3-Carboxy-cis,cis-muconate lactonizing enzyme from Pseudomonas putida is homologous to the class II fumarase family: a new reaction in the evolution of a mechanistic motif

Williams, Suzanne E.; Woolridge, Elisa M.; Ransom, Stephen C.; Landro, James A.; Babbitt, Patricia C.; Kozarich, John W.

doi:10.1021/bi00155a033

Cited by 70 publications

(50 citation statements)

References 53 publications

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“…Thus, the gene order is pcaDC(HG)B. The pcaHG genes from Acinetobacter calcoaceticus occupy about 1.36 kb (15), while the pcaB gene from Pseudomonas putida encompasses 1.05 kb (51). Assuming similar sizes for the genes from A. tumefaciens, pcaB is contiguous to pcaH and pcaG, with no space for an additional gene between them.…”

Section: Resultsmentioning

confidence: 99%

Supraoperonic clustering of pca genes for catabolism of the phenolic compound protocatechuate in Agrobacterium tumefaciens

Parke

1995

J Bacteriol

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The protocatechuate branch of the ␤-ketoadipate pathway comprises the last six enzymatic steps in the catabolism of diverse phenolic compounds to citric acid cycle intermediates. In this paper, the regulation and tight supraoperonic clustering of the protocatechuate (pca) genes from Agrobacterium tumefaciens A348 are elucidated. A previous study found that the pcaD gene is controlled by an adjacent regulatory gene, pcaQ, which encodes an activator. The activator responded to ␤-carboxy-cis,cis-muconate and was shown to control the synthesis of at least three genes (pcaD and pcaHG). In this work, eight genes required for the catabolism of protocatechuate were localized within a 13.5-kb SalI region of DNA. Isolation and characterization of transposon Tn5 mutant strains facilitated the localization of pca genes. Five structural genes were found to respond to the tricarboxylic acid and to be contiguous in an operon transcribed in the order pcaDCHGB. These genes encode enzymes ␤-ketoadipate enol-lactone hydrolase, ␥-carboxymuconolactone decarboxylase, protocatechuate 3,4-dioxygenase (pcaHG), and ␤-carboxy-cis,cis-muconate lactonizing enzyme, respectively. Approximately 4 kb from the pcaD gene are the pcaIJ genes, which encode ␤-ketoadipate succinyl-coenzyme A transferase for the next-to-last step of the pathway. The pcaIJ genes are transcribed divergently from the pcaDCHGB operon and are expressed in response to ␤-ketoadipate. The pattern of induction of pca genes by ␤-carboxy-cis,cis-muconate and ␤-ketoadipate in A. tumefaciens is similar to that observed in Rhizobium leguminosarum bv. trifolii and is distinct from induction patterns for the genes from other microbial groups.Diverse aromatic compounds, arising in soil and water from origins in living plants, plant litter, or industrial processes, are degraded to common diphenolic intermediates, catechol and protocatechuate. Specific dioxygenases cleave these two phenolics, initiating the two branches of the ␤-ketoadipate pathway which funnel aromatic compounds into the tricarboxylic acid cycle (48). The ability of members of the bacterial family Rhizobiaceae to catabolize numerous aromatic compounds via the catechol or protocatechuate branch of the ␤-ketoadipate pathway has been documented (6,7,26,37,38). Remarkably, the protocatechuate branch of the pathway (Fig. 1) appears to be universally distributed among members of this highly diverse bacterial group (21, 37). Previous research has demonstrated the inducibility of enzymes of the ␤-ketoadipate pathway in fast-growing representatives of the family Rhizobiaceae and the constitutivity of most enzymes in slowly growing Bradyrhizobium species (38).As a multistep ensemble, peripheral to the heart of bacterial metabolism, the ␤-ketoadipate pathway provides a model system for studying the mechanisms of regulation and evolution of catabolic pathways. Its acquisition and maintenance in the face of different selection pressures might be expected to be mediated by diversification of gene organization and regulation. The reg...

