The oxygen-evolving complex of chloroplast membranes

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Abstract

The oxygen-evolving complex (OEC) of plants is the main energy-transforming structure of chloroplast membranes, in which light energy is used for photosynthetic oxidation of intracellular water and oxygen formation. The conducted research has resulted in isolation of functionally active OEC of higher plants and elucidation of its molecular composition, photochemical properties and structural organization. The OEC has been revealed to represent the dimer of the pigment-lipoprotein complexes of photosystem 2 (PLPC PS-2) associated in a chloroplast membrane according to the mirror symmetry rule into an integrate structure based on hydrophobic bonds. The model has been developed for the structure of the dimeric complex of PS-2 that has the function of oxygen formation. This model was confirmed by the X-ray analysis of crystals of the dimeric complex of PS-2. The concept about the fact that the “hydrophobic boiler” determining the formation of the water-oxidizing center of the OEC is formed in the area of association of the reaction centers of monomeric PLPCs PS-2 was advanced based on the regularities of change in the functional activity of the OEC under the action of stress-factors. The new scheme has been advanced for the two-anode organization of the water-oxidizing center as the main condition for realizing the process of molecular oxygen formation. The mechanism of the process of photosynthetic water oxidation and molecular oxygen formation has been developed based on the experimental data about the structural organization of the OEC and its water-oxidizing center. The quantum-chemical modeling of the process showed that its course corresponds to the mechanism suggested.

Key words

oxygen-evolving complex of chloroplast membranes photosystem 2 water oxidation oxygen formation 

