Two small RNAs, CrcY and CrcZ, act in concert to sequester the Crc global regulator in Pseudomonas putida, modulating catabolite repression

Molecular Microbiology

Volumn 83, Issue 1, 2012, Pages 24-40

  Moreno, Renata ^a   Fonseca, Pilar ^a   Rojo, Fernando ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN CRC; PROTEIN CRCY; PROTEIN CRCZ; REPRESSOR PROTEIN; RNA; SIGMA FACTOR RPON; SMALL RNA; TRANSCRIPTOME; TRANSFER RNA; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL STRAIN; BINDING SITE; CARBON METABOLISM; CARBON SOURCE; CATABOLITE REPRESSION; COMPLEX FORMATION; DNA SEQUENCE; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS PUTIDA; PSEUDOMONAS SYRINGAE; TRANSCRIPTION INITIATION SITE;

BACTERIAL PROTEINS; BASE SEQUENCE; CATABOLITE REPRESSION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, REGULATOR; MOLECULAR SEQUENCE DATA; OPERON; PSEUDOMONAS PUTIDA; REPRESSOR PROTEINS; RNA, BACTERIAL; RNA, SMALL UNTRANSLATED;

PSEUDOMONAS AERUGINOSA; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS PUTIDA; PSEUDOMONAS SYRINGAE;

EID: 84155165433     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2011.07912.x     Document Type: Article

References (51)

