Abstract
ABSTRACTComplete biodegradation of the abundant and persistent fluoroaromatics requires enzymatic cleavage of an arylic C–F bond, probably the most stable single bond of a biodegradable organic molecule. While in aerobic microorganisms defluorination of fluoroaromatics is initiated by oxygenases, arylic C–F bond cleavage has never been observed in the absence of oxygen. Here, an oxygen-independent enzymatic aryl fluoride bond cleavage is described during the complete degradation of 4-fluorobenzoate or 4-fluorotoluene to CO2 and HF in the denitrifying Thauera aromatica: the ATP-dependent defluorination of 4-fluorobenzoyl-coenzyme A (4-F-BzCoA) to benzoyl-coenzyme A (BzCoA) and HF, catalyzed by class I BzCoA reductase (BCR). Adaptation to growth with the fluoroaromatics was accomplished by the downregulation of a promiscuous benzoate-CoA ligase and the concomitant upregulation of 4-F-BzCoA-defluorinating/dearomatizing BCR on the transcriptional level. We propose an unprecedented mechanism for reductive arylic C–F bond cleavage via a Birch reduction-like mechanism resulting in a formal nucleophilic aromatic substitution. In the proposed anionic 4-fluorodienoyl-CoA transition state, fluoride elimination to BzCoA is favored over protonation to a fluorinated cyclic dienoyl-CoA.
Highlights
Complete biodegradation of the abundant and persistent fluoroaromatics requires enzymatic cleavage of an arylic C–F bond, probably the most stable single bond of a biodegradable organic molecule
The reductions of benzoyl-coenzyme A (BzCoA), 3-Br-BzCoA, 3-Cl-BzCoA, and 4-F-BzCoA during the complete degradation of the corresponding halogenated aromatic acids and other monocyclic compounds are likely all initiated by similar electron transfer and protonation events yielding a common anionic state [32] (Fig. 6)
Depending on the position and nature of substituents on the aromatic ring, three different scenarios may occur for the subsequent conversion of the anion. (i) During BzCoA dearomatization, the anion is protonated at the C-3 position in an essentially irreversible manner, yielding dienoyl-coenzyme A (CoA) [24, 32]. (ii) In the case of 3-Cl-/3-Br-BzCoA reduction, the same protonation yields the 3-Cl-/3-Br-dienoyl-CoA intermediates that are prone to spontaneous one-step E2 elimination of HCl/HBr, driven by rearomatization [26]
Summary
Complete biodegradation of the abundant and persistent fluoroaromatics requires enzymatic cleavage of an arylic C–F bond, probably the most stable single bond of a biodegradable organic molecule. An oxygen-independent enzymatic aryl fluoride bond cleavage is described during the complete degradation of 4-fluorobenzoate or 4-fluorotoluene to CO2 and HF in the denitrifying Thauera aromatica: the ATP-dependent defluorination of 4-fluorobenzoyl-coenzyme A (4-F-BzCoA) to benzoyl-coenzyme A (BzCoA) and HF, catalyzed by class I BzCoA reductase (BCR). We report a strategy for the complete biodegradation of a fluoroaromatic to CO2 and HF in a denitrifying bacterium via activation to a CoA ester, followed by oxygen-independent arylic C–F bond cleavage catalyzed by an ATP-dependent enzyme. This reaction, in conjunction with a transcriptional adaptation to fluorinated growth substrates, is essential for the anoxic biodegradation of 4-fluorobenzoate/4-F-toluene and probably other fluoroaromatics. The enzymatic processes involved in defluorination during growth with 2- and 4-F-benzoate have remained unknown
Sign-in/Register to view highlights & summary Talk to us
Join us for a 30 min session where you can share your feedback and ask us any queries you have
Schedule a callDisclaimer: All third-party content on this website/platform is and will remain the property of their respective owners and is provided on "as is" basis without any warranties, express or implied. Use of third-party content does not indicate any affiliation, sponsorship with or endorsement by them. Any references to third-party content is to identify the corresponding services and shall be considered fair use under The CopyrightLaw.
