Genomic analysis and growth-phase-dependent regulation of the SEF14 fimbriae of serovar Enteritidis

The GenBank accession number for the sequence reported in this paper is AF239978.

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Abstract

serovar Enteritidis is a leading cause of food poisoning in the USA and Europe. Although serovars share many fimbrial operons, a few fimbriae are limited to specific serovars. SEF14 fimbriae are restricted to group D and the genes encoding this virulence factor were acquired relatively recently. Genomic, genetic and gene expression studies have been integrated to investigate the ancestry, regulation and expression of the genes. Genomic comparisons of the serovars sequenced revealed that the operon is inserted in in Enteritidis, Paratyphi and Typhi, and revealed the presence of a previously unidentified 25 kb pathogenicity island in Typhimurium at this location. Enteritidis contains a region of homology between the virulence plasmid and the chromosome downstream of the operon. The operon itself consists of four co-transcribed genes, , and adjacent to there is an AraC-like transcriptional activator that is required for expression of the genes. Expression of the genes was optimal during growth in late exponential phase and was repressed during stationary phase. The regulation was coordinated by the RpoS sigma factor.

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2001-10-01
2024-03-28
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References

  1. Ahmer B. M., Tran M., Heffron F. 1999; The virulence plasmid of Salmonella typhimurium is self-transmissible. J Bacteriol 181:1364–1368
    [Google Scholar]
  2. Alexeyev M. F., Shokolenko I. N., Croughan T. P. 1995; New mini-Tn 5 derivatives for insertion mutagenesis and genetic engineering in gram-negative bacteria. Can J Microbiol 41:1053–1055 [CrossRef]
    [Google Scholar]
  3. Altschul S. F., Gish W. 1996; Local alignment statistics. Methods Enzymol 266:460–480
    [Google Scholar]
  4. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410 [CrossRef]
    [Google Scholar]
  5. Altschul S. F., Boguski M. S., Gish W., Wootton J. C. 1994; Issues in searching molecular sequence databases. Nat Genet 6:119–129 [CrossRef]
    [Google Scholar]
  6. Bäumler A. J., Tsolis R. M., Bowe F. A., Kusters J. G., Hoffmann S., Heffron F. 1996a; 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 64:61–68
    [Google Scholar]
  7. Bäumler A. J., Tsolis R. M., Heffron F. 1996b; The lpf fimbrial operon mediates adhesion of Salmonella typhimurium to murine Peyer’s patches. Proc Natl Acad Sci USA 93:279–283 [CrossRef]
    [Google Scholar]
  8. Bäumler A. J., Gilde A. J., Tsolis R. M., van der Velden A. W., Ahmer B. M., Heffron F. 1997; Contribution of horizontal gene transfer and deletion events to development of distinctive patterns of fimbrial operons during evolution of Salmonella serotypes. J Bacteriol 179:317–322
    [Google Scholar]
  9. Caron J., Coffield L. M., Scott J. R. 1989; A plasmid-encoded regulatory gene, rns , required for expression of the CS1 and CS2 adhesins of enterotoxigenic Escherichia coli . Proc Natl Acad Sci USA 86:963–967 [CrossRef]
    [Google Scholar]
  10. Choudhury D., Thompson A., Stojanoff V., Langermann S., Pinkner J., Hultgren S. J., Knight S. D. 1999; X-ray structure of the FimC–FimH chaperone–adhesin complex from uropathogenic Escherichia coli . Science 285:1061–1066 [CrossRef]
    [Google Scholar]
  11. Clouthier S. C., Muller K. H., Doran J. L., Collinson S. K., Kay W. W. 1993; Characterization of three fimbrial genes, sefABC , of Salmonella enteritidis . J Bacteriol 175:2523–2533
    [Google Scholar]
