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An in vitro chicken gut model demonstrates transfer of a multidrug resistance plasmid from salmonella to commensal escherichia coli

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Card, Roderick M., Cawthraw, Shaun A., Nunez-Garcia, Javier, Ellis, Richard J., Kay, Gemma, Pallen, Mark J., Woodward, Martin J. and Anjum, Muna F. (2017) An in vitro chicken gut model demonstrates transfer of a multidrug resistance plasmid from salmonella to commensal escherichia coli. mBio, 8 (4). e00777-17. doi:10.1128/mBio.00777-17 ISSN 2150-7511.

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Official URL: https://doi.org/10.1128/mBio.00777-17

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Abstract

The chicken gastrointestinal tract is richly populated by commensal bacteria that fulfill various beneficial roles for the host, including helping to resist colonization by pathogens. It can also facilitate the conjugative transfer of multidrug resistance (MDR) plasmids between commensal and pathogenic bacteria which is a significant public and animal health concern as it may affect our ability to treat bacterial infections. We used an in vitro chemostat system to approximate the chicken cecal microbiota, simulate colonization by an MDR Salmonella pathogen, and examine the dynamics of transfer of its MDR plasmid harboring several genes, including the extended-spectrum beta-lactamase blaCTX-M1 We also evaluated the impact of cefotaxime administration on plasmid transfer and microbial diversity. Bacterial community profiles obtained by culture-independent methods showed that Salmonella inoculation resulted in no significant changes to bacterial community alpha diversity and beta diversity, whereas administration of cefotaxime caused significant alterations to both measures of diversity, which largely recovered. MDR plasmid transfer from Salmonella to commensal Escherichia coli was demonstrated by PCR and whole-genome sequencing of isolates purified from agar plates containing cefotaxime. Transfer occurred to seven E. coli sequence types at high rates, even in the absence of cefotaxime, with resistant strains isolated within 3 days. Our chemostat system provides a good representation of bacterial interactions, including antibiotic resistance transfer in vivo It can be used as an ethical and relatively inexpensive approach to model dissemination of antibiotic resistance within the gut of any animal or human and refine interventions that mitigate its spread before employing in vivo studies.IMPORTANCE The spread of antimicrobial resistance presents a grave threat to public health and animal health and is affecting our ability to respond to bacterial infections. Transfer of antimicrobial resistance via plasmid exchange is of particular concern as it enables unrelated bacteria to acquire resistance. The gastrointestinal tract is replete with bacteria and provides an environment for plasmid transfer between commensals and pathogens. Here we use the chicken gut microbiota as an exemplar to model the effects of bacterial infection, antibiotic administration, and plasmid transfer. We show that transfer of a multidrug-resistant plasmid from the zoonotic pathogen Salmonella to commensal Escherichia coli occurs at a high rate, even in the absence of antibiotic administration. Our work demonstrates that the in vitro gut model provides a powerful screening tool that can be used to assess and refine interventions that mitigate the spread of antibiotic resistance in the gut before undertaking animal studies. [Abstract copyright: Copyright © 2017 Card et al.]

Item Type: Journal Article
Divisions: Faculty of Science, Engineering and Medicine > Medicine > Warwick Medical School > Biomedical Sciences > Microbiology & Infection
Faculty of Science, Engineering and Medicine > Medicine > Warwick Medical School
SWORD Depositor: Library Publications Router
Journal or Publication Title: mBio
Publisher: American Society for Microbiology
ISSN: 2150-7511
Official Date: 18 July 2017
Dates:
DateEvent
18 July 2017Published
6 June 2017Accepted
Volume: 8
Number: 4
Article Number: e00777-17
DOI: 10.1128/mBio.00777-17
Status: Peer Reviewed
Publication Status: Published
Reuse Statement (publisher, data, author rights): ** From PubMed via Jisc Publications Router.
Access rights to Published version: Restricted or Subscription Access

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