Small RNAs Controlled by Two-Component Systems

  • Claudio Valverde
  • Dieter Haas
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 631)


Two-component systems (TCSs) allow bacteria to monitor diverse environmental cues and to adjust gene expression accordingly at the transcriptional level. It has been recently recognized that prokaryotes also regulate many genes and operons at a posttranscriptional level with the participation of small, noncoding RNAs which serve to control translation initiation and stability of target mRNAs, either directly by establishing antisense interactions or indirectly by antagonizing RNA-binding proteins. Interestingly, the expression of a subset of these small RNAs is regulated by TCSs and in this way, the small RNAs expand the scope of genetic control exerted by TCSs. Here we review the regulatory mechanisms and biological relevance of a number of small RNAs under TCS control in Gram-negative and-positive bacteria. These regulatory systems govern, for instance, porin-dependent permeability of the outer membrane, quorum-sensing control of pathogenicity, or biocontrol activity. Most likely, this emerging and rapidly expanding field of molecular microbiology will provide more and more examples in the near future.


Small RNAs Ribosome Binding Site Carotovora Subsp Cognate Response Regulator Conserve Aspartate Residue 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Cashin P, Goldsack L, Hall D et al. Contrasting signal transduction mechanisms in bacterial and eukaryotic gene transcription. FEMS Microbiol Lett 2006; 261:155–164.PubMedCrossRefGoogle Scholar
  2. 2.
    Galperin MY. Structural classification of bacterial response regulators: diversity of output domains and domain combinations. J Bacteriol 2006; 188:4169–4182.PubMedCrossRefGoogle Scholar
  3. 3.
    Gottesman S. Micros for microbes: noncoding regulatory RNAs in bacteria. Trends Genet 2005; 21:399–404.PubMedCrossRefGoogle Scholar
  4. 4.
    Majdalani N, Vanderpool CK, Gottesman S. Bacterial small RNA regulators. Crit Rev Biochem Mol Biol 2005; 40:93–113.PubMedCrossRefGoogle Scholar
  5. 5.
    Hüttenhofer A, Vogel J. Experimental approaches to identify noncoding RNAs. Nucleic Acids Res 2006; 34:635–646.PubMedCrossRefGoogle Scholar
  6. 6.
    Livny J, Brencic A, Lory S et al. Identification of 17 Pseudomonas aeruginosa sRNAs and prediction of sRNA-encoding genes in 10 diverse pathogens using the bioinformatic tool, sRNAPredict. Nucleic Acids Res 2006; 34:3484–3493.PubMedCrossRefGoogle Scholar
  7. 7.
    Schumacher MA, Pearson RF, Møller T et al. Structures of the pleiotropic translational regulator Hfq and an Hfq-RNA complex: a bacterial Sm-like protein. EMBO J 2002; 21:3546–3556.PubMedCrossRefGoogle Scholar
  8. 8.
    Nikulin A, Stolboushkina E, Perederina A et al. Structure of Pseudomonas aeruginosa Hfq protein. Acta Crystallogr D Biol Crystallogr 2005; 61:141–146.PubMedCrossRefGoogle Scholar
  9. 9.
    Valentin-Hansen P, Eriksen M, Udesen C. The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol Microbiol 2004; 51:1525–1533.PubMedCrossRefGoogle Scholar
  10. 10.
    Kawamoto H, Koide Y, Morita T et al. Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq. Mol Microbiol 2006; 61:1013–1022.PubMedCrossRefGoogle Scholar
  11. 11.
    Vogel J, Argaman L, Wagner EG et al. The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide. Curr Biol 2004; 14:2271–2276.PubMedCrossRefGoogle Scholar
  12. 12.
    Morita T, Maki K, Aiba H. RNase E-based ribonucleoprotein complexes: mechanical basis of mRNA destabilization mediated by bacterial noncoding RNAs. Genes Dev 2005; 19:2176–2186.PubMedCrossRefGoogle Scholar
  13. 13.
    Udekwu KI, Darfeuille F, Vogel J et al. Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes Dev 2005; 19:2355–2366.PubMedCrossRefGoogle Scholar
  14. 14.
    Zamore PD. Ancient pathways programmed by small RNAs. Science 2002; 296:1265–1269.PubMedCrossRefGoogle Scholar
  15. 15.
    Opdyke JA, Kang JG, Storz G. GadY, a small-RNA regulator of acid response genes in Escherichia coli. J Bacteriol 2004; 186:6698–6705.PubMedCrossRefGoogle Scholar
  16. 16.
    Gutierrez P, Li Y, Osborne MJ et al. Solution structure of the carbon storage regulator protein CsrA from Escherichia coli. J Bacteriol 2005; 187:3496–3501.PubMedCrossRefGoogle Scholar
  17. 17.
    Rife C, Schwarzenbacher R, McMullan D et al. Crystal structure of the global regulatory protein CsrA from Pseudomonas putida at 2.05 Å resolution reveals a new fold. Proteins 2005; 61:449–453.PubMedCrossRefGoogle Scholar
  18. 18.
    Heeb S, Kuehne SA, Bycroft M et al. Functional analysis of the posttranscriptional regulator RsmA reveals a novel RNA-binding site. J Mol Biol 2006; 355:1026–1036.PubMedCrossRefGoogle Scholar
  19. 19.
    Baker CS, Morozov I, Suzuki K et al. CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli. Mol Microbiol 2002; 44:1599–1610.PubMedCrossRefGoogle Scholar
  20. 20.
    Wang X, Dubey AK, Suzuki K et al. CsrA posttranscriptionally represses pgaABCD, responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli. Mol Microbiol 2005; 56:1648–1663.PubMedCrossRefGoogle Scholar
  21. 21.
    Dubey AK, Baker CS, Romeo T et al. RNA sequence and secondary structure participate in high-affinity CsrA-RNA interaction. RNA 2005; 11:1579–1587.PubMedCrossRefGoogle Scholar
  22. 22.
    Liu MY, Gui G, Wei B et al. The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J Biol Chem 1997; 272:17502–17510.PubMedCrossRefGoogle Scholar
  23. 23.
