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Journal of Bacteriology, January 2006, p. 305-316, Vol. 188, No. 1
0021-9193/06/$08.00+0     doi:10.1128/JB.188.1.305-316.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Autoinducer 2 Controls Biofilm Formation in Escherichia coli through a Novel Motility Quorum-Sensing Regulator (MqsR, B3022)

Andrés F. González Barrios,1 Rongjun Zuo,1 Yoshifumi Hashimoto,2 Li Yang,2 William E. Bentley,2 and Thomas K. Wood1*

Departments of Chemical Engineering and Molecular & Cell Biology, University of Connecticut, 191 Auditorium Rd., Storrs, Connecticut 06269-3222,1 Department of Chemical and Biomolecular Engineering, University of Maryland, College Park, Center for Biosystems Research, UMBI, College Park, Maryland 207422

Received 28 August 2005/ Accepted 27 September 2005

The cross-species bacterial communication signal autoinducer 2 (AI-2), produced by the purified enzymes Pfs (nucleosidase) and LuxS (terminal synthase) from S-adenosylhomocysteine, directly increased Escherichia coli biofilm mass 30-fold. Continuous-flow cells coupled with confocal microscopy corroborated these results by showing the addition of AI-2 significantly increased both biofilm mass and thickness and reduced the interstitial space between microcolonies. As expected, the addition of AI-2 to cells which lack the ability to transport AI-2 (lsr null mutant) failed to stimulate biofilm formation. Since the addition of AI-2 increased cell motility through enhanced transcription of five motility genes, we propose that AI-2 stimulates biofilm formation and alters its architecture by stimulating flagellar motion and motility. It was also found that the uncharacterized protein B3022 regulates this AI-2-mediated motility and biofilm phenotype through the two-component motility regulatory system QseBC. Deletion of b3022 abolished motility, which was restored by expressing b3022 in trans. Deletion of b3022 also decreased biofilm formation significantly, relative to the wild-type strain in three media (46 to 74%) in 96-well plates, as well as decreased biomass (8-fold) and substratum coverage (19-fold) in continuous-flow cells with minimal medium (growth rate not altered and biofilm restored by expressing b3022 in trans). Deleting b3022 changed the wild-type biofilm architecture from a thick (54-µm) complex structure to one that contained only a few microcolonies. B3022 positively regulates expression of qseBC, flhD, fliA, and motA, since deleting b3022 decreased their transcription by 61-, 25-, 2.4-, and 18-fold, respectively. Transcriptome analysis also revealed that B3022 induces crl (26-fold) and flhCD (8- to 27-fold). Adding AI-2 (6.4 µM) increased biofilm formation of wild-type K-12 MG1655 but not that of the isogenic b3022, qseBC, fliA, and motA mutants. Adding AI-2 also increased motA transcription for the wild-type strain but did not stimulate motA transcription for the b3022 and qseB mutants. Together, these results indicate AI-2 induces biofilm formation in E. coli through B3022, which then regulates QseBC and motility; hence, b3022 has been renamed the motility quorum-sensing regulator gene (the mqsR gene).

* Corresponding author. Mailing address: Artie McFerrin Department of Chemical Engineering, Texas A & M University, 220 Jack E. Brown Building, College Station, TX 77843-3122. Phone: (979) 862-1588. Fax: (860) 845-6884. E-mail: Thomas.Wood{at}chemail.tamu.edu.

Journal of Bacteriology, January 2006, p. 305-316, Vol. 188, No. 1
0021-9193/06/$08.00+0     doi:10.1128/JB.188.1.305-316.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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