Skip to main content

Mechanism of Water Oxidation in Photosynthesis Elucidated by Interplay Between Experiment and Theory

  • Chapter
  • First Online:
Photosynthesis: Molecular Approaches to Solar Energy Conversion

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 47))

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 219.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 279.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 279.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Ames W, Pantazis DA, Krewald V, Cox N, Messinger J, Lubitz W, Neese F (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 133:19743–19757

    Article  CAS  PubMed  Google Scholar 

  • Anderson PW (1963) Theory of magnetic exchange interactios: exchange in insulators and semiconductors. Solid State Phys 14:99–214

    Article  CAS  Google Scholar 

  • Anderson PW (1987) The resonating valence bond state in La2CuO4 and super-conductivity. Sicence 235:1196–1198

    Article  CAS  Google Scholar 

  • Beal NJ, Corry TA, O’Malley PJ (2018) A comparison of experimental and broken symmetry density functional theory (BS-DFT) calculated electron para-magnetic resonance (EPR) parameters for intermediates involved in the S2 to S3 state transition of nature’s oxygen evolving complex. J Phys Chem B 122:1394–1407

    Article  CAS  PubMed  Google Scholar 

  • Boussac A (2019) Temperature dependence of the high-spin S2 to S3 transition in photosystem II: mechanistic consequences. Biochim Biophys Acta 1860:508–518

    Article  CAS  Google Scholar 

  • 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 35:6984–6989

    Article  CAS  PubMed  Google Scholar 

  • Boussac A, Sugiura M, Rutherford AW, Dorlet P (2009) Complete EPR spectrum of the S3-state of the oxygen-evolving photosystem II. J Am Chem Soc 131:5050–5051

    Article  CAS  PubMed  Google Scholar 

  • 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 Thermo synechcoccus elongatus. Biochim Biophys Acta 1847:576–586

    Article  CAS  PubMed  Google Scholar 

  • 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 1859:342–356

    Article  CAS  Google Scholar 

  • 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 52:11744–11749

    Article  CAS  Google Scholar 

  • Britt RD, Lorigan GA, Sauer K, Klein MP, Zimmermann JL (1992) The g = 2 multiline EPR signal of the S2 state of the photosynthetic oxygen-evolving complex originates from a ground spin state. Biochim Biophys Acta 1040:95–101

    Article  Google Scholar 

  • Britt RD, Peloquin JM, Campbell KA (2000) Pulsed and parallel-polarization EPR characterization of the photosystem II oxygen-evolving complex. Annu Rev Biphys Biomol Struct 29:463–495

    Article  CAS  Google Scholar 

  • Britt RD, Campbell KA, Peloquin JM (2004) Recent pulsed EPR studies of the photosystem II oxygen-evolving complex: implications as to water oxidation mechanisms. Biochim Biophys Acta 1655:158–171

    Article  CAS  PubMed  Google Scholar 

  • Carrell T, Tyryshkin A, Dismukes G (2002) An evaluation of structural models for the photosynthetic water-oxidizing complex derived from spectroscopic and X-ray diffraction signatures. J Biol Inorg Chem 7:2–22

    Article  CAS  PubMed  Google Scholar 

  • Chen H, Case DA, Dismukes GC (2018) Reconciling structural and spectroscopic fingerprints of the oxygen-evolving complex of photosystem II: a computational study of the S2 state. J Phys Chem B 122:11868–11882

    Article  CAS  PubMed  Google Scholar 

  • Chrysina M, Heyno E, Kutin Y, Reus M, Nilsson H, Nowaczyk MM, DeBeer S, Neese F, Messinger J, Lubitz W, Cox N (2019) Five-coordinate MnIV intermediate in the activation of nature’s water splitting cofactor. PNAS 116:16841–16846

    Google Scholar 

  • Concepcion JJ, Tsai M-K, Muckerman JT, Meyer TJ (2010) Mechanism of water oxidation by single-site ruthenium complex catalysts. J Am Chem Soc 132:1545–1557

    Article  CAS  PubMed  Google Scholar 

  • Cox N, Messinger J (2013) Reflections on substrate water and dioxygen formation. Biochim Biophys Acta 1827:1020–1030

    Article  CAS  PubMed  Google Scholar 

  • Cox N, Rapatskiy L, Su J-H, Pantazis DA, Sugiura M, Kulik L, Dorlet P, …, Messinger J (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 133:3635–3648

    Google Scholar 

  • 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 345:804–808

    Article  CAS  PubMed  Google Scholar 

  • Cukier RI, Nocera DG (1998) Proton-coupled electron transfer. Annu Rev Phys Chem 49:337–369

    Article  CAS  PubMed  Google Scholar 

  • Dau H, Limberg C, Reier T, Risch M, Roggan S, Strasser P (2010) The mechanism of water oxidation: from electrolysis via homogeneous to biological catalysis. ChemCatChem 2:724–761

