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First Identification of bla NDM-1 Producing Escherichia coli ST 9499 Isolated from Musca domestica in the Urban Center of Rio de Janeiro, Brazil

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Abstract

The present study presents phenotypic and molecular characterization of a multidrug-resistant strain of Escherichia coli (Lemef26), belonging to sequence type ST9499 carrying a blaNDM-1 carbapenem resistance gene. The bacterium was isolated from a specimen of Musca domestica, collected in proximity to a hospital in Rio de Janeiro City, Brazil. The strain was identified as E. coli by matrix-assisted laser desorption-ionization time of flight mass spectrometry (Maldi-TOF–MS) and via genotypic analysis (Whole-Genome Sequencing—WGS), followed by phylogenetic analysis, antibiotic resistance profiling (using phenotypic and genotypic methods) and virulence genotyping. Interestingly, the blaNDM-1 was the only resistance determinant detected using a panel of common resistance genes, as evaluated by PCR. In contrast, WGS detected genes conferring resistance to aminoglycosides, fluoroquinolones, quinolones, trimethoprim, beta-lactams, chloramphenicol, macrolides, sulfonamide, tetracycline, lincosamide and streptogramin B. Conjugation experiments demonstrated the transfer of carbapenem resistance, via acquisition of the blaNDM-1 sequence, to a sensitive receptor strain of E. coli, indicating that blaNDM-1 is located on a conjugative plasmid (most likely of the IncA/C incompatibility group, in association with the transposon Tn3000). Phylogenetic analyses placed Lemef26 within a clade of strains exhibiting allelic and environment diversity, with the greatest level of relatedness recorded with a strain isolated from a human source suggesting a possible anthropogenic origin. Analysis of the virulome revealed the presence of fimbrial and pilus genes, including a CFA/I fimbriae (cfaABCDE), common pilus (ecpABCDER), laminin-bind fimbrae (elfADG), hemorrhagic pilus (hcpABC) and fimbrial adherence determinants (stjC) indicates the ability of strain Lemef26 to colonize animal hosts. To the best of our knowledge, this study represents the first report of blaNDM-1 carbapenemase gene in an E. coli strain isolated from M. domestica. In concordance with the findings of previous studies on the carriage of MDR bacteria by flies, the data presented herein provide support to the idea that flies may represent a convenient means (as sentinel animals) for the monitoring of environmental contamination with multidrug-resistant bacteria.

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Acknowledgements

Isabel N Carramaschi acknowledges to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes). The authors acknowledge Faperj for financial support (proc n E-26/210.228/2018). The authors acknowledge Dr Alberto R. D´Avila (IOC/FIOCRUZ) for the opportunity to use Illumina MiSeq for Whole-Genome Sequencing.

Funding

Faperj 26/210.228/2018.

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Authors and Affiliations

  1. Laboratório de Entomologia Médica e Forense, Instituto Oswaldo Cruz, Fiocruz, Avenida Brasil, 4365, Manguinhos, Rio de Janeiro, RJ, Cep 21040-360, Brazil

    Isabel N. Carramaschi, Margareth M. de C Queiroz & Viviane Zahner

  2. Laboratório de Biologia Computacional e Sistemas, Instituto Oswaldo Cruz, Fiocruz, Avenida Brasil, 4365, Manguinhos, Rio de Janeiro, RJ, Cep 21040-360, Brazil

    Fabio Faria da Mota

  3. Instituto Nacional de Ciência e Tecnologia em Entomologia Molecular (INCT-EM), Rio de Janeiro, RJ, Brazil

    Fabio Faria da Mota

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  1. Isabel N. Carramaschi
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  2. Margareth M. de C Queiroz
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  3. Fabio Faria da Mota
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  4. Viviane Zahner
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Contributions

INC: sample collection and perform the experiments, data analysis, manuscript writing. MMdCQ: design the experiments concerning flies capture. FFdM: perform the experiments and data analysis, manuscript writing. VZ: conceive and design the experiments, data analysis, manuscript writing.

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Correspondence to Viviane Zahner.

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Carramaschi, I.N., de C Queiroz, M.M., da Mota, F.F. et al. First Identification of bla NDM-1 Producing Escherichia coli ST 9499 Isolated from Musca domestica in the Urban Center of Rio de Janeiro, Brazil. Curr Microbiol 80, 278 (2023). https://doi.org/10.1007/s00284-023-03393-y

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