Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1989 May;86(10):3818–3822. doi: 10.1073/pnas.86.10.3818

Genetic characterization of clones of the bacterium Listeria monocytogenes causing epidemic disease.

J C Piffaretti 1, H Kressebuch 1, M Aeschbacher 1, J Bille 1, E Bannerman 1, J M Musser 1, R K Selander 1, J Rocourt 1
PMCID: PMC287232  PMID: 2498876

Abstract

One hundred and seventy-five isolates of the pathogenic bacterium Listeria monocytogenes recovered from human clinical (blood and cerebrospinal fluid), animal, and environmental sources in Europe, North America, and elsewhere were analyzed electrophoretically for allelic variation at 16 genetic loci encoding metabolic enzymes. Forty-five distinctive allele profiles (electrophoretic types, ETs) were distinguished, among which mean genetic diversity per locus (H) was 0.424. Cluster analysis of a matrix of genetic distances between paired ETs revealed two primary phylogenetic divisions of the species separated at a distance of 0.54. ETs in division I were presented by strains of serotypes 4b, 1/2b, and 4a, whereas strains of ETs in division II were of serotypes 1/2a and 1/2c. Human and animal isolates did not represent distinctive subsets of ETs. The occurrence of linkage disequilibrium between enzyme loci and the widespread distribution of certain ETs indicate that the genetic structure of L. monocytogenes is clonal. One clone, marked by ET1, caused major epidemics of human disease in western Switzerland in the period 1983-1987 and in Los Angeles County, California, in 1985, both of which were attributed to contamination of soft cheese. ET 1 is closely related to the clone (ET7) that caused two large outbreaks of listeriosis in Massachusetts in 1979 and 1983.