    Article  CAS  Google Scholar 

  • Davis KM, Sullivan BT, Palenik MC (2018) Rapid evolution of the photosystem II electronic structure during water splitting. Phys Rev X 8:041014

    CAS  PubMed  PubMed Central  Google Scholar 

  • Debus RJ (1992) The manganese and calcium ions of photosynthetic oxygen evolution. Biochim Biophys Acta 1102:269–352

    Article  CAS  PubMed  Google Scholar 

  • Dismukes GC (1996) Manganese enzymes with binuclear active sites. Chem Rev 96:2909–2926

    Article  CAS  PubMed  Google Scholar 

  • Dismukes GC, Siderer Y (1981) Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water. Proc Natl Acad Sci U S A 78:274–278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dismukes GC, Brimblecombe R, Felton GAN, Pryadun RS, Sheats JE, Spiccia L, Swiegers GF (2009) Development of bioinspired Mn4O4-cubane water oxidation catalysts: lessons from photosynthsis. Acc Chem Res 42:1936–1943

    Article  CAS  Google Scholar 

  • Ferreira K N, Iverson T M, Maghlaoui K, Baber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303:1831–1838

    Google Scholar 

  • Glöckner C, Kern J, Broser M, Zouni A, Yachandra V, Yano J (2013) Structural changes of the oxygen-evolving complex in photosystem II during the catalytic cycle. J Biol Chem 288:22607–22620

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Groves JT, Haushalter RC, Nakamura M (1981) High-valent iron-porphyrin complexes related to peroxidase and cytochrome P-450. J Am Chem Soc 103:2884–2886

    Article  CAS  Google Scholar 

  • Groves JT, Lee J, Marla SS (1997) Detection and characterization of an oxomanganese(V) porphyrin complex by rapid-mixing stopped-flow spectrophotometry. J Am Chem Soc 119:6269–6273

    Article  CAS  Google Scholar 

  • Grundmeier A, Dau H (2012) Structural models of the manganese complex of photosystem II and mechanistic implications. Biochim Biophys Acta 1817:88–105

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa K, Ono T, Inoue Y, Kusunokic M (1999) Spin-exchange interactions in the S2-state manganese tetramer in photosynthetic oxygen-evolving complex deduced from g=2 multiline EPR signal. Chem Phys Lett 300:9–19

    Article  CAS  Google Scholar 

  • Haumann M, Müller C, Liebisch P, Iuzzolino L, Dittmer J, Grabolle M, Neisius T, …, Dau H (2005) Structural and oxidation state changes of the photosystem II manganese complex in four transitions of the water oxidation cycle (S0 → S1, S1 → S2, S2 → S3, and S3,4 → S0) characterized by X-ray absorption spectroscopy at 20 K and room temperature. Biochemistry 44:1894–1908

    Google Scholar 

  • Heisenberg W (1932) Ãœber den Bau der Atomkerne. I. Z Phys 77:1–11

    Article  CAS  Google Scholar 

  • Hillier W, Wydrzynski T (2008) 18O-water exchange in photosystem II: substrate binding and intermediates of the water splitting cycle. Coord Chem Rev 252:306–317

    Article  CAS  Google Scholar 

  • Huynh MHV, Meyer TJ (2007) Proton-coupled electron transfer. Chem Rev 107:5004–5064

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim M, Fransson T, Chatterjee R, Cheah MH, Hussein R, Lassalle L, Sutherlin KD, …, Yano J (2020) Untangling the sequence of events during the S2 → S3 transition in photosystem II and implications for the water oxidation mechanism. Proc Natl Acad Sci U S A 117:12624–12635

    Google Scholar 

  • Isobe H, Soda T, Kitagawa Y, Takano Y, Kawakami T, Yoshioka Y, Yamaguchi K (2001) EHF theory of chemical reactions V. Nature of manganese–oxygen bonds by hybrid density functional theory (DFT) and coupled-cluster (CC) methods. Int J Quant Chem 85:34–43

    Article  CAS  Google Scholar 

  • Isobe H, Shoji M, Koizumi K, Kitagawa Y, Yamanaka S, Kuramitsu S, Yamaguchi K (2005) Electronic and spin structures of manganese clusters in the photosynthesis II system. Polyhedron 24:2767–2777

    Article  CAS  Google Scholar 

  • Isobe H, Shoji M, Yamanaka S, Umena Y, Kawakami K, Kamiya N, Shen J-R, Yamaguchi K (2012) Theoretical illumination of water-inserted structures of the CaMn4O5 cluster in the S2 and S3 states of oxygen-evolving complex of photosystem II: full geometry optimizations by B3LYP hybrid density functional. Dalton Trans 41:13727–13740

