubitz W et al. 2016. A five-coordinate Mn(IV) intermediate in biological water oxidation: spectroscopic signature and a pivot mechanism for water binding. Chem. Sci. 7:72–84
    [Google Scholar]
  122. 122. 
    Capone M, Narzi D, Bovi D, Guidoni L 2016. Mechanism of water delivery to the active site of photosystem II along the S2 to S3 transition. J. Phys. Chem. Lett. 7:592–96
    [Google Scholar]
  123. 123. 
    Boussac A. 2019. Temperature dependence of the high-spin S2 to S3 transition in photosystem II: mechanistic consequences. Biochim. Biophys. Acta Bioenerget. 1860:508–18
    [Google Scholar]
  124. 124. 
    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 116:16841–46
    [Google Scholar]
  125. 125. 
    Oyala PH, Stich TA, Stull JA, Yu F, Pecoraro VL, Britt RD 2014. Pulse electron paramagnetic resonance studies of the interaction of methanol with the S2 state of the Mn4O5Ca cluster of photosystem II. Biochemistry 53:7914–28
    [Google Scholar]
  126. 126. 
    Retegan M, Pantazis DA. 2016. Interaction of methanol with the oxygen-evolving complex: atomistic models, channel identification, species dependence, and mechanistic implications. Chem. Sci. 7:6463–76
    [Google Scholar]
  127. 127. 
    Retegan M, Pantazis DA. 2017. Differences in the active site of water oxidation among photosynthetic organisms. J. Am. Chem. Soc. 139:14340–43
    [Google Scholar]
  128. 128. 
    Kim CJ, Debus RJ. 2017. Evidence from FTIR difference spectroscopy that a substrate H2O molecule for O2 formation in photosystem II is provided by the Ca ion of the catalytic Mn4CaO5 cluster. Biochemistry 56:2558–70
    [Google Scholar]
  129. 129. 
    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 58:3185–92
    [Google Scholar]
  130. 130. 
    Shoji M, Isobe H, Shigeta Y, Nakajima T, Yamaguchi K 2018. Concerted mechanism of water insertion and O2 release during the S4 to S0 transition of the oxygen-evolving complex in photosystem II. J. Phys. Chem. Lett. B 122:6491–502
    [Google Scholar]
  131. 131. 
    Krewald V, Neese F, Pantazis DA 2019. Implications of structural heterogeneity for the electronic structure of the final oxygen-evolving intermediate in photosystem II. J. Inorg. Biochem. 199:110797
    [Google Scholar]
  132. 132. 
    Messinger J. 2004. Evaluation of different mechanistic proposals for water oxidation in photosynthesis on the basis of Mn4OxCa structures for the catalytic site and spectroscopic data. Phys. Chem. Chem. Phys. 6:4764–71
    [Google Scholar]
  133. 133. 
    McEvoy JP, Brudvig GW. 2006. Water-splitting chemistry of photosystem II. Chem. Rev. 106:4455–83
    [Google Scholar]
  134. 134. 
    Sproviero EM, Gascón 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. 130:3428–42
    [Google Scholar]
  135. 135. 
    Siegbahn PEM. 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]
  136. 136. 
    Li X, Siegbahn PEM. 2015. Alternative mechanisms for O2 release and O-O bond formation in the oxygen evolving complex of photosystem II. Phys. Chem. Chem. Phys. 17:12168–74
    [Google Scholar]
  137. 137. 
    Shoji M, Isobe H, Shigeta Y, Nakajima T, Yamaguchi K 2018. Nonadiabatic one-electron transfer mechanism for the O-O bond formation in the oxygen-evolving complex of photosystem II. Chem. Phys. Lett. 698:138–46
    [Google Scholar]
  138. 138. 
    Yamaguchi K, Shoji M, Isobe H, Yamanaka S, Kawakami T et al. 2018. Theory of chemical bonds in metalloenzymes XXI. Possible mechanisms of water oxidation in oxygen evolving complex of photosystem II. Mol. Phys. 116:717–45
    [Google Scholar]
  139. 139. 
