Molecular genetic relationships of the salmonellae (original) (raw)

Abstract

A multilocus enzyme electrophoresis analysis of 96 strains of the salmonellae distinguished 80 electrophoretic types (ETs) and placed them in eight groups, seven of which correspond precisely to the seven taxonomic groups (I, II, IIIa, IIIb, IV, V, and VI) previously defined on the basis of biotype and genomic DNA hybridization. In addition, multilocus enzyme electrophoresis identified an eighth distinctive group (designated VII) composed of five strains that had been assigned to group IV on the basis of biotype. An analysis of variation in the combined nucleotide sequences of five housekeeping genes among 16 strains representing all eight groups yielded estimates of overall genetic relationships that are fully consistent with those indicated by DNA hybridization. However, the nucleotide sequences of seven invasion genes (inv/spa) in the strains of group VII were closely similar to those of strains of group IV. These findings are interpreted as evidence that group VII represents an old, differentiated lineage to which one or more large parts of the chromosomal genome of the group IV lineage, including the 40-kb segment on which the invasion genes are located, have been horizontally transferred. All lines of molecular genetic evidence indicate that group V is very strongly differentiated from all other groups, thus supporting its current taxonomic treatment as a species, Salmonella bongori, separate from S. enterica. The Salmonella Reference Collection C, composed of the 16 strains used in DNA sequence studies, has been established for research on variation in natural populations.

Full Text

The Full Text of this article is available as a PDF (184.6 KB).

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. Beltran P., Plock S. A., Smith N. H., Whittam T. S., Old D. C., Selander R. K. Reference collection of strains of the Salmonella typhimurium complex from natural populations. J Gen Microbiol. 1991 Mar;137(3):601–606. doi: 10.1099/00221287-137-3-601. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. Boyd E. F., Wang F. S., Beltran P., Plock S. A., Nelson K., Selander R. K. Salmonella reference collection B (SARB): strains of 37 serovars of subspecies I. J Gen Microbiol. 1993 Jun;139(Pt 6):1125–1132. doi: 10.1099/00221287-139-6-1125. [DOI] [PubMed] [Google Scholar]
  5. Crosa J. H., Brenner D. J., Ewing W. H., Falkow S. Molecular relationships among the Salmonelleae. J Bacteriol. 1973 Jul;115(1):307–315. doi: 10.1128/jb.115.1.307-315.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Herzer P. J., Inouye S., Inouye M., Whittam T. S. Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J Bacteriol. 1990 Nov;172(11):6175–6181. doi: 10.1128/jb.172.11.6175-6181.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Le Minor L., Popoff M. Y., Laurent B., Hermant D. Individualisation d'une septième sous-espèce de Salmonella: S. choleraesuis subsp. indica subsp. nov. Ann Inst Pasteur Microbiol. 1986 Sep-Oct;137B(2):211–217. [PubMed] [Google Scholar]
  8. Le Minor L., Véron M., Popoff M. Taxonomie des Salmonella. Ann Microbiol (Paris) 1982 Sep-Oct;133(2):223–243. [PubMed] [Google Scholar]
  9. Li J., Ochman H., Groisman E. A., Boyd E. F., Solomon F., Nelson K., Selander R. K. Relationship between evolutionary rate and cellular location among the Inv/Spa invasion proteins of Salmonella enterica. Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7252–7256. doi: 10.1073/pnas.92.16.7252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Mills D. M., Bajaj V., Lee C. A. A 40 kb chromosomal fragment encoding Salmonella typhimurium invasion genes is absent from the corresponding region of the Escherichia coli K-12 chromosome. Mol Microbiol. 1995 Feb;15(4):749–759. doi: 10.1111/j.1365-2958.1995.tb02382.x. [DOI] [PubMed] [Google Scholar]
  11. Nei M., Gojobori T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986 Sep;3(5):418–426. doi: 10.1093/oxfordjournals.molbev.a040410. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Nelson K., Selander R. K. Intergeneric transfer and recombination of the 6-phosphogluconate dehydrogenase gene (gnd) in enteric bacteria. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):10227–10231. doi: 10.1073/pnas.91.21.10227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Ochman H., Selander R. K. Standard reference strains of Escherichia coli from natural populations. J Bacteriol. 1984 Feb;157(2):690–693. doi: 10.1128/jb.157.2.690-693.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Reeves M. W., Evins G. M., Heiba A. A., Plikaytis B. D., Farmer J. J., 3rd Clonal nature of Salmonella typhi and its genetic relatedness to other salmonellae as shown by multilocus enzyme electrophoresis, and proposal of Salmonella bongori comb. nov. J Clin Microbiol. 1989 Feb;27(2):313–320. doi: 10.1128/jcm.27.2.313-320.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. 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]
  21. Stoleru G. H., Le Minor L., Lhéritier A. M. Polynucleotide sequence divergence among strains of Salmonella sub-genus IV and closely related organisms. Ann Microbiol (Paris) 1976 May-Jun;127(4):477–486. [PubMed] [Google Scholar]
  22. Thampapillai G., Lan R., Reeves P. R. Molecular evolution in the gnd locus of Salmonella enterica. Mol Biol Evol. 1994 Nov;11(6):813–828. doi: 10.1093/oxfordjournals.molbev.a040165. [DOI] [PubMed] [Google Scholar]