    Article  CAS  PubMed  Google Scholar 

  • Isobe H, Shoji M, Yamanaka S, Mino H, Umena Y, Kawakami K, Kamiya N, …, Yamaguchi K (2014) Generalized approximate spin projection calculations of effective exchange integrals of the CaMn4O5 cluster in the S1 and S3 states of the oxygen evolving complex of photosystem II. Phys Chem Chem Phys 16:11911–11923

    Google Scholar 

  • Isobe H, Shoji M, Shen JR, Yamaguchi K (2016) Chemical equilibrium models for the S3 state of the oxygen-evolving complex of photosystem II. Inorg Chem 55:502–511

    Article  CAS  PubMed  Google Scholar 

  • Isobe H, Shoji M, Suzuki T, Shen J-R, Yamaguchi K (2019) Spin, valence, and structural isomerism in the S3 state of the oxygen-evolving complex of photosystem II as a manifestation of multimetallic cooperativity. J Chem Theory Comput 15:2375–2391

    Article  CAS  PubMed  Google Scholar 

  • Iwata S, Barber J (2004) Structure of photosystem II and molecular architectture of the oxygen-evolving Centre. Curr Opin Struct Biol 14:447–453

    Article  CAS  PubMed  Google Scholar 

  • Joliot P, Barbieri G, Chabaud R (1969) Un nouveau modele des centres photochimiques du systeme 2. Photochem Photobiol 10:309–329

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kammel M, Kern J, Lubitz W, Bittl R (2003) Photosystem II single crystals studied by transient EPR: the light-induced triplet state. Biochim Biophys Acta 1605:47–54

    Article  CAS  PubMed  Google Scholar 

  • Kanda K, Yamanaka S, Saito T, Kawakami T, Kitagawa Y, Okumura M, Nakamura H, Yamaguchi K (2011a) Ab initio study of magnetic interactions of manganese-oxide clusters. Polyhedron 30:3256–3261

    Article  CAS  Google Scholar 

  • Kanda K, Yamanaka S, Saito T, Umena Y, Kawakami K, Shen J-R, Kamiya N, …, Yamaguchi K (2011b) Labile electronic and spin states of the CaMn4O5 cluster in the PSII system refined to the 1.9 Ã… X-ray resolution. UB3LYP computational results. Chem Phys Lett 506:98–103

    Google Scholar 

  • Karplus M (2006) Spinach on the ceiling: a theoretical chemist’s return to biology. Annu Rev Biophys Biomol Struct 35:1–47

    Article  CAS  PubMed  Google Scholar 

  • Kawashima K, Takaoka T, Kimura H, Saito K, Ishikita H (2018) O2 evolution and recovery of the water-oxidizing enzyme. Nat Commun 9:1247

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kern J, Alonso-Mori R, Tran R, Hattne J, Gildea RJ, Echols N, Glöckner C, …, Yano J (2013) Simultaneous femtosecond X-ray spectroscopy and diffraction of photosystem II at room temperature. Science 340:491–495

    Google Scholar 

  • Kern J, Chatterjee R, Young ID, Fuller FD, Lassalle L, Ibrahim M, Gul S, …, Yachandra VK (2018) Structures of the intermediates of Kok’s photosynthetic water oxidation clock. Nature 563:421–425

    Google Scholar 

  • Kim DH, Britt RD, Klein MP, Sauer K (1992) The manganese site of the photosynthetic oxygen-evolving complex probed by EPR spectroscopy of oriented photosystem II membranes: the g = 4 and g = 2 multiline signals. Biochemistry 31:541–547

    Article  CAS  PubMed  Google Scholar 

  • Koizumi K, Shoji M, Nishiyama Y, Maruno Y, Kitagawa Y, Soda K, Yamanaka S, …, Yamaguchi K (2004) The electronic structure and magnetic property of metal-oxo, porphyrin manganese-oxo, and μ-oxo-bridged manganese porphyrin dimer. Int J Quant Chem 100:943–956

    Google Scholar 

  • Kok B, Forbush B, McGloin M (1970) Cooperation of charges in photosynthetic O2 evolution. I. A linear four step mechanism. Photochem Photobiol 11:457–475

    Article  CAS  PubMed  Google Scholar 

  • Krewald V, Retegan M, Cox N (2015) Metal oxidation states in biological water splitting. Chem Sci 6:1676–1695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kulik LV, Epel B, Lubitz W, Messinger J (2005a) 55Mn pulse ENDOR at 34 GHz of the S0 and S2 states of the oxygen-evolving complex in photosystem II. J Am Chem Soc 127:2392–2393

    Article  CAS  PubMed  Google Scholar 

  • Kulik LV, Epel B, Messinger J, Lubitz W (2005b) Pulse EPR, 55Mn-ENDOR and ELDOR-detected NMR of the S2-state of the oxygen evolving complex in photosystem II. Photosynth Res 84:347–353

