This Article Full Text Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Reprints and Permissions Copyright Information Books from ASM Press MicrobeWorld Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Suzuki, K. Articles by Romeo, T. Search for Related Content PubMed PubMed Citation Articles by Suzuki, K. Articles by Romeo, T.

Regulatory Circuitry of the CsrA/CsrB and BarA/UvrY Systems of Escherichia coli

Department of Microbiology and Immunology, Emory University, Atlanta, Georgia 30322,¹ Microbiology and Tumorbiology Center, Karolinska Institutet, SE-171 77 Stockholm, Sweden,² Departamento de Genética Molecular, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, 04510 Mexico City, Mexico,³ Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania 16802⁴

Received 27 March 2002/ Accepted 14 June 2002

The global regulator CsrA (carbon storage regulator) is an RNA binding protein that coordinates central carbon metabolism, activates flagellum biosynthesis and motility, and represses biofilm formation in Escherichia coli. CsrA activity is antagonized by the untranslated RNA CsrB, to which it binds and forms a globular ribonucleoprotein complex. CsrA indirectly activates csrB transcription, in an apparent autoregulatory mechanism. In the present study, we elucidate the intermediate regulatory circuitry of this system. Mutations affecting the BarA/UvrY two-component signal transduction system decreased csrB transcription but did not affect csrA'-'lacZ expression. The uvrY defect was severalfold more severe than that of barA. Both csrA and uvrY were required for optimal barA expression. The latter observation suggests an autoregulatory loop for UvrY. Ectopic expression of uvrY suppressed the csrB-lacZ expression defects caused by uvrY, csrA, or barA mutations; csrA suppressed csrA or barA defects; and barA complemented only the barA mutation. Purified UvrY protein stimulated csrB-lacZ expression approximately sixfold in S-30 transcription-translation reactions, revealing a direct effect of UvrY on csrB transcription. Disruption of sdiA, which encodes a LuxR homologue, decreased the expression of uvrY'-'lacZ and csrB-lacZ fusions but did not affect csrA'-'lacZ. The BarA/UvrY system activated biofilm formation. Ectopic expression of uvrY stimulated biofilm formation by a csrB-null mutant, indicative of a CsrB-independent role for UvrY in biofilm development. Collectively, these results demonstrate that uvrY resides downstream from csrA in a signaling pathway for csrB and that CsrA stimulates UvrY-dependent activation of csrB expression by BarA-dependent and -independent mechanisms.

This article has been cited by other articles:

• 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]  
• Hinchliffe, S. J., Howard, S. L., Huang, Y. H., Clarke, D. J., Wren, B. W. (2008). The importance of the Rcs phosphorelay in the survival and pathogenesis of the enteropathogenic yersiniae. Microbiology 154: 1117-1131 [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]  
• Baker, C. S., Eory, L. A., 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 [Abstract] [Full Text]  
• Mondragon, V., Franco, B., Jonas, K., Suzuki, K., Romeo, T., Melefors, O., Georgellis, D. (2006). pH-Dependent Activation of the BarA-UvrY Two-Component System in Escherichia coli. J. Bacteriol. 188: 8303-8306 [Abstract] [Full Text]  
• Goller, C., Wang, X., Itoh, Y., Romeo, T. (2006). The Cation-Responsive Protein NhaR of Escherichia coli Activates pgaABCD Transcription, Required for Production of the Biofilm Adhesin Poly-{beta}-1,6-N-Acetyl-D-Glucosamine. J. Bacteriol. 188: 8022-8032 [Abstract] [Full Text]  
• Teplitski, M., Al-Agely, A., Ahmer, B. M. M. (2006). Contribution of the SirA regulon to biofilm formation in Salmonella enterica serovar Typhimurium.. Microbiology 152: 3411-3424 [Abstract] [Full Text]  
• Romeo, T. (2006). When the Party Is Over: a Signal for Dispersal of Pseudomonas aeruginosa Biofilms. J. Bacteriol. 188: 7325-7327 [Full Text]  
• Suzuki, K., Babitzke, P., Kushner, S. R., 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 [Abstract] [Full Text]  
• Herren, C. D., Mitra, A., Palaniyandi, S. K., Coleman, A., Elankumaran, S., Mukhopadhyay, S. (2006). The BarA-UvrY Two-Component System Regulates Virulence in Avian Pathogenic Escherichia coli O78:K80:H9.. Infect. Immun. 74: 4900-4909 [Abstract] [Full Text]  
• Davey, M. E., Duncan, M. J. (2006). Enhanced Biofilm Formation and Loss of Capsule Synthesis: Deletion of a Putative Glycosyltransferase in Porphyromonas gingivalis.. J. Bacteriol. 188: 5510-5523 [Abstract] [Full Text]  
• Kulkarni, P. R., Cui, X., Williams, J. W., Stevens, A. M., Kulkarni, R. V. (2006). Prediction of CsrA-regulating small RNAs in bacteria and their experimental verification in Vibrio fischeri. Nucleic Acids Res 34: 3361-3369 [Abstract] [Full Text]  
• Pruss, B. M., Besemann, C., Denton, A., Wolfe, A. J. (2006). A Complex Transcription Network Controls the Early Stages of Biofilm Development by Escherichia coli. J. Bacteriol. 188: 3731-3739 [Full Text]  
• Hansmeier, N., Albersmeier, A., Tauch, A., Damberg, T., Ros, R., Anselmetti, D., Puhler, A., Kalinowski, J. (2006). The surface (S)-layer gene cspB of Corynebacterium glutamicum is transcriptionally activated by a LuxR-type regulator and located on a 6 kb genomic island absent from the type strain ATCC 13032.. Microbiology 152: 923-935 [Abstract] [Full Text]  
• Tomenius, H., Pernestig, A.-K., Mendez-Catala, C. F., Georgellis, D., Normark, S., Melefors, O. (2005). Genetic and Functional Characterization of the Escherichia coli BarA-UvrY Two-Component System: Point Mutations in the HAMP Linker of the BarA Sensor Give a Dominant-Negative Phenotype. J. Bacteriol. 187: 7317-7324 [Abstract] [Full Text]  
• Wolfe, A. J. (2005). The Acetate Switch. Microbiol. Mol. Biol. Rev. 69: 12-50 [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]  
• 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]  
• Wang, X., Preston, J. F. III, 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 [Abstract] [Full Text]  
• Whistler, C. A., Ruby, E. G. (2003). GacA Regulates Symbiotic Colonization Traits of Vibrio fischeri and Facilitates a Beneficial Association with an Animal Host. J. Bacteriol. 185: 7202-7212 [Abstract] [Full Text]  
• Teplitski, M., Goodier, R. I., Ahmer, B. M. M. (2003). Pathways Leading from BarA/SirA to Motility and Virulence Gene Expression in Salmonella. J. Bacteriol. 185: 7257-7265 [Abstract] [Full Text]  
• Zhou, L., Lei, X.-H., Bochner, B. R., Wanner, B. L. (2003). Phenotype MicroArray Analysis of Escherichia coli K-12 Mutants with Deletions of All Two-Component Systems. J. Bacteriol. 185: 4956-4972 [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]  
• Pernestig, A.-K., 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 [Abstract] [Full Text]  
• Gottesman, S. (2002). Stealth regulation: biological circuits with small RNA switches. Genes Dev. 16: 2829-2842 [Full Text]