A metalloradical mechanism for the generation of oxygen from water in photosynthesis.

In plants and algae, photosystem II uses light energy to oxidize water to oxygen at a metalloradical site that comprises a tetranuclear manganese cluster and a tyrosyl radical. A model is proposed whereby the tyrosyl radical functions by abstracting hydrogen atoms from substrate water bound as terminal ligands to two of the four manganese ions. Molecular oxygen is produced in the final step in which hydrogen atom transfer and oxygen-oxygen bond formation occur together in a concerted reaction. This mechanism establishes clear analogies between photosynthetic water oxidation and amino acid radical function in other enzymatic reactions.

[1]  F. Albert Cotton,et al.  Advanced Inorganic Chemistry , 1999 .

[2]  John Moncrieff,et al.  Photosynthesis: from Light to Biosphere , 1995 .

[3]  T. J. Collins,et al.  A water-stable manganese(V)-oxo complex: definitive assignment of a .nu.Mnv.tplbond.O infrared vibration , 1990 .

[4]  M. Haumann,et al.  Photosynthetic oxygen evolution: H/D isotope effects and the coupling between electron and proton transfer during transitions S2⟹3 and S3⟹S4→S0 , 1996 .

[5]  Johan Lind,et al.  The one-electron reduction potential of 4-substituted phenoxyl radicals in water , 1990 .

[6]  G. Waldo,et al.  Structural characterization of the binuclear Mn site in Lactobacillus plantarum manganese catalase , 1992 .

[7]  G. Renger,et al.  Studies on the reaction coordinates of the water oxidase in PS II membrane fragments from spinach , 1992, FEBS letters.

[8]  G. Brudvig,et al.  Mechanism for photosynthetic O2 evolution. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[9]  M. Haumann,et al.  Photosystem II of green plants. Oxidation and deprotonation of the same component (histidine?) on S1∗ ⇒ S2∗ in chloride-depleted centers as on S2 ⇒ S3 in controls , 1996 .

[10]  J. Penner‐Hahn,et al.  Reduced derivatives of the Mn cluster in the oxygen-evolving complex of photosystem II: An EXAFS study , 1996 .

[11]  M. Kusunoki,et al.  X-ray Detection of the Period-Four Cycling of the Manganese Cluster in Photosynthetic Water Oxidizing Enzyme , 1992, Science.

[12]  Rebekka M. Wachter,et al.  Molecular modeling studies on oxidation of hexopyranoses by galactose oxidase. An active site topology apparently designed to catalyze radical reactions, either concerted or stepwise , 1996 .

[13]  C. Ingold,et al.  Structure and Mechanism in Organic Chemistry , 1953 .

[14]  Donald R. Ort,et al.  Oxygenic Photosynthesis: The Light Reactions , 1996, Advances in Photosynthesis and Respiration.

[15]  C. Yocum.  Calcium activation of photosynthetic water oxidation , 1991 .

[16]  H. Witt.  Primary reactions of oxygenic photosynthesis , 1996 .

[17]  V. Pecoraro,et al.  Energetics of proton-coupled electron transfer in high-valent Mn2(μ-O)2 systems: Models for water oxidation by the oxygen-evolving complex of photosystem II , 1996 .

[18]  R. Debus,et al.  Directed mutagenesis indicates that the donor to P+680 in photosystem II is tyrosine-161 of the D1 polypeptide. , 1988, Biochemistry.

[19]  Susan W. Gersten,et al.  Structure and redox properties of the water-oxidation catalyst [(bpy)2(OH2)RuORu(OH2)(bpy)2]4+ , 1985 .

[20]  R. Sands,et al.  Multifrequency EPR investigations into the origin of the S2-state signal at g = 4 of the O2-evolving complex. , 1992, Biochimica et biophysica acta.

[21]  L. Krishtalik.  Activation energy of photosynthetic oxygen evolution: an attempt at theoretical analysis , 1990 .

[22]  G. Dismukes,et al.  Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[23]  C. Yocum,et al.  The photosynthetic oxygen evolving complex requires chloride for its redox state S2-->S3 and S3-->S0 transitions but not for S0-->S1 or S1-->S2 transitions. , 1997, Biochemistry.

[24]  J. Mayer,et al.  Understanding C-H bond oxidations: H. and H- transfer in the oxidation of toluene by permanganate. , 1995, Science.

[25]  K. Irrgang,et al.  Analysis of the reaction coordinate of photosynthetic water oxidation by kinetic measurements of 355 nm absorption changes at different temperatures in photosystem II preparations suspended in either H2O or D2O. , 1997, Biochemistry.

[26]  M. Haumann,et al.  Extent and rate of proton release by photosynthetic water oxidation in thylakoids: electrostatic relaxation versus chemical production. , 1994, Biochemistry.

[27]  Vincent L. Pfxoraro.  STRUCTURAL PROPOSALS FOR THE MANGANESE CENTERS OF THE OXYGEN EVOLVING COMPLEX: AN INORGANIC CHEMIST'S PERSPECTIVE * , 1988 .

[28]  JoAnne Stubbe,et al.  Reconsideration of X, the Diiron Intermediate Formed during Cofactor Assembly in E. coli Ribonucleotide Reductase , 1996 .

