Interplay between the cell envelope and mobile genetic elements shapes gene flow in populations of the nosocomial pathogen Klebsiella pneumoniae.

Mobile genetic elements (MGEs) drive genetic transfers between bacteria using mechanisms that require a physical interaction with the cellular envelope. In the high-priority multidrug-resistant nosocomial pathogens (ESKAPE), the first point of contact between the cell and virions or conjugative pili...

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Autores principales:	Matthieu Haudiquet, Amandine Buffet, Olaya Rendueles, Eduardo P C Rocha
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2021
Materias:	Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/258e9bb9fbeb4bbb913ebcedb82d8167
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spelling	oai:doaj.org-article:258e9bb9fbeb4bbb913ebcedb82d81672021-12-02T19:54:24ZInterplay between the cell envelope and mobile genetic elements shapes gene flow in populations of the nosocomial pathogen Klebsiella pneumoniae.1544-91731545-788510.1371/journal.pbio.3001276https://doaj.org/article/258e9bb9fbeb4bbb913ebcedb82d81672021-07-01T00:00:00Zhttps://doi.org/10.1371/journal.pbio.3001276https://doaj.org/toc/1544-9173https://doaj.org/toc/1545-7885Mobile genetic elements (MGEs) drive genetic transfers between bacteria using mechanisms that require a physical interaction with the cellular envelope. In the high-priority multidrug-resistant nosocomial pathogens (ESKAPE), the first point of contact between the cell and virions or conjugative pili is the capsule. While the capsule can be a barrier to MGEs, it also evolves rapidly by horizontal gene transfer (HGT). Here, we aim at understanding this apparent contradiction by studying the covariation between the repertoire of capsule genes and MGEs in approximately 4,000 genomes of Klebsiella pneumoniae (Kpn). We show that capsules drive phage-mediated gene flow between closely related serotypes. Such serotype-specific phage predation also explains the frequent inactivation of capsule genes, observed in more than 3% of the genomes. Inactivation is strongly epistatic, recapitulating the capsule biosynthetic pathway. We show that conjugative plasmids are acquired at higher rates in natural isolates lacking a functional capsular locus and confirmed experimentally this result in capsule mutants. This suggests that capsule inactivation by phage pressure facilitates its subsequent reacquisition by conjugation. Accordingly, capsule reacquisition leaves long recombination tracts around the capsular locus. The loss and regain process rewires gene flow toward other lineages whenever it leads to serotype swaps. Such changes happen preferentially between chemically related serotypes, hinting that the fitness of serotype-swapped strains depends on the host genetic background. These results enlighten the bases of trade-offs between the evolution of virulence and multidrug resistance and caution that some alternatives to antibiotics by selecting for capsule inactivation may facilitate the acquisition of antibiotic resistance genes (ARGs).Matthieu HaudiquetAmandine BuffetOlaya RenduelesEduardo P C RochaPublic Library of Science (PLoS)articleBiology (General)QH301-705.5ENPLoS Biology, Vol 19, Iss 7, p e3001276 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Biology (General) QH301-705.5
spellingShingle	Biology (General) QH301-705.5 Matthieu Haudiquet Amandine Buffet Olaya Rendueles Eduardo P C Rocha Interplay between the cell envelope and mobile genetic elements shapes gene flow in populations of the nosocomial pathogen Klebsiella pneumoniae.
description	Mobile genetic elements (MGEs) drive genetic transfers between bacteria using mechanisms that require a physical interaction with the cellular envelope. In the high-priority multidrug-resistant nosocomial pathogens (ESKAPE), the first point of contact between the cell and virions or conjugative pili is the capsule. While the capsule can be a barrier to MGEs, it also evolves rapidly by horizontal gene transfer (HGT). Here, we aim at understanding this apparent contradiction by studying the covariation between the repertoire of capsule genes and MGEs in approximately 4,000 genomes of Klebsiella pneumoniae (Kpn). We show that capsules drive phage-mediated gene flow between closely related serotypes. Such serotype-specific phage predation also explains the frequent inactivation of capsule genes, observed in more than 3% of the genomes. Inactivation is strongly epistatic, recapitulating the capsule biosynthetic pathway. We show that conjugative plasmids are acquired at higher rates in natural isolates lacking a functional capsular locus and confirmed experimentally this result in capsule mutants. This suggests that capsule inactivation by phage pressure facilitates its subsequent reacquisition by conjugation. Accordingly, capsule reacquisition leaves long recombination tracts around the capsular locus. The loss and regain process rewires gene flow toward other lineages whenever it leads to serotype swaps. Such changes happen preferentially between chemically related serotypes, hinting that the fitness of serotype-swapped strains depends on the host genetic background. These results enlighten the bases of trade-offs between the evolution of virulence and multidrug resistance and caution that some alternatives to antibiotics by selecting for capsule inactivation may facilitate the acquisition of antibiotic resistance genes (ARGs).
format	article
author	Matthieu Haudiquet Amandine Buffet Olaya Rendueles Eduardo P C Rocha
author_facet	Matthieu Haudiquet Amandine Buffet Olaya Rendueles Eduardo P C Rocha
author_sort	Matthieu Haudiquet
title	Interplay between the cell envelope and mobile genetic elements shapes gene flow in populations of the nosocomial pathogen Klebsiella pneumoniae.
title_short	Interplay between the cell envelope and mobile genetic elements shapes gene flow in populations of the nosocomial pathogen Klebsiella pneumoniae.
title_full	Interplay between the cell envelope and mobile genetic elements shapes gene flow in populations of the nosocomial pathogen Klebsiella pneumoniae.
title_fullStr	Interplay between the cell envelope and mobile genetic elements shapes gene flow in populations of the nosocomial pathogen Klebsiella pneumoniae.
title_full_unstemmed	Interplay between the cell envelope and mobile genetic elements shapes gene flow in populations of the nosocomial pathogen Klebsiella pneumoniae.
title_sort	interplay between the cell envelope and mobile genetic elements shapes gene flow in populations of the nosocomial pathogen klebsiella pneumoniae.
publisher	Public Library of Science (PLoS)
publishDate	2021
url	https://doaj.org/article/258e9bb9fbeb4bbb913ebcedb82d8167
work_keys_str_mv	AT matthieuhaudiquet interplaybetweenthecellenvelopeandmobilegeneticelementsshapesgeneflowinpopulationsofthenosocomialpathogenklebsiellapneumoniae AT amandinebuffet interplaybetweenthecellenvelopeandmobilegeneticelementsshapesgeneflowinpopulationsofthenosocomialpathogenklebsiellapneumoniae AT olayarendueles interplaybetweenthecellenvelopeandmobilegeneticelementsshapesgeneflowinpopulationsofthenosocomialpathogenklebsiellapneumoniae AT eduardopcrocha interplaybetweenthecellenvelopeandmobilegeneticelementsshapesgeneflowinpopulationsofthenosocomialpathogenklebsiellapneumoniae
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Interplay between the cell envelope and mobile genetic elements shapes gene flow in populations of the nosocomial pathogen Klebsiella pneumoniae.

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