1887

Journal of Medical Microbiology logo

Volume 38, Issue 2

Evolutionary origin and radiation of the avian-adapted non-motile salmonellae Free

Abstract

Summary

Multilocus enzyme electrophoresis was employed to estimate chromosomal genotypic diversity and relationships among 131 isolates of the non-motile biotypes Gallinarum and Pullorum (serotype , 9, 12:–:–) that cause fowl typhoid and pullorum disease, respectively. Thirteen electrophoretic types (ETs), marking clones, were distinguished, and construction of a neighbour-joining phylogenetic tree revealed three lineages: one consisted of five ETs of Gallinarum, a second included seven ETs of Pullorum, and a third was represented by a single ET (Ga/Pu 1) that is intermediate between those of the other two lineages in both multilocus enzyme genotype and biochemical properties. Enzyme genotype analysis and comparative nucleotide sequencing of the phase 1 flagellin gene (), the hook-associated protein 1 gene (), and the 6-phosphogluconate dehydrogenase gene () identified serotype Enteritidis (, 9,12:g, m:–) as a close relative of the non-motile salmonellae. In most strains of biotype Gallinarum, the gene is complete, intact and identical in sequence to that of Enteritidis, but isolates of three ETs had a stop codon at position 495. The sequences of the ETs of Pullorum differed from that of Enteritidis in having non-synonymous changes in either two or three codons and a synonymous change in one codon. The sharing of distinctive alleles at three metabolic enzyme loci and a stop codon in indicates that the non-motile salmonellae are monophyletic and that their most recent common ancestor was non-motile. Since diverging from that ancestor, the Pullorum lineage has evolved more rapidly than the Gallinarum and Ga/Pu 1 lineages.

  • Received:
  • Accepted:
  • Published Online:
© Society for General Microbiology, 1993
Loading

Article metrics loading...

/content/journal/jmm/10.1099/00222615-38-2-129
1993-02-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jmm/38/2/medmicro-38-2-129.html?itemId=/content/journal/jmm/10.1099/00222615-38-2-129&mimeType=html&fmt=ahah

