An <italic toggle="yes">In Vitro</italic> Chicken Gut Model Demonstrates Transfer of a Multidrug Resistance Plasmid from <italic toggle="yes">Salmonella</italic> to Commensal <italic toggle="yes">Escherichia coli</italic>

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 an...

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Autores principales:	Roderick M. Card, Shaun A. Cawthraw, Javier Nunez-Garcia, Richard J. Ellis, Gemma Kay, Mark J. Pallen, Martin J. Woodward, Muna F. Anjum
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	Escherichia coli Salmonella antimicrobial resistance enteric pathogens horizontal gene transfer plasmids Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/fcbcd0da39ce44bd8ccb85030835a4ed
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spelling	oai:doaj.org-article:fcbcd0da39ce44bd8ccb85030835a4ed2021-11-15T15:51:44ZAn <italic toggle="yes">In Vitro</italic> Chicken Gut Model Demonstrates Transfer of a Multidrug Resistance Plasmid from <italic toggle="yes">Salmonella</italic> to Commensal <italic toggle="yes">Escherichia coli</italic>10.1128/mBio.00777-172150-7511https://doaj.org/article/fcbcd0da39ce44bd8ccb85030835a4ed2017-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00777-17https://doaj.org/toc/2150-7511ABSTRACT 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.Roderick M. CardShaun A. CawthrawJavier Nunez-GarciaRichard J. EllisGemma KayMark J. PallenMartin J. WoodwardMuna F. AnjumAmerican Society for MicrobiologyarticleEscherichia coliSalmonellaantimicrobial resistanceenteric pathogenshorizontal gene transferplasmidsMicrobiologyQR1-502ENmBio, Vol 8, Iss 4 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	Escherichia coli Salmonella antimicrobial resistance enteric pathogens horizontal gene transfer plasmids Microbiology QR1-502
spellingShingle	Escherichia coli Salmonella antimicrobial resistance enteric pathogens horizontal gene transfer plasmids Microbiology QR1-502 Roderick M. Card Shaun A. Cawthraw Javier Nunez-Garcia Richard J. Ellis Gemma Kay Mark J. Pallen Martin J. Woodward Muna F. Anjum An <italic toggle="yes">In Vitro</italic> Chicken Gut Model Demonstrates Transfer of a Multidrug Resistance Plasmid from <italic toggle="yes">Salmonella</italic> to Commensal <italic toggle="yes">Escherichia coli</italic>
description	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.
format	article
author	Roderick M. Card Shaun A. Cawthraw Javier Nunez-Garcia Richard J. Ellis Gemma Kay Mark J. Pallen Martin J. Woodward Muna F. Anjum
author_facet	Roderick M. Card Shaun A. Cawthraw Javier Nunez-Garcia Richard J. Ellis Gemma Kay Mark J. Pallen Martin J. Woodward Muna F. Anjum
author_sort	Roderick M. Card
title	An <italic toggle="yes">In Vitro</italic> Chicken Gut Model Demonstrates Transfer of a Multidrug Resistance Plasmid from <italic toggle="yes">Salmonella</italic> to Commensal <italic toggle="yes">Escherichia coli</italic>
title_short	An <italic toggle="yes">In Vitro</italic> Chicken Gut Model Demonstrates Transfer of a Multidrug Resistance Plasmid from <italic toggle="yes">Salmonella</italic> to Commensal <italic toggle="yes">Escherichia coli</italic>
title_full	An <italic toggle="yes">In Vitro</italic> Chicken Gut Model Demonstrates Transfer of a Multidrug Resistance Plasmid from <italic toggle="yes">Salmonella</italic> to Commensal <italic toggle="yes">Escherichia coli</italic>
title_fullStr	An <italic toggle="yes">In Vitro</italic> Chicken Gut Model Demonstrates Transfer of a Multidrug Resistance Plasmid from <italic toggle="yes">Salmonella</italic> to Commensal <italic toggle="yes">Escherichia coli</italic>
title_full_unstemmed	An <italic toggle="yes">In Vitro</italic> Chicken Gut Model Demonstrates Transfer of a Multidrug Resistance Plasmid from <italic toggle="yes">Salmonella</italic> to Commensal <italic toggle="yes">Escherichia coli</italic>
title_sort	<italic toggle="yes">in vitro</italic> chicken gut model demonstrates transfer of a multidrug resistance plasmid from <italic toggle="yes">salmonella</italic> to commensal <italic toggle="yes">escherichia coli</italic>
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/fcbcd0da39ce44bd8ccb85030835a4ed
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An <italic toggle="yes">In Vitro</italic> Chicken Gut Model Demonstrates Transfer of a Multidrug Resistance Plasmid from <italic toggle="yes">Salmonella</italic> to Commensal <italic toggle="yes">Escherichia coli</italic>

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