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

Kuenne C, Billion A, Mraheil MA, Strittmatter A, Daniel R, Goesmann A, Barbuddhe S, Hain T, Chakraborty T (2013)
BMC Genomics 14(1): 47.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
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Kuenne, Carsten; Billion, André; Mraheil, Mobarak Abu; Strittmatter, Axel; Daniel, Rolf; Goesmann, AlexanderUniBi ; Barbuddhe, Sukhadeo; Hain, Torsten; Chakraborty, Trinad
Abstract / Bemerkung
ABSTRACT: 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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Kuenne C, Billion A, Mraheil MA, et al. Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome. BMC Genomics. 2013;14(1): 47.
Kuenne, C., Billion, A., Mraheil, M. A., Strittmatter, A., Daniel, R., Goesmann, A., Barbuddhe, S., et al. (2013). Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome. BMC Genomics, 14(1), 47. doi:10.1186/1471-2164-14-47
Kuenne, Carsten, Billion, André, Mraheil, Mobarak Abu, Strittmatter, Axel, Daniel, Rolf, Goesmann, Alexander, Barbuddhe, Sukhadeo, Hain, Torsten, and Chakraborty, Trinad. 2013. “Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome”. BMC Genomics 14 (1): 47.
Kuenne, C., Billion, A., Mraheil, M. A., Strittmatter, A., Daniel, R., Goesmann, A., Barbuddhe, S., Hain, T., and Chakraborty, T. (2013). Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome. BMC Genomics 14:47.
Kuenne, C., et al., 2013. Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome. BMC Genomics, 14(1): 47.
C. Kuenne, et al., “Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome”, BMC Genomics, vol. 14, 2013, : 47.
Kuenne, C., Billion, A., Mraheil, M.A., Strittmatter, A., Daniel, R., Goesmann, A., Barbuddhe, S., Hain, T., Chakraborty, T.: Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome. BMC Genomics. 14, : 47 (2013).
Kuenne, Carsten, Billion, André, Mraheil, Mobarak Abu, Strittmatter, Axel, Daniel, Rolf, Goesmann, Alexander, Barbuddhe, Sukhadeo, Hain, Torsten, and Chakraborty, Trinad. “Reassessment of the Listeria monocytogenes pan-genome reveals dynamic integration hotspots and mobile genetic elements as major components of the accessory genome”. BMC Genomics 14.1 (2013): 47.

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Hamon M, Bierne H, Cossart P., Nat. Rev. Microbiol. 4(6), 2006
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Christiansen JK, Nielsen JS, Ebersbach T, Valentin-Hansen P, Sogaard-Andersen L, Kallipolitis BH., RNA 12(7), 2006
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Listeria monocytogenes internalins are highly diverse and evolved by recombination and positive selection.
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Augur--a computational pipeline for whole genome microbial surface protein prediction and classification.
Billion A, Ghai R, Chakraborty T, Hain T., Bioinformatics 22(22), 2006
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GECO--linear visualization for comparative genomics.
Kuenne CT, Ghai R, Chakraborty T, Hain T., Bioinformatics 23(1), 2006
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Identification of new noncoding RNAs in Listeria monocytogenes and prediction of mRNA targets.
Mandin P, Repoila F, Vergassola M, Geissmann T, Cossart P., Nucleic Acids Res. 35(3), 2007
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PILER-CR: fast and accurate identification of CRISPR repeats.
Edgar RC., BMC Bioinformatics 8(), 2007
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Two variable lymphocyte receptor genes of the inshore hagfish are located far apart on the same chromosome.
Kasamatsu J, Suzuki T, Ishijima J, Matsuda Y, Kasahara M., Immunogenetics 59(4), 2007
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Assessment of phylogenomic and orthology approaches for phylogenetic inference.
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Novel factor rescues ribosomes trapped on non-stop mRNAs.
Himeno H., Mol. Microbiol. 78(4), 2010
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BIGSdb: Scalable analysis of bacterial genome variation at the population level.
Jolley KA, Maiden MC., BMC Bioinformatics 11(), 2010
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Comparative genomics of the bacterial genus Listeria: Genome evolution is characterized by limited gene acquisition and limited gene loss.
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