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Escherichia coli carrying blaNDM-1 obtained from a migratory penguin (Spheniscus magellanicus) in the Brazilian seacoast

  • Veterinary Microbiology - Short Communication
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Abstract

The reservoirs for NDM-producing Enterobacterales are increasing, not only in hospitals, but also in the environment and in the community, challenging the therapeutic efficacy of carbapenems. We aimed to characterize an isolate of Escherichia coli harboring the blaNDM-1 gene recovered from the bloodstream of a penguin (Spheniscus magellanicus) in Southern Brazil. A total of 74 bacterial isolates recovered from arterial blood samples from dead birds were submitted to species identification and antibiotic susceptibility evaluation. One isolate presented resistance to carbapenems (E. coli 89PenNDM) and proved to harbor the blaNDM-1 gene by multiplex high-resolution melting real-time PCR (PCR-HRM). Conjugation experiments indicated that the blaNDM-1 was transmissible to E. coli J53. Whole genome sequencing (WGS) confirmed the presence of the blaNDM-1 gene in a conjugative plasmid (IncA/C2 plasmid) in both the E. coli 89PenNDM and its transconjugants. The isolate was classified as ST 156 and many other resistance genes (e.g., sul1, sul,2, strA, floR, tet(A)) were identified, all carried in the same IncA/C2 plasmid. This is the first report of blaNDM-1-producing E. coli isolated from a penguin in the Brazilian seacoast. The presence of a carbapenemase gene in wildlife animals is of concern as they may become reservoirs of multidrug-resistant bacteria and disseminate them to the environment.

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Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

Code availability

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References

  1. Nordmann P, Cuzon G, Naas T (2009) The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet Infect Dis 9:228–236. https://doi.org/10.1016/S1473-3099(09)70054-4

    Article  CAS  PubMed  Google Scholar 

  2. Johnson AP, Woodford N (2013) Global spread of antibiotic resistance: the example of New Delhi metallo-β-lactamase (NDM)-mediated carbapenem resistance. J Med Microbiol 62:499–513. https://doi.org/10.1099/jmm.0.052555-0

    Article  CAS  PubMed  Google Scholar 

  3. Dortet L, Poirel L, Nordmann P (2014) Worldwide dissemination of the NDM-type carbapenemases in Gram-negative bacteria. Biomed Res Int 2014:249856. https://doi.org/10.1155/2014/249856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Nordmann P, Naas T, Poirel L (2011) Global spread of carbapenemase producing Enterobacteriaceae. Emerg Infect Dis 17:1791–1798. https://doi.org/10.3201/eid1710.110655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Köck R, Daniels-Haardt I, Becker K, Mellmann A, Friedrich AW, Mevius D, Schwarz S, Jurke A (2018) Carbapenem-resistant Enterobacteriaceae in wildlife, food-producing, and companion animals: a systematic review. Clin Microbiol Infect 24:1241–1250. https://doi.org/10.1016/j.cmi.2018.04.004

    Article  PubMed  Google Scholar 

  6. Guerra B, Fischer J, Helmuth R (2014) An emerging public health problem: acquired carbapenemase-producing microorganisms are present in food-producing animals, their environment, companion animals and wild birds. Vet Microbiol 171:290–297. https://doi.org/10.1016/j.vetmic.2014.02.001

    Article  PubMed  Google Scholar 

  7. Quinete N, Hauser-Davis RA, Lemos LS, Moura JF, Siciliano S, Gardinali PR (2020) Occurrence and tissue distribution of organochlorinated compounds and polycyclic aromatic hydrocarbons in Magellanic penguins (Spheniscus magellanicus) from the southeastern coast of Brazil. Sci Total Environ 749:141473. https://doi.org/10.1016/j.scitotenv.2020.141473

    Article  CAS  PubMed  Google Scholar 

  8. Clinical and Laboratory Standards Institute (2014) Performance standards for antimicrobial susceptibility testing. Twenty-Fourth informational supplement. M100–S24. CLSI, Wayne

    Google Scholar 

  9. Pires J, Novais A, Peixe L (2013) Blue-carba, an easy biochemical test for detection of diverse carbapenemase producers directly from bacterial cultures. J Clin Microbiol 51:4281–4283. https://doi.org/10.1128/JCM.01634-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Monteiro J, Widen RH, Pignatari AC, Kubasek C, Silbert S (2012) Rapid detection of carbapenemase genes by multiplex real-time PCR. J Antimicrob Chemother 67:906–909. https://doi.org/10.1093/jac/dkr563

