A cluster of bacterial genes for anaerobic benzene ring biodegradation

Egland, Paul G.; Pelletier, Dale A.; Dispensa, Marilyn; Gibson, Jane; Harwood, Caroline S.

doi:10.1073/pnas.94.12.6484

Cited by 154 publications

(235 citation statements)

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“…Strategy for pathway reconstruction In order to determine whether the F. placidus genome contained genes with homology to genes known to be involved in anaerobic benzoate and phenol metabolism in other microorganisms, comparisons were made to the characterized aromatic degradation pathway genes in T. aromatica (Breese et al, 1998;Breinig et al, 2000), Aromatoleum aromaticum EbN1 (Rabus et al, 2005), G. metallireducens (Wischgoll et al, 2005;Butler et al, 2007;Schleinitz et al, 2009) and R. palustris (Egland et al, 1997;Harwood et al, 1999). Despite the substantial phylogenetic distance between F. placidus and these mesophilic benzoate-and phenol-degrading bacteria, candidate genes for benzoate and phenol metabolism with high homology to those in the mesophilic bacteria could be identified in the F. placidus genome (Supplementary Tables 4 and 5).…”

Section: Resultsmentioning

confidence: 99%

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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%

“…The best-studied class I BCRs include those from the facultative denitrifying species Thauera aromatica (Boll and Fuchs, 1995), Azoarcus spp. (Lopez Barragan et al, 2004) and the phototroph Rhodopseudomonas palustris (Egland et al, 1997).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2011

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“…Note that the nonphysiologic substrate hydroxylamine becomes ATP dependently reduced by BCR (2). [8][9][10][11][12][13][14] C]ATP from unlabeled ATP in the absence of an electron-accepting substrate was followed (Fig. 3).…”

Section: Resultsmentioning

confidence: 99%

“…BCR contains three cysteine-ligated [4Fe-4S] ϩ1/ϩ2 clusters with midpoint potentials more negative than Ϫ500 mV (10). The four subunits of BCR in T. aromatica (11) and in the phototrophic bacterium Rhodopseudomonas palustris (12) show Ϸ70% identity to each other. Furthermore, the subunits of BCR show 38 -52% similarities to the twocomponent enzyme system activase (Hgd C-homodimer)͞2-hydroxyglutaryl-CoA dehydratase (Hgd A͞B-heterodimer) of Acidaminococcus fermentans (11,13).…”

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confidence: 99%

Mechanism of ATP-driven electron transfer catalyzed by the benzene ring-reducing enzyme benzoyl- CoA reductase

Unciuleac

Boll

2001

Proc. Natl. Acad. Sci. U.S.A.

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Benzoyl-CoA reductase (BCR) from the bacterium Thauera aromatica catalyzes the two-electron reduction of benzoyl-CoA (BCoA) to a nonaromatic cyclic diene. In a process analogous to enzymatic nitrogen reduction, BCR couples the electron transfer to the aromatic ring to a stoichiometric hydrolysis of 2 ATP͞2e ؊ . Reduced but not oxidized BCR hydrolyzes ATP to ADP. In this work, purified BCR was shown to catalyze an isotope exchange from [ 14 C]ADP to [ 14 C]ATP, which was Ϸ15% of the ATPase activity in the presence of equimolar amounts of ADP and ATP. In accordance, BCR (␣␤␥␦-composition) autophosphorylated its ␥-subunit when incubated with [␥-32 P]ATP. Formation of the enzyme-phosphate was independent of the redox state, whereas only dithionitereduced BCR catalyzed a dephosphorylation associated with the ATPase activity. This finding suggests that the ATPase-and autophosphatase-partial activities of BCR exhibit identical redox dependencies. BCoA or the nonphysiological electron-accepting substrate hydroxylamine stimulated the redox-dependent effects; the rates of both the overall ATPase and the autophosphatase activities of reduced BCR were increased 6-fold. In contrast, BCoA and hydroxylamine had no effect on oxidized and phosphorylated BCR. The reactivity of the phosphoamino acid fits best with a phosphoamidate or acylphosphate linkage. The results obtained suggest a mechanism of ATP hydrolysis-driven electron transfer, which differs from that of nitrogenase by the transient formation of a phosphorylated enzyme.B enzoyl-CoA (BCoA) is a central intermediate in the metabolism of many aromatic compounds in anaerobic bacteria. This compound becomes reduced by benzoyl-CoA reductase (BCR), a key enzyme in anaerobic aromatic metabolism (1, 2). It catalyzes the reductive dearomatization of BCoA to cyclohexa-1,5-diene-1-carbonyl-CoA ( Fig. 1; ref. 3). In this reaction, the hydrolysis of two ATP to ADP and Pi is stoichiometrically coupled to the transfer of two single electrons from reduced ferredoxin to the aromatic substrate. Notably, BCR also catalyzes the ATP-dependent reduction of the nonphysiological substrate hydroxylamine (2). The stoichiometric coupling of ATP hydrolysis to an electron transfer process has long been considered as a unique feature of nitrogenases (4, 5). However, there are no amino acid sequence similarities between BCR and nitrogenases.The reduction of the aromatic ring is a mechanistically and energetically difficult process that in organic synthesis requires solvated electrons, which are generated by dissolving alkali metals in liquid ammonia. In a so-called Birch mechanism, the reduction of the aromatic ring proceeds in single electron and proton transfer steps by means of radical intermediates (6). A similar mechanism has been proposed for enzymatic benzene ring reduction (7). The crucial step is the first electron transfer to the aromatic ring yielding a nonaromatic radical anion, which requires a redox potential of Ϫ1.9 V (3). BCR overcomes this high redox barrier by coupling a stoichiomet...

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“…Lignin degradation is very slow under anaerobic conditions and, depending on pressure and time scale, leads to the accumulation of humus to form peat, organic soil matter, lignite, and coal (Heider & Fuchs 1997). Although polymeric lignin remains stable in anaerobic environments for long periods of time, bacterial consortia actively metabolise smaller degradation products (Egland et al 1997;Elder & Kelly 1994).…”

Section: Toxicity Of Lignin-carbohydrate Complexes and Lignocellulosementioning

confidence: 99%

Lignocellulose biodegradation: Fundamentals and applications

Malherbe

Cloete

2002

Rev Environ Sci Biotechnol

398

163

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A cluster of bacterial genes for anaerobic benzene ring biodegradation

Cited by 154 publications

References 38 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

Mechanism of ATP-driven electron transfer catalyzed by the benzene ring-reducing enzyme benzoyl- CoA reductase

Lignocellulose biodegradation: Fundamentals and applications

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