Evolution of a chlorobenzene degradative pathway among bacteria in a contaminated groundwater mediated by a genomic island in Ralstonia.

The genetic structure of two Ralstonia spp., strain JS705 and strain JS745, isolated from the same groundwater aquifer, was characterized with respect to the degradation capacities for toluene and chlorobenzene degradation. Cosmid library construction, cloning, DNA sequencing and mating experiments indicated that the genes for chlorobenzene degradation in strain JS705 were a mosaic of the clc genes, previously described for Pseudomonas sp. strain B13, and a 5 kb fragment identical to strain JS745. The 5 kb fragment identical to both JS705 and JS745 was flanked in JS705 by one complete and one incomplete insertion (IS) element. This suggested involvement of the IS element in mobilizing the genes from JS745 to JS705, although insertional activity of the IS element in its present configuration could not be demonstrated. The complete genetic structure for chlorobenzene degradation in strain JS705 resided on a genomic island very similar to the clc element (Ravatn, R., Studer, S., Springael, D., Zehnder, A.J., van der Meer, J.R. 1998. Chromosomal integration, tandem amplification, and deamplification in Pseudomonas putida F1 of a 105-kilobase genetic element containing the chlorocatechol degradative genes from Pseudomonas sp. strain B13. J Bacteriol 180: 4360-4369). The unique reconstruction of formation of a metabolic pathway through the activity of IS elements and a genomic island in the chlorobenzene-degrading strain JS705 demonstrated how pathway evolution can occur under natural conditions in a few 'steps'.

[1]  M. Mergeay,et al.  Community shifts in a seeded 3-chlorobenzoate degrading membrane biofilm reactor: indications for involvement of in situ horizontal transfer of the clc-element from inoculum to contaminant bacteria. , 2002, Environmental microbiology.

[2]  A. Arment,et al.  Cloning, Nucleotide Sequencing, and Functional Analysis of a Novel, Mobile Cluster of Biodegradation Genes fromPseudomonas aeruginosa Strain JB2 , 2001, Applied and Environmental Microbiology.

[3]  R. Wing,et al.  Complete Nucleotide Sequence and Organization of the Atrazine Catabolic Plasmid pADP-1 from Pseudomonassp. Strain ADP , 2001, Journal of bacteriology.

[4]  V. Sentchilo,et al.  The clc element of Pseudomonas sp. strain B13 and other mobile degradative elements employing phage-like integrases , 2001, Archives of Microbiology.

[5]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[6]  G. Paoli,et al.  Sequence Analysis and Initial Characterization of Two Isozymes of Hydroxylaminobenzene Mutase from Pseudomonas pseudoalcaligenes JS45 , 2000, Applied and Environmental Microbiology.

[7]  J. Ramos,et al.  Toluene metabolism by the solvent-tolerant Pseudomonas putida DOT-T1 strain, and its role in solvent impermeabilization. , 1999, Gene.

[8]  J. Kingma,et al.  Conversion of 3-Chlorocatechol by Various Catechol 2,3-Dioxygenases and Sequence Analysis of the Chlorocatechol Dioxygenase Region of Pseudomonas putida GJ31 , 1999, Journal of bacteriology.

[9]  K. Timmis,et al.  Genetic and Biochemical Analyses of thetec Operon Suggest a Route for Evolution of Chlorobenzene Degradation Genes , 1999, Journal of bacteriology.

[10]  A. Zehnder,et al.  Int-B13, an Unusual Site-Specific Recombinase of the Bacteriophage P4 Integrase Family, Is Responsible for Chromosomal Insertion of the 105-Kilobase clc Element ofPseudomonas sp. Strain B13 , 1998, Journal of bacteriology.

[11]  J. R. van der Meer,et al.  Evolution of a Pathway for Chlorobenzene Metabolism Leads to Natural Attenuation in Contaminated Groundwater , 1998, Applied and Environmental Microbiology.

[12]  J. Tiedje,et al.  Evidence for Interspecies Gene Transfer in the Evolution of 2,4-Dichlorophenoxyacetic Acid Degraders , 1998, Applied and Environmental Microbiology.

[13]  J. R. van der Meer,et al.  Chromosomal Integration, Tandem Amplification, and Deamplification in Pseudomonas putida F1 of a 105-Kilobase Genetic Element Containing the Chlorocatechol Degradative Genes from Pseudomonas sp. Strain B13 , 1998, Journal of bacteriology.

[14]  J. R. van der Meer,et al.  Low-Frequency Horizontal Transfer of an Element Containing the Chlorocatechol Degradation Genes fromPseudomonas sp. Strain B13 to Pseudomonas putidaF1 and to Indigenous Bacteria in Laboratory-Scale Activated-Sludge Microcosms , 1998, Applied and Environmental Microbiology.

[15]  F. Fava,et al.  Structures of Homologous Composite Transposons Carrying cbaABC Genes from Europe and North America , 1998, Applied and Environmental Microbiology.

