Terrence J. Collins

Fast Water Oxidation Using Iron

Photolysis of water, a long-studied strategy for storing solar energy, involves two half-reactions: the reduction of protons to dihydrogen and the oxidation of water to dioxygen. Proton reduction is well-understood, with catalysts achieving quantum yields of 34% when driven by visible light. Water oxidation, on the other hand, is much less advanced, typically involving expensive metal centers and rarely working in conjunction with a photochemically powered system. Before further progress can be made in the field of water splitting, significant developments in the catalysis of oxygen evolution are needed. Herein we present an iron-centered tetraamido macrocyclic ligand (Fe-TAML) that efficiently catalyzes the oxidative conversion of water to dioxygen. When the catalyst is combined in unbuffered solution with ceric ammonium nitrate, its turnover frequency exceeds 1.3 s(-1). Real-time UV-vis and oxygen monitoring of the active complex give insights into the reaction and decay kinetics.

FeIII–TAML-catalyzed green oxidative degradation of the azo dye Orange II by H2O2 and organic peroxides: products, toxicity, kinetics, and mechanisms

Oxidation of Orange II ([4-[(2-hydroxynaphtyl)azo]benzenesulfonic acid], sodium salt) by hydrogen peroxide catalyzed by iron(III) complexed to tetra amido macrocyclic ligands (FeIII–TAML activators) in aqueous solutions at pH 9–11 leads to CO2, CO, phthalic acid and smaller aliphatic carboxylic acids as major mineralization products. The products are non-toxic according to the Daphnia magna test. Several organic intermediates have been identified by HPLC and GC-MS that allowed the detailed description of Orange II degradation. The catalytic oxidation can also be performed by organic oxidants such as benzoyl peroxide, tert-butyl and cumyl hydroperoxides. Kinetic studies of the catalyzed oxidation indicated that FeIII–TAML activators react first with ROOR′ to form an oxidized catalyst (kI), which then oxidizes Orange II (kII). Neglecting the reversibility of the first step, the rate equation is rate = kIkII[FeIII][ROOR′][Dye]/(kI[ROOR′] + kII[Dye]); here FeIII and ROOR′ represent the catalyst and peroxide, respectively. The rate constant kI equals (74 ± 3) × 103, (1.4 ± 0.1) × 103, 24 ± 2, and 11 ± 1 M−1 s−1 for benzoyl peroxide, H2O2, t-BuOOH, and cumyl hydroperoxide at pH 9 and 25 °C, respectively. An average value of kII equals (3.1 ± 0.9) × 104 M−1 s−1 under the same conditions. The unraveling of the kinetic mechanism allows the comprehension of the robust reactivity, and this is discussed in detail using the representative results of DFT calculations.

Formation of a Room Temperature Stable Fe V (O) Complex: Reactivity Toward Unactivated C−H Bonds

An Fe(V)(O) complex has been synthesized from equimolar solutions of (Et4N)2[Fe(III)(Cl)(biuret-amide)] and mCPBA in CH3CN at room temperature. The Fe(V)(O) complex has been characterized by UV-vis, EPR, Mössbauer, and HRMS and shown to be capable of oxidizing a series of alkanes having C-H bond dissociation energies ranging from 99.3 kcal mol(-1) (cyclohexane) to 84.5 kcal mol(-1) (cumene). Linearity in the Bell-Evans-Polayni graph and the finding of a large kinetic isotope effect suggest that hydrogen abstraction is engaged the rate-determining step.

(TAML)FeIV═O Complex in Aqueous Solution: Synthesis and Spectroscopic and Computational Characterization

Recently, we reported the characterization of the S = (1)/ 2 complex [Fe (V)(O)B*] (-), where B* belongs to a family of tetraamido macrocyclic ligands (TAMLs) whose iron complexes activate peroxides for environmentally useful applications. The corresponding one-electron reduced species, [Fe (IV)(O)B*] (2-) ( 2), has now been prepared in >95% yield in aqueous solution at pH > 12 by oxidation of [Fe (III)(H 2O)B*] (-) ( 1), with tert-butyl hydroperoxide. At room temperature, the monomeric species 2 is in a reversible, pH-dependent equilibrium with dimeric species [B*Fe (IV)-O-Fe (IV)B*] (2-) ( 3), with a p K a near 10. In zero field, the Mössbauer spectrum of 2 exhibits a quadrupole doublet with Delta E Q = 3.95(3) mm/s and delta = -0.19(2) mm/s, parameters consistent with a S = 1 Fe (IV) state. Studies in applied magnetic fields yielded the zero-field splitting parameter D = 24(3) cm (-1) together with the magnetic hyperfine tensor A/ g nbeta n = (-27, -27, +2) T. Fe K-edge EXAFS analysis of 2 shows a scatterer at 1.69 (2) A, a distance consistent with a Fe (IV)O bond. DFT calculations for [Fe (IV)(O)B*] (2-) reproduce the experimental data quite well. Further significant improvement was achieved by introducing hydrogen bonding of the axial oxygen with two solvent-water molecules. It is shown, using DFT, that the (57)Fe hyperfine parameters of complex 2 give evidence for strong electron donation from B* to iron.

