Stochasticity of TOL plasmid catabolic promoters sets a bimodal expression regime in Pseudomonas putida mt-2 exposed to m-xylene

Molecular Microbiology

Volumn 86, Issue 1, 2012, Pages 199-211

  Silva Rocha, Rafael ^a   de Lorenzo, Víctor ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

REGULATOR PROTEIN; UNCLASSIFIED DRUG; XYLR PROTEIN; XYLS PROTEIN;

ARTICLE; BACTERIAL CELL; CONTROLLED STUDY; GENE EXPRESSION; GENE REGULATORY NETWORK; NONHUMAN; PLASMID; PLASMID TOL; PM PROMOTER; PR PROMOTER; PRIORITY JOURNAL; PROMOTER REGION; PS PROMOTER; PSEUDOMONAS PUTIDA; PU PROMOTER; REGULATOR GENE; XYLR GENE;

ARTIFICIAL GENE FUSION; BETA-GALACTOSIDASE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; METABOLIC NETWORKS AND PATHWAYS; PLASMIDS; PROMOTER REGIONS, GENETIC; PSEUDOMONAS PUTIDA; TRANSCRIPTIONAL ACTIVATION; XYLENES;

BACTERIA (MICROORGANISMS); PSEUDOMONAS PUTIDA;

EID: 84867080098     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08184.x     Document Type: Article

References (60)

