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PMID: 8990281 Published · ppublish English Journal Article

Contribution of horizontal gene transfer and deletion events to development of distinctive patterns of fimbrial operons during evolution of Salmonella serotypes.

Journal of bacteriology ·Vol. 179 ·No. 2 ·1997-01-00 ·Pages 317-22

Bäumler AJ, Gilde AJ, Tsolis RM, van der Velden AW, Ahmer BM, Heffron F

Abstract

Only certain serotypes of Salmonella represent 99% of all human clinical isolates. We determined whether the phylogenetic distribution of fimbrial operons would account for the host adaptations observed for Salmonella serotypes. We found that three fimbrial operons, fim, lpf, and agf, were present in a lineage ancestral to Salmonella. While the fim and agf fimbrial operons were highly conserved among all Salmonella serotypes, sequence analysis suggested that the lpf operon was lost from many distantly related lineages. As a consequence, the distribution of the lpf operon cannot be explained easily and may be a consequence of positive and negative selection in different hosts for the presence of these genes. Two other fimbrial operons, sef and pef, each entered two distantly related Salmonella lineages and each is present only in a small number of serotypes. These results show that horizontal gene transfer and deletion events have created unique combinations of fimbrial operons among Salmonella serotypes. The presence of sef and pef correlated with serotypes frequently isolated from common domesticated animals.

