Photosynthesis Research

, Volume 84, Issue 1–3, pp 325–331 | Cite as

Considerations on the mechanism of photosynthetic water oxidation – dual role of oxo-bridges between Mn ions in (i) redox-potential maintenance and (ii) proton abstraction from substrate water



Two mechanistic problems of photosynthetic water oxidation at the Mn complex of Photosystem II (PS II) are considered. (I) In the four Mn-oxidizing transitions, any pure Mn oxidation is predicted to cause an increase in redox potential that renders subsequent oxidation steps impossible (redox-potential problem). Formation of unprotonated oxo-bridges may counteract the potential increase. (II) The O–O formation step without any high-pK bases acting as proton acceptors is energetically unfavorable (acceptor-base problem). The pK of oxides in a bridging position between Mn ions may increase drastically upon reduction of Mn in the water-oxidation step (>10 units), thus rendering them favorable proton acceptors. It is proposed that in PS II, in the course of the four oxidizing transitions at least two unprotonated oxo-bridges are formed. Thereby (i) a redox potential increase is prevented and (ii) proton acceptors are prepared for the O–O formation step. Water oxidation in the O–O bond formation step is facilitated by simultaneous Mn reduction and proton transfer to bridging oxides amounting to hydrogen atom or hydride transfer from substrate water to the Mn-oxo core of the Mn complex of PS II.