References

  1. Ewing WH. Edwards and Ewing’s identification of Enterobacteriaceae. , 4th edn. New York: Elsevier Science; 1986181–318
     [Google Scholar]
  2. Le Minor L. Salmonella Lignieres 1900, 389. In: Krieg NR, Holt JG. (eds) Bergey’s manual of systematic bacteriology vol 1 Baltimore: Williams and Wilkins; 1984428–458
     [Google Scholar]
  3. Le Minor L, Popoff MY. Antigenic formulas of the Salmonella serovars. , 5th edn. Paris: WHO Collaborating Centre for Reference and Research on Salmonella, Institut Pasteur; 19881–146
     [Google Scholar]
  4. Pomeroy BS. Fowl typhoid. In: Hofstad MS, Barnes HJ, Calneck BW, Reid WM, Yoder HW. (eds) Diseases of poultry, 8th edn. Ames: Iowa State University Press; 198479–91
     [Google Scholar]
  5. Snoeyenbos GH. Pullorum disease. In: Hofstad MS, Barnes HJ, Calneck BW, Reid WM, Yoder HW. (eds) Diseases of poultry, 8th edn. Ames: Iowa State University Press; 198466–79
     [Google Scholar]
  6. Timoney JF, Gillespie JH, Scott FW, Barlough JE. (eds) Hagan and Bruner’s microbiology and infectious disease of domestic animals. , 8th edn.. Ithaca, NY: Comstock Publishing Associates; 198874–88
     [Google Scholar]
  7. Blaxland JD, Sojka WJ, Smither AM. A study of Salm. pullorum and Salm. gallinarum strains isolated from field outbreaks of disease. J Comp Pathol 1956; 6:270–277
     [Google Scholar]
  8. Cox NA, Williams JE. A simplified biochemical system to screen Salmonella isolates from poultry for serotyping. Poult Sci 1976; 55:1968–1971
     [Google Scholar]
  9. Guinée PAM, Van Leeuwen WJ. Phage typing of Salmonella. In: Bergan T, Norris JR. (eds) Methods in microbiology vol 11 London: Academic Press; 1978157–191
     [Google Scholar]
  10. Lilleengen K. Typing of Salmonella gallinarum and Salmonella pullorum by means of bacteriophage. Acta Pathol Microbiol Scand 1952; 30:194–202
     [Google Scholar]
  11. Crichton PB, Old DC. Salmonellae of serotypes Gallinarum and Pullorum grouped by biotyping and fimbrial-gene probing. J Med Microbiol 1990; 32:145–152
     [Google Scholar]
  12. Selander RK, Caugant DA, Ochman H, Musser JM, Gilmour MN, Whittam TS. Methods of multilocus enzyme electrophoresis for bacterial population genetics and sys-tematics. Appl Environ Microbiol 1986; 51:873–884
     [Google Scholar]
  13. Beltran P, Musser JM, Helmuth R. et al. 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 USA 1988; 85:7753–7757
     [Google Scholar]
  14. Wilson K. Preparation of genomic DNA from bacteria. In: Ausubel FM, Brent R, Kingston RE. et al. (eds) Current protocols in molecular biology vol 1 New York: Wiley; 19902.4.1–2.4.5
     [Google Scholar]
  15. Smith NH, Selander RK. Sequence invariance of the antigencoding central region of the phase 1 flagellar filament gene (fliC) among strains of Salmonella typhimurium. J Bacteriol 1990; 172:603–609
     [Google Scholar]
  16. Saiki RK, Gelfand DH, Stoffel S. et al. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 1988; 239:487–491
     [Google Scholar]
  17. Higuchi RG, Ochman H. Production of single-stranded DNA templates by exonuclease digestion following the polymerase chain reaction. Nucleic Acids Res 1989; 17:5865
     [Google Scholar]
  18. Reeves P, Stevenson G. Cloning and nucleotide sequence of the Salmonella typhimurium LT2 gnd gene and its homology with the corresponding sequence of Escherichia coli K12. Mol Gen Genet 1989; 217:182–184
     [Google Scholar]
  19. Nasoff MS, Baker HV, Wolf RE. DNA sequence of the Escherichia coli gene, gnd, for 6-phosphogluconate dehydrogenase. Gene 1984; 27:253–264
     [Google Scholar]
  20. Nei M. Molecular evolutionary genetics. New York: Columbia University Press; 19871–512
     [Google Scholar]
  21. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425
     [Google Scholar]
  22. Selander RK, Beltran P, Smith NH. et al. Genetic population structure, clonal phylogeny, and pathogenicity of Salmonella paratyphi B. Infect Immun 1990; 58:1891–1901
     [Google Scholar]
  23. Selander RK, Beltran P, Smith NH. et al. Evolutionary genetic relationships of clones of Salmonella serovars that cause human typhoid and other enteric fevers. Infect Immun 1990; 58:2262–2275
