Segmented all‐electron relativistically contracted (SARC) basis sets are presented for the elements 37Rb–54Xe, for use with the second‐order Douglas–Kroll–Hess approach and the zeroth‐order regular ...approximation. The basis sets have a common set of exponents produced with established heuristic procedures, but have contractions optimized individually for each scalar relativistic Hamiltonian. Their compact size and loose segmented contraction, which is in line with the construction of SARC basis sets for heavier elements, makes them suitable for routine calculations on large systems and when core spectroscopic properties are of interest. The basis sets are of triple‐zeta quality and come in singly or doubly polarized versions, which are appropriate for both density functional theory and correlated wave function theory calculations. The quality of the basis sets is assessed against large decontracted reference basis sets for a number of atomic and ionic properties, while their general applicability is demonstrated with selected molecular examples.
Segmented all‐electron relativistically contracted (SARC) basis sets are constructed for the elements Rb–Xe, for use with the popular second‐order Douglas–Kroll–Hess approach and zeroth‐order regular approximation scalar relativistic Hamiltonians.
Photosystem II (PSII) is a multisubunit pigment-protein complex that uses light-induced charge separation to power oxygenic photosynthesis. Its reaction center chromophores, where the charge transfer ...cascade is initiated, are arranged symmetrically along the D1 and D2 core polypeptides and comprise four chlorophyll (P
, P
, Chl
, Chl
) and two pheophytin molecules (Pheo
and Pheo
). Evolution favored productive electron transfer only via the D1 branch, with the precise nature of primary excitation and the factors that control asymmetric charge transfer remaining under investigation. Here we present a detailed atomistic description for both. We combine large-scale simulations of membrane-embedded PSII with high-level quantum-mechanics/molecular-mechanics (QM/MM) calculations of individual and coupled reaction center chromophores to describe reaction center excited states. We employ both range-separated time-dependent density functional theory and the recently developed domain based local pair natural orbital (DLPNO) implementation of the similarity transformed equation of motion coupled cluster theory with single and double excitations (STEOM-CCSD), the first coupled cluster QM/MM calculations of the reaction center. We find that the protein matrix is exclusively responsible for both transverse (chlorophylls versus pheophytins) and lateral (D1 versus D2 branch) excitation asymmetry, making Chl
the chromophore with the lowest site energy. Multipigment calculations show that the protein matrix renders the Chl
→ Pheo
charge-transfer the lowest energy excitation globally within the reaction center, lower than any pigment-centered local excitation. Remarkably, no low-energy charge transfer states are located within the "special pair" P
-P
, which is therefore excluded as the site of initial charge separation in PSII. Finally, molecular dynamics simulations suggest that modulation of the electrostatic environment due to protein conformational flexibility enables direct excitation of low-lying charge transfer states by far-red light.
The electronic and geometric structures of the water‐oxidizing complex of photosystem II in the steps of the catalytic cycle that precede dioxygen evolution remain hotly debated. Recent structural ...and spectroscopic investigations support contradictory redox formulations for the active‐site Mn4CaOx cofactor in the final metastable S3 state. These range from the widely accepted MnIV4 oxo‐hydroxo model, which presumes that O−O bond formation occurs in the ultimate transient intermediate (S4) of the catalytic cycle, to a MnIII2MnIV2 peroxo model representative of the contrasting “early‐onset” O−O bond formation hypothesis. Density functional theory energetics of suggested S3 redox isomers are inconclusive because of extreme functional dependence. Here, we use the power of the domain‐based local pair natural orbital approach to coupled cluster theory, DLPNO‐CCSD(T), to present the first correlated wave function theory calculations of relative stabilities for distinct redox‐isomeric forms of the S3 state. Our results enabled us to evaluate conflicting models for the S3 state of the oxygen‐evolving complex (OEC) and to quantify the accuracy of lower‐level theoretical approaches. Our assessment of the relevance of distinct redox‐isomeric forms for the mechanism of biological water oxidation strongly disfavors the scenario of early‐onset O−O formation advanced by literal interpretations of certain crystallographic models. This work serves as a case study in the application of modern coupled cluster implementations to redox isomerism problems in oligonuclear transition metal systems.
The domain‐based local pair natural orbital–coupled cluster approach, DLPNO‐CCSD(T), was employed to obtain reliable relative energetics for distinct redox‐isomeric forms of the Mn4Ca cofactor of the oxygen‐evolving complex of photosystem II in its final metastable S3 state. It is shown that the MnIV4 oxo‐hydroxo model is significantly more stable than the MnIII2MnIV2 peroxo model, thus disfavoring the scenario of early‐onset O−O bond formation in biological water oxidation.
Biological water oxidation Cox, Nicholas; Pantazis, Dimitrios A; Neese, Frank ...
