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ATP-Dependent C–F Bond Cleavage Allows the Complete Degradation of 4-Fluoroaromatics without Oxygen

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. While in aerobic microorganisms defluorination of fluoroaromatics is initiated by oxygenases, arylic C–F...

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Autores principales: Tiedt, Oliver, Mergelsberg, Mario, Boll, Kerstin, Müller, Michael, Adrian, Lorenz, Jehmlich, Nico, von Bergen, Martin, Boll, Matthias
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4992971/
https://www.ncbi.nlm.nih.gov/pubmed/27507824
http://dx.doi.org/10.1128/mBio.00990-16
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author Tiedt, Oliver
Mergelsberg, Mario
Boll, Kerstin
Müller, Michael
Adrian, Lorenz
Jehmlich, Nico
von Bergen, Martin
Boll, Matthias
author_facet Tiedt, Oliver
Mergelsberg, Mario
Boll, Kerstin
Müller, Michael
Adrian, Lorenz
Jehmlich, Nico
von Bergen, Martin
Boll, Matthias
author_sort Tiedt, Oliver
collection PubMed
description 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. 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 CO(2) 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.
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spelling pubmed-49929712016-08-23 ATP-Dependent C–F Bond Cleavage Allows the Complete Degradation of 4-Fluoroaromatics without Oxygen Tiedt, Oliver Mergelsberg, Mario Boll, Kerstin Müller, Michael Adrian, Lorenz Jehmlich, Nico von Bergen, Martin Boll, Matthias mBio Research Article 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. 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 CO(2) 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. American Society for Microbiology 2016-08-09 /pmc/articles/PMC4992971/ /pubmed/27507824 http://dx.doi.org/10.1128/mBio.00990-16 Text en Copyright © 2016 Tiedt et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Tiedt, Oliver
Mergelsberg, Mario
Boll, Kerstin
Müller, Michael
Adrian, Lorenz
Jehmlich, Nico
von Bergen, Martin
Boll, Matthias
ATP-Dependent C–F Bond Cleavage Allows the Complete Degradation of 4-Fluoroaromatics without Oxygen
title ATP-Dependent C–F Bond Cleavage Allows the Complete Degradation of 4-Fluoroaromatics without Oxygen
title_full ATP-Dependent C–F Bond Cleavage Allows the Complete Degradation of 4-Fluoroaromatics without Oxygen
title_fullStr ATP-Dependent C–F Bond Cleavage Allows the Complete Degradation of 4-Fluoroaromatics without Oxygen
title_full_unstemmed ATP-Dependent C–F Bond Cleavage Allows the Complete Degradation of 4-Fluoroaromatics without Oxygen
title_short ATP-Dependent C–F Bond Cleavage Allows the Complete Degradation of 4-Fluoroaromatics without Oxygen
title_sort atp-dependent c–f bond cleavage allows the complete degradation of 4-fluoroaromatics without oxygen
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4992971/
https://www.ncbi.nlm.nih.gov/pubmed/27507824
http://dx.doi.org/10.1128/mBio.00990-16
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