Coupled binuclear copper (CBC) sites are employed by many metalloenzymes to catalyze a broad set of biochemical transformations. Typically, the CBC catalytic sites are activated by the O2 molecule to form various [Cu2 O2 ] reactive species. This has also inspired synthesis and development of various biomimetic inorganic complexes featuring the CBC core. From theoretical perspective, the [Cu2 O2 ] reactivity often hinges on the side-on-peroxo-dicopper(II) (P) vs. bis-μ-oxo-dicopper(III) (O) isomerism - an equilibrium that has become almost iconic in theoretical bioinorganic chemistry. Herein, we present a comprehensive calibration and evaluation of the performance of various composite computational protocols available in contemporary computational chemistry, involving coupled-cluster and multireference (relativistic) wave function methods, popular density functionals and solvation models. Starting with the well-studied reference [Cu2 O2 (NH3 )6 ]2+ system, we compared the performance of electronic structure methods and discussed the relativistic effects. This allowed us to select several 'calibrated' DFT functionals that can be conveniently employed to study ten experimentally well-characterized [Cu2 O2 ] inorganic systems. We mostly predicted the lowest-energy structures (P vs. O) of the studied systems correctly. In addition, we present calibration of the used electronic structure methods for prediction of the spectroscopic features of the [Cu2 O2 ] core, mostly provided by the resonance Raman (rR) spectroscopy.

Faculty of Science Charles University Albertov 2038 6 Prague 2 128 43 Czech Republic

Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences Flemingovo náměstí 2 166 10 Praha 6 Czech Republic

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E. I. Solomon, D. E. Heppner, E. M. Johnston, J. W. Ginsbach, J. Cirera, M. Qayyum, M. T. Kieber-Emmons, C. H. Kjaergaard, R. G. Hadt, L. Tian, Chem. Rev. 2014, 114, 3659-3853.

C. E. Elwell, N. L. Gagnon, B. D. Neisen, D. Dhar, A. D. Spaeth, G. M. Yee, W. B. Tolman, Chem. Rev. 2017, 117, 2059-2107.

H. Decker, T. Schweikardt, D. Nillius, U. Salzbrunn, E. Jaenicke, F. Tuczek, Gene 2007, 398, 183-191.

Y. Matoba, T. Kumagai, A. Yamamoto, H. Yoshitsu, M. Sugiyama, J. Biol. Chem. 2006, 281, 8981-8990.

K. A. Magnus, B. Hazes, H. Ton-That, C. Bonaventura, J. Bonaventura, W. G. J. Hol, Proteins Struct. Funct. Genet. 1994, 19, 302-309.

J. M. Brown, L. Powers, B. Kincaid, J. A. Larrabee, T. G. Spiro, J. Am. Chem. Soc. 1980, 102, 4210-4216.

G. L. Woolery, L. Powers, M. Winkler, E. I. Solomon, K. Lerch, T. G. Spiro, Biochim. Biophys. Acta 1984, 788, 155-161.

E. Solem, F. Tuczek, H. Decker, Angew. Chem. Int. Ed. 2016, 55, 2884-2888;

Angew. Chem. 2016, 128, 2934-2938.

L. M. Mirica, M. Vance, D. J. Rudd, B. Hedman, K. O. Hodgson, E. I. Solomon, T. D. P. Stack, Science 2005, 308, 1890.

M. F. Qayyum, R. Sarangi, K. Fujisawa, T. D. P. Stack, K. D. Karlin, K. O. Hodgson, B. Hedman, E. I. Solomon, J. Am. Chem. Soc. 2013, 135, 17417-17431.

S. Binder, M. Salomone-Stagni, R. Haase, B. Schulz, A. Eich, G. Henkel, M. Rübhausen, S. Herres-Pawlis, W. Meyer-Klaucke, J. Phys. Conf. Ser. 2009, 190, 012201.

S. Herres-Pawlis, U. Flörke, G. Henkel, Eur. J. Inorg. Chem. 2005, 2005, 3815-3824.

K. D. Karlin, J. C. Hayes, Y. Gultneh, R. W. Cruse, J. W. McKown, J. P. Hutchinson, J. Zubieta, J. Am. Chem. Soc. 1984, 106, 2121-2128.

N. Kitajima, K. Fujisawa, C. Fujimoto, Y. Morooka, S. Hashimoto, T. Kitagawa, K. Toriumi, K. Tatsumi, A. Nakamura, J. Am. Chem. Soc. 1992, 114, 1277-1291.

