Possible Peroxo State of the Dicopper Site of Particulate Methane

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Possible Peroxo State of the Dicopper Site of Particulate Methane Monooxygenase from Combined Quantum Mechanics and Molecular Mechanics Calculations Shuhei Itoyama,† Kazuki Doitomi,† Takashi Kamachi,† Yoshihito Shiota,† and Kazunari Yoshizawa*,†,‡ †

Institute for Materials Chemistry and Engineering, Kyushu University, Fukuoka 819-0395, Japan Elements Strategy Initiative for Catalysts and Batteries, Kyoto University, Kyoto 615-8245, Japan

‡

S Supporting Information *

ABSTRACT: Enzymatic methane hydroxylation is proposed to efficiently occur at the dinuclear copper site of particulate methane monooxygenase (pMMO), which is an integral membrane metalloenzyme in methanotrophic bacteria. The resting state and a possible peroxo state of the dicopper active site of pMMO are discussed by using combined quantum mechanics and molecular mechanics calculations on the basis of reported X-ray crystal structures of the resting state of pMMO by Rosenzweig and coworkers. The dicopper site has a unique structure, in which one copper is coordinated by two histidine imidazoles and another is chelated by a histidine imidazole and primary amine of an N-terminal histidine. The resting state of the dicopper site is assignable to the mixed-valent CuICuII state from a computed Cu−Cu distance of 2.62 Å from calculations at the B3LYP-D/TZVP level of theory. A μ-η2:η2-peroxo-CuII2 structure similar to those of hemocyanin and tyrosinase is reasonably obtained by using the resting state structure and dioxygen. Computed Cu−Cu and O−O distances are 3.63 and 1.46 Å, respectively, in the open-shell singlet state. Structural features of the dicopper peroxo species of pMMO are compared with those of hemocyanin and tyrosinase and synthetic dicopper model compounds. Optical features of the μ-η2:η2peroxo-CuII2 state are calculated and analyzed with TD-DFT calculations.

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INTRODUCTION Methanotrophic bacteria oxidize methane using molecular dioxygen to form methanol, formaldehyde, formic acid, and finally carbon dioxide.1 In the initial stages of the oxidation pathway, methane is converted into methanol by methane monooxygenase (MMO) under physiological conditions. This initial methane oxidation is conducted by methanotrophs such as Methylococcus capsulatus (Bath) and Methylosinus trichosporium OB3b. In both species of methanotrophs, two different forms are known to exist under different conditions, a soluble form of MMO (sMMO) and a particulate form of MMO (pMMO). The well-characterized former form has a diiron active site for methane hydroxylation,2−5 while the latter form is a copper-containing membrane protein.6,7 In contrast to sMMO, the structure and reactivity of pMMO are not well characterized because of the difficulty in handling purified pMMO. Structural analysis of pMMO from Methylococcus capsulatus (Bath) revealed that the enzyme consists of three subunits, pmoB, pmoA, and pmoC, organized in an α3β3γ3 trimer.8 The pMMO active site is considered to contain two Cu ions with a Cu−Cu distance of about 2.58 Å within the pmoB subunit. One copper is coordinated by two histidine imidazoles, and another is chelated by a histidine imidazole and primary amine of an N-terminal histidine, as shown in Scheme 1. The ligation of primary amine is uncommon in biological dicopper enzymes. © XXXX American Chemical Society

Scheme 1. Possible Formation of a Peroxo Species in the Dicopper Site of pMMO

There is debate with respect to the reactivity of the dicopper site to methane hydroxylation. Rosenzweig and co-workers9 recently detected a putative oxygenated pMMO by optical spectroscopy and suggested that an absorbance peak at 345 nm is similar to those of the μ-η2:η2-peroxo-CuII2 species formed in dicopper enzymes and synthetic model compounds.10 In solution, there is possibly an equilibrium between this peroxo species and the high-valent bis(μ-oxo)CuIII2 species, which is relevant to the reactivity of dicopper-dioxygen species.11 In fact, a similar dioxo model species, in which the copper ions are coordinated by a histidine imidazole and primary amine, is able to abstract a H atom from secondary C−H bonds with bond dissociation energies (BDEs) of less than ∼80 kcal/mol; Received: November 11, 2015

