Growth phase-dependent transcription of the sigma(54)-dependent Po promoter controlling the Pseudomonas-derived (methyl)phenol dmp operon of pVI150
10.1128/jb.178.13.3727-3735.1996
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

Transcription from Pseudomonas-derived -24, -12 Po promoter of the pVI150-encoded dmp operon is mediated by the sigma 54-dependent DmpR activator in response to the presence of aromatic pathway substrates in the medium. However, global regulatory mechanisms are superimposed on this regulatory system so that the specific response to aromatic effectors is absent in cultures until the stationary phase is reached. Here we genetically dissect the system to show that the growth phase response is faithfully mimicked by a minimal system composed of the dmpR regulatory gene and the Po promoter regulatory region and can be reproduced in heterologous Escherichia coli. Using this system, we show that the growth phase-dependent DmpR-mediated response to aromatic compounds is limited to fast-growing cultures. Thus, during exponential growth of cultures in minimal media containing different carbon sources, the response to aromatics is immediate, while the response is suppressed in cultures grown on rich media until the exponential-to-stationary phase transition. Elements known to be involved in the DmpR-mediated transcription from Po were analyzed for the ability to influence the growth phase response. Most dramatically, overexpression of DmpR was shown to completely abolish the growth phase response, suggesting that a negatively acting factor may mediate this level of regulation. The possible mechanism of action and integration (of the specific regulation of the dmp operon-encoded catabolic enzymes with the physiological status of the bacteria are discussed.

Bibliography

Sze, C. C., Moore, T., & Shingler, V. (1996). Growth phase-dependent transcription of the sigma(54)-dependent Po promoter controlling the Pseudomonas-derived (methyl)phenol dmp operon of pVI150. Journal of Bacteriology, 178(13), 3727–3735.

Authors 3
  1. C C Sze (first)
  2. T Moore (additional)
  3. V Shingler (additional)
References 46 Referenced 65
  1. Austin , S. , and R. Dixon . 1992 . The prokaryotic enhancer binding protein NtrC has an ATPase activity which is phosphorylation and DNA dependent . EMBO J. 11 : 2219 - 2228 . (10.1002/j.1460-2075.1992.tb05281.x) / EMBO J. / The prokaryotic enhancer binding protein NtrC has an ATPase activity which is phosphorylation and DNA dependent by Austin S. (1992)
  2. Aviv , M. , H. Giladi , G. Schreiber , A. B. Oppenheim , and G. Glaser . 1994 . Expression of the genes encoding for the Escherichia coli integration host factor are controlled by growth phase, rpoS, ppGpp and by autoregulation . Mol. Microbiol. 14 : 1021 - 1031 . (10.1111/j.1365-2958.1994.tb01336.x) / Mol. Microbiol. / Expression of the genes encoding for the Escherichia coli integration host factor are controlled by growth phase, rpoS, ppGpp and by autoregulation by Aviv M. (1994)
  3. Balke , V. L. , and J. D. Gralla . 1987 . Changes in the linking number of supercoiled DNA accompanying growth transition in Escherichia coli . J. Bacteriol. 169 : 4499 - 4506 . (10.1128/JB.169.10.4499-4506.1987) / J. Bacteriol. / Changes in the linking number of supercoiled DNA accompanying growth transition in Escherichia coli by Balke V. L. (1987)
