1887

Abstract

Carbon catabolite repression is an important mechanism allowing efficient carbon source utilization. In the soil bacterium , this mechanism has been shown to apply to the aromatic degradative pathways for the substrates protocatechuate, -hydroxybenzoate and vanillate. In this investigation, transcriptional fusions with the gene for luciferase in the gene clusters for the degradation of benzyl esters, anthranilate, benzoate, hydroxycinnamates and dicarboxylates (, , , and genes) were constructed and established in the chromosome of . The respective strains revealed the presence of strong carbon catabolite repression at the transcriptional level. In all cases, succinate and acetate in combination had the strongest repressing effect, and pyruvate (or lactate in case of the and genes) allowed the highest expression when these carbon sources were supplied together with the respective inducer. The pattern of repression for the different cosubstrates was similar for all operons investigated and was also observed in the absence of the respective inducing compounds, indicating a mechanism that is independent of the respective specific regulators. Repression by acetate and succinate varied between 88 % for the genes and 99 % for the genes.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2008/016907-0
2008-10-01
2024-05-01
Loading full text...

Full text loading...

/deliver/fulltext/micro/154/10/3095.html?itemId=/content/journal/micro/10.1099/mic.0.2008/016907-0&mimeType=html&fmt=ahah

References

  1. Barbe V., Vallenet D., Fonknechten N., Kreimeyer A., Oztas S., Labarre L., Cruveiller S., Robert C., Duprat S. other authors 2004; Unique features revealed by the genome sequence of Acinetobacter sp. ADP1, a versatile and naturally transformation competent bacterium. Nucleic Acids Res 32:5766–5779
    [Google Scholar]
  2. Bundy B. M., Campbell A. L., Neidle E. L. 1998; Similarities between the antABC-encoded anthranilate dioxygenase and the benABC-encoded benzoate dioxygenase of Acinetobacter sp. strain ADP1. J Bacteriol 180:4466–4474
    [Google Scholar]
  3. Bundy B. M., Collier L. S., Hoover T. R., Neidle E. L. 2002; Synergistic transcriptional activation by one regulatory protein in response to two metabolites. Proc Natl Acad Sci U S A 99:7693–7698
    [Google Scholar]
  4. Cánovas J. L., Stanier R. Y. 1967; Regulation of the enzymes of the β-ketoadipate pathway in Moraxella calcoacetica. 1. General aspects. Eur J Biochem 1:289–300
    [Google Scholar]
  5. Cases I., Lopez J. A., Albar J. P., De Lorenzo V. 2001; Evidence of multiple regulatory functions for the PtsN (IIANtr) protein of Pseudomonas putida . J Bacteriol 183:1032–1037
    [Google Scholar]
  6. Collier D. N., Hager P. W., Phibbs P. V. Jr 1996; Catabolite repression control in the pseudomonads. Res Microbiol 147:551–561
    [Google Scholar]
  7. Collier L. S., Gaines G. L., Neidle E. L. 1998; Regulation of benzoate degradation in Acinetobacter sp. strain ADP1 by BenM, a LysR-type transcriptional activator. J Bacteriol 180:2493–2501
    [Google Scholar]
  8. Dal S., Steiner I., Gerischer U. 2002; Multiple operons connected with catabolism of aromatic compounds in Acinetobacter sp. strain ADP1 are under carbon catabolite repression. J Mol Microbiol Biotechnol 4:389–404
    [Google Scholar]
  9. Dinamarca M. A., Ruiz-Manzano A., Rojo F. 2002; Inactivation of cytochrome o ubiquinol oxidase relieves catabolic repression of the Pseudomonas putida GPo1 alkane degradation pathway. J Bacteriol 184:3785–3793
    [Google Scholar]
  10. Eby D. M., Beharry Z. M., Coulter E. D., Kurtz D. M., Neidle E. L. 2001; Characterization and evolution of anthranilate 1,2-dioxygenase from Acinetobacter sp. strain ADP1. J Bacteriol 183:109–118
