Skip to main content
Log in

Post-transcriptional global regulation by CsrA in bacteria

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Global regulation allows bacteria to rapidly modulate the expression of a large variety of unrelated genes in response to environmental changes. Global regulators act at different levels of gene expression. This review focuses on CsrA, a post-transcriptional regulator that affects translation of its gene targets by binding mRNAs. CsrA controls a large variety of physiological processes such as central carbon metabolism, motility and biofilm formation. The activity of CsrA is itself tightly regulated by the CsrB and CsrC small RNAs and the BarA-UvrY two-component system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Magnusson LU, Farewell A, Nystrom T (2005) ppGpp: a global regulator in Escherichia coli. Trends Microbiol 13:236–242

    Article  PubMed  CAS  Google Scholar 

  2. Dougan DA, Mogk A, Bukau B (2002) Protein folding and degradation in bacteria: to degrade or not to degrade? That is the question. Cell Mol Life Sci 59:1607–1616

    Article  PubMed  CAS  Google Scholar 

  3. Carmel-Harel O, Storz G (2000) Roles of the glutathione- and thioredoxin-dependent reduction systems in the Escherichia coli and Saccharomyces cerevisiae responses to oxidative stress. Annu Rev Microbiol 54:439–461

    Article  PubMed  CAS  Google Scholar 

  4. Fujita Y (2009) Carbon catabolite control of the metabolic network in Bacillus subtilis. Biosci Biotechnol Biochem 73:245–259

    Article  PubMed  CAS  Google Scholar 

  5. Campbell EA, Greenwell R, Anthony JR, Wang S, Lim L, Das K, Sofia HJ, Donohue TJ, Darst SA (2007) A conserved structural module regulates transcriptional responses to diverse stress signals in bacteria. Mol Cell 27:793–805

    Article  PubMed  CAS  Google Scholar 

  6. Giuliodori AM, Gualerzi CO, Soto S, Vila J, Tavio MM (2007) Review on bacterial stress topics. Ann N Y Acad Sci 1113:95–104

    Article  PubMed  CAS  Google Scholar 

  7. Gorke B, Stulke J (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6:613–624

    Article  PubMed  CAS  Google Scholar 

  8. Marles-Wright J, Lewis RJ (2007) Stress responses of bacteria. Curr Opin Struct Biol 17:755–760

    Article  PubMed  CAS  Google Scholar 

  9. Gottesman S (1984) Bacterial regulation: global regulatory networks. Annu Rev Genet 18:415–441

    Article  PubMed  CAS  Google Scholar 

  10. Nogueira T, Springer M (2000) Post-transcriptional control by global regulators of gene expression in bacteria. Curr Opin Microbiol 3:154–158

    Article  PubMed  CAS  Google Scholar 

  11. Gruber TM, Gross CA (2003) Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57:441–466

    Article  PubMed  CAS  Google Scholar 

  12. Potvin E, Sanschagrin F, Levesque RC (2008) Sigma factors in Pseudomonas aeruginosa. FEMS Microbiol Rev 32:38–55

    Article  PubMed  CAS  Google Scholar 

  13. Kroos L (2007) The Bacillus and Myxococcus developmental networks and their transcriptional regulators. Annu Rev Genet 41:13–39

    Article  PubMed  CAS  Google Scholar 

  14. Atlung T, Ingmer H (1997) H-NS: a modulator of environmentally regulated gene expression. Mol Microbiol 24:7–17

    Article  PubMed  CAS  Google Scholar 

  15. Jauregui R, Abreu-Goodger C, Moreno-Hagelsieb G, Collado-Vides J, Merino E (2003) Conservation of DNA curvature signals in regulatory regions of prokaryotic genes. Nucleic Acids Res 31:6770–6777

    Article  PubMed  CAS  Google Scholar 

  16. Lang B, Blot N, Bouffartigues E, Buckle M, Geertz M, Gualerzi CO, Mavathur R, Muskhelishvili G, Pon CL, Rimsky S, Stella S, Babu MM, Travers A (2007) High-affinity DNA binding sites for H-NS provide a molecular basis for selective silencing within proteobacterial genomes. Nucleic Acids Res 35:6330–6337

    Article  PubMed  CAS  Google Scholar 

  17. Yamada H, Muramatsu S, Mizuno T (1990) An Escherichia coli protein that preferentially binds to sharply curved DNA. J Biochem 108:420–425