    Liu Y, Cui Y, Mukherjee A et al. Characterization of a novel RNA regulator of Erwinia carotovora ssp. carotovora that controls production of extracellular enzymes and secondary metabolites. Mol Microbiol 1998; 29:219–234.PubMedCrossRefGoogle Scholar
  24. 24.
    Aarons S, Abbas A, Adams C et al. A regulatory RNA (PrrB RNA) modulates expression of secondary metabolite genes in Pseudomonas fluorescens F113. J Bacteriol 2000; 182:3913–3919.PubMedCrossRefGoogle Scholar
  25. 25.
    Heeb S, Blumer C, Haas D. Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescens, CHA0 J Bacteriol 2002; 184:1046–1056.PubMedCrossRefGoogle Scholar
  26. 26.
    Romeo T. Global regulation by the small RNA-binding protein CsrA and the noncoding RNA molecule CsrB. Mol Microbiol 1998; 29:1321–1330.PubMedCrossRefGoogle Scholar
  27. 27.
    Valverde C, Lindell M, Wagner EG et al. A repeated GGA motif is critical for the activity and stability of the riboregulator RsmY of Pseudomonas fluorescens. J Biol Chem 2004; 279:25066–25074.PubMedCrossRefGoogle Scholar
  28. 28.
    Romeo T. Posttranscriptional regulation of bacterial carbohydrate metabolism: evidence that the gene product CsrA is a global mRNA decay factor. Res Microbiol 1996; 147:505–512.PubMedCrossRefGoogle Scholar
  29. 29.
    Wei BL, Brun-Zinkernagel AM, Simecka JW et al. Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol Microbiol 2001; 40:245–256.PubMedCrossRefGoogle Scholar
  30. 30.
    Nikaido H. Proins and specific channels of bacterial outer membranes. Mol Microbiol 1992; 6:435–442.PubMedCrossRefGoogle Scholar
  31. 31.
    Wang Y. The function of OmpA in Escherichia coli. Biochem Biophys Res Commun 2002; 292:396–401.PubMedCrossRefGoogle Scholar
  32. 32.
    Kaeriyama M, Machida K, Kitakaze A et al. OmpC and OmpF are required for growth under hyperosmotic stress above pH 8 in Escherichia coli. Lett Appl Microbiol 2006; 42:195–201.PubMedCrossRefGoogle Scholar
  33. 33.
    Rasmussen AA, Eriksen M, Gilany K et al. Regulation of ompA mRNA stability: the role of a small regulatory RNA in growth phase-dependent control. Mol Microbiol 2005; 58:1421–1429.PubMedCrossRefGoogle Scholar
  34. 34.
    Yoshida T, Qin L, Egger LA et al. Transcription regulation of ompF and ompC by a single transcription factor OmpR. J Biol Chem 2006; 281: 17114–17123.PubMedCrossRefGoogle Scholar
  35. 35.
    Aiba H, Matsuyama S, Mizuno T et al. Function of micF, as an antisense RNA in osmoregulatory expression of the ompF gene in Escherichia coli. J Bacteriol 1987; 169:3007–3012.PubMedGoogle Scholar
  36. 36.
    Chen S, Zhang A, Blyn LB et al. MicC, a second small-RNA regulator of Omp protein expression in Escherichia coli. J Bacteriol 2004; 186:6689–6697.PubMedCrossRefGoogle Scholar
  37. 37.
    Delihas N, Forst S. MicF: an antisense RNA gene involved in response of Escherichia coli to global stress factors. J Mol Biol 2001; 313:1–12.PubMedCrossRefGoogle Scholar
  38. 38.
    Zhang A, Wassarman KM, Rosenow C et al. Global analysis of small RNA and mRNA targets of Hfq. Mol Microbiol 2003; 50:1111–1124.PubMedCrossRefGoogle Scholar
  39. 39.
    Demple B. Redox signaling and gene control in the Escherichia coli soxRS oxidative stress regulon—a review. Gene 1996; 179:53–57.PubMedCrossRefGoogle Scholar
  40. 40.
    Castillo-Keller M, Vuong P, Misra R. Novel mechanism of Escherichia coli porin, regulation. J Bacteriol 2006; 188:576–586.PubMedCrossRefGoogle Scholar
  41. 41.
    Douchin V, Bohn C, Bouloc P. Down-regulation of porins by a small RNA bypasses the essentiality of the regulated intramembrane proteolysis protease RseP in Escherichia coli. J Biol Chem 2006; 281:12253–12259.PubMedCrossRefGoogle Scholar
  42. 42.
    Johansen J, Rasmussen AA, Overgaard M et al. Conserved small noncoding RNAs that belong to the sigmaE regulon: role in down-regulation of outer membrane proteins. J Mol Biol 2006; 364:1–8.PubMedCrossRefGoogle Scholar
  43. 43.
    Guillier M, Gottesman S. Remodelling of the Escherichia coli outer membrane by two small regulatory RNAs. Mol Microbiol 2006; 59:231–247.PubMedCrossRefGoogle Scholar
  44. 44.
    Guillier M, Gottesman S, Storz G. Modulating the outer membrane with small RNAs. Genes Dev 2006; 20:2338–2348.PubMedCrossRefGoogle Scholar
  45. 45.
    Vogel J, Papenfort K. Small noncoding RNAs and the bacterial outer membrane. Curr Opin Microbiol 2006; 9:1–7.CrossRefGoogle Scholar
  46. 46.
    Novick RP. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 2003; 48:1429–1449.PubMedCrossRefGoogle Scholar
  47. 47.
    Otto M. Quorum-sensing control in Staphylococci—a target for antimicrobial drug therapy? FEMS Microbiol Lett 2004; 241:135–141.PubMedCrossRefGoogle Scholar
  48. 48.
    Romby P, Vandenesch F, Wagner EG. The role of RNAs in the regulation of virulence-gene expression. Curr Opin Microbiol 2006; 9:229–236.PubMedCrossRefGoogle Scholar
  49. 49.