A

DOI: 10.1021/acs.inorgchem.5b02603 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry

empirical formula by Grimme et al.34 The QM region contains the two Cu ions, His33, His137, His139, Tyr374, and Glu35 for the resting state, and, in addition, two oxygen atoms for the peroxo state. The CHARMm force field21,22 was run through the DL_POLY program35 to handle the MM part of the system. During the QM/MM calculations, the QM region and the MM region within a distance of 10 Å around the copper centers were relaxed and fully optimized. Link atoms were introduced to saturate the valence of the QM boundary atoms with the L2 scheme,36 where the linking H atom does not interact with the MM atoms of the adjacent neutral charge group. A standard electronic embedding scheme was chosen; the fixed MM atomic charges are included in the one-electron Hamiltonian of the QM calculations.37

however, its reactivity is not sufficient for the activation of the methyl C−H bond of toluene (BDE = 89 kcal/mol).12 The experimental observations are reasonable because the bis(μ-oxo)CuIII2 species is essentially a closed-shell system with limited reactivity toward stronger C−H bonds. The spin density of oxo species is highly correlated with the ability of the activation of the methane C−H bond (BDE = 104 kcal/mol).13 Therefore, it is necessary to consider a more reactive dicopperdioxygen species that can activate the methane C−H bond. We showed from DFT and quantum mechanics/molecular mechanics (QM/MM) calculations that the mixed-valent bis(μ-oxo)CuIICuIII and (μ-oxo)(μ-hydroxo)CuIICuIII species, which are equielectron systems with doublet spin state (S = 1/ 2), can abstract a H atom from methane with reasonable activation energies of less than 20 kcal/mol.14 We recently proposed that the tyrosine residue located in the second coordination sphere of the dicopper site of pMMO donates a H atom to the μ-η2:η2-peroxo-CuII2 species and the resultant (μoxo)(μ-hydroxo)CuIICuIII species can effectively abstract a H atom from methane.14d Chan and co-workers15 proposed that a mixed-valent trinuclear CuIICuIIICuIII cluster, based on X-ray absorption edge and EPR experiments, should play a role for methane hydroxylation by pMMO. Recently, they reported that trinuclear synthetic model complexes can actually oxidize methane.15c In this Article, we report structural features of the μ-η2:η2peroxo-CuII2 species of pMMO to compare with those of hemocyanin and tyrosinase and synthetic dicopper model complexes. It is a key intermediate or a precursor that can generate a more reactive dicopper-dioxygen species for methane hydroxylation. Our present QM/MM study is useful for the characterization of the possible peroxo species in the dicopper site of pMMO.9

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RESULTS AND DISCUSSION A computed Cu−Cu distance in the CuICuI state in a previous cluster model was 3.63 Å.14d Protein environmental effects were not considered in this cluster model. A possible reason for this long Cu−Cu distance in the CuICuI state would be a Coulomb repulsion between the two CuI ions. Therefore, we first optimized the resting state structure of pMMO using the structure of PDB code 1YEW following the procedure described above. Figure 1 (left) shows a structure of the

Figure 1. QM/MM optimized structures of the resting state of the dicopper site of pMMO, in which the two copper ions are assumed to be in the oxidation state of CuI2 (left) and CuICuII (right) at the B3LYP-D/TZVP level of theory.

