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Volume 129, Issue 9

Enzyme Polymorphism and Genetic Population Structure in and Free

Abstract

Electrophoretically demonstrable variation in 12 enzymes was studied in more than 1600 isolates of from human and animal sources and in 123 strains of the four species of . All 12 enzymes were polymorphic; and the number of allozymes (mobility variants), which were equated with alleles, averaged 9·3 per locus in . For species, the mean number of alleles was 2·9 per locus. Some 77% of the allozymes recorded in were shared with . A total of 302 unique genotypic combinations of alleles over the 12 loci (electrophoretic types, ETs) was distinguished, of which 279 represented and 23 were . Among electrophoretic types, mean allelic diversity per locus was 0·52 for and 0·29 for . It was estimated that there are, on the average, about 0·3 detectable codon differences per locus between pairs of strains of and , which is roughly equivalent to 1·2 amino acid differences per enzyme. Evidence that the enzyme loci studied are a random sample of the genome is provided by a significant positive correlation between estimates of genetic divergence between pairs of strains obtained by DNA reassociation tests and estimates of genetic distance between the same strains based on electrophoresis.

A principal components analysis of allozyme profiles revealed that the 302 ETs fall into three overlapping clusters, reflecting strong non-random associations of alleles, largely at four loci. Each of the four ETs of that have been most frequently recovered from natural populations has an allozyme profile that is very similar to, or identical with, the hypothetical modal ET of one of the groups. ETs of fall into two of the groups. No biological significance can at present be attributed to the genetic structure revealed by multilocus electrophoretic techniques. The electrophoretic data are fully compatible with other molecular and more conventional evidence of a close affinity between and , and they raise questions regarding the present assignments of certain strains to species. In support of evidence from DNA reassociation tests and serotyping, the present study suggests that is homogeneous in chromosomal genotype.

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© Society for General Microbiology 1983
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1983-09-01
2024-05-04
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References

  1. Achtman M., Mercer A., Kusecek B., Pohl A., Heuzenroeder H., Aaronson W., Sutton A., Silver R.P. 1983; Six widespread bacterial clones among Escherichia coli K1 isolates. Infection and Immunity 39:315–335
     [Google Scholar]
  2. Anilionis A., Riley M. 1980; Conservation and variation of nucleotide sequences within bacterial genomes: Escherichia coli strains. Journal of Bacteriology 143:355–365
     [Google Scholar]
  3. Ayala F.J. (Editor) 1976 Molecular Evolution. Sunderland, Massachusetts: Sinauer Associates.;
     [Google Scholar]
  4. Ayala F.J. 1982; Genetic variation in natural populations: problems of electrophoretically cryptic alleles. Proceedings of the National Academy of Sciences of the United States of America 79:550–554
     [Google Scholar]
  5. Bachmann B.J. 1972; Pedigrees of some mutant strains of Escherichia coli K-12. Bacteriological Reviews 36:525–557
     [Google Scholar]
  6. Bachmann B.J., Low K.B. 1980; Linkage map of Escherichia coli K-12, Edition 6. Microbiological Reviews 44:1–56
     [Google Scholar]
  7. Baptist J.N., Shaw C.R., Mandel M. 1969; Zone electrophoresis of enzymes in bacterial taxonomy. Journal of Bacteriology 99:180–188
     [Google Scholar]
  8. Baptist J.N., Thomas D., Butler M.A., Matney T.S. 1975; Genetic studies of bacterial isozymes. In Isozymes, IV. Genetics and Evolution pp. 371–379 Markert C.L. Edited by New York: Academic Press;
     [Google Scholar]
  9. Bergstrom S., Olsson O., Normark S. 1982; Common evolutionary origin of chromosomal beta-lactamase genes in enterobacteria. Journal of Bacteriology 150:528–534
     [Google Scholar]
  10. Bettelheim K.A. 1978; The source of ‘OH’ serotypes of Escherichia coli. Journal of Hygiene 80:83–113
     [Google Scholar]
