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Journal of Bacteriology, January 2008, p. 275-285, Vol. 190, No. 1
0021-9193/08/$08.00+0     doi:10.1128/JB.00844-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.

Distribution, Functional Expression, and Genetic Organization of Cif, a Phage-Encoded Type III-Secreted Effector from Enteropathogenic and Enterohemorrhagic Escherichia coli{triangledown}

Estelle Loukiadis,1 Rika Nobe,1 Sylvia Herold,2 Clara Tramuta,3 Yoshitoshi Ogura,4,5 Tadasuke Ooka,4,5 Stefano Morabito,6 Monique Kérourédan,1 Hubert Brugère,1 Herbert Schmidt,7 Tetsuya Hayashi,5,6 and Eric Oswald1*

INRA, UMR 1225, Ecole Nationale Vétérinaire de Toulouse, Toulouse 31076, France,1 Institute of Medical Microbiology and Hygiene, Technical University of Dresden, 01307 Dresden, Germany,2 Dipartimento di Produzioni Animali, Epidemiologia ed Ecologia, Facoltà di Medicina Veterinaria, Università degli Studi di Torino, 10095 Grugliasco (TO), Italy,3 Division of Bioenvironmental Science, Frontier Science Research Center, University of Miyazaki, Miyazaki 889-1692, Japan,4 Division of Microbiology, Department of Infectious Diseases, Faculty of Medicine, University of Miyazaki, Miyazaki 889-1692, Japan,5 Istituto Superiore di Sanità, Dipartimento di Sanità Alimentare e Animale, 00161 Rome, Italy,6 Institute of Food Science and Biotechnology, Department of Food Microbiology, University of Hohenheim, 70599 Stuttgart, Germany7

Received 31 May 2007/ Accepted 6 September 2007

Enteropathogenic Escherichia coli (EPEC) and enterohemorrhagic E. coli (EHEC) inject effector proteins into host cells via a type III secretion system encoded by the locus of enterocyte effacement (LEE). One of these effectors is Cif, encoded outside the LEE by a lambdoid prophage. In this study, we demonstrated that the Cif-encoding prophage of EPEC strain E22 is inducible and produces infectious phage particles. We investigated the distribution and functional expression of Cif in 5,049 E. coli strains of human, animal, and environmental origins. A total of 115 E. coli isolates from diverse origins and geographic locations carried cif. The presence of cif was tightly associated with the LEE, since all the cif-positive isolates were positive for the LEE. These results suggested that the Cif-encoding prophages have been widely disseminated within the natural population of E. coli but positively selected within the population of LEE-positive strains. Nonetheless, 66% of cif-positive E. coli strains did not induce a typical Cif-related phenotype in eukaryotic cells due to frameshift mutations or insertion of an IS element in the cif gene. The passenger region of the prophages carrying cif was highly variable and showed various combinations of IS elements and genes coding for other effectors such as nleB, nleC, nleH, nleG, espJ, and nleA/espI (some of which were also truncated). This diversity and the presence of nonfunctional effectors should be taken into account to assess EPEC and EHEC pathogenicity and tropism.

* Corresponding author. Mailing address: INRA, UMR1225 Interactions Hôtes-Agents Pathogènes, Ecole Nationale Vétérinaire de Toulouse, BP 87614, 23 chemin des Capelles, F-31076 Toulouse Cedex 03, France. Phone: 33 (0)5 61 19 39 91. Fax: 33 (0)5 61 19 39 75. E-mail: e.oswald{at}envt.fr

{triangledown} Published ahead of print on 14 September 2007.

Journal of Bacteriology, January 2008, p. 275-285, Vol. 190, No. 1
0021-9193/08/$08.00+0     doi:10.1128/JB.00844-07
Copyright © 2008, American Society for Microbiology. All Rights Reserved.



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