N. Kitajima, K. Fujisawa, Y. Morooka, K. Toriumi, J. Am. Chem. Soc. 1989, 111, 8975-8976.

J. Serrano-Plana, I. Garcia-Bosch, A. Company, M. Costas, Acc. Chem. Res. 2015, 48, 2397-2406.

J. L. DuBois, P. Mukherjee, A. M. Collier, J. M. Mayer, E. I. Solomon, B. Hedman, T. D. P. Stack, K. O. Hodgson, J. Am. Chem. Soc. 1997, 119, 8578-8579.

C. X. Zhang, H.-C. Liang, E.-i. Kim, Q.-F. Gan, Z. Tyeklár, K.-C. Lam, A. L. Rheingold, S. Kaderli, A. D. Zuberbühler, K. D. Karlin, Chem. Commun. 2001, 137, 631-632.

H.-C. Liang, C. X. Zhang, M. J. Henson, R. D. Sommer, K. R. Hatwell, S. Kaderli, A. D. Zuberbühler, A. L. Rheingold, E. I. Solomon, K. D. Karlin, J. Am. Chem. Soc. 2002, 124, 4170-4171.

T. Osako, K. Ohkubo, M. Taki, Y. Tachi, S. Fukuzumi, S. Itoh, J. Am. Chem. Soc. 2003, 125, 11027-11033.

M. Taki, S. Teramae, S. Nagatomo, Y. Tachi, T. Kitagawa, S. Itoh, S. Fukuzumi, J. Am. Chem. Soc. 2002, 124, 6367-6377.

A. P. Cole, V. Mahadevan, L. M. Mirica, X. Ottenwaelder, T. D. P. Stack, Inorg. Chem. 2005, 44, 7345-7364.

D. Maiti, J. S. Woertink, A. A. Narducci Sarjeant, E. I. Solomon, K. D. Karlin, Inorg. Chem. 2008, 47, 3787-3800.

R. Haase, T. Beschnitt, U. Flörke, S. Herres-Pawlis, Inorg. Chim. Acta 2011, 374, 546-557.

M. T. Kieber-Emmons, J. W. Ginsbach, P. K. Wick, H. R. Lucas, M. E. Helton, B. Lucchese, M. Suzuki, A. D. Zuberbühler, K. D. Karlin, E. I. Solomon, Angew. Chem. Int. Ed. 2014, 53, 4935-4939;

Angew. Chem. 2014, 126, 5035-5039.

J. A. Halfen, S. Mahapatra, E. C. Wilkinson, S. Kaderli, V. G. Young, L. Que, A. D. Zuberbühler, W. B. Tolman, Science 1996, 271, 1397.

G. J. Karahalis, A. Thangavel, B. Chica, J. Bacsa, R. B. Dyer, C. C. Scarborough, Inorg. Chem. 2016, 55, 1102-1107.

L. Q. Hatcher, M. A. Vance, A. A. Narducci Sarjeant, E. I. Solomon, K. D. Karlin, Inorg. Chem. 2006, 45, 3004-3013.

V. Mahadevan, Z. Hou, A. P. Cole, D. E. Root, T. K. Lal, E. I. Solomon, T. D. P. Stack, J. Am. Chem. Soc. 1997, 119, 11996-11997.

H. V. Obias, Y. Lin, N. N. Murthy, E. Pidcock, E. I. Solomon, M. Ralle, N. J. Blackburn, Y.-M. Neuhold, A. D. Zuberbühler, K. D. Karlin, J. Am. Chem. Soc. 1998, 120, 12960-12961.

V. Mahadevan, M. J. Henson, E. I. Solomon, T. D. P. Stack, J. Am. Chem. Soc. 2000, 122, 10249-10250.

J. Cahoy, P. L. Holland, W. B. Tolman, Inorg. Chem. 1999, 38, 2161-2168.

K. D. Karlin, M. S. Nasir, B. I. Cohen, R. W. Cruse, S. Kaderli, A. D. Zuberbuehler, J. Am. Chem. Soc. 1994, 116, 1324-1336.

