Heterogeneity in the frequency and characteristics of homologous recombination in pneumococcal evolution.

The bacterium Streptococcus pneumoniae (pneumococcus) is one of the most important human bacterial pathogens, and a leading cause of morbidity and mortality worldwide. The pneumococcus is also known for undergoing extensive homologous recombination via transformation with exogenous DNA. It has been...

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Main Authors: Rafal Mostowy, Nicholas J Croucher, William P Hanage, Simon R Harris, Stephen Bentley, Christophe Fraser
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2014-05-01
Series:PLoS Genetics
Online Access:https://doi.org/10.1371/journal.pgen.1004300
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author Rafal Mostowy
Nicholas J Croucher
William P Hanage
Simon R Harris
Stephen Bentley
Christophe Fraser
author_facet Rafal Mostowy
Nicholas J Croucher
William P Hanage
Simon R Harris
Stephen Bentley
Christophe Fraser
author_sort Rafal Mostowy
collection DOAJ
description The bacterium Streptococcus pneumoniae (pneumococcus) is one of the most important human bacterial pathogens, and a leading cause of morbidity and mortality worldwide. The pneumococcus is also known for undergoing extensive homologous recombination via transformation with exogenous DNA. It has been shown that recombination has a major impact on the evolution of the pathogen, including acquisition of antibiotic resistance and serotype-switching. Nevertheless, the mechanism and the rates of recombination in an epidemiological context remain poorly understood. Here, we proposed several mathematical models to describe the rate and size of recombination in the evolutionary history of two very distinct pneumococcal lineages, PMEN1 and CC180. We found that, in both lineages, the process of homologous recombination was best described by a heterogeneous model of recombination with single, short, frequent replacements, which we call micro-recombinations, and rarer, multi-fragment, saltational replacements, which we call macro-recombinations. Macro-recombination was associated with major phenotypic changes, including serotype-switching events, and thus was a major driver of the diversification of the pathogen. We critically evaluate biological and epidemiological processes that could give rise to the micro-recombination and macro-recombination processes.
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spelling doaj-art-260aa7ceca9f422ba0362f920a3e4acc2025-08-20T02:34:07ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042014-05-01105e100430010.1371/journal.pgen.1004300Heterogeneity in the frequency and characteristics of homologous recombination in pneumococcal evolution.Rafal MostowyNicholas J CroucherWilliam P HanageSimon R HarrisStephen BentleyChristophe FraserThe bacterium Streptococcus pneumoniae (pneumococcus) is one of the most important human bacterial pathogens, and a leading cause of morbidity and mortality worldwide. The pneumococcus is also known for undergoing extensive homologous recombination via transformation with exogenous DNA. It has been shown that recombination has a major impact on the evolution of the pathogen, including acquisition of antibiotic resistance and serotype-switching. Nevertheless, the mechanism and the rates of recombination in an epidemiological context remain poorly understood. Here, we proposed several mathematical models to describe the rate and size of recombination in the evolutionary history of two very distinct pneumococcal lineages, PMEN1 and CC180. We found that, in both lineages, the process of homologous recombination was best described by a heterogeneous model of recombination with single, short, frequent replacements, which we call micro-recombinations, and rarer, multi-fragment, saltational replacements, which we call macro-recombinations. Macro-recombination was associated with major phenotypic changes, including serotype-switching events, and thus was a major driver of the diversification of the pathogen. We critically evaluate biological and epidemiological processes that could give rise to the micro-recombination and macro-recombination processes.https://doi.org/10.1371/journal.pgen.1004300
spellingShingle Rafal Mostowy
Nicholas J Croucher
William P Hanage
Simon R Harris
Stephen Bentley
Christophe Fraser
Heterogeneity in the frequency and characteristics of homologous recombination in pneumococcal evolution.
PLoS Genetics
title Heterogeneity in the frequency and characteristics of homologous recombination in pneumococcal evolution.
title_full Heterogeneity in the frequency and characteristics of homologous recombination in pneumococcal evolution.
title_fullStr Heterogeneity in the frequency and characteristics of homologous recombination in pneumococcal evolution.
title_full_unstemmed Heterogeneity in the frequency and characteristics of homologous recombination in pneumococcal evolution.
title_short Heterogeneity in the frequency and characteristics of homologous recombination in pneumococcal evolution.
title_sort heterogeneity in the frequency and characteristics of homologous recombination in pneumococcal evolution
url https://doi.org/10.1371/journal.pgen.1004300
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