    PubMed  CAS  Google Scholar 

  18. Bertin P, Hommais F, Krin E, Soutourina O, Tendeng C, Derzelle S, Danchin A (2001) H-NS and H-NS-like proteins in Gram-negative bacteria and their multiple role in the regulation of bacterial metabolism. Biochimie 83:235–241

    Article  PubMed  CAS  Google Scholar 

  19. Olsen PB, Schembri MA, Gally DL, Klemm P (1998) Differential temperature modulation by H-NS of the fimB and fimE recombinase genes which control the orientation of the type 1 fimbrial phase switch. FEMS Microbiol Lett 162:17–23

    Article  PubMed  CAS  Google Scholar 

  20. Schembri MA, Olsen PB, Klemm P (1998) Orientation-dependent enhancement by H-NS of the activity of the type 1 fimbrial phase switch promoter in Escherichia coli. Mol Gen Genet 259:336–344

    Article  PubMed  CAS  Google Scholar 

  21. Muller CM, Dobrindt U, Nagy G, Emody L, Uhlin BE, Hacker J (2006) Role of histone-like proteins H-NS and StpA in expression of virulence determinants of uropathogenic Escherichia coli. J Bacteriol 188:5428–5438

    Article  PubMed  CAS  Google Scholar 

  22. Bertin P, Terao E, Lee EH, Lejeune P, Colson C, Danchin A, Collatz E (1994) The H-NS protein is involved in the biogenesis of flagella in Escherichia coli. J Bacteriol 176:5537–5540

    PubMed  CAS  Google Scholar 

  23. Ko M, Park C (2000) Two novel flagellar components and H-NS are involved in the motor function of Escherichia coli. J Mol Biol 303:371–382

    Article  PubMed  CAS  Google Scholar 

  24. Landini P, Zehnder AJ (2002) The global regulatory hns gene negatively affects adhesion to solid surfaces by anaerobically grown Escherichia coli by modulating expression of flagellar genes and lipopolysaccharide production. J Bacteriol 184:1522–1529

    Article  PubMed  CAS  Google Scholar 

  25. Bruckner R, Titgemeyer F (2002) Carbon catabolite repression in bacteria: choice of the carbon source and autoregulatory limitation of sugar utilization. FEMS Microbiol Lett 209:141–148

    Article  PubMed  CAS  Google Scholar 

  26. Pruss BM, Besemann C, Denton A, Wolfe AJ (2006) A complex transcription network controls the early stages of biofilm development by Escherichia coli. J Bacteriol 188:3731–3739

    Article  PubMed  CAS  Google Scholar 

  27. Gutierrez-Rios RM, Freyre-Gonzalez JA, Resendis O, Collado-Vides J, Saier M, Gosset G (2007) Identification of regulatory network topological units coordinating the genome-wide transcriptional response to glucose in Escherichia coli. BMC Microbiol 7:53

    Article  PubMed  CAS  Google Scholar 

  28. De Lay N, Gottesman S (2009) The Crp-activated small noncoding regulatory RNA CyaR (RyeE) links nutritional status to group behavior. J Bacteriol 191:461–476

    Article  PubMed  CAS  Google Scholar 

  29. Muller CM, Aberg A, Straseviciene J, Emody L, Uhlin BE, Balsalobre C (2009) Type 1 fimbriae, a colonization factor of uropathogenic Escherichia coli, are controlled by the metabolic sensor CRP-cAMP. PLoS Pathog 5:e1000303

    Article  PubMed  CAS  Google Scholar 

  30. Zheng D, Constantinidou C, Hobman JL, Minchin SD (2004) Identification of the CRP regulon using in vitro and in vivo transcriptional profiling. Nucleic Acids Res 32:5874–5893

    Article  PubMed  CAS  Google Scholar 

  31. Gottesman S (2005) Micros for microbes: non-coding regulatory RNAs in bacteria. Trends Genet 21:399–404

    Article  PubMed  CAS  Google Scholar 

  32. Vanderpool CK, Gottesman S (2004) Involvement of a novel transcriptional activator and small RNA in post-transcriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system. Mol Microbiol 54:1076–1089

    Article  PubMed  CAS  Google Scholar 

  33. 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 U S A 104:20454–20459

    Article  PubMed  CAS  Google Scholar 

  34. Majdalani N, Vanderpool CK, Gottesman S (2005) Bacterial small RNA regulators. Crit Rev Biochem Mol Biol 40:93–113

    Article  PubMed  CAS  Google Scholar 

  35. Babitzke P, Romeo T (2007) CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 10:156–163

    Article  PubMed  CAS  Google Scholar 

  36. Doyle SM, Wickner S (2009) Hsp104 and ClpB: protein disaggregating machines. Trends Biochem Sci 34:40–48

    Article  PubMed  CAS  Google Scholar 

  37. Hengge R (2009) Proteolysis of sigmaS (RpoS) and the general stress response in Escherichia coli. Res Microbiol 160:667–676

