Acquisition of apparent DNA slippage structures during extensive evolutionary divergence of pcaD and catD genes encoding identical catalytic activities in Acinetobacter calcoaceticus

Gb, Hartnett; Ln, Ornston

doi:10.1016/0378-1119(94)90350-6

Cited by 30 publications

(21 citation statements)

References 12 publications

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“…3), still expressed PcaC, albeit at a very low level, indicated that the pcaC gene is directly downstream of pcaD. In Acinetobacter calcoaceticus, pcaD and pcaC encompass about 0.8 and 0.4 kb, respectively (15,17). It is likely that the 1.3-kb PstI-HindIII insertion of pARO148 contains little more than the pcaDC genes.…”

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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“…2). The Acinetobacter gene was blocked fortuitously by the ⌬pcaBDK1 deletion designed to cause intracellular accumulation of carboxymuconate from protocatechuate (17,18). As indicated in Fig.…”

Section: Fig 3 Compartmentation Of Quinate Catabolism In Acinetobacmentioning

confidence: 99%

Bacteria Are Not What They Eat: That Is Why They Are So Diverse

2000

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“…The information presented in Fig. 2 completes knowledge of the 14-kb nucleotide sequence containing the 11 structural genes required for catabolism of quinate, shikimate, and protocatechuate in A. calcoaceticus (12,17,24,25,31). The overall organization of these genes and two additional structural genes are transcribed in the same direction, and their expression is elicited by a single metabolite-inducer, protocatechuate.…”

Section: Downloaded Frommentioning

confidence: 66%

“…In many cases, a single ancestral enzyme was the evolutionary source of a range of enzymes catalyzing similar reactions with different substrates. 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).…”

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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Acquisition of apparent DNA slippage structures during extensive evolutionary divergence of pcaD and catD genes encoding identical catalytic activities in Acinetobacter calcoaceticus

Cited by 30 publications

References 12 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

Bacteria Are Not What They Eat: That Is Why They Are So Diverse

Unusual ancestry of dehydratases associated with quinate catabolism in Acinetobacter calcoaceticus

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