Π-Frontier Molecular Orbitals in S ¼ 2 Ferryl Species and Elucidation of Their Contributions to Reactivity

π-Frontier molecular orbitals in S ¼ 2 ferryl species and elucidation of their contributions to reactivity Martin Srneca,1, Shaun D. Wonga,1, Jason Englandb, Lawrence Que, Jr.b,2, and Edward I. Solomona,2 aDepartment of Chemistry, Stanford University, Stanford, CA 94305; and bDepartment of Chemistry and Center for Metals in Biocatalysis, University of Minnesota, Minneapolis, MN 55455 Contributed by Edward I. Solomon, July 30, 2012 (sent for review June 19, 2012) S ¼ 2FeIV═O species are key intermediates in the catalysis of 1 (17) (Fig. 1A, Inset) and further correlated to density functional most nonheme iron enzymes. This article presents detailed spectro- theory (DFT) and multiconfigurational ab initio calculations to scopic and high-level computational studies on a structurally- elucidate the electronic structure and contribution of electronic defined S ¼ 2FeIV═O species that define its frontier molecular structure to reactivity. MCD spectroscopy provides a direct probe orbitals, which allow its high reactivity. Importantly, there are both of the reactive FMOs and, when applied to 1, reveals new S ¼ 2 π- and σ-channels for reaction, and both are highly reactive because π-channels at the transition state (TS). In the absence of a steric they develop dominant oxyl character at the transition state. These barrier (as would be the case for NHFe enzymes), these π-chan- π- and σ-channels have different orientation dependences defining nels would lead to new reactivity with interesting Fe spin-state how the same substrate can undergo different reactions (H-atom contributions. Furthermore, the MCD data reveal the presence abstraction vs. electrophilic aromatic attack) with FeIV═O sites in of extensive excited-state spin-orbit coupling (SOC) interactions different enzymes, and how different substrates can undergo dif- in the absorption spectrum—hitherto unobserved in other ferent reactions (hydroxylation vs. halogenation) with an FeIV═O FeIV═O species—that lead to interesting spectral consequences, species in the same enzyme. including a dip in the absorption (abs) band and different vibronic progressions within one excited state that reflect distorted poten- excited-state potential energy surfaces ∣ reaction coordinates ∣ magnetic tial energy surfaces (PES). circular dichroism ∣ density functional calculations ∣ multiconfigurational calculations Results MCD and Absorption Spectroscopy. Fig. 1 shows the UV-visible abs he key reactive intermediates in the catalytic cycles of many and VT MCD spectra of 1. The abs spectrum shows a weaker −1 −1 mononuclear nonheme iron (NHFe) enzymes are known to feature at 12;000 cm and an intense feature at 25;000 cm T −1 −1 be S ¼ 2 FeIV═O species capable of abstracting an H-atom with a shoulder at 19;000 cm . The abs band at 12;000 cm , from an inert C─H bond as strong as 106 kcal∕mol (1–5). These in fact, exhibits a dip in its intensity that corresponds to a sharp transient intermediates have been difficult to trap in appreciable positive feature in the MCD spectrum at the same energy (Fig. 1, concentrations amenable to spectroscopic studies, but recent vertical dashed line). These otherwise featureless abs bands developments hold promise for future geometric and electronic become much more well-resolved and feature-rich in the MCD structural characterization (4, 6). spectrum, which thus allows definitive band assignments for elec- The synthesis and structural characterization of stable biomi- tronic-structure elucidation. −1 metic model complexes have greatly aided in understanding the In the near-IR (NIR) 6;000–15;000 cm region of the MCD −1 geometric and electronic structures and reactivity of the FeIV═O spectra, three distinct bands centered around 11;500 cm can unit. A series of intermediate-spin S ¼ 1 FeIV═O model com- be identified: a positively signed Franck–Condon vibronic pro- plexes, supported by amine, pyridine, and deprotonated amido gression, a negatively signed vibronic progression, and a sharp ligands, has become available for structural, reactivity, and spec- positive feature (indicated by the dashed vertical line in Fig. 1) troscopic investigations (7–13). Recently, high-spin S ¼ 2 overlapping the positive progression. The temperature-depen- FeIV═O complexes have also become available, with two being dence behaviors of the two progressions indicate that they are structurally defined (14–20), but notably their reactivity does both (x, y)-polarized (analyzed in Scheme S1 and Fig. S1). This not surpass that of the most reactive S ¼ 1 complexes (15, 18, 21). pair of vibronic progressions forms a derivative-shaped pseudo-A S ¼ 1 FeIV═O complexes have been spectroscopically shown term (with its negative component at higher