This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow An erratum has been published
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Pessi, G.
Right arrow Articles by Williams, P.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Pessi, G.
Right arrow Articles by Williams, P.

 Previous Article  |  Next Article 

Journal of Bacteriology, November 2001, p. 6676-6683, Vol. 183, No. 22
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.22.6676-6683.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

The Global Posttranscriptional Regulator RsmA Modulates Production of Virulence Determinants and N-Acylhomoserine Lactones in Pseudomonas aeruginosa

Gabriella Pessi,1,dagger Faye Williams,2,3 Zoë Hindle,2,Dagger Karin Heurlier,1 Matthew T. G. Holden,2,3,§ Miguel Cámara,2 Dieter Haas,1 and Paul Williams2,3,*

Laboratoire de Biologie Microbienne, Université de Lausanne, CH-1015 Lausanne, Switzerland,1 and School of Pharmaceutical Sciences, University of Nottingham, University Park, Nottingham NG7 2RD,2 and Institute of Infections and Immunity, University of Nottingham, Queen's Medical Centre, Nottingham NG7 2UH,3 United Kingdom

Received 12 April 2001/Accepted 20 August 2001

Posttranscriptional control is known to contribute to the regulation of secondary metabolism and virulence determinants in certain gram-negative bacteria. Here we report the isolation of a Pseudomonas aeruginosa gene which encodes a global translational regulatory protein, RsmA (regulator of secondary metabolites). Overexpression of rsmA resulted in a substantial reduction in the levels of extracellular products, including protease, elastase, and staphylolytic (LasA protease) activity as well as the PA-IL lectin, hydrogen cyanide (HCN), and the phenazine pigment pyocyanin. While inactivation of rsmA in P. aeruginosa had only minor effects on the extracellular enzymes and the PA-IL lectin, the production of HCN and pyocyanin was enhanced during the exponential phase. The influence of RsmA on N-acylhomoserine lactone-mediated quorum sensing was determined by assaying the levels of N-(3-oxododecanoyl)homoserine lactone (3-oxo-C12-HSL) and N-butanoylhomoserine lactone (C4-HSL) produced by the rsmA mutant and the rsmA-overexpressing strain. RsmA exerted a negative effect on the synthesis of both 3-oxo-C12-HSL and C4-HSL, which was confirmed by using lasI and rhlI translational fusions. These data also highlighted the temporal expression control of the lasI gene, which was induced much earlier and to a higher level during the exponential growth phase in an rsmA mutant. To investigate whether RsmA modulates HCN production solely via quorum-sensing control, hcn translational fusions were employed to monitor the regulation of the cyanide biosynthesis genes (hcnABC). RsmA was shown to exert an additional negative effect on cyanogenesis posttranscriptionally by acting on a region surrounding the hcnA ribosome-binding site. This suggests that, in P. aeruginosa, RsmA functions as a pleiotropic posttranscriptional regulator of secondary metabolites directly and also indirectly by modulating the quorum-sensing circuitry.


* Corresponding author. Mailing address: School of Pharmaceutical Sciences, University of Nottingham, University Park, Nottingham NG7 2RD, United Kingdom. Phone: 44 115 9515047. Fax: 44 115 8466296. E-mail: paul.williams{at}nottingham.ac.uk.

dagger Present address: Nestlé Research Center, CH-1000 Lausanne 26, Switzerland.

Dagger Present address: Microscience Ltd., Wokingham, Berks., RG41 5TU, United Kingdom.

§ Present address: The Sanger Centre, Wellcome Trust Genome Campus, Hinxton, Cambridge CB10 1SA, United Kingdom.


Journal of Bacteriology, November 2001, p. 6676-6683, Vol. 183, No. 22
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.22.6676-6683.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.



This article has been cited by other articles:

  • Cody, W. L., Pritchett, C. L., Jones, A. K., Carterson, A. J., Jackson, D., Frisk, A., Wolfgang, M. C., Schurr, M. J. (2009). Pseudomonas aeruginosa AlgR Controls Cyanide Production in an AlgZ-Dependent Manner. J. Bacteriol. 191: 2993-3002 [Abstract] [Full Text]  
  • Dekimpe, V., Deziel, E. (2009). Revisiting the quorum-sensing hierarchy in Pseudomonas aeruginosa: the transcriptional regulator RhlR regulates LasR-specific factors. Microbiology 155: 712-723 [Abstract] [Full Text]  
  • Yan, Q., Gao, W., Wu, X.-G., Zhang, L.-Q. (2009). Regulation of the PcoI/PcoR quorum-sensing system in Pseudomonas fluorescens 2P24 by the PhoP/PhoQ two-component system. Microbiology 155: 124-133 [Abstract] [Full Text]  
  • Sonnleitner, E., Sorger-Domenigg, T., Madej, M. J., Findeiss, S., Hackermuller, J., Huttenhofer, A., Stadler, P. F., Blasi, U., Moll, I. (2008). Detection of small RNAs in Pseudomonas aeruginosa by RNomics and structure-based bioinformatic tools. Microbiology 154: 3175-3187 [Abstract] [Full Text]  
  • Willcox, M. D. P., Zhu, H., Conibear, T. C. R., Hume, E. B. H., Givskov, M., Kjelleberg, S., Rice, S. A. (2008). Role of quorum sensing by Pseudomonas aeruginosa in microbial keratitis and cystic fibrosis. Microbiology 154: 2184-2194 [Abstract] [Full Text]  
  • Takaya, A., Tabuchi, F., Tsuchiya, H., Isogai, E., Yamamoto, T. (2008). Negative Regulation of Quorum-Sensing Systems in Pseudomonas aeruginosa by ATP-Dependent Lon Protease. J. Bacteriol. 190: 4181-4188 [Abstract] [Full Text]  
  • Fields, J. A., Thompson, S. A. (2008). Campylobacter jejuni CsrA Mediates Oxidative Stress Responses, Biofilm Formation, and Host Cell Invasion. J. Bacteriol. 190: 3411-3416 [Abstract] [Full Text]  
  • Goldberg, J. B., Hancock, R. E. W., Parales, R. E., Loper, J., Cornelis, P. (2008). Pseudomonas 2007. J. Bacteriol. 190: 2649-2662 [Full Text]  
  • Mulcahy, H., O'Callaghan, J., O'Grady, E. P., Macia, M. D., Borrell, N., Gomez, C., Casey, P. G., Hill, C., Adams, C., Gahan, C. G. M., 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 [Abstract] [Full Text]  
  • 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 [Abstract] [Full Text]  
  • Williams, P., Winzer, K., Chan, W. C, Camara, M. (2007). Look who's talking: communication and quorum sensing in the bacterial world. Phil Trans R Soc B 362: 1119-1134 [Abstract] [Full Text]  
  • Sakuragi, Y., Kolter, R. (2007). Quorum-Sensing Regulation of the Biofilm Matrix Genes (pel) of Pseudomonas aeruginosa. J. Bacteriol. 189: 5383-5386 [Abstract] [Full Text]  
  • Duan, K., Surette, M. G. (2007). Environmental Regulation of Pseudomonas aeruginosa PAO1 Las and Rhl Quorum-Sensing Systems. J. Bacteriol. 189: 4827-4836 [Abstract] [Full Text]  
  • Yang, S., Zhang, Q., Guo, J., Charkowski, A. O., Glick, B. R., Ibekwe, A. M., Cooksey, D. A., Yang, C.-H. (2007). Global Effect of Indole-3-Acetic Acid Biosynthesis on Multiple Virulence Factors of Erwinia chrysanthemi 3937. Appl. Environ. Microbiol. 73: 1079-1088 [Abstract] [Full Text]  
  • Lujan, A. M., Moyano, A. J., Segura, I., Argarana, C. E., Smania, A. M. (2007). Quorum-sensing-deficient (lasR) mutants emerge at high frequency from a Pseudomonas aeruginosa mutS strain. Microbiology 153: 225-237 [Abstract] [Full Text]  
  • Gonzalez, J. E., Keshavan, N. D. (2006). Messing with Bacterial Quorum Sensing. Microbiol. Mol. Biol. Rev. 70: 859-875 [Abstract] [Full Text]  
  • O'Grady, E. P., Mulcahy, H., O'Callaghan, J., Adams, C., O'Gara, F. (2006). Pseudomonas aeruginosa Infection of Airway Epithelial Cells Modulates Expression of Kruppel-Like Factors 2 and 6 via RsmA-Mediated Regulation of Type III Exoenzymes S and Y.. Infect. Immun. 74: 5893-5902 [Abstract] [Full Text]  
  • Kay, E., Humair, B., Denervaud, 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: 6026-6033 [Abstract] [Full Text]  
