Cargando…

Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome

BACKGROUND: Listeria monocytogenes is an important food-borne pathogen and model organism for host-pathogen interaction, thus representing an invaluable target considering research on the forces governing the evolution of such microbes. The diversity of this species has not been exhaustively explore...

Descripción completa

Detalles Bibliográficos
Autores principales: Kuenne, Carsten, Billion, André, Mraheil, Mobarak Abu, Strittmatter, Axel, Daniel, Rolf, Goesmann, Alexander, Barbuddhe, Sukhadeo, Hain, Torsten, Chakraborty, Trinad
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3556495/
https://www.ncbi.nlm.nih.gov/pubmed/23339658
http://dx.doi.org/10.1186/1471-2164-14-47
_version_ 1782257191081738240
author Kuenne, Carsten
Billion, André
Mraheil, Mobarak Abu
Strittmatter, Axel
Daniel, Rolf
Goesmann, Alexander
Barbuddhe, Sukhadeo
Hain, Torsten
Chakraborty, Trinad
author_facet Kuenne, Carsten
Billion, André
Mraheil, Mobarak Abu
Strittmatter, Axel
Daniel, Rolf
Goesmann, Alexander
Barbuddhe, Sukhadeo
Hain, Torsten
Chakraborty, Trinad
author_sort Kuenne, Carsten
collection PubMed
description BACKGROUND: Listeria monocytogenes is an important food-borne pathogen and model organism for host-pathogen interaction, thus representing an invaluable target considering research on the forces governing the evolution of such microbes. The diversity of this species has not been exhaustively explored yet, as previous efforts have focused on analyses of serotypes primarily implicated in human listeriosis. We conducted complete genome sequencing of 11 strains employing 454 GS FLX technology, thereby achieving full coverage of all serotypes including the first complete strains of serotypes 1/2b, 3c, 3b, 4c, 4d, and 4e. These were comparatively analyzed in conjunction with publicly available data and assessed for pathogenicity in the Galleria mellonella insect model. RESULTS: The species pan-genome of L. monocytogenes is highly stable but open, suggesting an ability to adapt to new niches by generating or including new genetic information. The majority of gene-scale differences represented by the accessory genome resulted from nine hyper variable hotspots, a similar number of different prophages, three transposons (Tn916, Tn554, IS3-like), and two mobilizable islands. Only a subset of strains showed CRISPR/Cas bacteriophage resistance systems of different subtypes, suggesting a supplementary function in maintenance of chromosomal stability. Multiple phylogenetic branches of the genus Listeria imply long common histories of strains of each lineage as revealed by a SNP-based core genome tree highlighting the impact of small mutations for the evolution of species L. monocytogenes. Frequent loss or truncation of genes described to be vital for virulence or pathogenicity was confirmed as a recurring pattern, especially for strains belonging to lineages III and II. New candidate genes implicated in virulence function were predicted based on functional domains and phylogenetic distribution. A comparative analysis of small regulatory RNA candidates supports observations of a differential distribution of trans-encoded RNA, hinting at a diverse range of adaptations and regulatory impact. CONCLUSIONS: This study determined commonly occurring hyper variable hotspots and mobile elements as primary effectors of quantitative gene-scale evolution of species L. monocytogenes, while gene decay and SNPs seem to represent major factors influencing long-term evolution. The discovery of common and disparately distributed genes considering lineages, serogroups, serotypes and strains of species L. monocytogenes will assist in diagnostic, phylogenetic and functional research, supported by the comparative genomic GECO-LisDB analysis server (http://bioinfo.mikrobio.med.uni-giessen.de/geco2lisdb).
format Online
Article
Text
id pubmed-3556495
institution National Center for Biotechnology Information
language English
publishDate 2013