    Article  CAS  PubMed  Google Scholar 

  • 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 129:13421–13435

    Article  CAS  PubMed  Google Scholar 

  • Kupitz C, Basu S, Grotjohann I, Fromme R, Zatsepin NA, Rendek KN, Hunter MS, …, Fromme P (2014) Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature 513:261–265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kusunoki M (2007) Mono manganese mechanism of the photosystem II water splitting reaction by a unique Mn4 cluster. Biochim Biophys Acta 1767:484–492

    Article  CAS  PubMed  Google Scholar 

  • Kuzek D, Pace RJ (2001) Probing the Mn oxidation states in the OEC: insights from spectroscopic, computational and kinetic data. Biochim Biophys Acta 1503:123–137

    Article  CAS  PubMed  Google Scholar 

  • Levitt M (2001) The birth of computational structural biology. Nat Struct Biol 8:392–393

    Article  CAS  PubMed  Google Scholar 

  • Lewis NS, Nocera DG (2006) Powering the planet: chemical challenges in solar energy utilization. Proc Natl Acad Sci U S A 103:15729–15735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Limburg J, Vrettos JS, Liable-Sands LM, Rheingold AL, Crabtree RH, Brudvig GW (1999) A functional model for O-O bond formation by the O2-evolving complex in photosystem II. Science 283:1524–1527

    Article  CAS  PubMed  Google Scholar 

  • Lorigan GA, Britt RD (1994) Temperature-dependent pulsed electron paramagnetic resonance studies of the S2 state multiline signal of the photosynthetic oxygen-evolving complex. Biochemistry 33:12072–12076

    Article  CAS  PubMed  Google Scholar 

  • Lubitz W, Chrysina M, Cox N (2019) Water oxidation in photosystem II. Photosynth Res 142:105–125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McEvoy JP, Brudvig GW (2006) Water-splitting chemistry of photosystem II. Chem Rev 106:4455–4483

    Article  CAS  PubMed  Google Scholar 

  • Messinger J, Badger M, Wydrzynski T (1995) Detection of one slowly exchanging substrate water molecule in the S3 state of photosystem II. Proc Natl Acad Sci U S A 92:3209–3213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Messinger J, Robblee JH, Bergmann U, Fernandez C, Glatzel P, Visser H, Cinco RM, …, Yachandra VK (2001) Absence of Mn-centered oxidation in the S2 → S3 transition: implications for the mechanism of photosynthetic water oxidation. J Am Chem Soc 123:7804–7820

    Google Scholar 

  • Mino H, Nagashima H (2020) Orientation of ligand field for dangling manganese in photosynthetic oxygen evolving complex of photosystem II. J Phys Chem B 124:128–133

    Article  CAS  PubMed  Google Scholar 

  • Miyagawa K, Kawakami T, Isobe H, Shoji M, Yamanaka S, Nakatani K, Okumura M, …, Yamaguchi K (2019) Domain-based local pair natural orbital CCSD(T) calculations of six different S1 structures of oxygen evolving complex of photosystem II: proposal of multi-intermediate models for the S1 state. Chem Phys Lett 732:136660

    Google Scholar 

  • Naruta Y, Sasayama M, Sasaki T (1994) Oxygen evolution by oxidation of water with manganese porphyrin dimers. Angew Chem Int Ed 33:1839–1841

    Article  Google Scholar 

  • Nilsson H, Rappaport F, Boussac A, Messinger J (2014) Substrate–water exchange in photosystem II is arrested before dioxygen formation. Nat Commun 5:4305

    Article  CAS  PubMed  Google Scholar 

  • Noguchi T (2008) FTIR detection of water reactions in the oxygen-evolving Centre of photosystem II. Phil Trans R Soc B 363:1189–1195

    Article  CAS  PubMed  Google Scholar 

  • 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 51:3205–3214

    Article  CAS  PubMed  Google Scholar 

  • Pace RJ, Jin L, Stranger R (2012) What spectroscopy reveals concerning the Mn oxidation levels in the oxygen evolving complex of photosystem II: X-ray to near infra-red. Dalton Trans 41:11145–11160

    Article  CAS  PubMed  Google Scholar 

  • 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 51:9935–9940

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Peloquin JM, Campbell KA, Randall DW, Evanchik MA, Pecoraro VL, Armstrong WH, Britt RD (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 122:10926–10942

    Article  CAS  Google Scholar 

  • Peterson S, Ã…hrling KA, Styring S (1999) The EPR signals from the S0 and S2 states of the Mn cluster in photosystem II relax differently. Biochemistry 38:15223–15230

    Google Scholar 

  • Petrie S, Stranger R, Pace RJ (2017) Rationalizing the 2.25Ã… resolution crystal structure of the water oxidising complex of photosystem II in the S3 state. Chem Phys Chem 18:2924–2931

