A Novel Pathway of Aerobic Benzoate Catabolism in the BacteriaAzoarcus evansii and Bacillus stearothermophilus

Zaar, Annette; Eisenreich, Wolfgang; Bacher, Adelbert; Fuchs, Georg

doi:10.1074/jbc.m100291200

Cited by 51 publications

(67 citation statements)

References 29 publications

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“…However, F. placidus is a strict anaerobe (Hafenbradl et al, 1996), and no genes for aerobic metabolism of benzoate via hydroxylation or the BOX pathway (Zaar et al, 2001;Gescher et al, 2002;Risso et al, 2009) were apparent in the genome. Multiple anaerobic BCLs have also been detected in other organisms.…”

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confidence: 99%

Genome-scale analysis of anaerobic benzoate and phenol metabolism in the hyperthermophilic archaeon Ferroglobus placidus

et al. 2011

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Insight into the mechanisms for the anaerobic metabolism of aromatic compounds by the hyperthermophilic archaeon Ferroglobus placidus is expected to improve understanding of the degradation of aromatics in hot (>80° C) environments and to identify enzymes that might have biotechnological applications. Analysis of the F. placidus genome revealed genes predicted to encode enzymes homologous to those previously identified as having a role in benzoate and phenol metabolism in mesophilic bacteria. Surprisingly, F. placidus lacks genes for an ATP-independent class II benzoyl-CoA (coenzyme A) reductase (BCR) found in all strictly anaerobic bacteria, but has instead genes coding for a bzd-type ATP-consuming class I BCR, similar to those found in facultative bacteria. The lower portion of the benzoate degradation pathway appears to be more similar to that found in the phototroph Rhodopseudomonas palustris, than the pathway reported for all heterotrophic anaerobic benzoate degraders. Many of the genes predicted to be involved in benzoate metabolism were found in one of two gene clusters. Genes for phenol carboxylation proceeding through a phenylphosphate intermediate were identified in a single gene cluster. Analysis of transcript abundance with a whole-genome microarray and quantitative reverse transcriptase polymerase chain reaction demonstrated that most of the genes predicted to be involved in benzoate or phenol metabolism had higher transcript abundance during growth on those substrates vs growth on acetate. These results suggest that the general strategies for benzoate and phenol metabolism are highly conserved between microorganisms living in moderate and hot environments, and that anaerobic metabolism of aromatic compounds might be analyzed in a wide range of environments with similar molecular targets.

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Section: Resultsmentioning

confidence: 99%

Genome-scale analysis of anaerobic benzoate and phenol metabolism in the hyperthermophilic archaeon Ferroglobus placidus

et al. 2011

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“…The well known ␤-ketoadipate pathway is the paradigm of this metabolic achievement (1,2). A new pathway for aerobic benzoate oxidation has been postulated for Azoarcus evansii and for a Bacillus stearothermophilus-like strain (3,4). In the meantime, this pathway or its characteristic genes were found in various other bacteria, either as the only pathway or as an additional benzoate metabolic pathway that comes into play under certain conditions (5,6).…”

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Coenzyme A-dependent Aerobic Metabolism of Benzoate via Epoxide Formation

Rather

Knapp

Haehnel

et al. 2010

Journal of Biological Chemistry

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In the aerobic metabolism of aromatic substrates, oxygenases use molecular oxygen to hydroxylate and finally cleave the aromatic ring. In the case of the common intermediate benzoate, the ring cleavage substrates are either catechol (in bacteria) or 3,4-dihydroxybenzoate (protocatechuate, mainly in fungi). We have shown before that many bacteria, e.g. Azoarcus evansii, the organism studied here, use a completely different mechanism. This elaborate pathway requires formation of benzoyl-CoA

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“…The third, semi-aerobic strategy to metabolize benzoate shares characteristic features of both of these options (3). Oxygen is still required for attacking the ring, as in the aerobic metabolism, whereas all metabolites are activated to CoA thioesters and ring cleavage is performed hydrolytically, as in the anaerobic pathway (Fig.…”

