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Stepwise evolution and convergent recombination underlie the global dissemination of carbapenemase-producing Escherichia coli.

ABSTRACT: BACKGROUND:Carbapenem-resistant Enterobacteriaceae are considered by WHO as "critical" priority pathogens for which novel antibiotics are urgently needed. The dissemination of carbapenemase-producing Escherichia coli (CP-Ec) in the community is a major public health concern. However, the global molecular epidemiology of CP-Ec isolates remains largely unknown as well as factors contributing to the acquisition of carbapenemase genes. METHODS:We first analyzed the whole-genome sequence and the evolution of the E. coli sequence type (ST) 410 and its disseminated clade expressing the carbapenemase OXA-181. We reconstructed the phylogeny of 19 E. coli ST enriched in CP-Ec and corresponding to a total of 2026 non-redundant isolates. Using the EpiCs software, we determined the significance of the association between specific mutations and the acquisition of a carbapenemase gene and the most probable order of events. The impact of the identified mutations was assessed experimentally by genetic manipulations and phenotypic testing. RESULTS:In 13 of the studied STs, acquisition of carbapenemase genes occurred in multidrug-resistant lineages characterized by a combination of mutations in ftsI encoding the penicillin-binding protein 3 and in the porin genes ompC and ompF. Mutated ftsI genes and a specific ompC allele related to that from ST38 inducing reduced susceptibility to diverse ?-lactams spread across the species by recombination. We showed that these mutations precede in most cases the acquisition of a carbapenemase gene. The ompC allele from ST38 might have contributed to the selection of CP-Ec disseminated lineages within this ST. On the other hand, in the pandemic ST131 lineage, CP-Ec were not associated with mutations in ompC or ftsI and show no signs of dissemination. CONCLUSIONS:Lineages of CP-Ec have started to disseminate globally. However, their selection is a multistep process involving mutations, recombination, acquisition of antibiotic resistance genes, and selection by ?-lactams from diverse families. This process did not yet occur in the high-risk lineage ST131.

SUBMITTER: Patino-Navarrete R

PROVIDER: S-EPMC6970295 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Stepwise evolution and convergent recombination underlie the global dissemination of carbapenemase-producing Escherichia coli.

Patiño-Navarrete Rafael R Rosinski-Chupin Isabelle I Cabanel Nicolas N Gauthier Lauraine L Takissian Julie J Madec Jean-Yves JY Hamze Monzer M Bonnin Remy A RA Naas Thierry T Glaser Philippe P

Genome medicine 20200120 1

<h4>Background</h4>Carbapenem-resistant Enterobacteriaceae are considered by WHO as "critical" priority pathogens for which novel antibiotics are urgently needed. The dissemination of carbapenemase-producing Escherichia coli (CP-Ec) in the community is a major public health concern. However, the global molecular epidemiology of CP-Ec isolates remains largely unknown as well as factors contributing to the acquisition of carbapenemase genes.<h4>Methods</h4>We first analyzed the whole-genome sequen ...[more]

PMID: 31955713

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Project description:BACKGROUND:The rapidly increasing dissemination of carbapenem-resistant Enterobacteriaceae (CRE) in both humans and animals poses a global threat to public health. However, the transmission of CRE between humans and animals has not yet been well studied. OBJECTIVES:We investigated the prevalence, risk factors, and drivers of CRE transmission between humans and their backyard animals in rural China. METHODS:We conducted a comprehensive sampling strategy in 12 villages in Shandong, China. Using the household [residents and their backyard animals (farm and companion animals)] as a single surveillance unit, we assessed the prevalence of CRE at the household level and examined the factors associated with CRE carriage through a detailed questionnaire. Genetic relationships among human- and animal-derived CRE were assessed using whole-genome sequencing-based molecular methods. RESULTS:A total of 88 New Delhi metallo-?-lactamases-type carbapenem-resistant Escherichia coli (NDM-EC), including 17 from humans, 44 from pigs, 12 from chickens, 1 from cattle, and 2 from dogs, were isolated from 65 of the 746 households examined. The remaining 12 NDM-EC were from flies in the immediate backyard environment. The NDM-EC colonization in households was significantly associated with a) the number of species of backyard animals raised/kept in the same household, and b) the use of human and/or animal feces as fertilizer. Discriminant analysis of principal components (DAPC) revealed that a large proportion of the core genomes of the NDM-EC belonged to strains from hosts other than their own, and several human isolates shared closely related core single-nucleotide polymorphisms and blaNDM genetic contexts with isolates from backyard animals. CONCLUSIONS:To our knowledge, we are the first to report evidence of direct transmission of NDM-EC between humans and animals. Given the rise of NDM-EC in community and hospital infections, combating NDM-EC transmission in backyard farm systems is needed. https://doi.org/10.1289/EHP5251.

Dataset Information

Stepwise evolution and convergent recombination underlie the global dissemination of carbapenemase-producing Escherichia coli.

Publications

Stepwise evolution and convergent recombination underlie the global dissemination of carbapenemase-producing Escherichia coli.

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