Advertisement

Applied Microbiology and Biotechnology

, Volume 91, Issue 1, pp 63–79 | Cite as

Small RNAs as regulators of primary and secondary metabolism in Pseudomonas species

  • Elisabeth Sonnleitner
  • Dieter Haas
Mini-Review

Abstract

Small RNAs (sRNAs) exert important functions in pseudomonads. Classical sRNAs comprise the 4.5S, 6S, 10Sa and 10Sb RNAs, which are known in enteric bacteria as part of the signal recognition particle, a regulatory component of RNA polymerase, transfer–messenger RNA (tmRNA) and the RNA component of RNase P, respectively. Their homologues in pseudomonads are presumed to have analogous functions. Other sRNAs of pseudomonads generally have little or no sequence similarity with sRNAs of enteric bacteria. Numerous sRNAs repress or activate the translation of target mRNAs by a base-pairing mechanism. Examples of this group in Pseudomonas aeruginosa are the iron-repressible PrrF1 and PrrF2 sRNAs, which repress the translation of genes encoding iron-containing proteins, and PhrS, an anaerobically inducible sRNA, which activates the expression of PqsR, a regulator of the Pseudomonas quinolone signal. Other sRNAs sequester RNA-binding proteins that act as translational repressors. Examples of this group in P. aeruginosa include RsmY and RsmZ, which are central regulatory elements in the GacS/GacA signal transduction pathway, and CrcZ, which is a key regulator in the CbrA/CbrB signal transduction pathway. These pathways largely control the extracellular activities (including virulence traits) and the selection of the energetically most favourable carbon sources, respectively, in pseudomonads.

Keywords

Small RNA Pseudomonas Virulence Carbon catabolite repression Secondary metabolism Quorum sensing 

Notes

Acknowledgments

This work was supported by the Swiss National Foundation, the Hertha-Firnberg Research fellowship from the Austrian Science Fund (to E.S.) and a genomics project of the University of Lausanne. We thank Cornelia Reimmann and Karine Lapouge for critically reading the manuscript.

References

  1. Aarons S, Abbas A, Adams C, Fenton A, O’Gara F (2000) A regulatory RNA (PrrB RNA) modulates expression of secondary metabolite genes in Pseudomonas fluorescens F113. J Bacteriol 182:3913–3919CrossRefGoogle Scholar
  2. Abdou L, Chou H-T, Haas D, Lu C-D (2011) Promoter recognition and activation by the global response regulator CbrB in Pseudomonas aeruginosa. J Bacteriol. doi: 10.1128/JB.00164-11 Google Scholar
  3. Altuvia S (2007) Identification of bacterial small non-coding RNAs: experimental approaches. Curr Opin Microbiol 10:257–261CrossRefGoogle Scholar
  4. Alvarez-Ortega C, Harwood CS (2007) Responses of Pseudomonas aeruginosa to low oxygen indicate that growth in the cystic fibrosis lung is by aerobic respiration. Mol Microbiol 65:153–165CrossRefGoogle Scholar
  5. Amador C, Canosa I, Govantes F, Santero E (2010) Lack of CbrB in Pseudomonas putida affects not only amino acid metabolism but also different stress responses and biofilm development. Environ Microbiol 12:1748–1761CrossRefGoogle Scholar
  6. Aranda-Olmedo I, Ramos JL, Marqués S (2005) Integration of signals through Crc and PtsN in catabolite repression of Pseudomonas putida TOL plasmid pWW0. Appl Environ Microbiol 71:4191–4198CrossRefGoogle Scholar
  7. Babitzke P, Romeo T (2007) CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 10:156–163CrossRefGoogle Scholar
  8. Backofen R, Hess WR (2010) Computational prediction of sRNAs and their targets in bacteria. RNA Biol 7:33–42CrossRefGoogle Scholar
  9. Barrick JE, Sudarsan N, Weinberg Z, Ruzzo WL, Breaker RR (2005) 6S RNA is a widespread regulator of eubacterial RNA polymerase that resembles an open promoter. RNA 11:774–784CrossRefGoogle Scholar
  10. Beisel CL, Storz G (2010) Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol Rev 34:866–882Google Scholar
