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Infection and Immunity, April 2005, p. 2135-2146, Vol. 73, No. 4
0019-9567/05/$08.00+0     doi:10.1128/IAI.73.4.2135-2146.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Regulation of Type III Secretion Hierarchy of Translocators and Effectors in Attaching and Effacing Bacterial Pathogens

Wanyin Deng,1 Yuling Li,1 Philip R. Hardwidge,1 Elizabeth A. Frey,2 Richard A. Pfuetzner,2 Sansan Lee,1 Samantha Gruenheid,1 Natalie C. J. Strynakda,2 Jose L. Puente,3 and B. Brett Finlay1*

Michael Smith Laboratories,1 Department of Biochemistry and Molecular Biology, University of British Columbia, Vancouver, British Columbia, Canada,2 Departamento de Microbiología Molecular, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Morelos, México3

Received 20 September 2004/ Returned for modification 9 November 2004/ Accepted 3 December 2004

Human enteropathogenic Escherichia coli (EPEC), enterohemorrhagic E. coli (EHEC), and the mouse pathogen Citrobacter rodentium (CR) belong to the family of attaching and effacing (A/E) bacterial pathogens. They possess the locus of enterocyte effacement (LEE) pathogenicity island, which encodes a type III secretion system. These pathogens secrete a number of proteins into culture media, including type III effector proteins and translocators that are required for the translocation of effectors into host cells. Preliminary evidence indicated that the LEE-encoded SepL and Rorf6/SepD may form a molecular switch that controls the secretion of translocators and effectors in CR. Here, we show that SepL and SepD indeed perform this function in A/E pathogens such as EHEC and EPEC. Their sepL and sepD mutants do not secrete translocators but exhibit enhanced secretion of effectors. We demonstrate that SepL and SepD interact with each other and that both SepL and SepD are localized to the bacterial membranes. Furthermore, we demonstrate that culture media influence the type III secretion profile of EHEC, EPEC, and CR and that low-calcium concentrations inhibit secretion of translocators but promote the secretion of effectors, similar to effects on type III secretion by mutations in sepL and sepD. However, the secretion profile of the sepD and sepL mutants is not affected by these culture conditions. Collectively, our results suggest that SepL and SepD not only are necessary for efficient translocator secretion in A/E pathogens but also control a switch from translocator to effector secretion by sensing certain environmental signals such as low calcium.

* Corresponding author. Mailing address: Michael Smith Laboratories, University of British Columbia, 301-2185, East Mall, Vancouver, British Columbia V6T 1Z4, Canada. Phone: (604) 822-2210. Fax: (604) 822-9830. E-mail: bfinlay{at}interchange.ubc.ca.

Editor: A. D. O'Brien

Infection and Immunity, April 2005, p. 2135-2146, Vol. 73, No. 4
0019-9567/05/$08.00+0     doi:10.1128/IAI.73.4.2135-2146.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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