Toward the Assignment of the Manganese Oxidation Pattern in the Water‐Oxidizing Complex of Photosystem II: A Time‐Dependent DFT Study of XANES Energies

Jaszewski, Adrian R.; Petrie, Simon; Pace, Ronald; Stranger, Rob

doi:10.1002/chem.201001996

Cited by 41 publications

(71 citation statements)

References 60 publications

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“…Most groups have favored the high‐oxidation state paradigm, mainly from spectroscopic interpretation (principally XANES, EPR)13 based on model Mn–oxo systems, never precise analogues of the actual Mn environment of the WOC. We have shown, using time‐dependent DFT, that when the metal–ligand environments are properly accounted for, the Mn XANES data are most consistent with the low oxidation state paradigm 14b,c. Re‐examination of other spectroscopic data also supports this observation 3b…”

Section: Key Distances From Extended‐range Exafs Studies7 9 and Thesupporting

confidence: 56%

Resolving the Differences Between the 1.9 Å and 1.95 Å Crystal Structures of Photosystem II: A Single Proton Relocation Defines Two Tautomeric Forms of the Water‐Oxidizing Complex

2015

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Great progress has been made in characterizing the water-oxidizing complex (WOC) in photosystem II (PSII) with the publication of a 1.9 Å resolution X-ray diffraction (XRD) and recently a 1.95 Å X-ray free-electron laser (XFEL) structure. However, these achievements are under threat because of perceived conflicts with other experimental data. For the earlier 1.9 Å structure, lack of agreement with extended X-ray absorption fine structure (EXAFS) data led to the notion that the WOC suffered from X-ray photoreduction. In the recent 1.95 Å structure, Mn photoreduction is not an issue, but poor agreement with computational models which adopt the 'high' oxidation state paradigm, has again resulted in criticism of the structure on the basis of contamination with lower S states of the WOC. Here we use DFT modeling to show that the distinct WOC geometries in the 1.9 and 1.95 Å structures can be straightforwardly accounted for when the Mn oxidation states are consistent with the 'low' oxidation state paradigm. Remarkably, our calculations show that the two structures are tautomers, related by a single proton relocation.

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Section: Key Distances From Extended‐range Exafs Studies7 9 and Thesupporting

confidence: 56%

Resolving the Differences Between the 1.9 Å and 1.95 Å Crystal Structures of Photosystem II: A Single Proton Relocation Defines Two Tautomeric Forms of the Water‐Oxidizing Complex

2015

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“…In the present study a ∆SCF Kohn Sham 30,32 method has been used in contrast to the previous study which used the TDDFT method. 24,25 The present method was chosen based both on its inherent superior properties and on previous experience. 32,36 The static exchange spectrum is constructed from a fully optimized core hole or a transition potential, allowing inclusion of orbital relaxation around the core hole, and avoiding the electron self-energy problem -two factors that increase steeply as one moves down the main shells of an atom.…”

Section: Discussionmentioning

confidence: 99%

“…25,61,62 A theoretical study of Mn K edge NEXAFS based on TDDTF by Jaszewski et al 25 proposes a "low" Mn oxidation state evolution, where the Mn 4 ator gauge invariance in a full basis set, which leads to "good quality" oscillator strengths also for limited basis sets -a major advantage for property calculations using TD methods. However, for core excitations the situation is completely different, something that follows from two neglected effects in TD methods: lack of orbital relaxation, which breaks the final state rule for NEXAFS, 63 and, in the case of DFT, the electron self-interaction error, which is very large for core electrons.…”

Section: Nexafs K Edge Spectra Of Models Of the Mn 4 Complexmentioning

confidence: 99%

Modeling Near-Edge Fine Structure X-ray Spectra of the Manganese Catalytic Site for Water Oxidation in Photosystem II

2012

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The Mn 1s Near Edge Absorption Fine Structure (NEXAFS) has been computed by means of transition potential gradient corrected Density Functional Theory (DFT) on four Mn 4 Ca clusters modeling the successive S 0 to S 3 steps of the oxygen evolving complex (OEC) in photosystem II (PSII). The model clusters were obtained from a previous theoretical study where they were determined by energy minimization. They are composed of Mn(III) and Mn(IV) atoms, progressing from Mn(III) 3 Mn(IV) for S 0 , to Mn(III) 2 Mn(IV) 2 for S 1 , to Mn(III)Mn(IV) 3 for S 2 , and to * To whom correspondence should be addressed † Uppsala University ‡ Stockholm University ¶ Royal Institute of Technology 1 Mn(IV) 4 for S 3 , implying an Mn centered oxidation during each step of the photosynthetic oxygen evolution. The DFT simulations of the Mn 1s absorption edge reproduce the experimentally measured curves quite well. Using the half-height method, the theoretical IPE's are shifted by 0.93 eV for the S 0 to S 1 transition, by 1.43 eV for the S 1 to S 2 transition, and by 0.63 eV for the S 2 to S 3 transition. The IPE shifts depend strongly on the method used to determine them, and the most interesting result is that the present clusters reproduce the shift in the S 2 to S 3 transition obtained both with the half-height and with the second derivative methods, thus giving strong support to the previously suggested structures and assignments.

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“…Recently, we have shown, using a new time‐dependent DFT approach, that when the metal‐ligand environments are properly accounted for, the available Mn XANES data are most consistent with the low oxidation paradigm 8b. c An extensive re‐examination of other spectroscopic data also supports this conclusion 8d. Further, a very recent study by Dismukes and co‐workers,9 employing a totally different approach that simply counts the electrons removed from four Mn II ions during photoassembly of the functional enzyme (from the apo‐protein), clearly establishes the validity of the low oxidation paradigm.…”

Section: Metal–metal Distances From Exafs Studies[5 6] and The Lollmentioning

confidence: 97%

Rationalizing the 1.9 Å Crystal Structure of Photosystem II—A Remarkable Jahn–Teller Balancing Act Induced by a Single Proton Transfer

et al. 2012

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Green plants and algae oxidize water to molecular oxygen in photosystem II (PS II) within a calcium/tetramanganese site known as the water-oxidizing complex (WOC). Oxygen is generated by the WOC in a four-electron process involving a series of intermediate states (S states, labeled S 0 …S 4 ) of increasingly higher mean oxidation level. [1] Over the past decade, X-ray crystallographic (XRD) structures of PS II at progressively improved resolution [2] have revealed much detail of the WOC. At present, only PS II from thermophilic cyanobacteria has been crystallized for XRD study and the enzyme is presumed to be in the dark stable S 1 state. The first PS II structure (at 3.5 resolution) to resolve side chain positions was presented by Barber and co-workers. [2c] Consistent with subsequent studies at higher resolution, it revealed the compact Mn 3 Ca "cube" structure of the WOC connected more distantly to a single Mn, referred to as the "dangler". More recent improved structures at 3.0 and 2.9 , [2d,e] substantially clarified the metal-and proteinsupplied ligand positions within the WOC, but were still of insufficient resolution to reveal the positions of bridging oxo groups and water molecules (including the substrate water molecules). Finally, Umena et al., [2f] using a new crystallization method, produced an atomic resolution structure at 1.9 , the most resolved to date. Despite this remarkable achievement, revealing, for the first time, the positions of bridging O atoms within the Mn 4 Ca core of the WOC, aspects of the new structure have been met with scepticism. [3,4] Central concerns over this structure involve 1) the identity and unexpected placement of the O(5) moiety (Figure 1), which appears to be either a weakly bound oxo, hydroxo, or water ligand at distances of 2.4-2.7 from four of the metal atoms in the WOC, and 2) the disparity in some key metalmetal distances when compared with earlier, high-precision extended X-ray absorption fine structure (EXAFS) results [5,6] and the previous lower-resolution XRD structures (see Table 1). Although the Mn EXAFS data do not unambiguously assign the individual near (less than 3 ) metal-metal distances within the cluster, they clearly indicate that two Mn-Mn vectors of a magnitude of approximately 2.7 exist within the functional WOC in the S 1 and S 2 states. These are totally consistent with the Mn1-Mn2 and Mn2-Mn3 distances of 2.65 and 2.70 in the 2.9 resolution XRD structure, but are significantly shorter than the corresponding Mn-Mn distances of 2.80 and 2.90 seen in the 1.9 resolution XRD structure.The discrepancies between the XRD and EXAFS data have led some to suggest [3,4,7] that the crystal structures generally, and the 1.9 resolution structure in particular, have undergone photoreduction of the Mn atoms during data collection, increasing the Mn II content and distorting the cluster from the functional S 1 state to as low as S À3 . This is despite the fact that in the later studies great pains were taken to minimize such X-ray exposure. The claims of ph...

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Toward the Assignment of the Manganese Oxidation Pattern in the Water‐Oxidizing Complex of Photosystem II: A Time‐Dependent DFT Study of XANES Energies

Cited by 41 publications

References 60 publications

Resolving the Differences Between the 1.9 Å and 1.95 Å Crystal Structures of Photosystem II: A Single Proton Relocation Defines Two Tautomeric Forms of the Water‐Oxidizing Complex

Resolving the Differences Between the 1.9 Å and 1.95 Å Crystal Structures of Photosystem II: A Single Proton Relocation Defines Two Tautomeric Forms of the Water‐Oxidizing Complex

Modeling Near-Edge Fine Structure X-ray Spectra of the Manganese Catalytic Site for Water Oxidation in Photosystem II

Rationalizing the 1.9 Å Crystal Structure of Photosystem II—A Remarkable Jahn–Teller Balancing Act Induced by a Single Proton Transfer

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