Global phylogenomic analysis of nonencapsulated Streptococcus pneumoniae reveals a deep-branching classic lineage that is distinct from multiple sporadic lineages

Markus Hilty, Daniel Wüthrich, Susannah J. Salter, Hansjürg Engel, Samuel Campbell, Raquel Sá-Leão, Hermínia De Lencastre, Peter Hermans, Ewa Sadowy, Paul Turner, Claire Chewapreecha, Mathew Diggle, Gerd Pluschke, Lesley McGee, Özgen Köseoʇlu Eser, Donald E. Low, Heidi Smith-Vaughan, Andrea Endimiani, Marianne Kü Ffer, Mélanie Dupasquier & 8 others Emmanuel Beaudoing, Johann Weber, Rémy Bruggmann, William P. Hanage, Julian Parkhill, Lucy J. Hathaway, Kathrin Mü Hlemann, Stephen D. Bentley

Research output: Contribution to journalArticleResearchpeer-review

Abstract

The surrounding capsule of Streptococcus pneumoniae has been identified as a major virulence factor and is targeted by pneumococcal conjugate vaccines (PCV). However, nonencapsulated S. pneumoniae (non-Ec-Sp) have also been isolated globally, mainly in carriage studies. It is unknown if non-Ec-Sp evolve sporadically, if they have high antibiotic nonsusceptiblity rates and a unique, specific gene content. Here, whole-genome sequencing of 131 non-Ec-Sp isolates sourced from 17 different locations around the world was performed. Results revealed a deep-branching classic lineage that is distinct from multiple sporadic lineages. The sporadic lineages clustered with a previously sequenced, global collection of encapsulated S. pneumoniae (Ec-Sp) isolates while the classic lineage is comprised mainly of the frequently identified multilocus sequences types (STs) ST344 (n = 39) and ST448 (n = 40). All ST344 and nine ST448 isolates had high nonsusceptiblity rates to β-lactams and other antimicrobials. Analysis of the accessory genome reveals that the classic non-Ec-Sp contained an increased number of mobile elements, than Ec-Sp and sporadic non-Ec-Sp. Performing adherence assays to human epithelial cells for selected classic and sporadic non-Ec-Sp revealed that the presence of a integrative conjugative element (ICE) results in increased adherence to human epithelial cells (P = 0.005). In contrast, sporadic non-Ec-Sp lacking the ICE had greater growth in vitro possibly resulting in improved fitness. In conclusion, non-Ec-Sp isolates from the classic lineage have evolved separately. They have spread globally, are well adapted to nasopharyngeal carriage and are able to coexist with Ec-Sp. Due to continued use of PCV, non-Ec-Sp may become more prevalent.

Original languageEnglish
Pages (from-to)3281-3294
Number of pages14
JournalGenome Biology and Evolution
Volume6
Issue number12
DOIs
Publication statusPublished - 2014

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Streptococcus pneumoniae
pneumonia
branching
Conjugate Vaccines
Pneumococcal Vaccines
vaccine
epithelial cells
analysis
genome
Epithelial Cells
Genome
lactams
vaccines
Lactams
Virulence Factors
virulence
antibiotics
Capsules
fitness
anti-infective agents