    Article  PubMed  CAS  Google Scholar 

  38. Van Melderen L, Aertsen A (2009) Regulation and quality control by Lon-dependent proteolysis. Res Microbiol 160:645–651

    Article  PubMed  CAS  Google Scholar 

  39. Barembruch C, Hengge R (2007) Cellular levels and activity of the flagellar sigma factor FliA of Escherichia coli are controlled by FlgM-modulated proteolysis. Mol Microbiol 65:76–89

    Article  PubMed  CAS  Google Scholar 

  40. Heuveling J, Possling A, Hengge R (2008) A role for Lon protease in the control of the acid resistance genes of Escherichia coli. Mol Microbiol 69:534–547

    Article  PubMed  CAS  Google Scholar 

  41. Klauck E, Typas A, Hengge R (2007) The sigmaS subunit of RNA polymerase as a signal integrator and network master regulator in the general stress response in Escherichia coli. Sci Prog 90:103–127

    PubMed  CAS  Google Scholar 

  42. Bougdour A, Cunning C, Baptiste PJ, Elliott T, Gottesman S (2008) Multiple pathways for regulation of sigmaS (RpoS) stability in Escherichia coli via the action of multiple anti-adaptors. Mol Microbiol 68:298–313

    Article  PubMed  CAS  Google Scholar 

  43. Gottesman S (2003) Proteolysis in bacterial regulatory circuits. Annu Rev Cell Dev Biol 19:565–587

    Article  PubMed  CAS  Google Scholar 

  44. Romeo T, Gong M, Liu MY, Brun-Zinkernagel AM (1993) Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J Bacteriol 175:4744–4755

    PubMed  CAS  Google Scholar 

  45. Timmermans J, Van Melderen L (2009) Conditional essentiality of the csrA gene in Escherichia coli. J Bacteriol 191:1722–1724

    Article  PubMed  CAS  Google Scholar 

  46. Baker CS, Morozov I, Suzuki K, Romeo T, Babitzke P (2002) CsrA regulates glycogen biosynthesis by preventing translation of glgC in Escherichia coli. Mol Microbiol 44:1599–1610

    Article  PubMed  CAS  Google Scholar 

  47. Dubey AK, Baker CS, Romeo T, Babitzke P (2005) RNA sequence and secondary structure participate in high-affinity CsrA-RNA interaction. RNA 11:1579–1587

    Article  PubMed  CAS  Google Scholar 

  48. Dubey AK, Baker CS, Suzuki K, Jones AD, Pandit P, Romeo T, Babitzke P (2003) CsrA regulates translation of the Escherichia coli carbon starvation gene, cstA, by blocking ribosome access to the cstA transcript. J Bacteriol 185:4450–4460

    Article  PubMed  CAS  Google Scholar 

  49. Liu MY, Romeo T (1997) The global regulator CsrA of Escherichia coli is a specific mRNA-binding protein. J Bacteriol 179:4639–4642

    PubMed  CAS  Google Scholar 

  50. Liu MY, Yang H, Romeo T (1995) The product of the pleiotropic Escherichia coli gene csrA modulates glycogen biosynthesis via effects on mRNA stability. J Bacteriol 177:2663–2672

    PubMed  CAS  Google Scholar 

  51. Romeo T (1996) Post-transcriptional regulation of bacterial carbohydrate metabolism: evidence that the gene product CsrA is a global mRNA decay factor. Res Microbiol 147:505–512

    Article  PubMed  CAS  Google Scholar 

  52. Yang H, Liu MY, Romeo T (1996) Coordinate genetic regulation of glycogen catabolism and biosynthesis in Escherichia coli via the CsrA gene product. J Bacteriol 178:1012–1017

    PubMed  CAS  Google Scholar 

  53. Baker CS, Eory LA, Yakhnin H, Mercante J, Romeo T, Babitzke P (2007) CsrA inhibits translation initiation of Escherichia coli hfq by binding to a single site overlapping the Shine-Dalgarno sequence. J Bacteriol 189:5472–5481

