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On the role of manganese in photosynthetic water oxidation
612
Abstracts
L03
ON THE ROLE OF MANGANESE IN PHOTOSYNTHETIC WATER OXIDATION G. Renger
Max-~'blmer-Institut fur Physikalische und Biophysikalische Chemie TU Berlin, Strafle des 1Z Juni 135, D-10623 Berlin, Germany Photosynthetic water oxidation into dioxygen and four protons takes place via a sequence of univalent oxidation steps at a functional unit containing four manganese and referred to as water oxidizing complex (WOC). This reaction is energetically driven by the light induced formation of a strongly oxidizing chlorophyll-a cation radical (P68W) including a tyrosine residue of the protein matrix as intermediate electron carrier. Manganese directly participates as redox active species and simultaneously provides the device for intermediary storage of oxidizing equivalents (these states are symbolized by Si, where i = number of stored holes above the formal redox state of water). Several key problems of photosynthetic water oxidation are still unresolved, e.g. the substrate entry, the essential step of O-O-bond formation, the nature of the coordination sphere of manganese, etc. [ 1]. This communication describes theoretical considerations and experimental results obtained by flash spectrophotomelry, ~ttonmle:ry raid an',ge;olu¢[ry. It i,,; sho~a:q: +
I. A kinetic analysis of the transitions Y~zXSi + wi+ l H20 ~ YzSi¢.l + ninlume n + ~i302 (wi ~I number of substrate water molecules which are bound in the redox transitions S 1 ~ Si+ 1 and ~i3 --: 1 fo; i = 3, oLhcrwlse z¢'fo) wit,hiv, the fiam~'work of the Marcus theory of nonadiabatic electron transfer leads to the following reorganisation energies: Li i~ I = 0.6; 0.6; 1.6 and 1.1 eV (above 6°C) for i = 0, 1, 2, 3, respectively [21. 2. H/~ exchange gives rise ~o a~ isot%'-¢ ~:ffect of abeut 30% on the or:JdaOon kinetics of 5 3. It is ilfferred that 02 formation is coupled with the break of hydrogeil bonds. 3. Selective treatment with small hydrophilic reductants that are isoelectronic with H202 (NH2OH, NH2NH2) permits the formation and high population of the redox states So, S 1 and S. 2 131. 4. Binuclear manganese complexes with aromatic ligands are highly efficient in restoring a fully competent WOC in samples deprived of their manganese [4]. 5. Modification of the WOC by removing regulator), subunits causes a change of the reaction pathway with preferential formation of H202 instead of O 2. The EPR multiline signal at g = 2 that is indicative of mixed valence Mn(IIl) Mn(IV) in redox state S2 is not significantly affected under these conditions. 6. Based on the above mentioned experimental results and theoretical considerations a model of photosynthetic water oxidation is proposed comprising the following postulates: (i) O2-formation takes place at a binuclear manganese template via an oxidant (Y~zx) induced reduction of redox state S3 to SO and concomitant O2-formation (ii) the essential O-O bond is formed at the redox level S3 with an electronic configuration and nuclear geometry of peroxidic type. A fast equilibrium is assumed to exist between this state and a hydroxylic type configuration of S3. dCooperation with W. Lubitz, S. Allakhverdiev and S. Padhye and financial support by Deutsche Forschungsgemeinschaft are gratefully acknowledged. 1. Renger, G., Photosynth. Res. 38, 227 (1993) 2. Renger, G. and Hanssum, B. FEBS Lett. 299, 28 (1992) 3. Messinger, G. and Renger, G. Biochemistry 32, 9378 (1993) 4. Allakhverdiev, S. et. al., Biochemistry. 33, 12210 (1994)
Abstracts
L03
ON THE ROLE OF MANGANESE IN PHOTOSYNTHETIC WATER OXIDATION G. Renger
Max-~'blmer-Institut fur Physikalische und Biophysikalische Chemie TU Berlin, Strafle des 1Z Juni 135, D-10623 Berlin, Germany Photosynthetic water oxidation into dioxygen and four protons takes place via a sequence of univalent oxidation steps at a functional unit containing four manganese and referred to as water oxidizing complex (WOC). This reaction is energetically driven by the light induced formation of a strongly oxidizing chlorophyll-a cation radical (P68W) including a tyrosine residue of the protein matrix as intermediate electron carrier. Manganese directly participates as redox active species and simultaneously provides the device for intermediary storage of oxidizing equivalents (these states are symbolized by Si, where i = number of stored holes above the formal redox state of water). Several key problems of photosynthetic water oxidation are still unresolved, e.g. the substrate entry, the essential step of O-O-bond formation, the nature of the coordination sphere of manganese, etc. [ 1]. This communication describes theoretical considerations and experimental results obtained by flash spectrophotomelry, ~ttonmle:ry raid an',ge;olu¢[ry. It i,,; sho~a:q: +
I. A kinetic analysis of the transitions Y~zXSi + wi+ l H20 ~ YzSi¢.l + ninlume n + ~i302 (wi ~I number of substrate water molecules which are bound in the redox transitions S 1 ~ Si+ 1 and ~i3 --: 1 fo; i = 3, oLhcrwlse z¢'fo) wit,hiv, the fiam~'work of the Marcus theory of nonadiabatic electron transfer leads to the following reorganisation energies: Li i~ I = 0.6; 0.6; 1.6 and 1.1 eV (above 6°C) for i = 0, 1, 2, 3, respectively [21. 2. H/~ exchange gives rise ~o a~ isot%'-¢ ~:ffect of abeut 30% on the or:JdaOon kinetics of 5 3. It is ilfferred that 02 formation is coupled with the break of hydrogeil bonds. 3. Selective treatment with small hydrophilic reductants that are isoelectronic with H202 (NH2OH, NH2NH2) permits the formation and high population of the redox states So, S 1 and S. 2 131. 4. Binuclear manganese complexes with aromatic ligands are highly efficient in restoring a fully competent WOC in samples deprived of their manganese [4]. 5. Modification of the WOC by removing regulator), subunits causes a change of the reaction pathway with preferential formation of H202 instead of O 2. The EPR multiline signal at g = 2 that is indicative of mixed valence Mn(IIl) Mn(IV) in redox state S2 is not significantly affected under these conditions. 6. Based on the above mentioned experimental results and theoretical considerations a model of photosynthetic water oxidation is proposed comprising the following postulates: (i) O2-formation takes place at a binuclear manganese template via an oxidant (Y~zx) induced reduction of redox state S3 to SO and concomitant O2-formation (ii) the essential O-O bond is formed at the redox level S3 with an electronic configuration and nuclear geometry of peroxidic type. A fast equilibrium is assumed to exist between this state and a hydroxylic type configuration of S3. dCooperation with W. Lubitz, S. Allakhverdiev and S. Padhye and financial support by Deutsche Forschungsgemeinschaft are gratefully acknowledged. 1. Renger, G., Photosynth. Res. 38, 227 (1993) 2. Renger, G. and Hanssum, B. FEBS Lett. 299, 28 (1992) 3. Messinger, G. and Renger, G. Biochemistry 32, 9378 (1993) 4. Allakhverdiev, S. et. al., Biochemistry. 33, 12210 (1994)