  4. Biek , D. P. , and S. N. Cohen . 1989 . Involvement of integration host factor (IHF) in maintenance of plasmid pSC101 in Escherichia coli: characterization of pSC101 mutants that replicate in the absence of IHF . J. Bacteriol. 171 : 2056 - 2065 . (10.1128/jb.171.4.2056-2065.1989) / J. Bacteriol. / Involvement of integration host factor (IHF) in maintenance of plasmid pSC101 in Escherichia coli: characterization of pSC101 mutants that replicate in the absence of IHF by Biek D. P. (1989)
  5. Casadaban , M. J. , and S. N. Cohen . 1980 . Analysis of gene control signals by DNA fusion and cloning in Escherichia coli . J. Mol. Biol. 138 : 179 - 207 . (10.1016/0022-2836(80)90283-1) / J. Mol. Biol. / Analysis of gene control signals by DNA fusion and cloning in Escherichia coli by Casadaban M. J. (1980)
  6. Cases , I. , V. de Lorenzo , and J. Pérez-Martín . 1996 . Involvement of sigma factor ~54 in exponential silencing of the Pseudomonas putida TOL plasmid Pu promoter . Mol. Microbiol. 19 : 7 - 17 . (10.1046/j.1365-2958.1996.345873.x) / Mol. Microbiol. / Involvement of sigma factor ~54 in exponential silencing of the Pseudomonas putida TOL plasmid Pu promoter by Cases I. (1996)
  7. Cronan , J. E. 1968 . Phospholipid alterations during growth of Escherichia coli . J. Bacteriol. 95 : 2054 - 2061 . (10.1128/jb.95.6.2054-2061.1968) / J. Bacteriol. / Phospholipid alterations during growth of Escherichia coli by Cronan J. E. (1968)
  8. Delgado , A. , and J. L. Ramos . 1994 . Genetic evidence for activation of the positive transcriptional regulator XylR, a member of the NtrC family of regulators, by effector binding . J. Biol. Chem. 269 : 8059 - 8062 . (10.1016/S0021-9258(17)37159-4) / J. Biol. Chem. / Genetic evidence for activation of the positive transcriptional regulator XylR, a member of the NtrC family of regulators, by effector binding by Delgado A. (1994)
  9. de Lorenzo , V. , I. Cases , M. Herrero , and K. N. Timmis . 1993 . Early and late response of TOL promoters to pathway inducers: identification of postexponential promoters in Pseudomonas putida with lacZ-tet bicistronic reporters . J. Bacteriol. 175 : 6902 - 6907 . (10.1128/JB.175.21.6902-6907.1993) / J. Bacteriol. / Early and late response of TOL promoters to pathway inducers: identification of postexponential promoters in Pseudomonas putida with lacZ-tet bicistronic reporters by de Lorenzo V. (1993)
  10. de Lorenzo , V. , L. Eltis , B. Kessler , and K. N. Timmis . 1993 . Analysis of Pseudomonas gene products using lacIq/Ptrp-lac plasmids and transposons that confer conditional phenotypes . Gene 123 : 17 - 24 . (10.1016/0378-1119(93)90533-9) / Gene / Analysis of Pseudomonas gene products using lacIq/Ptrp-lac plasmids and transposons that confer conditional phenotypes by de Lorenzo V. (1993)
  11. de Lorenzo , V. , M. Herrero , U. Jakubzik , and K. N. Timmis . 1990 . Mini-Tn5 transposon derivatives for insertional mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria . J. Bacteriol. 172 : 6568 - 6572 . (10.1128/JB.172.11.6568-6572.1990) / J. Bacteriol. / Mini-Tn5 transposon derivatives for insertional mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria by de Lorenzo V. (1990)
  12. Ditto , M. D. , D. Roberts , and R. A. Weisberg . 1994 . Growth phase variation of integration host factor level in Escherichia coli . J. Bacteriol. 176 : 3738 - 3748 . (10.1128/JB.176.12.3738-3748.1994) / J. Bacteriol. / Growth phase variation of integration host factor level in Escherichia coli by Ditto M. D. (1994)
