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Journal of Bacteriology, August 2006, p. 5682-5692, Vol. 188, No. 16
0021-9193/06/$08.00+0     doi:10.1128/JB.00352-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

The GrlR-GrlA Regulatory System Coordinately Controls the Expression of Flagellar and LEE-Encoded Type III Protein Secretion Systems in Enterohemorrhagic Escherichia coli

Sunao Iyoda,1* Nobuo Koizumi,1 Hitomi Satou,1 Yan Lu,1 Takehito Saitoh,2 Makoto Ohnishi,1 and Haruo Watanabe1

Department of Bacteriology,1 Infectious Diseases Surveillance Center, National Institute of Infectious Diseases, Toyama 1-23-1, Shinjuku-ku, Tokyo 162-8640, Japan2

Received 12 March 2006/ Accepted 30 May 2006

The gene function of the locus of enterocyte effacement (LEE) is essential for full virulence of enterohemorrhagic Escherichia coli (EHEC). Strict control of LEE gene expression is mediated by the coordinated activities of several regulatory elements. We previously reported that the ClpX/ClpP protease positively controls LEE expression by down-regulating intracellular levels of GrlR, a negative regulator of LEE gene expression. We further revealed that the negative effect of GrlR on LEE expression was mediated through GrlA, a positive regulator of LEE expression. In this study, we found that the FliC protein, a major component of flagellar filament, was overproduced in clpXP mutant EHEC, as previously reported for Salmonella. We further found that FliC expression was reduced in a clpXP grlR double mutant. To determine the mediators of this phenotype, FliC protein levels in wild-type, grlR, grlA, and grlR grlA strains were compared. Steady-state levels of FliC protein were reduced only in the grlR mutant, suggesting that positive regulation of FliC expression by GrlR is mediated by GrlA. Correspondingly, cell motility was also reduced in the grlR mutant, but not in the grlA or grlR grlA mutant. Because overexpression of grlA from a multicopy plasmid strongly represses the FliC level, as well as cell motility, we conclude that GrlA acts as a negative regulator of flagellar-gene expression. The fact that an EHEC strain constitutively expressing FlhD/FlhC cannot adhere to HeLa cells leads us to hypothesize that GrlA-dependent repression of the flagellar regulon is important for efficient cell adhesion of EHEC to host cells.

* Corresponding author. Mailing address: Department of Bacteriology, National Institute of Infectious Diseases, Toyama 1-23-1, Shinjuku-ku, Tokyo 162-8640, Japan. Phone: 81-3-5285-1111. Fax: 81-3-5285-1163. E-mail: siyoda{at}nih.go.jp.

Journal of Bacteriology, August 2006, p. 5682-5692, Vol. 188, No. 16
0021-9193/06/$08.00+0     doi:10.1128/JB.00352-06
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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