1887

Abstract

The surface molecule InlA interacts with E-cadherin to promote invasion of into selected host cells. DNA sequencing of for 40 isolates revealed 107 synonymous and 45 nonsynonymous substitutions. A frameshift mutation in a homopolymeric tract encoding part of the InlA signal peptide was identified in three lineage II isolates, which also showed reduced ability to invade human intestinal epithelial cells. Phylogenies showed clear separation of sequences into lineages I and II. Thirteen recombination events, predominantly involving lineage II strains as recipients (12 events), were detected and a number of amino acid residues were shown to be under positive selection. Four of the 45 non-synonymous changes were found to be under positive selection with posterior probabilities >95 %. Mapping of polymorphic and positively selected amino acid sites on the partial crystal structure for InlA showed that the internalin surface of the leucine-rich repeat (LRR) region that faces the InlA receptor E-cadherin does not include any polymorphic sites; all polymorphic and positively selected amino acids mapped to the outer face of the LRR region or to other InlA regions. The data show that (i) is highly polymorphic and evolution of involved a considerable number of recombination events in lineage II isolates; (ii) positive selection at specific amino acid sites appears to contribute to evolution of , including fixation of recombinant events; and (iii) single-nucleotide deletions in a lineage II-specific 3′ homopolymeric tract in lead to complete loss of InlA or to production of truncated InlA, which conveys reduced invasiveness. In conclusion, has a complex evolutionary history, which is consistent with ’ natural history as an environmental pathogen with broad host-range, including its adaptation to environments and hosts where different alleles may provide a selective advantage or where may not be required.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.2007/007310-0
2007-08-01
2019-10-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/8/2666.html?itemId=/content/journal/micro/10.1099/mic.0.2007/007310-0&mimeType=html&fmt=ahah

