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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1999 Apr 29;354(1384):701–710. doi: 10.1098/rstb.1999.0423

Bacterial population genetics, evolution and epidemiology.

B G Spratt 1, M C Maiden 1
PMCID: PMC1692550  PMID: 10365396

Abstract

Asexual bacterial populations inevitably consist of an assemblage of distinct clonal lineages. However, bacterial populations are not entirely asexual since recombinational exchanges occur, mobilizing small genome segments among lineages and species. The relative contribution of recombination, as opposed to de novo mutation, in the generation of new bacterial genotypes varies among bacterial populations and, as this contribution increases, the clonality of a given population decreases. In consequence, a spectrum of possible population structures exists, with few bacterial species occupying the extremes of highly clonal and completely non-clonal, most containing both clonal and non-clonal elements. The analysis of collections of bacterial isolates, which accurately represent the natural population, by nucleotide sequence determination of multiple housekeeping loci provides data that can be used both to investigate the population structure of bacterial pathogens and for the molecular characterization of bacterial isolates. Understanding the population structure of a given pathogen is important since it impacts on the questions that can be addressed by, and the methods and samples required for, effective molecular epidemiological studies.

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Selected References

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  1. ATWOOD K. C., SCHNEIDER L. K., RYAN F. J. Periodic selection in Escherichia coli. Proc Natl Acad Sci U S A. 1951 Mar;37(3):146–155. doi: 10.1073/pnas.37.3.146. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Achtman M. Microevolution and epidemic spread of serogroup A Neisseria meningitidis--a review. Gene. 1997 Jun 11;192(1):135–140. doi: 10.1016/s0378-1119(97)00083-8. [DOI] [PubMed] [Google Scholar]
  3. Altwegg M., Hickman-Brenner F. W., Farmer J. J., 3rd Ribosomal RNA gene restriction patterns provide increased sensitivity for typing Salmonella typhi strains. J Infect Dis. 1989 Jul;160(1):145–149. doi: 10.1093/infdis/160.1.145. [DOI] [PubMed] [Google Scholar]
  4. Bandelt H. J., Dress A. W. Split decomposition: a new and useful approach to phylogenetic analysis of distance data. Mol Phylogenet Evol. 1992 Sep;1(3):242–252. doi: 10.1016/1055-7903(92)90021-8. [DOI] [PubMed] [Google Scholar]
  5. Bowler L. D., Zhang Q. Y., Riou J. Y., Spratt B. G. Interspecies recombination between the penA genes of Neisseria meningitidis and commensal Neisseria species during the emergence of penicillin resistance in N. meningitidis: natural events and laboratory simulation. J Bacteriol. 1994 Jan;176(2):333–337. doi: 10.1128/jb.176.2.333-337.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Boyd E. F., Nelson K., Wang F. S., Whittam T. S., Selander R. K. Molecular genetic basis of allelic polymorphism in malate dehydrogenase (mdh) in natural populations of Escherichia coli and Salmonella enterica. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1280–1284. doi: 10.1073/pnas.91.4.1280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Boyd E. F., Wang F. S., Whittam T. S., Selander R. K. Molecular genetic relationships of the salmonellae. Appl Environ Microbiol. 1996 Mar;62(3):804–808. doi: 10.1128/aem.62.3.804-808.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brown A. H., Feldman M. W., Nevo E. Multilocus Structure of Natural Populations of HORDEUM SPONTANEUM. Genetics. 1980 Oct;96(2):523–536. doi: 10.1093/genetics/96.2.523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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 Neisseria meningitidis clones of the ET-5 complex. Antonie Van Leeuwenhoek. 1987;53(6):389–394. doi: 10.1007/BF00415492. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Caugant D. A., Mocca L. F., Frasch C. E., Frøholm L. O., Zollinger W. D., Selander R. K. Genetic structure of Neisseria meningitidis populations in relation to serogroup, serotype, and outer membrane protein pattern. J Bacteriol. 1987 Jun;169(6):2781–2792. doi: 10.1128/jb.169.6.2781-2792.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Enright M. C., Spratt B. G. A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease. Microbiology. 1998 Nov;144(Pt 11):3049–3060. doi: 10.1099/00221287-144-11-3049. [DOI] [PubMed] [Google Scholar]
