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Infection and Immunity, December 2004, p. 7282-7293, Vol. 72, No. 12
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.12.7282-7293.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Regulators Encoded in the Escherichia coli Type III Secretion System 2 Gene Cluster Influence Expression of Genes within the Locus for Enterocyte Effacement in Enterohemorrhagic E. coli O157:H7

Lihong Zhang,1 Roy R. Chaudhuri,1 Chrystala Constantinidou,2 Jon L. Hobman,2 Mala D. Patel,2 Antony C. Jones,2 Donatella Sarti,2 Andrew J. Roe,3 Isabella Vlisidou,4 Robert K. Shaw,5 Francesco Falciani,2 Mark P. Stevens,4 David L. Gally,3 Stuart Knutton,5 Gad Frankel,6 Charles W. Penn,2 and Mark J. Pallen1*

Bacterial Pathogenesis and Genomics Unit, Division of Immunity and Infection, Medical School,1 School of Biosciences,2 Division of Reproductive Physiology and Child Health, Institute for Child Health, University of Birmingham, Birmingham,5 Zoonotic and Animal Pathogens Research Laboratory, Medical Microbiology, University of Edinburgh, Edinburgh,3 Institute for Animal Health, Division of Microbiology, Compton, Berkshire,4 Centre for Molecular Microbiology and Infection, Imperial College of Science, Technology and Medicine, London, United Kingdom6

Received 29 April 2004/ Returned for modification 21 June 2004/ Accepted 20 August 2004

Enterohemorrhagic Escherichia coli (EHEC) O157:H7 subverts host cells through a type III secretion system encoded by the locus for enterocyte effacement (LEE). Genome sequencing of this pathotype revealed the existence of a gene cluster encoding components of a second cryptic type III secretion system, E. coli type III secretion system 2 (ETT2). Recently, we showed that the ETT2 gene cluster is present in whole or in part in the majority of E. coli strains but is unable to encode a functional secretion system in most strains, including EHEC O157:H7. However, here we show that mutational inhibition of two regulatory genes (ECs3720 or etrA and ECs3734 or eivF) from the ETT2 cluster in EHEC O157:H7 leads to greatly increased secretion of proteins encoded by the LEE and to increased adhesion to human intestinal cells. Studies in which transcriptional fusions and microarrays were used indicated that EtrA and EivF exert profound negative effects on gene transcription within the LEE. Consistent with these observations, expression of these regulators in an EHEC O26:H- strain led to suppression of protein secretion under LEE-inducing conditions. These findings provide fresh examples of the influence of mobile genetic elements on regulation of the LEE and of cross talk between type III secretion system gene clusters. In addition, they provide a cautionary tale because they show that the effects of regulatory genes can outlive widespread decay of other genes in a functionally coherent gene cluster, a phenomenon that we have named the "Cheshire cat effect." It also seems likely that variations in the ETT2 regulator repertoire might account for strain-to-strain variation in secretion of LEE-encoded proteins.

* Corresponding author. Mailing address: Bacterial Pathogenesis and Genomics Unit, Division of Immunity and Infection, Medical School, University of Birmingham, Birmingham B15 2TT, United Kingdom. Phone: (44) 121 414 7163. Fax: (44) 121 414 3454. E-mail: m.pallen{at}bham.ac.uk.

Editor: A. D. O'Brien

Infection and Immunity, December 2004, p. 7282-7293, Vol. 72, No. 12
0019-9567/04/$08.00+0     DOI: 10.1128/IAI.72.12.7282-7293.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



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