1887

Abstract

sp. strain DBF63 is capable of degrading fluorene (FN) to tricarboxylic acid cycle intermediates via phthalate and protocatechuate. Genes were identified for the protocatechuate branch of the -ketoadipate pathway (, ) by sequence analysis of a 70 kb DNA region of the FN-catabolic linear plasmid pDBF1. RT-PCR analysis of RNA from DBF63 cells grown with FN, dibenzofuran, and protocatechuate indicated that the operon was expressed during both FN and protocatechuate degradation in strain DBF63. The gene encoding -ketoadipate enol-lactone hydrolase () was not fused to the next gene, which encodes -carboxymuconolactone decarboxylase (), in strain DBF63, even though the presence of the gene (the fusion of and ) within a gene cluster has been thought to be a Gram-positive trait. Quantitative RT-PCR analysis revealed that mRNA levels increased sharply in response to protocatechuate, and a biotransformation experiment with ,-muconate using carrying both and indicated that PcaD exhibited -ketoadipate enol-lactone hydrolase activity. The location of the gene cluster on the linear plasmid, and the insertion sequences around the gene cluster suggest that the ecologically important -ketoadipate pathway genes, usually located chromosomally, may be spread widely among bacterial species via horizontal transfer or transposition events.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28215-0
2005-11-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/151/11/3713.html?itemId=/content/journal/micro/10.1099/mic.0.28215-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Madden T. L., Schaffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3420 [CrossRef]
    [Google Scholar]
  2. Buchan A., Neidle E. L., Moran M. A. 2004; Diverse organization of genes of the β -ketoadipate pathway in members of the marine Rosebacter lineage. Appl Environ Microbiol 70:1658–1668 [CrossRef]
    [Google Scholar]
  3. Cerniglia C. E. 1992; Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351–368 [CrossRef]
    [Google Scholar]
  4. Dagley S., Evans W. C., Ribbons D. W. 1960; New pathways in the oxidative metabolism of aromatic compounds by micro-organisms. Nature 188:560–566 [CrossRef]
    [Google Scholar]
  5. Eaton R. W. 2001; Plasmid-encoded phthalate catabolic pathway in Arthrobacter keyseri 12B. J Bacteriol 183:3689–3703 [CrossRef]
    [Google Scholar]
  6. Eckstein T. M., Inamine J. M., Lambert M. L., Belisle J. T. 2000; A genetic mechanism for deletion of the ser2 gene cluster and formation of rough morphological variants of Mycobacterium avium . J Bacteriol 182:6177–6182 [CrossRef]
    [Google Scholar]
  7. Eulberg D., Lakner S., Golovleva L. A, Schlömann M. 1998; Characterization of a protocatechuate catabolic gene cluster from Rhodococcus opacus 1CP: evidence for a merged enzyme with 4-carboxymuconolactone-decarboxylating and 3-oxoadipate enol-lactone-hydrolyzing activity. J Bacteriol 180:1072–1081
    [Google Scholar]
  8. Finan T. M., Weidner S., Wong K. 9 other authors 2001; The complete sequence of the 1,683-kb pSymB megaplasmid from the N2-fixing endosymbiont Sinorhizobium meliloti . Proc Natl Acad Sci U S A 98:9889–9894 [CrossRef]
    [Google Scholar]
  9. Grifoll M., Selifonov S. A., Chapman P. J. 1995a; Transformation of substituted fluorenes and fluorene analogs by Pseudomonas sp. strain F274. Appl Environ Microbiol 61:3490–3493
    [Google Scholar]
