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. 1996 Feb;178(3):662–667. doi: 10.1128/jb.178.3.662-667.1996

Salmonella enteritidis agfBAC operon encoding thin, aggregative fimbriae.

S K Collinson 1, S C Clouthier 1, J L Doran 1, P A Banser 1, W W Kay 1
PMCID: PMC177709  PMID: 8550497

Abstract

Salmonella enteritidis produces thin, aggregative fimbriae, named SEF17, which are composed of polymerized AgfA fimbrin proteins. DNA sequence analysis of a 2-kb region of S. enteritidis DNA revealed three contiguous genes, agfBAC. The 453-bp agfA gene encodes the AgfA fimbrin, which was predicted to be 74% identical and 86% similar in primary sequence to the Escherichia coli curli structural protein, CsgA. pHAG, a pUC18 derivative containing a 3.0-kb HindIII fragment encoding agfBAC, directed the in vitro expression of the major AgfA fimbrin, with an M(r) of 17,000, and a minor AgfB protein, with an M(r) of 16,000, encoded by the 453-bp agfB gene. AgfA was not expressed from pDAG, a pUC18 derivative containing a 3.1-kb DraI DNA fragment encoding agfA but not agfB. Primer extension analysis identified two adjacent transcription start sites located immediately upstream of agfB in positions analogous to those of the E. coli curlin csgBA operon. No transcription start sites were located immediately upstream of agfA or agfC. Northern (RNA) blot analysis confirmed that transcription of agfA was initiated from the agfB promoter region. Secondary-structure analysis of the putative mRNA transcript for agfBAC predicted the formation of a stem-loop structure (delta Gzero, -22 kcal/mol [-91 kJ/mol]) in the intercistronic region between agfA and agfC, which may be involved in stabilization of the agfBA portion of the agfBAC transcript. agfBAC and flanking regions had a high degree of sequence similarity with those counterparts of the E. coli curlin csgBA region for which sequence data are available. These data are demonstrative of the high degree of similarity between S. enteritidis SEF17 fimbriae and E. coli curli with respect to fimbrin amino acid sequence and genetic organization and, therefore, are indicative of a common and relatively recent ancestry.