E. Pidcock, H. V. Obias, C. X. Zhang, K. D. Karlin, E. I. Solomon, J. Am. Chem. Soc. 1998, 120, 7841-7847.

C. J. Cramer, M. Włoch, P. Piecuch, C. Puzzarini, L. Gagliardi, J. Phys. Chem. A 2006, 110, 1991-2004.

Y. Kurashige, J. Chalupský, T. N. Lan, T. Yanai, J. Chem. Phys. 2014, 141, 174111.

J. L. Lewin, D. E. Heppner, C. J. Cramer, J. Biol. Inorg. Chem. 2007, 12, 1221-1234.

D. G. Liakos, F. Neese, J. Chem. Theory Comput. 2011, 7, 1511-1523.

F. Neese, D. G. Liakos, S. Ye, J. Biol. Inorg. Chem. 2011, 16, 821-829.

Q. M. Phung, S. Wouters, K. Pierloot, J. Chem. Theory Comput. 2016, 12, 4352-4361.

M. Witte, S. Herres-Pawlis, Phys. Chem. Chem. Phys. 2017, 19, 26880-26889.

M. Rohrmüller, S. Herres-Pawlis, M. Witte, W. G. Schmidt, J. Comput. Chem. 2013, 34, 1035-1045.

S. Herres-Pawlis, P. Verma, R. Haase, P. Kang, C. T. Lyons, E. C. Wasinger, U. Flörke, G. Henkel, T. D. P. Stack, J. Am. Chem. Soc. 2009, 131, 1154-1169.

S. Herres-Pawlis, R. Haase, P. Verma, A. Hoffmann, P. Kang, T. D. P. Stack, Eur. J. Inorg. Chem. 2015, 2015, 5426-5436.

A. Hoffmann, S. Herres-Pawlis, Phys. Chem. Chem. Phys. 2016, 18, 6430-6440.

A. Hoffmann, S. Herres-Pawlis, Chem. Commun. 2014, 50, 403-405.

B. T. Op't Holt, M. A. Vance, L. M. Mirica, D. E. Heppner, T. D. P. Stack, E. I. Solomon, J. Am. Chem. Soc. 2009, 131, 6421-6438.

M. Rohrmüller, A. Hoffmann, C. Thierfelder, S. Herres-Pawlis, W. G. Schmidt, J. Comput. Chem. 2015, 36, 1672-1685.

University of Karlsruhe and Forschungszentrum Karlsruhe GmbH 1989-2007, p. http://www.turbomole.com.

D. Peng, M. Reiher, Theor. Chem. Acc. 2012, 131, 1081.

P. A. M. Dirac, R. H. Fowler, Proc. R. Soc. Lond. A Math. Phys. Sci. 1929, 123, 714-733.

J. P. Perdew, Y. Wang, Phys. Rev. B 1992, 45, 13244-13249.

J. C. Slater, Phys. Rev. 1951, 81, 385-390.

J. Tao, J. P. Perdew, V. N. Staroverov, G. E. Scuseria, Phys. Rev. Lett. 2003, 91, 146401.

P. Pollak, F. Weigend, J. Chem. Theory Comput. 2017, 13, 3696-3705.

S. Grimme, J. Antony, S. Ehrlich, H. Krieg, J. Chem. Phys. 2010, 132.

A. Klamt, G. Schüürmann, J. Chem. Soc. Perkin Trans. 2 1993, 799-805.

L. Noodleman, J. Chem. Phys. 1981, 74, 5737-5743.

L. Noodleman, E. R. Davidson, Chem. Phys. 1986, 109, 131-143.

J. P. Perdew, K. Burke, M. Ernzerhof, Phys. Rev. Lett. 1996, 77, 3865-3868.

A. D. Becke, Phys. Rev. A 1988, 38, 3098-3100.

J. P. Perdew, Phys. Rev. B 1986, 33, 8822-8824.

S. H. Vosko, L. Wilk, M. Nusair, Can. J. Phys. 1980, 58, 1200-1211.

S. Grimme, J. Comput. Chem. 2006, 27, 1787-1799.

V. N. Staroverov, G. E. Scuseria, J. Tao, J. P. Perdew, J. Chem. Phys. 2003, 119, 12129-12137.

A. D. Becke, J. Chem. Phys. 1993, 98, 5648-5652.

C. Lee, W. Yang, R. G. Parr, Phys. Rev. B 1988, 37, 785-789.

Y. Zhao, D. G. Truhlar, Theor. Chem. Acc. 2008, 120, 215-241.

T. Yanai, D. P. Tew, N. C. Handy, Chem. Phys. Lett. 2004, 393, 51-57.

A. V. Arbuznikov, M. Kaupp, J. Chem. Phys. 2014, 141, 204101.

D. F. Aycock, Org. Process Res. Dev. 2007, 11, 156-159.

Q. M. Phung, C. Martín-Fernández, J. N. Harvey, M. Feldt, J. Chem. Theory Comput. 2019, 15, 4297-4304.

A. S. Petit, R. C. R. Pennifold, J. N. Harvey, Inorg. Chem. 2014, 53, 6473-6481.

J. N. Harvey, M. Aschi, Faraday Discuss. 2003, 124, 129-143.

F. Weigend, R. Ahlrichs, Phys. Chem. Chem. Phys. 2005, 7, 3297-3305.

G. Li Manni, R. K. Carlson, S. Luo, D. Ma, J. Olsen, D. G. Truhlar, L. Gagliardi, J. Chem. Theory Comput. 2014, 10, 3669-3680.