manganese complex oxygen evolution Photosystem II X-ray absorption spectroscopy 



electron paramagnetic resonance


extended X-ray absorption fine-structure




Tyr 161 of the D1 protein of PS II


X-ray absorption near-edge structure


X-ray absorption spectroscopy


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ahlbrink, R, Haumann, M, Cherepanov, D, Boegershausen, O, Mulkidjanian, A, Junge, W 1998Function of tyrosine-Z in water oxidation by Photosystem II: electrostatical promotor instead of hydrogen abstractorBiochemistry3711311142PubMedGoogle Scholar
  2. Baldwin, MJ, Pecoraro, VL 1996Energetics of proton-coupled electron transfer in high-valent Mn2(μ-O)2 systems: models for water oxidation by the oxygen-evolving complex of Photosystem IIJ Am Chem Soc1181132511326CrossRefGoogle Scholar
  3. Bernat, G, Morvaridi, F, Feyziyev, Y, Styring, S 2002pH-dependence of the four individual transitions in the catalytic S-cycle during photosynthetic oxygen evolutionBiochemistry4158305843PubMedGoogle Scholar
  4. Caudle, MT, Pecoraro, VL 1997Thermodynamic viability of hydrogen atom transfer from water coordinated to the oxygen-evolving complex of Photosystem IIJ Am Chem Soc11934153416CrossRefGoogle Scholar
  5. Clausen, J, Junge, W 2004Detection of an intermediate of photosynthetic water oxidationNature430480483PubMedGoogle Scholar
  6. Dau, H, Iuzzolino, L, Dittmer, J 2001The tetra-manganese complex of Photosystem II during its redox cycle X-ray absorption results and mechanistic implicationsBiochim Biophys Acta15032439PubMedGoogle Scholar
  7. Dau, H, Liebisch, P, Haumann, M 2003X-ray absorption spectroscopy to analyze nuclear geometry and electronic structure of biological metal centers – potential and questions examined with special focus on the tetra-nuclear manganese complex of oxygenic photosynthesisAnal Bioanal Chem376562583PubMedGoogle Scholar
  8. Dau H, Liebisch P and Haumann M (2005a) 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 Scripta, in pressGoogle Scholar
  9. Dau, H, Liebisch, P, Haumann, M 2005bThe structure of the manganese complex of Photosystem II in its dark-stable S1-state – EXAFS results in relation to recent crystallographic dataPhys Chem Chem Phys647814792CrossRefGoogle Scholar
  10. Paula, JC, Innes, JB, Brudvig, GW 1985Electron transfer in Photosystem II at cryogenic temperaturesBiochemistry2481148120PubMedGoogle Scholar
  11. Goodson, PA, Glerup, J, Hodgson, DJ, Michelsen, K, Pedersen, E 1990Binuclear bis(μ-oxo)dimanganese(III,IV) and -(IV,IV) complexes with N,N’-bis(2-pyridylmethyl)-1, 2-ethanediamineInorg Chem29503508CrossRefGoogle Scholar
  12. Haumann, M, Junge, W 1994Extent and rate of proton release by photosynthetic water oxidation in thylakoids: electrostatic relaxation versus chemical productionBiochemistry33864872PubMedGoogle Scholar
  13. Haumann, M, Junge, W 1996Protons and charge indicators in oxygen evolutionOrt, DYocum, CF eds. Oxygenic Photosynthesis – The Light ReactionsKluwer Academic PublishersDordrecht165192Google Scholar
  14. Haumann, M, Grabolle, M, Neisius, T, Dau, H 2002The first room-temperature X-ray absorption spectra of higher oxidation states of the tetra-manganese complex of Photosystem IIFEBS Lett512116120PubMedGoogle Scholar
  15. Haumann M, Müller C, Liebisch P, Iuzzolino L, Dittmer J, Grabolle M, Neisius T, Meyer-Klaucke W and 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 → S3,4, S0) characterized by X-ray absorption spectroscopy at 20K as well as at room temperature. Biochemistry (E-pub ahead of print)Google Scholar
  16. Hendry, G, Wydrzynski, T 2002The two substrate-water molecules are already bound to the oxygen-evolving complex in the S2-state of Photosystem IIBiochemistry411332813334PubMedGoogle Scholar
  17. Hoganson, CW, Babcock, GT 1997A metalloradical mechanism for the generation of oxygen from water in photosynthesisScience27719531956PubMedGoogle Scholar
  18. Huang P, Magnuson A, Lomoth R, Abrahamsson M, Tamm M, Sun L, Rotterdam Bv, Park J, Hammarström L, Åkermark B and Styring S (2002) Photo-induced oxidation of a dinuclear Mn2II,II complex to the Mn2III,IV state by inter- and intramolecular electron transfer to RuIIItris-bipyridine. J Inorg Biochem 91: 159–172Google Scholar
  19. Junge, W, Haumann, M, Ahlbrink, R, Mulkidjanian, A, Clausen, J 2002Electrostatics and proton transfer in photosynthetic water oxidationPhil Trans R Soc London Ser B35714071418CrossRefGoogle Scholar
  20. Krishtalik, LI 1989Energetics of the reaction of photosynthetic evolution of oxygenBiofizika34883886Google Scholar
  21. Lomoth, R, Huang, P, Zheng, J, Sun, L, Hammarström, L, Akermark, B, Styring, S 2002Synthesis and characterization of a dinuclear manganese(III,III) complex with three phenolate ligandsEur J Inorg Chem200229652974CrossRefGoogle Scholar
  22. Nugent JHA (ed) (2001) Biochim et Biophysica Acta 1503 (special issue on Photosynthetic Water Oxidation). Elsevier, AmsterdamGoogle Scholar
  23. Ort D, Yocum CF (1996). Oxygenic Photosynthesis – The Light Reactions. Kluwer Academic Publishers, DordrechtGoogle Scholar
  24. Peloquin, JM, Britt, RD 2001EPR/ENDOR characterization of the physical and electronic structure of the OEC Mn clusterBiochim Biophys Acta150396111PubMedGoogle Scholar
  25. Rappaport, F, Lavergne, J 1991Proton release during successive oxidation steps of the photosynthetic water oxidation process: stoichiometries and pH dependenceBiochemistry301000410012PubMedGoogle Scholar
  26. Rappaport, F, Blanchard-Desce, M, Lavergne, J 1994Kinetics of electron transfer and electrochromic change during the redox transition of the photosynthetic oxygen-evolving complexBiochim Biophys Acta1184178192Google Scholar
  27. Razeghifard, MR, Pace, RJ 1999EPR kinetic studies of oxygen release in thylakoids and PS II membranes: an intermediate in the S3 to S0 transitionBiochemistry3812521257PubMedGoogle Scholar
  28. Robblee, JH, Cinco, RM, Yachandra, VK 2001X-ray spectroscopy-based structure of the Mn cluster and mechanism of photosynthetic oxygen evolutionBiochim Biophys Acta1503723PubMedGoogle Scholar
  29. Schlodder, E, Witt, HT 1999Stoichiometry of proton release from the catalytic center in photosynthetic water oxidation. Reexamination by a glass electrode study at pH 5.5–7.2J Biol Chem2743038730392PubMedGoogle Scholar
  30. Vrettos, JS, Limburg, J, Brudvig, GW 2001Mechanism of photosynthetic water oxidation: combining biophysical studies of Photosystem II with inorganic model chemistryBiochim Biophys Acta1503229245PubMedGoogle Scholar

Copyright information

© Springer 2005

Authors and Affiliations

  1. 1.Freie Universität BerlinBerlinGermany

Personalised recommendations