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J Bacteriol. Jan 1997; 179(2): 317–322.
PMCID: PMC178699

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


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.

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  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. [PubMed]
  • Aoyama K, Haase AM, Reeves PR. 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):829–838. [PubMed]
  • Bäumler AJ, Heffron F. Identification and sequence analysis of lpfABCDE, a putative fimbrial operon of Salmonella typhimurium. J Bacteriol. 1995 Apr;177(8):2087–2097. [PMC free article] [PubMed]
  • Bäumler AJ, Tsolis RM, Bowe FA, Kusters JG, Hoffmann S, Heffron F. 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):61–68. [PMC free article] [PubMed]
  • Bäumler AJ, Tsolis RM, Heffron F. 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):279–283. [PMC free article] [PubMed]
  • Beltran P, Musser JM, Helmuth R, Farmer JJ, 3rd, Frerichs WM, Wachsmuth IK, Ferris K, McWhorter AC, Wells JG, Cravioto A, 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 U S A. 1988 Oct;85(20):7753–7757. [PMC free article] [PubMed]
  • Boyd EF, Nelson K, Wang FS, Whittam TS, Selander RK. 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. [PMC free article] [PubMed]
  • Boyd EF, Wang FS, Beltran P, Plock SA, Nelson K, Selander RK. Salmonella reference collection B (SARB): strains of 37 serovars of subspecies I. J Gen Microbiol. 1993 Jun;139(Pt 6):1125–1132. [PubMed]
  • Buisán M, Rodríguez-Peña JM, Rotger R. Restriction map of the Salmonella enteritidis virulence plasmid and its homology with the plasmid of Salmonella typhimurium. Microb Pathog. 1994 Feb;16(2):165–169. [PubMed]
  • Chiodini RJ, Sundberg JP. Salmonellosis in reptiles: a review. Am J Epidemiol. 1981 May;113(5):494–499. [PubMed]
  • Clegg S, Hull S, Hull R, Pruckler J. Construction and comparison of recombinant plasmids encoding type 1 fimbriae of members of the family Enterobacteriaceae. Infect Immun. 1985 May;48(2):275–279. [PMC free article] [PubMed]
  • Clegg S, Purcell BK, Pruckler J. Characterization of genes encoding type 1 fimbriae of Klebsiella pneumoniae, Salmonella typhimurium, and Serratia marcescens. Infect Immun. 1987 Feb;55(2):281–287. [PMC free article] [PubMed]
  • Clouthier SC, Collinson SK, Kay WW. Unique fimbriae-like structures encoded by sefD of the SEF14 fimbrial gene cluster of Salmonella enteritidis. Mol Microbiol. 1994 Jun;12(6):893–901. [PubMed]
  • Clouthier SC, Müller KH, Doran JL, Collinson SK, Kay WW. Characterization of three fimbrial genes, sefABC, of Salmonella enteritidis. J Bacteriol. 1993 May;175(9):2523–2533. [PMC free article] [PubMed]
  • Collinson SK, Clouthier SC, Doran JL, Banser PA, Kay WW. Salmonella enteritidis agfBAC operon encoding thin, aggregative fimbriae. J Bacteriol. 1996 Feb;178(3):662–667. [PMC free article] [PubMed]
  • Collinson SK, Liu SL, Clouthier SC, Banser PA, Doran JL, Sanderson KE, Kay WW. 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. [PubMed]
  • Crichton PB, Yakubu DE, Old DC, Clegg S. 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):283–291. [PubMed]
  • Crosa JH, Brenner DJ, Ewing WH, Falkow S. Molecular relationships among the Salmonelleae. J Bacteriol. 1973 Jul;115(1):307–315. [PMC free article] [PubMed]
  • Doolittle RF, Feng DF, Tsang S, Cho G, Little E. Determining divergence times of the major kingdoms of living organisms with a protein clock. Science. 1996 Jan 26;271(5248):470–477. [PubMed]
  • Doran JL, Collinson SK, Burian J, Sarlós G, Todd EC, Munro CK, Kay CM, Banser PA, Peterkin PI, Kay WW. DNA-based diagnostic tests for Salmonella species targeting agfA, the structural gene for thin, aggregative fimbriae. J Clin Microbiol. 1993 Sep;31(9):2263–2273. [PMC free article] [PubMed]
  • Duguid JP, Anderson ES, Alfredsson GA, Barker R, Old DC. A new biotyping scheme for Salmonella typhimurium and its phylogenetic significance. J Med Microbiol. 1975 Feb;8(1):149–166. [PubMed]
  • Duguid JP, Anderson ES, Campbell I. Fimbriae and adhesive properties in Salmonellae. J Pathol Bacteriol. 1966 Jul;92(1):107–138. [PubMed]
