Pilus operon evolution in Streptococcus pneumoniae is driven by positive selection and recombination.

BACKGROUND: The evolution of bacterial organelles involved in host-pathogen interactions is subject to intense and competing selective pressures due to the need to maintain function while escaping the host immune response. To characterize the interplay of these forces in an important pathogen, we se...

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Main Authors: Alessandro Muzzi, Monica Moschioni, Antonello Covacci, Rino Rappuoli, Claudio Donati
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2008-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC2576445?pdf=render
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spelling doaj-8d72d8c35722427fa3ca877d7765e39c2020-11-25T01:46:42ZengPublic Library of Science (PLoS)PLoS ONE1932-62032008-01-01311e366010.1371/journal.pone.0003660Pilus operon evolution in Streptococcus pneumoniae is driven by positive selection and recombination.Alessandro MuzziMonica MoschioniAntonello CovacciRino RappuoliClaudio DonatiBACKGROUND: The evolution of bacterial organelles involved in host-pathogen interactions is subject to intense and competing selective pressures due to the need to maintain function while escaping the host immune response. To characterize the interplay of these forces in an important pathogen, we sequenced the rlrA islet, a chromosomal region encoding for a pilus-like structure involved in adherence to lung epithelial cells in vitro and in colonization in a murine model of infection, in 44 clinical isolates of Streptococcus pneumoniae. RESULTS: We found that the rrgA and rrgB genes, encoding the main structural components of the pilus, are under the action of positive selection. In contrast, the rrgC gene, coding for a component present in low quantities in the assembled pilus, and the srtB, srtC and srtD genes, coding for three sortase enzymes essential for pilus assembly but probably not directly exposed to the host immune system, show no evidence of positive selection. We found several events of homologous recombination in the region containing these genes, identifying 4 major recombination hotspots. An analysis of the most recent recombination events shows a high level of mosaicism of the region coding for the rrgC, srtB, srtC and srtD genes. CONCLUSIONS: In the rlrA islet, the genes coding for proteins directly exposed to the host immune response are under the action of positive selection, and exist in distinct forms in the population of circulating strains. The genes coding for proteins not directly exposed on the surface of the bacterial cell are more conserved probably due to the homogenizing effect of recombination.http://europepmc.org/articles/PMC2576445?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Alessandro Muzzi
Monica Moschioni
Antonello Covacci
Rino Rappuoli
Claudio Donati
spellingShingle Alessandro Muzzi
Monica Moschioni
Antonello Covacci
Rino Rappuoli
Claudio Donati
Pilus operon evolution in Streptococcus pneumoniae is driven by positive selection and recombination.
PLoS ONE
author_facet Alessandro Muzzi
Monica Moschioni
Antonello Covacci
Rino Rappuoli
Claudio Donati
author_sort Alessandro Muzzi
title Pilus operon evolution in Streptococcus pneumoniae is driven by positive selection and recombination.
title_short Pilus operon evolution in Streptococcus pneumoniae is driven by positive selection and recombination.
title_full Pilus operon evolution in Streptococcus pneumoniae is driven by positive selection and recombination.
title_fullStr Pilus operon evolution in Streptococcus pneumoniae is driven by positive selection and recombination.
title_full_unstemmed Pilus operon evolution in Streptococcus pneumoniae is driven by positive selection and recombination.
title_sort pilus operon evolution in streptococcus pneumoniae is driven by positive selection and recombination.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2008-01-01
description BACKGROUND: The evolution of bacterial organelles involved in host-pathogen interactions is subject to intense and competing selective pressures due to the need to maintain function while escaping the host immune response. To characterize the interplay of these forces in an important pathogen, we sequenced the rlrA islet, a chromosomal region encoding for a pilus-like structure involved in adherence to lung epithelial cells in vitro and in colonization in a murine model of infection, in 44 clinical isolates of Streptococcus pneumoniae. RESULTS: We found that the rrgA and rrgB genes, encoding the main structural components of the pilus, are under the action of positive selection. In contrast, the rrgC gene, coding for a component present in low quantities in the assembled pilus, and the srtB, srtC and srtD genes, coding for three sortase enzymes essential for pilus assembly but probably not directly exposed to the host immune system, show no evidence of positive selection. We found several events of homologous recombination in the region containing these genes, identifying 4 major recombination hotspots. An analysis of the most recent recombination events shows a high level of mosaicism of the region coding for the rrgC, srtB, srtC and srtD genes. CONCLUSIONS: In the rlrA islet, the genes coding for proteins directly exposed to the host immune response are under the action of positive selection, and exist in distinct forms in the population of circulating strains. The genes coding for proteins not directly exposed on the surface of the bacterial cell are more conserved probably due to the homogenizing effect of recombination.
url http://europepmc.org/articles/PMC2576445?pdf=render
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