    Article  PubMed  CAS  Google Scholar 

  54. Jonas K, Edwards AN, Simm R, Romeo T, Romling U, Melefors O (2008) The RNA binding protein CsrA controls cyclic di-GMP metabolism by directly regulating the expression of GGDEF proteins. Mol Microbiol 70:236–257

    Article  PubMed  CAS  Google Scholar 

  55. Mercante J, Suzuki K, Cheng X, Babitzke P, Romeo T (2006) Comprehensive alanine-scanning mutagenesis of Escherichia coli CsrA defines two subdomains of critical functional importance. J Biol Chem 281:31832–31842

    Article  PubMed  CAS  Google Scholar 

  56. 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 14:807–813

    Article  PubMed  CAS  Google Scholar 

  57. Sorger-Domenigg T, Sonnleitner E, Kaberdin VR, Blasi U (2007) Distinct and overlapping binding sites of Pseudomonas aeruginosa Hfq and RsmA proteins on the non-coding RNA RsmY. Biochem Biophys Res Commun 352:769–773

    Article  PubMed  CAS  Google Scholar 

  58. Wang X, Dubey AK, Suzuki K, Baker CS, Babitzke P, Romeo T (2005) CsrA post-transcriptionally represses pgaABCD, responsible for synthesis of a biofilm polysaccharide adhesin of Escherichia coli. Mol Microbiol 56:1648–1663

    Article  PubMed  CAS  Google Scholar 

  59. Yakhnin H, Pandit P, Petty TJ, Baker CS, Romeo T, Babitzke P (2007) CsrA of Bacillus subtilis regulates translation initiation of the gene encoding the flagellin protein (hag) by blocking ribosome binding. Mol Microbiol 64:1605–1620

    Article  PubMed  CAS  Google Scholar 

  60. Jonas K, Edwards AN, Ahmad I, Romeo T, Romling U, Melefors O (2010) Complex regulatory network encompassing the Csr, c-di-GMP and motility systems of Salmonella typhimurium. Environ Microbiol 12:524–540

    Article  PubMed  CAS  Google Scholar 

  61. Bhatt S, Edwards AN, Nguyen HT, Merlin D, Romeo T, Kalman D (2009) The RNA binding protein CsrA is a pleiotropic regulator of the locus of enterocyte effacement pathogenicity island of enteropathogenic Escherichia coli. Infect Immun 77:3552–3568

    Article  PubMed  CAS  Google Scholar 

  62. Wei BL, Brun-Zinkernagel AM, Simecka JW, Pruss BM, Babitzke P, Romeo T (2001) Positive regulation of motility and flhDC expression by the RNA-binding protein CsrA of Escherichia coli. Mol Microbiol 40:245–256

    Article  PubMed  CAS  Google Scholar 

  63. Liu MY, Gui G, Wei B, Preston JF 3rd, Oakford L, Yuksel U, Giedroc DP, Romeo T (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

    Article  PubMed  CAS  Google Scholar 

  64. Suzuki K, Wang X, Weilbacher T, Pernestig AK, Melefors O, Georgellis D, Babitzke P, Romeo T (2002) Regulatory circuitry of the CsrA/CsrB and BarA/UvrY systems of Escherichia coli. J Bacteriol 184:5130–5140

    Article  PubMed  CAS  Google Scholar 

  65. Weilbacher T, Suzuki K, Dubey AK, Wang X, Gudapaty S, Morozov I, Baker CS, Georgellis D, Babitzke P, Romeo T (2003) A novel sRNA component of the carbon storage regulatory system of Escherichia coli. Mol Microbiol 48:657–670

    Article  PubMed  CAS  Google Scholar 

  66. Ang S, Horng YT, Shu JC, Soo PC, Liu JH, Yi WC, Lai HC, Luh KT, Ho SW, Swift S (2001) The role of RsmA in the regulation of swarming motility in Serratia marcescens. J Biomed Sci 8:160–169

    PubMed  CAS  Google Scholar 

  67. Brencic A, Lory S (2009) Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol Microbiol 72:612–632

    Article  PubMed  CAS  Google Scholar 

  68. 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 152:405–418

    Article  PubMed  CAS  Google Scholar 

  69. Chao NX, Wei K, Chen Q, Meng QL, Tang DJ, He YQ, Lu GT, Jiang BL, Liang XX, Feng JX, Chen B, Tang JL (2008) The rsmA-like gene rsmA(Xcc) of Xanthomonas campestris pv. campestris is involved in the control of various cellular processes, including pathogenesis. Mol Plant Microbe Interact 21:411–423