    Article  CAS  PubMed  Google Scholar 

  • Petrie S, Stranger R, Pace RJ (2018) Explaining the different geometries of the water oxidising complex in the nominal S3 state crystal structures of photosystem II at 2.25Ã… and 2.35Ã…. Chem Phys Chem 19:3296–3309

    Article  CAS  Google Scholar 

  • Pizarro SA, Glatzel P, Visser H, Robblee JH, Christou G, Bergmann U, Yachandra VK (2004) Mn oxidation states in tri- and tetra-nuclear Mn compounds structurally relevant to photosystem II: Mn K-edge X-ray absorption and Kβ X-ray emission spectroscopy studies. Phys Chem Chem Phys 6:4864–4870

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pollock CJ, Delgado-Jaime MU, Atanasov M, Neese F, DeBeer S (2014) Kβ mainline X-ray emission spectroscopy as an experimental probe of metal–ligand covalency. J Am Chem Soc 136:9453–9463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pushkar Y, Yano J, Glatzel P, Messinger J, Lewis A, Sauer K, Bergmann U, Yachandra V (2006) Structure and orientation of the Mn4Ca cluster in plant photosystem II membranes studied by polarized range-extended X-ray absorption spectroscopy. J Biol Chem 282:7198–7208

    Article  PubMed  CAS  Google Scholar 

  • 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 9:3525–3531

    Article  CAS  PubMed  Google Scholar 

  • Rapatskiy L, Cox N, Savitsky A, Ames WM, Sander J, Nowaczyk MM, Rögner M, …, Lubitz W (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 134:16619–16634

    Article  CAS  PubMed  Google Scholar 

  • Rappaport F, Lavergne J (2001) Coupling of electron and proton transfer in the photosynthetic water oxidase. Biochim Biophys Acta 1503:246–259

    Article  CAS  PubMed  Google Scholar 

  • Rappaport F, Blanchard-Desce M, Lavergne J (1994) Kinetics of electron transfer and electrochromic change during the redox transitions of the photosynthetic oxygen-evolving complex. Biochim Biophys Acta 1184:178–192

    Article  CAS  Google Scholar 

  • Razeghifard MR, Pace RJ (1999) EPR kinetic studies of oxygen release in thylakoids and PSII membranes: a kinetic intermediate in the S3 to S0 transition. Biochemistry 38:1252–1257

    Article  CAS  PubMed  Google Scholar 

  • Renger G (2012) Mechanism of light induced water splitting in photosystem II of oxygen evolving photosynthetic organisms. Biochim Biophys Acta 1817:1164–1176

    Article  CAS  PubMed  Google Scholar 

  • 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 1503:7–23

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruettinger WF, Ho DM, Dismukes GC (1999) Protonation and dehydration reactions of the Mn4O4L6 cubane and synthesis and crystal structure of the oxidized cubane [Mn4O4L6]+: a model for the photosynthetic water oxidizing complex. Inorg Chem 38:1036–1037

    Article  CAS  PubMed  Google Scholar 

  • Saito T, Yamanaka S, Kanda K, Isobe H, Takano Y, Shigeta Y, Umena Y, …, Yamaguchi K (2012) Possible mechanisms of water splitting reaction based on proton and electron release pathways revealed for CaMn4O5 cluster of PSII refined to 1.9 Ã… resolutions. Int J Quant Chem 112: 253–276

    Article  CAS  Google Scholar 

  • Sauer K, Yano J, Yachandra VK (2008) X-ray spectroscopy of the photosynthetic oxygen-evolving complex. Coord Chem Rev 252:318–335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shoji M, Isobe H, Yamanaka S, Umena Y, Kawakami K, Kamiya N, Shen J-R, Yamaguchi K (2013) Theoretical insight in to hydrogen-bonding networks and proton wire for the CaMn4O5 cluster of photosystem II: elongation of Mn–Mn distances with hydrogen bonds. Cat Sci Technol 3:1831–1848

    Article  CAS  Google Scholar 

  • Shoji M, Isobe H, Yamanaka S, Umena Y, Kawakami K, Kamiya N, Shen J-R, …, Yamaguchi K (2015a) Large-scale QM/MM calculations of hydrogen bonding networks for proton transfer and water inlet channels for water oxidation: theoretical system models of the oxygen-evolving complex of photosystem II. Adv Quant Chem 70:325–413

    Article  CAS  Google Scholar 

  • Shoji M, Isobe H, Yamaguchi K (2015b) QM/MM study of the S2 to S3 transition in the oxygen-evolvin complex of photosystem II. Chem Phys Lett 636:172–179

