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PMID: 14742555 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

New aspects regarding evolution and virulence of Listeria monocytogenes revealed by comparative genomics and DNA arrays.

Infection and immunity ·Vol. 72 ·No. 2 ·2004-02-00 ·Pages 1072-83

Doumith M, Cazalet C, Simoes N, Frangeul L, Jacquet C, Kunst F, Martin P, Cossart P, Glaser P, Buchrieser C

Abstract

Listeria monocytogenes is a food-borne bacterial pathogen that causes a wide spectrum of diseases, such as meningitis, septicemia, abortion, and gastroenteritis, in humans and animals. Among the 13 L. monocytogenes serovars described, invasive disease is mostly associated with serovar 4b strains. To investigate the genetic diversity of L. monocytogenes strains with different virulence potentials, we partially sequenced an epidemic serovar 4b strain and compared it with the complete sequence of the nonepidemic L. monocytogenes EGDe serovar 1/2a strain. We identified an unexpected genetic divergence between the two strains, as about 8% of the sequences were serovar 4b specific. These sequences included seven genes coding for surface proteins, two of which belong to the internalin family, and three genes coding for transcriptional regulators, all of which might be important in different steps of the infectious process. Based on the sequence information, we then characterized the gene content of 113 Listeria strains by using a newly designed Listeria array containing the "flexible" part of the sequenced Listeria genomes. Hybridization results showed that all of the previously identified virulence factors of L. monocytogenes were present in the 93 L. monocytogenes strains tested. However, distinct patterns of the presence or absence of other genes were identified among the different L. monocytogenes serovars and Listeria species. These results allow new insights into the evolution of L. monocytogenes, suggesting that early divergence of the ancestral L. monocytogenes serovar 1/2c strains from the serovar 1/2b strains led to two major phylogenetic lineages, one of them including the serogroup 4 strains, which branched off the serovar 1/2b ancestral lineage, leading (mostly by gene loss) to the species Listeria innocua. The identification of 30 L. monocytogenes-specific and several serovar-specific marker genes, such as three L. monocytogenes serovar 4b-specific surface protein-coding genes, should prove powerful for the rapid tracing of listeriosis outbreaks, but it also represents a fundamental basis for the functional study of virulence differences between L. monocytogenes strains.