  11. Bonhomme F., Selander R.K. 1978; The extent of allelic diversity underlying electrophoretic protein variation in the house mouse. In Origins of Inbred Mice pp. 569–589 Morse H.C.III Edited by New York: Academic Press;
     [Google Scholar]
  12. Bowman J.E., Brubaker R.R., Frischer H., Carson P.E. 1967; Characterization of enterobacteria by starch-gel electrophoresis of glucose-6-phosphate dehydrogenase and phosphogluconate dehydrogenase. Journal of Bacteriology 94:544–551
     [Google Scholar]
  13. Braun G., Cole S.T. 1982; The nucleotide sequence for major outer membrane protein OmpA of Shigella dysenteriae. Nucleic Acids Research 10:2367–2378
     [Google Scholar]
  14. Brenner D.J. 1981; Introduction to the family Enterobacteriaceae. In The Prokaryotes II pp. 1105–1127 Starr M.P., Stolp H.G., Truper A., Balows J.N., Schlegel H.G. Edited by Berlin: Springer-Verlag;
     [Google Scholar]
  15. Brenner D.J., Falkow S. 1971; Molecular relationships among members of the Enterobacteriaceae. Advances in Genetics 16:81–118
     [Google Scholar]
  16. Brenner D.J., Fanning G.R., Johnson K.E., Citarella R.V., Falkow S. 1969; Polynucleotide sequence relationships among members of Enterobacteriaceae. Journal of Bacteriology 98:637–650
     [Google Scholar]
  17. Brenner D.J., Fanning G.R., Skerman F.J., Falkow S. 1972a; Polynucleotide sequence divergence among strains of Escherichia coli and closely related organisms. Journal of Bacteriology 109:953–965
     [Google Scholar]
  18. Brenner D.J., Fanning G.R., Steigerwalt A.G., ØRSKOV I., ØRSKOV F. 1972b; Polynucleotide sequence relatedness among three groups of pathogenic Escherichia coli strains. Infection and Immunity 6:308–315
     [Google Scholar]
  19. Brenner D.J., Fanning G.R., Miklos G.V., Steigerwalt A.G. 1973; Polynucleotide sequence relatedness among Shigella species. International Journal of Systematic Bacteriology 23:1–7
     [Google Scholar]
  20. Brenner D.J., Fanning G.R., Steigerwalt A.G., Sodd M.A., Doctor B.P. 1977; Conservation of transfer ribonucleic acid and 5S ribonucleic acid cistrons in Enterobacteriaceae. Journal of Bacteriology 129:1435–1439
     [Google Scholar]
  21. Brown A.H.D., Feldman M.W., Nevo E. 1980; Multilocus structure of natural populations of Hor-deum spontaneum. Genetics 96:523–536
     [Google Scholar]
  22. Caugant D.A., Levin B.R., Selander R.K. 1981; Genetic diversity and temporal variation in the E. coli population of a human host. Genetics 98:467–490
     [Google Scholar]
  23. Caugant D.A., Levin B.R., Lidin-JANSON G., Whittam T.S., SvanborgedéN C., Selander R.K. 1983; Genetic diversity and relationships among strains of E. coli in the intestine and those causing urinary tract infections. In Host Parasite Relationships in Gram-negative Infections (Progress in Allergy) 33 pp. 203–227 Hanson L. A., Kallos P., Westphal O. Edited by Basel: Karger;
     [Google Scholar]
  24. Colwell R.R., Johnson R., Wan L., Lovelace T.E., Brenner D.J. 1974; Numerical taxonomy and deoxyribonucleic acid reassociation in the taxonomy of some gram-negative fermentive bacteria. International Journal of Systematic Bacteriology 24:422–433
     [Google Scholar]
  25. Crichton P.B., Old D.C. 1979; Biotyping of Escherichia coli. Journal of Medical Microbiology 12:473–486
     [Google Scholar]
  26. Crichton P.B., Old D.C. 1982; A biotyping scheme for the subspecific discrimination of Escherichia coli. Journal of Medical Microbiology 15:233–242
     [Google Scholar]
  27. Dodd C.E.R., Jones D. 1982; A numerical taxonomic study of the genus Shigella. Journal of General Microbiology 128:1933–1957
     [Google Scholar]
  28. Edwards P.R., Ewing W.H. 1972 Identification of Enterobacteriaceae. Minneapolis: Burgess Publish-ing Co.;
     [Google Scholar]
  29. Elek S.D., Davies J.R., Miles R. 1973; Resistotyping of Shigella sonnei. Journal of Medical Microbiology 6:329–345
     [Google Scholar]
  30. Elwell L.P., Shipley P.L. 1980; Plasmid-mediated factors associated with virulence of bacteria to animals. Annual Review of Microbiology 34:465–496
     [Google Scholar]
  31. Eveland W.C., Oliver W.J., Neel J.V. 1971; Characteristics of Escherichia coli serotypes in the Yanomama, a primitive Indian tribe of South America. Infection and Immunity 4:753–756
     [Google Scholar]