  • Mulcahy, H., O'Callaghan, J., O'Grady, E. P., 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 [Abstract] [Full Text]  
  • Lequette, Y., Lee, J.-H., Ledgham, F., Lazdunski, A., Greenberg, E. P. (2006). A Distinct QscR Regulon in the Pseudomonas aeruginosa Quorum-Sensing Circuit. J. Bacteriol. 188: 3365-3370 [Abstract] [Full Text]  
  • Dubuis, C., Rolli, J., Lutz, M., Defago, G., Haas, D. (2006). Thiamine-Auxotrophic Mutants of Pseudomonas fluorescens CHA0 Are Defective in Cell-Cell Signaling and Biocontrol Factor Expression. Appl. Environ. Microbiol. 72: 2606-2613 [Abstract] [Full Text]  
  • Roberts, C., Anderson, K. L., Murphy, E., Projan, S. J., Mounts, W., Hurlburt, B., Smeltzer, M., Overbeek, R., Disz, T., Dunman, P. M. (2006). Characterizing the Effect of the Staphylococcus aureus Virulence Factor Regulator, SarA, on Log-Phase mRNA Half-Lives.. J. Bacteriol. 188: 2593-2603 [Abstract] [Full Text]  
  • Furukawa, S., Kuchma, S. L., O'Toole, G. A. (2006). Keeping Their Options Open: Acute versus Persistent Infections. J. Bacteriol. 188: 1211-1217 [Full Text]  
  • 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 [Abstract] [Full Text]  
  • Rampioni, G., Bertani, I., Zennaro, E., Polticelli, F., Venturi, V., Leoni, L. (2006). The Quorum-Sensing Negative Regulator RsaL of Pseudomonas aeruginosa Binds to the lasI Promoter. J. Bacteriol. 188: 815-819 [Abstract] [Full Text]  
  • Gingues, S., Kooi, C., Visser, M. B., Subsin, B., Sokol, P. A. (2005). Distribution and Expression of the ZmpA Metalloprotease in the Burkholderia cepacia Complex. J. Bacteriol. 187: 8247-8255 [Abstract] [Full Text]  
  • Soo, P.-C., Wei, J.-R., Horng, Y.-T., Hsieh, S.-C., Ho, S.-W., Lai, H.-C. (2005). Characterization of the dapA-nlpB Genetic Locus Involved in Regulation of Swarming Motility, Cell Envelope Architecture, Hemolysin Production, and Cell Attachment Ability in Serratia marcescens. Infect. Immun. 73: 6075-6084 [Abstract] [Full Text]  
  • Heurlier, K., Denervaud, V., Haenni, M., Guy, L., Krishnapillai, V., Haas, D. (2005). Quorum-Sensing-Negative (lasR) Mutants of Pseudomonas aeruginosa Avoid Cell Lysis and Death. J. Bacteriol. 187: 4875-4883 [Abstract] [Full Text]  
  • Lai, H.-C., Soo, P.-C., Wei, J.-R., Yi, W.-C., Liaw, S.-J., Horng, Y.-T., Lin, S.-M., Ho, S.-W., Swift, S., Williams, P. (2005). The RssAB Two-Component Signal Transduction System in Serratia marcescens Regulates Swarming Motility and Cell Envelope Architecture in Response to Exogenous Saturated Fatty Acids. J. Bacteriol. 187: 3407-3414 [Abstract] [Full Text]  
  • Park, S.-Y., Kang, H.-O., Jang, H.-S., Lee, J.-K., Koo, B.-T., Yum, D.-Y. (2005). Identification of Extracellular N-Acylhomoserine Lactone Acylase from a Streptomyces sp. and Its Application to Quorum Quenching. Appl. Environ. Microbiol. 71: 2632-2641 [Abstract] [Full Text]  
  • Aendekerk, S., Diggle, S. P., Song, Z., Hoiby, N., Cornelis, P., Williams, P., Camara, M. (2005). The MexGHI-OpmD multidrug efflux pump controls growth, antibiotic susceptibility and virulence in Pseudomonas aeruginosa via 4-quinolone-dependent cell-to-cell communication. Microbiology 151: 1113-1125 [Abstract] [Full Text]  
  • Brencic, A., Winans, S. C. (2005). Detection of and Response to Signals Involved in Host-Microbe Interactions by Plant-Associated Bacteria. Microbiol. Mol. Biol. Rev. 69: 155-194 [Abstract] [Full Text]  
  • 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 [Abstract] [Full Text]  
  • Carterson, A. J., Morici, L. A., Jackson, D. W., Frisk, A., Lizewski, S. E., Jupiter, R., Simpson, K., Kunz, D. A., Davis, S. H., Schurr, J. R., Hassett, D. J., Schurr, M. J. (2004). The Transcriptional Regulator AlgR Controls Cyanide Production in Pseudomonas aeruginosa. J. Bacteriol. 186: 6837-6844 [Abstract] [Full Text]  