  13. Duetz , W. A. , S. Marqués , C. de Jong , J. L. Ramos , and J. G. van Andel . 1994 . Inducibility of the TOL catabolic pathway in Pseudomonas putida (pWW0) growing on succinate in continuous culture: evidence of carbon catabolite repression control . J. Bacteriol. 176 : 2354 - 2361 . (10.1128/JB.176.8.2354-2361.1994) / J. Bacteriol. / Inducibility of the TOL catabolic pathway in Pseudomonas putida (pWW0) growing on succinate in continuous culture: evidence of carbon catabolite repression control by Duetz W. A. (1994)
  14. Férnandez , S. , V. Shingler , and V. de Lorenzo . 1995 . Cross-regulation by XylR and DmpR activators of Pseudomonas putida suggest that transcriptional control of biodegradation operons evolves independently of catabolic genes . J. Bacteriol. 176 : 5052 - 5058 . (10.1128/JB.176.16.5052-5058.1994) / J. Bacteriol. / Cross-regulation by XylR and DmpR activators of Pseudomonas putida suggest that transcriptional control of biodegradation operons evolves independently of catabolic genes by Férnandez S. (1995)
  15. Finkel , S. E. , and R. C. Johnson . 1992 . The Fis protein: it's not just for DNA inversion anymore . Mol. Microbiol. 6 : 3257 - 3265 . (10.1111/j.1365-2958.1992.tb02193.x) / Mol. Microbiol. / The Fis protein: it's not just for DNA inversion anymore by Finkel S. E. (1992)
  16. Franklin , F. C. H. , M. Bagdasarian , M. M. Bagdasarian , and K. N. Timmis . 1981 . Molecular and functional analysis of the TOL plasmid pWW0 from Pseudomonas putida and cloning of genes for the entire regulated aromatic ring meta-cleavage pathway . Proc. Natl. Acad. Sci. USA 78 : 7458 - 7462 . (10.1073/pnas.78.12.7458) / Proc. Natl. Acad. Sci. USA / Molecular and functional analysis of the TOL plasmid pWW0 from Pseudomonas putida and cloning of genes for the entire regulated aromatic ring meta-cleavage pathway by Franklin F. C. H. (1981)
  17. Fürste , J. P. , W. Pansegrau , R. Frank , H. Blöcker , P. Scholz , M. Bagdasarian , and E. Lanka . 1987 . Molecular cloning of the RP4 DNA primase region in a multirange tacP expression vector . Gene 55 : 19 - 28 . / Gene / Molecular cloning of the RP4 DNA primase region in a multirange tacP expression vector by Fürste J. P. (1987)
  18. Goosen , N. , and P. van de Putte . 1995 . The regulation of transcription by initiation host factor . Mol. Microbiol. 16 : 1 - 7 . (10.1111/j.1365-2958.1995.tb02386.x) / Mol. Microbiol. / The regulation of transcription by initiation host factor by Goosen N. (1995)
  19. Gu , B. , J. H. Lee , T. R. Hoover , D. Scholl , and B. T. Nixon . 1994 . Rhizobium meliloti DctD, a ~54-dependent transcriptional activator, may be negatively controlled by a subdomain in the C-terminal end of its two-component receiver module . Mol. Microbiol. 13 : 51 - 66 . (10.1111/j.1365-2958.1994.tb00401.x) / Mol. Microbiol. / Rhizobium meliloti DctD, a ~54-dependent transcriptional activator, may be negatively controlled by a subdomain in the C-terminal end of its two-component receiver module by Gu B. (1994)
  20. Holtel , A. , S. Marqués , I. Möhler , U. Jakubzik , and K. N. Timmis . 1994 . Carbon source-dependent inhibition of xyl operon expression of the Pseudomonas putida TOL plasmid . J. Bacteriol. 176 : 1773 - 1776 . (10.1128/JB.176.6.1773-1776.1994) / J. Bacteriol. / Carbon source-dependent inhibition of xyl operon expression of the Pseudomonas putida TOL plasmid by Holtel A. (1994)