1. Abdou, L., Chou, H.T., Haas, D., and Lu, C.D. (2011) Promoter recognition and activation by the global response regulator CbrB in Pseudomonas aeruginosa. J Bacteriol 193: 2784-2792.
2. Babitzke, P., and Romeo, T. (2007) CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 10: 156-163.
3. Bauchop, T., and Eldsen, S.R. (1960) The growth of microorganisms in relation to their energy supply. J Gen Microbiol 23: 457-569.
4. Bellavia, D., Sisino, G., Papadopoulos, G.L., Forte, G.I., and Barbieri, R. (2009) Mung bean nuclease mapping of RNAs 3′ end. Immun Ageing 6: 6.
5. Brencic, A., and Lory, S. (2009) Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol Microbiol 73: 612-632.
6. Browne, P., Barret, M., O'Gara, F., and Morrissey, J.P. (2010) Computational prediction of the Crc regulon identifies genus-wide and species-specific targets of catabolite repression control in Pseudomonas bacteria. BMC Microbiol 10: 300.
7. Cases, I., de Lorenzo, V., and Pérez-Martín, J. (1996) Involvement of sigma 54 in exponential silencing of the Pseudomonas putida TOL plasmid Pu promoter. Mol Microbiol 19: 7-17.
8. del Castillo, T., and Ramos, J.L. (2007) Simultaneous catabolite repression between glucose and toluene metabolism in Pseudomonas putida is channeled through different signaling pathways. J Bacteriol 189: 6602-6610.
9. Chavez, R.G., Alvarez, A.F., Romeo, T., and Georgellis, D. (2010) The physiological stimulus for the BarA sensor kinase. J Bacteriol 192: 2009-2012.
10. Dennis, J.J., and Zylstra, G.J. (1998) Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of Gram-negative bacterial genomes. Appl Environ Microbiol 64: 2710-2715.
11. Deutscher, J. (2008) The mechanisms of carbon catabolite repression in bacteria. Curr Opin Microbiol 11: 87-93.
12. Edwards, A.N., Patterson-Fortin, L.M., Vakulskas, C.A., Mercante, J.W., Potrykus, K., Vinella, D., etal. (2011) Circuitry linking the Csr and stringent response global regulatory systems. Mol Microbiol 80: 1561-1580.
13. Filiatrault, M.J., Stodghill, P.V., Bronstein, P.A., Moll, S., Lindeberg, M., Grills, G., etal. (2010) Transcriptome analysis of Pseudomonas syringae identifies new genes, noncoding RNAs, and antisense activity. J Bacteriol 192: 2359-2372.
14. Förster-Fromme, K., Hoschle, B., Mack, C., Bott, M., Armbruster, W., and Jendrossek, D. (2006) Identification of genes and proteins necessary for catabolism of acyclic terpenes and leucine/isovalerate in Pseudomonas aeruginosa. Appl Environ Microbiol 72: 4819-4828.
15. Frank, S., Klockgether, J., Hagendorf, P., Geffers, R., Schock, U., Pohl, T., etal. (2011) Pseudomonas putida KT2440 genome update by cDNA sequencing and microarray transcriptomics. Environ Microbiol 13: 1309-1326.
16. 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 Nat Acad Sci USA 78: 7458-7462.
17. Görke, B., and Stülke, J. (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6: 613-624.
18. Hester, K.L., Lehman, J., Najar, F., Song, L., Roe, B.A., MacGregor, C.H., etal. (2000) Crc is involved in catabolite repression control of the bkd operons of Pseudomonas putida and Pseudomonas aeruginosa. J Bacteriol 182: 1144-1149.
19. Kaniga, K., Delor, I., and Cornelis, G.R. (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.
20. Kay, E., Dubuis, C., and Haas, D. (2005) Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Proc Natl Acad Sci USA 102: 17136-17141.
21. Lapouge, K., Schubert, M., Allain, F.H., and Haas, D. (2008) Gac/Rsm signal transduction pathway of gamma-proteobacteria: from RNA recognition to regulation of social behaviour. Mol Microbiol 67: 241-253.
22. Li, W., and Lu, C.D. (2007) Regulation of carbon and nitrogen utilization by CbrAB and NtrBC two-component systems in Pseudomonas aeruginosa. J Bacteriol 189: 5413-5420.
23. Linares, J.F., Moreno, R., Fajardo, A., Martínez-Solano, L., Escalante, R., Rojo, F., and Martínez, J.L. (2010) The global regulator Crc modulates metabolism, susceptibility to antibiotics and virulence in Pseudomonas aeruginosa. Environ Microbiol 12: 3196-3212.
24. Liu, M.Y., Gui, G., Wei, B., Preston, J.F., 3rd, Oakford, L., Yuksel, U., etal. (1997) The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J Biol Chem 272: 17502-17510.
25. -ΔΔCt Method. Methods 25: 402-408.
26. de Lorenzo, V., Herrero, M., Jakubzik, U., and Timmis, K.N. (1990) Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in Gram-negative eubacteria. J Bacteriol 172: 6568-6572.
27. MacGregor, C.H., Wolff, J.A., Arora, S.K., and 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.
28. Maxam, A.M., and Gilbert, W. (1980) Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol 65: 499-560.
29. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
30. Moll, S., Schneider, D.J., Stodghill, P., Myers, C.R., Cartinhour, S.W., and Filiatrault, M.J. (2010) Construction of an rsmX co-variance model and identification of five rsmX non-coding RNAs in Pseudomonas syringae pv. tomato DC3000. RNA Biol 7: 508-516.
31. Morales, G., Linares, J.F., Beloso, A., Albar, J.P., Martínez, J.L., and 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.
32. Morales, G., Ugidos, A., and 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.
33. Moreno, R., and Rojo, F. (2008) The target for the Pseudomonas putida Crc global regulator in the benzoate degradation pathway is the BenR transcriptional regulator. J Bacteriol 190: 1539-1545.
34. Moreno, R., Ruiz-Manzano, A., Yuste, L., and 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.
35. Moreno, R., Martínez-Gomariz, M., Yuste, L., Gil, C., and Rojo, F. (2009a) The Pseudomonas putida Crc global regulator controls the hierarchical assimilation of amino acids in a complete medium: evidence from proteomic and genomic analyses. Proteomics 9: 2910-2928.
36. Moreno, R., Marzi, S., Romby, P., and Rojo, F. (2009b) The Crc global regulator binds to an unpaired A-rich motif at the Pseudomonas putida alkS mRNA coding sequence and inhibits translation initiation. Nucleic Acids Res 37: 7678-7690.
37. 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.
38. Nishijyo, T., Haas, D., and Itoh, Y. (2001) The CbrA-CbrB two-component regulatory system controls the utilization of multiple carbon and nitrogen sources in Pseudomonas aeruginosa. Mol Microbiol 40: 917-931.
39. Patton, J.R., and Chae, C.B. (1983) A method for mapping RNA initiation, termination, splice, and protein binding sites. Ribosome binding sites on beta-globin messenger RNA. J Biol Chem 258: 3991-3995.
40. Reimmann, C., Valverde, C., Kay, E., and Haas, D. (2005) Posttranscriptional repression of GacS/GacA-controlled genes by the RNA-binding protein RsmE acting together with RsmA in the biocontrol strain Pseudomonas fluorescens CHA0. J Bacteriol 187: 276-285.
41. Rojo, F. (2010) Carbon catabolite repression in Pseudomonas: optimizing metabolic versatility and interactions with the environment. FEMS Microbiol Rev 34: 658-684.
42. Rosenberg, A.H., Lade, B.N., Chui, D.S., Lin, S.W., Dunn, J.J., and Studier, F.W. (1987) Vectors for selective expression of cloned DNAs by T7 RNA polymerase. Gene 56: 125-135.
43. 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.
44. Sambrook, J., and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
45. Silby, M.W., Winstanley, C., Godfrey, S.A., Levy, S.B., and Jackson, R.W. (2011) Pseudomonas genomes: diverse and adaptable. FEMS Microbiol Rev 35: 652-680.
46. Sonnleitner, E., Abdou, L., and Haas, D. (2009) Small RNA as global regulator of carbon catabolite repression in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 106: 21866-21871.
47. Takeuchi, K., Kiefer, P., Reimmann, C., Keel, C., Dubuis, C., Rolli, J., etal. (2009) Small RNA-dependent expression of secondary metabolism is controlled by Krebs cycle function in Pseudomonas fluorescens. J Biol Chem 284: 34976-34985.
48. Weilbacher, T., Suzuki, K., Dubey, A.K., Wang, X., Gudapaty, S., Morozov, I., etal. (2003) A novel sRNA component of the carbon storage regulatory system of Escherichia coli. Mol Microbiol 48: 657-670.
49. Wolff, J.A., MacGregor, C.H., Eisenberg, R.C., and Phibbs, P.V., Jr (1991) Isolation and characterization of catabolite repression control mutants of Pseudomonas aeruginosa PAO. J Bacteriol 173: 4700-4706.
50. Yuste, L., and Rojo, F. (2001) Role of the crc gene in catabolic repression of the Pseudomonas putida GPo1 alkane degradation pathway. J Bacteriol 183: 6197-6206.
51. Yuste, L., Hervás, A.B., Canosa, I., Tobes, R., Jiménez, J.I., Nogales, J., etal. (2006) Growth-phase dependent expression of the Pseudomonas putida KT2440 transcriptional machinery analyzed with a genome-wide DNA microarray. Environ Microbiol 8: 165-177.