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References

  1. 1.
    Shutilova, N.I., On the Principles of Molecular Organization and Functioning of the Oxygen-Evolving Complex of Chloroplast Photosystem 2, Uspekhi sovremennoi biologii (Rus.), 1999, vol. 119, pp. 42–55.Google Scholar
  2. 2.
    Kutyurin, V.M., On the Mechanism of Water Decomposition in the Process of Photosynthesis, Izv. Akad. Nauk. SSSR, Ser. Biol. (Rus.), 1970, no. 4, pp. 569–580.Google Scholar
  3. 3.
    Vinogradov, A.P. and Teis, R.V., The Isotopic Composition of Oxygen of Different Origin (the Photosynthetic Oxygen, Air Oxygen, CO2, H2O), Dokl. Akad. Nauk SSSR (Rus.), 1941, vol. 33, pp. 496–501.Google Scholar
  4. 4.
    Ruben, S., Randall, M., Kamen, M.D., and Hyde, J.L., Heavy O (O18) as a Tracer in Study of Photosynthesis, J. Am. Chem. Soc. (Rus.), 1941, vol. 63, pp. 877–880.CrossRefGoogle Scholar
  5. 5.
    Shutiliva, N.I., The Oxygen-Evolving Pigment-Lipoprotein Complex of Chloroplast Photosystem 2: Dr. Sci. (Biol.) Disssertation (Rus.), Moscow, Emanuel Institute of Biochemical Physics of the Russian Academy of Sciences, 1997, p. 153.Google Scholar
  6. 6.
    Shutilova, N.I., The Possible Mechanism of Water Oxidation in the Dimeric Oxygen-Evolving Complex (OEC) of Chloroplast Photosystem II, Proc. Internat. Conf. Molecular Biology and Genetics of Photosynthesis, Moscow, Moscow State Univ., pp. 22–23.Google Scholar
  7. 7.
    Shutilova, N.I., On the Mechanism of Photosynthetic Water Oxidation in the Dimeric Oxygen-Evolving Complex of Chloroplast Photosystem II, Biofizika (Rus.), 2000, vol. 45, pp. 51–57.Google Scholar
  8. 8.
    Joliot, P., Barbieri, R., and Chabaud, R., Un nouveau modéle des centres photochimiques du systéme II, Photochem. Photobiol., 1969, vol. 10, pp. 309–329.CrossRefGoogle Scholar
  9. 9.
    Kok, B., Forbush, B., and McGloin, M., The Cooperation of Charges in Photosynthetic O2 Evolution. 1. A Linear Four-Step Mechanism, Photochem. Photobiol., 1970, vol. 11, pp. 457–475.CrossRefPubMedGoogle Scholar
  10. 10.
    Rutherford, A.W., Photosystem II, the Water-Splitting Enzyme, Trends Biochem. Sci., 1989, vol. 14, pp. 227–232.CrossRefPubMedGoogle Scholar
  11. 11.
    Vermaas, W.F.G., Styring, S., Schröder, W.P., and Andersson, B., Photosynthetic Water Oxidation: The Protein Framework, Photosynth. Res., 1993, vol. 38, pp. 249–263.CrossRefGoogle Scholar
  12. 12.
    Debus, R.J., The Manganese and Calcium Ions of Photosynthetic Oxygen Evolution, Biochim. Biophys. Acta, 1992, vol. 1102, pp. 269–352.CrossRefPubMedGoogle Scholar
  13. 13.
    Dau, H. and Haumann, M., Eight Steps Preceding O-O bond Formation in Oxygenic Photosynthesis — A Basic Reaction Cycle of the Photosystem II Manganese Complex, Biochim. Biophys. Acta, 2007, vol. 1767, pp. 472–483.CrossRefPubMedGoogle Scholar
  14. 14.
    Vrettos, J.S., Limberg, J., and Brudvig, G.W., Mechanism of Photosynthetic Water Oxidation: Combining Biophysical Studies of Photosystem II with Inorganic Model Chemistry, Biochim. Biophys. Acta, 2001, vol. 1503, pp. 229–245.CrossRefPubMedGoogle Scholar
  15. 15.
    Messinger, J., 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., 2004, no. 6, pp. 4764–4771.Google Scholar
  16. 16.
    Hiller, W. and Wydrzynski, T., Oxygen Ligand Exchange at Metal Sites-Implications for the O2 Evolving Mechanism of Photosystem II, Biochim. Biophys. Acta., 2001, vol. 1503, pp. 197–209.CrossRefGoogle Scholar
  17. 17.
    Blyumenfeld, L.A., Problemy biologicheskoi fiziki (Problems of Biological Physics), Moscow, Nauka, 1977.Google Scholar
  18. 18.
    Semyonov, N.N., Shilov, A.E., and Likhtenshtein, G.I., Multielectron Processes in Chemistry and Biology, Dokl. Akad. Nauk SSSR (Rus.), 1975, vol. 221, no. 6, pp. 1374–1377.Google Scholar
  19. 19.
    Shutilova, N.I. and Kutyurin, V.M., Isolating and Studying Three Types of Pigment-Lipoprotein Chloroplast Complexes: the Complex Containing the Reaction Center of PS-2, Complex Containing the Reaction Center of PS-2, and Light-Collecting Complex, Fiziologiya Rastenii (Rus.), 1976, vol. 23, pp. 43–49.Google Scholar
  20. 20.
    Shutilova, N.I., Klimov, V.V., Shuvalov, V.A., and Kutyurin, V.M., Researching the Photochemical and Spectral Properties of Subchloroplast PS-2 Fragments Highly Purified from the Admixture of PS-1, Biofizika (Rus.), 1975, vol. 20, pp. 844–847.Google Scholar
  21. 21.
    Shutilova, N.I., Faludi-Daniel, A., and Klimov, V.V., A Rapid Procedure for Isolating the Photosystem II Reaction Centers in a Highly Enriched Form, FEBS Lett., 1982, vol. 138, pp. 255–260.CrossRefGoogle Scholar