References

  1. Andrews, T. D. & Gojobori, T. ( 2004; ). Strong positive selection and recombination drive the antigenic variation of the PilE protein of the human pathogen Neisseria meningitidis. Genetics 166, 25–32.[CrossRef]
    [Google Scholar]
  2. Anisimova, M., Nielsen, R. & Yang, Z. ( 2003; ). Effect of recombination on the accuracy of the likelihood method for detecting positive selection at amino acid sites. Genetics 164, 1229–1236.
    [Google Scholar]
  3. Bakardjiev, A. I., Stacy, B. A., Fisher, S. J. & Portnoy, D. A. ( 2004; ). Listeriosis in the pregnant guinea pig: a model of vertical transmission. Infect Immun 72, 489–497.[CrossRef]
    [Google Scholar]
  4. Berman, H. M., Bhat, T. N., Bourne, P. E., Feng, Z., Gilliland, G., Weissig, H. & Westbrook, J. ( 2000; ). The Protein Data Bank and the challenge of structural genomics. Nat Struct Biol 7 (Suppl.), 957–959.[CrossRef]
    [Google Scholar]
  5. Bishop, D. K. & Hinrichs, D. J. ( 1987; ). Adoptive transfer of immunity to Listeria monocytogenes. The influence of in vitro stimulation on lymphocyte subset requirements. J Immunol 139, 2005–2009.
    [Google Scholar]
  6. Dhar, G., Faull, K. F. & Schneewind, O. ( 2000; ). Anchor structure of cell wall surface proteins in Listeria monocytogenes. Biochemistry 39, 3725–3733.[CrossRef]
    [Google Scholar]
  7. Dramsi, S., Kocks, C., Forestier, C. & Cossart, P. ( 1993; ). Internalin-mediated invasion of epithelial cells by Listeria monocytogenes is regulated by the bacterial growth state, temperature and the pleiotropic activator prfA. Mol Microbiol 9, 931–941.[CrossRef]
    [Google Scholar]
  8. Gaillard, J. L., Berche, P., Frehel, C., Gouin, E. & Cossart, P. ( 1991; ). Entry of L. monocytogenes into cells is mediated by internalin, a repeat protein reminiscent of surface antigens from gram-positive cocci. Cell 65, 1127–1141.[CrossRef]
    [Google Scholar]
  9. Gray, M. J., Zadoks, R. N., Fortes, E. D., Dogan, B., Cai, S., Chen, Y., Scott, V. N., Gombas, D. E., Boor, K. J. & Wiedmann, M. ( 2004; ). Listeria monocytogenes isolates from foods and humans form distinct but overlapping populations. Appl Environ Microbiol 70, 5833–5841.[CrossRef]
    [Google Scholar]
  10. Jeffers, G. T., Bruce, J. L., McDonough, P. L., Scarlett, J., Boor, K. J. & Wiedmann, M. ( 2001; ). Comparative genetic characterization of Listeria monocytogenes isolates from human and animal listeriosis cases. Microbiology 147, 1095–1104.
    [Google Scholar]
  11. Jonquieres, R., Bierne, H., Mengaud, J. & Cossart, P. ( 1998; ). The inlA gene of Listeria monocytogenes LO28 harbors a nonsense mutation resulting in release of internalin. Infect Immun 66, 3420–3422.
    [Google Scholar]
  12. Kearns, D. B., Chu, F., Rudner, R. & Losick, R. ( 2004; ). Genes governing swarming in Bacillus subtilis and evidence for a phase variation mechanism controlling surface motility. Mol Microbiol 52, 357–369.[CrossRef]
    [Google Scholar]
  13. Lecuit, M., Dramsi, S., Gottardi, C., Fedor-Chaiken, M., Gumbiner, B. & Cossart, P. ( 1999; ). A single amino acid in E-cadherin responsible for host specificity towards the human pathogen Listeria monocytogenes. EMBO J 18, 3956–3963.[CrossRef]
    [Google Scholar]
  14. Lecuit, M., Vandormael-Pournin, S., Lefort, J., Huerre, M., Gounon, P., Dupuy, C., Babinet, C. & Cossart, P. ( 2001; ). A transgenic model for listeriosis: role of internalin in crossing the intestinal barrier. Science 292, 1722–1725.[CrossRef]
    [Google Scholar]
  15. Lecuit, M., Nelson, D. M., Smith, S. D., Khun, H., Huerre, M., Vacher-Lavenu, M. C., Gordon, J. I. & Cossart, P. ( 2004; ). Targeting and crossing of the human maternofetal barrier by Listeria monocytogenes: role of internalin interaction with trophoblast E-cadherin. Proc Natl Acad Sci U S A 101, 6152–6157.[CrossRef]
    [Google Scholar]
  16. Mansfield, B. E., Dionne, M. S., Schneider, D. S. & Freitag, N. E. ( 2003; ). Exploration of host–pathogen interactions using Listeria monocytogenes and Drosophila melanogaster. Cell Microbiol 5, 901–911.[CrossRef]