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Selected References

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  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. Arnqvist A., Olsén A., Normark S. Sigma S-dependent growth-phase induction of the csgBA promoter in Escherichia coli can be achieved in vivo by sigma 70 in the absence of the nucleoid-associated protein H-NS. Mol Microbiol. 1994 Sep;13(6):1021–1032. doi: 10.1111/j.1365-2958.1994.tb00493.x. [DOI] [PubMed] [Google Scholar]
  3. Arnqvist A., Olsén A., Pfeifer J., Russell D. G., Normark S. The Crl protein activates cryptic genes for curli formation and fibronectin binding in Escherichia coli HB101. Mol Microbiol. 1992 Sep;6(17):2443–2452. doi: 10.1111/j.1365-2958.1992.tb01420.x. [DOI] [PubMed] [Google Scholar]
  4. Belasco J. G., Higgins C. F. Mechanisms of mRNA decay in bacteria: a perspective. Gene. 1988 Dec 10;72(1-2):15–23. doi: 10.1016/0378-1119(88)90123-0. [DOI] [PubMed] [Google Scholar]
  5. Bilge S. S., Apostol J. M., Jr, Aldape M. A., Moseley S. L. mRNA processing independent of RNase III and RNase E in the expression of the F1845 fimbrial adhesin of Escherichia coli. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1455–1459. doi: 10.1073/pnas.90.4.1455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bäumler A. J., Heffron F. Identification and sequence analysis of lpfABCDE, a putative fimbrial operon of Salmonella typhimurium. J Bacteriol. 1995 Apr;177(8):2087–2097. doi: 10.1128/jb.177.8.2087-2097.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Båga M., Göransson M., Normark S., Uhlin B. E. Processed mRNA with differential stability in the regulation of E. coli pilin gene expression. Cell. 1988 Jan 29;52(2):197–206. doi: 10.1016/0092-8674(88)90508-9. [DOI] [PubMed] [Google Scholar]
  8. Chen C. Y., Beatty J. T., Cohen S. N., Belasco J. G. An intercistronic stem-loop structure functions as an mRNA decay terminator necessary but insufficient for puf mRNA stability. Cell. 1988 Feb 26;52(4):609–619. doi: 10.1016/0092-8674(88)90473-4. [DOI] [PubMed] [Google Scholar]
  9. Clouthier S. C., Müller K. H., Doran J. L., Collinson S. K., Kay W. W. Characterization of three fimbrial genes, sefABC, of Salmonella enteritidis. J Bacteriol. 1993 May;175(9):2523–2533. doi: 10.1128/jb.175.9.2523-2533.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Collinson S. K., Doig P. C., Doran J. L., Clouthier S., Trust T. J., Kay W. W. Thin, aggregative fimbriae mediate binding of Salmonella enteritidis to fibronectin. J Bacteriol. 1993 Jan;175(1):12–18. doi: 10.1128/jb.175.1.12-18.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Collinson S. K., Emödy L., Müller K. H., Trust T. J., Kay W. W. Purification and characterization of thin, aggregative fimbriae from Salmonella enteritidis. J Bacteriol. 1991 Aug;173(15):4773–4781. doi: 10.1128/jb.173.15.4773-4781.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Collinson S. K., Emödy L., Trust T. J., Kay W. W. Thin aggregative fimbriae from diarrheagenic Escherichia coli. J Bacteriol. 1992 Jul;174(13):4490–4495. doi: 10.1128/jb.174.13.4490-4495.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. De Graaf F. K. Fimbrial structures of enterotoxigenic E. coli. Antonie Van Leeuwenhoek. 1988;54(5):395–404. doi: 10.1007/BF00461857. [DOI] [PubMed] [Google Scholar]
  14. Doran J. L., Collinson S. K., Burian J., Sarlós G., Todd E. C., Munro C. K., Kay C. M., Banser P. A., Peterkin P. I., Kay W. W. 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. doi: 10.1128/jcm.31.9.2263-2273.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gold L. Posttranscriptional regulatory mechanisms in Escherichia coli. Annu Rev Biochem. 1988;57:199–233. doi: 10.1146/annurev.bi.57.070188.001215. [DOI] [PubMed] [Google Scholar]
  16. Gong M., Makowski L. Helical structure of P pili from Escherichia coli. Evidence from X-ray fiber diffraction and scanning transmission electron microscopy. J Mol Biol. 1992 Dec 5;228(3):735–742. doi: 10.1016/0022-2836(92)90860-m. [DOI] [PubMed] [Google Scholar]
  17. Hultgren S. J., Normark S., Abraham S. N. Chaperone-assisted assembly and molecular architecture of adhesive pili. Annu Rev Microbiol. 1991;45:383–415. doi: 10.1146/annurev.mi.45.100191.002123. [DOI] [PubMed] [Google Scholar]
  18. Jordi B. J., op den Camp I. E., de Haan L. A., van der Zeijst B. A., Gaastra W. Differential decay of RNA of the CFA/I fimbrial operon and control of relative gene expression. J Bacteriol. 1993 Dec;175(24):7976–7981. doi: 10.1128/jb.175.24.7976-7981.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kuehn M. J., Heuser J., Normark S., Hultgren S. J. P pili in uropathogenic E. coli are composite fibres with distinct fibrillar adhesive tips. Nature. 1992 Mar 19;356(6366):252–255. doi: 10.1038/356252a0. [DOI] [PubMed] [Google Scholar]
  20. Marck C. 'DNA Strider': a 'C' program for the fast analysis of DNA and protein sequences on the Apple Macintosh family of computers. Nucleic Acids Res. 1988 Mar 11;16(5):1829–1836. doi: 10.1093/nar/16.5.1829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. McCormick J. R., Zengel J. M., Lindahl L. Intermediates in the degradation of mRNA from the lactose operon of Escherichia coli. Nucleic Acids Res. 1991 May 25;19(10):2767–2776. doi: 10.1093/nar/19.10.2767. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Olsén A., Arnqvist A., Hammar M., Sukupolvi S., Normark S. The RpoS sigma factor relieves H-NS-mediated transcriptional repression of csgA, the subunit gene of fibronectin-binding curli in Escherichia coli. Mol Microbiol. 1993 Feb;7(4):523–536. doi: 10.1111/j.1365-2958.1993.tb01143.x. [DOI] [PubMed] [Google Scholar]
  23. Oudega B., De Graaf F. K. Genetic organization and biogenesis of adhesive fimbriae of Escherichia coli. Antonie Van Leeuwenhoek. 1988;54(4):285–299. doi: 10.1007/BF00393521. [DOI] [PubMed] [Google Scholar]
  24. Paranchych W., Frost L. S. The physiology and biochemistry of pili. Adv Microb Physiol. 1988;29:53–114. doi: 10.1016/s0065-2911(08)60346-x. [DOI] [PubMed] [Google Scholar]
  25. Reznikoff W. S., Siegele D. A., Cowing D. W., Gross C. A. The regulation of transcription initiation in bacteria. Annu Rev Genet. 1985;19:355–387. doi: 10.1146/annurev.ge.19.120185.002035. [DOI] [PubMed] [Google Scholar]
  26. Sawers G., Böck A. Novel transcriptional control of the pyruvate formate-lyase gene: upstream regulatory sequences and multiple promoters regulate anaerobic expression. J Bacteriol. 1989 May;171(5):2485–2498. doi: 10.1128/jb.171.5.2485-2498.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  28. von Heijne G. The signal peptide. J Membr Biol. 1990 May;115(3):195–201. doi: 10.1007/BF01868635. [DOI] [PubMed] [Google Scholar]

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