Halogen transfer to aromatic and aliphatic C-H bonds: A combined enzymological and computational study

  • Emilie Gerard

Student thesis: Phd

Abstract

Enzymatic halogenases and haloperoxidases catalyse unique reactions, whereby a halogen atom is inserted into an inert C-H bond as part of natural product synthesis. These reactions could be relevant to biotechnology through the selective synthesis of organic C-X bonds. However, little is known on the mechanisms and origins of the selectivity. In this thesis, the electrophilic halogenation pathway in vanadium haloperoxidases and the radical halogenation pathway in non-heme iron halogenases have been studied. Vanadium haloperoxidases halogenate substrates via the production of a hypohalide intermediate from H2O2 and halide. Here, a two-step process is established in the production of hypohalide. First, H2O2 is activated and binds the vanadium centre as an end-on hydroperoxo ligand. Next, OH+ is transferred to chloride in the formation of HOCl. The HOX is released from the active site to halogenate aromatic compounds. Through experimental and computational methods, a putative substrate-binding pocket has been proposed. The enzyme is essential for the substrate halogenation step. Electric field effect calculations and an electric field gradient on the protein structure, that highlights the presence of a large dipole orientation, could explain halogen transfer in the substrate-binding pocket. Non-heme iron halogenases perform radical halogenation on aliphatic C-H bonds. An FeIII(OH)(X) intermediate is proposed to be formed during the catalytic cycle, but it is unknown what controls the halogenation over hydroxylation in these enzymes. A first FeIII(OMe) model complex demonstrated OMe rebound to tertiary carbon radicals in a radical transfer reaction. DFT calculations further determined that the OMe transfer is carried out in a concerted manner. Next, a FeIII(OH)(X) complex reacted with tertiary carbon radicals to give hydroxylated products. However, when reacted with secondary carbons, halogenated products are observed. A DFT study helped understand the reasons for this selectivity. It was found that halogen transfer to tertiary carbon radicals resulted in a non-productive equilibrium despite relatively low energy barriers, whereas the hydroxyl transfer is highly exothermic and irreversible. In contrast, halogen transfer to secondary carbon radicals results in thermodynamically stable products. These observations correlate to C-X bond strengths formed at tertiary versus secondary carbon centres. Additionally, secondary-coordination sphere effects, such as steric and hydrogen-bonding interactions, impact the halogen transfer energy barriers.
Date of Award1 Aug 2023
Original languageEnglish
Awarding Institution
  • The University of Manchester
SupervisorSamuel De Visser (Supervisor), Sam Hay (Supervisor), Derren Heyes (Supervisor) & Christopher Blanford (Supervisor)

Keywords

  • biophysics
  • DFT
  • non-heme iron halogenases
  • halogenases
  • vanadium haloperoxidases

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