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Journal of Bacteriology, August 2007, p. 6011-6020, Vol. 189, No. 16
0021-9193/07/$08.00+0     doi:10.1128/JB.00014-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Quorum Sensing in Escherichia coli Is Signaled by AI-2/LsrR: Effects on Small RNA and Biofilm Architecture{triangledown} ,{dagger}

Jun Li,1,3 Can Attila,5 Liang Wang,1,4 Thomas K. Wood,5 James J. Valdes,6 and William E. Bentley1,2,3*

Center for Biosystems Research, University of Maryland Biotechnology Institute,1 Fischell Department of Bioengineering,2 Department of Chemical and Bimolecular Engineering,3 Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, Maryland 20742,4 Department of Chemical Engineering, Texas A&M University, College Station, Texas,5 Army Edgewood Chemical Biological Center, Aberdeen Proving Ground, Maryland 210106

Received 3 January 2007/ Accepted 28 May 2007

The regulatory network for the uptake of Escherichia coli autoinducer 2 (AI-2) is comprised of a transporter complex, LsrABCD; its repressor, LsrR; and a cognate signal kinase, LsrK. This network is an integral part of the AI-2 quorum-sensing (QS) system. Because LsrR and LsrK directly regulate AI-2 uptake, we hypothesized that they might play a wider role in regulating other QS-related cellular functions. In this study, we characterized physiological changes due to the genomic deletion of lsrR and lsrK. We discovered that many genes were coregulated by lsrK and lsrR but in a distinctly different manner than that for the lsr operon (where LsrR serves as a repressor that is derepressed by the binding of phospho-AI-2 to the LsrR protein). An extended model for AI-2 signaling that is consistent with all current data on AI-2, LuxS, and the LuxS regulon is proposed. Additionally, we found that both the quantity and architecture of biofilms were regulated by this distinct mechanism, as lsrK and lsrR knockouts behaved identically. Similar biofilm architectures probably resulted from the concerted response of a set of genes including flu and wza, the expression of which is influenced by lsrRK. We also found for the first time that the generation of several small RNAs (including DsrA, which was previously linked to QS systems in Vibrio harveyi) was affected by LsrR. Our results suggest that AI-2 is indeed a QS signal in E. coli, especially when it acts through the transcriptional regulator LsrR.

* Corresponding author. Mailing address: Center for Biosystems Research, University of Maryland Biotechnology Institute, College Park, MD 20742. Phone: (301) 405-4321. Fax: (301) 314-9075. E-mail: bentley{at}eng.umd.edu

{triangledown} Published ahead of print on 8 June 2007.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.

Journal of Bacteriology, August 2007, p. 6011-6020, Vol. 189, No. 16
0021-9193/07/$08.00+0     doi:10.1128/JB.00014-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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