    Morfeldt E, Taylor D, von Gabain A et al. Activation of alpha-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J 1995; 14:4569–4577.PubMedGoogle Scholar
  50. 50.
    Huntzinger E, Boisset S, Saveanu C et al. Staphylococeus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. EMBO J 2005; 24:824–835.PubMedCrossRefGoogle Scholar
  51. 51.
    Geisinger E, Adhikari RP, Jin R et al. Inhibition of rot translation by RNAIII, a key feature of agr function. Mol Microbiol 2006; 61:1038–1048.PubMedCrossRefGoogle Scholar
  52. 52.
    Said-Salim B, Dunman PM, McAleese FM et al. Global regulation of Staphylococcus aureus genes by Rot. J Bacteriol 2003; 185:610–619.PubMedCrossRefGoogle Scholar
  53. 53.
    Haas D, Keel C. Regulation of antibiotic production in root-colonizing Pseudomonas spp. and relevance for biological control of plant disease. Annu Rev Phytopathol 2003; 41:117–153.PubMedCrossRefGoogle Scholar
  54. 54.
    Haas D, Défago G. Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 2005; 3:307–319.PubMedCrossRefGoogle Scholar
  55. 55.
    Laville J, Voisard C, keel C et al. Global control in Pseudomonas fluorescens mediating antibiotic synthesis and suppression of black root rot of tobacco. Proc Natl Acad Sci USA 1992; 89:1562–1566.PubMedCrossRefGoogle Scholar
  56. 56.
    Gaffney TD, Lam ST, Ligon J et al. Global regulation of expression of antifungal factors by a Pseudomonas fluorescens biological control strain. Mol Plant Microbe Interact 1994; 7:455–463.PubMedGoogle Scholar
  57. 57.
    Corbell N, Loper JE. A global regulator of secondary metabolite production in Pseudomonas fluorescens Pf-5. J Bacteriol 1995; 177:6230–6236.PubMedGoogle Scholar
  58. 58.
    Heeb S, Haas D. Regulatory roles of the GacS/GacA two-component system in plant-associated and other gram-negative bacteria. Mol Plant Microbe Interact 2001; 14: 1351–1363.PubMedCrossRefGoogle Scholar
  59. 59.
    van den Broek D, Chin-A-Woeng TF, Eijkemans K et al. Biocontrol traits of Pseudomnas spp. are regulated by phase variation. Mol Plant Microbe Interact 2003; 16:1003–12.PubMedCrossRefGoogle Scholar
  60. 60.
    Zuber S, Carruthers F, Keel C et al. GacS sensor domains pertinent to the regulation of exoproduct formation and to the biocontrol potential of Pseudomonas fluorescens CHAO. Mol Plant Microbe Interact 2003; 16:634–644.PubMedCrossRefGoogle Scholar
  61. 61.
    Dubuis C, Rolli J, Lutz M et al. Thiamine-auxotrophic mutants of Pseudomonas fluorescens CHAO are defective in cell-cell signaling and biocontrol factor expression. Appl Environ Microbiol 2006; 72:2606–2613.PubMedCrossRefGoogle Scholar
  62. 62.
    Dubuis C, Haas D. Cross-species GacA-controlled induction of antibiosis in pseudomonads. Appl Environ Microbiol 2007; 73:650–654.PubMedCrossRefGoogle Scholar
  63. 63.
    Wang N, Lu SE, Wang J et al. The expression of genes encoding lipodepsipeptide phytotoxins by Pseudomonas syringae pv. syringae is coordinated in response to plant signal molecules. Mol Plant Microbe Interact 2006; 19:257–269.PubMedCrossRefGoogle Scholar
  64. 64.
    Koch B, Nielsen TH, Sorensen D et al. Lipopeptide production in Pseudomonas sp. strain DSS73 is regulated by components of sugar beet seed exudate via the Gac two-component regulatory system. Appl Environ Microbiol 2002; 68:4509–4516.PubMedCrossRefGoogle Scholar
  65. 65.
    Valverde C, Heeb S, Keel C et al. RsmY, a small regulatory RNA, is required in concert with RsmZ for GacA-dependent expression of biocontrol traits in Pseudomonas fluorescents CHAO. Mol Microbiol 2003; 50:1361–1379.PubMedCrossRefGoogle Scholar
  66. 66.
    Kay E, Dubuis C, Haas D. Three small RNAs jointly ensure secondary metabolism and biocontrol in Pseudomonas fluorescens CHA0. Proc Natl Acad Sci USA 2005; 102:17136–17141.PubMedCrossRefGoogle Scholar
  67. 67.
    Kulkarni PR, Cui X, Williams JW et al. Prediction of CsrA-regulating small RNAs in bacteria and their exprimental verification in Vibrio fischeri. Nucleic Acids Res 2006; 34:3361–3369.PubMedCrossRefGoogle Scholar
  68. 68.
    Blumer C, Heeb S, Pessi G et al. Global GacA-steered control of cyanide and exoprotease production in Pseudomonas fluorescens involves specific ribosome binding sites. Proc Natl Acad Sci USA 1999; 96;14073–14078.PubMedCrossRefGoogle Scholar
  69. 69.
    Reimmann C, Valverde C, Kay E et al. Posttranscriptional repression of GacS/GacA-controlled genes by the RNA-binding protein RsmE acting together with RsmA in the biocontrol strain Pseudomonas fluorescens CHAO. J Bacteriol 2005; 187:276–285.PubMedCrossRefGoogle Scholar
  70. 70.
    Heeb S, Valverde C, Gigot-Bonnefoy C et al. Role of the stress sigma factor RpoS in GacA/RsmA-controlled secondary metabolism and resistance to oxidative stress in Pseudomonas fluorescens CHAO. FEMS Microbiol Lett 2005; 243:251–258.PubMedCrossRefGoogle Scholar
  71. 71.
    Hrabak EM, Willis DK. 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 1992; 174:3011–3020.PubMedGoogle Scholar
  72. 72.
    Hrabak EM, Willis DK. Involvement of the lemA gene inproduction of syringomycin and protease by Pseudomonas syringae pv. syringae. Mol Plant Microbe Interact 1993; 6:368–375.Google Scholar
  73. 73.