  11. Blumer C, Haas D (2000a) Iron regulation of the hcnABC genes encoding hydrogen cyanide synthase depend on the anaerobic regulator ANR rather than on the global activator GacA in Pseudomonas fluorescens CHA0. Microbiology 146:2417–2424Google Scholar
  12. Blumer C, Haas D (2000b) Multicopy suppression of a gacA mutation by the infC operon in Pseudomonas fluorescens CHA0: competition with the global translational regulator RsmA. FEMS Microbiol Lett 187:53–58CrossRefGoogle Scholar
  13. Blumer C, Heeb S, Pessi G, Haas D (1999) Global GacA-steered control of cyanide and exoprotease production in Pseudomonas fluorescens involves specific ribosome binding sites. Proc Natl Acad Sci USA 96:14073–14078CrossRefGoogle Scholar
  14. Boisset S, Geissmann T, Huntzinger E, Fechter P, Bendridi N, Possedko M, Chevalier C, Helfer AC, Benito Y, Jacquier A, Gaspin C, Vandenesch F, Romby P (2007) Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 21:1353–1366CrossRefGoogle Scholar
  15. Bordi C, Lamy M-C, Ventre I, Termine E, Hachani A, Fillet S, Roche B, Bleves S, Méjean V, Lazdunski A, Filloux A (2010) Regulatory RNAs and the HptB/RetS signalling pathways fine tune Pseudomonas aeruginosa pathogenesis. Mol Microbiol 76:1427–1443CrossRefGoogle Scholar
  16. Brencic A, Lory S (2009) Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol Microbiol 72:612–632CrossRefGoogle Scholar
  17. Brencic A, McFarland KA, McManus HR, Castang S, Mogno I, Dove SL, Lory S (2009) The GacS/GacA signal transduction system of Pseudomonas aeruginosa acts exclusively through its control over the transcription of the RsmY and RsmZ regulatory small RNAs. Mol Microbiol 73:434–445CrossRefGoogle Scholar
  18. Bronstein PA, Filiatrault MJ, Myers CR, Rutzke M, Schneider DJ, Cartinhour SW (2008) Global transcriptional responses of Pseudomonas syringae DC3000 to changes in iron bioavailability in vitro. BMC Microbiol 8:209CrossRefGoogle Scholar
  19. Brown D (2010) A mathematical model of the Gac/Rsm quorum sensing network in Pseudomonas fluorescens. Biosystems 101:200–212CrossRefGoogle Scholar
  20. Burrowes E, Abbas A, O’Neill A, Adams C, O’Gara F (2005) Characterisation of the regulatory RNA RsmB from Pseudomonas aeruginosa PAO1. Res Microbiol 156:7–16CrossRefGoogle Scholar
  21. Burrowes E, Baysse C, Adams C, O’Gara F (2006) Influence of the regulatory protein RsmA on cellular functions in Pseudomonas aeruginosa PAO1, as revealed by transcriptome analysis. Microbiology 152:405–418CrossRefGoogle Scholar
  22. Cases I, Pérez-Martín J, de Lorenzo V (1999) The IIANtr (PtsN) protein of Pseudomonas putida mediates the C source inhibition of the σ54-dependent Pu promoter of the TOL plasmid. J Biol Chem 274:15562–15568CrossRefGoogle Scholar
  23. Collier DN, Hager PW, Phibbs PV Jr (1996) Catabolite repression control in the pseudomonads. Res Microbiol 147:551–561CrossRefGoogle Scholar
  24. Comolli JC, Donohue TJ (2004) Differences in two Pseudomonas aeruginosa cbb 3 cytochrome oxidases. Mol Microbiol 51:1193–1203CrossRefGoogle Scholar
  25. Cornelis P (2010) Iron uptake and metabolism in pseudomonads. Appl Microbiol Biotechnol 86:1637–1645CrossRefGoogle Scholar
  26. Dubey AK, Baker CS, Romeo T, Babitzke P (2005) RNA sequence and secondary structure participate in high-affinity CsrA–RNA interaction. RNA 11:1579–1587CrossRefGoogle Scholar
  27. Dubuis C, Keel C, Haas D (2007) Dialogues of root-colonizing biocontrol pseudomonads. Eur J Plant Pathol 119:311–328CrossRefGoogle Scholar
  28. Filiatrault MJ, Stodghill PV, Bronstein PA, Moll S, Lindeberg M, Grills G, Schweitzer P, Wang W, Schroth GP, Luo S, Khrebtukova I, Yang Y, Thannhauser T, Butcher BG, Cartinhour S, Schneider DJ (2010) Transcriptome analysis of Pseudomonas syringae identifies new genes, noncoding RNAs, and antisense activity. J Bacteriol 192:2359–2372CrossRefGoogle Scholar
  29. Gaffney TD, Lam ST, Ligon J, Gates K, Frazelle A, Di Maio J, Hill S, Goodwin S, Torkewitz N, Allshouse AM, Kempf H-J, Becker JO (1994) Global regulation of antifungal factors by a Pseudomonas fluorescens biological control strain. Mol Plant-Microb Interact 7:455–463CrossRefGoogle Scholar
