JB Accepts, published online ahead of print on 8 June 2007

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J. Bacteriol. doi:10.1128/JB.00014-07
Copyright (c) 2007, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.

Quorum Sensing in E. coli is Signaled by AI-2/LsrR: Effects on sRNA and Biofilm Architecture

JUN LI, CAN ATTILA, LIANG WANG, THOMAS K. WOOD, JAMES J. VALDES, and WILLIAM E. BENTLEY^*

Center for Biosystems Research, University of Maryland Biotechnology Institute, Fischell Department of Bioengineering, Department of Chemical and Bimolecular Engineering, Department of Cell Biology & Molecular Genetics, University of Maryland, College Park, Maryland 20742, Department of Chemical Engineering, Texas A&M University, College Station, Texas and Army Edgewood Chemical Biological Center, Aberdeen Proving Ground, Maryland 21010

^* To whom correspondence should be addressed. Email: bentley{at}eng.umd.edu.

The regulatory network for the uptake of E. coli autoinducer, AI-2, is comprised of a transporter complex, LsrABCD, its repressor, LsrR and 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 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 co-regulated by lsrK and lsrR but in a distinctly different manner than 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 is proposed that is consistent with all current data on AI-2, LuxS, and the LuxS-regulon. 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 are 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 V. harveyi) was affected by LsrR. Our results suggest that AI-2 is indeed a quorum sensing signal in E. coli, especially when it acts through transcriptional regulator, LsrR.

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