A calcium-specific site influences the structure and activity of the manganese cluster responsible for photosynthetic water oxidation
- 1 November 1989
- journal article
- research article
- Published by American Chemical Society (ACS) in Biochemistry
- Vol. 28 (24), 9459-9464
- https://doi.org/10.1021/bi00450a032
Abstract
EPR studies have revealed that removal of calcium using citric acid from the site in spinach photosystem II which is coupled to the photosynthetic O2-evolving process produces a structural change in the manganese cluster responsible for water oxidation. If done in the dark, this yields a modified S1'' oxidation state which can be photooxidized above 250 K to form a structurally altered S''2 state, as seen by formation of a "modified" multiline EPR signal. Compared to the "normal" S2 state, this new S''2-state EPR signal has more lines (at least 25) and 25% narrower 55Mn hyperfine splittings, indicative of disruption of the ligands to manganese. The calcium-depleted S2 oxidation state is greatly stabilized compared to the native S2 oxidation state, as seen by a large increase in the lifetime of the S''2 EPR signal. Calcium reconstitution results in the reduction of the oxidized tyrosine residue 161YD+ (Em .apprx. 0.7-0.8 V, NHE) within the reaction center D1 protein in both the S''1 and S''2 states, as monitored by its EPR signal intensity. We attribute this to reduction by Mn. Thus a possible structural role which calcium plays is to bring YD+ into redox equilibrium with the Mn cluster. Photooxidation of S''2 above 250 K produces a higher S state (S3 or S4) having a new EPR signal at g = 2.004 .+-. 0.003 and a symmetric line width of 163 .+-. 3 G, suggestive of oxidation of an organic donor, possibly an amino acid, in magnetic contact with the Mn cluster. This EPR signal forms in a stoichiometry of 1-2 relative to YD+. This state is photoaccumulated, dose not evolve O2, and decays in the dark to the stable S''2 state. The enhanced stability and apparent lowered redox potential of the S states can be explained if calcium depletion exposes the Mn cluster to an increased solvent activity, resulting in the binding and hydrolysis of additional water ligands (hydroxo and oxo). The possibility that this causes disproportionation of MnIII to MnII + MnIV is considered on the basis of analogy to the hydrolysis-induced disproportionation observed for synthetic dimanganese complexes. A "gatekeeper" role for calcium in limiting access of substrate water to the catalytic Mn cluster is indicated.This publication has 12 references indexed in Scilit:
- Isolation of an oxygen-evolving Photosystem II preparation containing only one tightly bound calcium atom from a chlorophyll b-deficient mutant of riceBiochimica et Biophysica Acta (BBA) - Bioenergetics, 1988
- Synthesis, crystal structures, reactivity, and magnetochemistry of a series of binuclear complexes of manganese(II), -(III), and -(IV) of biological relevance. The crystal structure of [L'MnIV(.mu.-O)3MnIVL'](PF6)2.H2O containing an unprecedented short Mn.cntdot..cntdot..cntdot.Mn distance of 2.296 .ANG.Journal of the American Chemical Society, 1988
- Nature of the inhibition of the oxygen-evolving enzyme of photosystem II induced by sodium chloride washing and reversed by the addition of calcium(2+) or strontium(2+)Biochemistry, 1988
- In the oxygen-evolving complex of photosystem II the S0 state is oxidized to the S1 state by D+ (signal IIslow)Biochemistry, 1987
- Binuclear manganese(III) complexes of potential biological significanceJournal of the American Chemical Society, 1987
- The flash number dependence of EPR Signal II decay as a probe for charge accumulation in Photosystem IIBiochimica et Biophysica Acta (BBA) - Bioenergetics, 1987
- A model for the mechanism of chloride activation of oxygen evolution in photosystem IIPhotosynthesis Research, 1987
- Reactivation of oxygen evolution of NaCl-washed Photosystem-II particles by Ca2+ and/or the 24 kDa proteinBiochimica et Biophysica Acta (BBA) - Bioenergetics, 1985
- Kinetics of the oxygen-evolving complex in salt-washed photosystem II preparationsBiochimica et Biophysica Acta (BBA) - Bioenergetics, 1984
- Midpoint potential of signal II (slow) in Tris-washed photosystem-II particlesBiochimica et Biophysica Acta (BBA) - Bioenergetics, 1984