  • Lizewski, S. E., Schurr, J. R., Jackson, D. W., Frisk, A., Carterson, A. J., Schurr, M. J. (2004). Identification of AlgR-Regulated Genes in Pseudomonas aeruginosa by Use of Microarray Analysis. J. Bacteriol. 186: 5672-5684 [Abstract] [Full Text]  
  • Ovadis, M., Liu, X., Gavriel, S., Ismailov, Z., Chet, I., Chernin, L. (2004). The Global Regulator Genes from Biocontrol Strain Serratia plymuthica IC1270: Cloning, Sequencing, and Functional Studies. J. Bacteriol. 186: 4986-4993 [Abstract] [Full Text]  
  • Valverde, C., Lindell, M., Wagner, E. G. H., 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: 25066-25074 [Abstract] [Full Text]  
  • Heurlier, K., Williams, F., Heeb, S., Dormond, C., Pessi, G., Singer, D., Camara, 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 [Abstract] [Full Text]  
  • Juhas, M., Wiehlmann, L., Huber, B., Jordan, D., Lauber, J., Salunkhe, P., Limpert, A. S., von Gotz, F., Steinmetz, I., Eberl, L., Tummler, B. (2004). Global regulation of quorum sensing and virulence by VqsR in Pseudomonas aeruginosa. Microbiology 150: 831-841 [Abstract] [Full Text]  
  • Chen, H., Teplitski, M., Robinson, J. B., Rolfe, B. G., Bauer, W. D. (2003). Proteomic Analysis of Wild-Type Sinorhizobium meliloti Responses to N-Acyl Homoserine Lactone Quorum-Sensing Signals and the Transition to Stationary Phase. J. Bacteriol. 185: 5029-5036 [Abstract] [Full Text]  
  • Dubey, A. K., Baker, C. S., Suzuki, K., Jones, A. D., 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 [Abstract] [Full Text]  
  • Schuster, M., Lostroh, C. P., Ogi, T., Greenberg, E. P. (2003). Identification, Timing, and Signal Specificity of Pseudomonas aeruginosa Quorum-Controlled Genes: a Transcriptome Analysis. J. Bacteriol. 185: 2066-2079 [Abstract] [Full Text]  
  • Heurlier, K., Denervaud, V., Pessi, G., Reimmann, C., Haas, D. (2003). Negative Control of Quorum Sensing by RpoN ({sigma}54) in Pseudomonas aeruginosa PAO1. J. Bacteriol. 185: 2227-2235 [Abstract] [Full Text]  
  • Medina, G., Juarez, K., Soberon-Chavez, G. (2003). The Pseudomonas aeruginosa rhlAB Operon Is Not Expressed during the Logarithmic Phase of Growth Even in the Presence of Its Activator RhlR and the Autoinducer N-Butyryl-Homoserine Lactone. J. Bacteriol. 185: 377-380 [Abstract] [Full Text]  
  • Finking, R., Solsbacher, J., Konz, D., Schobert, M., Schafer, A., Jahn, D., Marahiel, M. A. (2002). Characterization of a New Type of Phosphopantetheinyl Transferase for Fatty Acid and Siderophore Synthesis in Pseudomonas aeruginosa. J. Biol. Chem. 277: 50293-50302 [Abstract] [Full Text]  
  • Suzuki, K., Wang, X., Weilbacher, T., Pernestig, A.-K., 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 [Abstract] [Full Text]  
  • Wilkinson, A., Danino, V., Wisniewski-Dye, F., Lithgow, J. K., Downie, J. A. (2002). N-Acyl-Homoserine Lactone Inhibition of Rhizobial Growth Is Mediated by Two Quorum-Sensing Genes That Regulate Plasmid Transfer. J. Bacteriol. 184: 4510-4519 [Abstract] [Full Text]  
  • Stevenson, B., Babb, K. (2002). LuxS-Mediated Quorum Sensing in Borrelia burgdorferi, the Lyme Disease Spirochete. Infect. Immun. 70: 4099-4105 [Abstract] [Full Text]  
  • Chatterjee, A., Cui, Y., Chatterjee, A. K. (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 [Abstract] [Full Text]  
  • Pearson, J. P. (2002). Early Activation of Quorum Sensing. J. Bacteriol. 184: 2569-2571 [Full Text]  
  • Diggle, S. P., Winzer, K., Lazdunski, A., Williams, P., Camara, M. (2002). Advancing the Quorum in Pseudomonas aeruginosa: MvaT and the Regulation of N-Acylhomoserine Lactone Production and Virulence Gene Expression. J. Bacteriol. 184: 2576-2586 [Abstract] [Full Text]  
  • 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 [Abstract] [Full Text]