Advantage of the F2A1B- IncF Pandemic Plasmid over IncC Plasmids in In Vitro Acquisition and Evolution of bla(CTX-M )Gene-Bearing Plasmids in Escherichia coli

• Published in: Antimicrobial agents and chemotherapy 2019, Vol.63 (10), p.e01130-19
• Main Authors: Maherault, Anne-Claire, Kemble, Harry, Magnan, Mélanie, Gachet, Benoit, Roche, David, Le Nagard, Hervé, Tenaillon, Olivier, Denamur, Erick, Branger, Catherine, Landraud, Luce
• Format: Article
• Language: English
• Subjects: Computer Science; Digital Libraries
• ISSN: 0066-4804; 1098-6596
• DOI: 10.1128/AAC.01130-19

Despite a fitness cost imposed on bacterial hosts, large conjugative plasmids play a key role in the diffusion of resistance determinants, such as CTX-M extended-spectrum beta-lactamases. Among the large conjugative plasmids, IncF plasmids are the most predominant group, and an F2A1B- IncF-type plasmid encoding a CTX-M-15 variant was recently described as being strongly associated with the emerging worldwide Escherichia coli sequence type 131 (ST131)-O25bH4 H30Rx/C2 sublineage. In this context, we investigated the fitness cost of narrow-range F-type plasmids, including the F2A1B- IncF-type CTX-M-15 plasmid, and of broad-range C-type plasmids in the K-12-like J53-2 E. coli strain. Although all plasmids imposed a significant fitness cost to the bacterial host immediately after conjugation, we show, using an experimental-evolution approach, that a negative impact on the fitness of the host strain was maintained throughout 1,120 generations with the IncC-IncR plasmid, regardless of the presence or absence of cefotaxime, in contrast to the F2 A1B- IncF plasmid, whose cost was alleviated. Many chromosomal and plasmid rear-rangements were detected after conjugation in transconjugants carrying the IncC plasmids but not in transconjugants carrying the F2A1B- IncF plasmid, except for insertion sequence (IS) mobilization from the filM gene leading to the restoration of motility of the recipient strains. Only a few mutations occurred on the chromosome of each transconjugant throughout the experimental-evolution assay. Our findings indicate that the F2A1B- IncF CTX-M-15 plasmid is well adapted to the E. coli strain studied, contrary to the IncC-IncR CTX-M-15 plasmid, and that such plasmid-host adaptation could participate in the evolutionary success of the CTX-M-15-producing pandemic E. coli ST131-O25bH4 lineage.