  30. Gallagher LA, Manoil C (2001) Pseudomonas aeruginosa PAO1 kills Caenorhabditis elegans by cyanide poisoning. J Bacteriol 183:6207–6214CrossRefGoogle Scholar
  31. González N, Heeb S, Valverde C, Kay E, Reimmann C, Junier T, Haas D (2008) Genome-wide search reveals a novel GacA-regulated small RNA in Pseudomonas species. BMC Genomics 9:167CrossRefGoogle Scholar
  32. Goodman AL, Kulasekara B, Rietsch A, Boyd D, Smith RS, Lory S (2004) A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell 7:745–754CrossRefGoogle Scholar
  33. Goodman AL, Merighi M, Hyodo M, Ventre I, Filloux A, Lory S (2009) Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev 23:249–259CrossRefGoogle Scholar
  34. Görke B, Stülke J (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6:613–624CrossRefGoogle Scholar
  35. Haas D, Défago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319CrossRefGoogle Scholar
  36. Haas D, Gamper M, Zimmermann A (1992) Anaerobic control in Pseudomonas aeruginosa. In: Galli E, Silver S, Witholt B (eds) Pseudomonas, molecular biology and biotechnology. American Society for Microbiology, Washington, pp 177–187Google Scholar
  37. Hassan KA, Johnson A, Shaffer BT, Ren Q, Kidarsa TA, Elbourne LDH, Hartney S, Duboy R, Goebel NC, Zabriskie MT, Paulsen IT, Loper JE (2010) Inactivation of the GacA response regulator in Pseudomonas fluorescens Pf-5 has far-reaching transcriptomic consequences. Environ Microbiol 12:899–915CrossRefGoogle Scholar
  38. Heeb S, Blumer C, Haas D (2002) Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescens CHA0. J Bacteriol 184:1046–1056CrossRefGoogle Scholar
  39. Heeb S, Heurlier K, Valverde C, Cámara M, Haas D, Williams P (2004) Post-transcriptional regulation in Pseudomonas spp. via the Gac/Rsm regulatory network. In: Ramos J-L (ed) Pseudomonas—virulence and gene regulation, vol 2. Kluwer Academic, New York, pp 239–255Google Scholar
  40. Heeb S, Valverde C, Gigot-Bonnefoy C, Haas D (2005) Role of the stress sigma factor RpoS in GacA/RsmA-controlled secondary metabolism and resistance to oxidative stress in Pseudomonas fluorescens CHA0. FEMS Microbiol Lett 243:251–258CrossRefGoogle Scholar
  41. Heeb S, Kuehne SA, Bycroft M, Crivii S, Allen MD, Haas D, Cámara M, Williams P (2006) Functional analysis of the post-transcriptional regulator RsmA reveals a novel RNA-binding site. J Mol Biol 355:1026–1036CrossRefGoogle Scholar
  42. Heeb S, Fletcher MP, Chhabra SR, Diggle SP, Williams P, Camara M (2011) Quinolones: from antibiotics to autoinducers. FEMS Microbiol Rev 35:247–274CrossRefGoogle Scholar
  43. Hemm MR, Paul BJ, Schneider TD, Storz G, Rudd KE (2008) Small membrane proteins found by comparative genomics and ribosome binding site models. Mol Microbiol 70:1487–1501CrossRefGoogle Scholar
  44. Heurlier K, Williams F, Heeb S, Dormond C, Pessi G, Singer D, Cámara M, Williams P, Haas D (2004) Positive control of swarming, rhamnolipid synthesis, and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J Bacteriol 186:2936–2945CrossRefGoogle Scholar
  45. Hobbs EC, Astarita JL, Storz G (2010) Small RNAs and small proteins involved in resistance to cell envelope stress and acid shock in Escherichia coli: analysis of a bar-coded mutant collection. J Bacteriol 192:59–67CrossRefGoogle Scholar
  46. Hood RD, Singh P, Hsu F, Güvener T, Carl MA, Trinidad RR, Silverman JM, Ohlson BB, Hicks KG, Plemel RL, Li M, Schwarz S, Wang WY, Merz AJ, Goodlett DR, Mougous JD (2010) A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7:25–37CrossRefGoogle Scholar
  47. Hrabak EM, Willis DK (1992) The lemA gene required for pathogenicity of Pseudomonas syringae pv. syringae on bean is a member of a family of two-component regulators. J Bacteriol 174:3011–3020Google Scholar
  48. Hsu J-L, Chen H-C, Peng H-L, Chang H-Y (2008) Characterization of the histidine-containing phosphotransfer protein B-mediated multistep phosphorelay system in Pseudomonas aeruginosa PAO1. J Biol Chem 283:9933–9944CrossRefGoogle Scholar