Accounts of chemical research,
2013-Jul-16, Letnik:
46, Številka:
7
Journal Article
Recenzirano
Photosystem II (PSII), a multisubunit pigment-protein supercomplex found in cyanobacteria, algae, and plants, catalyzes a unique reaction in nature: the light-driven oxidation of water. Remarkable ...recent advances in the structural analysis of PSII now give a detailed picture of the static supercomplex on the molecular level. These data provide a solid foundation for future functional studies, in particular the mechanism of water oxidation and oxygen release. The catalytic core of the PSII is a tetramanganese-calcium cluster (Mn₄O₅Ca), commonly referred to as the oxygen-evolving complex (OEC). The function of the OEC rests on its ability to cycle through five metastable states (Si, i = 0-4), transiently storing four oxidizing equivalents, and in so doing, facilitates the four electron water splitting reaction. While the latest crystallographic model of PSII gives an atomic picture of the OEC, the exact connectivity within the inorganic core and the S-state(s) that the X-ray model represents remain uncertain. In this Account, we describe our joint experimental and theoretical efforts to eliminate these ambiguities by combining the X-ray data with spectroscopic constraints and introducing computational modeling. We are developing quantum chemical methods to predict electron paramagnetic resonance (EPR) parameters for transition metal clusters, especially focusing on spin-projection approaches combined with density functional theory (DFT) calculations. We aim to resolve the geometric and electronic structures of all S-states, correlating their structural features with spectroscopic observations to elucidate reactivity. The sequence of manganese oxidations and concomitant charge compensation events via proton transfer allow us to rationalize the multielectron S-state cycle. EPR spectroscopy combined with theoretical calculations provides a unique window into the tetramangenese complex, in particular its protonation states and metal ligand sphere evolution, far beyond the scope of static techniques such as X-ray crystallography. This approach has led, for example, to a detailed understanding of the EPR signals in the S₂-state of the OEC in terms of two interconvertible, isoenergetic structures. These two structures differ in their valence distribution and spin multiplicity, which has important consequences for substrate binding and may explain its low barrier exchange with solvent water. New experimental techniques and innovative sample preparations are beginning to unravel the complex sequence of substrate uptake/inclusion, which is coupled to proton release. The introduction of specific site perturbations, such as replacing Ca²⁺ with Sr²⁺, provides discrete information about the ligand environment of the individual Mn ions. In this way, we have identified a potential open coordination site for one Mn center, which may serve as a substrate binding site in the higher S-states, such as S₃ and S₄. In addition, we can now monitor the binding of the substrate water in the lower S-states (S₁ and S₂) using new EPR-detected NMR spectroscopies. These studies provided the first evidence that one of the substrates is subsumed into the complex itself and forms an oxo-bridge between two Mn ions. This result places important new restrictions on the mechanism of O-O bond formation. These new insights from nature's water splitting catalyst provide important criteria for the rational design of bioinspired synthetic catalysts.
The tetramanganese–calcium cluster of the oxygen‐evolving complex of photosystem II adopts electronically and magnetically distinct but interconvertible valence isomeric forms in its first ...light‐driven oxidized catalytic state, S2. This bistability is implicated in gating the final catalytic states preceding O−O bond formation, but it is unknown how the biological system enables its emergence and controls its effect. Here we show that the Mn4CaO5 cluster in the resting (dark‐stable) S1 state adopts orientational Jahn–Teller isomeric forms arising from a directional change in electronic configuration of the “dangler” MnIII ion. The isomers are consistent with available structural data and explain previously unresolved electron paramagnetic resonance spectroscopic observations on the S1 state. This unique isomerism in the resting state is shown to be the electronic origin of valence isomerism in the S2 state, establishing a functional role of orientational Jahn–Teller isomerism unprecedented in biological or artificial catalysis.
The dark‐stable resting state of the biological oxygen‐evolving complex is shown to accommodate a rare type of functionally important MnIII orientational Jahn–Teller isomerism that is identified as the electronic origin of subsequent valence isomerism in the catalytic cycle of water oxidation.
Water channels and networks within photosystem II (PSII) of oxygenic photosynthesis are critical for enzyme structure and function. They control substrate delivery to the oxygen-evolving center and ...mediate proton transfer at both the oxidative and reductive endpoints. Current views on PSII hydration are derived from protein crystallography, but structural information may be compromised by sample dehydration and technical limitations. Here, we simulate the physiological hydration structure of a cyanobacterial PSII model following a thorough hydration procedure and large-scale unconstrained all-atom molecular dynamics enabled by massively parallel simulations. We show that crystallographic models of PSII are moderately to severely dehydrated and that this problem is particularly acute for models derived from X-ray free electron laser (XFEL) serial femtosecond crystallography. We present a fully hydrated representation of cyanobacterial PSII and map all water channels, both static and dynamic, associated with the electron donor and acceptor sides. Among them, we describe a series of transient channels and the attendant conformational gating role of protein components. On the acceptor side, we characterize a channel system that is absent from existing crystallographic models but is likely functionally important for the reduction of the terminal electron acceptor plastoquinone Q
. The results of the present work build a foundation for properly (re)evaluating crystallographic models and for eliciting new insights into PSII structure and function.
Photosystem‐II uses sunlight to trigger charge separation and catalyze water oxidation. Intrinsic properties of chlorophyll a pigments define a natural “red limit” of photosynthesis at ≈680 nm. ...Nevertheless, charge separation can be triggered with far‐red photons up to 800 nm, without altering the nature of light‐harvesting pigments. Here we identify the electronic origin of this remarkable phenomenon using quantum chemical and multiscale simulations on a native Photosystem‐II model. We find that the reaction center is preorganized for charge separation in the far‐red region by specific chlorophyll–pheophytin pairs, potentially bypassing the light‐harvesting apparatus. Charge transfer can occur along two distinct pathways with one and the same pheophytin acceptor (PheoD1). The identity of the donor chlorophyll (ChlD1 or PD1) is wavelength‐dependent and conformational dynamics broaden the sampling of the far‐red region by the two charge‐transfer states. The two pathways rationalize spectroscopic observations and underpin designed extensions of the photosynthetically active radiation limit.
Differential protein electrostatics enable excitation of the Photosystem‐II reaction center chlorophyll–pheophytin pigment pairs by far‐red light along two distinct, conformation‐ and wavelength‐dependent charge‐transfer pathways.
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