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Proc Natl Acad Sci U S A. May 15, 1993; 90(10): 4384–4388.
PMCID: PMC46515

How clonal are bacteria?

Abstract

Data from multilocus enzyme electrophoresis of bacterial populations were analyzed using a statistical test designed to detect associations between genes at different loci. Some species (e.g., Salmonella) were found to be clonal at all levels of analysis. At the other extreme, Neisseria gonorrhoeae is panmictic, with random association between loci. Two intermediate types of population structure were also found. Neisseria meningitidis displays what we have called an "epidemic" structure. There is significant association between loci, but this arises only because of the recent, explosive, increase in particular electrophoretic types; when this effect is eliminated the population is found to be effectively panmictic. In contrast, linkage disequilibrium in a population of Rhizobium meliloti exists because the sample consisted of two genetically isolated divisions, often fixed for different alleles: within each division association between loci was almost random. The method of analysis is appropriate whenever there is doubt about the extent of genetic recombination between members of a population. To illustrate this we analyzed data on protozoan parasites and again found panmictic, epidemic, and clonal population structures.

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  • Orskov F, Orskov I. From the national institutes of health. Summary of a workshop on the clone concept in the epidemiology, taxonomy, and evolution of the enterobacteriaceae and other bacteria. J Infect Dis. 1983 Aug;148(2):346–357. [PubMed]
  • Selander RK, Levin BR. Genetic diversity and structure in Escherichia coli populations. Science. 1980 Oct 31;210(4469):545–547. [PubMed]
  • Caugant DA, Levin BR, Selander RK. Genetic diversity and temporal variation in the E. coli population of a human host. Genetics. 1981 Jul;98(3):467–490. [PMC free article] [PubMed]
  • Ochman H, Whittam TS, Caugant DA, Selander RK. Enzyme polymorphism and genetic population structure in Escherichia coli and Shigella. J Gen Microbiol. 1983 Sep;129(9):2715–2726. [PubMed]
  • Whittam TS, Ochman H, Selander RK. Multilocus genetic structure in natural populations of Escherichia coli. Proc Natl Acad Sci U S A. 1983 Mar;80(6):1751–1755. [PMC free article] [PubMed]
  • Selander RK, McKinney RM, Whittam TS, Bibb WF, Brenner DJ, Nolte FS, Pattison PE. Genetic structure of populations of Legionella pneumophila. J Bacteriol. 1985 Sep;163(3):1021–1037. [PMC free article] [PubMed]
  • Musser JM, Barenkamp SJ, Granoff DM, Selander RK. Genetic relationships of serologically nontypable and serotype b strains of Haemophilus influenzae. Infect Immun. 1986 Apr;52(1):183–191. [PMC free article] [PubMed]
  • Caugant DA, Mocca LF, Frasch CE, Frøholm LO, Zollinger WD, Selander RK. Genetic structure of Neisseria meningitidis populations in relation to serogroup, serotype, and outer membrane protein pattern. J Bacteriol. 1987 Jun;169(6):2781–2792. [PMC free article] [PubMed]
  • Musser JM, Bemis DA, Ishikawa H, Selander RK. Clonal diversity and host distribution in Bordetella bronchiseptica. J Bacteriol. 1987 Jun;169(6):2793–2803. [PMC free article] [PubMed]
  • Denny TP, Gilmour MN, Selander RK. Genetic diversity and relationships of two pathovars of Pseudomonas syringae. J Gen Microbiol. 1988 Jul;134(7):1949–1960. [PubMed]
  • Musser JM, Kroll JS, Moxon ER, Selander RK. Clonal population structure of encapsulated Haemophilus influenzae. Infect Immun. 1988 Aug;56(8):1837–1845. [PMC free article] [PubMed]
  • Pinero D, Martinez E, Selander RK. Genetic diversity and relationships among isolates of Rhizobium leguminosarum biovar phaseoli. Appl Environ Microbiol. 1988 Nov;54(11):2825–2832. [PMC free article] [PubMed]
  • Eardly BD, Materon LA, Smith NH, Johnson DA, Rumbaugh MD, Selander RK. Genetic structure of natural populations of the nitrogen-fixing bacterium Rhizobium meliloti. Appl Environ Microbiol. 1990 Jan;56(1):187–194. [PMC free article] [PubMed]
  • Smith JM, Dowson CG, Spratt BG. Localized sex in bacteria. Nature. 1991 Jan 3;349(6304):29–31. [PubMed]
  • Souza V, Nguyen TT, Hudson RR, Piñero D, Lenski RE. Hierarchical analysis of linkage disequilibrium in Rhizobium populations: evidence for sex? Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):8389–8393. [PMC free article] [PubMed]
  • Whittam TS, Ochman H, Selander RK. Geographic components of linkage disequilibrium in natural populations of Escherichia coli. Mol Biol Evol. 1983 Dec;1(1):67–83. [PubMed]