  49. Humair B, González N, Mossialos D, Reimmann C, Haas D (2009) Temperature-responsive sensing regulates biocontrol factor expression in Pseudomonas fluorescens CHA0. ISME J 3:955–965CrossRefGoogle Scholar
  50. Humair B, Wackwitz B, Haas D (2010) GacA-controlled activation of promoters for small RNA genes in Pseudomonas fluorescens. Appl Environ Microbiol 76:1497–1506CrossRefGoogle Scholar
  51. Itoh Y, Nishijyo T, Nakada Y (2007) Histidine catabolism and catabolic regulation. In: Ramos J-L, Filloux A (eds) Pseudomonas–a model system in biology, vol 5. Springer, Dordrecht, pp 371–395Google Scholar
  52. Jacobs MA, Alwood A, Thaipisuttikul I, Spencer D, Haugen E, Ernst S, Will O, Kaul R, Raymond C, Levy R, Chun-Rong L, Guenthner D, Bovee D, Olson MV, Manoil C (2003) Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 100:14339–14344CrossRefGoogle Scholar
  53. James BD, Olsen GJ, Liu JS, Pace NR (1988) The secondary structure of ribonuclease P RNA, the catalytic element of a ribonucleoprotein enzyme. Cell 52:19–26CrossRefGoogle Scholar
  54. Jing X, Jaw J, Robinson HH, Schubot FD (2010) Crystal structure and oligomeric state of the RetS signaling kinase sensory domain. Proteins 78:1631–1640Google Scholar
  55. Juhas M, Eberl L, Tümmler B (2005) Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ Microbiol 7:459–471CrossRefGoogle Scholar
  56. Jung YS, Kwon YM (2008) Small RNA ArrF regulates the expression of sodB and feSII genes in Azotobacter vinelandii. Curr Microbiol 57:593–597CrossRefGoogle Scholar
  57. Kawakami T, Kuroki M, Ishii M, Igarashi Y, Arai H (2010) Differential expression of multiple terminal oxidases for aerobic respiration in Pseudomonas aeruginosa. Environ Microbiol 12:1399–1412Google Scholar
  58. Kay E, Dubuis C, Haas D (2005) Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Proc Natl Acad Sci USA 102:17136–17141CrossRefGoogle Scholar
  59. Kay E, Humair B, Dénervaud V, Riedel K, Spahr S, Eberl L, Valverde C, Haas D (2006) Two GacA-dependent small RNAs modulate the quorum sensing response in Pseudomonas aeruginosa. J Bacteriol 188:6026–6033CrossRefGoogle Scholar
  60. Keenan RJ, Freymann DM, Stroud RM, Walter P (2001) The signal recognition particle. Annu Rev Biochem 70:755–775CrossRefGoogle Scholar
  61. Keiler KC (2007) Physiology of tmRNA: what gets tagged and why? Curr Opin Microbiol 10:169–175CrossRefGoogle Scholar
  62. Kitten T, Willis DK (1996) Suppression of a sensor kinase-dependent phenotype in Pseudomonas syringae by ribosomal proteins L35 and L20. J Bacteriol 178:1548–1555Google Scholar
  63. Kulkarni PR, Cui X, Williams JW, Stevens AM, Kulkarni RV (2006) Prediction of CsrA-regulating small RNAs in bacteria and their experimental verification in Vibrio fischeri. Nucleic Acids Res 34:3361–3369CrossRefGoogle Scholar
  64. Lapouge K, Sineva E, Lindell M, Starke K, Baker CS, Babitzke P, Haas D (2007) Mechanism of hcnA mRNA recognition in the Gac/Rsm signal transduction pathway of Pseudomonas fluorescens. Mol Microbiol 66:341–356CrossRefGoogle Scholar
  65. Lapouge K, Schubert M, Allain FHT, Haas D (2008) Gac/Rsm signal transduction pathway of γ-proteobacteria: from RNA recognition to regulation of social behaviour. Mol Microbiol 67:241–253CrossRefGoogle Scholar
  66. Laskowski MA, Kazmierczak BI (2006) Mutational analysis of RetS, an unusual sensor kinase-response regulator hybrid required for Pseudomonas aeruginosa virulence. Infect Immun 74:4462–4473CrossRefGoogle Scholar
  67. Laville J, Voisard C, Keel C, Maurhofer M, Défago G, Haas D (1992) Global control in Pseudomonas fluorescens mediating antibiotic synthesis and suppression of black root rot of tobacco. Proc Natl Acad Sci USA 89:1562–1566CrossRefGoogle Scholar
  68. Lazdunski AM, Ventre I, Bleves S (2007) Cell-cell communication: quorum sensing and regulatory circuits in Pseudomonas aeruginosa. In: Ramos J-L, Filloux A (eds) Pseudomonas, a model system in biology, vol 5. Springer, Dordrecht, pp 279–310Google Scholar
