The RpoT regulon of Pseudomonas putida DOT-T1E and its role in stress endurance against solvents

Journal of Bacteriology

Volumn 189, Issue 1, 2007, Pages 207-219

  Duque, Estrella ^a   Rodríguez Herva, José Juan ^a   De La Torre, Jesús ^a   Domínguez Cuevas, Patricia ^a   Muñoz Rojas, Jesús ^a,b   Ramos, Juan Luis ^a  

^a CSIC   (Spain)

^b Instituto de Ciencias   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; BACTERIAL PROTEIN; BENZOIC ACID; DODECYL SULFATE SODIUM; EXTRACYTOPLASMIC SIGMA FACTOR; GENE PRODUCT; HYDROGEN PEROXIDE; MEMBRANE PROTEIN; ORGANIC SOLVENT; PARAQUAT; PERIPLASMIC PROTEIN; SODIUM CHLORIDE; TOLUENE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM MUTANT; CELL MEMBRANE; CHEMICAL STRESS; CISTRON; CONTROLLED STUDY; CYTOPLASM; DNA FLANKING REGION; DOWN REGULATION; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; HEAT; HOMOLOGOUS RECOMBINATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OPERON; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PSEUDOMONAS PUTIDA; REGULON; RNA TRANSLATION; RPOT GENE; UPREGULATION; WILD TYPE;

BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MEMBRANE PROTEINS; OPEN READING FRAMES; PERIPLASMIC BINDING PROTEINS; PSEUDOMONAS PUTIDA; REGULON; SIGMA FACTOR; TOLUENE;

PSEUDOMONAS PUTIDA;

EID: 33845964750     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00950-06     Document Type: Article

References (68)