  10. Grifoll M., Selifonov S. A., Gatlin C. V., Chapman P. J. 1995b; Actions of a versatile fluorene-degrading bacterial isolate on polycyclic aromatic compounds. Appl Environ Microbiol 61:3711–3723
    [Google Scholar]
  11. Habe H., Omori T. 2003; Genetics of polycyclic aromatic hydrocarbon metabolism in diverse aerobic bacteria. Biosci Biotechnol Biochem 67:225–243 [CrossRef]
    [Google Scholar]
  12. Habe H., Miyakoshi M., Chung J.-S., Kasuga K., Yoshida T., Nojiri H., Omori T. 2003; Phthalate catabolic gene cluster is linked to the angular dioxygenase gene in Terrabacter sp. strain DBF63. Appl Microbiol Biotechnol 61:44–54 [CrossRef]
    [Google Scholar]
  13. Habe H., Chung J.-S., Kato H., Ayabe Y., Kasuga K., Yoshida T., Nojiri H., Yamane H., Omori T. 2004; Characterization of the upper pathway genes for fluorene metabolism in Terrabacter sp. strain DBF63. J Bacteriol 186:5938–5944 [CrossRef]
    [Google Scholar]
  14. Hanahan D. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580 [CrossRef]
    [Google Scholar]
  15. Harwood C. S., Parales R. E. 1996; The β -ketoadipate pathway and the biology of self identity. Annu Rev Microbiol 50:553–590 [CrossRef]
    [Google Scholar]
  16. Iwagami S. G., Yang K., Davies J. 2000; Characterization of the protocatechuic acid catabolic gene cluster from Streptomyces sp. strain 2065. Appl Environ Microbiol 66:1499–1508 [CrossRef]
    [Google Scholar]
  17. Jensen T. J., Hites R. A. 1983; Aromatic diesel emissions as a function of engine conditions. Anal Chem 55:594–599 [CrossRef]
    [Google Scholar]
  18. Jimenez J. I., Minambres B., Garcia J. L., Diaz E. 2002; Genomic analysis of the aromatic catabolic pathways from Pseudomonas putida KT2440. Environ Microbiol 4:824–841 [CrossRef]
    [Google Scholar]
  19. Kanaly R. A., Harayama S. 2000; Biodegradation of high-molecular-weight polycyclic aromatic hydrocarbons by bacteria. J Bacteriol 182:2059–2067 [CrossRef]
    [Google Scholar]
  20. Kasuga K., Nojiri H., Yamane H., Kodama T., Omori T. 1997; Cloning and characterization of the genes involved in the degradation of dibenzofuran by Terrabacter sp. strain DBF63. J Ferment Bioeng 84:387–399 [CrossRef]
    [Google Scholar]
  21. Kasuga K., Habe H., Chung J.-S., Yoshida T., Nojiri H., Yamane H., Omori T. 2001; Isolation and characterization of the genes encoding a novel oxygenase component of angular dioxygenase from the gram-positive dibenzofuran-degrader Terrabacter sp. strain DBF63. Biochem Biophys Res Commun 283:195–204 [CrossRef]
    [Google Scholar]
  22. Keith L. H., Telliard W. A. 1979; Priority pollutants. I. A perspective view. Environ Sci Technol 13:416–423 [CrossRef]
    [Google Scholar]
  23. König C., Eulberg D., Gröning J., Lakner S., Seibert V., Kaschabek S. R., Schlömann M. 2004; A linear megaplasmid, p1CP, carrying the genes for chlorocatechol catabolism of Rhodococcus opacus 1CP. Microbiology 150:3075–3087 [CrossRef]
    [Google Scholar]
  24. Monna L., Omori T., Kodama T. 1993; Microbial degradation of dibenzofuran, fluorene, and dibenzo- p -dioxin by Staphylococcus auriculans DBF63. Appl Environ Microbiol 59:285–289
    [Google Scholar]
  25. Nojiri H., Kamakura M., Urata M., Tanaka T., Chung J.-S., Takemura T., Yoshida T., Habe H., Omori T. 2002a; Dioxin catabolic genes are dispersed on the Terrabacter sp. DBF63 genome. Biochem Biophys Res Commun 296:233–240 [CrossRef]
    [Google Scholar]
  26. Nojiri H., Maeda K., Sekiguchi H., Urata M., Shintani M., Yoshida T., Habe H., Omori T. 2002b; Organization and transcriptional characterization of catechol degradation genes involved in carbazole degradation by Pseudomonas resinovorans strain CA10. Biosci Biotechnol Biochem 66:897–901 [CrossRef]