    Rich JJ, Kinscherf TG, Kitten T et al. Genetic evidence that the gacA gene encodes the cognate response regulator for the lemA sensor in Pseudomonas syringae. J Bacteriol 1994; 176:7468–7475PubMedGoogle Scholar
  74. 74.
    Chatterjee A, Cui Y, Yang H et al. GacA, the response regulator of a two-component system, acts as a master regulator in Pseudomonas syringae pv. tomato DC3000 by controlling regulatory RNA, transcriptional activators and alternate sigma factors. Mol Plant Microbe Interact 2003; 16:1106–1117.PubMedCrossRefGoogle Scholar
  75. 75.
    Kitten T, Kinscherf TG, McEvoy JL et al. A newly identified regulator is required for virulence and toxin production in Pseudomonas syringae. Mol Microbiol 1998; 28:917–929.PubMedCrossRefGoogle Scholar
  76. 76.
    Lenz DH, Miller MB, Zhu J et al. OsrA and three redundant small RNAs regulate quorum sensing in Vibrio cholerae. Mol Microbiol 2005; 58:1186–1202.PubMedCrossRefGoogle Scholar
  77. 77.
    Rowley KB, Clements DE, Mandel M et al. Multiple copies of a DNA sequence from Pseudomonas syringae pathovar phaseolicola abolish thermoregulation of phaseolotoxin production. Mol Microbiol 1993; 8:625–635.PubMedCrossRefGoogle Scholar
  78. 78.
    Lazdunski AM, Ventre I, Sturgis JN. Regulatory circuits and communication in Gram-negative bacteria. Nat Rev Microbiol 2004; 2:581–592.PubMedCrossRefGoogle Scholar
  79. 79.
    Juhas M, Eberl L, Tümmler B. Quorum sensing: the power of cooperation in the world of Pseudomonas. Environ Microbiol 2005; 7:459–471.PubMedCrossRefGoogle Scholar
  80. 80.
    Diggle SP, Cornelis P, Williams P et al. 4-quinolone signalling in Pseudomonas aeruginosa: old molecules, new perspectives. Int J Med Microbiol 2006; 296:83–91.PubMedCrossRefGoogle Scholar
  81. 81.
    Heurlier K, Williams F, Heeb S et al. Positive control of swarming, rhamnolipid synthesis and lipase production by the posttranscriptional RsmA/RsmZ system in Pseudomonas aeruginosa PAO1. J Bacteriol 2004; 186:2936–2945.PubMedCrossRefGoogle Scholar
  82. 82.
    Burrowes E, Abbas A, O’Neill A et al. Characterisation of the regulatory RNA RsmB from Pseudomonas aeruginosa PAO1. Res Microbiol 2005; 156:7–16.PubMedCrossRefGoogle Scholar
  83. 83.
    Kay E, Humair B, Dénervaud V et al. Two GacA-dependent small RNAs modulate the quorum-sensing response in Pseudomonas aeruginosa. J Bacteriol 2006; 188:6026–633.PubMedCrossRefGoogle Scholar
  84. 84.
    Sonnleitner E, Schuster M, Sorger-Domenigg T et al. Hfq-dependent alterations of the transcriptome profile and effects on quorum sensing in Pseudomonas aeruginosa. Mol Microbiol 2006; 59:1542–1558.PubMedCrossRefGoogle Scholar
  85. 85.
    Mahajan-Miklos S, Rahme LG, Ausubel EM. Elucidating the molecular mechanisms of bacterial virulence using nonmammalian hosts. Mol Microbiol 2000; 37:981–988.PubMedCrossRefGoogle Scholar
  86. 86.
    Jander G, Rahme LG, Ausubel FM. Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol 2000; 182:3843–3845.PubMedCrossRefGoogle Scholar
  87. 87.
    Gallagher LA, Manoil C. Pseudomonas aeruginosa PAO1 kills Caenorhabditis elegans by cyanide poisoning. J Bacteriol 2001; 183:6207–6014.PubMedCrossRefGoogle Scholar
  88. 88.
    Reimmann C, Beyeler M, Latifi A et al. The global activator GacA of Pseudomonas aeruginosa PAO positively controls the production of the autoinducer N-butyryl-homoserine lactone and the formation of the virulence factors pyocyanin, cyanide and lipase. Mol Microbiol 1997; 24:309–319.PubMedCrossRefGoogle Scholar
  89. 89.
    Mahajan-Miklos S, Tan MW, Rahme LG et al. Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 1999; 96:47–56.PubMedCrossRefGoogle Scholar
  90. 90.
    Reimmann C, Ginet N, Michel L et al. Genetically programmed autoinducer destruction reduces virulence gene expression and swarming mobility in Pseudomonas aeruginosa PAO1. Microbiology 2002; 148:923–932.PubMedGoogle Scholar
  91. 91.
    Pessi G, Williams F, Hindle Z et al. The global posttranscriptional regulator RsmA modulates production of virulence determinants and N-acylhomoserine lactones in Pseudomonas aeruginosa. J Bacteriol 2001; 183:6676–6683.PubMedCrossRefGoogle Scholar
  92. 92.
    Pessi G, Haas D. Dual control of hydrogen cyanide biosynthesis by the global activator GacA in Pseudomonas aeruginosa PAO1. FEMS Microbiol Lett 2001; 200:73–78.PubMedCrossRefGoogle Scholar
  93. 93.
    Parkins MD, Ceri H, Storey DG. Pseudomonas aeruginosa GacA, a factor in multihost virulence, is also essential for biofilm formation. Mol Microbiol 2001; 40:1215–1226.PubMedCrossRefGoogle Scholar
  94. 94.
    Goodman AL, Kulasekara B, Rietsch A et al. A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell 2004; 7:745–754.PubMedCrossRefGoogle Scholar
  95. 95.
    Ventre I, Goodman AL, Vallet-Gely I et al. Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc Natl Acad Sci USA 2006; 103:171–176.PubMedCrossRefGoogle Scholar
  96. 96.