    Article  CAS  Google Scholar 

  • Shoji M, Isobe H, Nakajima T, Shigeta Y, Suga M, Akita F, Shen J-R, Yamaguchi K (2017) Large-scale QM/MM calculations of the CaMn4O5 cluster in the S3 state of the oxygen evolving complex of photosystem II: comparison between water-inserted and no water-inserted structures. Faraday Discuss 198:83–106

    Article  CAS  PubMed  Google Scholar 

  • Shoji M, Isobe H, Shigeta Y, Nakajima T, Yamaguchi K (2018a) Nonadiabatic one-electron transfer mechanism for the O–O bond formation in the oxygen-evolving complex of photosystem II. Chem Phys Lett 698:138–146

    Article  CAS  Google Scholar 

  • Shoji M, Isobe H, Shigeta Y, Nakajima T, Yamaguchi K (2018b) 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 B 122:6491–6502

    Article  CAS  PubMed  Google Scholar 

  • Shoji M, Isobe H, Miyagawa K, Yamaguchi K (2019a) Possibility of the right-opened Mn-oxo intermediate (R-oxo(4444)) among all nine intermediates in the S3 state of the oxygen-evolving complex of photosystem II revealed by large-scale QM/MM calculations. Chem Phys 518:81–90

    Article  CAS  Google Scholar 

  • Shoji M, Isobe H, Yamanaka S, Umena Y, Kawakami K, Kamiya N, Yamaguchi K (2019b) Theoretical elucidation of geometrical structures of the CaMn4O5 cluster in oxygen evolving complex of photosystem II: scope and applicability of estimation formulae of structural deformations via the mixed-valence and Jahn–Teller effects. Adv Quant Chem 78:307–451

    Article  CAS  Google Scholar 

  • Shoji M, Isobe H, Yamaguchi K (2019c) Concerted bond switching mechanism coupled with one-electron transfer for the oxygen-oxygen bond formation in the oxygen-evolving complex of photosystem II. Chem Phys Lett 714:219–226

    Article  CAS  Google Scholar 

  • Siegbahn PEM (2009) Structures and energetics for O2 formation in photosystem II. Acc Chem Res 42:1871–1880

    Article  CAS  PubMed  Google Scholar 

  • Siegbahn PEM (2013a) Substrate water exchange for the oxygen evolving complex in PSII in the S1, S2, and S3 states. J Am Chem Soc 135:9442–9449

    Article  CAS  PubMed  Google Scholar 

  • Siegbahn PEM (2013b) Water oxidation mechanism in photosystem II, including oxidations, proton release pathways, O–O bond formation and O2 release. Biochim Biophys Acta 1827:1003–1019

    Article  CAS  PubMed  Google Scholar 

  • Soda T, Kitagawa Y, Onishi T, Takano Y, Shigeta Y, Nagao H, Yoshioka Y, Yamaguchi K (2000) Ab initio computations of effective exchange integrals for H–H, H–He–H and Mn2O2 complex: comparison of broken-symmetry approaches. Chem Phys Lett 319:223–230

    Article  CAS  Google Scholar 

  • 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 130:3428–3442

    Article  CAS  PubMed  Google Scholar 

  • Suga M, Akita F, Hirata K, Ueno G, Murakami H, Nakajima Y, Shimizu T, …, Shen J-R (2015) Native structure of photosystem II at 1.95 Ã… resolution viewed by femtosecond X-ray pulses. Nature 517:99–103

    Article  CAS  PubMed  Google Scholar 

  • Suga M, Akita F, Sugahara M, Kubo M, Nakajima Y, Nakane T, Yamashita K, …, Shen J-R (2017) Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL. Nature 543:131–135

    Article  CAS  PubMed  Google Scholar 

  • Suga M, Akita F, Yamashita K, Nakajima Y, Ueno G, Li H, Yamane T, …, Shen J-R (2019) An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser. Science 366:334–338

    Article  CAS  PubMed  Google Scholar 

  • 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 139:1718–1721

    Article  CAS  PubMed  Google Scholar 

  • Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Ã…. Nature 473:55–60

    Article  CAS  PubMed  Google Scholar 

  • Vinyard DJ, Ananyev GM, Dismukes GC (2013) Photosystem II: the reaction center of oxygenic photosynthesis. Annu Rev Biochem 82:577–606

    Article  CAS  PubMed  Google Scholar 

  • Visser H, Anxolabéhère-Mallart E, Bergmann U, Glatzel P, Robblee JH, Cramer SP, Girerd J-J, …, Yachandra VK (2001) Mn K-edge XANES and Kβ XES studies of two Mn−Oxo binuclear complexes: investigation of three different oxidation states relevant to the oxygen-evolving complex of photosystem II. J Am Chem Soc 123:7031–7039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warshel A, Levitt M (1976) Theoretical studies of enzymic reactions: dielectric, electrostatic and steric stabilization of the carbonium ion in the reaction of lysozyme. J Mol Biol 103:227–249