1. E during initiation, adaptation, and shut off of the extracytoplasmic heat shock response in Escherichia coli. J. Bacteriol. 185:2512-2519.
2. 2. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
3. B regulon. J. Bacteriol. 186:4085-4089.
4. Brazma, A., P. Hingamp, J. Quackenbush, G. Sherlock, P. Spellman, C. Stoeckert, J. Aach, W. Ansorge, C. A. Ball, H. C. Causton, T. Gaasterland, P. Glenisson, F. C. P. Holstege, I. F. Kim, V. Markowitz, J. C. Matese, H. Parkinson, A. Robinson, U. Sarkans, S. Schulze-Kremer, J. Stewart, R. Taylor, J. Vilo, and M. Vingron. 2001. Minimum information about a microarray experiment (M1AME)-towards standards for microarray data. Nat. Genet. 29:365-371.
5. B activation under environmental and energy stress conditions in Listeria monocytogenes. Appl. Environ. Microbiol. 72:5197-5203.
6. E RNA polymerase. J. Biol. Chem. 275:33898-33904.
7. E regulon. J. Biol. Chem. 276:20866-20875.
8. De Smet, M. J., J. Kingman, and B. Witholt. 1978. The effect of toluene on the structure and permeability of the outer and cytoplasmic membranes of Escherichia coli. Biochim. Biophys. Acta 506:64-80.
9. DeVries, C. A., and D. E. Ohman. 1994. Mucoid-to-nonmucoid conversion in alginate-producing Pseudomonas aeruginosa often results from spontaneous mutations in algT, encoding a putative alternate sigma factor, and shows evidence for autoregulation. J. Bacteriol. 176:6677-6687.
10. Dinamarca, M. A., A. Ruíz-Manzano, and F. Rojo. 2002. Inactivation of cytochrome o ubiquinol oxidase relieves catabolic repression of the Pseudomonas putida GPo1 alkane degradation pathway. J. Bacteriol. 184:3785-3793.
11. Domínguez-Cuevas, P., J. E. González-Pastor, S. Marqués, J. L. Ramos, and V. de Lorenzo. 2006. Transcriptional tradeoff between metabolic and stress-response programs in Pseudomonas putida KT2440 cells exposed to toluene. J. Biol. Chem. 281:11981- 11991.
12. Duque, E., A. Segura, G. Mosqueda, and J. L. Ramos. 2001. Global and cognate regulators control the expression of the organic solvent efflux pumps TtgABC and TtgDEF of Pseudomonas putida. Mol. Microbiol. 39:1100-1106.
13. Egler, M., C. Grosse, G. Grass, and D. H. Nies. 2005. Role of the extracytoplasmic function protein family sigma factor RpoE in metal resistance of Escherichia coli. J. Bacteriol. 187:2297-2307.
14. Godoy, P., M. I. Ramos-González, and J. L. Ramos. 2004. Pseudomonas putida mutants in the exbBexbDtonB gene cluster are hypersensitive to environmental and chemical stressors. Environ. Microbiol. 6:605-610.
15. Grosse, C., G. Grass, A. Anton, S. Franke, A. Navarrete Santos, B. Lawley, N. L. Brown, and D. H. Nies. 1999. Transcriptional organization of the czc heavy metal homoeostasis determinant from Alcaligenes eutrophus. J. Bacteriol. 181:2385-2393.
16. Guazzaroni, M. E., T. Krell, A. Felipe, R. Ruíz, C. Meng, X. Zhang, M. T. Gallegos, and J. L. Ramos. 2005. The multidrug efflux regulator TtgV recognizes a wide range of structurally different effectors in solution and complexed with target DNA. J. Biol. Chem. 280:20887-20893.
17. Helmann, J. D. 2002. The extracytoplasmic function (ECF) sigma factors. Adv. Microb. Physiol. 46:47-110.
18. Herrero, M., V. de Lorenzo, and K. N. Timmis. 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.
19. Heusipp, G., M. A. Schmidt, and V. L. Miller. 2003. Identification of rpoE and nadB as host responsive elements of Yersinia enterocolitica. FEMS Microbiol. Lett. 226:291-298.
20. Hiratsu, N., M. Amemura, H. Nashimoto, H. Shinawaga, and K. Makino. 1995. The rpoE gene of Escherichia coli, which encodes sigma E, is essential for bacterial growth at high temperature. J. Bacteriol. 177:2918-2922.
21. Hughes, K. T., and K. Mathee. 1998. The anti-sigma factors. Annu. Rev. Microbiol. 52:231-286.
22. E, is critically important for the virulence of Salmonella typhimurium. Infect. Immun. 67:1560-1568.
23. Kaniga, K., I. Delar, and G. R. Cornelis. 1991. A wide-host-range suicide vector for improving reverse genetics in Gram-negative bacteria: inactivation of the blaA gene of Yersinia enterocolitica. Gene 109:137-141.
