Virulence evolution of the human pathogen Neisseria meningitidis by recombination in the core and accessory genome.

<h4>Background</h4>Neisseria meningitidis is a naturally transformable, facultative pathogen colonizing the human nasopharynx. Here, we analyze on a genome-wide level the impact of recombination on gene-complement diversity and virulence evolution in N. meningitidis. We combined comparat...

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Autores principales: Biju Joseph, Roland F Schwarz, Burkhard Linke, Jochen Blom, Anke Becker, Heike Claus, Alexander Goesmann, Matthias Frosch, Tobias Müller, Ulrich Vogel, Christoph Schoen
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spelling oai:doaj.org-article:0810640c04a14a60b381312e2c365c522021-11-18T06:55:11ZVirulence evolution of the human pathogen Neisseria meningitidis by recombination in the core and accessory genome.1932-620310.1371/journal.pone.0018441https://doaj.org/article/0810640c04a14a60b381312e2c365c522011-04-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/21541312/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>Neisseria meningitidis is a naturally transformable, facultative pathogen colonizing the human nasopharynx. Here, we analyze on a genome-wide level the impact of recombination on gene-complement diversity and virulence evolution in N. meningitidis. We combined comparative genome hybridization using microarrays (mCGH) and multilocus sequence typing (MLST) of 29 meningococcal isolates with computational comparison of a subset of seven meningococcal genome sequences.<h4>Principal findings</h4>We found that lateral gene transfer of minimal mobile elements as well as prophages are major forces shaping meningococcal population structure. Extensive gene content comparison revealed novel associations of virulence with genetic elements besides the recently discovered meningococcal disease associated (MDA) island. In particular, we identified an association of virulence with a recently described canonical genomic island termed IHT-E and a differential distribution of genes encoding RTX toxin- and two-partner secretion systems among hyperinvasive and non-hyperinvasive lineages. By computationally screening also the core genome for signs of recombination, we provided evidence that about 40% of the meningococcal core genes are affected by recombination primarily within metabolic genes as well as genes involved in DNA replication and repair. By comparison with the results of previous mCGH studies, our data indicated that genetic structuring as revealed by mCGH is stable over time and highly similar for isolates from different geographic origins.<h4>Conclusions</h4>Recombination comprising lateral transfer of entire genes as well as homologous intragenic recombination has a profound impact on meningococcal population structure and genome composition. Our data support the hypothesis that meningococcal virulence is polygenic in nature and that differences in metabolism might contribute to virulence.Biju JosephRoland F SchwarzBurkhard LinkeJochen BlomAnke BeckerHeike ClausAlexander GoesmannMatthias FroschTobias MüllerUlrich VogelChristoph SchoenPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 6, Iss 4, p e18441 (2011)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Biju Joseph
Roland F Schwarz
Burkhard Linke
Jochen Blom
Anke Becker
Heike Claus
Alexander Goesmann
Matthias Frosch
Tobias Müller
Ulrich Vogel
Christoph Schoen
Virulence evolution of the human pathogen Neisseria meningitidis by recombination in the core and accessory genome.
description <h4>Background</h4>Neisseria meningitidis is a naturally transformable, facultative pathogen colonizing the human nasopharynx. Here, we analyze on a genome-wide level the impact of recombination on gene-complement diversity and virulence evolution in N. meningitidis. We combined comparative genome hybridization using microarrays (mCGH) and multilocus sequence typing (MLST) of 29 meningococcal isolates with computational comparison of a subset of seven meningococcal genome sequences.<h4>Principal findings</h4>We found that lateral gene transfer of minimal mobile elements as well as prophages are major forces shaping meningococcal population structure. Extensive gene content comparison revealed novel associations of virulence with genetic elements besides the recently discovered meningococcal disease associated (MDA) island. In particular, we identified an association of virulence with a recently described canonical genomic island termed IHT-E and a differential distribution of genes encoding RTX toxin- and two-partner secretion systems among hyperinvasive and non-hyperinvasive lineages. By computationally screening also the core genome for signs of recombination, we provided evidence that about 40% of the meningococcal core genes are affected by recombination primarily within metabolic genes as well as genes involved in DNA replication and repair. By comparison with the results of previous mCGH studies, our data indicated that genetic structuring as revealed by mCGH is stable over time and highly similar for isolates from different geographic origins.<h4>Conclusions</h4>Recombination comprising lateral transfer of entire genes as well as homologous intragenic recombination has a profound impact on meningococcal population structure and genome composition. Our data support the hypothesis that meningococcal virulence is polygenic in nature and that differences in metabolism might contribute to virulence.
format article
author Biju Joseph
Roland F Schwarz
Burkhard Linke
Jochen Blom
Anke Becker
Heike Claus
Alexander Goesmann
Matthias Frosch
Tobias Müller
Ulrich Vogel
Christoph Schoen
author_facet Biju Joseph
Roland F Schwarz
Burkhard Linke
Jochen Blom
Anke Becker
Heike Claus
Alexander Goesmann
Matthias Frosch
Tobias Müller
Ulrich Vogel
Christoph Schoen
author_sort Biju Joseph
title Virulence evolution of the human pathogen Neisseria meningitidis by recombination in the core and accessory genome.
title_short Virulence evolution of the human pathogen Neisseria meningitidis by recombination in the core and accessory genome.
title_full Virulence evolution of the human pathogen Neisseria meningitidis by recombination in the core and accessory genome.
title_fullStr Virulence evolution of the human pathogen Neisseria meningitidis by recombination in the core and accessory genome.
title_full_unstemmed Virulence evolution of the human pathogen Neisseria meningitidis by recombination in the core and accessory genome.
title_sort virulence evolution of the human pathogen neisseria meningitidis by recombination in the core and accessory genome.
publisher Public Library of Science (PLoS)
publishDate 2011
url https://doaj.org/article/0810640c04a14a60b381312e2c365c52
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