METHOD OF CALCULATION

We built structures of the resting state on the basis of the X-ray crystal structure (PDB code 1YEW) and the peroxo state by adding dioxygen to the resting state. A model having 13 052 atoms was used for the following calculations. The protonation states of titratable residues at pH 6 were estimated by the generalized-Born method.16−18 The protonation states were cross-checked with another pKa prediction program, PROPKA3.1.19,20 After the prediction of protonation states, the hydrogen atoms are equilibrated (15 ps of heating to 300 K and 15 ps of equilibration run) and then minimized with 1000 steps of the steepest descent minimization. The system was relaxed by performing MD simulations at the CHARMm level of theory.21,22 The whole system was heated from 50 to 300 K with harmonic restraints by using a force constant of 5 kcal (mol Å2)−1 for the protein backbone, 2.5 kcal (mol Å2)−1 for the side chains. The heating time was 15 ps with a 1 fs time step. The system was then equilibrated at 300 K for 300 ps. The harmonic restraints used in the heating step were retained for the first 25 ps equilibration. They were reduced to half of the initial values during the second 25 ps. The harmonic constraints for side chains were removed during the third 25 ps, and no harmonic constraints were used in the last 225 ps. Finally, we extracted the final structure (300 ps) in the equilibration trajectory, which was minimized with the conjugated gradient minimization for 5000 steps. During the initial minimization and MD simulation, the structures of the monocopper site, the dicopper site, and the first coordination residues (three Cu ions, His33, His48, His72, His137, and His139) were kept fixed. These histidine residues coordinate to the Cu ions. All the MD simulations were carried out with Discovery Studio 3.5.23 Subsequent QM/MM calculations were performed with the ChemShell software24 by integrating the TURBOMOLE package25 for QM calculations at the B3LYP-D,26−29 BP86-D,26,30 B97-D,31 and M06-D32 functionals with the TZVP33 basis set. Dispersion corrections were added by using the

resting state of pMMO, in which the CuI−CuI distance is optimized to be 2.50 Å at the B3LYP-D/TZVP level of theory. Since those of PDB codes 1YEW, 3RFR, and 3RGB are 2.58, 2.71, and 2.65 Å, respectively, the QM/MM optimized CuI− CuI distance of 2.50 Å is a little short in comparison with these X-ray crystal structures. Since resolution is relatively high in the analysis of 3RGB (revised 1YEW), the Cu−Cu distance of approximately 2.6 Å is probably a reasonable value for the resting state at present; in contrast, the Cu−Cu distance in PDB code 3CHX is exceptionally long, 3.13 Å. An isolated pMMO from a third organism Methylocystis species strain M was reported to contain a mixture of CuI and CuII on the basis of electron paramagnetic resonance (EPR) signals.38 We, therefore, looked at the Cu−Cu distances in the CuICuI and CuICuII states. Table 1 summarizes optimized Cu−Cu distances in the different oxidation states at the B3LYP-D, BP86-D, B97-D, and M06-D levels of theory combined with the TZVP basis set. The Cu−Cu distances in the CuICuII state are approximately 0.1 Å longer than those of the CuICuI state in general, due to increased Coulomb repulsions in the CuICuII state. A clear-cut conclusion cannot be derived from the computed Cu−Cu distances for the assignment of the oxidation state of the resting state about the two Cu ions. Although the resting state of the B


Article

Inorganic Chemistry Table 1. Optimized Cu−Cu Distances in the Resting State of the Dicopper Site of pMMO at Some Levels of DFT Combined with the TZVP Basis Set by Using the Structure of PDB Code 1YEW as an Initial Geometry functional

CuI−CuI (Å)

CuI−CuII (Å)

B3LYP-D BP86-D B97-D M06-D

2.50 2.43 2.49 2.49

2.62 2.50 2.56 2.56

Table 2. List of Cu−Cu and O−O Distances in Å and Cu− O−O−Cu Dihedral Angles (τ) in Degrees for QM/MM Optimized Structures of the Dicopper Site of pMMO and Xray Crystal Structures of Dicopper Enzymes and Synthetic Model Complexes this work pMMO enzymes hemocyanin

active sites of dicopper enzymes is usually assumed to be CuICuI, it is assigned by EPR measurements to CuICuII in the dicopper site of pMMO, as mentioned above. In this sense, the resting state of the dicopper site is also assignable to the CuICuII state from the computed results. On the basis of the computational results on the resting state, we next optimized the structure of the μ-η2:η2-peroxo-CuII2 state and compared with those of hemocyanin and tyrosinase and synthetic dicopper model complexes. Figure 2 shows an