  69. Li Y, Altman S (2004) In search of RNase P RNA from microbial genomes. RNA 10:1533–1540CrossRefGoogle Scholar
  70. Li W, Lu C-D (2007) Regulation of carbon and nitrogen utilization by CbrAB and NtrBC two-component systems in Pseudomonas aeruginosa. J Bacteriol 189:5413–5420CrossRefGoogle Scholar
  71. Linares JF, Moreno R, Fajardo A, Martínez L, Escalante R, Rojo F, Martínez JL (2010) The global regulator Crc modulates metabolism, susceptibility to antibiotics and virulence in Pseudomonas aeruginosa. Environ Microbiol 12:3196–3212CrossRefGoogle Scholar
  72. Liu JM, Camilli A (2010) A broadening world of bacterial small RNAs. Curr Opin Microbiol 13:18–23CrossRefGoogle Scholar
  73. Livny J, Brencic A, Lory S, Waldor MK (2006) Identification of 17 Pseudomonas aeruginosa sRNAs and prediction of sRNA-encoding genes in 10 diverse pathogens using the bioinformatic tool sRNAPredict2. Nucleic Acids Res 34:3484–3493CrossRefGoogle Scholar
  74. Loper JE, Kobayashi DY, Paulsen IT (2007) The genomic sequence of Pseudomonas fluorescens Pf-5: insights into biological control. Phytopathology 97:233–238CrossRefGoogle Scholar
  75. MacGregor CH, Wolff JA, Arora SK, Phibbs PV 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 173:7204–7212Google Scholar
  76. Massé E, Gottesman S (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci USA 99:4620–4625CrossRefGoogle Scholar
  77. Moreno R, Rojo F (2008) The target for the Pseudomonas putida Crc global regulator in the benzoate degradation pathway is the BenR transcriptional regulator. J Bacteriol 190:1539–1545CrossRefGoogle Scholar
  78. 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 64:665–675CrossRefGoogle Scholar
  79. Moreno R, Marzi S, Romby P, Rojo F (2009) 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 37:7678–7690CrossRefGoogle Scholar
  80. Moreno R, Fonseca P, Rojo F (2010) The Crc global regulator inhibits the Pseudomonas putida pWW0 toluene/xylene assimilation pathway by repressing translation of regulatory and structural genes. J Biol Chem 285:24412–24419CrossRefGoogle Scholar
  81. Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, Gifford CA, Goodman AL, Joachimiak G, Ordoñez CL, Lory S, Walz T, Joachimiak A, Mekalanos JJ (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312:1526–1530CrossRefGoogle Scholar
  82. Müsken M, Di Fiore S, Dötsch A, Fischer R, Häussler S (2010) Genetic determinants of Pseudomonas aeruginosa biofilm establishment. Microbiology 156:431–441CrossRefGoogle Scholar
  83. Nishijyo T, Haas D, Itoh Y (2001) The CbrA–CbrB two-component regulatory system controls the utilization of multiple carbon and nitrogen sources in Pseudomonas aeruginosa. Mol Microbiol 40:917–931CrossRefGoogle Scholar
  84. Oglesby AG, Farrow JM 3rd, Lee JH, Tomaras AP, Greenberg EP, Pesci EC, Vasil ML (2008) The influence of iron on Pseudomonas aeruginosa physiology: a regulatory link between iron and quorum sensing. J Biol Chem 283:15558–15567CrossRefGoogle Scholar
  85. Oglesby-Sherrouse AG, Vasil ML (2010) Characterization of a heme-regulated non-coding RNA encoded by the prrF locus of Pseudomonas aeruginosa. PLoS ONE 5:e9930CrossRefGoogle Scholar
  86. O’Toole GA, Gibbs KA, Hager PW, Phibbs PV Jr, Kolter R (2000) The global carbon metabolism regulator Crc is a component of a signal transduction pathway required for biofilm development by Pseudomonas aeruginosa. J Bacteriol 182:425–431CrossRefGoogle Scholar
  87. Parkins MD, Ceri H, Storey DG (2001) Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol Microbiol 40:1215–1226CrossRefGoogle Scholar
  88. Pernestig AK, Melefors O, Georgellis D (2001) Identification of UvrY as the cognate response regulator for the BarA sensor kinase in Escherichia coli. J Biol Chem 276:225–231CrossRefGoogle Scholar
  89. Pessi G, Haas D (2001) Dual control of hydrogen cyanide biosynthesis by the global activator GacA in Pseudomonas aeruginosa PAO1. FEMS Microbiol Lett 200:73–78CrossRefGoogle Scholar
