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Evolutionary and functional history of the Escherichia coli K1 capsule

Escherichia coli is a leading cause of invasive bacterial infections in humans. Capsule polysaccharide has an important role in bacterial pathogenesis, and the K1 capsule has been firmly established as one of the most potent capsule types in E. coli through its association with severe infections. Ho...

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Autores principales: Arredondo-Alonso, Sergio, Blundell-Hunter, George, Fu, Zuyi, Gladstone, Rebecca A., Fillol-Salom, Alfred, Loraine, Jessica, Cloutman-Green, Elaine, Johnsen, Pål J., Samuelsen, Ørjan, Pöntinen, Anna K., Cléon, François, Chavez-Bueno, Susana, De la Cruz, Miguel A., Ares, Miguel A., Vongsouvath, Manivanh, Chmielarczyk, Agnieszka, Horner, Carolyne, Klein, Nigel, McNally, Alan, Reis, Joice N., Penadés, José R., Thomson, Nicholas R., Corander, Jukka, Taylor, Peter W., McCarthy, Alex J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10272209/
https://www.ncbi.nlm.nih.gov/pubmed/37322051
http://dx.doi.org/10.1038/s41467-023-39052-w
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author Arredondo-Alonso, Sergio
Blundell-Hunter, George
Fu, Zuyi
Gladstone, Rebecca A.
Fillol-Salom, Alfred
Loraine, Jessica
Cloutman-Green, Elaine
Johnsen, Pål J.
Samuelsen, Ørjan
Pöntinen, Anna K.
Cléon, François
Chavez-Bueno, Susana
De la Cruz, Miguel A.
Ares, Miguel A.
Vongsouvath, Manivanh
Chmielarczyk, Agnieszka
Horner, Carolyne
Klein, Nigel
McNally, Alan
Reis, Joice N.
Penadés, José R.
Thomson, Nicholas R.
Corander, Jukka
Taylor, Peter W.
McCarthy, Alex J.
author_facet Arredondo-Alonso, Sergio
Blundell-Hunter, George
Fu, Zuyi
Gladstone, Rebecca A.
Fillol-Salom, Alfred
Loraine, Jessica
Cloutman-Green, Elaine
Johnsen, Pål J.
Samuelsen, Ørjan
Pöntinen, Anna K.
Cléon, François
Chavez-Bueno, Susana
De la Cruz, Miguel A.
Ares, Miguel A.
Vongsouvath, Manivanh
Chmielarczyk, Agnieszka
Horner, Carolyne
Klein, Nigel
McNally, Alan
Reis, Joice N.
Penadés, José R.
Thomson, Nicholas R.
Corander, Jukka
Taylor, Peter W.
McCarthy, Alex J.
author_sort Arredondo-Alonso, Sergio
collection PubMed
description Escherichia coli is a leading cause of invasive bacterial infections in humans. Capsule polysaccharide has an important role in bacterial pathogenesis, and the K1 capsule has been firmly established as one of the most potent capsule types in E. coli through its association with severe infections. However, little is known about its distribution, evolution and functions across the E. coli phylogeny, which is fundamental to elucidating its role in the expansion of successful lineages. Using systematic surveys of invasive E. coli isolates, we show that the K1-cps locus is present in a quarter of bloodstream infection isolates and has emerged in at least four different extraintestinal pathogenic E. coli (ExPEC) phylogroups independently in the last 500 years. Phenotypic assessment demonstrates that K1 capsule synthesis enhances E. coli survival in human serum independent of genetic background, and that therapeutic targeting of the K1 capsule re-sensitizes E. coli from distinct genetic backgrounds to human serum. Our study highlights that assessing the evolutionary and functional properties of bacterial virulence factors at population levels is important to better monitor and predict the emergence of virulent clones, and to also inform therapies and preventive medicine to effectively control bacterial infections whilst significantly lowering antibiotic usage.
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spelling pubmed-102722092023-06-17 Evolutionary and functional history of the Escherichia coli K1 capsule Arredondo-Alonso, Sergio Blundell-Hunter, George Fu, Zuyi Gladstone, Rebecca A. Fillol-Salom, Alfred Loraine, Jessica Cloutman-Green, Elaine Johnsen, Pål J. Samuelsen, Ørjan Pöntinen, Anna K. Cléon, François Chavez-Bueno, Susana De la Cruz, Miguel A. Ares, Miguel A. Vongsouvath, Manivanh Chmielarczyk, Agnieszka Horner, Carolyne Klein, Nigel McNally, Alan Reis, Joice N. Penadés, José R. Thomson, Nicholas R. Corander, Jukka Taylor, Peter W. McCarthy, Alex J. Nat Commun Article Escherichia coli is a leading cause of invasive bacterial infections in humans. Capsule polysaccharide has an important role in bacterial pathogenesis, and the K1 capsule has been firmly established as one of the most potent capsule types in E. coli through its association with severe infections. However, little is known about its distribution, evolution and functions across the E. coli phylogeny, which is fundamental to elucidating its role in the expansion of successful lineages. Using systematic surveys of invasive E. coli isolates, we show that the K1-cps locus is present in a quarter of bloodstream infection isolates and has emerged in at least four different extraintestinal pathogenic E. coli (ExPEC) phylogroups independently in the last 500 years. Phenotypic assessment demonstrates that K1 capsule synthesis enhances E. coli survival in human serum independent of genetic background, and that therapeutic targeting of the K1 capsule re-sensitizes E. coli from distinct genetic backgrounds to human serum. Our study highlights that assessing the evolutionary and functional properties of bacterial virulence factors at population levels is important to better monitor and predict the emergence of virulent clones, and to also inform therapies and preventive medicine to effectively control bacterial infections whilst significantly lowering antibiotic usage. Nature Publishing Group UK 2023-06-15 /pmc/articles/PMC10272209/ /pubmed/37322051 http://dx.doi.org/10.1038/s41467-023-39052-w Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Arredondo-Alonso, Sergio
Blundell-Hunter, George
Fu, Zuyi
Gladstone, Rebecca A.
Fillol-Salom, Alfred
Loraine, Jessica
Cloutman-Green, Elaine
Johnsen, Pål J.
Samuelsen, Ørjan
Pöntinen, Anna K.
Cléon, François
Chavez-Bueno, Susana
De la Cruz, Miguel A.
Ares, Miguel A.
Vongsouvath, Manivanh
Chmielarczyk, Agnieszka
Horner, Carolyne
Klein, Nigel
McNally, Alan
Reis, Joice N.
Penadés, José R.
Thomson, Nicholas R.
Corander, Jukka
Taylor, Peter W.
McCarthy, Alex J.
Evolutionary and functional history of the Escherichia coli K1 capsule
title Evolutionary and functional history of the Escherichia coli K1 capsule
title_full Evolutionary and functional history of the Escherichia coli K1 capsule
title_fullStr Evolutionary and functional history of the Escherichia coli K1 capsule
title_full_unstemmed Evolutionary and functional history of the Escherichia coli K1 capsule
title_short Evolutionary and functional history of the Escherichia coli K1 capsule
title_sort evolutionary and functional history of the escherichia coli k1 capsule
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10272209/
https://www.ncbi.nlm.nih.gov/pubmed/37322051
http://dx.doi.org/10.1038/s41467-023-39052-w
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