    [Google Scholar]
  17. McGraw, E. A., Li, J., Selander, R. K. & Whittam, T. S. ( 1999; ). Molecular evolution and mosaic structure of α, β, and γ intimins of pathogenic Escherichia coli. Mol Biol Evol 16, 12–22.[CrossRef]
    [Google Scholar]
  18. Meinersmann, R. J., Phillips, R. W., Wiedmann, M. & Berrang, M. E. ( 2004; ). Multilocus sequence typing of Listeria monocytogenes by use of hypervariable genes reveals clonal and recombination histories of three lineages. Appl Environ Microbiol 70, 2193–2203.[CrossRef]
    [Google Scholar]
  19. Mengaud, J., Lecuit, M., Lebrun, M., Nato, F., Mazie, J. C. & Cossart, P. ( 1996; ). Antibodies to the leucine-rich repeat region of internalin block entry of Listeria monocytogenes into cells expressing E-cadherin. Infect Immun 64, 5430–5433.
    [Google Scholar]
  20. Milkman, R., Jaeger, E. & McBride, R. D. ( 2003; ). Molecular evolution of the Escherichia coli chromosome. VI. Two regions of high effective recombination. Genetics 163, 475–483.
    [Google Scholar]
  21. Nielsen, R. ( 2001; ). Statistical tests of selective neutrality in the age of genomics. Heredity 86, 641–647.[CrossRef]
    [Google Scholar]
  22. Nightingale, K. K., Windham, K. & Wiedmann, M. ( 2005a; ). Evolution and molecular phylogeny of Listeria monocytogenes isolated from human and animal listeriosis cases and foods. J Bacteriol 187, 5537–5551.[CrossRef]
    [Google Scholar]
  23. Nightingale, K. K., Windham, K., Martin, K. E., Yeung, M. & Wiedmann, M. ( 2005b; ). Select Listeria monocytogenes subtypes commonly found in foods carry distinct nonsense mutations in inlA, leading to expression of truncated and secreted internalin A, and are associated with a reduced invasion phenotype for human intestinal epithelial cells. Appl Environ Microbiol 71, 8764–8772.[CrossRef]
    [Google Scholar]
  24. Olier, M., Pierre, F., Lemaitre, J. P., Divies, C., Rousset, A. & Guzzo, J. ( 2002; ). Assessment of the pathogenic potential of two Listeria monocytogenes human faecal carriage isolates. Microbiology 148, 1855–1862.
    [Google Scholar]
  25. Olier, M., Pierre, F., Rousseaux, S., Lemaitre, J. P., Rousset, A., Piveteau, P. & Guzzo, J. ( 2003; ). Expression of truncated internalin A is involved in impaired internalization of some Listeria monocytogenes isolates carried asymptomatically by humans. Infect Immun 71, 1217–1224.[CrossRef]
    [Google Scholar]
  26. Peek, A. S., Souza, V., Eguiarte, L. E. & Gaut, B. S. ( 2001; ). The interaction of protein structure, selection, and recombination on the evolution of the type-1 fimbrial major subunit (fimA) from Escherichia coli. J Mol Evol 52, 193–204.
    [Google Scholar]
  27. Polley, S. D. & Conway, D. J. ( 2001; ). Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene. Genetics 158, 1505–1512.
    [Google Scholar]
  28. Posada, D. & Crandall, K. A. ( 1998; ). modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.[CrossRef]
    [Google Scholar]
  29. Roberts, A., Nightingale, K., Jeffers, G., Fortes, E., Kongo, J. M. & Wiedmann, M. ( 2006; ). Genetic and phenotypic characterization of Listeria monocytogenes lineage III. Microbiology 152, 685–693.[CrossRef]
    [Google Scholar]
  30. Rousseaux, S., Olier, M., Lemaitre, J. P., Piveteau, P. & Guzzo, J. ( 2004; ). Use of PCR-restriction fragment length polymorphism of inlA for rapid screening of Listeria monocytogenes strains deficient in the ability to invade Caco-2 cells. Appl Environ Microbiol 70, 2180–2185.[CrossRef]
    [Google Scholar]
  31. Rozas, J. & Rozas, R. ( 1999; ). DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174–175.[CrossRef]
    [Google Scholar]
  32. Sauders, B. D., Durak, M. Z., Fortes, E., Windham, K., Schukken, Y., Lembo, A. J., Jr, Akey, B., Nightingale, K. K. & Wiedmann, M. ( 2006; ). Molecular characterization of Listeria monocytogenes from natural and urban environments. J Food Prot 69, 93–105.