  13. Feil E., Zhou J., Maynard Smith J., Spratt B. G. A comparison of the nucleotide sequences of the adk and recA genes of pathogenic and commensal Neisseria species: evidence for extensive interspecies recombination within adk. J Mol Evol. 1996 Dec;43(6):631–640. doi: 10.1007/BF02202111. [DOI] [PubMed] [Google Scholar]
  14. Go M. F., Kapur V., Graham D. Y., Musser J. M. Population genetic analysis of Helicobacter pylori by multilocus enzyme electrophoresis: extensive allelic diversity and recombinational population structure. J Bacteriol. 1996 Jul;178(13):3934–3938. doi: 10.1128/jb.178.13.3934-3938.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gutjahr T. S., O'Rourke M., Ison C. A., Spratt B. G. Arginine-, hypoxanthine-, uracil-requiring isolates of Neisseria gonorrhoeae are a clonal lineage with a non-clonal population. Microbiology. 1997 Feb;143(Pt 2):633–640. doi: 10.1099/00221287-143-2-633. [DOI] [PubMed] [Google Scholar]
  16. Guttman D. S., Dykhuizen D. E. Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science. 1994 Nov 25;266(5189):1380–1383. doi: 10.1126/science.7973728. [DOI] [PubMed] [Google Scholar]
  17. Kohl P. K., Knapp J. S., Hofmann H., Gruender K., Petzoldt D., Tams M. R., Holmes K. K. Epidemiological analysis of Neisseria gonorrhoeae in the Federal Republic of Germany by auxotyping and serological classification using monoclonal antibodies. Genitourin Med. 1986 Jun;62(3):145–150. doi: 10.1136/sti.62.3.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Lorenz M. G., Wackernagel W. Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev. 1994 Sep;58(3):563–602. doi: 10.1128/mr.58.3.563-602.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Maiden M. C., Bygraves J. A., Feil E., Morelli G., Russell J. E., Urwin R., Zhang Q., Zhou J., Zurth K., Caugant D. A. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3140–3145. doi: 10.1073/pnas.95.6.3140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Maiden M. C. Horizontal genetic exchange, evolution, and spread of antibiotic resistance in bacteria. Clin Infect Dis. 1998 Aug;27 (Suppl 1):S12–S20. doi: 10.1086/514917. [DOI] [PubMed] [Google Scholar]
  21. Maynard Smith J., Smith N. H. Detecting recombination from gene trees. Mol Biol Evol. 1998 May;15(5):590–599. doi: 10.1093/oxfordjournals.molbev.a025960. [DOI] [PubMed] [Google Scholar]
  22. Morelli G., Malorny B., Müller K., Seiler A., Wang J. F., del Valle J., Achtman M. Clonal descent and microevolution of Neisseria meningitidis during 30 years of epidemic spread. Mol Microbiol. 1997 Sep;25(6):1047–1064. doi: 10.1046/j.1365-2958.1997.5211882.x. [DOI] [PubMed] [Google Scholar]
  23. Musser J. M. Molecular population genetic analysis of emerged bacterial pathogens: selected insights. Emerg Infect Dis. 1996 Jan-Mar;2(1):1–17. doi: 10.3201/eid0201.960101. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Navarro F., Llovet T., Echeita M. A., Coll P., Aladueña A., Usera M. A., Prats G. Molecular typing of Salmonella enterica serovar typhi. J Clin Microbiol. 1996 Nov;34(11):2831–2834. doi: 10.1128/jcm.34.11.2831-2834.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nelson K., Selander R. K. Evolutionary genetics of the proline permease gene (putP) and the control region of the proline utilization operon in populations of Salmonella and Escherichia coli. J Bacteriol. 1992 Nov;174(21):6886–6895. doi: 10.1128/jb.174.21.6886-6895.