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Structure and Mechanism of the Diiron Benzoyl-Coenzyme A Epoxidase BoxB

Rather

Weinert

Demmer

et al. 2011

Journal of Biological Chemistry

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The coenzyme A (CoA)-dependent aerobic benzoate metabolic pathway uses an unprecedented chemical strategy to overcome the high aromatic resonance energy by forming the nonaromatic 2,3-epoxybenzoyl-CoA. The crucial dearomatizing reaction is catalyzed by three enzymes, BoxABC, where BoxA is an NADPH-dependent reductase, BoxB is a benzoyl-CoA 2,3-epoxidase, and BoxC is an epoxide ring hydrolase. We characterized the key enzyme BoxB from Azoarcus evansii by structural and Mössbauer spectroscopic methods as a new member of class I diiron enzymes. Several family members were structurally studied with respect to the diiron center architecture, but no structure of an intact diiron enzyme with its natural substrate has been reported. X-ray structures between 1.9 and 2.5 Å resolution were determined for BoxB in the diferric state and with bound substrate benzoyl-CoA in the reduced state. The substrate-bound reduced state is distinguished from the diferric state by increased iron-ligand distances and the absence of directly bridging groups between them. The position of benzoylCoA inside a 20 Å long channel and the position of the phenyl ring relative to the diiron center are accurately defined. The C2 and C3 atoms of the phenyl ring are closer to one of the irons. Therefore, one oxygen of activated O 2 must be ligated predominantly to this proximate iron to be in a geometrically suitable position to attack the phenyl ring. Consistent with the observed iron/phenyl geometry, BoxB stereoselectively should form the 2S,3R-epoxide. We postulate a reaction cycle that allows a charge delocalization because of the phenyl ring and the electron-withdrawing CoA thioester.The metabolism of aromatic compounds has attracted broad attention due to its importance in the biogeochemical carbon cycle (includes 10 -20% of the biomass) and because of the chemistry necessary to overcome the high resonance energy of the conjugated cyclic ring. A central intermediate of the aromatic metabolism is benzoate, which can be degraded by microorganisms using three different strategies. The first strategy in the presence of oxygen uses mono-and dioxygenases to hydroxylate benzoate to catechol or protocatechuate. Central ring-cleaving dioxygenases with mononuclear iron centers subsequently cleave the aromatic ring either between the two hydroxyl groups (ortho cleavage, ␤-ketoadipate pathway) or next to one of the hydroxyl groups (meta cleavage) (1). The second strategy under anoxic conditions involves benzoylCoA, which is reduced by two electrons to a non-aromatic cyclic diene followed by hydrolytic ring opening. Benzoyl-CoA reduction is accomplished by two completely different enzyme systems that may catalyze a Birch-like reduction (2).The third, semi-aerobic strategy to metabolize benzoate shares characteristic features of both of these options (3). Oxygen is still required for attacking the ring, as in the aerobic metabolism, whereas all metabolites are activated to CoA thioesters and ring cleavage is performed hydrolytically, as in the anaerobic pathwa...

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A Novel Pathway of Aerobic Benzoate Catabolism in the BacteriaAzoarcus evansii and Bacillus stearothermophilus

Abstract: The aerobic catabolism of benzoate was studied in the Gram-negative proteobacterium Azoarcus evansii and in the Gram-positive bacterium Bacillus stearothermophilus. In contrast to earlier proposals, benzoate was not converted into hydroxybenzoate or gentisate.

Cited by 51 publications

References 29 publications

Genome-scale analysis of anaerobic benzoate and phenol metabolism in the hyperthermophilic archaeon Ferroglobus placidus

Genome-scale analysis of anaerobic benzoate and phenol metabolism in the hyperthermophilic archaeon Ferroglobus placidus

Coenzyme A-dependent Aerobic Metabolism of Benzoate via Epoxide Formation

Structure and Mechanism of the Diiron Benzoyl-Coenzyme A Epoxidase BoxB

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