  90. Pessi G, Williams F, Hindle Z, Heurlier K, Holden MT, Cámara M, Haas D, Williams P (2001) The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. J Bacteriol 183:6676–6683CrossRefGoogle Scholar
  91. Petrova OE, Sauer K (2010) The novel two-component regulatory system BfiSR regulates biofilm development by controlling the small RNA rsmZ through CafA. J Bacteriol 192:5275–5288CrossRefGoogle Scholar
  92. Petruschka L, Burchhardt G, Müller C, Weihe C, Herrmann H (2001) The cyo operon of Pseudomonas putida is involved in catabolic repression of phenol degradation. Mol Genet Genomics 266:199–206CrossRefGoogle Scholar
  93. Pyla R, Kim TJ, Silva JL, Jung YS (2009) Overproduction of poly-β-hydroxybutyrate in the Azotobacter vinelandii mutant that does not express small RNA ArrF. Appl Microbiol Biotechnol 84:717–724CrossRefGoogle Scholar
  94. Rahme LG, Ausubel FM, Cao H, Drenkard E, Goumnerov BC, Lau GW, Mahajan-Miklos S, Plotnikova J, Tan MW, Tsongalis J, Walendziewicz CL, Tompkins RG (2000) Plants and animals share functionally common bacterial virulence factors. Proc Natl Acad Sci USA 97:8815–8821CrossRefGoogle Scholar
  95. Reimmann C, Beyeler M, Latifi A, Winteler H, Foglino M, Lazdunski A, Haas D (1997) The global activator GacA of Pseudomonas aeruginosa PAO1 positively controls the production of the autoinducer N-butyryl-homoserine lactone and the formation of the virulence factors pyocyanin, cyanide, and lipase. Mol Microbiol 24:309–319CrossRefGoogle Scholar
  96. Reimmann C, Valverde C, Kay E, 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 187:276–285CrossRefGoogle Scholar
  97. Rich JJ, Kinscherf TG, Kitten T, Willis DK (1994) Genetic evidence that the gacA gene encodes the cognate response regulator for the lemA sensor in Pseudomonas syringae. J Bacteriol 176:7468–7475Google Scholar
  98. Rojo F (2010) Carbon catabolite repression in Pseudomonas: optimizing metabolic versatility and the interaction with the environment. FEMS Microbiol Rev 34:658–784Google Scholar
  99. Rowley KB, Clements DE, Mandel M, Humphreys T, Patil SS (1993) Multiple copies of a DNA sequence from Pseudomonas syringae pathovar phaseolicola abolish thermoregulation of phaseolotoxin production. Mol Microbiol 8:625–635CrossRefGoogle Scholar
  100. Ruiz-Manzano A, Yuste L, Rojo F (2005) Levels and activity of the Pseudomonas putida global regulatory protein Crc vary according to growth conditions. J Bacteriol 187:3678–3686CrossRefGoogle Scholar
  101. Sabra W, Kim EJ, Zeng AP (2002) Physiological responses of Pseudomonas aeruginosa PAO1 to oxidative stress in controlled microaerobic and aerobic cultures. Microbiology 148:3195–3202Google Scholar
  102. Schobert M, Tielen P (2010) Contribution of oxygen-limiting conditions to persistent infection of Pseudomonas aeruginosa. Future Microbiol 5:603–621CrossRefGoogle Scholar
  103. Schubert M, Lapouge K, Duss O, Oberstrass FC, Jelesarov I, Haas D, Allain FH (2007) Molecular basis of messenger RNA recognition by the specific bacterial repressing clamp RsmA/CsrA. Nat Struct Mol Biol 14:807–813CrossRefGoogle Scholar
  104. Sharma CM, Vogel J (2009) Experimental approaches for the discovery and characterization of regulatory small RNA. Curr Opin Microbiol 12:536–546CrossRefGoogle Scholar
  105. Siegel LS, Hylemon PB, Phibbs PV Jr (1977) Cyclic adenosine 3′,5′-monophosphate levels and activities of adenyl cyclase and cyclic adenosine 3′,5′-monophosphate phosphodiesterase in Pseudomonas and Bacteroides. J Bacteriol 129:87–96Google Scholar
  106. Silby MW, Rainey PB, Levy SB (2004) IVET experiments in Pseudomonas fluorescens reveal cryptic promoters at loci associated with recognizable overlapping genes. Microbiology 150:518–520CrossRefGoogle Scholar
  107. Smyth PF, Clarke PH (1975) Catabolite repression of Pseudomonas aeruginosa amidase: the effect of carbon source on amidase synthesis. J Gen Microbiol 90:81–90Google Scholar
