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Is Mn-Bound Substrate Water Protonated in the S(2) State of Photosystem II?

ABSTRACT: In spite of great progress in resolving the geometric structure of the water-splitting Mn(4)O(x)Ca cluster in photosystem II, the binding sites and modes of the two substrate water molecules are still insufficiently characterized. While time-resolved membrane-inlet mass spectrometry measurements indicate that both substrate water molecules are bound to the oxygen-evolving complex (OEC) in the S(2) and S(3) states (Hendry and Wydrzynski in Biochemistry 41:13328-13334, 2002), it is not known (1) if they are both Mn-bound, (2) if they are terminal or bridging ligands, and (3) in what protonation state they are bound in the different oxidation states S(i) (i = 0, 1, 2, 3, 4) of the OEC. By employing (17)O hyperfine sublevel correlation (HYSCORE) spectroscopy we recently demonstrated that in the S(2) state there is only one (type of) Mn-bound oxygen that is water exchangeable. We therefore tentatively identified this oxygen as one substrate 'water' molecule, and on the basis of the finding that it has a hyperfine interaction of about 10 MHz with the electron spin of the Mn(4)O(x)Ca cluster, we suggest that it is bound as a Mn-O-Mn bridge within a bis-mu(2) oxo-bridged unit (Su et al. in J Am Chem Soc 130:786-787, 2008). Employing pulse electron paramagnetic resonance, (1)H/(2)H Mims electron-nuclear double resonance and (2)H-HYSCORE spectroscopies together with (1)H/(2)H-exchange here, we test this hypothesis by probing the protonation state of this exchangeable oxygen. We conclude that this oxygen is fully deprotonated. This result is discussed in the light of earlier reports in the literature.

SUBMITTER: Su JH

PROVIDER: S-EPMC2784071 | biostudies-other | 2010 Jan

REPOSITORIES: biostudies-other

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Project description:Highlights • We derive a model that provides an exact solution to the substrate-water exchange kinetics in a double-conformation system.• This model is used to interpret recently published data for Ca2+- and Sr2+-containing PSII in the S2 state, in which the g = 2.0 and g = 4.1 conformations coexist.• The component concentrations derived from the kinetic model provide an analytic description of the substrate-water exchange kinetics.• Contrary to previous reports, there is no significant effect of substituting Sr2+ for Ca2+ on any of the exchange rate constants.• The exchange rate of the slowly-exchanging water (Ws) in the S2 state g = 4.1 conformation is much faster than that in the g = 2.0 conformation, consistent with the assignment of Ws to W1 or W2 bound as terminal ligands to Mn4. We derive a model that provides an exact solution to the substrate-water exchange kinetics in a double-conformation system and use this model to interpret recently published data for Ca2+- and Sr2+-containing PSII in the S2 state, in which the g = 2.0 and g = 4.1 conformations coexist. The component concentrations derived from the kinetic model provide an analytic description of the substrate-water exchange kinetics, allowing us to more accurately interpret the results. Based on this model and the previously reported data on the S2 state g = 2.0 conformation, we obtain the substrate-water exchange rates of the g = 4.1 conformation and the conformational change rates. Two conclusions are made from the analyses. First, contrary to previous reports, there is no significant effect of substituting Sr2+ for Ca2+ on any of the exchange rate constants. Second, the exchange rate of the slowly-exchanging water (Ws) in the S2 state g = 4.1 conformation is much faster than that in the S2 state g = 2.0 conformation. The second conclusion is consistent with the assignment of Ws to W1 or W2 bound as terminal ligands to Mn4; Mn4 has been proposed to undergo an oxidation state change from Mn(IV) in the g = 2.0 conformation to Mn(III) in the g = 4.1 conformation.

Project description:The oxygen-evolving complex of Photosystem II in plants and cyanobacteria catalyzes the oxidation of two water molecules to one molecule of dioxygen. A tetranuclear Mn complex is believed to cycle through five intermediate states (S0-S4) to couple the four-electron oxidation of water with the one-electron photochemistry occurring at the Photosystem II reaction center. We have used X-ray absorption spectroscopy to study the local structure of the Mn complex and have proposed a model for it, based on studies of the Mn K-edges and the extended X-ray absorption fine structure of the S1 and S2 states. The proposed model consists of two di-?-oxo-bridged binuclear Mn units with Mn-Mn distances of ~2.7 Å that are linked to each other by a mono-?-oxo bridge with a Mn-Mn separation of ~3.3 Å. The Mn-Mn distances are invariant in the native S1 and S2 states. This report describes the application of X-ray absorption spectroscopy to S3 samples created under physiological conditions with saturating flash illumination. Significant changes are observed in the Mn-Mn distances in the S3 state compared to the S1 and the S2 states. The two 2.7 Å Mn-Mn distances that characterize the di-?-oxo centers in the S1 and S2 states are lengthened to ~2.8 and 3.0 Å in the S3 state, respectively. The 3.3 Å Mn-Mn and Mn-Ca distances also increase by 0.04-0.2 Å. These changes in Mn-Mn distances are interpreted as consequences of the onset of substrate/water oxidation in the S3 state. Mn-centered oxidation is evident during the S0?S1 and S1?S2 transitions. We propose that the changes in Mn-Mn distances during the S2?S3 transition are the result of ligand or water oxidation, leading to the formation of an oxyl radical intermediate formed at a bridging or terminal position. The reaction of the oxyl radical with OH(-), H2O, or an oxo group during the subsequent S state conversion is proposed to lead to the formation of the O-O bond. Models that can account for changes in the Mn-Mn distances in the S3 state and the implications for the mechanism of water oxidation are discussed.

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Is Mn-Bound Substrate Water Protonated in the S(2) State of Photosystem II?

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