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Gene sharing among plasmids and chromosomes reveals barriers for antibiotic resistance gene transfer

The emergence of antibiotic resistant bacteria is a major threat to modern medicine. Rapid adaptation to antibiotics is often mediated by the acquisition of plasmids carrying antibiotic resistance (ABR) genes. Nonetheless, the determinants of plasmid-mediated ABR gene transfer remain debated. Here,...

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Detalles Bibliográficos
Autores principales: Wang, Yiqing, Batra, Aditi, Schulenburg, Hinrich, Dagan, Tal
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8628082/
https://www.ncbi.nlm.nih.gov/pubmed/34839702
http://dx.doi.org/10.1098/rstb.2020.0467
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author Wang, Yiqing
Batra, Aditi
Schulenburg, Hinrich
Dagan, Tal
author_facet Wang, Yiqing
Batra, Aditi
Schulenburg, Hinrich
Dagan, Tal
author_sort Wang, Yiqing
collection PubMed
description The emergence of antibiotic resistant bacteria is a major threat to modern medicine. Rapid adaptation to antibiotics is often mediated by the acquisition of plasmids carrying antibiotic resistance (ABR) genes. Nonetheless, the determinants of plasmid-mediated ABR gene transfer remain debated. Here, we show that the propensity of ABR gene transfer via plasmids is higher for accessory chromosomal ABR genes in comparison with core chromosomal ABR genes, regardless of the resistance mechanism. Analysing the pattern of ABR gene occurrence in the genomes of 2635 Enterobacteriaceae isolates, we find that 33% of the 416 ABR genes are shared between chromosomes and plasmids. Phylogenetic reconstruction of ABR genes occurring on both plasmids and chromosomes supports their evolution by lateral gene transfer. Furthermore, accessory ABR genes (encoded in less than 10% of the chromosomes) occur more abundantly in plasmids in comparison with core ABR genes (encoded in greater than or equal to 90% of the chromosomes). The pattern of ABR gene occurrence in plasmids and chromosomes is similar to that in the total Escherichia genome. Our results thus indicate that the previously recognized barriers for gene acquisition by lateral gene transfer apply also to ABR genes. We propose that the functional complexity of the underlying ABR mechanism is an important determinant of ABR gene transferability. This article is part of the theme issue ‘The secret lives of microbial mobile genetic elements’.
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spelling pubmed-86280822021-12-23 Gene sharing among plasmids and chromosomes reveals barriers for antibiotic resistance gene transfer Wang, Yiqing Batra, Aditi Schulenburg, Hinrich Dagan, Tal Philos Trans R Soc Lond B Biol Sci Articles The emergence of antibiotic resistant bacteria is a major threat to modern medicine. Rapid adaptation to antibiotics is often mediated by the acquisition of plasmids carrying antibiotic resistance (ABR) genes. Nonetheless, the determinants of plasmid-mediated ABR gene transfer remain debated. Here, we show that the propensity of ABR gene transfer via plasmids is higher for accessory chromosomal ABR genes in comparison with core chromosomal ABR genes, regardless of the resistance mechanism. Analysing the pattern of ABR gene occurrence in the genomes of 2635 Enterobacteriaceae isolates, we find that 33% of the 416 ABR genes are shared between chromosomes and plasmids. Phylogenetic reconstruction of ABR genes occurring on both plasmids and chromosomes supports their evolution by lateral gene transfer. Furthermore, accessory ABR genes (encoded in less than 10% of the chromosomes) occur more abundantly in plasmids in comparison with core ABR genes (encoded in greater than or equal to 90% of the chromosomes). The pattern of ABR gene occurrence in plasmids and chromosomes is similar to that in the total Escherichia genome. Our results thus indicate that the previously recognized barriers for gene acquisition by lateral gene transfer apply also to ABR genes. We propose that the functional complexity of the underlying ABR mechanism is an important determinant of ABR gene transferability. This article is part of the theme issue ‘The secret lives of microbial mobile genetic elements’. The Royal Society 2022-01-17 2021-11-29 /pmc/articles/PMC8628082/ /pubmed/34839702 http://dx.doi.org/10.1098/rstb.2020.0467 Text en © 2021 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Articles
Wang, Yiqing
Batra, Aditi
Schulenburg, Hinrich
Dagan, Tal
Gene sharing among plasmids and chromosomes reveals barriers for antibiotic resistance gene transfer
title Gene sharing among plasmids and chromosomes reveals barriers for antibiotic resistance gene transfer
title_full Gene sharing among plasmids and chromosomes reveals barriers for antibiotic resistance gene transfer
title_fullStr Gene sharing among plasmids and chromosomes reveals barriers for antibiotic resistance gene transfer
title_full_unstemmed Gene sharing among plasmids and chromosomes reveals barriers for antibiotic resistance gene transfer
title_short Gene sharing among plasmids and chromosomes reveals barriers for antibiotic resistance gene transfer
title_sort gene sharing among plasmids and chromosomes reveals barriers for antibiotic resistance gene transfer
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8628082/
https://www.ncbi.nlm.nih.gov/pubmed/34839702
http://dx.doi.org/10.1098/rstb.2020.0467
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