24. Klein, G., C. Dartigalongue, and S. Raina. 2003. Phosphorylation-mediated regulation of heat shock response in Escherichia coli. Mol. Microbiol. 48: 269-285.
25. Kovach, M. E., P. H. Elzer, D. S. Hill, G. T. Robertson, M. A. Farris, R. M. Roop II, and K. M. Peterson. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
26. E plays an important role in intestinal survival and virulence in Vibrio cholerae. Infect. Immun. 70:5355-5362.
27. Krogh, A., B. Larsson, G. von Heijne, and E. L. L. Sonnhammer. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580.
28. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
29. B by an anti- and an anti-anti-sigma factor in Streptomyces coelicolor in response to osmotic stress. J. Bacteriol. 186:8490-8498.
30. Llamas, M. A., J. L. Ramos, and J. J. Rodríguez-Herva. 2000. Mutations in each of the tol genes of Pseudomonas putida reveal that they are critical for maintenance of outer membrane stability. J. Bacteriol. 182:4764-4772.
31. Lonetto, M. A., K. L. Brown, K. E. Rudd, and M. J. Buttner. 1994. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial σ factors involved in the regulation of extracytoplasmic functions. Proc. Natl. Acad. Sci. USA 91:7573-7577.
32. E role in global gene expression and survival in macrophages. Mol. Microbiol. 41:423-437.
33. Manoil, C., J. J. Mekalanos, and J. Beckwith. 1990. Alkaline phosphatase fusions: sensors of subcellular location. J. Bacteriol. 172:515-518.
34. Marck, C. 1988. 'DNA Strider': a 'C' program for the fast analysis of DNA and protein sequences on the Apple Macintosh family of computers. Nucleic Acids Res. 16:1829-1836.
35. Martínez-Bueno, M., R. Tobes, M. Rey, and J. L. Ramos. 2002. Detection of multiple extractoplasmatic function (ECF) sigma factors in the genome of Pseudomonas putida KT2440 and their counterparts in Pseudomonas aeruginosa PAO1. Environ. Microbiol. 4:842-855.
36. 22 for expression of the alginate regulon in Pseudomonas aeruginosa and localization of its antagonist proteins MucA and MucB (AlgN). J. Bacteriol. 179:3711-3720.
37. Ménard, R., P. J. Sansonetti, and C. Parsot. 1993. Nonpolar mutagenesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J. Bacteriol. 175:5899-5906.
38. M, an extracytoplasmic function sigma factor, and is conferred by YqjL and BcrC. J. Bacteriol. 187:2948-2956.
39. Mosqueda, G., and J. L. Ramos. 2000. A set of genes encoding a second toluene efflux system in Pseudomonas putida DOT-T1E is linked to the tod genes for toluene metabolism. J. Bacteriol. 182:937-943.
40. Muñoz-Rojas, J., P. Bernal, E. Duque, P. Godoy, A. Segura, and J. L. Ramos. 2006. Involvement of cyclopropane fatty acids in the response of Pseudomonas putida KT2440 to freeze-drying. Appl. Environ. Microbiol. 72:472-477.
41. Nelson, K. E., C. Weinel, I. T. Paulsen, R. J. Dodson, H. Hilbert, V. A. Martins dos Santos, et al. 2002. Complete genome sequence and comparative analysis of the metabolically versatile Pseudomonas putida KT2440. Environ. Microbiol. 4:799-808.
42. 24 heat shock sigma factor of Escherichia coli. EMBO J. 14:1043-1055.
43. Raivio, T. L. 2005. Envelope stress responses and gram-negative bacterial pathogenesis. Mol. Microbiol. 56:1119-1128.
44. Raivio, T. L., and T. J. Silhavy. 2001. Periplasmic stress and ECF sigma factors. Annu. Rev. Microbiol. 55:591-624.
45. Ramos, J. L., E. Duque, M. T. Gallegos, P. Godoy, M. I. Ramos-González, A. Rojas, W. Terán, and A. Segura. 2002. Mechanisms of solvent tolerance in gram-negative bacteria. Annu. Rev. Microbiol. 56:743-768.
46. Ramos, J. L., E. Duque, P. Godoy, and A. Segura. 1998. Efflux pumps involved in toluene tolerance in Pseudomonas putida DOT-T1E. J. Bacteriol. 180:3323-3329.
47. Ramos, J. L., E. Duque, M. J. Huertas, and A. Haïdour. 1995. Isolation and expansion of the catabolic potential of a Pseudomonas putida strain able to grow in the presence of high concentrations of aromatic hydrocarbons. J. Bacteriol. 177:3911-3916.