    Article  PubMed  CAS  Google Scholar 

  70. Gaskell AA, Crack JC, Kelemen GH, Hutchings MI, Le Brun NE (2007) RsmA is an anti-sigma factor that modulates its activity through a [2Fe-2S] cluster cofactor. J Biol Chem 282:31812–31820

    Article  PubMed  CAS  Google Scholar 

  71. Ge Y, Yang S, Fang Y, Yang R, Mou D, Cui J, Wen L (2007) RpoS as an intermediate in RsmA-dependent regulation of secondary antifungal metabolites biosynthesis in Pseudomonas sp. M18. FEMS Microbiol Lett 268:81–87

    Article  PubMed  CAS  Google Scholar 

  72. 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 186:2936–2945

    Article  PubMed  CAS  Google Scholar 

  73. Jackson DW, Suzuki K, Oakford L, Simecka JW, Hart ME, Romeo T (2002) Biofilm formation and dispersal under the influence of the global regulator CsrA of Escherichia coli. J Bacteriol 184:290–301

    Article  PubMed  CAS  Google Scholar 

  74. Liaw SJ, Lai HC, Ho SW, Luh KT, Wang WB (2003) Role of RsmA in the regulation of swarming motility and virulence factor expression in Proteus mirabilis. J Med Microbiol 52:19–28

    Article  PubMed  CAS  Google Scholar 

  75. Lucchetti-Miganeh C, Burrowes E, Baysse C, Ermel G (2008) The post-transcriptional regulator CsrA plays a central role in the adaptation of bacterial pathogens to different stages of infection in animal hosts. Microbiology 154:16–29

    Article  PubMed  CAS  Google Scholar 

  76. Mukherjee A, Cui Y, Liu Y, Dumenyo CK, Chatterjee AK (1996) Global regulation in Erwinia species by Erwinia carotovora rsmA, a homologue of Escherichia coli csrA: repression of secondary metabolites, pathogenicity and hypersensitive reaction. Microbiology 142(Pt 2):427–434

    Article  PubMed  CAS  Google Scholar 

  77. Mulcahy H, O’Callaghan J, O’Grady EP, Adams C, O’Gara F (2006) The posttranscriptional regulator RsmA plays a role in the interaction between Pseudomonas aeruginosa and human airway epithelial cells by positively regulating the type III secretion system. Infect Immun 74:3012–3015

    Article  PubMed  CAS  Google Scholar 

  78. Mulcahy H, O’Callaghan J, O’Grady EP, Maciá MD, Borrell N, Gómez C, Casey PG, Hill C, Adams C, Gahan CG, Oliver A, O’Gara F (2008) Pseudomonas aeruginosa RsmA plays an important role during murine infection by influencing colonization, virulence, persistence, and pulmonary inflammation. Infect Immun 76:632–638

    Article  PubMed  CAS  Google Scholar 

  79. Pessi G, Williams F, Hindle Z, Heurlier K, Holden MT, Camara 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 183:6676–6683

    Article  PubMed  CAS  Google Scholar 

  80. Sabnis NA, Yang H, Romeo T (1995) Pleiotropic regulation of central carbohydrate metabolism in Escherichia coli via the gene csrA. J Biol Chem 270:29096–29104

    Article  PubMed  CAS  Google Scholar 

  81. Wei B, Shin S, LaPorte D, Wolfe AJ, Romeo T (2000) Global regulatory mutations in csrA and rpoS cause severe central carbon stress in Escherichia coli in the presence of acetate. J Bacteriol 182:1632–1640

    Article  PubMed  CAS  Google Scholar 

  82. White D, Hart ME, Romeo T (1996) Phylogenetic distribution of the global regulatory gene csrA among eubacteria. Gene 182:221–223

    Article  PubMed  CAS  Google Scholar 

  83. 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 U S A 96:14073–14078

    Article  PubMed  CAS  Google Scholar 

  84. Chatterjee A, Cui Y, Liu Y, Dumenyo CK, Chatterjee AK (1995) 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 Environ Microbiol 61:1959–1967