    [Google Scholar]
  27. Noumura T., Habe H., Widada J., Chung J.-S., Yoshida T., Nojiri H., Omori T. 2004; Genetic characterization of the dibenzofuran-degrading Actinobacteria carrying the dbfA1A2 gene homologues isolated from activated sludge. FEMS Microbiol Lett 239:147–155 [CrossRef]
    [Google Scholar]
  28. Orville A. M., Lipscomb J. D., Ohlendorf D. H. 1997; Crystal structures of substrate and substrate analog complexes of protocatechuate 3,4-dioxygenase: endogenous Fe3+ ligand displacement in response to substrate binding. Biochemistry 36:10052–10066 [CrossRef]
    [Google Scholar]
  29. Parke D. 1995; Supraoperonic clustering of pca genes for catabolism of the phenolic compound protocatechuate in Agrobacterium tumefaciens . J Bacteriol 177:3808–3817
    [Google Scholar]
  30. Parke D. 1997; Acquisition, reorganization, and merger of genes: novel management of the β -ketoadipate pathway in Agrobacterium tumefaciens . FEMS Microbiol Lett 146:3–12 [CrossRef]
    [Google Scholar]
  31. Parke D., D'Argenio D. A., Ornston L. N. 2000; Bacteria are not what they eat: that is why they are so diverse. J Bacteriol 182:257–263 [CrossRef]
    [Google Scholar]
  32. Pathak D., Ashley G., Ollis D. 1991; Thiol protease-like active site found in the enzyme dienelactone hydrolase: localization using biochemical, genetic and structural tools. Proteins 9:267–279 [CrossRef]
    [Google Scholar]
  33. Patrauchan M. A., Florizone C., Dosanjh M., Mohn W. W., Davies J., Eltis L. D. 2005; Catabolism of benzoate and phthalate in Rhodococcus sp. strain RHA1: redundancies and convergence. J Bacteriol 187:4050–4063 [CrossRef]
    [Google Scholar]
  34. Pinyakong O., Habe H., Omori T. 2003; The unique aromatic catabolic genes in sphingomonads degrading polycyclic aromatic hydrocarbons. J Gen Appl Microbiol 49:1–19 [CrossRef]
    [Google Scholar]
  35. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  36. Shine J., Dalgarno L. 1975; Determination of cistron specificity in bacterial ribosomes. Nature 254:34–38 [CrossRef]
    [Google Scholar]
  37. Shuttleworth K. L., Cerniglia C. E. 1995; Environmental aspects of PAH biodegradation. Appl Biochem Biotechnol 54:291–302 [CrossRef]
    [Google Scholar]
  38. Stecker C., Johann A., Herzberg C., Averhoff B., Gottschalk G. 2003; Complete nucleotide sequence and genetic organization of the 210-kilobase linear plasmid of Rhodococcus erythropolis BD2. J Bacteriol 185:5269–5274 [CrossRef]
    [Google Scholar]
  39. Vetting M. W., D'Argenio D. A., Ornston L. N., Ohlendorf D. H. 2000; Structures of Acinetobacter strain ADP1 protocatechuate 3,4-dioxygenase at 2·2 Å resolution: implications for the mechanism of an intradiol dioxygenase. Biochemistry 39:7943–7955 [CrossRef]
    [Google Scholar]
  40. Winstanley C., Taylor S. C., Williams P. A. 1987; pWW174: a large plasmid from Acinetobacter calcoaceticus encoding benzene catabolism by the β -ketoadipate pathway. Mol Microbiol 1:219–227 [CrossRef]
    [Google Scholar]
  41. Yamasaki M., Redenbach M., Kinashi H. 2001; Integrated structures of the linear plasmid SCP1 in two bidirectional donor strains of Streptomyces coelicolor A3(2). Mol Gen Genet 264:634–642 [CrossRef]
    [Google Scholar]
  42. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28215-0
Loading
/content/journal/micro/10.1099/mic.0.28215-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error