    Guo Y, Li H, He L-L, Zhao D-X, Gong L-D, Yang Z-Z 2017. The open-cubane oxo–oxyl coupling mechanism dominates photosynthetic oxygen evolution: a comprehensive DFT investigation on O–O bond formation in the S4 state. Phys. Chem. Chem. Phys. 19:13909–23
    [Google Scholar]
  140. 140. 
    Codola Z, Gomez L, Kleespies ST, Que L, Costas M, Lloret-Fillol J 2015. Evidence for an oxygen evolving iron-oxo-cerium intermediate in iron-catalysed water oxidation. Nat. Commun. 6:5865
    [Google Scholar]
  141. 141. 
    Siegbahn PEM. 2017. Nucleophilic water attack is not a possible mechanism for O–O bond formation in photosystem II. PNAS 114:4966–68
    [Google Scholar]
  142. 142. 
    Sala X, Romero I, Rodríguez M, Escriche L, Llobet A 2009. Molecular catalysts that oxidize water to dioxygen. Angew. Chem. Int. Ed. 48:2842–52
    [Google Scholar]
  143. 143. 
    Blakemore JD, Crabtree RH, Brudvig GW 2015. Molecular catalysts for water oxidation. Chem. Rev. 115:12974–3005
    [Google Scholar]
  144. 144. 
    Nilsson H, Rappaport F, Boussac A, Messinger J 2014. Substrate–water exchange in photosystem II is arrested before dioxygen formation. Nat. Commun.54305
    [Google Scholar]
  145. 145. 
    Isobe H, Shoji M, Shen J-R, Yamaguchi K 2016. Chemical equilibrium models for the S3 state of the oxygen-evolving complex of photosystem II. Inorg. Chem. 55:502–11
    [Google Scholar]
  146. 146. 
    Corry TA, O'Malley PJ. 2018. Evidence of O−O bond formation in the final metastable S3 state of nature's water oxidizing complex implying a novel mechanism of water oxidation. J. Phys. Chem. Lett. 9:6269–74
    [Google Scholar]
  147. 147. 
    Renger G. 1978. Theoretical studies about the structural and functional organization of the photosynthetic oxygen evolution. Photosynthetic Oxygen Evolution229–48 London: Academic
    [Google Scholar]
  148. 148. 
    Zhang BB, Sun LC. 2018. Why nature chose the Mn4CaO5 cluster as water-splitting catalyst in photosystem II: a new hypothesis for the mechanism of O-O bond formation. Dalton Trans 47:14381–87
    [Google Scholar]
  149. 149. 
    Dilbeck PL, Hwang HJ, Zaharieva I, Gerencser L, Dau H, Burnap RL 2012. The D1-D61N mutation in Synechocystis sp PCC 6803 allows the observation of pH-sensitive intermediates in the formation and release of O2 from photosystem II. Biochemistry 51:1079–91
    [Google Scholar]
  150. 150. 
    Bao H, Burnap RL. 2015. Structural rearrangements preceding dioxygen formation by the water oxidation complex of photosystem II. PNAS 112:6139–47
    [Google Scholar]
  151. 151. 
    Kim CJ, Bao H, Burnap RL, Debus RJ 2018. Impact of D1-V185 on the water molecules that facilitate O2 formation by the catalytic Mn4CaO5 cluster in photosystem II. Biochemistry 57:4299–311
    [Google Scholar]
  152. 152. 
    Loll B, Kern J, Saenger W, Zouni A, Biesiadka J 2005. Towards complete cofactor arrangement in the 3.0Å resolution structure of photosystem II. Nature 438:1040–44
    [Google Scholar]
  153. 153. 
    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. 16:334–42
    [Google Scholar]
  154. 154. 
    Zimmermann JL, Rutherford AW. 1984. EPR studies of the oxygen-evolving enzyme of photosystem II. Biochim. Biophys. Acta 767:160–67
    [Google Scholar]
  155. 155. 
    Cox N, Rapatskiy L, Su J-H, Pantazis DA, Sugiura M 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]
  156. 156. 
    Hillier W, Messinger J, Wydrzynski T 1998. Substrate water 18O exchange kinetics in the S2 state of photosystem II. Photosynthesis: Mechanisms and Effects G Garab 1307–10 Dordrecht, Neth: Springer
    [Google Scholar]
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