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nelson K., Whittam T. S., Selander R. K. Nucleotide polymorphism and evolution in the glyceraldehyde-3-phosphate dehydrogenase gene (gapA) in natural populations of Salmonella and Escherichia coli. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6667–6671. doi: 10.1073/pnas.88.15.6667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. O'Rourke M., Ison C. A., Renton A. M., Spratt B. G. Opa-typing: a high-resolution tool for studying the epidemiology of gonorrhoea. Mol Microbiol. 1995 Sep;17(5):865–875. doi: 10.1111/j.1365-2958.1995.mmi_17050865.x. [DOI] [PubMed] [Google Scholar]
  28. Reeves P. R. Variation in O-antigens, niche-specific selection and bacterial populations. FEMS Microbiol Lett. 1992 Dec 15;100(1-3):509–516. doi: 10.1111/j.1574-6968.1992.tb14085.x. [DOI] [PubMed] [Google Scholar]
  29. Salaün L., Audibert C., Le Lay G., Burucoa C., Fauchère J. L., Picard B. Panmictic structure of Helicobacter pylori demonstrated by the comparative study of six genetic markers. FEMS Microbiol Lett. 1998 Apr 15;161(2):231–239. doi: 10.1111/j.1574-6968.1998.tb12953.x. [DOI] [PubMed] [Google Scholar]
  30. Sawyer S. Statistical tests for detecting gene conversion. Mol Biol Evol. 1989 Sep;6(5):526–538. doi: 10.1093/oxfordjournals.molbev.a040567. [DOI] [PubMed] [Google Scholar]
  31. Selander R. K., Beltran P., Smith N. H., Barker R. M., Crichton P. B., Old D. C., Musser J. M., Whittam T. S. Genetic population structure, clonal phylogeny, and pathogenicity of Salmonella paratyphi B. Infect Immun. 1990 Jun;58(6):1891–1901. doi: 10.1128/iai.58.6.1891-1901.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Selander R. K., Beltran P., Smith N. H., Helmuth R., Rubin F. A., Kopecko D. J., Ferris K., Tall B. D., Cravioto A., Musser J. M. Evolutionary genetic relationships of clones of Salmonella serovars that cause human typhoid and other enteric fevers. Infect Immun. 1990 Jul;58(7):2262–2275. doi: 10.1128/iai.58.7.2262-2275.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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]
  34. Shortridge V. D., Stone G. G., Flamm R. K., Beyer J., Versalovic J., Graham D. W., Tanaka S. K. Molecular typing of Helicobacter pylori isolates from a multicenter U.S. clinical trial by ureC restriction fragment length polymorphism. J Clin Microbiol. 1997 Feb;35(2):471–473. doi: 10.1128/jcm.35.2.471-473.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Smith J. M., Dowson C. G., Spratt B. G. Localized sex in bacteria. Nature. 1991 Jan 3;349(6304):29–31. doi: 10.1038/349029a0. [DOI] [PubMed] [Google Scholar]
  36. Smith J. M., Smith N. H., O'Rourke M., Spratt B. G. How clonal are bacteria? Proc Natl Acad Sci U S A. 1993 May 15;90(10):4384–4388. doi: 10.1073/pnas.90.10.4384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sved J. A. The stability of linked systems of loci with a small population size. Genetics. 1968 Aug;59(4):543–563. doi: 10.1093/genetics/59.4.543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Vázquez J. A., Berrón S., O'Rourke M., Carpenter G., Feil E., Smith N. H., Spratt B. G. Interspecies recombination in nature: a meningococcus that has acquired a gonococcal PIB porin. Mol Microbiol. 1995 Mar;15(6):1001–1007. doi: 10.1111/j.1365-2958.1995.tb02275.x. [DOI] [PubMed] [Google Scholar]
  39. Whittam T. S., Ochman H., Selander R. K. Multilocus genetic structure in natural populations of Escherichia coli. Proc Natl Acad Sci U S A. 1983 Mar;80(6):1751–1755. doi: 10.1073/pnas.80.6.1751. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Zhou J., Bowler L. D., Spratt B. G. Interspecies recombination, and phylogenetic distortions, within the glutamine synthetase and shikimate dehydrogenase genes of Neisseria meningitidis and commensal Neisseria species. Mol Microbiol. 1997 Feb;23(4):799–812. doi: 10.1046/j.1365-2958.1997.2681633.x. [DOI] [PubMed] [Google Scholar]

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