  21. Hopper , S. , and A. Böck . 1995 . Effector-mediate stimulation of ATPase activity by the ~54-dependent transcriptional activator FHLA from Escherichia coli . J. Bacteriol. 177 : 2798 - 2803 . (10.1128/JB.177.10.2798-2803.1995) / J. Bacteriol. / Effector-mediate stimulation of ATPase activity by the ~54-dependent transcriptional activator FHLA from Escherichia coli by Hopper S. (1995)
  22. Hugouvieux-Cotte-Pattat N. T. Köhler M. Rekik and S. Harayama. Growth-phase-dependent expression of the Pseudomonas putida TOL plasmid pWW0 catabolic genes. J. Bacteriol. 172:6651-6660. (10.1128/JB.172.12.6651-6660.1990)
  23. Johnson , R. C. , C. A. Ball , D. Pfeffer , and M. I. Simon . 1988 . Isolation of the Hin recombinational enhancer binding protein . Proc. Natl. Acad. Sci. USA 85 : 3484 - 3488 . (10.1073/pnas.85.10.3484) / Proc. Natl. Acad. Sci. USA / Isolation of the Hin recombinational enhancer binding protein by Johnson R. C. (1988)
  24. Kaasen , I. , P. Falkenberg , O. B. Styrvold , and A. Strom . 1992 . Molecular cloning and physical mapping of the otsBA genes, which encode the osmoregulatory trehalose pathway of Escherichia coli: evidence that transcription is activated by KatF (AppR) . J. Bacteriol. 174 : 889 - 898 . (10.1128/jb.174.3.889-898.1992) / J. Bacteriol. / Molecular cloning and physical mapping of the otsBA genes, which encode the osmoregulatory trehalose pathway of Escherichia coli: evidence that transcription is activated by KatF (AppR) by Kaasen I. (1992)
  25. Kim , Y. , L. S. Watrud , and A. Matin . 1995 . A carbon starvation survival gene of Pseudomonas putida is regulated by ~54 . J. Bacteriol. 177 : 1850 - 1859 . (10.1128/jb.177.7.1850-1859.1995) / J. Bacteriol. / A carbon starvation survival gene of Pseudomonas putida is regulated by ~54 by Kim Y. (1995)
  26. Lange , R. , and R. Hengge-Aronis . 1991 . Growth phase-regulated expression of bolA and morphology of stationery-phase Escherichia coli cells are controlled by the novel sigma factor ~s . J. Bacteriol. 173 : 4474 - 4481 . (10.1128/JB.173.14.4474-4481.1991) / J. Bacteriol. / Growth phase-regulated expression of bolA and morphology of stationery-phase Escherichia coli cells are controlled by the novel sigma factor ~s by Lange R. (1991)
  27. Loewen , P. C. , and R. Hengge-Aronis . 1994 . The role of sigma factor ~s (KatF) in bacterial global regulation. Annu . Rev. Microbiol. 48 : 53 - 80 . (10.1146/annurev.mi.48.100194.000413) / Rev. Microbiol. / The role of sigma factor ~s (KatF) in bacterial global regulation. Annu by Loewen P. C. (1994)
  28. Marqués , S. , A. Holtel , K. N. Timmis , and J. L. Ramos . 1994 . Transcription induction kinetics from the promoters of the catabolic pathways of TOL plasmid pWW0 of Pseudomonas putida for metabolism of aromatics . J. Bacteriol. 176 : 2517 - 2524 . (10.1128/JB.176.9.2517-2524.1994) / J. Bacteriol. / Transcription induction kinetics from the promoters of the catabolic pathways of TOL plasmid pWW0 of Pseudomonas putida for metabolism of aromatics by Marqués S. (1994)
  29. Morett , E. , and L. Segovia . 1993 . The ~54 bacterial enhancer-binding protein family: mechanism of action and phylogenetic relationship of their functional domains . J. Bacteriol. 175 : 6067 - 6074 . (10.1128/JB.175.19.6067-6074.1993) / J. Bacteriol. / The ~54 bacterial enhancer-binding protein family: mechanism of action and phylogenetic relationship of their functional domains by Morett E. (1993)