     [Google Scholar]
  24. Iino T, Lederberg J. Genetics of Salmonella. In: Van Oye E. (ed) The world problem of salmonellosis The Hague: Dr W. Junk; 1964111–142
     [Google Scholar]
  25. Lederberg J, Edwards PR. Serotypic recombination in Salmonella. J Immunol 1953; 71:232–240
     [Google Scholar]
  26. Frankel G, Newton SMC, Schoolnik GK, Stocker BAD. Intragenic recombination in a flagellin gene: characterization of the H1-j gene of Salmonella typhi. EMBO J 1989; 8:3149–3152
     [Google Scholar]
  27. Joys TM. The covalent structure of the phase-1 flagellar filament protein of Salmonella typhimurium and its comparison with other flagellins. J Biol them 1985; 260:15758–15761
     [Google Scholar]
  28. Joys TM, Schödel F. Epitope mapping of the d flagellar antigen of Salmonella muenchen. Infect Immun 1991; 59:3330–3332
     [Google Scholar]
  29. Wei LN, Joys TM. Covalent structure of three phase-1 flagellar filament proteins of Salmonella. J Mol Biol 1985; 186:791–803
     [Google Scholar]
  30. Yamaguchi S, Iino T. Genetic determination of the antigenic specificity of flagellar protein in Salmonella. J Gen Microbiol 1969; 55:59–74
     [Google Scholar]
  31. Macnab RM. Flagella. In: Neidhardt FC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE. (eds) Escherichia coli and Salmonella typhimurium. Cellular and molecular biology vol 1 Washington, D.C: American Society for Microbiology; 198770–83
     [Google Scholar]
  32. Homma M, Kutsukake K, Hasebe M, Iino T, Macnab RM, Flg B, Flg C, Flg F, and Flg G. A family of structurally related proteins in the flagellar basal body of Salmonella typhi-murium. J Mol Biol 1990; 211:465–477
     [Google Scholar]
  33. Homma M, De Rosier DJ, Macnab RM. Flagellar hook and hook-associated proteins of Salmonella typhimurium and their relationships to other axial components of the flagellum. J Mol Biol 1990; 213:819–832
     [Google Scholar]
  34. Kutsukake K, Ohya Y, Iino T. Transcriptional analysis of the flagellar regulon of Salmonella typhimurium. J Bacteriol 1990; 172:741–747
     [Google Scholar]
  35. Ohnishi K, Kutsukake K, Suzuki H, Iino T. Gene fliA encodes an alternative sigma factor specific for flagellar opérons in Salmonella typhimurium. Mol Gen Genet 1990; 221:139–147
     [Google Scholar]
  36. Smith NH, Selander RK. Molecular genetic basis for complex flagellar antigen expression in a triphasic serovar of Salmonella. Proc Natl Acad Sci USA 1991; 88:956–960
     [Google Scholar]
  37. Smith NH, Beltran P, Selander RK. Recombination of Sal monella phase 1 flagellin genes generates new serovars. J Bacteriol 1990; 172:2209–2216
     [Google Scholar]
  38. Barrow PA, Simpson JM, Lovell MA, Binns MM. Contribution of Salmonella gallinarum large plasmid toward virulence in fowl typhoid. Infect Immun 1987; 55:388–392
     [Google Scholar]
  39. Barrow PA, Lovell MA. The association between a large molecular mass plasmid and virulence in a strain of Salmonella pullorum. J Gen Microbiol 1988; 134:2307–2316
     [Google Scholar]
  40. Barrow PA, Lovell MA. Functional homology of virulence plasmids in Salmonella gallinarum, S. pullorum, and S. typhimurium. Infect Immun 1989; 57:3136–3141
     [Google Scholar]
  41. Burgin AB, Parodos K, Lane DJ, Pace NR. The excision of intervening sequences from Salmonella 23S ribosomal RNA. Cell 1990; 60:405–114
     [Google Scholar]
  42. Hsu D, Zee YC, Ingraham J, Shih L-M. Diversity of cleavage patterns of Salmonella 23S rRNA. J Gen Microbiol 1992; 138:199–203
     [Google Scholar]
  43. Müller K-H, Trust TJ, Kay WW. Fimbriation genes of Salmonella enteritidis. J Bacteriol 1989; 171:4648–4654
     [Google Scholar]
  44. Selander RK, Smith NH, Li J. et al. Molecular evolutionary genetics of the cattle-adapted serovar Salmonella dublin. J Bacteriol 1992; 174:3587–3592
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/00222615-38-2-129
Loading
Evolutionary origin and radiation of the avian-adapted non-motile salmonellae
J. Med. Microbiol. 38, 129 (1993); https://doi.org/10.1099/00222615-38-2-129
/content/journal/jmm/10.1099/00222615-38-2-129
/content/journal/jmm/10.1099/00222615-38-2-129
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error