  • Milkman R, Bridges MM. Molecular evolution of the Escherichia coli chromosome. III. Clonal frames. Genetics. 1990 Nov;126(3):505–517. [PMC free article] [PubMed]
  • Nelson K, Whittam TS, Selander RK. 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. [PMC free article] [PubMed]
  • Nelson K, Selander RK. 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. [PMC free article] [PubMed]
  • Istock CA, Duncan KE, Ferguson N, Zhou X. Sexuality in a natural population of bacteria--Bacillus subtilis challenges the clonal paradigm. Mol Ecol. 1992 Aug;1(2):95–103. [PubMed]
  • Rayssiguier C, Thaler DS, Radman M. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature. 1989 Nov 23;342(6248):396–401. [PubMed]
  • Tibayrenc M, Kjellberg F, Arnaud J, Oury B, Brenière SF, Dardé ML, Ayala FJ. Are eukaryotic microorganisms clonal or sexual? A population genetics vantage. Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5129–5133. [PMC free article] [PubMed]
  • Brown AH, Feldman MW, Nevo E. Multilocus Structure of Natural Populations of HORDEUM SPONTANEUM. Genetics. 1980 Oct;96(2):523–536. [PMC free article] [PubMed]
  • Musser JM, Kroll JS, Granoff DM, Moxon ER, Brodeur BR, Campos J, Dabernat H, Frederiksen W, Hamel J, Hammond G, et al. Global genetic structure and molecular epidemiology of encapsulated Haemophilus influenzae. Rev Infect Dis. 1990 Jan-Feb;12(1):75–111. [PubMed]
  • Selander RK, Beltran P, Smith NH, Helmuth R, Rubin FA, Kopecko DJ, Ferris K, Tall BD, Cravioto A, Musser JM. Evolutionary genetic relationships of clones of Salmonella serovars that cause human typhoid and other enteric fevers. Infect Immun. 1990 Jul;58(7):2262–2275. [PMC free article] [PubMed]
  • Babiker HA, Creasey AM, Fenton B, Bayoumi RA, Arnot DE, Walliker D. Genetic diversity of Plasmodium falciparum in a village in eastern Sudan. 1. Diversity of enzymes, 2D-PAGE proteins and antigens. Trans R Soc Trop Med Hyg. 1991 Sep-Oct;85(5):572–577. [PubMed]
  • Mihok S, Otieno LH, Darji N. Population genetics of Trypanosoma brucei and the epidemiology of human sleeping sickness in the Lambwe Valley, Kenya. Parasitology. 1990 Apr;100(Pt 2):219–233. [PubMed]
  • Zhang Q, Tibayrenc M, Ayala FJ. Linkage disequilibrium in natural populations of Trypanosoma cruzi (flagellate), the agent of Chagas' disease. J Protozool. 1988 Feb;35(1):81–85. [PubMed]
  • Spratt BG. Hybrid penicillin-binding proteins in penicillin-resistant strains of Neisseria gonorrhoeae. Nature. 1988 Mar 10;332(6160):173–176. [PubMed]
  • Seifert HS, Ajioka RS, Marchal C, Sparling PF, So M. DNA transformation leads to pilin antigenic variation in Neisseria gonorrhoeae. Nature. 1988 Nov 24;336(6197):392–395. [PubMed]
  • Connell TD, Black WJ, Kawula TH, Barritt DS, Dempsey JA, Kverneland K, Jr, Stephenson A, Schepart BS, Murphy GL, Cannon JG. Recombination among protein II genes of Neisseria gonorrhoeae generates new coding sequences and increases structural variability in the protein II family. Mol Microbiol. 1988 Mar;2(2):227–236. [PubMed]
  • Feavers IM, Heath AB, Bygraves JA, Maiden MC. Role of horizontal genetic exchange in the antigenic variation of the class 1 outer membrane protein of Neisseria meningitidis. Mol Microbiol. 1992 Feb;6(4):489–495. [PubMed]
  • Halter R, Pohlner J, Meyer TF. Mosaic-like organization of IgA protease genes in Neisseria gonorrhoeae generated by horizontal genetic exchange in vivo. EMBO J. 1989 Sep;8(9):2737–2744. [PMC free article] [PubMed]
  • Spratt BG, Zhang QY, Jones DM, Hutchison A, Brannigan JA, Dowson CG. Recruitment of a penicillin-binding protein gene from Neisseria flavescens during the emergence of penicillin resistance in Neisseria meningitidis. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8988–8992. [PMC free article] [PubMed]
  • Spratt BG, Bowler LD, Zhang QY, Zhou J, Smith JM. Role of interspecies transfer of chromosomal genes in the evolution of penicillin resistance in pathogenic and commensal Neisseria species. J Mol Evol. 1992 Feb;34(2):115–125. [PubMed]
  • Kroll JS, Moxon ER. Capsulation in distantly related strains of Haemophilus influenzae type b: genetic drift and gene transfer at the capsulation locus. J Bacteriol. 1990 Mar;172(3):1374–1379. [PMC free article] [PubMed]
  • Jenni L, Marti S, Schweizer J, Betschart B, Le Page RW, Wells JM, Tait A, Paindavoine P, Pays E, Steinert M. Hybrid formation between African trypanosomes during cyclical transmission. Nature. 1986 Jul 10;322(6075):173–175. [PubMed]
  • Smith NH, Beltran P, Selander RK. Recombination of Salmonella phase 1 flagellin genes generates new serovars. J Bacteriol. 1990 May;172(5):2209–2216. [PMC free article] [PubMed]

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