  108. Sonnleitner E, Schuster M, Sorger-Domenigg T, Greenberg EP, Bläsi U (2006) Hfq-dependent alterations of the transcriptome profile and effects on quorum sensing in Pseudomonas aeruginosa. Mol Microbiol 59:1542–1558CrossRefGoogle Scholar
  109. Sonnleitner E, Sorger-Domenigg T, Madej MJ, Findeiss S, Hackermüller J, Hüttenhofer A, Stadler PF, Bläsi U, Moll I (2008) Detection of small RNAs in Pseudomonas aeruginosa by RNomics and structure-based bioinformatic tools. Microbiology 154:3175–3187CrossRefGoogle Scholar
  110. Sonnleitner E, Abdou L, Haas D (2009) Small RNA as global regulator of carbon catabolite repression in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 106:21866–21871CrossRefGoogle Scholar
  111. Sonnleitner E, González N, Haas D (2010) Small RNAs of Pseudomonas spp. In: Ramos J-L, Filloux A (eds) Pseudomonas—molecular microbiology, infection and biodiversity, vol 6. Springer, Dordrecht, pp 3–28Google Scholar
  112. Sonnleitner E, Gonzalez N, Sorger-Domenigg T, Heeb S, Richter AS, Backofen R, Williams P, Hüttenhofer A, Haas D, Bläsi U (2011) The small RNA PhrS stimulates synthesis of the Pseudomonas aeruginosa quinolone signal. Mol Microbiol. doi: 10.1111/j.1365-2958.2011.07620.x Google Scholar
  113. Soper T, Mandin P, Majdalani N, Gottesman S, Woodson SA (2010) Positive regulation by small RNAs and the role of Hfq. Proc Natl Acad Sci USA 107:9602–9607CrossRefGoogle Scholar
  114. Sorek R, Cossart P (2010) Prokaryotic transcriptomics: a new view on regulation, physiology and pathogenicity. Nat Rev Genet 11:9–16CrossRefGoogle Scholar
  115. Sorger-Domenigg T, Sonnleitner E, Kaberdin VR, Bläsi U (2007) Distinct and overlapping binding sites of Pseudomonas aeruginosa Hfq and RsmA proteins on the non-coding RNA RsmY. Biochem Biophys Res Commun 352:769–773CrossRefGoogle Scholar
  116. Soscia C, Hachani A, Bernadac A, Filloux A, Bleves S (2007) Cross talk between type III secretion and flagellar assembly systems in Pseudomonas aeruginosa. J Bacteriol 189:3124–3132CrossRefGoogle Scholar
  117. Suh S-J, Runyen-Janecky LJ, Maleniak TC, Hager P, MacGregor CH, Zielinski-Mozny NA, Phibbs PV Jr, West SHE (2002) Effect of vfr mutation on global gene expression and catabolite repression control of Pseudomonas aeruginosa. Microbiology 148:1561–1569Google Scholar
  118. Takeuchi K, Kiefer P, Reimmann C, Keel C, Dubuis C, Rolli J, Vorholt JA, Haas D (2009) Small RNA-dependent expression of secondary metabolism is controlled by Krebs cycle function in Pseudomonas fluorescens. J Biol Chem 284:34976–34985CrossRefGoogle Scholar
  119. Toschka HY, Struck JC, Erdmann VA (1989) The 4.5S RNA gene from Pseudomonas aeruginosa. Nucleic Acids Res 17:31–36CrossRefGoogle Scholar
  120. Toyofuku M, Nomura N, Kuno E, Tashiro Y, Nakajima T, Uchiyama HJ (2008) Influence of the Pseudomonas quinolone signal on denitrification in Pseudomonas aeruginosa. J Bacteriol 190:7947–7956CrossRefGoogle Scholar
  121. Valverde C, Heeb S, Keel C, Haas D (2003) RsmY, a small regulatory RNA, is required in concert with RsmZ for GacA-dependent expression of biocontrol traits in Pseudomonas fluorescens CHA0. Mol Microbiol 50:1361–1379CrossRefGoogle Scholar
  122. Valverde C, Lindell M, Wagner EG, Haas D (2004) A repeated GGA motif is critical for the activity and stability of the riboregulator RsmY of Pseudomonas fluorescens. J Biol Chem 279:25066–25074CrossRefGoogle Scholar
  123. Vasil ML (2007) How we learnt about iron acquisition in Pseudomonas aeruginosa: a series of very fortunate events. Biometals 20:587–601CrossRefGoogle Scholar
  124. Ventre I, Goodman AL, Valley-Gely I, Vasseur P, Soscia C, Molin S, Bleves S, Lazdunski A, Lory S, Filloux A (2006) Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc Natl Acad Sci USA 103:171–176CrossRefGoogle Scholar
  125. Ventre I, Goodman AL, Filloux A, Lory S (2007) Modulation of bacterial lifestyles via two-component regulatory networks. In: Ramos J-L, Filloux A (eds) Pseudomonas—a model system in biology, vol 5. Springer, Dordrecht, pp 311–340Google Scholar
