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Contribution of Different Mechanisms to Ciprofloxacin Resistance in Salmonella spp.

Development of fluoroquinolone resistance can involve several mechanisms that include chromosomal mutations in genes (gyrAB and parCE) encoding the target bacterial topoisomerase enzymes, increased expression of the AcrAB-TolC efflux system, and acquisition of transmissible quinolone-resistance gene...

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Autores principales: Chang, Man-Xia, Zhang, Jin-Fei, Sun, Yin-Huan, Li, Rong-Sheng, Lin, Xiao-Ling, Yang, Ling, Webber, Mark A., Jiang, Hong-Xia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8137344/
https://www.ncbi.nlm.nih.gov/pubmed/34025618
http://dx.doi.org/10.3389/fmicb.2021.663731
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author Chang, Man-Xia
Zhang, Jin-Fei
Sun, Yin-Huan
Li, Rong-Sheng
Lin, Xiao-Ling
Yang, Ling
Webber, Mark A.
Jiang, Hong-Xia
author_facet Chang, Man-Xia
Zhang, Jin-Fei
Sun, Yin-Huan
Li, Rong-Sheng
Lin, Xiao-Ling
Yang, Ling
Webber, Mark A.
Jiang, Hong-Xia
author_sort Chang, Man-Xia
collection PubMed
description Development of fluoroquinolone resistance can involve several mechanisms that include chromosomal mutations in genes (gyrAB and parCE) encoding the target bacterial topoisomerase enzymes, increased expression of the AcrAB-TolC efflux system, and acquisition of transmissible quinolone-resistance genes. In this study, 176 Salmonella isolates from animals with a broad range of ciprofloxacin MICs were collected to analyze the contribution of these different mechanisms to different phenotypes. All isolates were classified according to their ciprofloxacin susceptibility pattern into five groups as follows: highly resistant (HR), resistant (R), intermediate (I), reduced susceptibility (RS), and susceptible (S). We found that the ParC T57S substitution was common in strains exhibiting lowest MICs of ciprofloxacin while increased MICs depended on the type of GyrA mutation. The ParC T57S substitution appeared to incur little cost to bacterial fitness on its own. The presence of PMQR genes represented an route for resistance development in the absence of target-site mutations. Switching of the plasmid-mediated quinolone resistance (PMQR) gene location from a plasmid to the chromosome was observed and resulted in decreased ciprofloxacin susceptibility; this also correlated with increased fitness and a stable resistance phenotype. The overexpression of AcrAB-TolC played an important role in isolates with small decreases in susceptibility and expression was upregulated by MarA more often than by RamA. This study increases our understanding of the relative importance of several resistance mechanisms in the development of fluoroquinolone resistance in Salmonella from the food chain.
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spelling pubmed-81373442021-05-21 Contribution of Different Mechanisms to Ciprofloxacin Resistance in Salmonella spp. Chang, Man-Xia Zhang, Jin-Fei Sun, Yin-Huan Li, Rong-Sheng Lin, Xiao-Ling Yang, Ling Webber, Mark A. Jiang, Hong-Xia Front Microbiol Microbiology Development of fluoroquinolone resistance can involve several mechanisms that include chromosomal mutations in genes (gyrAB and parCE) encoding the target bacterial topoisomerase enzymes, increased expression of the AcrAB-TolC efflux system, and acquisition of transmissible quinolone-resistance genes. In this study, 176 Salmonella isolates from animals with a broad range of ciprofloxacin MICs were collected to analyze the contribution of these different mechanisms to different phenotypes. All isolates were classified according to their ciprofloxacin susceptibility pattern into five groups as follows: highly resistant (HR), resistant (R), intermediate (I), reduced susceptibility (RS), and susceptible (S). We found that the ParC T57S substitution was common in strains exhibiting lowest MICs of ciprofloxacin while increased MICs depended on the type of GyrA mutation. The ParC T57S substitution appeared to incur little cost to bacterial fitness on its own. The presence of PMQR genes represented an route for resistance development in the absence of target-site mutations. Switching of the plasmid-mediated quinolone resistance (PMQR) gene location from a plasmid to the chromosome was observed and resulted in decreased ciprofloxacin susceptibility; this also correlated with increased fitness and a stable resistance phenotype. The overexpression of AcrAB-TolC played an important role in isolates with small decreases in susceptibility and expression was upregulated by MarA more often than by RamA. This study increases our understanding of the relative importance of several resistance mechanisms in the development of fluoroquinolone resistance in Salmonella from the food chain. Frontiers Media S.A. 2021-05-06 /pmc/articles/PMC8137344/ /pubmed/34025618 http://dx.doi.org/10.3389/fmicb.2021.663731 Text en Copyright © 2021 Chang, Zhang, Sun, Li, Lin, Yang, Webber and Jiang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Chang, Man-Xia
Zhang, Jin-Fei
Sun, Yin-Huan
Li, Rong-Sheng
Lin, Xiao-Ling
Yang, Ling
Webber, Mark A.
Jiang, Hong-Xia
Contribution of Different Mechanisms to Ciprofloxacin Resistance in Salmonella spp.
title Contribution of Different Mechanisms to Ciprofloxacin Resistance in Salmonella spp.
title_full Contribution of Different Mechanisms to Ciprofloxacin Resistance in Salmonella spp.
title_fullStr Contribution of Different Mechanisms to Ciprofloxacin Resistance in Salmonella spp.
title_full_unstemmed Contribution of Different Mechanisms to Ciprofloxacin Resistance in Salmonella spp.
title_short Contribution of Different Mechanisms to Ciprofloxacin Resistance in Salmonella spp.
title_sort contribution of different mechanisms to ciprofloxacin resistance in salmonella spp.
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8137344/
https://www.ncbi.nlm.nih.gov/pubmed/34025618
http://dx.doi.org/10.3389/fmicb.2021.663731
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