[29]  R. D. Britt,et al.  Proximity of the manganese cluster of photosystem II to the redox-active tyrosine YZ. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[30]  R. Debus,et al.  Amino acid residues that influence the binding of manganese or calcium to photosystem II. 1. The lumenal interhelical domains of the D1 polypeptide. , 1995, Biochemistry.

[31]  Y. Naruta,et al.  Oxygen Evolution by Oxidation of Water with Manganese Porphyrin Dimers , 1994 .

[32]  M. Chan,et al.  55Mn ESE-ENDOR of a Mixed Valence Mn(III)Mn(IV) Complex: Comparison with the Mn Cluster of the Photosynthetic Oxygen-Evolving Complex , 1995 .

[33]  R. Debus,et al.  Amino acid residues that influence the binding of manganese or calcium to photosystem II. 2. The carboxy-terminal domain of the D1 polypeptide. , 1995, Biochemistry.

[34]  G. Babcock,et al.  Tyrosine radicals are involved in the photosynthetic oxygen-evolving system. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[35]  J. Penner‐Hahn,et al.  Reduced Derivatives of the Manganese Cluster in the Photosynthetic Oxygen-Evolving Complex , 1992 .

[36]  B. Forbush,et al.  COOPERATION OF CHARGES IN PHOTOSYNTHETIC O2 EVOLUTION–I. A LINEAR FOUR STEP MECHANISM , 1970, Photochemistry and photobiology.

[37]  J. Andrews,et al.  Oxidation states of the manganese cluster during the flash-induced S-state cycle of the photosynthetic oxygen-evolving complex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[38]  H. Eichler,et al.  Effects of hydrogen/deuterium exchange on photosynthetic water cleavage in PS II core complexes from spinach , 1996, FEBS letters.

[39]  J. Andrews,et al.  Structural consequences of ammonia binding to the manganese center of the photosynthetic oxygen-evolving complex: an X-ray absorption spectroscopy study of isotropic and oriented photosystem II particles. , 1995, Biochemistry.

[40]  I. Vass,et al.  pH-dependent charge equilibria between tyrosine-D and the S states in photosystem II. Estimation of relative midpoint redox potentials. , 1991, Biochemistry.

[41]  R. Debus,et al.  Water oxidation in photosystem II: from radical chemistry to multielectron chemistry. , 1989, Biochemistry.

[42]  M. Badger,et al.  Detection of one slowly exchanging substrate water molecule in the S3 state of photosystem II. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[43]  C. Tommos,et al.  Tyrosyl radicals in enzyme catalysis: some properties and a focus on photosynthetic water oxidation. , 1997, Acta chemica Scandinavica.

[44]  R. D. Britt,et al.  Manganese−Tyrosine Interaction in the Photosystem II Oxygen-Evolving Complex , 1996 .

[45]  G. Christou,et al.  A molecular ‘double-pivot’ mechanism for water oxidation , 1987 .

[46]  J. Klinman.  Mechanisms Whereby Mononuclear Copper Proteins Functionalize Organic Substrates. , 1996, Chemical reviews.

[47]  J. Klinman,et al.  Oxygen-18 kinetic isotope effects in the dopamine beta-monooxygenase reaction: evidence for a new chemical mechanism in non-heme metallomonooxygenases. , 1994, Biochemistry.

[48]  K. Sauer,et al.  Reaction kinetics for positive charge accumulation on the water side of choloplast photosystem II , 1976, FEBS letters.

[49]  R. Pace,et al.  Electron paramagnetic resonance kinetic studies of the S states in spinach thylakoids. , 1997, Biochemistry.

[50]  G. Dismukes,et al.  The dimanganese(III,IV) oxidation state of catalase from Thermus thermophilus: electron nuclear double resonance analysis of water and protein ligands in the active site. , 1993, Biochemistry.

[51]  B. Diner,et al.  Spin-Density Distribution, Conformation, and Hydrogen Bonding of the Redox-Active Tyrosine YZ in Photosystem II from Multiple-Electron Magnetic-Resonance Spectroscopies: Implications for Photosynthetic Oxygen Evolution , 1995 .

[52]  J. Dekker,et al.  Absorbance difference spectra of the successive redox states of the oxygen-evolving apparatus of photosynthesis , 1984 .

[53]  B. Diner,et al.  Identification of histidine at the catalytic site of the photosynthetic oxygen-evolving complex. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[54]  V. Yachandra,et al.  Manganese Cluster in Photosynthesis: Where Plants Oxidize Water to Dioxygen. , 1996, Chemical reviews.

[55]  Y. Inoue,et al.  Temperature dependence of S-state transition in a thermophilic cyanobacterium, Synechococcus vulcanus Copeland measured by absorption changes in the ultraviolet region , 1987 .

[56]  V. DeRose,et al.  Where plants make oxygen: a structural model for the photosynthetic oxygen-evolving manganese cluster , 1993 .

[57]  R. Debus.  The manganese and calcium ions of photosynthetic oxygen evolution. , 1992, Biochimica et biophysica acta.

[58]  A. Boussac,et al.  Inhibition of tyrosine Z photooxidation after formation of the S3-state in calcium-depleted and chloride-depleted photosystem-II , 1992 .