    PubMed  CAS  Google Scholar 

  85. 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 187:276–285

    Article  PubMed  CAS  Google Scholar 

  86. Rife C, Schwarzenbacher R, McMullan D, Abdubek P, Ambing E, Axelrod H, Biorac T, Canaves JM, Chiu HJ, Deacon AM, DiDonato M, Elsliger MA, Godzik A, Grittini C, Grzechnik SK, Hale J, Hampton E, Han GW, Haugen J, Hornsby M, Jaroszewski L, Klock HE, Koesema E, Kreusch A, Kuhn P, Lesley SA, Miller MD, Moy K, Nigoghossian E, Paulsen J, Quijano K, Reyes R, Sims E, Spraggon G, Stevens RC, van den Bedem H, Velasquez J, Vincent J, White A, Wolf G, Xu Q, Hodgson KO, Wooley J, Wilson IA (2005) Crystal structure of the global regulatory protein CsrA from Pseudomonas putida at 2.05 A resolution reveals a new fold. Proteins 61:449–453

    Article  PubMed  CAS  Google Scholar 

  87. Gutierrez P, Li Y, Osborne MJ, Pomerantseva E, Liu Q, Gehring K (2005) Solution structure of the carbon storage regulator protein CsrA from Escherichia coli. J Bacteriol 187:3496–3501

    Article  PubMed  CAS  Google Scholar 

  88. Valverde R, Edwards L, Regan L (2008) Structure and function of KH domains. FEBS J 275:2712–2726

    Article  PubMed  CAS  Google Scholar 

  89. Romeo T, Gong M (1993) Genetic and physical mapping of the regulatory gene csrA on the Escherichia coli K-12 chromosome. J Bacteriol 175:5740–5741

    PubMed  CAS  Google Scholar 

  90. Mercante J, Edwards AN, Dubey AK, Babitzke P, Romeo T (2009) Molecular geometry of CsrA (RsmA) binding to RNA and its implications for regulated expression. J Mol Biol 392:511–528

    Article  PubMed  CAS  Google Scholar 

  91. Stoltenburg R, Reinemann C, Strehlitz B (2007) SELEX – a (r)evolutionary method to generate high-affinity nucleic acid ligands. Biomol Eng 24:381–403

    Article  PubMed  CAS  Google Scholar 

  92. Smith TG, Hoover TR (2009) Deciphering bacterial flagellar gene regulatory networks in the genomic era. Adv Appl Microbiol 67:257–295

    Article  PubMed  CAS  Google Scholar 

  93. Holms WH (1986) The central metabolic pathways of Escherichia coli: relationship between flux and control at a branch point, efficiency of conversion to biomass, and excretion of acetate. Curr Top Cell Regul 28:69–105

    PubMed  CAS  Google Scholar 

  94. Preiss J, Yung SG, Baecker PA (1983) Regulation of bacterial glycogen synthesis. Mol Cell Biochem 57:61–80

    Article  PubMed  CAS  Google Scholar 

  95. Dauvillee D, Kinderf IS, Li Z, Kosar-Hashemi B, Samuel MS, Rampling L, Ball S, Morell MK (2005) Role of the Escherichia coli glgX gene in glycogen metabolism. J Bacteriol 187:1465–1473

    Article  PubMed  CAS  Google Scholar 

  96. Hengge-Aronis R, Fischer D (1992) Identification and molecular analysis of glgS, a novel growth-phase-regulated and rpoS-dependent gene involved in glycogen synthesis in Escherichia coli. Mol Microbiol 6:1877–1886

    Article  PubMed  CAS  Google Scholar 

  97. Kozlov G, Elias D, Cygler M, Gehring K (2004) Structure of GlgS from Escherichia coli suggests a role in protein–protein interactions. BMC Biol 2:10

    Article  PubMed  Google Scholar 

  98. Schultz JE, Matin A (1991) Molecular and functional characterization of a carbon starvation gene of Escherichia coli. J Mol Biol 218:129–140

    Article  PubMed  CAS  Google Scholar 

  99. Lawhon SD, Frye JG, Suyemoto M, Porwollik S, McClelland M, Altier C (2003) Global regulation by CsrA in Salmonella typhimurium. Mol Microbiol 48:1633–1645

    Article  PubMed  CAS  Google Scholar 

  100. Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346

    Article  PubMed  CAS  Google Scholar 

  101. Cui Y, Chatterjee A, Liu Y, Dumenyo CK, Chatterjee AK (1995) Identification of a global repressor gene, rsmA, of Erwinia carotovora subsp. carotovora that controls extracellular enzymes, N-(3-oxohexanoyl)-l-homoserine lactone, and pathogenicity in soft-rotting Erwinia spp. J Bacteriol 177:5108–5115