    [Google Scholar]
  11. Ezezika O. C., Haddad S., Clark T. J., Neidle E. L., Momany C. 2007a; Distinct effector-binding sites enable synergistic transcriptional activation by BenM, a LysR-type regulator. J Mol Biol 367:616–629
    [Google Scholar]
  12. Ezezika O. C., Haddad S., Neidle E. L., Momany C. 2007b; Oligomerization of BenM, a LysR-type transcriptional regulator: structural basis for the aggregation of proteins in this family. Acta Crystallogr Sect F Struct Biol Cryst Commun 63:361–368
    [Google Scholar]
  13. Gerischer U. 2002; Specific and global regulation of genes associated with the degradation of aromatic compounds in bacteria. J Mol Microbiol Biotechnol 4:111–121
    [Google Scholar]
  14. Gerischer U., Jerg B., Fischer R. 2008; Spotlight on the Acinetobacter baylyi β-ketoadipate pathway: multiple levels of regulation. In Acinetobacter Molecular Biology pp 203–230 Edited by Gerischer U. Caister Scientific Press;
    [Google Scholar]
  15. Hanahan D. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580
    [Google Scholar]
  16. Harwood C. S., Parales R. E. 1996; The β-ketoadipate pathway and the biology of self-identity. Annu Rev Microbiol 50:553–590
    [Google Scholar]
  17. Hester K. L., Lehman J., Najar F., Song L., Roe B. A., MacGregor C. H., Hager P. W., Phibbs P. V. Jr, Sokatch J. R. 2000a; Crc is involved in catabolite repression control of the bkd operons of Pseudomonas putida and Pseudomonas aeruginosa . J Bacteriol 182:1144–1149
    [Google Scholar]
  18. Hester K. L., Madhusudhan K. T., Sokatch J. R. 2000b; Catabolite repression control by Crc in 2×YT medium is mediated by posttranscriptional regulation of bkdR expression in Pseudomonas putida . J Bacteriol 182:1150–1153
    [Google Scholar]
  19. Jones R. M., Williams P. A. 2001; areCBA is an operon in Acinetobacter sp. strain ADP1 and is controlled by AreR, a σ 54-dependent regulator. J Bacteriol 183:405–409
    [Google Scholar]
  20. Jones R. M., Collier L. S., Neidle E. L., Williams P. A. 1999; areABC genes determine the catabolism of aryl esters in Acinetobacter sp. strain ADP1. J Bacteriol 181:4568–4575
    [Google Scholar]
  21. MacGregor C. H., Wolff J. A., Arora S. K., Phibbs P. V. Jr 1991; Cloning of a catabolite repression control ( crc) gene from Pseudomonas aeruginosa, expression of the gene in Escherichia coli, and identification of the gene product in Pseudomonas aeruginosa . J Bacteriol 173:7204–7212
    [Google Scholar]
  22. Morales G., Linares J. F., Beloso A., Albar J. P., Martinez J. L., Rojo F. 2004; The Pseudomonas putida Crc global regulator controls the expression of genes from several chromosomal catabolic pathways for aromatic compounds. J Bacteriol 186:1337–1344
    [Google Scholar]
  23. Morales G., Ugidos A., Rojo F. 2006; Inactivation of the Pseudomonas putida cytochrome o ubiquinol oxidase leads to a significant change in the transcriptome and to increased expression of the CIO and cbb3-1 terminal oxidases. Environ Microbiol 8:1764–1774
    [Google Scholar]
  24. Moreno R., Rojo F. 2007; The target for the Pseudomonas putida Crc global regulator at the benzoate degradation pathway is the BenR transcriptional regulator. J Bacteriol 190:1539–1545
    [Google Scholar]
  25. Moreno R., Ruiz-Manzano A., Yuste L., Rojo F. 2007; The Pseudomonas putida Crc global regulator is an RNA binding protein that inhibits translation of the AlkS transcriptional regulator. Mol Microbiol 64:665–675
    [Google Scholar]
  26. Müller C., Petruschka L., Cuypers H., Burchhardt G., Herrmann H. 1996; Carbon catabolite repression of phenol degradation in Pseudomonas putida is mediated by the inhibition of the activator protein PhlR. J Bacteriol 178:2030–2036
