Low temperature magnetic circular dichroism (LT MCD) spectroscopy in combination with quantum-chemical calculations are used to define the electronic structure associated with the geometric structure of the Fe(IV)═O intermediate in SyrB2 that was previously determined by nuclear resonance vibrational spectroscopy. These studies elucidate key frontier molecular orbitals (FMOs) and their contribution to H atom abstraction reactivity. The VT MCD spectra of the enzymatic S = 2 Fe(IV)═O intermediate with Br(-) ligation contain information-rich features that largely parallel the corresponding spectra of the S = 2 model complex (TMG3tren)Fe(IV)═O (Srnec, M.; Wong, S. D.; England, J; Que, L; Solomon, E. I. Proc. Natl. Acad. Sci. USA 2012, 109, 14326-14331). However, quantitative differences are observed that correlate with π-anisotropy and oxo donor strength that perturb FMOs and affect reactivity. Due to π-anisotropy, the Fe(IV)═O active site exhibits enhanced reactivity in the direction of the substrate cavity that proceeds through a π-channel that is controlled by perpendicular orientation of the substrate C-H bond relative to the halide-Fe(IV)═O plane. Also, the increased intrinsic reactivity of the SyrB2 intermediate relative to the ferryl model complex is correlated to a higher oxyl character of the Fe(IV)═O at the transition states resulting from the weaker ligand field of the halogenase.

Department of Chemistry Pennsylvania State University University Park Pennsylvania 16802 United States

Department of Chemistry Stanford University Stanford California 94305 5080 United States

J Heyrovský Institute of Physical Chemistry The Czech Academy of Sciences Dolejškova 2155 3 182 23 Prague 8 Czech Republic

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Matthews ML, Neumann CS, Miles LA, Grove TL, Booker SJ, Krebs C, Walsh CT, Bollinger JM., Jr Proc Natl Acad Sci U S A. 2009;106:17723–17728. PubMed PMC

Price JC, Barr EW, Tirupati B, Bollinger JM, Jr, Krebs C. Biochemistry. 2003;42:7497–7508. PubMed

Riggs-Gelasco PJ, Price JC, Guyer RB, Brehm JH, Barr EW, Bollinger JM, Jr, Krebs C. J Am Chem Soc. 2004;126:8108–8109. PubMed

Hoffart LM, Barr EW, Guyer RB, Bollinger JM, Jr, Krebs C. Proc Natl Acad Sci U S A. 2006;103:14738–14743. PubMed PMC

Galonić DP, Barr EW, Walsh CT, Bollinger JM, Jr, Krebs C. Nat Chem Biol. 2007;3:113–116. PubMed

Fujimori DG, Barr EW, Matthews ML, Koch GM, Yonce JR, Walsh CT, Bollinger JM, Jr, Krebs C, Riggs-Gelasco PJ. J Am Chem Soc. 2007;129:13408–13409. PubMed

Matthews ML, Krest CM, Barr EW, Vaillancourt FH, Walsh CT, Green MT, Krebs C, Bollinger JM., Jr Biochemistry. 2009;48:4331–4343. PubMed PMC

Chang W, Guo Y, Wang C, Butch SE, Rosenzweig AC, Boal AK, Krebs C, Bollinger JM., Jr Science. 2014;343:1140–1144. PubMed PMC

Eser BE, Barr EW, Frantom PA, Saleh L, Bollinger JM, Jr, Krebs C, Fitzpatrick PF. J Am Chem Soc. 2007;129:11334–11335. PubMed PMC

Panay AJ, Lee M, Krebs C, Bollinger JM, Jr, Fitzpatrick PF. Biochemistry. 2011;50:1928–1933. PubMed PMC

Blasiak LC, Vaillancourt FH, Walsh CT, Drennan CL. Nature. 2006;440:368–371. PubMed

Vaillancourt FH, Yin J, Walsh CT. Proc Natl Acad Sci U S A. 2005;102:10111–10116. PubMed PMC

McDonald AR, Que L., Jr Coord Chem Rev. 2013;257:414–428.