    PubMed  CAS  Google Scholar 

  102. Chatterjee A, Cui Y, Chatterjee AK (2002) 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 184:4089–4095

    Article  PubMed  CAS  Google Scholar 

  103. Moons P, Michiels CW, Aertsen A (2009) Bacterial interactions in biofilms. Crit Rev Microbiol 35:157–168

    Article  PubMed  CAS  Google Scholar 

  104. Itoh Y, Rice JD, Goller C, Pannuri A, Taylor J, Meisner J, Beveridge TJ, Preston JF 3rd, Romeo T (2008) Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin poly-beta-1,6-N-acetyl-d-glucosamine. J Bacteriol 190:3670–3680

    Article  PubMed  CAS  Google Scholar 

  105. Izano EA, Sadovskaya I, Wang H, Vinogradov E, Ragunath C, Ramasubbu N, Jabbouri S, Perry MB, Kaplan JB (2008) Poly-N-acetylglucosamine mediates biofilm formation and detergent resistance in Aggregatibacter actinomycetemcomitans. Microb Pathog 44:52–60

    Article  PubMed  CAS  Google Scholar 

  106. Wang X, Preston JF 3rd, Romeo T (2004) The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J Bacteriol 186:2724–2734

    Article  PubMed  CAS  Google Scholar 

  107. Jin Y, Watt RM, Danchin A, Huang JD (2009) Use of a riboswitch-controlled conditional hypomorphic mutation to uncover a role for the essential csrA gene in bacterial autoaggregation. J Biol Chem 284:28738–28745

    Article  PubMed  CAS  Google Scholar 

  108. Fields JA, Thompson SA (2008) Campylobacter jejuni CsrA mediates oxidative stress responses, biofilm formation, and host cell invasion. J Bacteriol 190:3411–3416

    Article  PubMed  CAS  Google Scholar 

  109. Jones MK, Warner EB, Oliver JD (2008) csrA inhibits the formation of biofilms by Vibrio vulnificus. Appl Environ Microbiol 74:7064–7066

    Article  PubMed  CAS  Google Scholar 

  110. Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7:263–273

    Article  PubMed  CAS  Google Scholar 

  111. Altier C, Suyemoto M, Ruiz AI, Burnham KD, Maurer R (2000) Characterization of two novel regulatory genes affecting Salmonella invasion gene expression. Mol Microbiol 35:635–646

    Article  PubMed  CAS  Google Scholar 

  112. Barnard FM, Loughlin MF, Fainberg HP, Messenger MP, Ussery DW, Williams P, Jenks PJ (2004) Global regulation of virulence and the stress response by CsrA in the highly adapted human gastric pathogen Helicobacter pylori. Mol Microbiol 51:15–32

    Article  PubMed  CAS  Google Scholar 

  113. Forsbach-Birk V, McNealy T, Shi C, Lynch D, Marre R (2004) Reduced expression of the global regulator protein CsrA in Legionella pneumophila affects virulence-associated regulators and growth in Acanthamoeba castellanii. Int J Med Microbiol 294:15–25

    Article  PubMed  CAS  Google Scholar 

  114. Kerrinnes T, Zelas ZB, Streckel W, Faber F, Tietze E, Tschape H, Yaron S (2009) CsrA and CsrB are required for the post-transcriptional control of the virulence-associated effector protein AvrA of Salmonella enterica. Int J Med Microbiol 299:333–341

    Article  PubMed  CAS  Google Scholar 

  115. Rasis M, Segal G (2009) The LetA-RsmYZ-CsrA regulatory cascade, together with RpoS and PmrA, post-transcriptionally regulates stationary phase activation of Legionella pneumophila Icm/Dot effectors. Mol Microbiol 72:995–1010

    Article  PubMed  CAS  Google Scholar 

  116. Sahr T, Bruggemann H, Jules M, Lomma M, Albert-Weissenberger C, Cazalet C, Buchrieser C (2010) Two small ncRNAs jointly govern virulence and transmission in Legionella pneumophila. Mol Microbiol 72:741–762

    Article  CAS  Google Scholar 

  117. Teplitski M, Goodier RI, Ahmer BM (2003) Pathways leading from BarA/SirA to motility and virulence gene expression in Salmonella. J Bacteriol 185:7257–7265

    Article  PubMed  CAS  Google Scholar 

  118. Molofsky AB, Swanson MS (2003) Legionella pneumophila CsrA is a pivotal repressor of transmission traits and activator of replication. Mol Microbiol 50:445–461

    Article  PubMed  CAS  Google Scholar 

  119. Mukherjee A, Cui Y, Ma W, Liu Y, Ishihama A, Eisenstark A, Chatterjee AK (1998) RpoS (sigma-S) controls expression of rsmA, a global regulator of secondary metabolites, harpin, and extracellular proteins in Erwinia carotovora. J Bacteriol 180:3629–3634