  30. North , A. K. , K. E. Klose , K. M. Stedman , and S. Kustu . 1993 . Prokaryotic enhancer-binding proteins reflect eukaryotic-like modularity: the puzzle of nitrogen regulatory protein C . J. Bacteriol. 175 : 4267 - 4273 . (10.1128/JB.175.14.4267-4273.1993) / J. Bacteriol. / Prokaryotic enhancer-binding proteins reflect eukaryotic-like modularity: the puzzle of nitrogen regulatory protein C by North A. K. (1993)
  31. Nozaki , M. 1970 . Metapyrocatechase (Pseudomonas) . Methods Enzymol. 17 : 522 - 525 . (10.1016/0076-6879(71)17235-7) / Methods Enzymol. / Metapyrocatechase (Pseudomonas) by Nozaki M. (1970)
  32. Olsson , O. , C. Konez , and A. A. Szalay . 1988 . The use of the luxA gene of the bacterial Iuciferase operon as a reporter gene . Mol. Gen. Genet. 215 : 1 - 9 . (10.1007/BF00331295) / Mol. Gen. Genet. / The use of the luxA gene of the bacterial Iuciferase operon as a reporter gene by Olsson O. (1988)
  33. Pavel , H. , M. Forsman , and V. Shingler . 1994 . An aromatic effector specificity mutant of the transcriptional regulator DmpR overcomes the growth constraints of Pseudomonas sp. strain CF600 on para-substituted methylphenols . J. Bacteriol. 176 : 7550 - 7557 . (10.1128/JB.176.24.7550-7557.1994) / J. Bacteriol. / An aromatic effector specificity mutant of the transcriptional regulator DmpR overcomes the growth constraints of Pseudomonas sp. strain CF600 on para-substituted methylphenols by Pavel H. (1994)
  34. Pérez-Martin , J. , F. Rojo , and V. de Lorenzo . 1994 . Promoters responsive to DNA bending: a common theme in prokaryotic gene expression . Microbiol. Rev. 58 : 268 - 290 . (10.1128/MR.58.2.268-290.1994) / Microbiol. Rev. / Promoters responsive to DNA bending: a common theme in prokaryotic gene expression by Pérez-Martin J. (1994)
  35. Powlowski , J. , and V. Shingler . 1994 . Genetics and biochemistry of phenol degradation by Pseudomonas sp. strain CF600 . Biodegradation 5 : 1 - 18 . (10.1007/BF00696461) / Biodegradation / Genetics and biochemistry of phenol degradation by Pseudomonas sp. strain CF600 by Powlowski J. (1994)
  36. Rouviere , P. E. , A. De Las Penas , J. Mecsas , C. Z. Lu , K. E. Rudd , and C. A. Gross . 1995 . rpoE, the gene encoding the second heat-shock sigma factor, sigma E, in Escherichia coli . EMBO J. 14 : 1032 - 1042 . (10.1002/j.1460-2075.1995.tb07084.x) / EMBO J. / rpoE, the gene encoding the second heat-shock sigma factor, sigma E, in Escherichia coli by Rouviere P. E. (1995)
  37. Sambrook J. E. F. Fritsch and T. Maniatis. 1989. Molecular cloning: a laboratory manual 2nd ed. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  38. Shingler , V. 1996 . Signal sensing by ~54-dependent regulators: derepression as a control mechanism . Mol. Microbiol. 19 : 409 - 416 . (10.1046/j.1365-2958.1996.388920.x) / Mol. Microbiol. / Signal sensing by ~54-dependent regulators: derepression as a control mechanism by Shingler V. (1996)
  39. Shingler , V. , M. Bartilson , and T. Moore . 1993 . Cloning and nucleotide sequence of the positive regulator, DmpR, of the phenol catabolic pathway of pVI150: a member of the NtrC family of transcriptional activators . J. Bacteriol. 175 : 1596 - 1604 . (10.1128/jb.175.6.1596-1604.1993) / J. Bacteriol. / Cloning and nucleotide sequence of the positive regulator, DmpR, of the phenol catabolic pathway of pVI150: a member of the NtrC family of transcriptional activators by Shingler V. (1993)