1. Abril, M.A., Michan, C., Timmis, K.N., and Ramos, J.L. (1989) Regulator and enzyme specificities of the TOL plasmid-encoded upper pathway for degradation of aromatic hydrocarbons and expansion of the substrate range of the pathway. J Bacteriol 171: 6782-6790.
2. Ali Azam, T., Iwata, A., Nishimura, A., Ueda, S., and Ishihama, A. (1999) Growth phase-dependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 181: 6361-6370.
3. Aranda-Olmedo, I., Ramos, J.L., and Marques, S. (2005) Integration of signals through Crc and PtsN in catabolite repression of Pseudomonas putida TOL plasmid pWW0. Appl Environ Microbiol 71: 4191-4198.
4. Arkin, A., Ross, J., and McAdams, H.H. (1998) Stochastic kinetic analysis of developmental pathway bifurcation in phage lambda-infected Escherichia coli cells. Genetics 149: 1633-1648.
5. Becskei, A., and Serrano, L. (2000) Engineering stability in gene networks by autoregulation. Nature 405: 590-593.
6. Bertoni, G., Perez-Martin, J., and de Lorenzo, V. (1997) Genetic evidence of separate repressor and activator activities of the XylR regulator of the TOL plasmid, pWW0, of Pseudomonas putida. Mol Microbiol 23: 1221-1227.
7. 54-RNA polymerase to the Pu promoter of Pseudomonas putida: role of IHF and αCTD. EMBO J 17: 5120-5128.
8. 70 promoters at the divergent Pr/Ps region of the TOL plasmid. Mol Microbiol 27: 651-659.
9. Boyer, H.W., and Roulland-Dussoix, D. (1969) A complementation analysis of the restriction and modification of DNA in Escherichia coli. J Mol Biol 41: 459-472.
10. Cases, I., and de Lorenzo, V. (2005) Promoters in the environment: transcriptional regulation in its natural context. Nat Rev Microbiol 3: 105-118.
11. 54-dependent Pu promoter of the TOL plasmid. J Biol Chem 274: 15562-15568.
12. 32. J Biol Chem 280: 41315-41323.
13. Dublanche, Y., Michalodimitrakis, K., Kummerer, N., Foglierini, M., and Serrano, L. (2006) Noise in transcription negative feedback loops: simulation and experimental analysis. Mol Syst Biol 2: 41.
14. Eldar, A., and Elowitz, M.B. (2010) Functional roles for noise in genetic circuits. Nature 467: 167-173.
15. Elowitz, M.B., and Leibler, S. (2000) A synthetic oscillatory network of transcriptional regulators. Nature 403: 335-338.
16. Elowitz, M.B., Levine, A.J., Siggia, E.D., and Swain, P.S. (2002) Stochastic gene expression in a single cell. Science 297: 1183-1186.
17. Fraile, S., Roncal, F., Fernandez, L.A., and de Lorenzo, V. (2001) Monitoring intracellular levels of XylR in Pseudomonas putida with a single-chain antibody specific for aromatic-responsive enhancer-binding proteins. J Bacteriol 183: 5571-5579.
18. Franklin, F.C., Bagdasarian, M., Bagdasarian, M.M., and Timmis, K.N. (1981) Molecular and functional analysis of the TOL plasmid pWWO from Pseudomonas putida and cloning of genes for the entire regulated aromatic ring meta cleavage pathway. Proc Natl Acad Sci USA 78: 7458-7462.
19. Gonzalez-Perez, M.M., Ramos, J.L., and Marques, S. (2004) Cellular XylS levels are a function of transcription of xylS from two independent promoters and the differential efficiency of translation of the two mRNAs. J Bacteriol 186: 1898-1901.
20. Herrero, M., de Lorenzo, V., and Timmis, K.N. (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in gram-negative bacteria. J Bacteriol 172: 6557-6567.
21. Holtel, A., Timmis, K.N., and Ramos, J.L. (1992) Upstream binding sequences of the XylR activator protein and integration host factor in the xylS gene promoter region of the Pseudomonas TOL plasmid. Nucleic Acids Res 20: 1755-1762.
22. Holtel, A., Marques, S., Mohler, I., Jakubzik, U., and Timmis, K.N. (1994) Carbon source-dependent inhibition of xyl operon expression of the Pseudomonas putida TOL plasmid. J Bacteriol 176: 1773-1776.
23. Inouye, S., Nakazawa, A., and Nakazawa, T. (1983) Molecular cloning of regulatory gene xylR and operator-promoter regions of the xylABC and xylDEGF operons of the TOL plasmid. J Bacteriol 155: 1192-1199.
24. Inouye, S., Nakazawa, A., and Nakazawa, T. (1987) Expression of the regulatory gene xylS on the TOL plasmid is positively controlled by the xylR gene product. Proc Natl Acad Sci USA 84: 5182-5186.
25. Jurado, P., Fernandez, L.A., and de Lorenzo, V. (2003) Sigma 54 levels and physiological control of the Pseudomonas putida Pu promoter. J Bacteriol 185: 3379-3383.
26. Keen, N.T., Tamaki, S., Kobayashi, D., and Trollinger, D. (1988) Improved broad-host-range plasmids for DNA cloning in gram-negative bacteria. Gene 70: 191-197.
27. Kessler, B., de Lorenzo, V., and Timmis, K.N. (1992) A general system to integrate lacZ fusions into the chromosomes of gram-negative eubacteria: regulation of the Pm promoter of the TOL plasmid studied with all controlling elements in monocopy. Mol Gen Genet 233: 293-301.
28. Kessler, B., Marques, S., Kohler, T., Ramos, J.L., Timmis, K.N., and de Lorenzo, V. (1994) Cross talk between catabolic pathways in Pseudomonas putida: XylS-dependent and -independent activation of the TOL meta operon requires the same cis-acting sequences within the Pm promoter. J Bacteriol 176: 5578-5582.
29. de Lorenzo, V., and Timmis, K.N. (1994) Analysis and construction of stable phenotypes in gram-negative bacteria with Tn5- and Tn10-derived minitransposons. Methods Enzymol 235: 386-405.
30. de Lorenzo, V., Herrero, M., Metzke, M., and Timmis, K.N. (1991) An upstream XylR- and IHF-induced nucleoprotein complex regulates the sigma 54-dependent Pu promoter of TOL plasmid. EMBO J 10: 1159-1167.
31. Maamar, H., and Dubnau, D. (2005) Bistability in the Bacillus subtilis K-state (competence) system requires a positive feedback loop. Mol Microbiol 56: 615-624.