    Article  CAS  PubMed  Google Scholar 

  11. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, Olson R, Overbeek R, Parrello B, Pusch GD, Shukla M, Thomason JA 3rd, Stevens R, Vonstein V, Wattam AR, Xia F (2015) RASTtk: a modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 5:8365. https://doi.org/10.1038/srep08365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Tang B, Chang J, Cao L, Luo Q, Xu H, Lyu W, Qian M, Ji X, Zhang Q, Xia X, Yang H (2019) Characterization of an NDM-5 carbapenemase-producing Escherichia coli ST156 isolate from a poultry farm in Zhejiang, China. BMC Microbiol 25:19–82. https://doi.org/10.1186/s12866-019-1454-2

    Article  Google Scholar 

  14. Fischer J, Schmoger S, Jahn S, Helmuth R, Guerra B (2013) NDM-1 carbapenemase-producing Salmonella enterica subsp. enterica serovar Corvallis isolated from a wild bird in Germany. J Antimicrob Chemother 68:2954–2956. https://doi.org/10.1093/jac/dkt260

    Article  CAS  PubMed  Google Scholar 

  15. Villa L, Guerra B, Schmoger S, Fischer J, Helmuth R, Zong Z, García-Fernández A, Carattoli A (2015) IncA/C plasmid carrying bla(NDM-1), bla(CMY-16), and fosA3 in a Salmonella enterica serovar Corvallis strain isolated from a migratory wild bird in Germany. Antimicrob Agents Chemother 59:6597–6600. https://doi.org/10.1128/AAC.00944-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Wailan AM, Sidjabat HE, Yam WK, Alikhan NF, Petty NK, Sartor AL, Williamson DA, Forde BM, Schembri MA, Beatson SA, Paterson DL, Walsh TR, Partridge SR (2016) Mechanisms involved in acquisition of blaNDM genes by IncA/C2 and IncFIIY plasmids. Antimicrob Agents Chemother 60:4082–8. https://doi.org/10.1128/AAC.00368-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Hadziabdic S, Fischer J, Malorny B, Borowiak M, Guerra B, Kaesbohrer A, Gonzalez-Zorn B, Szabo I (2018) In vivo transfer and microevolution of avian native IncA/C2blaNDM-1-carrying plasmid pRH-1238 during a broiler chicken infection study. Antimicrob Agents Chemother 62:e02128-e2217. https://doi.org/10.1128/AAC.02128-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Wink PL, Almeida EK, Crispim MN, de Lima-Morales D, Zavascki AP, Barth AL (2020) First report of IMP-1 in a clinical isolate of Escherichia coli in Latin America. Infect Control Hosp Epidemiol 41:997–998. https://doi.org/10.1017/ice.2020.44

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors would like to thank Evelin Kern Almeida, Helena de Ávila Peixoto e Silva, Marina Crispin, Cristiane Kiyomi Miyaji Kolesnikovas, and Bruna Silva da Silva for technical support.

Funding

This work was supported by INPRA — Instituto Nacional de Pesquisa em Resistência Antimicrobiana — Brazil (FIPE/HCPA: 2019–0203, INCT/CNPq: 465718/2014–0 and INCT/FAPERGS: 17/2551–0000514-7).

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Authors

Contributions

All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Priscila L. Wink, Daiana de Lima-Morales, and Rafael Meurer. The first draft of the manuscript was written by Priscila L. Wink and Daiana de Lima-Morales and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Afonso L. Barth.

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Ethics approval

Animals were collected under ABIO 640/2015, emitted as part of the environmental licensing process required by IBAMA for oil production and transportation by Petrobras in the pre-salt province.

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The authors declare no competing interests.

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Responsible Editor: Nilton Lincopan

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Nucleotide sequence accession number

This Whole Genome Shotgun project has been deposited at DDBJ/ENA/GenBank under the accession WTFK00000000. The version described in this paper is version WTFK01000000.

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Wink, P.L., Lima-Morales, D., Meurer, R. et al. Escherichia coli carrying blaNDM-1 obtained from a migratory penguin (Spheniscus magellanicus) in the Brazilian seacoast. Braz J Microbiol 53, 499–502 (2022). https://doi.org/10.1007/s42770-021-00652-7

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  • DOI: https://doi.org/10.1007/s42770-021-00652-7

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