Magnetic interactions in the catalyst used by nature to split water: a DFT plus U multiscale study on the Mn4CaO5 core in photosystem II

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Pathway for Mn-cluster oxidation by tyrosine-Z in the S2 state of photosystem II

Water oxidation in photosynthetic organisms occurs through the five intermediate steps S0-S4 of the Kok cycle in the oxygen evolving complex of photosystem II (PSII). Along the catalytic cycle, four electrons are subsequently removed from the Mn4CaO5 core by the nearby tyrosine Tyr-Z, which is in turn oxidized by the chlorophyll special pair P680, the photo-induced primary donor in PSII. Recently, two Mn4CaO5 conformations, consistent with the S2 state (namely, S2 A and S2 B models) were suggested to exist, perhaps playing a different role within the S 2-to-S3 transition. Here we report multiscale ab initio density functional theory plus U simulations revealing that upon such oxidation the relative thermodynamic stability of the two previously proposed geometries is reversed, the S2 B state becoming the leading conformation. In this latter state a proton coupled electron transfer is spontaneously observed at ∼100 fs at room temperature dynamics. Upon oxidation, the Mn cluster, which is tightly electronically coupled along dynamics to the Tyr-Z tyrosyl group, releases a proton from the nearby W1 water molecule to the close Asp-61 on the femtosecond timescale, thus undergoing a conformational transition increasing the available space for the subsequent coordination of an additional water molecule. The results can help to rationalize previous spectroscopic experiments and confirm, for the first time to our knowledge, that the water-splitting reaction has to proceed through the S2 B conformation, providing the basis for a structural model of the S3 state

The S-2 State of the Oxygen-Evolving Complex of Photosystem II Explored by QM/MM Dynamics: Spin Surfaces and Metastable States Suggest a Reaction Path Towards the S-3 State

Split and polish: Quantum mechanics/molecular mechanics simulations reveal the role of spin surfaces, kinetics, and thermodynamics on the interconversion between two structural models of the {Mn4CaO5} cluster (see picture) in the S2 state of the water-splitting Kok's cycle in photosystem-II. The results account for the temperature, illumination, and procedure dependence of historical EPR experiments and suggest a detailed pathway for the S2 to S3 transition. Copyright © 2013 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim

Magnetic coupling constants and vibrational frequencies by extended broken symmetry approach with hybrid functionals

The description of the electronic structure and magnetic properties of multi-centers transition metal complexes, especially of mixed-valence compounds, still represents a challenge for density functional theory (DFT) methods. The energies and the geometries of the correctly symmetrized low-spin ground state are estimated using the Heisenberg-Dirac-van Vleck spin Hamiltonian within the extended broken symmetry method introduced by Marx and co-workers [Nair et al., J. Chem. Theory Comput. 4, 1174-1188 (2008)]. In the present work we extend the application of this technique, originally implemented using the DFT+U scheme, to the use of hybrid functionals, investigating the ground-state properties of di-iron and di-manganese compounds. The calculated magnetic coupling and vibrational properties of ferredoxin molecular models are in good agreements with experimental results and DFT+U calculations. Six different mixed-valence Mn(III)-Mn(IV) compounds have been extensively studied optimizing the geometry in low-spin, high-spin, and broken-symmetry states and with different functionals. The magnetic coupling constants calculated by the extended broken symmetry approach using B3LYP functional presents a remarkable agreement with the experimental results, revealing that the proposed methodology provides a consistent and accurate DFT approach to the electronic structure of multi-centers transition metal complexes. (C) 2012 American Institute of Physics. [http://dx.doi.org/10.1063/1.4752398

Vibrational fingerprints of the Mn4CaO5 cluster in Photosystem II by mixed quantum-classical molecular dynamics

A detailed knowledge of the structures of the catalytic steps along the Kok-Joliot cycle of Photosystem II may help to understand the strategies adopted by this unique enzyme to achieve water oxidation. Vibrational spectroscopy has probed in the last decades the intermediate states of the catalytic cycle, although the interpretation of the data turned out to be often problematic. In the present work we use QM/MM molecular dynamics on the S-2 state to obtain the vibrational density of states at room temperature. To help the interpretation of the computational and experimental data we propose a decomposition of the Mn4CaO5 moiety into five separate parts, composed by "diamond" motifs involving four atoms. The spectral signatures arising from this analysis can be easily interpreted to assign experimentally known bands to specific molecular motions. In particular, we focused in the low frequency region of the vibrational spectrum of the S-2 state. We can therefore identify the observed bands around 600-620 cm(-1) as characteristic for the stretching vibrations involving Mn1-O1-Mn2 or Mn3-O5 moieties. (C) 2016 Elsevier B.V. All rights reserved

A Spotlight on the Compatibility between XFEL and Ab Initio Structures of the Oxygen Evolving Complex in Photosystem II

The Mn4CaO5 cluster of photosystem II promotes a crucial step in the oxygenic photosynthesis, namely, the water-splitting reaction. The structure of such cluster in the S-1 state of the Kok-Joliot's cycle has been recently resolved by femtosecond X-ray free-electron laser (XFEL) measurements. However, the XFEL results are characterized by appreciable discrepancies with previous X-ray diffraction (XRD), as well as with S-1 models based on ab initio calculations. We provide here a unifying picture based on a combined set of DFT-based structures and molecular dynamics simulations of the S-0 and S-1 states. Our findings indicate that the XFEL results cannot be interpreted on the grounds of a single structure. A combination of two S-1 stable isomers together with a minority contribution of the S-0 state is necessary to reproduce XFEL results within 0.16 angstrom

Mechanism of Water Delivery to the Active Site of Photosystem II along the S₂ to S₃ Transition

The two water molecules serving as substrate for the oxygen evolution in Photosystem II are already bound in the S₂ state of the Kok–Joliot’s cycle. Nevertheless, an additional water molecule is supposed to bind the cluster during the transition between the S₂ and S₃ states, which has been recently revealed to have the Mn₄CaO₅ catalytic cluster arranged in an open cubane fashion. In this Letter, by means of ab initio calculations, we investigated the possible pathways for the binding of the upcoming water molecule. Upon the four different possibilities checked in our calculations, the binding of the crystallographic water molecule, originally located nearby the Cl^– binding site, showed the lowest activation energy barrier. Our findings therefore support the view in which the W2 hydroxyl group and the O5 oxygen act as substrates for the oxygen evolution. Within this framework the role of the open and closed Mn₄CaO₅ conformers is clarified as well as the exact mechanistic events occurring along the S₂ to S₃ transition

Mechanism of Water Delivery to the Active Site of Photosystem II along the S₂ to S₃ Transition

The two water molecules serving as substrate for the oxygen evolution in Photosystem II are already bound in the S₂ state of the Kok–Joliot’s cycle. Nevertheless, an additional water molecule is supposed to bind the cluster during the transition between the S₂ and S₃ states, which has been recently revealed to have the Mn₄CaO₅ catalytic cluster arranged in an open cubane fashion. In this Letter, by means of ab initio calculations, we investigated the possible pathways for the binding of the upcoming water molecule. Upon the four different possibilities checked in our calculations, the binding of the crystallographic water molecule, originally located nearby the Cl^– binding site, showed the lowest activation energy barrier. Our findings therefore support the view in which the W2 hydroxyl group and the O5 oxygen act as substrates for the oxygen evolution. Within this framework the role of the open and closed Mn₄CaO₅ conformers is clarified as well as the exact mechanistic events occurring along the S₂ to S₃ transition