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Journal of Bacteriology, December 2007, p. 8528-8536, Vol. 189, No. 23
0021-9193/07/$08.00+0     doi:10.1128/JB.01013-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

A New O-Antigen Gene Cluster Has a Key Role in the Virulence of the Escherichia coli Meningitis Clone O45:K1:H7

Laboratoire d'Études de Génétique Bactérienne dans les Infections de l'Enfant (EA 3105), Université Paris Diderot-Paris 7, Hôpital Robert Debré (APHP), 75019 Paris,¹ Commissariat à l'Energie Atomique, Direction des Sciences du Vivant, Institut de Génomique, Génoscope, 91057 Evry Cedex,² Commissariat à l'Energie Atomique, Direction des Sciences du Vivant, Institut de Génomique, Atelier de Génomique Comparative, CNRS UMR8030, 91057 Evry Cedex,³ Institut National de la Santé et de la Recherche Médicale U722, 75018 Paris,⁴ Université Paris Diderot-Paris 7, site Xavier Bichat, 75018 Paris, France⁵

Received 26 June 2007/ Accepted 20 September 2007

A new highly pathogenic clone of Escherichia coli meningitis strains harboring the unusual serogroup O45 has recently emerged in France. To gain insight into the pathogenicity of this new clone, we investigated the possible role of antigen O45 in the virulence of strain S88 (O45:K1:H7), representative of this emerging clone. We first showed that the S88 O-antigen gene cluster sequence differs from that of O45 in the reference strain E. coli 96-3285, suggesting that the two O45 polysaccharides, while probably sharing a community of epitopes, represent two different antigens. The unique functional organization of the two O-antigen gene clusters and the low DNA sequence homology of the orthologous genes suggest that the two loci originated from a common ancestor and have since undergone multiple recombination events. Phylogenetic analysis based on the flanking gene gnd sequences indicates that the S88 antigen O45 (O45_S88) gene cluster may have been acquired, at least in part, from another member of the Enterobacteriaceae. Mutagenesis of the O45_S88 antigen gene cluster was used for functional analysis of the loci and revealed the crucial role of the O polysaccharide in S88 virulence in a neonatal rat meningitis model. We also developed a PCR method to specifically identify the O45_S88 antigen gene cluster. Together, our findings suggest that horizontal acquisition of a new O-antigen gene cluster, at least partly from another species, may have been a key event in the emergence and virulence of the E. coli O45:K1:H7 clone in France.

Published ahead of print on 28 September 2007.