    Laskowski MA, Kazmierczak BI. Mutational analysis of RetS, an unusual sensor kinase-response regulator hybrid required for Pseudomonas aeruginosa virulence. Infect Immun 2006; 74:4462–4473.PubMedCrossRefGoogle Scholar
  97. 97.
    Zolfaghar I, Angus AA, Kang PJ et al. Mutation of retS, encoding a putative hybrid two-component regulatory protein in Pseudomonas aeruginosa, attenuates multiple virulence mechanisms. Microbes Infect 2005; 7:1305–1316.PubMedCrossRefGoogle Scholar
  98. 98.
    Zolfaghar I, Evans DJ, Ronaghi R et al. Type III secretion-dependent modulation of innate immunity as one of multiple factors regulated by Pseudomonas aeruginosa RetS. Infect Immun 2006; 74:3880–3889.PubMedCrossRefGoogle Scholar
  99. 99.
    Castañeda M, Guzman J, Moreno S et al. The GacS sensor kinase regulates alginate and poly-beta-hydroxybutyrate Production in Azobacter vinelandii. J Bacteriol 2000; 182:2624–2628.PubMedCrossRefGoogle Scholar
  100. 100.
    Castañeda M, Sánchez J, Moreno S et al. The global regulators GacA and sigma(S) form part of a cascade that controls alginate production in Azotobacter vinelandii. J Bacteriol 2001; 183:6787–6793.PubMedCrossRefGoogle Scholar
  101. 101.
    Mulcahy H, O’Callaghan J, O’Grady EP et al. The postransciptional regulator RamA plays a role in the interaction between Pscudomonas aerugionsa and human airway epithelial cells by positively regulating the type III secretion system. Infect Immun 2006; 74:3012–3015.PubMedCrossRefGoogle Scholar
  102. 102.
    Pernestig AK, Melefors O, Georgellis D. Identification of UvrY as the cognate response regulator for the BarA sensor kinase in Escherichia coli. J Biol Chem 2001; 276:225–231.PubMedCrossRefGoogle Scholar
  103. 103.
    Tomenius H, Pernestig AK, Mendez-Catala CF et al. Genetic and functional characterization of the Escherichia coli BarA-UvrY two-components system: point mutations in the HAMP linker of the BarA sensor give a dominant-negative phenotype. J Bacteriol 2005; 187:7317–7324.PubMedCrossRefGoogle Scholar
  104. 104.
    Nagasawa S, Tokishita S, Aiba H et al. A novel sensor-regulator protein that belongs to the homologous family of signal-transduction proteins involved in adaptive responses in Escherichia coli Mol Microbiol 1992; 6:799–807.PubMedCrossRefGoogle Scholar
  105. 105.
    Moolenaar GF, van Sluis CA, Backendorf C et al. Regulation of the Escherichia coli excision repair gene uvrC-overlap between the uvrC structural gene and the region coding for a 24 kD protein. Nucleic Acids Res 1987; 15:4273–4289.PubMedCrossRefGoogle Scholar
  106. 106.
    Ronen M, Rosenberg R, Shraiman BI et al. Assigning numbers to the arrows: parameterizing a gene regulation network by using accurate expression kineties. Proc Natl Acad Sci USA 2002; 99:10555–10560.PubMedCrossRefGoogle Scholar
  107. 107.
    Oshima T, Aiba H, Masuda Y et al. Transcriptome analysis of all two-component regulatory system mutants of Escherichia coli K-12. Mol Microbiol 2002; 46:281–291.PubMedCrossRefGoogle Scholar
  108. 108.
    Mukhopadhyay S, Audia JP, Roy RN et al. Transcriptional induction of the conserved alternative sigma factor RpoS in Escherichia coli is dependent on BarA, a probable two-component regulator. Mol Microbiol 2000; 37:371–381.PubMedCrossRefGoogle Scholar
  109. 109.
    Zhang JP, Normark S. Induction of gene expression in Escherichia coli after pilus-mediated adherence. Science 1996; 273:1234–1236.PubMedCrossRefGoogle Scholar
  110. 110.
    Tomenius H, Pernestig AK, Jonas K et al. The Escherichia coli BarA-UvrY two-component system is a virulence determinant in the urinary tract. BMC Microbiol 2006; 6:27.PubMedCrossRefGoogle Scholar
  111. 111.
    Johnston C, Pegues DA, Hueck CJ et al. Transcriptional activation of Salmonella typhimurium invasion genes by a member of the phosphorylated response-regulator superfamily. Mol Microbiol 1996; 22:715–727.PubMedCrossRefGoogle Scholar
  112. 112.
    Ahmer BM, van Recuwijk J, Watson PR et al. Salmonella SirA is a global regulator of genes medlating enteropathogenesis. Mol Microbiol 1999; 31:971–982.PubMedCrossRefGoogle Scholar
  113. 113.
    Goodier RI, Ahmer BM. SirA orthologs affect both motility and virulence. J Bacteriol 2001; 183:2249–2258.PubMedCrossRefGoogle Scholar
  114. 114.
    Altier C, Suyemoto M, Lawhon SD. Regulation of Salmonella enterica serovar typhimurium invasion genes by csrA. Infect Immun 2000; 68:6790–6797.PubMedCrossRefGoogle Scholar
  115. 115.
    Lawhon SD, Maurer R, Suyemoto M et al. Intestinal short-chain fatty acids alter Salmonella typhimurium invasion gene expression and virulence through BarA/SirA. Mol Microbiol 2002; 46:1451–1464.PubMedCrossRefGoogle Scholar
  116. 116.
    Weilbacher T, Suzuki K, Dubey AK et al. A novel sRNA component of the carbon storage regulatory system of Escherichia coli. Mol Microbiol 2003; 48:657–670.PubMedCrossRefGoogle Scholar
  117. 117.
    Fortune DR, Suyemoto M, Altier C. Identification of CsrC and characterization of its role in epithelial cell invasion in Salmonella enterica serovar typhimurium. Infect Immun 2006; 74:331–339.PubMedCrossRefGoogle Scholar
  118. 118.