Jackson TA, Rohde JU, Seo MS, Sastri CV, DeHont R, Ohta T, Kitagawa T, Münck E, Nam W, Que L., Jr J Am Chem Soc. 2008;130:12394–12407. PubMed PMC

Martinho M, Banse F, Bartoli JF, Mattioli TA, Battioni P, Horner O, Bourcier S, Girerd JJ. Inorg Chem. 2005;44:9592–9596. PubMed

Kaizer J, Klinker EJ, Oh NY, Rohde JU, Song WJ, Stubna A, Kim J, Münck E, Nam W, Que L., Jr J Am Chem Soc. 2004;126:472–473. PubMed

England J, Bigelow JO, Van Heuvelen KM, Farquhar ER, Martinho M, Meier KK, Frisch JR, Münck E, Que L., Jr Chem Sci. 2014;5:1204–1215. PubMed PMC

Comba P, Fukuzumi S, Kotani S, Wunderlich S. Angew Chem, Int Ed. 2010;49:2622–2625. PubMed

Rohde J-U, Stubna A, Bominaar EL, Münck E, Nam W, Que L., Jr Inorg Chem. 2006;45:6435–6445. PubMed

Planas O, Clemancey M, Latour J-M, Company A, Costas M. Chem Commun. 2014;50:10887–10890. PubMed

England J, Guo Y, Farquhar ER, Young VG, Jr, Münck E, Que L., Jr J Am Chem Soc. 2010;132:8635–8644. PubMed PMC

Biswas AN, Puri M, Meier KK, Oloo WN, Rohde GT, Bominaar EL, Münck E, Que L., Jr J Am Chem Soc. 2015;137:2428–2431. PubMed

Lacy DC, Gupta R, Stone KL, Greaves J, Ziller JW, Hendrich MP, Borovik AS. J Am Chem Soc. 2010;132:12188–12190. PubMed PMC

England J, Guo Y, Van Heuvelen KM, Cranswick MA, Rohde GT, Bominaar EL, Münck E, Que L., Jr J Am Chem Soc. 2011;133:11880–11883. PubMed PMC

Srnec M, Wong SD, England J, Que L, Jr, Solomon EI. Proc Natl Acad Sci U S A. 2012;109:14326–14331. PubMed PMC

Decker A, Rohde JU, Klinker EJ, Wong SD, Que L, Jr, Solomon EI. J Am Chem Soc. 2007;129:15983–15996. PubMed PMC

Solomon EI, Light KM, Liu LV, Srnec M, Wong SD. Acc Chem Res. 2013;46:2725–2739. PubMed PMC

Shaik S, Chen H, Janardanan D. Nat Chem. 2011;3:19–27. PubMed

Ye S, Neese F. Proc Natl Acad Sci U S A. 2011;108:1228–1233. PubMed PMC

Neidig ML, Decker A, Choroba OW, Huang F, Kavana M, Moran GR, Spencer JB, Solomon EI. Proc Natl Acad Sci U S A. 2006;103:12966–12973. PubMed PMC

Decker A, Clay MD, Solomon EI. J Inorg Biochem. 2006;100:697–706. PubMed

Wong SD, Srnec M, Matthews ML, Liu LV, Kwak Y, Park K, Bell CB, III, Alp EE, Zhao J, Yoda Y, Kitao S, Seto M, Krebs C, Bollinger JM, Jr, Solomon EI. Nature. 2013;499:320–323. PubMed PMC

Diebold AR, Brown-Mashall CD, Neidig ML, Brownlee JM, Moran GR, Solomon EI. J Am Chem Soc. 2011;133:18148–18160. PubMed PMC

The PyMOL Molecular Graphics System, Version 1.5.0.4. Schrödinger, LLC;

Chovancova E, Pavelka A, Benes P, Strnad O, Brezovsky J, Kozlikova B, Gora A, Sustr V, Klvana M, Medek P, Biedermannova L, Sochor J, Damborsky J. PLoS Comput Biol. 2012;8:e1002708. PubMed PMC

Ahlrichs R, Bär M, Häser M, Horn H, Kölmel C. Chem Phys Lett. 1989;162:165–169.