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-35564952013-01-29 Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome Kuenne, Carsten Billion, André Mraheil, Mobarak Abu Strittmatter, Axel Daniel, Rolf Goesmann, Alexander Barbuddhe, Sukhadeo Hain, Torsten Chakraborty, Trinad BMC Genomics Research Article BACKGROUND: Listeria monocytogenes is an important food-borne pathogen and model organism for host-pathogen interaction, thus representing an invaluable target considering research on the forces governing the evolution of such microbes. The diversity of this species has not been exhaustively explored yet, as previous efforts have focused on analyses of serotypes primarily implicated in human listeriosis. We conducted complete genome sequencing of 11 strains employing 454 GS FLX technology, thereby achieving full coverage of all serotypes including the first complete strains of serotypes 1/2b, 3c, 3b, 4c, 4d, and 4e. These were comparatively analyzed in conjunction with publicly available data and assessed for pathogenicity in the Galleria mellonella insect model. RESULTS: The species pan-genome of L. monocytogenes is highly stable but open, suggesting an ability to adapt to new niches by generating or including new genetic information. The majority of gene-scale differences represented by the accessory genome resulted from nine hyper variable hotspots, a similar number of different prophages, three transposons (Tn916, Tn554, IS3-like), and two mobilizable islands. Only a subset of strains showed CRISPR/Cas bacteriophage resistance systems of different subtypes, suggesting a supplementary function in maintenance of chromosomal stability. Multiple phylogenetic branches of the genus Listeria imply long common histories of strains of each lineage as revealed by a SNP-based core genome tree highlighting the impact of small mutations for the evolution of species L. monocytogenes. Frequent loss or truncation of genes described to be vital for virulence or pathogenicity was confirmed as a recurring pattern, especially for strains belonging to lineages III and II. New candidate genes implicated in virulence function were predicted based on functional domains and phylogenetic distribution. A comparative analysis of small regulatory RNA candidates supports observations of a differential distribution of trans-encoded RNA, hinting at a diverse range of adaptations and regulatory impact. CONCLUSIONS: This study determined commonly occurring hyper variable hotspots and mobile elements as primary effectors of quantitative gene-scale evolution of species L. monocytogenes, while gene decay and SNPs seem to represent major factors influencing long-term evolution. The discovery of common and disparately distributed genes considering lineages, serogroups, serotypes and strains of species L. monocytogenes will assist in diagnostic, phylogenetic and functional research, supported by the comparative genomic GECO-LisDB analysis server (http://bioinfo.mikrobio.med.uni-giessen.de/geco2lisdb). BioMed Central 2013-01-22 /pmc/articles/PMC3556495/ /pubmed/23339658 http://dx.doi.org/10.1186/1471-2164-14-47 Text en Copyright ©2013 Kuenne et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Kuenne, Carsten
Billion, André
Mraheil, Mobarak Abu
Strittmatter, Axel
Daniel, Rolf
Goesmann, Alexander
Barbuddhe, Sukhadeo
Hain, Torsten
Chakraborty, Trinad
Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome
title Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome
title_full Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome
title_fullStr Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome
title_full_unstemmed Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome
title_short Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome
title_sort reassessment of the listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3556495/
https://www.ncbi.nlm.nih.gov/pubmed/23339658
http://dx.doi.org/10.1186/1471-2164-14-47
work_keys_str_mv AT kuennecarsten reassessmentofthelisteriamonocytogenespangenomerevealsdynamicintegrationhotspotsandmobilegeneticelementsasmajorcomponentsoftheaccessorygenome
AT billionandre reassessmentofthelisteriamonocytogenespangenomerevealsdynamicintegrationhotspotsandmobilegeneticelementsasmajorcomponentsoftheaccessorygenome
AT mraheilmobarakabu reassessmentofthelisteriamonocytogenespangenomerevealsdynamicintegrationhotspotsandmobilegeneticelementsasmajorcomponentsoftheaccessorygenome
AT strittmatteraxel reassessmentofthelisteriamonocytogenespangenomerevealsdynamicintegrationhotspotsandmobilegeneticelementsasmajorcomponentsoftheaccessorygenome
AT danielrolf reassessmentofthelisteriamonocytogenespangenomerevealsdynamicintegrationhotspotsandmobilegeneticelementsasmajorcomponentsoftheaccessorygenome
AT goesmannalexander reassessmentofthelisteriamonocytogenespangenomerevealsdynamicintegrationhotspotsandmobilegeneticelementsasmajorcomponentsoftheaccessorygenome
AT barbuddhesukhadeo reassessmentofthelisteriamonocytogenespangenomerevealsdynamicintegrationhotspotsandmobilegeneticelementsasmajorcomponentsoftheaccessorygenome
AT haintorsten reassessmentofthelisteriamonocytogenespangenomerevealsdynamicintegrationhotspotsandmobilegeneticelementsasmajorcomponentsoftheaccessorygenome
AT chakrabortytrinad reassessmentofthelisteriamonocytogenespangenomerevealsdynamicintegrationhotspotsandmobilegeneticelementsasmajorcomponentsoftheaccessorygenome