    Wassarman KM, Repoila F, Rosenow C et al. Identification of novel small RNAs using comparative genomies and microrrays. Genes Dev 2001; 15:1637–1651.PubMedCrossRefGoogle Scholar
  119. 119.
    Teplitski M, Goodier RI, Ahmer BM. Pathways leading from BarA/SirA to motility and virulence gene expression in Salmonella. J Bacteriol 2003; 185:7257–7265.PubMedCrossRefGoogle Scholar
  120. 120.
    Teplitski M, Goodier RI, Ahmer BM. Catabolite repression of the SirA regulatory cascade in Salmonella enterica. Int J Med Microbiol 2006; 296:449–466.PubMedCrossRefGoogle Scholar
  121. 121.
    Suzuki K, Wang X, Weilbacher T et al. Regulatory circultry of the CsrA/CsrB and BarA/UvrY systems of Escherichia coli. J Bacteriol 2002; 184:5130–5140.PubMedCrossRefGoogle Scholar
  122. 122.
    Prouty AM, Gunn JS. Salmonella enterica serovar typhimurium invasion is repressed in the presence of bile. Infect Immun 2000; 68:6763–6769.PubMedCrossRefGoogle Scholar
  123. 123.
    Lawhon SD, Frye JG, Suyemoto M et al. Global regulation by CsrA in Salmonella typhimurium. Mol Microbiol 2003; 48:1633–1645.PubMedCrossRefGoogle Scholar
  124. 124.
    Ellermeier CD, Ellermeier JR, Slauch JM, HilD, HilC and RtsA constitute a feed forward loop that controls expression of the SPI1 type three secretion system regulator hilA a Salmonella enterica serovar typhimurium. Mol Microbiol 2005; 57:691–705.PubMedCrossRefGoogle Scholar
  125. 125.
    Altler C. Genetic and environmental control of Salmonella invasion. J Microbiol 2005; 43:85–92.Google Scholar
  126. 126.
    Liu MY, Romeo T. The global regulator CsrA of Escherichia coli is a specific mRNA-binding protein. J Bacteriol 1997; 179:4639–4642.PubMedGoogle Scholar
  127. 127.
    Baker CS, Morozov I, Suzuki K et al. CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli. Mol Microbiol 2002; 44:1599–1610.PubMedCrossRefGoogle Scholar
  128. 128.
    Wang X, Preston JF 3rd, Romeo T. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J Bacteriol 2004; 186:2724–2734.PubMedCrossRefGoogle Scholar
  129. 129.
    Wang X, Dubey AK, Suzuki K et al. CsrA posttranscriptionally represses pgaABCD, responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli. Mol Microbiol 2005; 56:1648–1663.PubMedCrossRefGoogle Scholar
  130. 130.
    Dubey AK, Baker CS, Suzuki K et al. CsrA regulates translation of the Escherichia coli carbon starvation gene, cstA, by blocking ribosome access to the cstA transcript J Bacteriol 2003; 185:4450–4460.PubMedCrossRefGoogle Scholar
  131. 131.
    Jackson DW, Suzuki K, Oakford L et al. Biofilm formation and dispersal under the influence of the glogal regulator CsrA of Escherichia coli. J Bacteriol 2002; 184:3406–3410.PubMedCrossRefGoogle Scholar
  132. 132.
    Murray EL, Conway T. Multiple regulators control expression of the Entner-Doudoroff aldolase (Eda) of Escherichia coli. J Bacteriol 2005; 187:991–1000.PubMedCrossRefGoogle Scholar
  133. 133.
    Gudapaty S, Suzuki K, Wang X et al. Regulatory interactions of Csr components: the RNA binding protein CsrA activates csrB transcription in Escherichia coli. J Bacteriol 2001; 183:6017–6027.PubMedCrossRefGoogle Scholar
  134. 134.
    Pernestig AK, Georgellis D, Romeo T et al The Escherichia coli BarA-UvrY two-component system is needed for efficient switching between glycolytic and gluconeogenic carbon sources. J Bacteriol 2003; 185:843–853.PubMedCrossRefGoogle Scholar
  135. 135.
    Frederick RD, Chiu J, Bennetzen JL et al. Indentification of a pathogenicity locus, rpfA, in Erwinia carotovora subsp, carotovora that encodes a two-component sensor-regulator protein. Mol Plant Microbe Interact 1997; 10:407–415.PubMedCrossRefGoogle Scholar
  136. 136.
    Eriksson AR, Andersson RA, Pirhonen M et al. Two-component regulators involved in the global control of virulence in Erwinia carotovora subsp, carotovora. Mol Plant Microbe Interact 1998; 11:743–752.PubMedCrossRefGoogle Scholar
  137. 137.
    Cui Y, Chatterjee A, Chatterjee AK. Effects of the two-component system comprising GacA and GacS of Erwinia carotovora subsp. carotovora ont he production of global regulatory rsmB RNA, extracellular enzymes and HarpinEce. Mol Plant Microbe Interact 2001; 14:516–526.PubMedCrossRefGoogle Scholar
  138. 138.
    Liu Y, Cui Y, Mukherjee A et al. Characterization of a novel RNA regulator of Erwinia carotovora ssp. carotovora that controls production of extracellular enzymes and secondary metabolites. Mol Microbiol 1998; 29:219–234.PubMedCrossRefGoogle Scholar
  139. 139.
    Ma W, Cui Y, Liu Y et al. Molecular characterization of global regulatory RNA species that control pathogenicity factors in Erwinia amylovora and Erwinia herbicola pv. gypsophilae. J Bacteriol 2001; 183:1870–1880.PubMedCrossRefGoogle Scholar
  140. 140.
    Cui Y, Mukherjee A, Dumenyo CK et al. rsmC of the soft-rotting bacterium Erwinia carotovora subsp, carotovora negatively controls extracelular enzyme and Harpin (Ecc) production and virulence by modulating levels of regulatory RNA (rsmB) and RNA-binding protein (RsmA). J Bacteriol 1999; 181:6042–6052.PubMedGoogle Scholar
  141. 141.
