Absence of Mn-Centered Oxidation in the S<sub>2</sub> → S<sub>3</sub> Transition:  Implications for the Mechanism of Photosynthetic Water Oxidation

Messinger, Johannes; Robblee, John H.; Bergmann, Uwe; Fernandez, Carmen; Glatzel, Pieter; Visser, Hendrik G.; Cinco, Roehl M.; McFarlane, Karen L.; Bellacchio, Emanuele; Pizarro, Shelly A.; Cramer, Stephen P.; Sauer, Kenneth; Klein, Melvin P.; Yachandra, Vittal K.

doi:10.1021/ja004307+

Cited by 285 publications

(552 citation statements)

References 128 publications

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“…Mn(1)ZIV, Mn(2)ZIV, Mn(3)ZIII, Mn(4)ZIII) and model (b) where an additional water ligand is completing the hexacoordinated shell of Mn(4) and the oxidation states are Mn 4 (IV,III,III,IV ). These results are partially consistent with EPR and X-ray spectroscopic evidence (Ono et al 1992;Yachandra et al 1993;Roelofs et al 1996;Bergmann et al 1998;Iuzzolino et al 1998;Dau et al 2001;Messinger et al 2001) but disagree with the suggested low-valent Mn 4 (III,III,III,III ) state (Zheng & Dismukes 1996;Kuzek & Pace 2001).…”

Section: Structural Models Of the O 2 -Evolving Centresupporting

confidence: 49%

QM/MM computational studies of substrate water binding to the oxygen-evolving centre of photosystem II

Sproviero

Shinopoulos

Gascón

et al. 2007

Phil. Trans. R. Soc. B

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This paper reports computational studies of substrate water binding to the oxygen-evolving centre (OEC) of photosystem II (PSII ), completely ligated by amino acid residues, water, hydroxide and chloride. The calculations are based on quantum mechanics/molecular mechanics hybrid models of the OEC of PSII, recently developed in conjunction with the X-ray crystal structure of PSII from the cyanobacterium Thermosynechococcus elongatus. The model OEC involves a cuboidal Mn 3 CaO 4 Mn metal cluster with three closely associated manganese ions linked to a single m 4 -oxo-ligated Mn ion, often called the 'dangling manganese'. Two water molecules bound to calcium and the dangling manganese are postulated to be substrate molecules, responsible for dioxygen formation. It is found that the energy barriers for the Mn(4)-bound water agree nicely with those of model complexes. However, the barriers for Ca-bound waters are substantially larger. Water binding is not simply correlated to the formal oxidation states of the metal centres but rather to their corresponding electrostatic potential atomic charges as modulated by charge-transfer interactions. The calculations of structural rearrangements during water exchange provide support for the experimental finding that the exchange rates with bulk 18 O-labelled water should be smaller for water molecules coordinated to calcium than for water molecules attached to the dangling manganese. The models also predict that the S 1 /S 2 transition should produce opposite effects on the two waterexchange rates.

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Section: Structural Models Of the O 2 -Evolving Centresupporting

confidence: 49%

QM/MM computational studies of substrate water binding to the oxygen-evolving centre of photosystem II

Sproviero

Shinopoulos

Gascón

et al. 2007

Phil. Trans. R. Soc. B

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“…The earlier analysis by Yachandra and coworkers (17) gave one change of more than 0.2 Å (or one of 0.2 and one of 0.1 Å). This change, supported by results of earlier and later XANES spectra (33), led to the conclusion that an oxygen rather than a manganese is oxidized in this transition, which strongly affected the suggested O-O bond formation mechanism (34,35). The conclusion from the XANES spectra has been questioned experimentally (36), and also recently on the basis of DFT model calculations (37).…”

Section: Resultsmentioning

confidence: 76%

Simulation of the isotropic EXAFS spectra for the S ₂ and S ₃ structures of the oxygen evolving complex in photosystem II

Siegbahn

Ryde

2015

Proc. Natl. Acad. Sci. U.S.A.

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Most of the main features of water oxidation in photosystem II are now well understood, including the mechanism for O-O bond formation. For the intermediate S 2 and S 3 structures there is also nearly complete agreement between quantum chemical modeling and experiments. Given the present high degree of consensus for these structures, it is of high interest to go back to previous suggestions concerning what happens in the S 2 -S 3 transition. Analyses of extended X-ray adsorption fine structure (EXAFS) experiments have indicated relatively large structural changes in this transition, with changes of distances sometimes larger than 0.3 Å and a change of topology. In contrast, our previous density functional theory (DFT)(B3LYP) calculations on a cluster model showed very small changes, less than 0.1 Å. It is here found that the DFT structures are also consistent with the EXAFS spectra for the S 2 and S 3 states within normal errors of DFT. The analysis suggests that there are severe problems in interpreting EXAFS spectra for these complicated systems.water oxidation | density functional theory | S-state structures | EXAFS refinement