  126. Vincent F, Round A, Reynaud A, Bordi C, Filloux A, Bourne Y (2010) Distinct oligomeric forms of the Pseudomonas aeruginosa RetS sensor domain modulate accessability to the ligand binding site. Environ Microbiol 12:1775–1786CrossRefGoogle Scholar
  127. Visca P (2004) Iron regulation and siderophore signalling in virulence by Pseudomonas aeruginosa. In: Ramos J-L (ed) Pseudomonas—virulence and gene regulation, vol 2. Springer, Dordrecht, pp 69–123Google Scholar
  128. Vogel J (2009) A rough guide to the non-coding RNA world of Salmonella. Mol Microbiol 71:1–11CrossRefGoogle Scholar
  129. Vogel DW, Hartmann RK, Struck JC, Ulbrich N, Erdmann VA (1987) The sequence of the 6S RNA gene of Pseudomonas aeruginosa. Nucleic Acids Res 15:4583–4591CrossRefGoogle Scholar
  130. Wadler CS, Vanderpool CK (2007) A dual function for a bacterial small RNA: SgrS performs base pairing-dependent regulation and encodes a functional polypeptide. Proc Natl Acad Sci USA 104:20454–20459CrossRefGoogle Scholar
  131. Wassarman KM (2007) 6S RNA: a regulator of transcription. Mol Microbiol 65:1425–1431CrossRefGoogle Scholar
  132. Wassarman KM, Zhang A, Storz G (1999) Small RNAs in Escherichia coli. Trends Microbiol 7:37–45CrossRefGoogle Scholar
  133. Waters LS, Storz G (2009) Regulatory RNAs in bacteria. Cell 136:615–628CrossRefGoogle Scholar
  134. Whistler CA, Corbell NA, Sarniguet A, Ream W, Loper JE (1998) The two-component regulators GacS and GacA influence accumulation of the stationary-phase sigma factor σS and the stress response in Pseudomonas fluorescens Pf-5. J Bacteriol 180:6635–6641Google Scholar
  135. Wilderman PJ, Sowa NA, FitzGerald DJ, FitzGerald PC, Gottesman S, Ochsner UA, Vasil ML (2004) Identification of tandem duplicate regulatory small RNAs in Pseudomonas aeruginosa involved in iron homeostasis. Proc Natl Acad Sci USA 101:9792–9797CrossRefGoogle Scholar
  136. Williams KP, Bartel DP (1996) Phylogenetic analysis of tmRNA secondary structure. RNA 2:1306–1310Google Scholar
  137. Winteler HV, Haas D (1996) The homologous regulators ANR of Pseudomonas aeruginosa and FNR of Escherichia coli have overlapping but distinct specificities for anaerobically inducible promoters. Microbiology 142:685–693CrossRefGoogle Scholar
  138. Workentine M-L, Chang L, Ceri H, Turner RJ (2009) The GacS–GacA two-component regulatory system of Pseudomonas fluorescens: a bacterial two-hybrid analysis. FEMS Microbiol Lett 292:50–56CrossRefGoogle Scholar
  139. Ye RW, Haas D, Ka JO, Krishnapillai V, Zimmermann A, Baird C, Tiedje JM (1995) Anaerobic activation of the entire denitrification pathway in Pseudomonas aeruginosa requires Anr, an analog of Fnr. J Bacteriol 177:3606–3609Google Scholar
  140. Zhang X-X, Liu Y-H, Rainey PB (2010) CbrAB-dependent regulation of pcnB, a pola(A) polymerase gene involved in polyadenylation of RNA in Pseudomonas fluorescens. Environ Microbiol 12:1674–1683CrossRefGoogle Scholar
  141. Zimmermann A, Reimmann C, Galimand M, Haas D (1991) Anaerobic growth and cyanide synthesis of Pseudomonas aeruginosa depend on anr, a regulatory gene homologous with fnr of Escherichia coli. Mol Microbiol 5:1483–1490CrossRefGoogle Scholar
  142. Zolfaghar I, Evans DJ, Ronaghi R, Fleiszig SM (2006) Type III secretion-dependent modulation of innate immunity as one of multiple factors regulated by Pseudomonas aeruginosa RetS. Infect Immun 74:3880–3889CrossRefGoogle Scholar
  143. Zuber S, Carruthers F, Keel C, Mattart A, Blumer C, Pessi G, Gigot-Bonnefoy C, Schnider-Keel U, Heeb S, Reimmann C, Haas D (2003) GacS sensor domains pertinent to the regulation of exoproduct formation and to the biocontrol potential of Pseudomonas fluorescens CHA0. Mol Plant-Microb Interact 16:634–644CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  1. 1.Max F. Perutz Laboratories, Department of Microbiology, Immunobiology and GeneticsUniversity of ViennaViennaAustria
  2. 2.Département de Microbiologie FondamentaleUniversité de LausanneLausanneSwitzerland

Personalised recommendations