    Liu Y, Jiang G, Cui Y et al. kdgREcc negatively regulates genes for pectinases, cellulase, protease, HarpinEcc and a global RNA regulator in Erwinia carotovora subsp, carotovora. J Bacteriol 1999; 181:2411–2421.PubMedGoogle Scholar
  142. 142.
    Mukherjee A, Cui Y, Ma W et al. hexA of Erwinia carotovora ssp. carotovora strain Ecc71 negatively regulates production of RpoS and rsmB RNA, a global regulator of extracellular proteins, plant virulence regulates production of RpoS and rsmB RNA, a global regulator of extracellular proteins, plant virulence and the quorum-sensing signal, N-(3-oxohexanoyl)-L-homoserine lactone. Environ Microbiol 2000; 2:203–215.PubMedCrossRefGoogle Scholar
  143. 143.
    Cui Y, Chatterjee A, Hasegawa H et al. Erwinia carotovora subspecies produce duplicate variants of ExpR, LuxR homologs that activate rsmA transcription but differ in their interactions with N-acylhomoserine lactone signals. J Bacteriol 2006; 188:4715–4726.PubMedCrossRefGoogle Scholar
  144. 144.
    Chatterjee A, Cui Y, Liu Y et al. Inactivation of rsmA leads to overproduction of extracellular pectinases, cellulases and proteases in Erwinia carotovora subsp. carotovora in the absence of the starvation/cell density-sensing signal, N-(3-oxohexanoyl)-L-homoserine lactone. Appl Envion Microbiol 1995; 61:1959–1967.Google Scholar
  145. 145.
    Cui Y, Chatterjee A, Liu Y et al. Identification of a global repressor gene, rsmA, of Erwiia carotovora subsp. carotovora that controls extracellular enzymes N-(3-oxohexanoyl)-L-homoserine lactone and pathogenicity in soft-rotting Erwinia spp. J Bacteriol 1995; 177:5108–5115.PubMedGoogle Scholar
  146. 146.
    Chatterjee A, Cui Y, Chatterjee AK. RsmA and the quorum-sensing signal, N-(3-oxohexanoyl)-L-homoserine lactone, control the levels of rsmB RNA in Erwinia carotovora subsp. carotovora by affecting its stability. J Bacteriol 2002; 184:4089–4095.PubMedCrossRefGoogle Scholar
  147. 147.
    Pemberton CL, Whitehead NA, Sebaihia M et al. Novel quorum-sensing-controlled genes in Erwinia carotovora subsp. carotovora: identification of a fungal elicitor homologue in a soft-rotting bacterium. Mol Plant Microbe Interact 2005; 18:343–353.PubMedCrossRefGoogle Scholar
  148. 148.
    Murata H, Chatterjee A, Liu Y et al. Regulation of the production of extracellular pectinase, cellulase and protease in the soft rot bacterium Erwinia carotovora subsp. carotovora: evidence that aepH of E. carotovora subsp. carotovora 71 activates gene expression in E. carotovora subsp. carotovora, E. carotovora subsp. atroseptica and Escherichia coli. Appl Environ Microbiol 1994; 60:3150–3159.PubMedGoogle Scholar
  149. 149.
    Lenz DH, Mok KC, Lilley BN et al. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 2004; 118:69–82.PubMedCrossRefGoogle Scholar
  150. 150.
    Wong SM, Carroll PA, Rahme LG et al. Modulation of expression of the ToxR regulon in Vibrio cholerae by a member of the two-component family of response regulators. Infect Immun 1998; 66:5854–5861.PubMedGoogle Scholar
  151. 151.
    Lenz DH, Bassler BL. The small nucleoid protein Fis is involved in Vibrio cholerae quorum sensing. Mol Microbiol 2007; 63:859–871.PubMedCrossRefGoogle Scholar
  152. 152.
    Dorsey CW, Tomaras AP, Actis LA. Genetic and phenotypic analysis of Acinetobacter baumaniilinsertion derivatives generated with a transposome system. Appl Environ Microbiol 2002; 68:6353–6360.PubMedCrossRefGoogle Scholar
  153. 153.
    Hammer BK, Tateda ES, Swanson MS. At two-component regulator induces the transmission phenotype of stationary-phase Legionella pneumophila. Mol Microbiol 2002; 44:107–118.PubMedCrossRefGoogle Scholar
  154. 154.
    Molofsky AB, Swanson MS. Legionella pneumophila CsrA is a pivotal repressor of transmission traits and activator of replication. Mol Microbiol 2003; 50:445–461.PubMedCrossRefGoogle Scholar
  155. 155.
    Kang BR, Cho BH, Anderson AJ et al. The global regulator GacS of a biocontrol bacterium Pseudomonas cholororaphis O6 regulates transcription from the rpoS gene encoding a stationary-phase sigma factor and affects survival in oxidative stress. Gene 2004; 325:137–143.PubMedCrossRefGoogle Scholar
  156. 156.
    Han SH, Lee SJ, Moon JH et al. GacS-dependent production of 2R,3R-butanediol by Pseudomonas chloraphis O6 is a major determinant for eliciting systemic resistance against Erwinia carotovora but not against Pseudomonas syringae pv. tabaci in tobacco. Mol Plant Microbe Interact 2006; 19:924–930.PubMedCrossRefGoogle Scholar
  157. 157.
    Chin-A-Woeng TF, van den Broek D, Lugtenberg BJ et al. The Pseudomonas chlororaphis PCL1391 sigma regulator psrA represses the production of the antifungal metabolite phenazine-1-carboxamide. Mol Plant Microbe Interact 2005; 18:244–253.PubMedCrossRefGoogle Scholar
  158. 158.
    Girard G, van Rij ET, Lugtenberg BJ et al. Regulatory roles of psrA and rpoS in phenazine-1-carboxamide synthesis by Pseudomonas chlororaphis PCL1391. Microbiology 2006; 152:43–58.PubMedCrossRefGoogle Scholar
  159. 159.
    Dubern JF, Bloemberg GV. Influence of environmental conditions on putisolvins I and II production in Pseudomonas putida strain PCL1445. FEMS Microbiol Lett 2006; 263:169–175.PubMedCrossRefGoogle Scholar
  160. 160.