R. K. Carlson, D. G. Truhlar, L. Gagliardi, J. Chem. Theory Comput. 2015, 11, 4077-4085.

K. Ruedenberg, M. W. Schmidt, M. M. Gilbert, S. T. Elbert, Chem. Phys. 1982, 71, 41-49.

B. O. Roos, in Adv. in Chem. Phys: Vol 69 (Eds.: K. P. Lawley), John Willy & Sons, Ltd., 1987, pp 399-445.

K. R. Shamasundar, G. Knizia, H. J. Werner, J. Chem. Phys. 2011, 135, 054101.

P.-O. Widmark, P.-Å. Malmqvist, B. O. Roos, Theor. Chim. Acta 1990, 77, 291-306.

B. O. Roos, R. Lindh, P.-Å. Malmqvist, V. Veryazov, P.-O. Widmark, J. Phys. Chem. A 2004, 108, 2851-2858.

B. O. Roos, R. Lindh, P.-Å. Malmqvist, V. Veryazov, P.-O. Widmark, J. Phys. Chem. A 2005, 109, 6575-6579.

M. Douglas, N. M. Kroll, Ann. Phys. 1974, 82, 89-155.

B. A. Hess, Phys. Rev. A 1986, 33, 3742-3748.

G. Jansen, B. A. Hess, Phys. Rev. A Gen. Phys. 1989, 39, 6016-6017.

F. Aquilante, J. Autschbach, R. K. Carlson, L. F. Chibotaru, M. G. Delcey, L. De Vico, I. Fdez Galván, N. Ferré, L. M. Frutos, L. Gagliardi, M. Garavelli, A. Giussani, C. E. Hoyer, G. Li Manni, H. Lischka, D. Ma, P. Malmqvist, T. Müller, A. Nenov, M. Olivucci, T. B. Pedersen, D. Peng, F. Plasser, B. Pritchard, M. Reiher, I. Rivalta, I. Schapiro, J. Segarra-Martí, M. Stenrup, D. G. Truhlar, L. Ungur, A. Valentini, S. Vancoillie, V. Veryazov, V. P. Vysotskiy, O. Weingart, F. Zapata, R. Lindh, J. Comput. Chem. 2016, 37, 506-541.

H.-J. Werner, P. J. Knowles, G. Knizia, F. R. Manby, M. Schütz, Wiley Interdiscip. Rev.: Comput. Mol. Sci. 2012, 2, 242-253.

S. Grimme, Eur. J. Chem. 2012, 18, 9955-9964.

F. Eckert, A. Klamt, L. Koch, S. Terzi, 19.0.0 (Revision 5239) ed., COSMOlogic GmbH & Co. KG 1999-2018, p. http://www.cosmologic.de.

J. D. Head, Int. J. Quantum Chem. 1997, 65, 827-838.

P. Å. Malmqvist, K. Pierloot, A. R. M. Shahi, C. J. Cramer, L. Gagliardi, J. Chem. Phys. 2008, 128, 204109.

M. F. Rode, H. J. Werner, Theor. Chem. Acc. 2005, 114, 309-317.

B. F. Gherman, C. J. Cramer, Coord. Chem. Rev. 2009, 253, 723-753.

M. Radoń, Phys. Chem. Chem. Phys. 2019, 21, 4854-4870.

M. Radoń, in Adv. Inorg. Chem., Vol. 73 (Eds.: R. van Eldik, R. Puchta), Academic Press 2019, pp. 221-264.

G. Drabik, J. Szklarzewicz, M. Radoń, Phys. Chem. Chem. Phys. 2021, 23, 151-172.

Q. M. Phung, M. Feldt, J. N. Harvey, K. Pierloot, J. Chem. Theory Comput. 2018, 14, 2446-2455.

Coupled Binuclear Copper Sites in Biology: An Experimentally-Calibrated Computational Perspective

Elucidation of the tyrosinase/O2/monophenol ternary intermediate that dictates the monooxygenation mechanism in melanin biosynthesis