Becke AD. Phys Rev A: At, Mol, Opt Phys. 1988;38:3098–3100. PubMed

Grimme S. J Comput Chem. 2004;25:1463–1473. PubMed

Grimme S. J Comput Chem. 2006;27:1787–1799. PubMed

Roos BO, Taylor PR, Siegbahn PEM. Chem Phys. 1980;48:157–173.

Siegbahn PEM, Almlöf J, Heiberg A, Roos BO. J Chem Phys. 1981;74:2384–2396.

Andersson K, Malmqvist P-Å, Roos BO, Sadlej AJ, Wolinski K. J Phys Chem. 1990;94:5483–5488.

Andersson K, Malmqvist P-Å, Roos BO. J Chem Phys. 1992;96:1218–1226.

Andersson K. Theor Chim Acta. 1995;91:31–46.

Finley J, Malmqvist P-Å, Roos BO, Serrano-Andrés L. Chem Phys Lett. 1998;288:299–306.

Aquilante F, De Vico L, Ferré N, Ghigo G, Malmqvist P-Å, Neogrády P, Pedersen TB, Pitoňák M, Reiher M, Roos BO, Serrano-Andrés L, Urban M, Veryazov V, Lindh R. J Comput Chem. 2010;31:224–247. PubMed

Douglas M, Kroll NM. Ann Phys (Amsterdam, Neth) 1974;82:89–155.

Hess BA. Phys Rev A: At, Mol, Opt Phys. 1986;33:3742–3748. PubMed

Jansen G, Hess BA. Phys Rev A: At, Mol, Opt Phys. 1989;39:6016–6017. PubMed

Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Mennucci B, Petersson GA, Nakatsuji H, Caricato M, Li X, Hratchian HP, Izmaylov AF, Bloino J, Zheng G, Sonnenberg JL, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Vreven T, Montgomery JA, Jr, Peralta JE, Ogliaro F, Bearpark M, Heyd JJ, Brothers E, Kudin KN, Staroverov VN, Kobayashi R, Normand J, Raghavachari K, Rendell A, Burant JC, Iyengar SS, Tomasi J, Cossi M, Rega N, Millam JM, Klene M, Knox JE, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Martin RL, Morokuma K, Zakrzewski VG, Voth GA, Salvador P, Dannenberg JJ, Dapprich S, Daniels AD, Farkas Ö, Foresman JB, Ortiz JV, Cioslowski J, Fox DJ. Gaussian G09, revision D.01. Gaussian Inc; Wallingford, CT: 2009.

Malmqvist P-Å, Rendell A, Roos BO. J Phys Chem. 1990;94:5477–5482.

Pierloot K. Mol Phys. 2003;101:2083–2094.

Hess BA, Marian CM, Wahlgren U, Gropen O. Chem Phys Lett. 1996;251:365–371.

Schimmelpfennig B. AMFI Program. University of Stockholm; Stockholm: 1996.

Malmqvist P-Å, Roos BO, Schimmelphennig B. Chem Phys Lett. 2002;357:230–240.

Roos BO, Andersson K. Chem Phys Lett. 1995;245:215–243.

Forsberg N, Malmqvist P-Å. Chem Phys Lett. 1997;274:196–204.

Neese F, Solomon EI. Inorg Chem. 1999;38:1847–1865. PubMed

Decker A, Rohde JU, Que L, Jr, Solomon EI. J Am Chem Soc. 2004;126:5378–5379. PubMed

Wayner DDM, Clark KB, Rauk A, Yu D, Armstrong DA. J Am Chem Soc. 1997;119:8925–8932.

Burkey TJ, Castelhano AL, Griller D, Lossing FP. J Am Chem Soc. 1983;105:4701–4703.

Marcus RA. J Phys Chem. 1968;72:891–899.

Gilmore K, Alabugin IV. Chem Rev. 2011;111:6513–6556. PubMed

Nuclear Resonance Vibrational Spectroscopic Definition of the Facial Triad FeIV═O Intermediate in Taurine Dioxygenase: Evaluation of Structural Contributions to Hydrogen Atom Abstraction

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