    Article  CAS  PubMed  Google Scholar 

  • Wydrzynski TJ, Satoh K (eds) (2005) Photosystem II: The Light-driven Water: Plastoquinone Oxidoreductase. Springer, Dordrecht

    Google Scholar 

  • Wydrzynski T, Ã…ngström J, VänngÃ¥rd T (1989) H2O2 formation by photosystem II. Biochim Biophys Acta 973:23–28

    Article  CAS  Google Scholar 

  • Yachandra VK, Sauer K, Klein MP (1996) Manganese cluster in photosynthesis: where plants oxidize water to dioxygen. Chem Rev 96:2927–2950

    Article  CAS  PubMed  Google Scholar 

  • Yamaguchi K (1974) Selection rule in free radical reactions. Chem Phys Lett 28:93–97

    Article  CAS  Google Scholar 

  • Yamaguchi K (1975a) The electronic structures of biradicals in the unrestricted Hartree-Fock approximation. Chem Phys Lett 33:330–335

    Article  CAS  Google Scholar 

  • Yamaguchi K (1975b) General spin structures of organic radicals. Chem Phys Lett 30:288–292

    Article  CAS  Google Scholar 

  • Yamaguchi K (1990) Instability in chemical bonds. In: Carbó R, Klobukowski M (eds) Self-Consistent Field: Theory and Applications. Elsevier, Amsterdam, pp 727–823

    Google Scholar 

  • Yamaguchi K, Takahara Y, Fueno T (1986) Ab-initio molecular orbital studies of structure and reactivity of transition metal OXO compounds. In: Smith VH Jr, Schaefer HF III, Morokuma K (eds) Applied Quantum Chemistry. D Reidel Pub Com, Lancaster, pp 155–184

    Chapter  Google Scholar 

  • Yamaguchi K, Tsunekawa T, Toyoda Y, Fueno T (1988) Ab initio molecular orbital calculations of effective exchange integrals between transition metal ions. Chem Phys Lett 143:371–376

    Article  CAS  Google Scholar 

  • Yamaguchi K, Yamanaka S, Nishino M, Takano Y, Kitagawa Y, Nagao H, Yoshioka Y (1999) Symmetry and broken symmetries in molecular orbital descriptions of unstable molecules II. Alignment, flustration and tunneling of spins in mesoscopic molecular magnets. Theor Chem Accounts 102:328–345

    Article  CAS  Google Scholar 

  • Yamaguchi K, Yamanaka S, Isobe H, Shoji M, Koizumi K, Kitagawa Y, Kawakami T, Okumura M (2007) Theory of chemical bonds in metalloenzymes VI: manganese–oxo bonds in the photosynthesis II system. Polyhedron 26:2216–2224

    Article  CAS  Google Scholar 

  • Yamaguchi K, Shoji M, Saito T, Isobe H, Nishihara S, Koizumi K, Yamada S, …, Okumura M (2010) Theory of chemical bonds in metallo-enzymes XV. Local singlet and triplet diradical mechanisms for radical coupling reactions in the oxygen evolving complex. Int J Quant Chem 110:3101–3128

    Article  CAS  Google Scholar 

  • Yamaguchi K, Isobe H, Yamanaka S, Saito T, Kanda K, Shoji M, Umena Y, …, Okumura M (2013) Full geometry optimizations of the mixed-valence CaMn4O4X(H2O)4 (X=OH or O) cluster in OEC of PS II: degree of symmetry breaking of the labile Mn-X-Mn bond revealed by several hybrid DFT calculations. Int J Quant Chem 113:525–541

    Article  CAS  Google Scholar 

  • Yamaguchi K, Yamanaka S, Shoji M, Isobe H, Kitagawa Y, Kawakami T, Yamada S, Okumura M (2014) Theory of chemical bonds in metalloenzymes XIX: labile manganese oxygen bonds of the CaMn4O5 cluster in oxygen evolving complex of photosystem II. Mol Phys 112:485–507

    Article  CAS  Google Scholar 

  • Yamaguchi K, Isobe H, Shoji M, Yamanaka S, Okumura M (2016) Theory of chemical bonds in metalloenzymes XX: magneto-structural correlations in the CaMn4O5 cluster in oxygen-evolving complex of photosystem II. Mol Phys 114:519–546

    CAS  Google Scholar 

  • Yamaguchi K, Shoji M, Isobe H, Yamanaka S, Umena Y, Kawakami K, Kamiya N (2017) On the guiding principles for understanding of geometrical structures of the CaMn4O5 cluster in oxygen-evolving complex of photosystem II: proposal of estimation formula of structural deformations via the Jahn–Teller effects. Mol Phys 115:636–666

    Article  CAS  Google Scholar 

  • Yamaguchi K, Shoji M, Isobe H, Miyagawa K, Nakatani K (2019a) Theory of chemical bonds in metallo-enzymes 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 117:2320–2354