tyrosinase

Cu−Cu

O−O

τ

triplet singlet

3.70 3.63

1.40 1.46

138.1 159.8

1OXY39 1NOL40 1WX241 1WX441

3.59 3.62 3.48 3.55

1.41 1.36 1.48 1.50

156.3 172.1 145.2 140.8

3.56 3.48 3.52 3.37 3.52 3.27 3.53

1.41 1.49 1.37 1.50 1.49 1.50 1.54

180.0 163.3 171.9 151.6 168.4 132.4 180.0

model complexes Kitajima et al. (1989)42 Kodera et al. (1999)43 Lam et al. (2000)44 Hu et al. (2001)45 Kodera et al. (2004)46 Funahashi et al. (2008)47 Park et al. (2012)48

state are in good agreement with the measured ones of hemocyanin and tyrosinase. As seen in Table 2, the side-on peroxo Cu2O2 core has a bent-butterfly structure in general. We could not obtain a planar structure for the peroxo species in the DFT calculations; the bent-butterfly structure is thus energetically more favorable in the peroxo species. Karlin and coworkers49 demonstrated from X-ray absorption and Raman spectroscopy that a μ-η2:η2-peroxo-CuII2 species shows a bentbutterfly structure. This structural observation was rationalized later by orbital interaction analysis.50 Detailed geometrical data are summarized in the Supporting Information. An MO diagram in the broken-symmetry scheme, in which the α- and β-spin parts are calculated separately in the singlet state, for the peroxo species is shown in Figure 3. We carried out TD-DFT calculation at the B3LYP-D/TZVP level of theory using a cluster model of the μ-η2:η2-peroxo-CuII2 state to look at and analyze the optical absorption. Rosenzweig and co-workers9 recently detected a putative oxygenated pMMO by optical spectroscopy and suggested that an absorbance peak at 345 nm is similar to those of the μ-η2:η2peroxo-CuII2 species formed in dicopper enzymes and synthetic model compounds. The TD-DFT calculation shows that the μη2:η2-peroxo-CuII2 species has a strong absorption peak at 370 nm, as shown in Figure 4. The calculated absorption peak position is 25 nm red-shifted compared with the experimental one at 345 nm. Rohrmüller et al. calculated the absorption spectrum for a synthetic μ-η2:η2-peroxo-CuII2 complex using TD-DFT calculations at various DFT levels and reported that calculations tend to underestimate the peak position of the synthetic peroxo complex by approximately 30 nm at the B3LYP level of theory.51 This band is assigned to derive from the HOMO-9 to LUMO transition in the β-spin part. In view of the MO diagram of Figure 3, the HOMO-9 and LUMO are the 150th and 160th orbitals, respectively, which are bonding and antibonding orbitals between the copper ions and the sideon O22−. Thus, the band at 370 nm in Figure 4 should be derived from the transition between these orbitals.

Figure 2. A QM/MM optimized structure of the μ-η2:η2-peroxo-CuII2 state of pMMO in the open-shell singlet state.

optimized structure of the side-on peroxo species in the openshell singlet state at the B3LYP-D/TZVP level of theory. The O−O distance was reasonably optimized to be 1.46 Å. This species can be viewed as an intermediate with antiferromagnetically coupled CuII ions, which can be reasonably calculated within the framework of the broken-symmetry scheme of DFT. We call this antiferromagnetic state as open-shell singlet because the relevant two orbitals are half opened. Since the triplet state lies 1.9 kcal/mol above the open-shell singlet state, the ground state is open-shell singlet as expected. Calculated spin densities are −0.45 and +0.44 for the Cu1 and Cu2 ions, respectively, and nearly zero for the bridging O1 and O2 atoms. Thus, spin density is substantially localized on the two CuII ions. Table 2 lists computed Cu−Cu and O−O bond distances and Cu−O−O−Cu dihedral angles of the dicopper site of pMMO at the B3LYP-D/TZVP level of theory in comparison with those of dicopper enzymes39−41 and synthetic model complexes.42−48 The Cu−Cu distance is 3.70 and 3.63 Å in the triplet and open-shell singlet states, respectively, and the O−O distance is 1.40 and 1.46 Å in the triplet and singlet states, respectively. The computed values in the open-shell singlet C


Article

Inorganic Chemistry

species. Our results and discussion about the reactivity to methane will be reported in due course.

