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Multiple acquisitions of CTX-M plasmids in the rare D₂ genotype of Escherichia coli provide evidence for convergent evolution

¹ INSERM U722 and Université Denis Diderot-Paris 7, Faculté de Médecine, Site Xavier Bichat, Paris, France
² AP-HP, Hôpital Louis Mourier, Service de Microbiologie-Hygiène, Colombes, France
³ EA 2392, Université Pierre et Marie Curie-Paris 6, Faculté de Médecine, Site Saint-Antoine, Laboratoire de Bactériologie, Paris, France
⁴ AP-HP, Hôpital Tenon, Service de Bactériologie-Hygiène, Paris, France

Over the last decade, CTX-M enzymes have become the most prevalent extended-spectrum β-lactamases (ESBLs) worldwide, mostly in Escherichia coli, causing a major health problem. An epidemiological relationship has been established between a rare genotype of E. coli, the D₂ genotype, and the presence of CTX-M genes. We investigated this striking association by exploring the genetic backgrounds of 18 D₂ genotype CTX-M-producing strains and of the plasmids encoding CTX-M enzymes. The 18 strains had different genetic backgrounds, as assessed by multilocus sequence and O typing, and were associated with various plasmids bearing diverse CTX-M genes. The region encompassing the genetic marker of the D₂ genotype (TSPE4.C2) was not correlated with the presence of CTX-M genes. CTX-M-producing D₂ strains had far fewer virulence factors than a control group of 8 non-ESBL-producing D₂ strains, and an inverse relationship was found between the number of co-resistances associated with the CTX-M gene and the number of virulence factors found in the strain. These findings provide evidence for multiple acquisitions of plasmids carrying CTX-M genes in different D₂ genotype strains. They strongly suggest that convergent evolution has occurred, and indicate that there has been selection for the association of a specific genetic background of the strain and the CTX-M gene. This fine-tuning of the relationship between the D₂ genotype and CTX-M genes presumably increases the fitness of the strain, indicating a role for the host cell in the acquisition and dissemination of CTX-M genes.

Correspondence
Catherine Branger
catherine.branger{at}lmr.aphp.fr

Supplementary figures showing a population genetics analysis based on MLST data and a schematic representation of the genetic environment of bla_CTX-M genes from the 18 ESBL-producing D₂ E. coli isolates studied, and a supplementary table of PCR primers are available with the online version of this paper.

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