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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 ; Abu Mraheil, Mobarak ; Strittmatter, Axel ; Daniel, Rolf ; Goesmann, Alexander ; Barbuddheand , Sukhadeo ; Hain, Torsten ; Chakraborty, Trinad

Originalveröffentlichung: (2013) BMC Genomics 14(1):47 doi:10.1186/1471-2164-14-47
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URN: urn:nbn:de:hebis:26-opus-104164

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Sammlung: Open Access - Publikationsfonds
Universität Justus-Liebig-Universität Gießen
Fachgebiet: Medizin
DDC-Sachgruppe: Medizin
Dokumentart: Aufsatz
Sprache: Englisch
Erstellungsjahr: 2013
Publikationsdatum: 06.12.2013
Kurzfassung auf Englisch: 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
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