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Infection and Immunity, November 2009, p. 4696-4703, Vol. 77, No. 11
0019-9567/09/$08.00+0 doi:10.1128/IAI.00522-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.
Genetic Structure and Distribution of the Colibactin Genomic Island among Members of the Family Enterobacteriaceae
,
Johannes Putze,1
Claire Hennequin,2
Jean-Philippe Nougayrède,3
Wenlan Zhang,4
Stefan Homburg,1
Helge Karch,4
Marie-Agnés Bringer,5
Corinne Fayolle,6
Elisabeth Carniel,6
Wolfgang Rabsch,7
Tobias A. Oelschlaeger,1
Eric Oswald,3
Christiane Forestier,2
Jörg Hacker,1,8 and
Ulrich Dobrindt1*
Julius-Maximilians-Universität Würzburg, Institut für Molekulare Infektionsbiologie, Röntgenring 11, 97070 Würzburg, Germany,1 Université d'Auvergne-Clermont1, UFR Pharmacie, Laboratoire de Bactériologie, 28 Place H. Dunant, 63000 Clermont-Ferrand, France,2 INRA, UMR1225, F-31076 Toulouse, France, and Université de Toulouse, ENVT, UMR1225, F-31076 Toulouse, France,3 Institut für Hygiene, Universität Münster, Robert Koch-Str. 41, 48149 Münster, Germany,4 Institut Pasteur, Unité de Pathogénie Microbienne Moléculaire and Unité INSERM 786, 28, Rue du Dr Roux, 75724 Paris, Cedex 15, France,5 Yersinia Research Unit, Institut Pasteur, 28, Rue du Dr Roux, 75724 Paris Cedex 15, France,6 Robert-Koch-Institut, Aussenstelle Wernigerode, Burgstrasse 37, 38855 Wernigerode, Germany,7 Robert-Koch Institut, Nordufer 20, 13353 Berlin, Germany8
Received 11 May 2009/ Returned for modification 16 June 2009/ Accepted 22 July 2009
A genomic island encoding the biosynthesis and secretion pathway of putative hybrid nonribosomal peptide-polyketide colibactin has been recently described in Escherichia coli. Colibactin acts as a cyclomodulin and blocks the eukaryotic cell cycle. The origin and prevalence of the colibactin island among enterobacteria are unknown. We therefore screened 1,565 isolates of different genera and species related to the Enterobacteriaceae by PCR for the presence of this DNA element. The island was detected not only in E. coli but also in Klebsiella pneumoniae, Enterobacter aerogenes, and Citrobacter koseri isolates. It was highly conserved among these species and was always associated with the yersiniabactin determinant. Structural variations between individual strains were only observed in an intergenic region containing variable numbers of tandem repeats. In E. coli, the colibactin island was usually restricted to isolates of phylogenetic group B2 and inserted at the asnW tRNA locus. Interestingly, in K. pneumoniae, E. aerogenes, C. koseri, and three E. coli strains of phylogenetic group B1, the functional colibactin determinant was associated with a genetic element similar to the integrative and conjugative elements ICEEc1 and ICEKp1 and to several enterobacterial plasmids. Different asn tRNA genes served as chromosomal insertion sites of the ICE-associated colibactin determinant: asnU in the three E. coli strains of ECOR group B1, and different asn tRNA loci in K. pneumoniae. The detection of the colibactin genes associated with an ICE-like element in several enterobacteria provides new insights into the spread of this gene cluster and its putative mode of transfer. Our results shed light on the mechanisms of genetic exchange between members of the family Enterobacteriaceae.
* Corresponding author. Mailing address: Institut für Molekulare Infektionsbiologie, Röntgenring 11, D-97070 Würzburg, Germany. Phone: 49 931 312155. Fax: 49 931 312578. E-mail: ulrich.dobrindt{at}mail.uni-wuerzburg.de
Published ahead of print on 31 August 2009.
Supplemental material for this article may be found at http://iai.asm.org/.
Infection and Immunity, November 2009, p. 4696-4703, Vol. 77, No. 11
0019-9567/09/$08.00+0 doi:10.1128/IAI.00522-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.
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