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Section: Resultsmentioning

confidence: 99%

Supraoperonic clustering of pca genes for catabolism of the phenolic compound protocatechuate in Agrobacterium tumefaciens

Parke

1995

J Bacteriol

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“…These reactions were analysed by HPLC because 3-sulfomuconate, unlike most other substituted muconates, does not have pronounced The accession numbers and references for the published sequences of the enzymes from P. putida, Acinetobacter sp. ADP1 and Agrobacterium tumefaciens C58 are P32427 (Williams et al, 1992), Q59092 (Kowalchuk et al, 1994), and AAK88905 (Wood et al, 2001), respectively. absorbance at 260 nm (Feigel & Knackmuss, 1993).…”

Section: Turnover Of 3-sulfomuconate By Hicmle2 and Arcmle2mentioning

confidence: 99%

“…The CMLE from Pseudomonas putida has been purified and the stereochemistry of the turnover of 3-carboxy-cis,cis-muconate has been analysed in some detail. In addition, the gene has been cloned and sequenced, and the crystal structure of the enzyme has been determined (Ornston, 1966;Williams et al, 1992;Yang et al, 2004).…”

Section: Introductionmentioning

confidence: 99%

Characterization of the genes encoding the 3-carboxy-cis,cis-muconate-lactonizing enzymes from the 4-sulfocatechol degradative pathways of Hydrogenophaga intermedia S1 and Agrobacterium radiobacter S2

et al. 2006

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Hydrogenophaga intermedia strain S1 and Agrobacterium radiobacter strain S2 form a mixed bacterial culture which degrades sulfanilate (4-aminobenzenesulfonate) by a novel variation of the b-ketoadipate pathway via 4-sulfocatechol and 3-sulfomuconate. It was previously proposed that the further metabolism of 3-sulfomuconate is catalysed by modified 3-carboxy-cis, cis-muconate-lactonizing enzymes (CMLEs) and that these 'type 2' enzymes were different from the conventional CMLEs ('type 1') from the protocatechuate pathway in their ability to convert 3-sulfomuconate in addition to 3-carboxy-cis,cis-muconate. In the present study the genes for two CMLEs (pcaB2S1 and pcaB2S2) were cloned from H. intermedia S1 and A. radiobacter S2, respectively. In both strains, these genes were located close to the previously identified genes encoding the 4-sulfocatechol-converting enzymes. The gene products of pcaB2S1 and pcaB2S2 were therefore tentatively identified as type 2 enzymes involved in the metabolism of 3-sulfomuconate. The genes were functionally expressed and the gene products were shown to convert 3-carboxy-cis,cis-muconate and 3-sulfomuconate. 4-Carboxymethylene-4-sulfo-but-2-en-olide (4-sulfomuconolactone) was identified by HPLC-MS as the product, which was enzymically formed from 3-sulfomuconate. His-tagged variants of both CMLEs were purified and compared with the CMLE from the protocatechuate pathway of Pseudomonas putida PRS2000 for the conversion of 3-carboxy-cis,cis-muconate and 3-sulfomuconate. The CMLEs from the 4-sulfocatechol pathway converted 3-sulfomuconate with considerably higher activities than 3-carboxy-cis,cis-muconate. Also the CMLE from P. putida converted 3-sulfomuconate, but this enzyme demonstrated a clear preference for 3-carboxy-cis,cis-muconate as substrate. Thus it was demonstrated that in the 4-sulfocatechol pathway, distinct CMLEs are formed, which are specifically adapted for the preferred conversion of sulfonated substrates.

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“…Thus, different evolutionary families are represented by each of the following genes (and encoded enzymes) associated with quinate catabolism in A. calcoaceticus: quiA (quinate/shikimate dehydrogenase) (12), pcaHG (protocatechuate 3,4-dioxygenase) (17,24,55), pcaD (␤-ketoadipate enol-lactone hydrolase) (25,40), pcaIJ (␤-ketoadipate-succinyl coenzyme A transferase) (31,44), and pcaF (␤-ketoadipyl coenzyme A thiolase) (26,31,45). Genes encoding the fumarase II family of dehydratases include pcaB, the structural gene for ␤-carboxymuconate cycloisomerase in bacteria (56). Cycloisomerases associated with the eucaryotic ␤-ketoadipate pathway can be traced to different ancestors (35), and comparative analysis has revealed a complex patchwork of evolutionary relationships among cycloisomerases associated with the ␤-ketoadipate pathway (36,37,46).…”