    Article  CAS  Google Scholar 

  • Yamaguchi K, Yamanaka S, Isobe H, Shoji M, Miyagawa K, Nakajima T, Kawakami T, Okumura M (2019b) Theoretical and computational investigations of geometrical, electronic and spin structures of the CaMn4OX (X = 5, 6) cluster in the Kok cycle Si (i = 0–3) of oxygen evolving complex of photosystem II. Physiol Plant 166:44–59

    Article  CAS  PubMed  Google Scholar 

  • Yamanaka S, Takeda R, Yamaguchi K (2003) Density functional study of tetrahedral manganese clusters. Polyhedron 22:2013–2017

    Article  CAS  Google Scholar 

  • Yamanaka S, Isobe H, Kanda K, Saito T, Umena Y, Kawakami K, Shen J-R, …, Yamaguchi K (2011) Possible mechanisms for the O–O bond formation in oxygen evolution reaction at the CaMn4O5(H2O)4 cluster of PSII refined to 1.9 Ã… X-ray resolution. Chem Phys Lett 511:138–145

    Article  CAS  Google Scholar 

  • Yamanaka S, Kanda K, Saito T, Umena Y, Kawakami K, Shen J-R, Kamiya N, …, Yamaguchi K (2012a) Electronic and spin structures of the CaMn4O5(H2O)4 cluster in OEC of PSII refined to 1.9 Ã… X-ray resolution. Adv Quant Chem 64:121–187

    Article  CAS  Google Scholar 

  • Yamanaka S, Saito T, Kanda K, Isobe H, Umena Y, Kawakami K, Shen J-R, …, Yamaguchi K (2012b) Structure and reactivity of the mixed-valence CaMn4O5(H2O)4 and CaMn4O4 (OH) (H2O)4 clusters at oxygen evolution complex of photosystem II. Hybrid DFT (UB3LYP and UBHandHLYP) calculations. Int J Quant Chem 112:321–343

    Article  CAS  Google Scholar 

  • Yamauchi T, Mino H, Matsukawa T, Kawamori A, Ono T (1997) Parallel polarization electron paramagnetic resonance studies of the S1-state manganese cluster in the photosynthetic oxygen-evolving system. Biochemistry 36:7520–7526

    Article  CAS  PubMed  Google Scholar 

  • Yano J, Yachandra V (2014) Mn4Ca cluster in photosynthesis: where and how water is oxidized to dioxygen. Chem Rev 114:4175–4205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yano J, Kern J, Irrgang K-D, Latimer MJ, Bergmann U, Glatzel P, Pushkar Y, …, Yachandra VK (2005a) X-ray damage to the Mn4Ca complex in single crystals of photosystem II: a case study for metalloprotein crystallography. Proc Natl Acad Sci U S A 102:12047–12052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yano J, Pushkar Y, Glatzel P, Lewis A, Sauer K, Messinger J, Bergmann U, Yachandra V (2005b) High-resolution Mn EXAFS of the oxygen-evolving complex in photosystem II: structural implications for the Mn4Ca cluster. J Am Chem Soc 127:14974–14975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshikawa S, Shimada A (2015) Reaction mechanism of cytochrome c oxidase. Chem Rev 115:1936–1989

    Article  CAS  PubMed  Google Scholar 

  • Yoshimori A (1959) A new type of antiferromagnetic structure in the rutile type crystal. J Phys Soc Jpn 14:807–821

    Article  Google Scholar 

  • Young ID, Ibrahim M, Chatterjee R, Gul S, Fuller FD, Koroidov S, Brewster, AS, …, Yano J (2016) Structure of photosystem II and substrate binding at room temperature. Nature 540:453–457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang B, Daniel Q, Fan L, Liu T, Meng Q, Sun L (2018) Identifying MnVII oxo species during electrochemical water oxidation by manganese oxide. iScience 4:144–152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zouni A, Witt H-T, Kern J, Fromme P, Krauss N, Saenger W, Orth P (2001) Crystal structure of photosystem II from synechococcus elongatus at 3.8 Ã… resolution. Nature 409:739–743

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kizashi Yamaguchi .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2021 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Yamaguchi, K., Yamanaka, S., Isobe, H., Shoji, M., Kawakami, T., Miyagawa, K. (2021). Mechanism of Water Oxidation in Photosynthesis Elucidated by Interplay Between Experiment and Theory. In: Shen, JR., Satoh, K., Allakhverdiev, S.I. (eds) Photosynthesis: Molecular Approaches to Solar Energy Conversion. Advances in Photosynthesis and Respiration, vol 47. Springer, Cham. https://doi.org/10.1007/978-3-030-67407-6_2

Download citation

Publish with us

Policies and ethics