Full text

PDF
3822

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Beltran P., Musser J. M., Helmuth R., Farmer J. J., 3rd, Frerichs W. M., Wachsmuth I. K., Ferris K., McWhorter A. C., Wells J. G., Cravioto A. Toward a population genetic analysis of Salmonella: genetic diversity and relationships among strains of serotypes S. choleraesuis, S. derby, S. dublin, S. enteritidis, S. heidelberg, S. infantis, S. newport, and S. typhimurium. Proc Natl Acad Sci U S A. 1988 Oct;85(20):7753–7757. doi: 10.1073/pnas.85.20.7753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Caugant D. A., Frøholm L. O., Bøvre K., Holten E., Frasch C. E., Mocca L. F., Zollinger W. D., Selander R. K. Intercontinental spread of a genetically distinctive complex of clones of Neisseria meningitidis causing epidemic disease. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4927–4931. doi: 10.1073/pnas.83.13.4927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Donker-Voet J. Proceedings: Listeria monocytogenes: some biochemical and serological aspects. Acta Microbiol Acad Sci Hung. 1972;19(4):287–291. [PubMed] [Google Scholar]
  4. Fleming D. W., Cochi S. L., MacDonald K. L., Brondum J., Hayes P. S., Plikaytis B. D., Holmes M. B., Audurier A., Broome C. V., Reingold A. L. Pasteurized milk as a vehicle of infection in an outbreak of listeriosis. N Engl J Med. 1985 Feb 14;312(7):404–407. doi: 10.1056/NEJM198502143120704. [DOI] [PubMed] [Google Scholar]
  5. Gaillard J. L., Berche P., Sansonetti P. Transposon mutagenesis as a tool to study the role of hemolysin in the virulence of Listeria monocytogenes. Infect Immun. 1986 Apr;52(1):50–55. doi: 10.1128/iai.52.1.50-55.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gray M. L., Killinger A. H. Listeria monocytogenes and listeric infections. Bacteriol Rev. 1966 Jun;30(2):309–382. doi: 10.1128/br.30.2.309-382.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ho J. L., Shands K. N., Friedland G., Eckind P., Fraser D. W. An outbreak of type 4b Listeria monocytogenes infection involving patients from eight Boston hospitals. Arch Intern Med. 1986 Mar;146(3):520–524. [PubMed] [Google Scholar]
  8. Kathariou S., Metz P., Hof H., Goebel W. Tn916-induced mutations in the hemolysin determinant affecting virulence of Listeria monocytogenes. J Bacteriol. 1987 Mar;169(3):1291–1297. doi: 10.1128/jb.169.3.1291-1297.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kathariou S., Rocourt J., Hof H., Goebel W. Levels of Listeria monocytogenes hemolysin are not directly proportional to virulence in experimental infections of mice. Infect Immun. 1988 Feb;56(2):534–536. doi: 10.1128/iai.56.2.534-536.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kuhn M., Goebel W. Identification of an extracellular protein of Listeria monocytogenes possibly involved in intracellular uptake by mammalian cells. Infect Immun. 1989 Jan;57(1):55–61. doi: 10.1128/iai.57.1.55-61.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kuhn M., Kathariou S., Goebel W. Hemolysin supports survival but not entry of the intracellular bacterium Listeria monocytogenes. Infect Immun. 1988 Jan;56(1):79–82. doi: 10.1128/iai.56.1.79-82.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Linnan M. J., Mascola L., Lou X. D., Goulet V., May S., Salminen C., Hird D. W., Yonekura M. L., Hayes P., Weaver R. Epidemic listeriosis associated with Mexican-style cheese. N Engl J Med. 1988 Sep 29;319(13):823–828. doi: 10.1056/NEJM198809293191303. [DOI] [PubMed] [Google Scholar]
  13. Malinverni R., Bille J., Perret C., Regli F., Tanner F., Glauser M. P. Listériose épidémique. Observation de 25 cas en 15 mois au Centre hospitalier universitaire vaudois. Schweiz Med Wochenschr. 1985 Jan 5;115(1):2–10. [PubMed] [Google Scholar]
  14. McLauchlin J., Audurier A., Taylor A. G. Aspects of the epidemiology of human Listeria monocytogenes infections in Britain 1967-1984; the use of serotyping and phage typing. J Med Microbiol. 1986 Dec;22(4):367–377. doi: 10.1099/00222615-22-4-367. [DOI] [PubMed] [Google Scholar]
  15. McLauchlin J., Audurier A., Taylor A. G. The evaluation of a phage-typing system for Listeria monocytogenes for use in epidemiological studies. J Med Microbiol. 1986 Dec;22(4):357–365. doi: 10.1099/00222615-22-4-357. [DOI] [PubMed] [Google Scholar]
