Yulia Pushkar

A Highly Reactive Mononuclear Non-Heme Manganese(IV)–Oxo Complex That Can Activate the Strong C–H Bonds of Alkanes

A mononuclear non-heme manganese(IV)-oxo complex has been synthesized and characterized using various spectroscopic methods. The Mn(IV)-oxo complex shows high reactivity in oxidation reactions, such as C-H bond activation, oxidations of olefins, alcohols, sulfides, and aromatic compounds, and N-dealkylation. In C-H bond activation, the Mn(IV)-oxo complex can activate C-H bonds as strong as those in cyclohexane. It is proposed that C-H bond activation by the non-heme Mn(IV)-oxo complex does not occur via an oxygen-rebound mechanism. The electrophilic character of the non-heme Mn(IV)-oxo complex is demonstrated by a large negative ρ value of -4.4 in the oxidation of para-substituted thioanisoles.

A Mononuclear Non-Heme Manganese(IV)−Oxo Complex Binding Redox-Inactive Metal Ions

Redox-inactive metal ions play pivotal roles in regulating the reactivities of high-valent metal-oxo species in a variety of enzymatic and chemical reactions. A mononuclear non-heme Mn(IV)-oxo complex bearing a pentadentate N5 ligand has been synthesized and used in the synthesis of a Mn(IV)-oxo complex binding scandium ions. The Mn(IV)-oxo complexes were characterized with various spectroscopic methods. The reactivities of the Mn(IV)-oxo complex are markedly influenced by binding of Sc(3+) ions in oxidation reactions, such as a ~2200-fold increase in the rate of oxidation of thioanisole (i.e., oxygen atom transfer) but a ~180-fold decrease in the rate of C-H bond activation of 1,4-cyclohexadiene (i.e., hydrogen atom transfer). The present results provide the first example of a non-heme Mn(IV)-oxo complex binding redox-inactive metal ions that shows a contrasting effect of the redox-inactive metal ions on the reactivities of metal-oxo species in the oxygen atom transfer and hydrogen atom transfer reactions.

X-ray Emission Spectroscopy to Study Ligand Valence Orbitals in Mn Coordination Complexes

We discuss a spectroscopic method to determine the character of chemical bonding and for the identification of metal ligands in coordination and bioinorganic chemistry. It is based on the analysis of satellite lines in X-ray emission spectra that arise from transitions between valence orbitals and the metal ion 1s level (valence-to-core XES). The spectra, in connection with calculations based on density functional theory (DFT), provide information that is complementary to other spectroscopic techniques, in particular X-ray absorption (XANES and EXAFS). The spectral shape is sensitive to protonation of ligands and allows ligands, which differ only slightly in atomic number (e.g., C, N, O...), to be distinguished. A theoretical discussion of the main spectral features is presented in terms of molecular orbitals for a series of Mn model systems: [Mn(H(2)O)(6)](2+), [Mn(H(2)O)(5)OH](+), and [Mn(H(2)O)(5)NH(3)](2+). An application of the method, with comparison between theory and experiment, is presented for the solvated Mn(2+) ion in water and three Mn coordination complexes, namely [LMn(acac)N(3)]BPh(4), [LMn(B(2)O(3)Ph(2))(ClO(4))], and [LMn(acac)N]BPh(4), where L represents 1,4,7-trimethyl-1,4,7-triazacyclononane, acac stands for the 2,4-pentanedionate anion, and B(2)O(3)Ph(2) represents the 1,3-diphenyl-1,3-dibora-2-oxapropane-1,3-diolato dianion.

Structure and orientation of the Mn4Ca cluster in plant photosystem II membranes studied by polarized range-extended X-ray absorption spectroscopy

X-ray absorption spectroscopy has provided important insights into the structure and function of the Mn4Ca cluster in the oxygen-evolving complex of Photosystem II (PS II). The range of manganese extended x-ray absorption fine structure data collected from PS II until now has been, however, limited by the presence of iron in PS II. Using a crystal spectrometer with high energy resolution to detect solely the manganese Kα fluorescence, we are able to extend the extended x-ray absorption fine structure range beyond the onset of the iron absorption edge. This results in improvement in resolution of the manganese-backscatterer distances in PS II from 0.14 to 0.09Å. The high resolution data obtained from oriented spinach PS II membranes in the S1 state show that there are three di-μ-oxo-bridged manganese-manganese distances of ∼2.7 and ∼2.8Å in a 2:1 ratio and that these three manganese-manganese vectors are aligned at an average orientation of ∼60° relative to the membrane normal. Furthermore, we are able to observe the separation of the Fourier peaks corresponding to the ∼3.2Å manganese-manganese and the ∼3.4Å manganese-calcium interactions in oriented PS II samples and determine their orientation relative to the membrane normal. The average of the manganese-calcium vectors at ∼3.4Å is aligned along the membrane normal, while the ∼3.2Å manganese-manganese vector is oriented near the membrane plane. A comparison of this structural information with the proposed Mn4Ca cluster models based on spectroscopic and diffraction data provides input for refining and selecting among these models.

Direct Detection of Oxygen Ligation to the Mn4Ca Cluster of Photosystem II by X‐ray Emission Spectroscopy

Direct Detection of Oxygen Ligation to the Mn 4 Ca Cluster of Photosystem II by X-ray Emission Spectroscopy Yulia Pushkar †,# , Xi Long †,‡ , Pieter Glatzel †,€ , Gary W. Brudvig § , G. Charles Dismukes ¶ , Terrence J. Collins

Focusing the view on nature's water-splitting catalyst

, Vittal K. Yachandra †,* , Junko Yano †,* , Uwe Bergmann ∆,* Physical Biosciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, § Dept. of Chemistry, Yale Univ., New Haven, CT, ¶ Dept. of Chemistry, Princeton Univ., Princeton, NJ,

Experimental demonstration of radicaloid character in a RuV=O intermediate in catalytic water oxidation

Dept. of Chemistry, Carnegie-Mellon Univ., Pittsburgh, PA, ∆ Stanford Synchrotron Radiation Lightsource, Menlo Park, CA. RECEIVED DATE (automatically inserted by publisher); vkyachandra@lbl.gov, jyano@lbl.gov, ubergmann@slac.stanford.edu Ligands play critical roles during the catalytic reactions in metalloproteins through bond formation/breaking, protonation/deprotonation, and electron/spin delocalization. While there are well-defined element-specific spectroscopic handles, such as X-ray spectroscopy and EPR, to follow the chemistry of metal catalytic sites in a large protein matrix, directly probing particular ligand atoms like C, N, and O is challenging due to their abundance in the protein. FTIR/Raman and ligand-sensitive EPR techniques such as ENDOR and ESEEM have been applied to study metal-ligand interactions. X-ray absorption spectroscopy (XAS) can also indirectly probe the ligand environment; its element-specificity allows us to focus only on the catalytic metal site, and EXAFS and XANES provide metal-ligand distances, coordination numbers, and symmetry of ligand environments. However, the information is limited, since one cannot distinguish among ligand elements with similar atomic number (i.e. C, N. and O). As an alternative and a more direct method to probe the specific metal-ligand chemistry in the protein matrix, we investigated the application of X-ray emission spectroscopy (XES). Using this technique we have identified the oxo-bridging ligands of the Mn 4 Ca complex of photosystem II (PS II), a multisubunit membrane protein, that catalyzes the water oxidizing reaction. 1 The catalytic mechanism has been studied intensively by Mn XAS. 2 The fundamental question of this reaction, however, is how the water molecules are ligated to the Mn 4 Ca cluster and how the O-O bond formation occurs before the evolution of O 2 . 3-5 This implies that it is necessary to follow the chemistry of the oxygen ligands in order to understand the mechanism. XES which is a complementary method to XAS, has the potential to directly probe ligation modes. 6 Among the several emission lines, Kβ 1,3 and Kβ′ lines originate from the metal 3p to 1s transition, and they have been used as an indicator of the charge and spin states on Mn in the OEC (Figure 1). 7,8 The higher energy region corresponds to valence to core transitions just below the Fermi level, and can be divided into the Kβ′′ and the Kβ 2,5 emission (Fig.1 left scheme). Kβ 2,5 emission is predominantly from ligand 2p (metal 4p) to metal 1s, and the Kβ′′ emission is assigned to a ligand 2s to metal 1s, and are referred to as crossover transitions. 9-11 Therefore, only direct ligands to the metal of interest are probed with Kβ ,2,5 /Kβ′′ emission; i.e. other C, N, and O atoms in the protein media do not contribute to the spectra. In this report, we focus on the Kβ′′ spectral region to characterize metal-ligand interactions, in particular contributions from ligated oxygens. The energy of the Kβ′′ transition is dependent on the difference between the metal 1s and ligand 2s binding energies, which is dependent on the environment of the Present addresses: # Dept. of Physics, Purdue Univ., West Lafayette, IN 47904; ‡ Dept. of Chemistry, Univ. of California, Santa Cruz, CA 95064; ESRF, BP 220, 38043 Grenoble Cedex, France. Figure 1. (A) Energy diagram of Mn Kβ transitions in MnO. The Kβ′′ and Kβ 2,5 transitions are from valence molecular orbitals, Kβ′′ is O 2s to Mn 1s ‘cross-over’ transition. (B) Logarithmic plot of MnO Kβ spectrum. The O-Mn cross-over Kβ′′ transition is highlighted. ligand due to orbital hybridization. Therefore the Kβ′′ energy is affected by the charge density on the metal, the ligand protonation state, and changes in the coordination environment. The Kβ′′ intensity is influenced by the spatial overlap between the wavefunction that describes the Mn 1s orbital and the molecular orbitals on the ligands. The Kβ′′ intensity is affected by the metal to ligand distance, and the number of ligands per metal ion. Shorter distances (e.g. from higher bond order or deprotonation) result in increased Kβ′′ intensity with an approximate exponential dependence. 9 On the other hand, a spread of the molecular wavefunction over next-nearest neighbor atoms will decrease the Kβ′′ spectral intensity. Therefore contribution from single atom ligands such as oxo-bridges, or terminal oxo ligands bonded to Mn is predominant (see below). These combination of factors makes the Kβ′′ spectrum a powerful tool for detection and characterization of oxo-bridges in the Mn 4 Ca cluster of PS II. However, because of the weak intensity of the Kβ′′ spectrum obtaining such spectra from biological samples as dilute as PS II (800µM Mn) has been difficult. For O ligation in a typical model compound, the signal is ~10 3 times weaker than that of Kα and there is an additional large background from both the Kβ 1,3 and the Kβ 2,5 spectral features (Fig. 1). Furthermore the work is challenging because of the high sensitivity of the Mn 4 Ca cluster to radiation damage. 12 This study of PS II became possible by using a new high resolution spectrometer equipped with 8-14 analyzer crystals collecting a large solid angle (Suppl. Info.). Fig. 2 shows the Kβ′′ spectrum of a sample of PS II in the S 1 state compared with a series of Mn oxide spectra. Each spectrum is normalized by the Kβ 1,3 peak intensity which is proportional to the number of Mn atoms in the system. The 1 st moment energy of

Electronic structural changes of Mn in the oxygen-evolving complex of photosystem II during the catalytic cycle.

Nature invented a catalyst about 3 Gyr ago, which splits water with high efficiency into molecular oxygen and hydrogen equivalents (protons and electrons). This reaction is energetically driven by sunlight and the active centre contains relatively cheap and abundant metals: manganese and calcium. This biological system therefore forms the paradigm for all man-made attempts for direct solar fuel production, and several studies are underway to determine the electronic and geometric structures of this catalyst. In this report we briefly summarize the problems and the current status of these efforts and propose a density functional theory-based strategy for obtaining a reliable high-resolution structure of this unique catalyst that includes both the inorganic core and the first ligand sphere.

High-resolution structure of the photosynthetic Mn4Ca catalyst from X-ray spectroscopy.

Water oxidation is the key half reaction in artificial photosynthesis. An absence of detailed mechanistic insight impedes design of new catalysts that are more reactive and more robust. A proposed paradigm leading to enhanced reactivity is the existence of oxyl radical intermediates capable of rapid water activation, but there is a dearth of experimental validation. Here, we show the radicaloid nature of an intermediate reactive toward formation of the O-O bond by assessing the spin density on the oxyl group by Electron Paramagnetic Resonance (EPR). In the study, an 17O-labeled form of a highly oxidized, short-lived intermediate in the catalytic cycle of the water oxidation catalyst cis,cis-[(2,2-bipyridine)2(H2O)RuIIIORuIII(OH2)(bpy)2]4+ was investigated. It contains Ru centers in oxidation states [4,5], has at least one RuV = O unit, and shows |Axx| = 60G 17O hyperfine splittings (hfs) consistent with the high spin density of a radicaloid. Destabilization of π-bonding in the d3 RuV = O fragment is responsible for the high spin density on the oxygen and its high reactivity.

Understanding the Electronic Structure of 4d Metal Complexes: From Molecular Spinors to L-Edge Spectra of a di-Ru Catalyst

The oxygen-evolving complex (OEC) in photosystem II (PS II) was studied in the S0 through S3 states using 1s2p resonant inelastic X-ray scattering spectroscopy. The spectral changes of the OEC during the S-state transitions are subtle, indicating that the electrons are strongly delocalized throughout the cluster. The result suggests that, in addition to the Mn ions, ligands are also playing an important role in the redox reactions. A series of Mn(IV) coordination complexes were compared, particularly with the PS II S3 state spectrum to understand its oxidation state. We find strong variations of the electronic structure within the series of Mn(IV) model systems. The spectrum of the S3 state best resembles those of the Mn(IV) complexes Mn3(IV)Ca2 and saplnMn2(IV)(OH)2. The current result emphasizes that the assignment of formal oxidation states alone is not sufficient for understanding the detailed electronic structural changes that govern the catalytic reaction in the OEC.