Lineage structure of Streptococcus pneumoniae may be driven by immune selection on the groEL heat-shock protein

Abstract Populations of Streptococcus pneumoniae (SP) are typically structured into groups of closely related organisms or lineages, but it is not clear whether they are maintained by selection or neutral processes. Here, we attempt to address this question by applying a machine learning technique t...

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Main Authors: José Lourenço, Eleanor R. Watkins, Uri Obolski, Samuel J. Peacock, Callum Morris, Martin C. J. Maiden, Sunetra Gupta
Format: Article
Language:English
Published: Nature Publishing Group 2017-08-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-017-08990-z
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spelling doaj-bf290c7880294f57a426bc31d0659b3d2020-12-08T02:16:24ZengNature Publishing GroupScientific Reports2045-23222017-08-017111110.1038/s41598-017-08990-zLineage structure of Streptococcus pneumoniae may be driven by immune selection on the groEL heat-shock proteinJosé Lourenço0Eleanor R. Watkins1Uri Obolski2Samuel J. Peacock3Callum Morris4Martin C. J. Maiden5Sunetra Gupta6Department of Zoology, University of OxfordDepartment of Zoology, University of OxfordDepartment of Zoology, University of OxfordDepartment of Zoology, University of OxfordUniversity of DurhamDepartment of Zoology, University of OxfordDepartment of Zoology, University of OxfordAbstract Populations of Streptococcus pneumoniae (SP) are typically structured into groups of closely related organisms or lineages, but it is not clear whether they are maintained by selection or neutral processes. Here, we attempt to address this question by applying a machine learning technique to SP whole genomes. Our results indicate that lineages evolved through immune selection on the groEL chaperone protein. The groEL protein is part of the groESL operon and enables a large range of proteins to fold correctly within the physical environment of the nasopharynx, thereby explaining why lineage structure is so stable within SP despite high levels of genetic transfer. SP is also antigenically diverse, exhibiting a variety of distinct capsular serotypes. Associations exist between lineage and capsular serotype but these can be easily perturbed, such as by vaccination. Overall, our analyses indicate that the evolution of SP can be conceptualized as the rearrangement of modular functional units occurring on several different timescales under different pressures: some patterns have locked in early (such as the epistatic interactions between groESL and a constellation of other genes) and preserve the differentiation of lineages, while others (such as the associations between capsular serotype and lineage) remain in continuous flux.https://doi.org/10.1038/s41598-017-08990-z
collection DOAJ
language English
format Article
sources DOAJ
author José Lourenço
Eleanor R. Watkins
Uri Obolski
Samuel J. Peacock
Callum Morris
Martin C. J. Maiden
Sunetra Gupta
spellingShingle José Lourenço
Eleanor R. Watkins
Uri Obolski
Samuel J. Peacock
Callum Morris
Martin C. J. Maiden
Sunetra Gupta
Lineage structure of Streptococcus pneumoniae may be driven by immune selection on the groEL heat-shock protein
Scientific Reports
author_facet José Lourenço
Eleanor R. Watkins
Uri Obolski
Samuel J. Peacock
Callum Morris
Martin C. J. Maiden
Sunetra Gupta
author_sort José Lourenço
title Lineage structure of Streptococcus pneumoniae may be driven by immune selection on the groEL heat-shock protein
title_short Lineage structure of Streptococcus pneumoniae may be driven by immune selection on the groEL heat-shock protein
title_full Lineage structure of Streptococcus pneumoniae may be driven by immune selection on the groEL heat-shock protein
title_fullStr Lineage structure of Streptococcus pneumoniae may be driven by immune selection on the groEL heat-shock protein
title_full_unstemmed Lineage structure of Streptococcus pneumoniae may be driven by immune selection on the groEL heat-shock protein
title_sort lineage structure of streptococcus pneumoniae may be driven by immune selection on the groel heat-shock protein
publisher Nature Publishing Group
series Scientific Reports
issn 2045-2322
publishDate 2017-08-01
description Abstract Populations of Streptococcus pneumoniae (SP) are typically structured into groups of closely related organisms or lineages, but it is not clear whether they are maintained by selection or neutral processes. Here, we attempt to address this question by applying a machine learning technique to SP whole genomes. Our results indicate that lineages evolved through immune selection on the groEL chaperone protein. The groEL protein is part of the groESL operon and enables a large range of proteins to fold correctly within the physical environment of the nasopharynx, thereby explaining why lineage structure is so stable within SP despite high levels of genetic transfer. SP is also antigenically diverse, exhibiting a variety of distinct capsular serotypes. Associations exist between lineage and capsular serotype but these can be easily perturbed, such as by vaccination. Overall, our analyses indicate that the evolution of SP can be conceptualized as the rearrangement of modular functional units occurring on several different timescales under different pressures: some patterns have locked in early (such as the epistatic interactions between groESL and a constellation of other genes) and preserve the differentiation of lineages, while others (such as the associations between capsular serotype and lineage) remain in continuous flux.
url https://doi.org/10.1038/s41598-017-08990-z
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