  • Evans DG, Silver RP, Evans DJ, Jr, Chase DG, Gorbach SL. Plasmid-controlled colonization factor associated with virulence in Esherichia coli enterotoxigenic for humans. Infect Immun. 1975 Sep;12(3):656–667. [PMC free article] [PubMed]
  • Friedrich MJ, Kinsey NE, Vila J, Kadner RJ. 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):543–558. [PubMed]
  • Gulig PA, Curtiss R., 3rd Plasmid-associated virulence of Salmonella typhimurium. Infect Immun. 1987 Dec;55(12):2891–2901. [PMC free article] [PubMed]
  • Isaacson RE, Nagy B, Moon HW. 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):531–539. [PubMed]
  • Le Minor L, Popoff MY, 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]
  • Li J, Nelson K, McWhorter AC, Whittam TS, Selander RK. Recombinational basis of serovar diversity in Salmonella enterica. Proc Natl Acad Sci U S A. 1994 Mar 29;91(7):2552–2556. [PMC free article] [PubMed]
  • Li J, Ochman H, Groisman EA, Boyd EF, Solomon F, Nelson K, Selander RK. 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. [PMC free article] [PubMed]
  • Lockman HA, Curtiss R., 3rd Isolation and characterization of conditional adherent and non-type 1 fimbriated Salmonella typhimurium mutants. Mol Microbiol. 1992 Apr;6(7):933–945. [PubMed]
  • Mills DM, Bajaj V, Lee CA. 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. [PubMed]
  • Montenegro MA, Morelli G, Helmuth R. Heteroduplex analysis of Salmonella virulence plasmids and their prevalence in isolates of defined sources. Microb Pathog. 1991 Dec;11(6):391–397. [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]
  • 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]
  • Nnalue NA, Newton S, Stocker BA. 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. [PubMed]
  • O'Brien TF, Hopkins JD, Gilleece ES, Medeiros AA, Kent RL, Blackburn BO, Holmes MB, Reardon JP, Vergeront JM, Schell WL, et al. 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. [PubMed]
  • Ochman H, Wilson AC. Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol. 1987;26(1-2):74–86. [PubMed]
  • Old DC, Payne SB. Antigens of the type-2 fimbriae of salmonellae: "cross-reacting material" (CRM) of type-1 fimbriae. J Med Microbiol. 1971 May;4(2):215–225. [PubMed]
  • Orskov I, Orskov F, Smith HW, Sojka WJ. 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):31–36. [PubMed]
  • Reeves MW, Evins GM, Heiba AA, Plikaytis BD, Farmer JJ., 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. [PMC free article] [PubMed]
  • Riley M, Anilionis A. Evolution of the bacterial genome. Annu Rev Microbiol. 1978;32:519–560. [PubMed]
  • Rodrigue DC, Tauxe RV, Rowe B. International increase in Salmonella enteritidis: a new pandemic? Epidemiol Infect. 1990 Aug;105(1):21–27. [PMC free article] [PubMed]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PMC free article] [PubMed]
  • Selander RK, Beltran P, Smith NH, Barker RM, Crichton PB, Old DC, Musser JM, Whittam TS. Genetic population structure, clonal phylogeny, and pathogenicity of Salmonella paratyphi B. Infect Immun. 1990 Jun;58(6):1891–1901. [PMC free article] [PubMed]
  • Sharp PM. 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. [PubMed]
  • Shea JE, Hensel M, Gleeson C, Holden DW. 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):2593–2597. [PMC free article] [PubMed]
  • Stein MA, Leung KY, Zwick M, Garcia-del Portillo F, Finlay BB. 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):151–164. [PubMed]
  • Swenson DL, Clegg S, Old DC. The frequency of fim genes among Salmonella serovars. Microb Pathog. 1991 Jun;10(6):487–492. [PubMed]
  • Thorns CJ, Sojka MG, Mclaren IM, Dibb-Fuller M. 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):300–308. [PubMed]
  • Thorns CJ, Turcotte C, Gemmell CG, Woodward MJ. Studies into the role of the SEF14 fimbrial antigen in the pathogenesis of Salmonella enteritidis. Microb Pathog. 1996 Apr;20(4):235–246. [PubMed]
  • Weiss SH, Blaser MJ, Paleologo FP, Black RE, McWhorter AC, Asbury MA, Carter GP, Feldman RA, Brenner DJ. 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):1056–1064. [PMC free article] [PubMed]

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