  32. Gillies R.R. 1978; Bacteriocin typing of Enterobacteriaceae. Methods in Microbiology 11:79–86
     [Google Scholar]
  33. Goullet P. 1973; An esterase zymogram of Escherichia coli. Journal of General Microbiology 77:27–35
     [Google Scholar]
  34. Goullet P. 1980; Esterase electrophoretic pattern relatedness between Shigella species and Escherichia coli. Journal of General Microbiology 117:493–500
     [Google Scholar]
  35. Harris H., Hopkinson D.A., Edwards Y.H. 1977; Polymorphism and the subunit structure of enzymes: a contribution to the neutralist-selectionist controversy. Proceedings of the National Academy of Sciences of the United States of America 74:698–701
     [Google Scholar]
  36. Harshman L., Riley M. 1980; Conservation and variation of nucleotide sequences in Escherichia colistrains isolated from nature. Journal of Bacteriology 144:560–568
     [Google Scholar]
  37. Helgason S., Old D.C. 1981; Comparison of four methods of differential typing of isolates of Shigella sonnei. Journal of Hygiene 87:339–355
     [Google Scholar]
  38. Hori H., Osawa S. 1978; Evolution of ribosomal proteins in Enterobacteriaceae. Journal of Bacteriology 133:1089–1095
     [Google Scholar]
  39. Hori H., Osawa S. 1979; Evolutionary change in 5S RNA secondary structure and a phylogenetic tree of 54 5S RNA species. Proceedings of the National Academy of Sciences of the United States of America 76:381–385
     [Google Scholar]
  40. Jacquard A. 1974 The Genetic Structure of Populations. New York: Springer-Verlag;
     [Google Scholar]
  41. Jamieson A.F., Bremner D.A., Bergquist P.L., Lane H.E.D. 1979; Characterization of plasmids from antibiotic-resistant Shigella isolates by agarose gel electrophoresis. Journal of General Microbiology 113:73–81
     [Google Scholar]
  42. Jann K., Jann B., Schmidt G. 1981; SDS polyacrylamide gel electrophoresis and serological analysis of pili from Escherichia coli of different pathogenic origin. FEMS Microbiology Letters 11:21–25
     [Google Scholar]
  43. Johnson R., Colwell R.R., Sakazaki R., Tamura K. 1975; Numerical taxonomy study of the Enterobacteriaceae. International Journal of Systematic Bacteriology 25:12–37
     [Google Scholar]
  44. Koch A.L. 1974; The pertinence of the periodic selection phenomenon to prokaryote evolution. Genetics 77:127–142
     [Google Scholar]
  45. Koch A.L. 1981; Evolution of antibiotic resistance gene function. Microbiological Reviews 45:355–378
     [Google Scholar]
  46. Kopecko D.J., Washington O., Formal S.B. 1980; Genetic and physical evidence for plasmid control of Shigella sonnei form I cell surface antigen. Infection and Immunity 29:207–214
     [Google Scholar]
  47. Krieg R.E., Lockhart W.R. 1966; Classification of enterobacteria based on overall similarity. Journal of Bacteriology 92:1275–1280
     [Google Scholar]
  48. Kubitschek H.E. 1974; Operation of selection pressure on microbial populations. Symposia of the Society for General Microbiology 24:105–130
     [Google Scholar]
  49. Lewontin R.C. 1974 The Genetic Basis of Evolutionary Change. New York: Columbia University Press;
     [Google Scholar]
  50. Lewontin R.C., Hubby J.L. 1966; A molecular approach to the study of genic heterozygosity in natural populations. II. Amount of variation and degree of heterozygosity in natural populations of Drosophila pseudoobscura. Genetics 54:595–609
     [Google Scholar]
  51. Li S.-L., Hoch S.O. 1974; Amino-terminal sequence of the tryptophan synthetase a chain of Bacillus subtilis. Journal of Bacteriology 118:187–191
     [Google Scholar]
  52. Maynard SMITH J., Haigh J. 1974; The hitchhiking effect of a favourable gene. Genetical Research 23:23–35
     [Google Scholar]
  53. Milch H. 1978; Phage typing of Escherichia coli. Methods in Microbiology II:87–155
     [Google Scholar]
  54. Milkman R. 1973; Electrophoretic variation in Escherichia coli from natural sources. Science 182:1024–1026
     [Google Scholar]
  55. Milkman R. 1975; Allozyme variation in E. coliof diverse natural origins. In Isozymes, IV. Genetics and Evolution pp. 273–285 Markert C.L. Edited by New York: Academic Press;
     [Google Scholar]
  56. Milkman R., Crawford I.P. 1983; Clustered third-base substitutions among wild strains of Escherichia coli. Science (in the Press).
