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Insight into the Mechanism Underlying <i>Dehalococcoides mccartyi</i> Strain CBDB1-Mediated B<sub>12</sub>-Dependent Aromatic Reductive Dehalogenation

Shangwei Zhang, Wu Wen, Xinghui Xia, Wei Ouyang, Bixian Mai, Lorenz Adrian, Gerrit Schüürmann

2023Environmental Science & Technology13 citationsDOI

Abstract

Anaerobic bacteria transform aromatic halides through reductive dehalogenation. This dehalorespiration is catalyzed by the supernucleophilic coenzyme vitamin B 12, cob(I)alamin, in reductive dehalogenases. So far, the underlying inner-sphere electron transfer (ET) mechanism has been discussed controversially. In the present study, all 36 chloro-, bromo-, and fluorobenzenes and full-size cobalamin are analyzed at the quantum chemical density functional theory level with respect to a wide range of theoretically possible inner-sphere ET mechanisms. The calculated reaction free energies within the framework of Co I ···X (X = F, Cl, and Br) attack rule out most of the inner-sphere pathways. The only route with feasible energetics is a proton-coupled two-ET mechanism that involves a B 12 side-chain tyrosine (modeled by phenol) as a proton donor. For 12 chlorobenzenes and 9 bromobenzenes with experimental data from Dehalococcoides mccartyi strain CBDB1, the newly proposed PC-TET mechanism successfully discriminates 16 of 17 active from 4 inactive substrates and correctly predicts the observed regiospecificity to 100%. Moreover, fluorobenzenes are predicted to be recalcitrant in agreement with experimental findings. Conceptually, based on the Bell–Evans–Polanyi principle, the computational approach provides novel mechanistic insights and may serve as a tool for predicting the energetic feasibility of reductive aromatic dehalogenation.

Topics & Concepts

DehalococcoidesReductive dechlorinationHalogenationStrain (injury)ChemistryMechanism (biology)StereochemistryEnvironmental chemistryBiologyOrganic chemistryPhysicsVinyl chlorideBiodegradationPolymerQuantum mechanicsAnatomyCopolymerPorphyrin Metabolism and DisordersHeme Oxygenase-1 and Carbon MonoxideMetal-Catalyzed Oxygenation Mechanisms
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