    [Google Scholar]
  33. Schubert, W. D., Urbanke, C., Ziehm, T., Beier, V., Machner, M. P., Domann, E., Wehland, J., Chakraborty, T. & Heinz, D. W. ( 2002; ). Structure of internalin, a major invasion protein of Listeria monocytogenes, in complex with its human receptor E-cadherin. Cell 111, 825–836.[CrossRef]
    [Google Scholar]
  34. Segura, A., Hurtado, A., Duque, E. & Ramos, J. L. ( 2004; ). Transcriptional phase variation at the flhB gene of Pseudomonas putida DOT-T1E is involved in response to environmental changes and suggests the participation of the flagellar export system in solvent tolerance. J Bacteriol 186, 1905–1909.[CrossRef]
    [Google Scholar]
  35. Snyder, A. & Marquis, H. ( 2003; ). Restricted translocation across the cell wall regulates secretion of the broad-range phospholipase C of Listeria monocytogenes. J Bacteriol 185, 5953–5958.[CrossRef]
    [Google Scholar]
  36. Theiss, P. & Wise, K. S. ( 1997; ). Localized frameshift mutation generates selective, high-frequency phase variation of a surface lipoprotein encoded by a mycoplasma ABC transporter operon. J Bacteriol 179, 4013–4022.
    [Google Scholar]
  37. Tsai, Y. H., Orsi, R. H., Nightingale, K. K. & Wiedmann, M. ( 2006; ). Listeria monocytogenes internalins are highly diverse and evolved by recombination and positive selection. Infect Genet Evol 6, 378–389.[CrossRef]
    [Google Scholar]
  38. Urwin, R., Holmes, E. C., Fox, A. J., Derrick, J. P. & Maiden, M. C. ( 2002; ). Phylogenetic evidence for frequent positive selection and recombination in the meningococcal surface antigen PorB. Mol Biol Evol 19, 1686–1694.[CrossRef]
    [Google Scholar]
  39. Vazquez-Boland, J. A., Kuhn, M., Berche, P., Chakraborty, T., Dominguez-Bernal, G., Goebel, W., Gonzalez-Zorn, B., Wehland, J. & Kreft, J. ( 2001; ). Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14, 584–640.[CrossRef]
    [Google Scholar]
  40. Ward, T. J., Gorski, L., Borucki, M. K., Mandrell, R. E., Hutchins, J. & Pupedis, K. ( 2004; ). Intraspecific phylogeny and lineage group identification based on the prfA virulence gene cluster of Listeria monocytogenes. J Bacteriol 186, 4994–5002.[CrossRef]
    [Google Scholar]
  41. Wiedmann, M., Bruce, J. L., Keating, C., Johnson, A. E., McDonough, P. L. & Batt, C. A. ( 1997; ). Ribotypes and virulence gene polymorphisms suggest three distinct Listeria monocytogenes lineages with differences in pathogenic potential. Infect Immun 65, 2707–2716.
    [Google Scholar]
  42. Wilson, R. L., Elthon, J., Clegg, S. & Jones, B. D. ( 2000; ). Salmonella enterica serovars Gallinarum and Pullorum expressing Salmonella enterica serovar Typhimurium type 1 fimbriae exhibit increased invasiveness for mammalian cells. Infect Immun 68, 4782–4785.[CrossRef]
    [Google Scholar]
  43. Yang, Z. ( 1997; ). paml: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13, 555–556.
    [Google Scholar]
  44. Yang, Z. & Nielsen, R. ( 2002; ). Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 19, 908–917.[CrossRef]
    [Google Scholar]
  45. Yang, Z., Nielsen, R., Goldman, N. & Pedersen, A. M. K. ( 2000; ). Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155, 431–449.
    [Google Scholar]
  46. Yang, Z., Wong, W. S. & Nielsen, R. ( 2005; ). Bayes empirical Bayes inference of amino acid sites under positive selection. Mol Biol Evol 22, 1107–1118.[CrossRef]
    [Google Scholar]
  47. Zhang, J., Nielsen, R. & Yang, Z. ( 2005; ). Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22, 2472–2479.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.2007/007310-0
Loading
/content/journal/micro/10.1099/mic.0.2007/007310-0
Loading

Data & Media loading...

isolates used and their characteristics. [PDF](37 KB)

PDF

Primers used for PCR and sequencing. [PDF](37 KB)

PDF

Recombination events in allelic types (AT) (detailed data). [PDF](41 KB)

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error