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“…A decrease in the fluorescence level after the flash indicates oxidation of the Mn complex, an increase reflects Mn reduction. [We note that the magnitude of ⌬F X-ray is S-state-dependent; for excitation at 6,552.5 eV, it is larger in S 1 3S 2 than in S 2 3S 3 (36)(37)(38).] At 0.2 bar O 2 , Mn reduction was absent on flash 1 and small on flash 2, whereas at 13 bar O 2 , significant Mn reduction occurred already on flash 2.…”

mentioning

confidence: 76%

Photosynthetic water oxidation at elevated dioxygen partial pressure monitored by time-resolved X-ray absorption measurements

Haumann

Grundmeier

Zaharieva

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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The atmospheric dioxygen (O2) is produced at a tetramanganese complex bound to the proteins of photosystem II (PSII). To investigate product inhibition at elevated oxygen partial pressure (pO 2 ranging from 0.2 to 16 bar), we monitored specifically the redox reactions of the Mn complex in its catalytic S-state cycle by rapid-scan and time-resolved X-ray absorption near-edge spectroscopy (XANES) at the Mn K-edge. By using a pressure cell for X-ray measurements after laser-flash excitation of PSII particles, we found a clear pO 2 influence on the redox reactions of the Mn complex, with a similar half-effect pressure as determined (2-3 bar). However, XANES spectra and the time courses of the X-ray fluorescence collected with microsecond resolution suggested that the O 2 evolution transition itself (S3fS0؉O2) was not affected. Additional (nonstandard) oxidation of the Mn complex at high pO 2 explains our experimental findings more readily. Our results suggest that photosynthesis at ambient conditions is not limited by product inhibition of the O 2 formation step. manganese complex ͉ photosystem II ͉ X-ray spectroscopy ͉ bioinorganic chemistry ͉ oxygen pressure I n oxygenic photosynthesis, plants, algae, and cyanobacteria facilitate the primary biomass formation by exploiting solar energy for driving the conversion of water (H 2 O) and carbon dioxide (CO 2 ) into carbohydrates (C n H 2n O n ). Dioxygen (O 2 ) is formed as product of the water oxidation chemistry of the photosystem II (PSII) protein complex (1-5). Photosynthetic CO 2 fixation and O 2 formation have shaped the Earth's atmosphere (6) by (i) lowering the CO 2 level to Ͻ0.04% and (ii) creation of a maximal O 2 concentration of 35% (7), Ϸ300 million years before the present and a current level of Ϸ20%.In photosynthetic organisms, the low level of atmospheric CO 2 can limit photosynthesis, related to the activity of CO 2 -fixing ribulose bisphosphate carboxylase (8, 9). It is less clear whether water oxidation by PSII is directly affected by the concentration of O 2 , the immediate product of light-driven water splitting. This question was only recently addressed experimentally by Clausen and Junge (10). They exposed PSII from cyanobacteria to oxygen partial pressures (pO 2 ) ranging from 0.2 to 30 bar and, analyzing flash-induced near-UV absorption changes, discovered a pO 2 effect with a half-saturation pressure of only Ϸ2 bar (10). Subsequently, in measurements of delayed Chl fluorescence, together with Clausen and Junge we confirmed that also the donor side of the plant PSII in its native membrane environment is affected by elevated pO 2 (11). The surprisingly low halfpressure of only 2-3 bar was taken as an indication that the efficiency of the O 2 formation step could be reduced significantly by product inhibition. Such a limitation of the water oxidation chemistry may have imposed restraints on the evolution of oxygenic photosynthesis (10). Notably, the pO 2 inside of photosynthetic cells in microbial mats and bioreactors can be severalfold higher th...

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Absence of Mn-Centered Oxidation in the S₂ → S₃ Transition: Implications for the Mechanism of Photosynthetic Water Oxidation

Cited by 285 publications

References 128 publications

QM/MM computational studies of substrate water binding to the oxygen-evolving centre of photosystem II

QM/MM computational studies of substrate water binding to the oxygen-evolving centre of photosystem II

Simulation of the isotropic EXAFS spectra for the S ₂ and S ₃ structures of the oxygen evolving complex in photosystem II

Photosynthetic water oxidation at elevated dioxygen partial pressure monitored by time-resolved X-ray absorption measurements

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Absence of Mn-Centered Oxidation in the S2 → S3 Transition: Implications for the Mechanism of Photosynthetic Water Oxidation

Cited by 285 publications

References 128 publications

QM/MM computational studies of substrate water binding to the oxygen-evolving centre of photosystem II

QM/MM computational studies of substrate water binding to the oxygen-evolving centre of photosystem II

Simulation of the isotropic EXAFS spectra for the S 2 and S 3 structures of the oxygen evolving complex in photosystem II

Photosynthetic water oxidation at elevated dioxygen partial pressure monitored by time-resolved X-ray absorption measurements

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Absence of Mn-Centered Oxidation in the S₂ → S₃ Transition: Implications for the Mechanism of Photosynthetic Water Oxidation

Simulation of the isotropic EXAFS spectra for the S ₂ and S ₃ structures of the oxygen evolving complex in photosystem II