MeSH Terms
Chromosomes, Bacterial Escherichia coli/genetics Evolution, Molecular Fimbriae, Bacterial/genetics Gene Deletion Operon Phylogeny Salmonella/classification,genetics Salmonella typhimurium/genetics Sequence Homology, Nucleic Acid Serotyping
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Bäumler A J
Department of Molecular Microbiology and Immunology, Oregon Health Sciences University, Portland 97201-3098, USA.
Gilde A J
Tsolis R M
van der Velden A W
Ahmer B M
Heffron F
References (51)
51 references, click to expand
  1. Studies into the role of the SEF14 fimbrial antigen in the pathogenesis of Salmonella enteritidis.
    Microb Pathog. 1996 Apr;20(4):235-46 PMID: 8737493
  2. Antigens of the type-2 fimbriae of salmonellae: "cross-reacting material" (CRM) of type-1 fimbriae.
    J Med Microbiol. 1971 May;4(2):215-25 PMID: 5570104
  3. The pef fimbrial operon of Salmonella typhimurium mediates adhesion to murine small intestine and is necessary for fluid accumulation in the infant mouse.
    Infect Immun. 1996 Jan;64(1):61-8 PMID: 8557375
  4. The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer's patches.
    Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):279-83 PMID: 8552622
  5. Salmonella enteritidis agfBAC operon encoding thin, aggregative fimbriae.
    J Bacteriol. 1996 Feb;178(3):662-7 PMID: 8550497
  6. Characterisation of monoclonal antibodies against a fimbrial structure of Salmonella enteritidis and certain other serogroup D salmonellae and their application as serotyping reagents.
    Res Vet Sci. 1992 Nov;53(3):300-8 PMID: 1361237
  7. Fimbriae and adhesive properties in Salmonellae.
    J Pathol Bacteriol. 1966 Jul;92(1):107-38 PMID: 5334095
  8. Unique fimbriae-like structures encoded by sefD of the SEF14 fimbrial gene cluster of Salmonella enteritidis.
    Mol Microbiol. 1994 Jun;12(6):893-901 PMID: 7934897
  9. Molecular relationships among the Salmonelleae.
    J Bacteriol. 1973 Jul;115(1):307-15 PMID: 4717519
  10. A new biotyping scheme for Salmonella typhimurium and its phylogenetic significance.
    J Med Microbiol. 1975 Feb;8(1):149-66 PMID: 1092863
  11. The establishment of K99, a thermolabile, transmissible escherichia coli K antigen, previously called "Kco", possessed by calf and lamb enteropathogenic strains.
    Acta Pathol Microbiol Scand B. 1975 Feb;83(1):31-6 PMID: 1093354
  12. Plasmid-controlled colonization factor associated with virulence in Esherichia coli enterotoxigenic for humans.
    Infect Immun. 1975 Sep;12(3):656-67 PMID: 1100526
  13. Colonization of porcine small intestine by Escherichia coli: colonization and adhesion factors of pig enteropathogens that lack K88.
    J Infect Dis. 1977 Apr;135(4):531-9 PMID: 323375
  14. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  15. Evolution of the bacterial genome.
    Annu Rev Microbiol. 1978;32:519-60 PMID: 360975
  16. Salmonellosis in reptiles: a review.
    Am J Epidemiol. 1981 May;113(5):494-9 PMID: 7013476
  17. Molecular epidemiology of antibiotic resistance in salmonella from animals and human beings in the United States.
    N Engl J Med. 1982 Jul 1;307(1):1-6 PMID: 6281645
  18. Construction and comparison of recombinant plasmids encoding type 1 fimbriae of members of the family Enterobacteriaceae.
    Infect Immun. 1985 May;48(2):275-9 PMID: 2580786
  19. Occurrence and distribution of serotypes of the Arizona subgroup of Salmonella strains in the United States from 1967 to 1976.
    J Clin Microbiol. 1986 Jun;23(6):1056-64 PMID: 3711296
  20. Characterization of genes encoding type 1 fimbriae of Klebsiella pneumoniae, Salmonella typhimurium, and Serratia marcescens.
    Infect Immun. 1987 Feb;55(2):281-7 PMID: 2879791
  21. Plasmid-associated virulence of Salmonella typhimurium.
    Infect Immun. 1987 Dec;55(12):2891-901 PMID: 3316027
  22. [Characterization of a 7th subspecies of Salmonella: S. choleraesuis subsp. indica subsp. nov].
    Ann Inst Pasteur Microbiol. 1986 Sep-Oct;137B(2):211-7 PMID: 3689588
  23. Evolution in bacteria: evidence for a universal substitution rate in cellular genomes.
    J Mol Evol. 1987;26(1-2):74-86 PMID: 3125340
  24. 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):7753-7 PMID: 3051004
  25. 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):313-20 PMID: 2915026
  26. Immunological and genetical relatedness of type-1 and type-2 fimbriae in salmonellas of serotypes Gallinarum, Pullorum and Typhimurium.
    J Appl Bacteriol. 1989 Sep;67(3):283-91 PMID: 2575611
  27. Genetic population structure, clonal phylogeny, and pathogenicity of Salmonella paratyphi B.
    Infect Immun. 1990 Jun;58(6):1891-901 PMID: 2341183
  28. International increase in Salmonella enteritidis: a new pandemic?
    Epidemiol Infect. 1990 Aug;105(1):21-7 PMID: 2200698
  29. Basic local alignment search tool.
    J Mol Biol. 1990 Oct 5;215(3):403-10 PMID: 2231712
  30. Lysogenization of Salmonella choleraesuis by phage 14 increases average length of O-antigen chains, serum resistance and intraperitoneal mouse virulence.
    Microb Pathog. 1990 Jun;8(6):393-402 PMID: 1702502
  31. 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):6667-71 PMID: 1862091
  32. Determinants of DNA sequence divergence between Escherichia coli and Salmonella typhimurium: codon usage, map position, and concerted evolution.
    J Mol Evol. 1991 Jul;33(1):23-33 PMID: 1909371
  33. The frequency of fim genes among Salmonella serovars.
    Microb Pathog. 1991 Jun;10(6):487-92 PMID: 1686630
  34. Heteroduplex analysis of Salmonella virulence plasmids and their prevalence in isolates of defined sources.
    Microb Pathog. 1991 Dec;11(6):391-7 PMID: 1795629
  35. Isolation and characterization of conditional adherent and non-type 1 fimbriated Salmonella typhimurium mutants.
    Mol Microbiol. 1992 Apr;6(7):933-45 PMID: 1351241
  36. 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):6886-95 PMID: 1400239
  37. Evidence for effect of random genetic drift on G+C content after lateral transfer of fucose pathway genes to Escherichia coli K-12.
    Mol Biol Evol. 1994 Nov;11(6):829-38 PMID: 7815923
  38. Identification and sequence analysis of lpfABCDE, a putative fimbrial operon of Salmonella typhimurium.
    J Bacteriol. 1995 Apr;177(8):2087-97 PMID: 7721701
  39. 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):749-59 PMID: 7783645
  40. 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):7252-6 PMID: 7638176
  41. Determining divergence times of the major kingdoms of living organisms with a protein clock.
    Science. 1996 Jan 26;271(5248):470-7 PMID: 8560259
  42. The location of four fimbrin-encoding genes, agfA, fimA, sefA and sefD, on the Salmonella enteritidis and/or S. typhimurium XbaI-BlnI genomic restriction maps.
    Gene. 1996 Feb 22;169(1):75-80 PMID: 8635753
  43. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium.
    Proc Natl Acad Sci U S A. 1996 Mar 19;93(6):2593-7 PMID: 8637919
  44. Characterization of three fimbrial genes, sefABC, of Salmonella enteritidis.
    J Bacteriol. 1993 May;175(9):2523-33 PMID: 8097515
  45. Nucleotide sequence of a 13.9 kb segment of the 90 kb virulence plasmid of Salmonella typhimurium: the presence of fimbrial biosynthetic genes.
    Mol Microbiol. 1993 May;8(3):543-58 PMID: 8100983
  46. Salmonella reference collection B (SARB): strains of 37 serovars of subspecies I.
    J Gen Microbiol. 1993 Jun;139 Pt 6:1125-32 PMID: 8360609
  47. DNA-based diagnostic tests for Salmonella species targeting agfA, the structural gene for thin, aggregative fimbriae.
    J Clin Microbiol. 1993 Sep;31(9):2263-73 PMID: 8104955
  48. 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):1280-4 PMID: 8108402
  49. Recombinational basis of serovar diversity in Salmonella enterica.
    Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2552-6 PMID: 8146152
  50. Restriction map of the Salmonella enteritidis virulence plasmid and its homology with the plasmid of Salmonella typhimurium.
    Microb Pathog. 1994 Feb;16(2):165-9 PMID: 8047003
  51. Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells.
    Mol Microbiol. 1996 Apr;20(1):151-64 PMID: 8861213
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1997-01-00
Pages
317-22
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC178699
Subset
IM
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