    PubMed  CAS  Google Scholar 

  120. Dong T, Schellhorn HE (2009) Control of RpoS in global gene expression of Escherichia coli in minimal media. Mol Genet Genomics 281:19–33

    Article  PubMed  CAS  Google Scholar 

  121. Patten CL, Kirchhof MG, Schertzberg MR, Morton RA, Schellhorn HE (2004) Microarray analysis of RpoS-mediated gene expression in Escherichia coli K-12. Mol Genet Genomics 272:580–591

    Article  PubMed  CAS  Google Scholar 

  122. Rahman M, Hasan MR, Oba T, Shimizu K (2006) Effect of rpoS gene knockout on the metabolism of Escherichia coli during exponential growth phase and early stationary phase based on gene expressions, enzyme activities and intracellular metabolite concentrations. Biotechnol Bioeng 94:585–595

    Article  PubMed  CAS  Google Scholar 

  123. 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 34:3361–3369

    Article  PubMed  CAS  Google Scholar 

  124. Suzuki K, Babitzke P, Kushner SR, Romeo T (2006) Identification of a novel regulatory protein (CsrD) that targets the global regulatory RNAs CsrB and CsrC for degradation by RNase E. Genes Dev 20:2605–2617

    Article  PubMed  CAS  Google Scholar 

  125. Jonas K, Tomenius H, Romling U, Georgellis D, Melefors O (2006) Identification of YhdA as a regulator of the Escherichia coli carbon storage regulation system. FEMS Microbiol Lett 264:232–237

    Article  PubMed  CAS  Google Scholar 

  126. Gudapaty S, Suzuki K, Wang X, Babitzke P, Romeo T (2001) Regulatory interactions of Csr components: the RNA binding protein CsrA activates csrB transcription in Escherichia coli. J Bacteriol 183:6017–6027

    Article  PubMed  CAS  Google Scholar 

  127. Jonas K, Melefors O (2009) The Escherichia coli CsrB and CsrC small RNAs are strongly induced during growth in nutrient-poor medium. FEMS Microbiol Lett 297:80–86

    Article  PubMed  CAS  Google Scholar 

  128. 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 184:1046–1056

    Article  PubMed  CAS  Google Scholar 

  129. Lapouge K, Schubert M, Allain FH, Haas D (2008) Gac/Rsm signal transduction pathway of gamma-proteobacteria: from RNA recognition to regulation of social behaviour. Mol Microbiol 67:241–253

    Article  PubMed  CAS  Google Scholar 

  130. Chavez RG, Alvarez AF, Romeo T, Georgellis D (2010) The physiological stimulus for the BarA sensor kinase. J Bacteriol 192:2009–2012

    Article  PubMed  CAS  Google Scholar 

  131. 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 284:34976–34985

    Article  PubMed  CAS  Google Scholar 

  132. Pernestig AK, Georgellis D, Romeo T, Suzuki K, Tomenius H, Normark S, Melefors O (2003) The Escherichia coli BarA-UvrY two-component system is needed for efficient switching between glycolytic and gluconeogenic carbon sources. J Bacteriol 185:843–853

    Article  PubMed  CAS  Google Scholar 

  133. Hyytiainen H, Montesano M, Palva ET (2001) Global regulators ExpA (GacA) and KdgR modulate extracellular enzyme gene expression through the RsmA-rsmB system in Erwinia carotovora subsp. carotovora. Mol Plant Microbe Interact 14:931–938

    Article  PubMed  CAS  Google Scholar 

  134. Krin E, Derzelle S, Bedard K, Adib-Conquy M, Turlin E, Lenormand P, Hullo MF, Bonne I, Chakroun N, Lacroix C, Danchin A (2008) Regulatory role of UvrY in adaptation of Photorhabdus luminescens growth inside the insect. Environ Microbiol 10:1118–1134

    Article  PubMed  CAS  Google Scholar 

  135. 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 50:1361–1379

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Johan Timmermans is supported by a Waleo 3 Program (no. 816876) from the Belgian Wallonia region.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Laurence Van Melderen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Timmermans, J., Van Melderen, L. Post-transcriptional global regulation by CsrA in bacteria. Cell. Mol. Life Sci. 67, 2897–2908 (2010). https://doi.org/10.1007/s00018-010-0381-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-010-0381-z

Keywords

Navigation