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ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.inorgchem.5b02603. Computational details for the resting state and the μη2:η2-peroxo-CuII2 state (PDF)

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS This work was supported by Grants-in-Aid (Nos. 24109014, 24550190, and 15K13710) from Japan Society for the Promotion of Science (JSPS) and the Ministry of Education, Culture, Sports, Science and Technology of Japan (MEXT), the MEXT Projects of “Integrated Research on Chemical Synthesis” and “Elements Strategy Initiative to Form Core Research Center”, and JST-CREST. K.D. thanks JSPS for a graduate fellowship.

Figure 3. MO diagram of the peroxo state in the broken-symmetry scheme.

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REFERENCES

(1) Hanson, R. S.; Hanson, T. E. Microbiol. Rev. 1996, 60, 439−471. (2) Feig, A. L.; Lippard, S. J. Chem. Rev. 1994, 94, 759−805. (3) Lipscomb, J. D. Annu. Rev. Microbiol. 1994, 48, 371−399. (4) Wallar, B. J.; Lipscomb, J. D. Chem. Rev. 1996, 96, 2625−2657. (5) Merkx, M.; Kopp, D. A.; Sazinsky, M. H.; Blazyk, J. L.; Müller, J.; Lippard, S. J. Angew. Chem., Int. Ed. 2001, 40, 2782−2807. (6) Lieberman, R. L.; Shrestha, D. B.; Doan, P. E.; Hoffman, B. M.; Stemmler, T. L.; Rosenzweig, A. C. Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 3820−3825. (7) Chan, S. I.; Chen, K. H.-C.; Yu, S. S.-F.; Chen, C.-Li.; Kuo, S. S.-J. Biochemistry 2004, 43, 4421−4430. (8) Lieberman, R. L.; Rosenzweig, A. C. Nature 2005, 434, 177−182. (9) Culpepper, M. A.; Cutsail, G. E., III; Hoffman, B. M.; Rosenzweig, A. C. J. Am. Chem. Soc. 2012, 134, 7640−7643. (10) (a) Mirica, L. M.; Ottenwaelder, X.; Stack, T. D. P. Chem. Rev. 2004, 104, 1013−1046. (b) Lewis, E. A.; Tolman, W. B. Chem. Rev. 2004, 104, 1047−1076. (c) Itoh, S.; Fukuzumi, S. Acc. Chem. Res. 2007, 40, 592−600. (11) Kieber-Emmons, M. T.; Ginsbach, J. W.; Wick, P. K.; Lucas, H. R.; Helton, M. E.; Lucchese, B.; Suzuki, M.; Zuberbühler, A. D.; Karlin, K. D.; Solomon, E. I. Angew. Chem., Int. Ed. 2014, 53, 4935−4939. (12) Citek, C.; Gary, J. B.; Wasinger, E. C.; Stack, T. D. P. J. Am. Chem. Soc. 2015, 137, 6991−6994. (13) (a) Yoshizawa, K. Acc. Chem. Res. 2006, 39, 375−382. (b) Yoshizawa, K. Bull. Chem. Soc. Jpn. 2013, 86, 1083−1116. (14) (a) Yoshizawa, K.; Suzuki, A.; Shiota, Y.; Yamabe, T. Bull. Chem. Soc. Jpn. 2000, 73, 815−827. (b) Yoshizawa, K.; Shiota, Y. J. Am. Chem. Soc. 2006, 128, 9873−9881. (c) Shiota, Y.; Yoshizawa, K. Inorg. Chem. 2009, 48, 838−845. (d) Shiota, Y.; Juhász, G.; Yoshizawa, K. Inorg. Chem. 2013, 52, 7907−7917. (15) (a) Chan, S. I.; Wang, V. C.-C.; Lai, J. C.-H.; Yu, S. S.-F.; Chen, P. P.-Y.; Chen, K. H.-C.; Chen, C.-L.; Chan, M. K. Angew. Chem., Int. Ed. 2007, 46, 1992−1994. (b) Chan, S. I.; Yu, S. S.-F. Acc. Chem. Res. 2008, 41, 969−979. (c) Chan, S. I.; Lu, Y.-J.; Nagababu, P.; Maji, S.; Hung, M.-C.; Lee, M. M.; Hsu, I.-J.; Minh, P. D.; Lai, J. C.-H.; Ng, K. Y.; Ramalingam, S.; Yu, S. S.-F.; Chan, M. K. Angew. Chem., Int. Ed. 2013, 52, 3731−3735.

