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The role of interspecies recombination in the evolution of antibiotic-resistant pneumococci

Multidrug-resistant Streptococcus pneumoniae emerge through the modification of core genome loci by interspecies homologous recombinations, and acquisition of gene cassettes. Both occurred in the otherwise contrasting histories of the antibiotic-resistant S. pneumoniae lineages PMEN3 and PMEN9. A si...

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Autores principales: D'Aeth, Joshua C, van der Linden, Mark PG, McGee, Lesley, de Lencastre, Herminia, Turner, Paul, Song, Jae-Hoon, Lo, Stephanie W, Gladstone, Rebecca A, Sá-Leão, Raquel, Ko, Kwan Soo, Hanage, William P, Breiman, Robert F, Beall, Bernard, Bentley, Stephen D, Croucher, Nicholas J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8321556/
https://www.ncbi.nlm.nih.gov/pubmed/34259624
http://dx.doi.org/10.7554/eLife.67113
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author D'Aeth, Joshua C
van der Linden, Mark PG
McGee, Lesley
de Lencastre, Herminia
Turner, Paul
Song, Jae-Hoon
Lo, Stephanie W
Gladstone, Rebecca A
Sá-Leão, Raquel
Ko, Kwan Soo
Hanage, William P
Breiman, Robert F
Beall, Bernard
Bentley, Stephen D
Croucher, Nicholas J
author_facet D'Aeth, Joshua C
van der Linden, Mark PG
McGee, Lesley
de Lencastre, Herminia
Turner, Paul
Song, Jae-Hoon
Lo, Stephanie W
Gladstone, Rebecca A
Sá-Leão, Raquel
Ko, Kwan Soo
Hanage, William P
Breiman, Robert F
Beall, Bernard
Bentley, Stephen D
Croucher, Nicholas J
author_sort D'Aeth, Joshua C
collection PubMed
description Multidrug-resistant Streptococcus pneumoniae emerge through the modification of core genome loci by interspecies homologous recombinations, and acquisition of gene cassettes. Both occurred in the otherwise contrasting histories of the antibiotic-resistant S. pneumoniae lineages PMEN3 and PMEN9. A single PMEN3 clade spread globally, evading vaccine-induced immunity through frequent serotype switching, whereas locally circulating PMEN9 clades independently gained resistance. Both lineages repeatedly integrated Tn916-type and Tn1207.1-type elements, conferring tetracycline and macrolide resistance, respectively, through homologous recombination importing sequences originating in other species. A species-wide dataset found over 100 instances of such interspecific acquisitions of resistance cassettes and flanking homologous arms. Phylodynamic analysis of the most commonly sampled Tn1207.1-type insertion in PMEN9, originating from a commensal and disrupting a competence gene, suggested its expansion across Germany was driven by a high ratio of macrolide-to-β-lactam consumption. Hence, selection from antibiotic consumption was sufficient for these atypically large recombinations to overcome species boundaries across the pneumococcal chromosome.
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spelling pubmed-83215562021-07-30 The role of interspecies recombination in the evolution of antibiotic-resistant pneumococci D'Aeth, Joshua C van der Linden, Mark PG McGee, Lesley de Lencastre, Herminia Turner, Paul Song, Jae-Hoon Lo, Stephanie W Gladstone, Rebecca A Sá-Leão, Raquel Ko, Kwan Soo Hanage, William P Breiman, Robert F Beall, Bernard Bentley, Stephen D Croucher, Nicholas J eLife Genetics and Genomics Multidrug-resistant Streptococcus pneumoniae emerge through the modification of core genome loci by interspecies homologous recombinations, and acquisition of gene cassettes. Both occurred in the otherwise contrasting histories of the antibiotic-resistant S. pneumoniae lineages PMEN3 and PMEN9. A single PMEN3 clade spread globally, evading vaccine-induced immunity through frequent serotype switching, whereas locally circulating PMEN9 clades independently gained resistance. Both lineages repeatedly integrated Tn916-type and Tn1207.1-type elements, conferring tetracycline and macrolide resistance, respectively, through homologous recombination importing sequences originating in other species. A species-wide dataset found over 100 instances of such interspecific acquisitions of resistance cassettes and flanking homologous arms. Phylodynamic analysis of the most commonly sampled Tn1207.1-type insertion in PMEN9, originating from a commensal and disrupting a competence gene, suggested its expansion across Germany was driven by a high ratio of macrolide-to-β-lactam consumption. Hence, selection from antibiotic consumption was sufficient for these atypically large recombinations to overcome species boundaries across the pneumococcal chromosome. eLife Sciences Publications, Ltd 2021-07-14 /pmc/articles/PMC8321556/ /pubmed/34259624 http://dx.doi.org/10.7554/eLife.67113 Text en https://creativecommons.org/publicdomain/zero/1.0/This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication (https://creativecommons.org/publicdomain/zero/1.0/) .
spellingShingle Genetics and Genomics
D'Aeth, Joshua C
van der Linden, Mark PG
McGee, Lesley
de Lencastre, Herminia
Turner, Paul
Song, Jae-Hoon
Lo, Stephanie W
Gladstone, Rebecca A
Sá-Leão, Raquel
Ko, Kwan Soo
Hanage, William P
Breiman, Robert F
Beall, Bernard
Bentley, Stephen D
Croucher, Nicholas J
The role of interspecies recombination in the evolution of antibiotic-resistant pneumococci
title The role of interspecies recombination in the evolution of antibiotic-resistant pneumococci
title_full The role of interspecies recombination in the evolution of antibiotic-resistant pneumococci
title_fullStr The role of interspecies recombination in the evolution of antibiotic-resistant pneumococci
title_full_unstemmed The role of interspecies recombination in the evolution of antibiotic-resistant pneumococci
title_short The role of interspecies recombination in the evolution of antibiotic-resistant pneumococci
title_sort role of interspecies recombination in the evolution of antibiotic-resistant pneumococci
topic Genetics and Genomics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8321556/
https://www.ncbi.nlm.nih.gov/pubmed/34259624
http://dx.doi.org/10.7554/eLife.67113
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