    [Google Scholar]
  57. Nei M. 1975 Molecular Population Genetics and Evolution. New York: Elsevier;
     [Google Scholar]
  58. Nichols B.P., Miozzari G.F., Van CLEEMPUT M., Bennett G.N., Yanofsky C. 1980; Nucleotide sequences of the trpG region of Escherichia coli, Shigella dysenteriae, Salmonella typhimurium and Serratia marcescens. Journal of Molecular Biology 142:503–517
     [Google Scholar]
  59. Nyman K., Nakamura K., Ohtsubo H., Ohtsubo E. 1981; Distribution of the insertion element IS7 in gram-negative bacteria. Nature 289:609–612
     [Google Scholar]
  60. Ohta T. 1982; Linkage disequilibrium with the island model. Genetics 101:139–155
     [Google Scholar]
  61. Old D.C., Crichton P.B., Maunder A.J., Wilson M.I. 1980; Discrimination of urinary strains of Escherichia coli by five typing methods. Journal of Medical Microbiology 13:437–444
     [Google Scholar]
  62. Old D.C., Helgason S., Scott A.C. 1981; Discrimination by multiple typing of isolates of Shigella sonnei in Dundee (1971-6). Journal of Hygiene 37:357–368
     [Google Scholar]
  63. ØRSKOV F., ØRSKOV I., Evans D.J.JR Sack B.B., Sack D.A., Wadstrom T. 1976; Special Escherichia coli serotypes among enterotoxigenic strains from diarrhoea in adults and children. Medical Microbiology and Immunology 162:73–80
     [Google Scholar]
  64. ØRSKOV I., ØRSKOV F., Jann B., Jann K. 1977; Serology, chemistry, and genetics of O and K antigens of Escherichia coli. Bacteriological Reviews 41:667–710
     [Google Scholar]
  65. Petrovskaya V.G., Bondarenko V.M. 1977; Recommended corrections to the classification of Shigella fiexneri on a genetic basis. International Journal of Systematic Bacteriology 27:171–175
     [Google Scholar]
  66. Petrovskaya V.G., Khomenko N.A. 1979; Proposals for improving the classification of members of the genus Shigella. International Journal of Systematic Bacteriology 29:400–402
     [Google Scholar]
  67. Ramshaw J.A.M., Coyne J.A., Lewontin R.C. 1979; The sensitivity of gel electrophoresis as an indicator of genetic variation. Genetics 93:1019–1037
     [Google Scholar]
  68. Rowe B., Gross R.J., Guiney M. 1976; Antigenic relationships between Escherichia coli O antigens 0149 to 0163 and Shigella O antigens. International Journal of Systematic Bacteriology 26:76–78
     [Google Scholar]
  69. Sakazaki R., Tamura K., Johnson R., Colwell R.R. 1976; Taxonomy of some recently described species in the family Enterobacteriaceae. International Journal of Systematic Bacteriology 26:158–179
     [Google Scholar]
  70. Sanderson K.E. 1976; Genetic relatedness in the family Enterobacteriaceae. Annual Review of Microbiology 30:327–349
     [Google Scholar]
  71. Sansonetti P.J., Kopecko D.J., Formal S.B. 1981; Shigella sonnei plasmids: evidence that a large plasmid is necessary for virulence. Infection and Immunity 34:75–83
     [Google Scholar]
  72. Sansonetti P.J., Kopecko D.J., Formal S.B. 1982; Involvement of a plasmid in the invasive ability of Shigella flexneri. Infection and Immunity 35:852–860
     [Google Scholar]
  73. Selander R.K., Levin B.R. 1980; Genetic diversity and structure in Escherichia coli populations. Science 210:545–547
     [Google Scholar]
  74. Selander R.K., Whittam T.S. 1983; Protein polymorphism and the genetic structure of populations. In Evolution of Genes and Proteins pp. 89–114 Nei M., Koehn P., Westphal R.K. Edited by Sunderland, Massachusetts: Sinauer Associates;
     [Google Scholar]
  75. Selander R.K., Smith M.H., Yang S.Y., Johnson W.E., Gentry J.B. 1971; Biochemical polymorphism and systematics in the genus Peromyscus. I. Variation in the old-field mouse (Peromyscus polionotus). Studies in Genetics VI (University of Texas Publication no. 7103) 49–90
     [Google Scholar]
  76. Sneath P.H.A., Sokal R.R. 1973 Numerical Taxonomy. San Francisco: Freeman;
     [Google Scholar]
  77. Szturm-RUBINSTEN S. 1964; Repartition geographi-que des biotypes et lysotypes de 743 souches de S sonnei. Annales de I’lnstitut. Pasteur 106:114–122
     [Google Scholar]
  78. Thomson G. 1977; The effect of a selected locus on linked neutral loci. Genetics 85:753–788
     [Google Scholar]
  79. Whittam T.S., Ochman H., Selander R.K. 1983; Multilocus genetic structure in natural populations of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 80:1751–1755
     [Google Scholar]
  80. Williams P.H., Warner P.J. 1980; ColV plasmid-mediated, colicin V-independent iron uptake system of invasive strains of Escherichia coli. Infection and Immunity 29:411–416
     [Google Scholar]
  81. Wilson A.C., Carlson S.S., White T.J. 1977; Biochemical evolution. Annual Review of Biochemistry 46:573–639
     [Google Scholar]
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Enzyme Polymorphism and Genetic Population Structure in Escherichia coli and Shigella
Microbiology 129, 2715 (1983); https://doi.org/10.1099/00221287-129-9-2715
/content/journal/micro/10.1099/00221287-129-9-2715
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