Prediction of high-valent iron K-edge absorption spectra by time-dependent Density Functional Theory

In recent years, a number of high-valent iron intermediates have been identified as reactive species in iron-containing metalloproteins. Inspired by the interest in these highly reactive species, chemists have synthesized Fe(IV) and Fe(V) model complexes with terminal oxo or nitrido groups, as well as a rare example of an Fe(VI)-nitrido species. In all these cases, X-ray absorption spectroscopy has played a key role in the identification and characterization of these species, with both the energy and intensity of the pre-edge features providing spectroscopic signatures for both the oxidation state and the local site geometry. Here we build on a time-dependent DFT methodology for the prediction of Fe K- pre-edge features, previously applied to ferrous and ferric complexes, and extend it to a range of Fe(IV), Fe(V) and Fe(VI) complexes. The contributions of oxidation state, coordination environment and spin state to the spectral features are discussed. These methods are then extended to calculate the spectra of the heme active site of P450 Compound II and the non-heme active site of TauD. The potential for using these methods in a predictive manner is highlighted.

Design of More Powerful Iron-TAML Peroxidase Enzyme Mimics

Environmentally useful, small molecule mimics of the peroxidase enzymes must exhibit very high reactivity in water near neutral pH. Here we describe the design and structural and kinetic characterization of a second generation of iron(III)-TAML activators with unprecedented peroxidase-mimicking abilities. Iterative design has been used to remove the fluorine that led to the best performers in first-generation iron-TAMLs. The result is a superior catalyst that meets a green chemistry objective by being comprised exclusively of biochemically common elements. The rate constants for bleaching at pH 7, 9, and 11 of the model substrate, Orange II, shows that the new Fe(III)-TAML has the fastest reactivity at pHs closer to neutral of any TAML activator to date. Under appropriate conditions, the new catalyst can decolorize Orange II without loss of activity for at least 10 half-lives, attesting to its exceptional properties as an oxidizing enzyme mimic.

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

On the reactivity of mononuclear iron(V)oxo complexes.

, 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,

Designing ligands to achieve robust oxidation catalysts. Iron based systems

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

Mechanistic considerations on the reactivity of green FeIII-TAML activators of peroxides

Ferric tetraamido macrocyclic ligand (TAML)-based catalysts [Fe{C(6)H(4)-1,2-(NCOCMe(2)NCO)(2)CR(2)}(OH(2))]PPh(4) [1; R = Me (a), Et (b)] are oxidized by m-chloroperoxybenzoic acid at -40 °C in acetonitrile containing trace water in two steps to form Fe(V)oxo complexes (2a,b). These uniquely authenticated Fe(V)(O) species comproportionate with the Fe(III) starting materials 1a,b to give μ-oxo-(Fe(IV))(2) dimers. The comproportionation of 1a-2a is faster and that of 1b-2b is slower than the oxidation by 2a,b of sulfides (p-XC(6)H(4)SMe) to sulfoxides, highlighting a remarkable steric control of the dynamics. Sulfide oxidation follows saturation kinetics in [p-XC(6)H(4)SMe] with electron-rich substrates (X = Me, H), but changes to linear kinetics with electron-poor substrates (X = Cl, CN) as the sulfide affinity for iron decreases. As the sulfide becomes less basic, the Fe(IV)/Fe(III) ratio at the end of reaction for 2b suggests a decreasing contribution of concerted oxygen-atom transfer (Fe(V) → Fe(III)) concomitant with increasing electron transfer oxidation (Fe(V) → Fe(IV)). Fe(V) is more reactive toward PhSMe than Fe(IV) by 4 orders of magnitude, a gap even larger than that known for peroxidase Compounds I and II. The findings reinforce prior work typecasting TAML activators as faithful peroxidase mimics.