48. Ramos, J. L., M. T. Gallegos, S. Marqués, M. I. Ramos-González, M. Espinosa-Urgel, and A. Segura. 2001. Responses of gram-negative bacteria to certain environmental stressors. Curr. Opinin. Microbiol. 4:166-171.
49. Ramos-González, M. I., E. Duque, and J. L. Ramos. 1991. Conjugational transfer of recombinant DNA in cultures and in soils: host range of Pseudomonas putida TOL plasmids. Appl. Environ. Microbiol. 57:3020-3027.
50. Rodríguez-Herva, J. J., and J. L. Ramos. 1996. Characterization of an OprL null mutant of Pseudomonas putida. J. Bacteriol. 178:5836-5840.
51. Rojas, A., E. Duque, G. Mosqueda, G. Golden, A. Hurtado, J. L. Ramos, and A. Segura. 2001. Three efflux pumps are required to provide efficient tolerance to toluene in Pseudomonas putida DOT-T1E. J. Bacteriol. 183:3967-3973.
52. Rojas, A., A. Segura, M. E. Guazzaroni, W. Teran, A. Hurtado, M. T. Gallegos, and J. L. Ramos. 2003. In vivo and in vitro evidence that TtgV is the specific regulator of the TtgGHI multidrug and solvent efflux pump of Pseudomonas putida. J. Bacteriol. 185:4755-4763.
53. 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.
54. Schurr, M. J., H. Yu, J. M. Martínez-Salazar, J. C. Boucher, and V. Deretic. 1995. Control of AlgU, a member of the sigma E-like family of stress sigma factors, by the negative regulators MucA and MucB and Pseudomonas aeruginosa conversion to mucoidy in cystic fibrosis. J. Bacteriol. 178:4997-5004.
55. Segura, A., A. Hurtado, E. Duque, and, J. L. Ramos. 2004. Transcriptional phase variation at the flhB gene of Pseudomonas putida DOT-T1E is involved in response to environmental changes and suggests the participation of the flagellar export system in solvent tolerance. J. Bacteriol. 186:1905-1909.
56. Sikkema, J., J. A. M. de Bont, and B. Poolman. 1994. Interactions of cyclic hydrocarbons with biological membranes. J. Biol. Chem. 269:8022-8028.
57. Silo-Suh, L., S.-J. Suh, P. V. Phibbs, and D. E. Ohman. 2005. Adaptations of Pseudomonas aeruginosa to the cystic fibrosis lung environment can include deregulation of zwf, encoding glucose-6-phosphate dehydrogenase. J. Bacteriol. 187:7561-7568.
58. Spaink, H. P., R. J. H. Oker, C. A. Wijffelman, E. Pees, and B. J. J. Lugtenberg. 1987. Promoters in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRJ151. Plant Mol. Biol. 9:27-39.
59. Strom, M. S., and S. Lory. 1987. Mapping of export signals of Pseudomonas aeruginosa pilin with alkaline phosphatase fusions. J. Bacteriol. 169:3181-3188.
60. Tart, A. H., C. Matthew, C. Wolfgang, and Daniel J. Wozniak. 2005. The alternative sigma factor AlgT represses Pseudomonas aeruginosa flagellum biosynthesis by inhibiting expression of fleQ. J. Bacteriol. 187:7955-7962.
61. Terán, W., A. Felipe, A. Segura, A. Rojas, J. L. Ramos, and M. T. Gallegos. 2003. Antibiotic-dependent induction of Pseudomonas putida DOT-T1E TtgABC efflux pump is mediated by the drug binding repressor TtgR. Antimicrob. Agents Chemother. 47:3067-3072.
62. Terán, W., T. Krell, J. L. Ramos, and M. T. Gallegos. 2006. Effector-repressor interactions. Binding of a single effector molecule to the operator bound TtgR homodimer mediates derepression. J. Biol. Chem. 281:7102-7109.
63. Wu, W., H. Badrane, S. Arora, H. V. Baker, and S. Jin. 2004. MucA-mediated coordination of type III secretion and alginate synthesis in Pseudomonas aeruginosa. J. Bacteriol. 186:7575-7585.
64. Yamamoto, K., and, A. Ishihama. 2005. Transcriptional response of Escherichia coli to external zinc. J. Bacteriol. 187:6333-6340.
65. Yang, Y. H., S. Dudoit, P. Luu, D. M. Lin, V. Peng, J. Ngai, and T. P. Speed. 2002. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30:e15.
66. Young, J. C., and F. V. Hartl. 2003. A stress sensor for the bacterial periplasm. Cell 113:1-2.
67. E). Infect. Immun. 64:2774-2781.
68. Yuste, L., A. B. Hervás, I. Canosa, R. Tobes, J. I. Jiménez, J. Nogales, M. M. Pérez-Pérez, E. Santero, E. Díaz, J. L. Ramos, V. de Lorenzo, and F. Rojo. 2006. Growth phase-dependent expression of the Pseudomonas putida KT2440 transcriptional machinery analysed with a genome-wide DNA microarray. Environ. Microbiol. 8:166-177.