  22. 22.
    Berthold, D.A., Babcock, G.T., and Yocum, C.F., A Highly Resolved, Oxygen-Evolving Photosystem II Preparation from Spinach Thylakoid Membranes — EPR and Electron-Transport Properties, FEBS Lett., 1981, vol. 134, pp. 231–234.CrossRefGoogle Scholar
  23. 23.
    Nanba, O. and Satoh, K., Isolation of a Photosystem II Reaction Center Consisting of D-1 and D-2 Polypeptides and Cytochrome b559, Proc. Natl. Acad. Sci. USA, 1987, vol. 84, pp. 109–112.CrossRefPubMedGoogle Scholar
  24. 24.
    Shutilova, N.I., Ananyev, G.M., and Zakrzhevskii, D.A., The Photo-Induced Proton Extraction by the Pigment-Lipoprotein Complex of Photosystem 2 in the Presence of Ferricyanide, Dokl. Akad. Nauk SSSR (Rus.), 1980, vol. 253, pp. 1263–1266.Google Scholar
  25. 25.
    Shutilova, N.I., Kadoshnikova, I.G., Kozlovskaya, N.G., Klevanik, A.V., and Zakrzhevskii, D.A., Optimizing the Conditions of Isolating Three Types of Pigment-Lipoprotein Complexes of Pea Chloroplasts during Solubilization with Triton X-100, Biokhimiya (Rus.), 1979, vol. 44, pp. 1160–1171.Google Scholar
  26. 26.
    Shutilova, N.I., Kadoshnikova, I.G., Smolova, T.N., and Klimov, V.V., The Reactivation of the Oxygen-Evolving Function in Subchloroplast Fragments of Photosystem 2 Washed from Proteins with Molecular Weight of 17, 23, and 33 kDa, Biokhimiya (Rus.), 1987, vol. 52, pp. 1958–1964.Google Scholar
  27. 27.
    Shutilova, N.I., Strizhova, V.P., Khristin, M.S., Antropova, T.M., and Klimov, V.V., Isolating, Stabilizing, and Researching the Oxygen-Evolving Pigment-Lipoprotein Complex of Chloroplast Membrane Photosystem II, Biol. Membrany (Rus.), 1990, vol. 7, pp. 359–367.Google Scholar
  28. 28.
    Shutilova, N.I., Klimov, V.V., Antropova, T.M., and Shnyrov, V.L., On the Mechanism of Thermoinactivation of the Oxygen-Evolving Complex in the Functional Nucleus of Chloroplast Photosystem 2, Biokhimiya (Rus.), 1992, vol. 57, pp. 1508–1518.Google Scholar
  29. 29.
    Shutilova, N.I., Semenova, D.A., Klimov, V.V., and Shnyrov, V.L., Temperature Induced Structural and Functional Transitions in the Oxygen-Evolving Complex of Photosystem II Subchloroplast Preparations, Biochem. Mol. Biol. Internat, 1995, vol. 35, pp. 1233–1243.Google Scholar
  30. 30.
    Semenova, G.A. and Shutilova, N.I., The Influence of Storage on the Structure, Functional Activity, and Changes in the Lipid Composition of Chloroplasts at Low Positive Temperatures, Biol. Membrany (Rus.), 1996, vol. 13, pp. 138–145.Google Scholar
  31. 31.
    Zouni, A., Witt, H., Kern, J., Fromme, P., Kraub, N., Saenger, W., and Orth, P., Crystal Structure of Photosystem II from Synechococcus Elongatus at 3.8 Å Resolution, Nature, 2001, vol. 409, pp. 739–743.CrossRefPubMedGoogle Scholar
  32. 32.
    Ferreira, K.N., Iverson, T.M., Maghaoui, K., Barber, J., and Iwata, S., Architecture of the Photosynthetic Oxygen-Evolving Center, Science, 2004, vol. 303, pp. 1831–1838.CrossRefPubMedGoogle Scholar
  33. 33.
    Loll, B., Kern, J., Saenger, W., Zouni, A., and Biesiadka, J., Towards Complete Cofactor Arrangement in the 3.0, Nature, 2005, vol. 438, pp. 1040–1044.CrossRefPubMedGoogle Scholar
  34. 34.
    Riznichenko, G.Yu., Belyaeva, N.E., Kovalenko, I.B., and Rubin, A.B., The Mathematical and Computer Modeling of Primary Photosynthetic Processes, Biofizika (Rus.), 2009, vol. 54,issue 1, pp. 16–33.Google Scholar
  35. 35.
    Shutilova, N.I., The Molecular Mechanisms of the Inhibitory Action of Heavy Metals on the Oxygen-Evolving Complex of Chloroplast Membranes, Biol. membrany (Rus.), 2006, vol. 23, pp. 355–363.Google Scholar
  36. 36.
    Laikov, D.N., Fast Evaluation of Density Functional Exchange-Correlation Terms Using the Expansion of the Electron Density in Auxiliary Basis Sets, Chem. Phys. Lett., 1997, vol. 281, nos. 1–3, pp. 151–156.CrossRefGoogle Scholar
  37. 37.
    Takahashi, T., Inoue-Kashino, N., Ozawa, S., Takahashi, Y., Kashino, Y., and Satoh, K., Photosystem II Complex in vivo is a Monomer, J. Biol. Chem., 2009, vol. 284, pp. 15598–15606.CrossRefPubMedGoogle Scholar
  38. 38.
    Barber, J., Photosystem II: the Engine of Life, Q. Rev. Biophys., 2003, vol. 36, pp. 71–89.CrossRefPubMedGoogle Scholar

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© Pleiades Publishing, Ltd. 2010

Authors and Affiliations

  1. 1.Institute of Fundamental Problems of BiologyRussian Academy of SciencesPushchino, Moscow oblastRussia

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