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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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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