Section: Discussionmentioning

confidence: 99%

Unusual ancestry of dehydratases associated with quinate catabolism in Acinetobacter calcoaceticus

Elsemore

Ornston

1995

J Bacteriol

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Catabolism of quinate to protocatechuate requires the consecutive action of quinate dehydrogenase (QuiA), dehydroquinate dehydratase (QuiB), and dehydroshikimate dehydratase (QuiC). Genes for catabolism of protocatechuate are encoded by the pca operon in the Acinetobacter calcoaceticus chromosome. Observations reported here demonstrate that A. calcoaceticus qui genes are clustered in the order quiBCXA directly downstream from the pca operon. Sequence comparisons indicate that quiX encodes a porin, but the specific function of this protein has not been clearly established. Properties of mutants created by insertion of ⍀ elements show that quiBC is expressed as part of a single transcript, but there is also an independent transcriptional initiation site directly upstream of quiA. The deduced amino acid sequence of QuiC does not resemble any other known sequence. A. calcoaceticus QuiB is most directly related to a family of enzymes with identical catalytic activity and biosynthetic AroD function in coliform bacteria. Evolution of A. calcoaceticus quiB appears to have been accompanied by fusion of a leader sequence for transport of the encoded protein into the inner membrane, and the location of reactions catalyzed by the mature enzyme may account for the failure of A. calcoaceticus aroD to achieve effective complementation of null mutations in quiB. Analysis of a genetic site where a DNA segment encoding a leader sequence was transposed adds to evidence suggesting horizontal transfer of nucleotide sequences within genes during evolution.Dehydroquinate dehydratase (QuiB) and dehydroshikimate dehydratase (QuiC) catalyze consecutive reactions allowing growth of microorganisms with quinate by its conversion to protocatechuate ( Fig. 1) and subsequent metabolism by the ␤-ketoadipate pathway (41, 52). The enzymatic activity of QuiB is identical to that of AroD, an enzyme that catalyzes biosynthetic formation of dehydroshikimate (Fig. 1). Enzymes with similar catalytic activities often can be traced to a common ancestor (32), and the similarity of dehydratases associated with dehydroshikimate metabolism raised the possibility that a single ancestral protein was the evolutionary precursor of two or more of these enzymes.In contrast to this prediction, biosynthetic dehydroquinate dehydratases differ substantially from catabolic enzymes with this activity (18,30). With the exception of the dehydroquinate dehydratases of gram-positive bacteria (13, 15), enzymes with the biosynthetic function indicated as AroD in Fig. 1 are classified as type I and are thermolabile, a property that distinguishes them from the isofunctional type II enzymes which are heat stable and mediate the activity indicated as QuiB in Fig. 1 Some gram-negative bacteria elaborate a single dehydroquinate dehydratase associated solely with the biosynthetic function indicated as AroD in Fig. 1. Genes for this enzyme from Enterococcus faecalis (3), Salmonella typhi (51), and Escherichia coli (10) have been sequenced and shown to encode type I enzymes. These fi...

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3-Carboxy-cis,cis-muconate lactonizing enzyme from Pseudomonas putida is homologous to the class II fumarase family: a new reaction in the evolution of a mechanistic motif

Cited by 70 publications

References 53 publications

Supraoperonic clustering of pca genes for catabolism of the phenolic compound protocatechuate in Agrobacterium tumefaciens

Supraoperonic clustering of pca genes for catabolism of the phenolic compound protocatechuate in Agrobacterium tumefaciens

Characterization of the genes encoding the 3-carboxy-cis,cis-muconate-lactonizing enzymes from the 4-sulfocatechol degradative pathways of Hydrogenophaga intermedia S1 and Agrobacterium radiobacter S2

Unusual ancestry of dehydratases associated with quinate catabolism in Acinetobacter calcoaceticus

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