[16]  L. Wackett,et al.  The Atrazine Catabolism Genes atzABC Are Widespread and Highly Conserved , 1998, Journal of bacteriology.

[17]  H. Wand,et al.  Acquisition of a deliberately introduced phenol degradation operon, pheBA, by different indigenous Pseudomonas species , 1997, Applied and environmental microbiology.

[18]  J. Leveau,et al.  Genetic characterization of insertion sequence ISJP4 on plasmid pJP4 from Ralstonia eutropha JMP134. , 1997, Gene.

[19]  D. Janssen,et al.  Microbial degradation of chloroaromatics: use of the meta-cleavage pathway for mineralization of chlorobenzene , 1997, Journal of bacteriology.

[20]  K. Timmis,et al.  Genetic and biochemical characterization of the broad spectrum chlorobenzene dioxygenase from Burkholderia sp. strain PS12--dechlorination of 1,2,4,5-tetrachlorobenzene. , 1997, European journal of biochemistry.

[21]  E. Madsen,et al.  Natural horizontal transfer of a naphthalene dioxygenase gene between bacteria native to a coal tar-contaminated field site , 1997, Applied and environmental microbiology.

[22]  J. R. Meer Evolution of novel metabolic pathways for the degradation of chloroaromatic compounds , 1997, Antonie van Leeuwenhoek.

[23]  J. R. van der Meer,et al.  The Broad Substrate Chlorobenzene Dioxygenase and cis-Chlorobenzene Dihydrodiol Dehydrogenase of Pseudomonas sp. Strain P51 Are Linked Evolutionarily to the Enzymes for Benzene and Toluene Degradation (*) , 1996, The Journal of Biological Chemistry.

[24]  J. Tiedje,et al.  2,4-Dichlorophenoxyacetic acid-degrading bacteria contain mosaics of catabolic genes , 1995, Applied and environmental microbiology.

[25]  Y. Wang,et al.  Sequence and expression of the todGIH genes involved in the last three steps of toluene degradation by Pseudomonas putida F1. , 1994, Gene.

[26]  C. Pettigrew,et al.  Biodegradation of chlorobenzene by indigenous bacteria , 1994 .

[27]  V. Beneš,et al.  M13 and pUC vectors with new unique restriction sites for cloning. , 1993, Gene.

[28]  S. Henikoff,et al.  Nucleotide sequence and initial functional characterization of the clcR gene encoding a LysR family activator of the clcABD chlorocatechol operon in Pseudomonas putida , 1993, Journal of bacteriology.

[29]  J. Spain,et al.  Chlorobenzene degradation by bacteria isolated from contaminated groundwater , 1992, Applied and environmental microbiology.

[30]  W. D. de Vos,et al.  Identification of a novel composite transposable element, Tn5280, carrying chlorobenzene dioxygenase genes of Pseudomonas sp. strain P51 , 1991, Journal of bacteriology.

[31]  D. Gibson,et al.  Location and sequence of the todF gene encoding 2-hydroxy-6-oxohepta-2,4-dienoate hydrolase in Pseudomonas putida F1. , 1991, Gene.

[32]  D. Gibson,et al.  Toluene degradation by Pseudomonas putida F1. Nucleotide sequence of the todC1C2BADE genes and their expression in Escherichia coli. , 1989, The Journal of biological chemistry.

[33]  D. Gibson,et al.  Toluene degradation by Pseudomonas putida F1: genetic organization of the tod operon , 1988, Applied and environmental microbiology.

[34]  B. Frantz,et al.  Organization and nucleotide sequence determination of a gene cluster involved in 3-chlorocatechol degradation. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[35]  J C Spain,et al.  Degradation of 1,4-dichlorobenzene by a Pseudomonas sp , 1987, Applied and environmental microbiology.

[36]  K. Timmis,et al.  Transposon mutagenesis and cloning analysis of the pathways for degradation of 2,4-dichlorophenoxyacetic acid and 3-chlorobenzoate in Alcaligenes eutrophus JMP134(pJP4) , 1985, Journal of bacteriology.

[37]  D. Helinski,et al.  Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[38]  W. Reineke,et al.  Construction of haloaromatics utilising bacteria , 1979, Nature.

[39]  W. Reineke,et al.  Isolation and characterization of a 3-chlorobenzoate degrading pseudomonad , 2004, Archives of Microbiology.

[40]  W Arber,et al.  Genetic variation: molecular mechanisms and impact on microbial evolution. , 2000, FEMS microbiology reviews.

[41]  Gapped BLAST and PSI-BLAST: A new , 1997 .

[42]  A. Pühler,et al.  Plasmid vectors for the genetic analysis and manipulation of rhizobia and other gram-negative bacteria. , 1986, Methods in enzymology.

[43]  C. Yanisch-Perron,et al.  Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. , 1985, Gene.