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Hilty, Markus ; Wüthrich, Daniel ; Salter, Susannah J. ; Engel, Hansjürg ; Campbell, Samuel ; Sá-Leão, Raquel ; De Lencastre, Hermínia ; Hermans, Peter ; Sadowy, Ewa ; Turner, Paul ; Chewapreecha, Claire ; Diggle, Mathew ; Pluschke, Gerd ; McGee, Lesley ; Eser, Özgen Köseoʇlu ; Low, Donald E. ; Smith-Vaughan, Heidi ; Endimiani, Andrea ; Ffer, Marianne Kü ; Dupasquier, Mélanie ; Beaudoing, Emmanuel ; Weber, Johann ; Bruggmann, Rémy ; Hanage, William P. ; Parkhill, Julian ; Hathaway, Lucy J. ; Hlemann, Kathrin Mü ; Bentley, Stephen D. / Global phylogenomic analysis of nonencapsulated Streptococcus pneumoniae reveals a deep-branching classic lineage that is distinct from multiple sporadic lineages. In: Genome Biology and Evolution. 2014 ; Vol. 6, No. 12. pp. 3281-3294.
@article{bfec7ec40d8140a3a4ed9c5b86b6e5f1,
title = "Global phylogenomic analysis of nonencapsulated Streptococcus pneumoniae reveals a deep-branching classic lineage that is distinct from multiple sporadic lineages",
abstract = "The surrounding capsule of Streptococcus pneumoniae has been identified as a major virulence factor and is targeted by pneumococcal conjugate vaccines (PCV). However, nonencapsulated S. pneumoniae (non-Ec-Sp) have also been isolated globally, mainly in carriage studies. It is unknown if non-Ec-Sp evolve sporadically, if they have high antibiotic nonsusceptiblity rates and a unique, specific gene content. Here, whole-genome sequencing of 131 non-Ec-Sp isolates sourced from 17 different locations around the world was performed. Results revealed a deep-branching classic lineage that is distinct from multiple sporadic lineages. The sporadic lineages clustered with a previously sequenced, global collection of encapsulated S. pneumoniae (Ec-Sp) isolates while the classic lineage is comprised mainly of the frequently identified multilocus sequences types (STs) ST344 (n = 39) and ST448 (n = 40). All ST344 and nine ST448 isolates had high nonsusceptiblity rates to β-lactams and other antimicrobials. Analysis of the accessory genome reveals that the classic non-Ec-Sp contained an increased number of mobile elements, than Ec-Sp and sporadic non-Ec-Sp. Performing adherence assays to human epithelial cells for selected classic and sporadic non-Ec-Sp revealed that the presence of a integrative conjugative element (ICE) results in increased adherence to human epithelial cells (P = 0.005). In contrast, sporadic non-Ec-Sp lacking the ICE had greater growth in vitro possibly resulting in improved fitness. In conclusion, non-Ec-Sp isolates from the classic lineage have evolved separately. They have spread globally, are well adapted to nasopharyngeal carriage and are able to coexist with Ec-Sp. Due to continued use of PCV, non-Ec-Sp may become more prevalent.",
keywords = "antiinfective agent, beta lactam, transposon, bacterial capsule, bacterial genome, cell line, drug effects, epithelium cell, gene locus, genetics, human, isolation and purification, microbiology, pathogenicity, phylogeny, species differentiation, Streptococcus pneumoniae, Anti-Bacterial Agents, Bacterial Capsules, beta-Lactams, Cell Line, DNA Transposable Elements, Epithelial Cells, Genetic Loci, Genetic Speciation, Genome, Bacterial, Humans, Phylogeny",
author = "Markus Hilty and Daniel W{\"u}thrich and Salter, {Susannah J.} and Hansj{\"u}rg Engel and Samuel Campbell and Raquel S{\'a}-Le{\~a}o and {De Lencastre}, Herm{\'i}nia and Peter Hermans and Ewa Sadowy and Paul Turner and Claire Chewapreecha and Mathew Diggle and Gerd Pluschke and Lesley McGee and Eser, {{\"O}zgen K{\"o}seoʇlu} and Low, {Donald E.} and Heidi Smith-Vaughan and Andrea Endimiani and Ffer, {Marianne K{\"u}} and M{\'e}lanie Dupasquier and Emmanuel Beaudoing and Johann Weber and R{\'e}my Bruggmann and Hanage, {William P.} and Julian Parkhill and Hathaway, {Lucy J.} and Hlemann, {Kathrin M{\"u}} and Bentley, {Stephen D.}",
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Hilty, M, Wüthrich, D, Salter, SJ, Engel, H, Campbell, S, Sá-Leão, R, De Lencastre, H, Hermans, P, Sadowy, E, Turner, P, Chewapreecha, C, Diggle, M, Pluschke, G, McGee, L, Eser, ÖK, Low, DE, Smith-Vaughan, H, Endimiani, A, Ffer, MK, Dupasquier, M, Beaudoing, E, Weber, J, Bruggmann, R, Hanage, WP, Parkhill, J, Hathaway, LJ, Hlemann, KM & Bentley, SD 2014, 'Global phylogenomic analysis of nonencapsulated Streptococcus pneumoniae reveals a deep-branching classic lineage that is distinct from multiple sporadic lineages', Genome Biology and Evolution, vol. 6, no. 12, pp. 3281-3294. https://doi.org/10.1093/gbe/evu263

Global phylogenomic analysis of nonencapsulated Streptococcus pneumoniae reveals a deep-branching classic lineage that is distinct from multiple sporadic lineages. / Hilty, Markus; Wüthrich, Daniel; Salter, Susannah J.; Engel, Hansjürg; Campbell, Samuel; Sá-Leão, Raquel; De Lencastre, Hermínia; Hermans, Peter; Sadowy, Ewa; Turner, Paul; Chewapreecha, Claire; Diggle, Mathew; Pluschke, Gerd; McGee, Lesley; Eser, Özgen Köseoʇlu; Low, Donald E.; Smith-Vaughan, Heidi; Endimiani, Andrea; Ffer, Marianne Kü; Dupasquier, Mélanie; Beaudoing, Emmanuel; Weber, Johann; Bruggmann, Rémy; Hanage, William P.; Parkhill, Julian; Hathaway, Lucy J.; Hlemann, Kathrin Mü; Bentley, Stephen D.

In: Genome Biology and Evolution, Vol. 6, No. 12, 2014, p. 3281-3294.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Global phylogenomic analysis of nonencapsulated Streptococcus pneumoniae reveals a deep-branching classic lineage that is distinct from multiple sporadic lineages

AU - Hilty, Markus

AU - Wüthrich, Daniel

AU - Salter, Susannah J.