MeSH Terms
Biological Evolution Cell Wall/chemistry Genetic Markers Genetic Variation Genome, Bacterial Listeria monocytogenes/classification,genetics,pathogenicity Nucleic Acid Hybridization/methods Teichoic Acids/metabolism Virulence
Chemicals
Genetic Markers Teichoic Acids
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Doumith Michel
Laboratoire des Listeria, Centre National de Référence des Listeria, World Health Organization Collaborating Center for Foodborne Listeriosis, Institut Pasteur, 75724 Paris 15, France.
Cazalet Christel
Simoes Natalie
Frangeul Lionel
Jacquet Christine
Kunst Frank
Martin Paul
Cossart Pascale
Glaser Philippe
Buchrieser Carmen
References (34)
34 references, click to expand
  1. Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease.
    Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1556-61 PMID: 11818571
  2. The bvr locus of Listeria monocytogenes mediates virulence gene repression by beta-glucosides.
    J Bacteriol. 1999 Aug;181(16):5024-32 PMID: 10438775
  3. Surface proteins and the pathogenic potential of Listeria monocytogenes.
    Trends Microbiol. 2002 May;10(5):238-45 PMID: 11973158
  4. Redefining bacterial populations: a post-genomic reformation.
    Nat Rev Genet. 2002 Jun;3(6):462-73 PMID: 12042773
  5. Listeria monocytogenes bile salt hydrolase is a PrfA-regulated virulence factor involved in the intestinal and hepatic phases of listeriosis.
    Mol Microbiol. 2002 Aug;45(4):1095-106 PMID: 12180927
  6. Application of DNA microarrays to study the evolutionary genomics of Yersinia pestis and Yersinia pseudotuberculosis.
    Genome Res. 2003 Sep;13(9):2018-29 PMID: 12952873
  7. CAAT-Box, Contigs-Assembly and Annotation Tool-Box for genome sequencing projects.
    Bioinformatics. 2004 Mar 22;20(5):790-7 PMID: 14752000
  8. Biochemistry of the cell surface of Listeria strains: a locating general view.
    Infection. 1988;16 Suppl 2:S92-7 PMID: 3417357
  9. Genetic characterization of clones of the bacterium Listeria monocytogenes causing epidemic disease.
    Proc Natl Acad Sci U S A. 1989 May;86(10):3818-22 PMID: 2498876
  10. Analysis of Listeria monocytogenes by multilocus enzyme electrophoresis and application of the method to epidemiologic investigations.
    Int J Food Microbiol. 1989 Jun;8(3):233-9 PMID: 2518381
  11. Phylogenetic analysis of the genus Listeria based on reverse transcriptase sequencing of 16S rRNA.
    Int J Syst Bacteriol. 1991 Apr;41(2):240-6 PMID: 1713054
  12. Subtyping of Listeria monocytogenes serovar 4b by use of low-frequency-cleavage restriction endonucleases and pulsed-field gel electrophoresis.
    Res Microbiol. 1991 Jul-Aug;142(6):667-75 PMID: 1961978
  13. Pulsed-field fingerprinting of listeriae: identification of genomic divisions for Listeria monocytogenes and their correlation with serovar.
    Appl Environ Microbiol. 1994 Jul;60(7):2584-92 PMID: 8074531
  14. Comparison of ribotyping and multilocus enzyme electrophoresis for subtyping of Listeria monocytogenes isolates.
    J Clin Microbiol. 1994 Dec;32(12):2936-43 PMID: 7883880
  15. Comparative analysis of 16S and 23S rRNA sequences of Listeria species.
    Int J Syst Bacteriol. 1996 Jul;46(3):669-74 PMID: 8782674
  16. Ribotypes and virulence gene polymorphisms suggest three distinct Listeria monocytogenes lineages with differences in pathogenic potential.
    Infect Immun. 1997 Jul;65(7):2707-16 PMID: 9199440
  17. Genome organization and the evolution of the virulence gene locus in Listeria species.
    Int J Med Microbiol. 2000 May;290(2):167-74 PMID: 11045921
  18. A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains.
    Proc Natl Acad Sci U S A. 2000 Dec 19;97(26):14668-73 PMID: 11121067
  19. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7.
    Nature. 2001 Jan 25;409(6819):529-33 PMID: 11206551
  20. J-Express: exploring gene expression data using Java.
    Bioinformatics. 2001 Apr;17(4):369-70 PMID: 11301307
  21. PulseNet standardized protocol for subtyping Listeria monocytogenes by macrorestriction and pulsed-field gel electrophoresis.
    Int J Food Microbiol. 2001 Apr 11;65(1-2):55-62 PMID: 11322701
  22. Comparative genetic characterization of Listeria monocytogenes isolates from human and animal listeriosis cases.
    Microbiology. 2001 May;147(Pt 5):1095-104 PMID: 11320113
  23. Gene fragments distinguishing an epidemic-associated strain from a virulent prototype strain of Listeria monocytogenes belong to a distinct functional subset of genes and partially cross-hybridize with other Listeria species.
    Infect Immun. 2001 Jun;69(6):3972-9 PMID: 11349066
  24. Listeria pathogenesis and molecular virulence determinants.
    Clin Microbiol Rev. 2001 Jul;14(3):584-640 PMID: 11432815
  25. Evolutionary genomics of Staphylococcus aureus: insights into the origin of methicillin-resistant strains and the toxic shock syndrome epidemic.
    Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8821-6 PMID: 11447287
  26. Comparative genomics of Listeria species.
    Science. 2001 Oct 26;294(5543):849-52 PMID: 11679669
  27. Hpt, a bacterial homolog of the microsomal glucose- 6-phosphate translocase, mediates rapid intracellular proliferation in Listeria.
    Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):431-6 PMID: 11756655
  28. Expression of ActA, Ami, InlB, and listeriolysin O in Listeria monocytogenes of human and food origin.
    Appl Environ Microbiol. 2002 Feb;68(2):616-22 PMID: 11823199
  29. Evolutionary genomics of pathogenic bacteria.
    Trends Microbiol. 2001 Nov;9(11):547-53 PMID: 11825715
  30. Comparison of PCR-based DNA fingerprinting techniques for the identification of Listeria species and their use for atypical Listeria isolates.
    Int J Syst Bacteriol. 1998 Jan;48 Pt 1:127-39 PMID: 9542083
  31. Cell wall teichoic acid glycosylation in Listeria monocytogenes serotype 4b requires gtcA, a novel, serogroup-specific gene.
    J Bacteriol. 1999 Jan;181(2):418-25 PMID: 9882654
  32. Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori.
    Nature. 1999 Jan 14;397(6715):176-80 PMID: 9923682
  33. Comparative genomics of BCG vaccines by whole-genome DNA microarray.
    Science. 1999 May 28;284(5419):1520-3 PMID: 10348738
  34. A new evolutionary scenario for the Mycobacterium tuberculosis complex.
    Proc Natl Acad Sci U S A. 2002 Mar 19;99(6):3684-9 PMID: 11891304
Article Info
Journal
Infection and immunity
Abbr.
Infect Immun
ISSN
0019-9567
Published
2004-02-00
Pages
1072-83
Language
English
Region
United States
NLM ID
0246127
PMCID
PMC321639
Subset
IM
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