    Schmidt-Eisenlohr H, Gast A, Baron C. Inactivation of gacS does not affect the competitiveness of Pseudomonas chlororaphis, in the Arabidopsis thaliana rhizosphere. Appl. Environ Microbiol 2003; 69: 1817–1826.PubMedCrossRefGoogle Scholar
  161. 161.
    Vodovar N, Vallenet D, Cruveiller S et al. Complete genome sequence of the entomopathogenic and metabolically versatile soil bacterium Pseudomonas entomophila. Nat Biotechnol 2006; 24:673–679.PubMedCrossRefGoogle Scholar
  162. 162.
    Jousset A, Lara E, Wall LG et al. Secondary metabolites help biocontrol strain Pseudomonas fluorescens CHAO to escape protozoan grazing. Appl Environ Microbiol 2006; 72:7083–7090.PubMedCrossRefGoogle Scholar
  163. 163.
    Sánchez-Contreras M, Martín M, Villacicros M et al. Phenotypic selection and phase variation occur during alfalfa root colonization by Pseudomonas fluorescens F113. J Bacteriol 2002; 184:1587–1596.PubMedCrossRefGoogle Scholar
  164. 164.
    Martinez-Granero F, Rivilla R, Martin M. Rhizosphere selection of highly motile phenotypic variants of Pseudomonas fluorescens with enhanced competitive colonization ability. Appl Environ Microbiol 2006; 72:3429–3434.PubMedCrossRefGoogle Scholar
  165. 165.
    Ge Y, Huang X, Wang S et al. Phenazine-1-carboxylic acid is negatively regulated and pyoluteorin positively regulated by gacA in Pseudomonas sp. M18. FEMS Microbiol Lett 2004; 237:41–47.PubMedCrossRefGoogle Scholar
  166. 166.
    van den Broek D, Chin-A-Woeng TF, Bloemberg GV et al. Molecular nature of spontaneous modifications in gacS which cause colony phase variation in Pseudomonas sp. strain PCL1171. J Bacteriol 2005; 187:593–600.PubMedCrossRefGoogle Scholar
  167. 167.
    Kang BR, Yang KY, Cho BH et al. Production of indole-3-acetic acid in the plant-beneficial strain Pseudomonas chlororaphis O6 is negatively regulated by the global sensor kinase Gacs. Curr Microbiol 2006; 52:473–476PubMedCrossRefGoogle Scholar
  168. 168.
    Dubern JF, Lagendijk EL, Lugtenberg BJ et al. The heat shock genes dnaK, dnaJ and grpE are involved in regulation of putisolvin biosynthesis in Pseudomonas putida PCL1445. J Bacteriol 2005; 187:5967–5976.PubMedCrossRefGoogle Scholar
  169. 169.
    Kang H, Gross DC. Characterization of a resistance-nodulation-cell division transporter system associated with the syr-syp genomic island of Pseudomonas syringae pv. syringae. Appl Environ Microbiol 2005; 71:5056–5065.PubMedCrossRefGoogle Scholar
  170. 170.
    Quinones B, Pujol CJ, Lindow SE. Regulation of AHL production and its contribution to epiphytic fitness in Pseudomonas syringae. Mol Plant Microbe Interact 2004; 17:521–531.PubMedCrossRefGoogle Scholar
  171. 171.
    Ovadis M, Liu X, Gavriel S et al. The global regulator genes from biocontrol strain Serratia plymuthica IC1270: cloning, sequencing and functional studies. J Bacteriol 2004; 186:4986–4993.PubMedCrossRefGoogle Scholar
  172. 172.
    Williamson NR, Fineran PC, Leeper FJ et al. The biosynthesis and regulation of bacterial prodignines. Nat Rev Microbiol 2006; 4:887–899.PubMedCrossRefGoogle Scholar
  173. 173.
    Whistler CA, Ruby EG. GacA regulates symbiotic colonization traits of Vibrio fischeri and facilitates a beneficial association with an animal host. J Bacteriol 2003; 185:7202–7212.PubMedCrossRefGoogle Scholar
  174. 174.
    Majdalani N, Gottesman S. The Res phosphorelay: a complex signal transduction system. Annu Rev Microbiol 2005; 59:379–405.PubMedCrossRefGoogle Scholar
  175. 175.
    Majdalani N, Hernandez D, Gottesman S. Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 2002; 46:813–826.PubMedCrossRefGoogle Scholar
  176. 176.
    Shimizu T, Yaguchi H, Ohtani K et al. Clostridial VirR/VirS regulon involves a regulatory RNA molecule for expression of toxins. Mol Microbiol 2002; 43:257–265.PubMedCrossRefGoogle Scholar
  177. 177.
    Ohtani K, Kawsar HI, Okumura K et al. The VirR/VirS regulatory cascade affects transcription of plasmid-encoded putative virulence genes in Clostridium perfringens strain 13. FEMS Microbiol Lett 2003; 222:137–141.PubMedCrossRefGoogle Scholar
  178. 178.
    Okumura K, Kawsar HI, Shimizu T et al. Identification and characterization of a cell-wall anchored DNase gene in Clostridium perfringens. FEMS Microbiol Lett 2005; 242:281–285.PubMedCrossRefGoogle Scholar
  179. 179.
    Silvaggi JM, Perkins JB, Losick R. Genes for small, noncoding RNAs under sporulation control in Bacillus subtilis. J Bacteriol 2006; 188:532–541.PubMedCrossRefGoogle Scholar
  180. 180.
    Kreikemeyer B, Boyle MD, Buttaro BA et al. Group A streptococcal growth phase-associated virulence factor regulation by a novel operon (Fas) with homologies to two-component-type regulators requires a small RNA molecule. Mol. Microbiol 2001; 39:392–406.PubMedCrossRefGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2008

Authors and Affiliations

  1. 1.Département de Microbiologie FondamentaleUniversité de LausanneLausanneSwitzerland
  2. 2.Program Interacciones Biológicas, Departamento de Ciencia y TecnologíaUniversidad Nacional de QuilmesBernalArgentina

Personalised recommendations