AU - Engel, Hansjürg

AU - Campbell, Samuel

AU - Sá-Leão, Raquel

AU - De Lencastre, Hermínia

AU - Hermans, Peter

AU - Sadowy, Ewa

AU - Turner, Paul

AU - Chewapreecha, Claire

AU - Diggle, Mathew

AU - Pluschke, Gerd

AU - McGee, Lesley

AU - Eser, Özgen Köseoʇlu

AU - Low, Donald E.

AU - Smith-Vaughan, Heidi

AU - Endimiani, Andrea

AU - Ffer, Marianne Kü

AU - Dupasquier, Mélanie

AU - Beaudoing, Emmanuel

AU - Weber, Johann

AU - Bruggmann, Rémy

AU - Hanage, William P.

AU - Parkhill, Julian

AU - Hathaway, Lucy J.

AU - Hlemann, Kathrin Mü

AU - Bentley, Stephen D.

PY - 2014

Y1 - 2014

N2 - The surrounding capsule of Streptococcus pneumoniae has been identified as a major virulence factor and is targeted by pneumococcal conjugate vaccines (PCV). However, nonencapsulated S. pneumoniae (non-Ec-Sp) have also been isolated globally, mainly in carriage studies. It is unknown if non-Ec-Sp evolve sporadically, if they have high antibiotic nonsusceptiblity rates and a unique, specific gene content. Here, whole-genome sequencing of 131 non-Ec-Sp isolates sourced from 17 different locations around the world was performed. Results revealed a deep-branching classic lineage that is distinct from multiple sporadic lineages. The sporadic lineages clustered with a previously sequenced, global collection of encapsulated S. pneumoniae (Ec-Sp) isolates while the classic lineage is comprised mainly of the frequently identified multilocus sequences types (STs) ST344 (n = 39) and ST448 (n = 40). All ST344 and nine ST448 isolates had high nonsusceptiblity rates to β-lactams and other antimicrobials. Analysis of the accessory genome reveals that the classic non-Ec-Sp contained an increased number of mobile elements, than Ec-Sp and sporadic non-Ec-Sp. Performing adherence assays to human epithelial cells for selected classic and sporadic non-Ec-Sp revealed that the presence of a integrative conjugative element (ICE) results in increased adherence to human epithelial cells (P = 0.005). In contrast, sporadic non-Ec-Sp lacking the ICE had greater growth in vitro possibly resulting in improved fitness. In conclusion, non-Ec-Sp isolates from the classic lineage have evolved separately. They have spread globally, are well adapted to nasopharyngeal carriage and are able to coexist with Ec-Sp. Due to continued use of PCV, non-Ec-Sp may become more prevalent.

AB - The surrounding capsule of Streptococcus pneumoniae has been identified as a major virulence factor and is targeted by pneumococcal conjugate vaccines (PCV). However, nonencapsulated S. pneumoniae (non-Ec-Sp) have also been isolated globally, mainly in carriage studies. It is unknown if non-Ec-Sp evolve sporadically, if they have high antibiotic nonsusceptiblity rates and a unique, specific gene content. Here, whole-genome sequencing of 131 non-Ec-Sp isolates sourced from 17 different locations around the world was performed. Results revealed a deep-branching classic lineage that is distinct from multiple sporadic lineages. The sporadic lineages clustered with a previously sequenced, global collection of encapsulated S. pneumoniae (Ec-Sp) isolates while the classic lineage is comprised mainly of the frequently identified multilocus sequences types (STs) ST344 (n = 39) and ST448 (n = 40). All ST344 and nine ST448 isolates had high nonsusceptiblity rates to β-lactams and other antimicrobials. Analysis of the accessory genome reveals that the classic non-Ec-Sp contained an increased number of mobile elements, than Ec-Sp and sporadic non-Ec-Sp. Performing adherence assays to human epithelial cells for selected classic and sporadic non-Ec-Sp revealed that the presence of a integrative conjugative element (ICE) results in increased adherence to human epithelial cells (P = 0.005). In contrast, sporadic non-Ec-Sp lacking the ICE had greater growth in vitro possibly resulting in improved fitness. In conclusion, non-Ec-Sp isolates from the classic lineage have evolved separately. They have spread globally, are well adapted to nasopharyngeal carriage and are able to coexist with Ec-Sp. Due to continued use of PCV, non-Ec-Sp may become more prevalent.

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KW - beta lactam

KW - transposon

KW - bacterial capsule

KW - bacterial genome

KW - cell line

KW - drug effects

KW - epithelium cell

KW - gene locus

KW - genetics

KW - human

KW - isolation and purification

KW - microbiology

KW - pathogenicity

KW - phylogeny

KW - species differentiation

KW - Streptococcus pneumoniae

KW - Anti-Bacterial Agents

KW - Bacterial Capsules

KW - beta-Lactams

KW - Cell Line

KW - DNA Transposable Elements

KW - Epithelial Cells

KW - Genetic Loci

KW - Genetic Speciation

KW - Genome, Bacterial

KW - Humans

KW - Phylogeny

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DO - 10.1093/gbe/evu263

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EP - 3294

JO - Genome Biology and Evolution

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SN - 1759-6653

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