Figure 4. Observed optical spectrum for O2 adduct of pMMO9 and TD-DFT analysis for a QM/MM optimized structure of the μ-η2:η2peroxo-CuII2 state of pMMO. The vertical lines on the x-axis indicate calculated oscillator strengths. The y-axis is normalized to the main absorption peak.

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CONCLUSION We have calculated and analyzed the resting state and the μη2:η2-peroxo-CuII2 state of the dicopper site of pMMO using the QM/MM methodology. The calculated Cu−Cu distances in the resting state are 2.50 Å in the CuI2 state and 2.62 Å in the CuICuII state. Thus, the resting state of the dicopper site is assignable to the mixed-valent CuICuII state. Computed values of the Cu−Cu and O−O distances in the open-shell singlet state of the peroxo state are in good agreement with the measured ones of hemocyanin and tyrosinase and synthetic dicopper models. The TD-DFT calculation suggests that the measured 345 nm band is assignable to the transition from the bonding to antibonding orbitals between the copper ions and the side-on O22−. We are now working on the formation of a more reactive dicopper-dioxygen species from the peroxo D


Article

Inorganic Chemistry (16) Bashford, D.; Karplus, M. J. Phys. Chem. 1991, 95, 9556−9561. (17) Dominy, B. N.; Brooks, C. L., III. J. Phys. Chem. B 1999, 103, 3765−3773. (18) Spassov, V. Z.; Yan, L. Protein Sci. 2008, 17, 1955−1970. (19) (a) Li, H.; Robertson, A. D.; Jensen, J. H. Proteins: Struct., Funct., Bioinf. 2005, 61, 704−721. (b) Bas, D. C.; Rogers, D. M.; Jensen, J. H. Proteins: Struct., Funct., Bioinf. 2008, 73, 765−783. (20) (a) Olsson, M. H. M.; Søndergaard, C. R.; Rostkowski, M.; Jensen, J. H. J. Chem. Theory Comput. 2011, 7, 525−537. (b) Søndergaard, C. R.; Olsson, M. H. M.; Rostkowski, M.; Jensen, J. H. J. Chem. Theory Comput. 2011, 7, 2284−2295. (21) (a) Momany, F. A.; Rone, R. J. Comput. Chem. 1992, 13, 888− 900. (b) Momany, F. A.; Rone, R.; Kunz, H.; Frey, R. F.; Newton, S. Q.; Schäfer, L. J. Mol. Struct.: THEOCHEM 1993, 286, 1−18. (22) Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; States, D. J.; Swaminathan, S.; Karplus, M. J. Comput. Chem. 1983, 4, 187−217. (23) Discovery Studio 3.5; Accelrys Software Inc.: San Diego, CA, 2012. (24) ChemShell: A Computational Chemistry Shell; see www. chemshell.org. (25) Ahlrichs, R.; Bär, M.; Häser, M.; Horn, H.; Kölmel, C. Chem. Phys. Lett. 1989, 162, 165−169. (26) Becke, A. D. Phys. Rev. A: At., Mol., Opt. Phys. 1988, 38, 3098− 3100. (27) Becke, A. D. J. Chem. Phys. 1993, 98, 5648−5652. (28) Lee, C.; Yang, W.; Parr, R. G. Phys. Rev. B: Condens. Matter Mater. Phys. 1988, 37, 785−789. (29) Vosko, S. H.; Wilk, L.; Nusair, M. Can. J. Phys. 1980, 58, 1200− 1211. (30) Perdew, J. P. Phys. Rev. B: Condens. Matter Mater. Phys. 1986, 33, 8822−8824. (31) Grimme, S. J. Comput. Chem. 2006, 27, 1787−1799. (32) Zhao, Y.; Truhlar, D. G. Theor. Chem. Acc. 2008, 120, 215−241. (33) Schäfer, A.; Huber, C.; Ahlrichs, R. J. Chem. Phys. 1994, 100, 5829−5835. (34) Grimme, S.; Antony, J.; Ehrlich, S.; Krieg, H. J. Chem. Phys. 2010, 132, 154104. (35) Smith, W.; Forester, T. R. J. Mol. Graphics 1996, 14, 136−141. (36) Antes, I.; Thiel, W. Hybrid Quantum Mechanical and Molecular Mechanical Methods; Gao, J., Ed.; ACS Symposium Series 712; American Chemical Society: Washington, DC, 1998; pp 50−65. (37) Bakowies, D.; Thiel, W. J. Phys. Chem. 1996, 100, 10580−10594. (38) Culpepper, M. A.; Cutsail, G. E., III; Gunderson, W. A.; Hoffman, B. M.; Rosenzweig, A. C. J. Am. Chem. Soc. 2014, 136, 11767−11775. (39) Magnus, K. A.; Hazes, B.; Ton-That, H.; Bonaventura, C.; Bonaventura, J.; Hol, W. G. J. Proteins: Struct., Funct., Genet. 1994, 19, 302−309. (40) Hazes, B.; Magnus, K. A.; Bonaventura, C.; Bonaventura, J.; Dauter, Z.; Kalk, K. H.; Hol, W. G. J. Protein Sci. 1993, 2, 597−619. (41) Matoba, Y.; Kumagai, T.; Yamamoto, A.; Yoshitsu, H.; Sugiyama, M. J. Biol. Chem. 2006, 281, 8981−8990. (42) Kitajima, N.; Fujisawa, K.; Moro-oka, Y.; Toriumi, K. J. Am. Chem. Soc. 1989, 111, 8975−8976. (43) Kodera, M.; Katayama, K.; Tachi, Y.; Kano, K.; Hirota, S.; Fujinami, S.; Suzuki, M. J. Am. Chem. Soc. 1999, 121, 11006−11007. (44) Lam, B. M. T.; Halfen, J. A.; Young, V. G., Jr.; Hagadorn, J. R.; Holland, P. L.; Lledós, A.; Cucurull-Sánchez, L.; Novoa, J. J.; Alvarez, S.; Tolman, W. B. Inorg. Chem. 2000, 39, 4059−4072. (45) Hu, Z.; George, G. N.; Gorun, S. M. Inorg. Chem. 2001, 40, 4812−4813. (46) Kodera, M.; Kajita, Y.; Tachi, Y.; Katayama, K.; Kano, K.; Hirota, S.; Fujinami, S.; Suzuki, M. Angew. Chem., Int. Ed. 2004, 43, 334−337. (47) Funahashi, Y.; Nishikawa, T.; Wasada-Tsutsui, Y.; Kajita, Y.; Yamaguchi, S.; Arii, H.; Ozawa, T.; Jitsukawa, K.; Tosha, T.; Hirota, S.; Kitagawa, T.; Masuda, H. J. Am. Chem. Soc. 2008, 130, 16444−16445.

(48) Park, G. Y.; Qayyum, M. F.; Woertink, J.; Hodgson, K. O.; Hedman, B.; Narducci Sarjeant, A. A.; Solomon, E. I.; Karlin, K. D. J. Am. Chem. Soc. 2012, 134, 8513−8524. (49) Blackburn, N. J.; Strange, R. W.; Farooq, A.; Haka, M. S.; Karlin, K. D. J. Am. Chem. Soc. 1988, 110, 4263−4272. (50) Pidcock, E.; Obias, H. V.; Abe, M.; Liang, H.-C.; Karlin, K. D.; Solomon, E. I. J. Am. Chem. Soc. 1999, 121, 1299−1308. (51) Rohrmüller, M.; Herres-Pawlis, S.; Witte, M.; Schmidt, W. G. J. Comput. Chem. 2013, 34, 1035−1045.

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Possible Peroxo State of the Dicopper Site of Particulate Methane

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