Genome diversification in phylogenetic lineages I and II of Listeria monocytogenes: Identification of segments unique to lineage II populations

Chaomei Zhang, Min Zhang, Jingliang Ju, Joseph Nietfeldt, John Wise, Philip M. Terry, Michael Olson, Stephen D. Kachman, Martin Wiedmann, Mansour Samadpour, Andrew K. Benson

Research output: Contribution to journalArticle

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Abstract

Thirteen different serotypes of Listeria monocytogenes can be distinguished on the basis of variation in somatic and flagellar antigens. Although the known virulence genes are present in all serotypes, greater than 90% of human cases of listeriosis are caused by serotypes 1/2a, 1/2b, and 4b and nearly all outbreaks of food-borne listeriosis have been caused by serotype 4b strains. Phylogenetic analysis of these three common clinical serotypes places them into two different lineages, with serotypes 1/2b and 4b belonging to lineage I and 1/2a belonging to lineage II. To begin examining evolution of the genome in these serotypes, DNA microarray analysis was used to identify lineage-specific and serotype-specific differences in genome content. A set of 44 strains representing serotypes 1/2a, 1/2b, and 4b was probed with a shotgun DNA microarray constructed from the serotype 1/2a strain 10403s. Clones spanning 47 different genes in 16 different contiguous segments relative to the lineage II 1/2a genome were found to be absent in all lineage I strains tested (serotype 4b and 1/2b) and an additional nine were altered exclusively in 4b strains. Southern hybridization confirmed that conserved alterations were, in all but two loci, due to absence of the segments from the genome. Genes within these contiguous segments comprise five functional categories, including genes involved in synthesis of cell surface molecules and regulation of virulence gene expression. Phylogenetic reconstruction and examination of compositional bias in the regions of difference are consistent with a model in which the ancestor of the two lineages had the 1/2 somatic serotype and the regions absent in the lineage I genome arose by loss of ancestral sequences.

Original languageEnglish (US)
Pages (from-to)5573-5584
Number of pages12
JournalJournal of bacteriology
Volume185
Issue number18
DOIs
StatePublished - Sep 1 2003

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Listeria monocytogenes
Genome
Population
Listeriosis
Oligonucleotide Array Sequence Analysis
Genes
Virulence
Serogroup
Firearms
Gene Expression Regulation
Microarray Analysis
Disease Outbreaks
Clone Cells

ASJC Scopus subject areas

  • Microbiology
  • Molecular Biology

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Genome diversification in phylogenetic lineages I and II of Listeria monocytogenes : Identification of segments unique to lineage II populations. / Zhang, Chaomei; Zhang, Min; Ju, Jingliang; Nietfeldt, Joseph; Wise, John; Terry, Philip M.; Olson, Michael; Kachman, Stephen D.; Wiedmann, Martin; Samadpour, Mansour; Benson, Andrew K.

In: Journal of bacteriology, Vol. 185, No. 18, 01.09.2003, p. 5573-5584.

Research output: Contribution to journalArticle

Zhang, Chaomei ; Zhang, Min ; Ju, Jingliang ; Nietfeldt, Joseph ; Wise, John ; Terry, Philip M. ; Olson, Michael ; Kachman, Stephen D. ; Wiedmann, Martin ; Samadpour, Mansour ; Benson, Andrew K. / Genome diversification in phylogenetic lineages I and II of Listeria monocytogenes : Identification of segments unique to lineage II populations. In: Journal of bacteriology. 2003 ; Vol. 185, No. 18. pp. 5573-5584.
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AU - Wise, John

AU - Terry, Philip M.

AU - Olson, Michael

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AB - Thirteen different serotypes of Listeria monocytogenes can be distinguished on the basis of variation in somatic and flagellar antigens. Although the known virulence genes are present in all serotypes, greater than 90% of human cases of listeriosis are caused by serotypes 1/2a, 1/2b, and 4b and nearly all outbreaks of food-borne listeriosis have been caused by serotype 4b strains. Phylogenetic analysis of these three common clinical serotypes places them into two different lineages, with serotypes 1/2b and 4b belonging to lineage I and 1/2a belonging to lineage II. To begin examining evolution of the genome in these serotypes, DNA microarray analysis was used to identify lineage-specific and serotype-specific differences in genome content. A set of 44 strains representing serotypes 1/2a, 1/2b, and 4b was probed with a shotgun DNA microarray constructed from the serotype 1/2a strain 10403s. Clones spanning 47 different genes in 16 different contiguous segments relative to the lineage II 1/2a genome were found to be absent in all lineage I strains tested (serotype 4b and 1/2b) and an additional nine were altered exclusively in 4b strains. Southern hybridization confirmed that conserved alterations were, in all but two loci, due to absence of the segments from the genome. Genes within these contiguous segments comprise five functional categories, including genes involved in synthesis of cell surface molecules and regulation of virulence gene expression. Phylogenetic reconstruction and examination of compositional bias in the regions of difference are consistent with a model in which the ancestor of the two lineages had the 1/2 somatic serotype and the regions absent in the lineage I genome arose by loss of ancestral sequences.

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