    [Google Scholar]
  27. Neidle E. L., Hartnett C., Ornston L. N., Bairoch A., Rekik M., Harayama S. 1991; Nucleotide sequences of the Acinetobacter calcoaceticus benABC genes for benzoate 1,2-dioxygenase reveal evolutionary relationships among multicomponent oxygenases. J Bacteriol 173:5385–5395
    [Google Scholar]
  28. Parke D., Ornston L. N. 2004; Toxicity caused by hydroxycinnamoyl-coenzyme A thioester accumulation in mutants of Acinetobacter sp. strain ADP1. Appl Environ Microbiol 70:2974–2983
    [Google Scholar]
  29. Parke D., Garcia M. A., Ornston L. N. 2001; Cloning and genetic characterization of dca genes required for beta-oxidation of straight-chain dicarboxylic acids in Acinetobacter sp. strain ADP1. Appl Environ Microbiol 67:4817–4827
    [Google Scholar]
  30. Petruschka L., Burchhardt G., Müller C., Weihe C., Herrmann H. 2001; The cyo operon of Pseudomonas putida is involved in carbon catabolite repression of phenol degradation. Mol Genet Genomics 266:199–206
    [Google Scholar]
  31. Podbielski A., Woischnik M., Leonard B. A., Schmidt K. H. 1999; Characterization of nra, a global negative regulator gene in group A streptococci. Mol Microbiol 31:1051–1064
    [Google Scholar]
  32. Sambrook J., Russell D. W. 2001 Molecular Cloning: a Laboratory Manual , 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  33. Siehler S. Y., Dal S., Fischer R., Patz P., Gerischer U. 2007; Multiple-level regulation of genes for protocatechuate degradation in Acinetobacter baylyi includes cross-regulation. Appl Environ Microbiol 73:232–242
    [Google Scholar]
  34. Smith M. A., Weaver V. B., Young D. M., Ornston L. N. 2003; Genes for chlorogenate and hydroxycinnamate catabolism ( hca) are linked to functionally related genes in the dca-pca-qui-pob-hca chromosomal cluster of Acinetobacter sp. strain ADP1. Appl Environ Microbiol 69:524–532
    [Google Scholar]
  35. Stülke J., Hillen W. 1999; Carbon catabolite repression in bacteria. Curr Opin Microbiol 2:195–201
    [Google Scholar]
  36. Trautwein G., Gerischer U. 2001; Effects exerted by transcriptional regulator PcaU from Acinetobacter sp. strain ADP1. J Bacteriol 183:873–881
    [Google Scholar]
  37. Vaneechoutte M., Young D. M., Ornston L. N., De Baere T., Nemec A., Van Der Reijden T., Carr E., Tjernberg I., Dijkshoorn L. 2006; Naturally transformable Acinetobacter sp. strain ADP1 belongs to the newly described species Acinetobacter baylyi . Appl Environ Microbiol 72:932–936
    [Google Scholar]
  38. Williams P., Kay C. M. 2008; The catabolism of aromatic compounds by Acinetobacter . In Acinetobacter Molecular Biology pp 99–118 Edited by Gerischer U. Norfolk, UK: Caister Academic Press;
    [Google Scholar]
  39. Wolff J. A., MacGregor C. H., Eisenberg R. C., Phibbs P. V. Jr 1991; Isolation and characterization of catabolite repression control mutants of Pseudomonas aeruginosa PAO. J Bacteriol 173:4700–4706
    [Google Scholar]
  40. Young D. M., Parke D., Ornston L. N. 2005; Oppotunities for genetic investigation afforded by Acinetobacter baylyi, a nutritionally versatile bacterial species that is highly competent for natural transformation. Annu Rev Microbiol 59:519–551
    [Google Scholar]
  41. Yuste L., Rojo F. 2001; Role of the crc gene in catabolic repression of the Pseudomonas putida GPo1 alkane degradation pathway. J Bacteriol 183:6197–6206
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2008/016907-0
Loading
/content/journal/micro/10.1099/mic.0.2008/016907-0
Loading

Data & Media loading...

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