  12. Clouthier S. C., Collinson S. K., Kay W. W. 1994; Unique fimbriae-like structures encoded by sefD of the SEF14 fimbrial gene cluster of Salmonella enteritidis . Mol Microbiol 12:893–903 [CrossRef]
    [Google Scholar]
  13. Clouthier S. C., Collinson S. K., White A. P., Banser P. A., Kay W. W. 1998; tRNA(Arg) (fimU) and expression of SEF14 and SEF21 in Salmonella enteritidis . J Bacteriol 180:840–845
    [Google Scholar]
  14. Collighan R. J., Woodward M. J. 2001; The SEF14 fimbrial antigen of Salmonella enterica serovar Enteritidis is encoded within a pathogenicity islet. Vet Microbiol 80:235–245 [CrossRef]
    [Google Scholar]
  15. Collinson S. K., Liu S. L., Clouthier S. C., Banser P. A., Doran J. L., Sanderson K. E., Kay W. W. 1996; The location of four fimbrin-encoding genes, agfA, fimA, sefA and sefD , on the Salmonella enteritidis and/or S. typhimurium Xba I– Bln I genomic restriction maps. Gene 169:75–80 [CrossRef]
    [Google Scholar]
  16. Edwards R. A., Puente J. L. 1998; Fimbrial expression in enteric bacteria: a critical step in intestinal pathogenesis. Trends Microbiol 6:282–287 [CrossRef]
    [Google Scholar]
  17. Edwards R. A., Schifferli D. M. 1997; Differential regulation of fasA and fasH expression of Escherichia coli 987P fimbriae by environmental cues. Mol Microbiol 25:797–809 [CrossRef]
    [Google Scholar]
  18. Edwards R. A., Cao J., Schifferli D. M. 1996; Identification of major and minor chaperone proteins involved in the export of 987P fimbriae. J Bacteriol 178:3426–3433
    [Google Scholar]
  19. Edwards R. A., Keller L. H., Schifferli D. M. 1998; Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression. Gene 207:149–157 [CrossRef]
    [Google Scholar]
  20. Edwards R., Helm R., Maloy S. 1999; Increasing DNA transfer efficiency by temporary inactivation of host restriction. BioTechniques 26:892–900
    [Google Scholar]
  21. Edwards R. A., Schifferli D. M., Maloy S. R. 2000; A role for Salmonella fimbriae in intraperitoneal infections. Proc Natl Acad Sci USA 97:1258–1262 [CrossRef]
    [Google Scholar]
  22. Fang F. C., Libby S. J., Buchmeier N. A., Loewen P. C., Switala J., Harwood J., Guiney D. G. 1992; The alternative sigma factor katF ( rpoS ) regulates Salmonella virulence. Proc Natl Acad Sci USA 89:11978–11982 [CrossRef]
    [Google Scholar]
  23. Gaastra W., Svennerholm A.-M. 1996; Colonization factors of human enterotoxigenic Escherichia coli (ETEC. Trends Microbiol 4:444–452 [CrossRef]
    [Google Scholar]
  24. Gallegos M. T., Schleif R., Bairoch A., Hofmann K., Ramos J. L. 1997; Arac/XylS family of transcriptional regulators. Microbiol Mol Biol Rev 61:393–410
    [Google Scholar]
  25. Guzman L. M., Belin D., Carson M. J., Beckwith J. 1995; Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121–4130
    [Google Scholar]
  26. Jordi B. J. 1992; The mode of action of CfaD of Escherichia coli and VirF of Shigella flexneri and other members of the AraC family of positive regulators. Mol Microbiol 6:3451
    [Google Scholar]
  27. Jost B. H., Adler B. 1993; Site of transcriptional activation of virB on the large plasmid of Shigella flexneri 2a by VirF, a member of the AraC family of transcriptional activators. Microb Pathog 14:481–488 [CrossRef]
    [Google Scholar]
  28. Keller L. H., Schifferli D. M., Benson C. E., Aslam S., Eckroade R. J. 1997; Invasion of chicken reproductive tissues and forming eggs is not unique to Salmonella enteritidis . Avian Dis 41:535–539 [CrossRef]
    [Google Scholar]
  29. Khan A. S., Schifferli D. M. 1994; A minor 987P protein different from the structural fimbrial subunit is the adhesin. Infect Immun 62:4223–4243
    [Google Scholar]
  30. Maloy S. 1990 Experimental Techniques in Bacterial Genetics , 1st edn. Boston, MA: Jones and Bartlett;
    [Google Scholar]