32. McAdams, H.H., and Arkin, A. (1997) Stochastic mechanisms in gene expression. Proc Natl Acad Sci USA 94: 814-819.
33. 54-RNA polymerase to the Pu promoter of Pseudomonas putida through integration host factor-mediated positioning switch of alpha subunit carboxyl-terminal domain on an UP-like element. J Biol Chem 278: 27695-27702.
34. Marques, S., Holtel, A., Timmis, K.N., and Ramos, J.L. (1994) Transcriptional 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.
35. Marques, S., Gallegos, M.T., Manzanera, M., Holtel, A., Timmis, K.N., and Ramos, J.L. (1998) Activation and repression of transcription at the double tandem divergent promoters for the xylR and xylS genes of the TOL plasmid of Pseudomonas putida. J Bacteriol 180: 2889-2894.
36. Mermod, N., Ramos, J.L., Bairoch, A., and Timmis, K.N. (1987) The xylS gene positive regulator of TOL plasmid pWWO: identification, sequence analysis and overproduction leading to constitutive expression of meta cleavage operon. Mol Gen Genet 207: 349-354.
37. Miller, W.G., and Lindow, S.E. (1997) An improved GFP cloning cassette designed for prokaryotic transcriptional fusions. Gene 191: 149-153.
38. Moreno, R., Fonseca, P., and Rojo, F. (2010) The Crc global regulator inhibits the Pseudomonas putida pWW0 toluene/xylene assimilation pathway by repressing the translation of regulatory and structural genes. J Biol Chem 285: 24412-24419.
39. Ozbudak, E.M., Thattai, M., Kurtser, I., Grossman, A.D., and van Oudenaarden, A. (2002) Regulation of noise in the expression of a single gene. Nat Genet 31: 69-73.
40. Pedraza, J.M., and van Oudenaarden, A. (2005) Noise propagation in gene networks. Science 307: 1965-1969.
41. Perez-Martin, J., and de Lorenzo, V. (1995) The sigma 54-dependent promoter Ps of the TOL plasmid of Pseudomonas putida requires HU for transcriptional activation in vivo by XylR. J Bacteriol 177: 3758-3763.
42. Perez-Martin, J., Timmis, K.N., and de Lorenzo, V. (1994) Co-regulation by bent DNA. Functional substitutions of the integration host factor site at sigma 54-dependent promoter Pu of the upper-TOL operon by intrinsically curved sequences. J Biol Chem 269: 22657-22662.
43. Ramos, J.L., Marques, S., and Timmis, K.N. (1997) Transcriptional control of the Pseudomonas TOL plasmid catabolic operons is achieved through an interplay of host factors and plasmid-encoded regulators. Annu Rev Microbiol 51: 341-373.
44. Rescalli, E., Saini, S., Bartocci, C., Rychlewski, L., de Lorenzo, V., and Bertoni, G. (2004) Novel physiological modulation of the Pu promoter of TOL plasmid: negative regulatory role of the TurA protein of Pseudomonas putida in the response to suboptimal growth temperatures. J Biol Chem 279: 7777-7784.
45. Ruiz-Manzano, A., Yuste, L., and Rojo, F. (2005) Levels and activity of the Pseudomonas putida global regulatory protein Crc vary according to growth conditions. J Bacteriol 187: 3678-3686.
46. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor.
47. Siegele, D.A., and Hu, J.C. (1997) Gene expression from plasmids containing the araBAD promoter at subsaturating inducer concentrations represents mixed populations. Proc Natl Acad Sci USA 94: 8168-8172.
48. Silva-Rocha, R., and de Lorenzo, V. (2010) Noise and robustness in prokaryotic regulatory networks. Annu Rev Microbiol 64: 257-275.
49. Silva-Rocha, R., and de Lorenzo, V. (2011) A composite feed-forward loop I4-FFL involving IHF and Crc stabilizes expression of the XylR regulator of Pseudomonas putida mt-2 from growth phase perturbations. Mol BioSyst 7: 2982-2990.
50. Silva-Rocha, R., and de Lorenzo, V. (2012) A GFP-lacZ bicistronic reporter system for promoter analysis in environmental Gram-negative bacteria. PLoS ONE 7: e34675.
51. Silva-Rocha, R., Tamames, J., dos Santos, V.M., and de Lorenzo, V. (2011a) The logicome of environmental bacteria: merging catabolic and regulatory events with Boolean formalisms. Environ Microbiol 13: 2389-2402.
52. Silva-Rocha, R., de Jong, H., Tamames, J., and de Lorenzo, V. (2011b) The logic layout of the TOL network of Pseudomonas putida pWW0 plasmid stems from a metabolic amplifier motif (MAM) that optimizes biodegradation of m-xylene. BMC Syst Biol 5: 191.
53. Silva-Rocha, R., Pérez-Pantoja, D., and de Lorenzo, V. (2012) Decoding the genetic networks of environmental bacteria: regulatory moonlighting of the TOL system of Pseudomonas putida mt-2. ISME J doi:10.1038/ismej.2012.98.
54. Spooner, R.A., Lindsay, K., and Franklin, F.C. (1986) Genetic, functional and sequence analysis of the xylR and xylS regulatory genes of the TOL plasmid pWW0. J Gen Microbiol 132: 1347-1358.
55. Sterberg, S., del Peso-Santos, T., and Shingler, V. (2011) Regulation of alternative sigma factor use. Annu Rev Microbiol 65: 37-55.
56. Tintut, Y., Wang, J.T., and Gralla, J.D. (1995) A novel bacterial transcription cycle involving sigma 54. Genes Dev 9: 2305-2313.
57. Tropel, D., and van der Meer, J.R. (2004) Bacterial transcriptional regulators for degradation pathways of aromatic compounds. Microbiol Mol Biol Rev 68: 474-500.
58. 54Pu promoter reveals that integration host factor couples transcriptional activity to growth phase. J Biol Chem 277: 2169-2175.
59. Williams, P.A., and Murray, K. (1974) Metabolism of benzoate and the methylbenzoates by Pseudomonas putida (arvilla) mt-2: evidence for the existence of a TOL plasmid. J Bacteriol 120: 416-423.
60. Worsey, M.J., and Williams, P.A. (1975) Metabolism of toluene and xylenes by Pseudomonas putida (arvilla) mt-2: evidence for a new function of the TOL plasmid. J Bacteriol 124: 7-13.