Chapter 16 : Degradative Plasmids

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Degradative plasmids carry genes that confer on the host bacteria the ability to degrade recalcitrant organic compounds not commonly found in nature. Many plasmid-encoded degradative gene clusters are also discrete regulons if they have regulators specialized for the regularion of the genes encoding degradative enzymes. The degradation pathway is composed of two segments when it is delimited by substrates for growth and the integrity as transcriptional units, each of which has a wide range of enzymatic substrate specificity toward alkyl-substituted aromatic compounds. The recent completion of the nucleotide sequencing of the whole pWWO plasmid revealed open reading frames (ORFs) related to plasmid replication, maintenance, and transfer. Other toluene-degradative (TOL) plasmid, such as pWW53 and pDK1 , have been found to have upper and lower pathways at different relative locations on the plasmids, although the organizations of the structural genes for the degradative enzymes in the respective cluster are highly conserved. Most of the 2,4-D plasmids were found in strains isolated by enrichment on 2,4-D as the sole source of carbon and energy, and some of them were found to take part in the degradation of a herbicide with a similar structure, 2-methyI-4-chlorophenoxyacetic acid. The lower pathway includes cleavage of the aromatic ring by dioxygenases with formation of (chloro)maleylacetates. The genes on TOL plasmids, including pWWO, and the related and genes have enabled comparative studies, as described. Transposon Tn5271 on plasmid pBRC60 is not flanked by target-site duplications on both sides, which are supposed to be generated during transposition.

Citation: Ogawa N, Chakrabarty A, Zaborina O. 2004. Degradative Plasmids, p 341-376. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch16

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Image of Figure 1.
Figure 1.

The catabolic pathways/genes involved in the degradation of xylene encoded by TOL plasmids and the corresponding genes in the degradative pathway for naphthalene and dimethylphcnol on NAH7 and pVI 150, respectively. The structure of the compound numbered 1 that serves as growth substrate for strain mt-2 is (Rl = R2 = H, toluene), (Rl = CH, R2 = H, -xylene), (Rl = H, R2 = CH, -xylene), (Rl = CH, R2 = H, 3-ethyltoluene), and (Rl = CH , R2 = CH, 1,2,4-trimethylbenzene). The metabolites numbered 2 to 11 in the case where the substrate is toluene are: 2, benzyl alcohol; 3, benzaldehyde; 4, benzoate; 5, benzoate dihydrodiol (l,2-dihydrocyclohexa-3,5-diene carboxylate); 6, catechol; 7, 2-hydroxymuconic semialdehyde; 8, 4-oxalocrotonate (enol); 9, 4-oxalocrotonate (keto); 10, 2-oxopentenoate (enol) or 2-hydroxypent-2,4-dienoate; and 11, 4-hydroxy-2-oxovalerate. Enzyme abbreviations are: XO, xylene oxygenase; BADH, benzyl alcohol dehydrogenase; BZDH, benzaldehyde dehydrogenase; TO, toluate 1,2-dioxygenase; DHCDH, 1,2-dihydroxycyclohexa-3,5-dicne carboxylate (benzoatc dihydrodiol) dehydrogenase; C230, catechol 2,3-dioxygenase; HMSH, 2-hydroxymuconic-scmialdehyde hydrolase; HMSD, 2-hydroxymuconic-semialdehyde dehydrogenase; 4OI, 4-oxalocrotonate isomerase; 4OD, 4-oxalocrotonate decarboxylase; OEH, 2-oxo-4-pemenoate (or 2-hydroxy-2,4-dienoate) hydratase; and HOA, 4-hydroxy-2-oxovalerate aldolase. The TOL pathway was adapted from that of Assindcr and Williams ( ) with permission from Elsevier. Respective pathways are described elsewhere ( ).

Citation: Ogawa N, Chakrabarty A, Zaborina O. 2004. Degradative Plasmids, p 341-376. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch16
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Image of Figure 2.
Figure 2.

(a) Regulatory circuits of the catabolic genes that degrade xylene/toluene on pWW0. Reproduced with permission from the ( ), © 1997 by Annual Reviews, (b) Relative locations of the catabolic and regulatory genes and the transposons on TOL and NAH plasmids. These plasmids share homologous catechol -cleavage pathway genes. The incongruity of relative locations of the genes and transposons suggests independent recruitment of the genes by the transposons. The figure is not drawn to scale. Precise maps are available elsewhere ( ).

Citation: Ogawa N, Chakrabarty A, Zaborina O. 2004. Degradative Plasmids, p 341-376. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch16
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Image of Figure 3.
Figure 3.