  40. Shingler , V. , F. C. H. Franklin , M. Tsuda D. Holroyd , and M. Bagdasarian . 1989 . Molecular analysis of a plasmid encoded phenol hydroxylase of Pseudomonas CF600 . J. Gen. Microbiol. 135 : 1083 - 1092 . / J. Gen. Microbiol. / Molecular analysis of a plasmid encoded phenol hydroxylase of Pseudomonas CF600 by Shingler V. (1989)
  41. Shingler , V. , and T. Moore . 1994 . Sensing of aromatic compounds by the DmpR transcriptional activator of phenol catabolizing Pseudomonas sp. strain CF600 . J. Bacteriol. 176 : 1555 - 1560 . (10.1128/JB.176.6.1555-1560.1994) / J. Bacteriol. / Sensing of aromatic compounds by the DmpR transcriptional activator of phenol catabolizing Pseudomonas sp. strain CF600 by Shingler V. (1994)
  42. Shingler , V. , and H. Pavel . 1995 . Direct regulation of the ATPase activity of the transcriptional activator DmpR by aromatic compounds . Mol. Microbiol. 17 : 505 - 513 . (10.1111/j.1365-2958.1995.mmi_17030505.x) / Mol. Microbiol. / Direct regulation of the ATPase activity of the transcriptional activator DmpR by aromatic compounds by Shingler V. (1995)
  43. Shingler , V. , J. Powlowski , and U. Marklund . 1992 . Nucleotide sequence and functional analysis of the complete phenol/3,4-dimethylphenol catabolic pathway of Pseudomonas sp. strain CF600 . J. Bacteriol. 174 : 711 - 724 . (10.1128/jb.174.3.711-724.1992) / J. Bacteriol. / Nucleotide sequence and functional analysis of the complete phenol/3,4-dimethylphenol catabolic pathway of Pseudomonas sp. strain CF600 by Shingler V. (1992)
  44. Silhavy T. J. M. L. Berman and L. W. Enquist. 1984. Experiments with gene fusions. Cold Spring Harbor Laboratory Cold Spring Harbor N.Y.
  45. Weiss , D. S. , J. Batut , K. E. Klose , J. Keener , and S. Kustu . 1991 . The phosphorylated form of enhancer-binding protein NTRC has an ATPase activity that is essential for activation of transcription . Cell 67 : 155 - 167 . (10.1016/0092-8674(91)90579-N) / Cell / The phosphorylated form of enhancer-binding protein NTRC has an ATPase activity that is essential for activation of transcription by Weiss D. S. (1991)
  46. Zambrano , M. M. , D. A. Siegel , M. Almirón , A. Tormo , and R. Kolter . 1993 . Microbial competition: Escherichia coli mutants that take over stationary phase cultures . Science 259 : 1757 - 1760 . (10.1126/science.7681219) / Science / Microbial competition: Escherichia coli mutants that take over stationary phase cultures by Zambrano M. M. (1993)
Dates
Type When
Created 8 years, 9 months ago (Nov. 29, 2016, 12:35 p.m.)
Deposited 4 years, 1 month ago (July 29, 2021, 1:57 p.m.)
Indexed 3 months ago (June 4, 2025, 5:27 p.m.)
Issued 29 years, 2 months ago (July 1, 1996)
Published 29 years, 2 months ago (July 1, 1996)
Published Print 29 years, 2 months ago (July 1, 1996)
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@article{Sze_1996, title={Growth phase-dependent transcription of the sigma(54)-dependent Po promoter controlling the Pseudomonas-derived (methyl)phenol dmp operon of pVI150}, volume={178}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.178.13.3727-3735.1996}, DOI={10.1128/jb.178.13.3727-3735.1996}, number={13}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Sze, C C and Moore, T and Shingler, V}, year={1996}, month=jul, pages={3727–3735} }