energy) that neces- Ã 5 to possess one channel for reactivity—the β-dxz∕yz π -frontier sarily results from in-state spin-orbit splitting of a E excited state IV molecular orbital (FMO) (22)—and the S ¼ 2 species had been of the S ¼ 2 Fe ═O species in C3v symmetry. Importantly, computationally predicted to have an additional σÃ-FMO for as indicated by brackets in Fig. 1B, the vibronic spacing of the reactivity by stabilization of its α-dz 2 orbital through spin polar- negative progression is considerably larger than that of the posi- ization (i.e., exchange stabilization) (22–24). In the S ¼ 2 com- tive progression (ν ¼ 880 and 710 cm−1, respectively). IV −1 plex ðTMG3trenÞFe ═O(1), which is the subject of this study, In the 15;000–30;000 cm region of the MCD spectrum, there Ã −1 it was shown that the accessibility of this α-dz 2 σ -FMO is are four bands under the envelope of the intense 25;000 cm restricted by an axial steric wall of methyl groups, giving a large absorption feature and its weaker low-energy shoulder. At steric contribution to its reaction barrier, rendering it only as 19;500 cm−1 and 23;500 cm−1, there are two z-polarized bands reactive as the S ¼ 1 complex ðN4PyÞFeIV═O (25). Importantly, ðN4PyÞFeIV═O also has a large steric barrier because the π-chan- ─ Author contributions: L.Q. and E.I.S. designed research; M.S., S.D.W., and J.E. performed nel requires an approach perpendicular to the Fe O bond for research; M.S., S.D.W., and E.I.S. analyzed data; and M.S., S.D.W., and E.I.S. wrote the orbital overlap, and this leads to the steric clash of the substrate paper. with the chelate ligand. In one case where the ligand completely The authors declare no conflict of interest. π S ¼ 1 σ excludes -approach, an complex can utilize a -channel 1M.S. and S.D.W. contributed equally to this work. S ¼ 2 for reactivity through a low-lying excited state (26). 2To whom correspondence may be addressed. E-mail: [email protected] or In this study, detailed variable-temperature (VT) magnetic [email protected]. circular dichroism (MCD) spectroscopic studies and analyses This article contains supporting information online at www.pnas.org/lookup/suppl/ are performed on the structurally defined S ¼ 2 model complex doi:10.1073/pnas.1212693109/-/DCSupplemental. 14326–14331 ∣ PNAS ∣ September 4, 2012 ∣ vol. 109 ∣ no. 36 www.pnas.org/cgi/doi/10.1073/pnas.1212693109 Downloaded by guest on October 2, 2021 Fig. 2. Spin-unrestricted MO energy-level diagram of 1 as determined by DFT calculations. Note the proximity in energy of the reactive α-dz 2 and β-dxz∕yz FMOs and the high-lying oxo π orbitals poised for oxo → Fe d CT. for the lowest-energy 5E excited state (Fig. 1B). In the MCD Fig. 1. (A) UV-visible absorption spectrum and (Inset) structure of 1.(B)VT spectrum two low-energy z-polarized CT transitions are observed MCD spectrum of 1 and (Inset) VT MCD data of a higher-concentration 23;500 −1— sample in the 16;000–22;000 cm−1 region allowing resolution of the vibronic at 19,500 and cm the former is assigned in MCD and progression. VT MCD spectra taken at 2, 10, 20, 40, and 80 K. Arrows show Absorption Spectroscopy based on polarization and vibronic intensity behavior of bands with respect to increasing temperature. structure as the lowest-energy oxo π → Fe CT transition. The TD-DFTcalculations predict that the two lowest oxo π → Fe CT (from the temperature dependence of the MCD data; Scheme S1 transitions are z-polarized at 23,000 and 27;000 cm−1 (Fig. S3); and Fig. S1) that can be assigned to charge-transfer (CT) transi- thus, the two low-energy CT transitions in MCD are assigned as tions on the basis of their small MCD-to-absorption intensity oxo π → Fe CT transitions, the lowest in energy being the oxo (C0∕D0) ratios of 0.040 and 0.002, respectively. In contrast, the π → d −1 xz∕yz CT. In addition, the TD-DFT calculations predict that C0∕D0 ratio of the pseudo-A term at 11;500 cm (vide supra)is there are several (x, y)-polarized CT transitions originating from 5E 0.250, which indicates that this state corresponds to the lowest- the oxo group and equatorial nitrogens; two of these could z −1 energy ligand-field (LF) transition. From its -polarization, the correspond to the CT bands in MCD at 25,500 and 27;500 cm , 19;500 −1 negative band at cm can be assigned as the lowest-energy but because of the uncertainty in the polarizations of these two CHEMISTRY π → oxo Fe CT transition. This has a vibronic progression with a MCD bands, no definitive assignments can be made. 490 −1 spacing of cm and an intensity distribution indicating an These TD-DFTassignments of the transitions for 1 are consis- ─ excited-state distortion of the Fe O bond of approximately tent with multireference CASPT2 calculations (SI Materials and 0.21 Å (Ta b l e S 1 ).

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