The catabolic pathways/genes involved in the degradation of 2,4-D, and the schematic representation of the catabolic gene region on pJP4 and pMAB1. The metabolites of 2,4-D (numbered 1, 2,4-dichlorophcnoxyacetate) arc numbered 2 to 7; 2, 2,4-dichlorophenol; 3, 3,5-dichlorocatechol; 4, 2,4-dichloro--muconate; 5,2-chlorodienelactone; 6, 2-chloromaleylacetate; and 7, β-ketoadipate. The genes and the corresponding enzymes are; , 2,4-dichloro phenoxyacetate/α-ketoglutarate dioxygenase; , 2,4-dichlorophcnol hydroxylase; , 3,5-dichlorocatechol 1,2-dioxygenase; , chloromuconatc cycloisomerasc; , dienlactone hydrolase; and , (chloro)maleylacetate reductase. An asterisk indicates ca. 200-bp intergenic region containing 71-bp sequence identical to downward extremity of ISJP4.

Citation: Ogawa N, Chakrabarty A, Zaborina O. 2004. Degradative Plasmids, p 341-376. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch16
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Image of Figure 4.
Figure 4.

The catabolic pathways/genes of benzoic acid, phenol, and 3-chlorobenzoic acid via -deavage pathways.

Citation: Ogawa N, Chakrabarty A, Zaborina O. 2004. Degradative Plasmids, p 341-376. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch16
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Image of Figure 5.
Figure 5.

Organization of the gene clusters of intradiol-cleavage pathways that degrade (chloro)catechol or (chloro)hydroxyquinol. Identities at amino acid sequence level between the corresponding genes are indicated numerically (%).

Citation: Ogawa N, Chakrabarty A, Zaborina O. 2004. Degradative Plasmids, p 341-376. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch16
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Image of Figure 10.
Figure 10.

The schematic representation of the catabolic gene regions on pENH91 and pP51. Reproduced from reference . The map of pP51 is based on references . , and .

Citation: Ogawa N, Chakrabarty A, Zaborina O. 2004. Degradative Plasmids, p 341-376. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch16
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Image of Figure 6.
Figure 6.

Replicons of AC1100. The sizes of rhe replicons are not drawn proportionally. The locations of the relevant genes are indicated by arrowheads.

Citation: Ogawa N, Chakrabarty A, Zaborina O. 2004. Degradative Plasmids, p 341-376. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch16
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Image of Figure 7.
Figure 7.

Pathway of 2,4,5-T degradation. The and genes encode two subunits of the 2,4,5-T oxygenase that convert 2,4,5-T into 2,4,5-TCP. A two-component flavin-containing monooxygenase encoded by the and genes catalyzes the para-hydroxylation of 2,4,5-TCP to yield 2,5-DCHQ. A second hydroxylation step by the same enzyme converts 2,5-DCHQ into 5-CHQ. The gene product, a dechlorinase, catalyzes dechlorination of 5-CHQ to yield HQox. An HBQ reductase reduces HQ-ox to HQ before HQDO, encoded by the gene, can catalyze ring cleavage to yield maleylacetate. Maleylacetate reductase, encoded by the gene, catalyzes the reduction of maleylacetate to β-ketoadipate, which ultimately is converted into tricarboxylic acid (TCA) cycle intermediates.

Citation: Ogawa N, Chakrabarty A, Zaborina O. 2004. Degradative Plasmids, p 341-376. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch16
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Image of Figure 8.
Figure 8.

A model of evolution of catechol weta-clcavage pathways and recruitment of other genes to form the lower pathways on NAH7, pWWO, and pVII50. Adapted from original by Harayama and Rekik ( ) with permission of the publisher.

Citation: Ogawa N, Chakrabarty A, Zaborina O. 2004. Degradative Plasmids, p 341-376. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch16
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Image of Figure 9.
Figure 9.

A model for the acquisition of the genes by a prototype plasmid of pENH91. The model is drawn based on the model of chromosome mobilization by IS proposed by Wyndham et al. ( ). While class II transposable elements to which IS belongs transfer by a replicative mechanism ( ), IS could transpose via a cut-and-paste (nonreplicative) mechanism in analogy with IS ( ). ( ) A prototype plasmid of pENH91 containing a single copy of IS. ( ) Tandem formation of IS on the plasmid, which facilitates the formation of cointegrate. ( ) Bacterial chromosome with a cbnRABCD gene cluster. The target sites (1 and 2) are written arbitrarily. No consensus target sequence is apparent for IS ( ). ( ) Cointegrate formation by the plasmid with the chromosome. Two to three nucleotides in the junction of IS tandem are lost during the reaction. ( ) Further insertion of another copy of IS beyond the catabolic region and subsequent deletion by homologous recombination beween the two distal copies of IS result in the formation of a plasmid with a composite transposon structure.

Citation: Ogawa N, Chakrabarty A, Zaborina O. 2004. Degradative Plasmids, p 341-376. In Funnell B, Phillips G (ed), Plasmid Biology. ASM Press, Washington, DC. doi: 10.1128/9781555817732.ch16
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