  31. Maloy S. R., Stewart V. J., Taylor R. K. 1996 Genetic Analysis of Pathogenic Bacteria Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  32. Martinez-Laguna Y., Calva E., Puente J. L. 1999; Autoactivation and environmental regulation of bfpT expression, the gene coding for the transcriptional activator of bfpA in enteropathogenic Escherichia coli . Mol Microbiol 33:153–166 [CrossRef]
    [Google Scholar]
  33. Nataro J. P., Yikang D., Yingkang D., Walker K. 1994; AggR, a transcriptional activator of aggregative adherence fimbria I expression in enteroaggregative Escherichia coli . J Bacteriol 176:4691–4699
    [Google Scholar]
  34. Pfeifer C. G., Marcus S. L., Steele-Mortimer O., Knodler L. A., Finlay B. B. 1999; Salmonella typhimurium virulence genes are induced upon bacterial invasion into phagocytic and nonphagocytic cells. Infect Immun 67:5690–5698
    [Google Scholar]
  35. Rodriguez-Pena J. M., Alvarez I., Ibanez M., Rotger R. 1997; Homologous regions of the Salmonella enteritidis virulence plasmid and the chromosome of Salmonella typhi encode thiol: disulphide oxidoreductases belonging to the DsbA thioredoxin family. Microbiology 143:1405–1413 [CrossRef]
    [Google Scholar]
  36. Romling U., Rohde M., Olsen A., Normark S., Reinkoster J. 2000; AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 36:10–23 [CrossRef]
    [Google Scholar]
  37. Sanderson K., Hessel A., Liu S., Rudd K. E. 1996; The genetic map of Salmonella typhimurium , edition VIII. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology pp 1903–1999 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  38. Sauer F. G., Fütterer K., Pinkner J. S., Dodson K. W., Hultgren S. J., Waksman G. 1999; Structural basis of chaperone function and pilus biogenesis. Science 285:1058–1061 [CrossRef]
    [Google Scholar]
  39. Slauch J. M., Silhavy T. J. 1991; cis -acting ompF mutations that result in OmpR-dependent constitutive expression. J Bacteriol 173:4039–4048
    [Google Scholar]
  40. Swords W. E., Cannon B. M., Benjamin W. H. Jr 1997; Avirulence of LT2 strains of Salmonella typhimurium results from a defective rpoS gene. Infect Immun 65:2451–2453
    [Google Scholar]
  41. Thorns C. J., Sojka M. G., Chasey D. 1990; Detection of a novel fimbrial structure on the surface of Salmonella enteritidis by using a monoclonal antibody. J Clin Microbiol 28:2409–2414
    [Google Scholar]
  42. Tinker J. K., Clegg S. 2000; Characterization of FimY as a coactivator of type 1 fimbrial expression in Salmonella enterica serovar Typhimurium. Infect Immun 68:3305–3313 [CrossRef]
    [Google Scholar]
  43. Tinker J. K., Clegg S. 2001; Control of FimY translation and type 1 fimbrial production by the arginine tRNA encoded by fimU in Salmonella enterica serovar Typhimurium. Mol Microbiol 40:757–768 [CrossRef]
    [Google Scholar]
  44. Tinker J. K., Hancox L. S., Clegg S. 2001; FimW is a negative regulator affecting type 1 fimbrial expression in Salmonella enterica serovar typhimurium. J Bacteriol 183:435–442 [CrossRef]
    [Google Scholar]
  45. Tobe T., Schoolnick G. K., Sohel I., Bustamante V. H., Puente J. L. 1996; Cloning and characterization of bfpTVW , genes required for the transcriptional activation of bfpA in enteropathogenic Escherichia coli . Mol Microbiol 21:963–975 [CrossRef]
    [Google Scholar]
  46. Townsend S. M., Kramer N. E., Edwards R. A. 7 other authors 2001; Salmonella enterica serotype Typhi possesses a unique repertoire of fimbrial genes. Infect Immun 69:2894–2901 [CrossRef]
    [Google Scholar]
  47. Turcotte C., Woodward M. J. 1993; Cloning, DNA nucleotide sequence and distribution of the gene encoding the SEF14 fimbrial antigen of Salmonella enteritidis . J Gen Microbiol 139:1477–1485 [CrossRef]
    [Google Scholar]
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