Coordination dynamics of iron enables the selective C-N coupling but bypasses unwanted C-H hydroxylation in Fe(II)/α-ketoglutarate- dependent non-heme enzymes

doi:10.1016/S1872-2067(24)60064-1

Abstract

Abstract:

Non-heme Fe(II)/α-ketoglutarate (αKG)-dependent enzymes catalyze numerous C-H activation and functionalization reactions. However, how αKG-dependent non-heme enzymes catalyzed C-H functionalization beyond the hydroxylation is largely unknown. Here, we addressed this issue in Fe(II)/ αKG-dependent oxygenase TqaL_Nc, which catalyzes the selective C-H amination but bypasses the thermodynamically favored C-H hydroxylation. Here, the extensive computational studies have shown that the aziridine formation involves the conformational change of the Fe(IV)=O species from the axial configuration to the equatorial one, the substrate deprotonation of NH₃⁺ group to form the NH-ligated intermediate, the C-H activation by the equatorial Fe(IV)=O species. Such mechanistic scenario has been cross-validated by oxidation of various substrates by TqaL_Nc and its variants, including the available experiments and our new experiments. While the presence of steric hindrance between the substrate and the second-sphere residues would inhibit the aziridination process, the intrinsic reactivity of aziridination vs. hydroxylation is dictated by the energy splitting between two key redox-active dπ* frontier molecular orbitals: dπ*_Fe-N and dπ*_Fe-OH. The present findings highlight the key roles of the coordination change and dynamics of iron cofactor in dictating the catalysis of non-heme enzymes and have far-reaching implications for the other non-heme Fe(II)/αKG-dependent enzymes catalyzed C-H functionalization beyond the hydroxylation.

Key words: Quantum mechanics/molecular, mechanics, C-H functionalization, Non-heme enzymes, Aziridination, Hydroxylation

Xuan Zhang, Jia Liu, Langxing Liao, Zikuan Wang, Binju Wang. Coordination dynamics of iron enables the selective C-N coupling but bypasses unwanted C-H hydroxylation in Fe(II)/α-ketoglutarate- dependent non-heme enzymes[J]. Chinese Journal of Catalysis, 2024, 62: 131-144.

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URL: https://www.cjcatal.com/EN/10.1016/S1872-2067(24)60064-1

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Figures/Tables 8

Fig. 1. Reactions, crystal structure and two possible mechanisms of TqaLNc. (a) Reactions catalyzed by TqaLNc with different substrates. L-Val is oxidated to aziridine product; L-Ile is oxidated to aziridine product and hydroxylation product. (b) Crystal structure of TqaLNc (PDB: 7EEH). Left part is the whole view of the protein. The right part is an enlarged view of the active site with the substrate docked into the active site and the loops ABC have been predicted by AlphaFold2. (c) Two possible catalytic mechanisms of TqaLNc for the formation of aziridine product.

Fig. 2. The formation and conformation isomerization of Fe(IV)=O species. (a) QM(UB3LYP/B2)/MM relative energies (kcal mol?1) for the Fe(IV)=O species formation with substrate L-Val by TqaLNc. The dispersion corrections and ZPEs are included in the relative energies. (b) QM(UB3LYP/B1)/MM-optimized geometries of key TS1b species involved in the reaction. Key distances are given in ?. Geometries of TS1a and TS1b are shown in Fig. S1. (c) (UB3LYP/B2)/MM relative energies (kcal mol?1) for the conformation change between structures ax-FeO and eq-FeO. The dispersion corrections and ZPEs are included in the relative energies and QM(UB3LYP/B1)/MM-optimized geometries of key species involved in the reaction. Key distances are given in ?.

Fig. 3. Aziridine formation from the axial Fe(IV)=O species through mechanism A in Fig. 1(c). (a) Representation snapshot of MD simulation of axial Fe(IV)=O species (ax-FeO). (b) QM(UB3LYP/B1)/MM relative energies (kcal mol?1) for the aziridine formation with substrate L-Val by the axial Fe(IV)=O species (ax-FeO) in three proposed routes. The dispersion corrections are included in the relative energies.

Fig. 4. The second deprotonation process beginning from F1’ and aziridine formation through mechanism B in Fig. 1(c). (a) QM(UB3LYP/B2)/MM relative energies (kcal mol?1) for the conversion from structure F1’ to F2. The dispersion corrections and ZPEs are included in the relative energies. QM(UB3LYP/B1)/MM-optimized geometries of key species involved in the reaction. Key distances are given in ?. (b) QM(UB3LYP/B2)/MM relative energies (kcal mol?1) for the aziridine formation reaction with substrate L-Val by TqaLNc via mechanism B on quintet state. The dispersion corrections and ZPEs are included in the relative energies. (c) QM(UB3LYP/B1)/MM-optimized geometries of key species involved in the reaction. Key distances are given in ?.

Fig. 5. Barriers of aziridination vs. hydroxylation between various substrates and enzymes. QM(UB3LYP/B2)/MM relative energies (kcal mol?1) for the TS barriers of aziridination reaction and hydroxylation reaction and QM(UB3LYP/B1)/MM-optimized geometries of key species of the Fe(III)-OH species for (a) the oxidation of substrate L-Val by TqaLNc, also see Fig. 4 for the full energy profile. (b) The oxidation of substrate L-Ile by TqaLNc, also see Fig. S13 for the full energy profile. (c) The oxidation of substrate L-Ile by F345A-TqaLNc, also see Fig. S14 for the full energy profile. The dispersion corrections and ZPEs are included in the relative energies. Key distances are given in ?.

Fig. 6. Further validation of mechanism through oxidation of L-homoalanine by TqaLNc through computational and experimental methods. (a) QM(UB3LYP/B2)/MM relative energies (kcal mol?1) for the aziridine formation reaction with substrate L-homoalanine by TqaLNc via mechanism B on quintet state. The dispersion corrections and ZPEs are included in the relative energies. (b) QM(UB3LYP/B1)/MM-optimized geometries of key species involved in the reaction. Key distances are given in ?. (c) LC-MS EIC results on new substrate L-homoalanine (1) oxidized by TqaLNc. EIC of [M+H]+ signals from Dns-1 (m/z = 335.1077), Dns-2 (m/z = 351.1026), and the product of 1 catalyzed by TqaLNc (m/z = 351.1024).

Fig. 7. Frontier orbitals calculated for (a) the substrate radical intermediate F3 (see Fig. 4 for the full reaction process) and (b) Int5 (see Fig. S18 for the full reaction process). The FMOs, dπ*Fe-N, dπ*Fe-OH, dσ*Fe-N, and dπ*Fe-OH are operative in aziridination and hydroxylation, respectively. The arrows indicate the interaction of the substrate orbital with FMOs and energy barrier gaps are in kcal mol?1.

Fig. 8. Proposed catalytic cycle of the aziridine formation by TqaLNc in this study.

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