  16. McLauchlin J. Listeria monocytogenes, recent advances in the taxonomy and epidemiology of listeriosis in humans. J Appl Bacteriol. 1987 Jul;63(1):1–11. doi: 10.1111/j.1365-2672.1987.tb02411.x. [DOI] [PubMed] [Google Scholar]
  17. Musser J. M., Bemis D. A., Ishikawa H., Selander R. K. Clonal diversity and host distribution in Bordetella bronchiseptica. J Bacteriol. 1987 Jun;169(6):2793–2803. doi: 10.1128/jb.169.6.2793-2803.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Musser J. M., Hewlett E. L., Peppler M. S., Selander R. K. Genetic diversity and relationships in populations of Bordetella spp. J Bacteriol. 1986 Apr;166(1):230–237. doi: 10.1128/jb.166.1.230-237.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Musser J. M., Kroll J. S., Moxon E. R., Selander R. K. Evolutionary genetics of the encapsulated strains of Haemophilus influenzae. Proc Natl Acad Sci U S A. 1988 Oct;85(20):7758–7762. doi: 10.1073/pnas.85.20.7758. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Musser J. M., Rapp V. J., Selander R. K. Clonal diversity in Haemophilus pleuropneumoniae. Infect Immun. 1987 May;55(5):1207–1215. doi: 10.1128/iai.55.5.1207-1215.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nei M. F-statistics and analysis of gene diversity in subdivided populations. Ann Hum Genet. 1977 Oct;41(2):225–233. doi: 10.1111/j.1469-1809.1977.tb01918.x. [DOI] [PubMed] [Google Scholar]
  22. Ochman H., Whittam T. S., Caugant D. A., Selander R. K. Enzyme polymorphism and genetic population structure in Escherichia coli and Shigella. J Gen Microbiol. 1983 Sep;129(9):2715–2726. doi: 10.1099/00221287-129-9-2715. [DOI] [PubMed] [Google Scholar]
  23. Olyhoek T., Crowe B. A., Achtman M. Clonal population structure of Neisseria meningitidis serogroup A isolated from epidemics and pandemics between 1915 and 1983. Rev Infect Dis. 1987 Jul-Aug;9(4):665–692. doi: 10.1093/clinids/9.4.665. [DOI] [PubMed] [Google Scholar]
  24. Portnoy D. A., Jacks P. S., Hinrichs D. J. Role of hemolysin for the intracellular growth of Listeria monocytogenes. J Exp Med. 1988 Apr 1;167(4):1459–1471. doi: 10.1084/jem.167.4.1459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Rocourt J., Audurier A., Courtieu A. L., Durst J., Ortel S., Schrettenbrunner A., Taylor A. G. A multi-centre study on the phage typing of Listeria monocytogenes. Zentralbl Bakteriol Mikrobiol Hyg A. 1985 Jul;259(4):489–497. doi: 10.1016/s0176-6724(85)80081-x. [DOI] [PubMed] [Google Scholar]
  26. Rocourt J., Seeliger H. P. Distribution des espèces du genre Listeria. Zentralbl Bakteriol Mikrobiol Hyg A. 1985 May;259(3):317–330. [PubMed] [Google Scholar]
  27. Schill W. B., Phelps S. R., Pyle S. W. Multilocus Electrophoretic Assessment of the Genetic Structure and Diversity of Yersinia ruckeri. Appl Environ Microbiol. 1984 Nov;48(5):975–979. doi: 10.1128/aem.48.5.975-979.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Schlech W. F., 3rd, Lavigne P. M., Bortolussi R. A., Allen A. C., Haldane E. V., Wort A. J., Hightower A. W., Johnson S. E., King S. H., Nicholls E. S. Epidemic listeriosis--evidence for transmission by food. N Engl J Med. 1983 Jan 27;308(4):203–206. doi: 10.1056/NEJM198301273080407. [DOI] [PubMed] [Google Scholar]
  29. Seeliger H. P. Modern taxonomy of the Listeria group relationship to its pathogenicity. Clin Invest Med. 1984;7(4):217–221. [PubMed] [Google Scholar]
  30. Selander R. K., Caugant D. A., Ochman H., Musser J. M., Gilmour M. N., Whittam T. S. Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl Environ Microbiol. 1986 May;51(5):873–884. doi: 10.1128/aem.51.5.873-884.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Selander R. K., Korhonen T. K., Väisänen-Rhen V., Williams P. H., Pattison P. E., Caugant D. A. Genetic relationships and clonal structure of strains of Escherichia coli causing neonatal septicemia and meningitis. Infect Immun. 1986 Apr;52(1):213–222. doi: 10.1128/iai.52.1.213-222.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Selander R. K., McKinney R. M., Whittam T. S., Bibb W. F., Brenner D. J., Nolte F. S., Pattison P. E. Genetic structure of populations of Legionella pneumophila. J Bacteriol. 1985 Sep;163(3):1021–1037. doi: 10.1128/jb.163.3.1021-1037.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Selander R. K., Musser J. M., Caugant D. A., Gilmour M. N., Whittam T. S. Population genetics of pathogenic bacteria. Microb Pathog. 1987 Jul;3(1):1–7. doi: 10.1016/0882-4010(87)90032-5. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES