Tuning the Type 1 Reduction Potential of Multicopper Oxidases: Uncoupling the Effects of Electrostatics and H-Bonding to Histidine Ligands

Singha, Asmita; Sekretareva, Alina; Tao, Lizhi; Lim, Hyeongtaek; Ha, Yang; Braun, Augustin; Jones, Stephen M.; Hedman, Britt; Hodgson, Keith O.; Britt, R. David; Kosman, Daniel J.; Solomon, Edward I.

doi:10.1021/jacs.3c03241

Title: Tuning the Type 1 Reduction Potential of Multicopper Oxidases: Uncoupling the Effects of Electrostatics and H-Bonding to Histidine Ligands

Journal Article · Fri Jun 09 00:00:00 EDT 2023 · Journal of the American Chemical Society

DOI:https://doi.org/10.1021/jacs.3c03241· OSTI ID:2001423

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^[1]; Tao, Lizhi ^[2];

^[1]; Ha, Yang ^[1];

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^[1]; Hedman, Britt ^[3]; Hodgson, Keith O. ^[4];

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Stanford Univ., CA (United States)
Univ. of California, Davis, CA (United States)
SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
Stanford Univ., CA (United States); SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)
Univ. at Buffalo, NY (United States)

In multicopper oxidases (MCOs), the type 1 (T1) Cu accepts electrons from the substrate and transfers these to the trinuclear Cu cluster (TNC) where O₂ is reduced to H₂O. The T1 potential in MCOs varies from 340 to 780 mV, a range not explained by the existing literature. Here, this study focused on the ~350 mV difference in potential of the T1 center in Fet3p and Trametes versicolor laccase (TvL) that have the same 2His1Cys ligand set. A range of spectroscopies performed on the oxidized and reduced T1 sites in these MCOs shows that they have equivalent geometric and electronic structures. However, the two His ligands of the T1 Cu in Fet3p are H-bonded to carboxylate residues, while in TvL they are H-bonded to noncharged groups. Electron spin echo envelope modulation spectroscopy shows that there are significant differences in the second-sphere H-bonding interactions in the two T1 centers. Redox titrations on type 2-depleted derivatives of Fet3p and its D409A and E185A variants reveal that the two carboxylates (D409 and E185) lower the T1 potential by 110 and 255–285 mV, respectively. Density functional theory calculations uncouple the effects of the charge of the carboxylates and their difference in H-bonding interactions with the His ligands on the T1 potential, indicating 90–150 mV for anionic charge and ~100 mV for a strong H-bond. Finally, this study provides an explanation for the generally low potentials of metallooxidases relative to the wide range of potentials of the organic oxidases in terms of different oxidized states of their TNCs involved in catalytic turnover.

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Research Organization:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 2001423

Journal Information:: Journal of the American Chemical Society, Vol. 145, Issue 24; ISSN 0002-7863

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

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Resonance Raman spectra of blue copper proteins: assignments from normal mode calculations and copper-63/copper-65 and H2O/D2O shifts for stellacyanin and laccase Nestor, Lisa; Larrabee, James A.; Woolery, Geoffrey Biochemistry, Vol. 23, Issue 6 https://doi.org/10.1021/bi00301a008	journal	March 1984
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Industrial and biotechnological applications of laccases: A review Rodríguez Couto, Susana; Toca Herrera, José Luis Biotechnology Advances, Vol. 24, Issue 5 https://doi.org/10.1016/j.biotechadv.2006.04.003	journal	September 2006
Low-temperature magnetic circular dichroism studies of native laccase: spectroscopic evidence for exogenous ligand bridging at a trinuclear copper active site. Allendorf, M. D.; Spira, D. J.; Solomon, E. I. Proceedings of the National Academy of Sciences, Vol. 82, Issue 10 https://doi.org/10.1073/pnas.82.10.3063	journal	May 1985
The nuclear modulation effect in electron spin echoes for complexes of Cu ²⁺ and imidazole with ¹⁴ N and ¹⁵ N Mims, W. B.; Peisach, J. The Journal of Chemical Physics, Vol. 69, Issue 11 https://doi.org/10.1063/1.436479	journal	December 1978
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EasySpin, a comprehensive software package for spectral simulation and analysis in EPR Stoll, Stefan; Schweiger, Arthur Journal of Magnetic Resonance, Vol. 178, Issue 1, p. 42-55 https://doi.org/10.1016/j.jmr.2005.08.013	journal	January 2006
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