Multiple insertions of fimbrial operons correlate with the evolution of Salmonella serovars responsible for human disease

Molecular Microbiology

Volumn 33, Issue 3, 1999, Pages 612-622

  Folkesson, Anders ^a   Advani, Abdolreza ^b   Sukupolvi, Soila ^c   Pfeifer, John D ^c   Normark, Staffan ^a,b   Löfdahl, Sven ^b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b SWEDISH INSTITUTE FOR INFECTIOUS DISEASE CONTROL   (Sweden)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL DNA; ESCHERICHIA COLI ENTEROTOXIN; INVASIN; TRANSFER RNA;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; CONTROLLED STUDY; DNA FLANKING REGION; ESCHERICHIA COLI; FEMALE; GENE CLUSTER; GENE INSERTION; GENE LOCATION; GENE LOCUS; GENE MAPPING; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OPERON; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATOR GENE; SALMONELLA; SALMONELLA ENTERICA; SALMONELLOSIS; SEQUENCE HOMOLOGY;

CHROMOSOME MAPPING; DNA TRANSPOSABLE ELEMENTS; EVOLUTION, MOLECULAR; FIMBRIAE, BACTERIAL; GENES, BACTERIAL; HUMANS; MUTATION; NUCLEIC ACID HYBRIDIZATION; OPERON; PHYLOGENY; RNA, TRANSFER; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SEROTYPING; VIRULENCE;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA; PROKARYOTA; SALMONELLA; SALMONELLA ENTERICA;

EID: 0032791139     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1999.01508.x     Document Type: Article

References (54)

1. Ausubel, F.M., Brent, M.R., Kingston, R.E., Moore, D.D., Siedman, J.G., Smith, J.A., et al. (1996) Current Protocols in Molecular Biology, Vols 1-3. New York: John Wiley.
2. Barondess, J.J., and Beckwith, J. (1990). A bacterial virulence determinant encoded by lysogenic coliphage lambda. Nature 346: 871-874.
3. Bäumler, A.J. (1997) The record of horizontal gene transfer. Trends Microbiol 5: 318-322.
4. Bäumler, A.J., Gilde, A.J., Tsolis, R.M., van der Welden, A.W.M., Ahmer, B.M.M., and 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.
5. Belitsky, B.R., Gustafsson, M.C., Sonenshein, A.L., and Von Wachenfeldt, C. (1997) An Irp-like gene of Bacillus subtilis involved in branched-chain amino acid transport. J Bacteriol 179: 5448-5457.
6. Blanc-Potard, A., and Groisman, E.A. (1997) The Salmonella selC locus contains a pathogenicity island mediating intra-macrophage survival. EMBO J 16: 5376-5385.
7. Blomen, L, Löfdahl, S., Stenström, T.A., and Norberg, R. (1993) Identification of enterotoxigenic Escherichia coli isolates: a comparison of PCR, DNA hybridization, ELISAs and bioassays. J Microbiol Methods 17: 181-191.
8. Blomfield, I.C., Vaughn, V., Rest, R.F., and Eisenstein, B.I. (1991) Allelic exchange in Escherichia coli using the Bacillus subtilis sacB gene and a temperature-sensitive pSC101 replicon. Mol Microbiol 5: 1447-1457.
9. Boyd, E.F., Wang, F., Whittam, T.S., and Selander, R.K. (1996) Molecular genetic relationship of the Salmonellae. Appl Environ Microbiol 62: 804-808.
10. Carniel, E., Guilvout, I., and Prentice, M. (1996) Characterization of a large chromosomal 'high-pathogenicity island' in biotype 1B Yersinia enterocolitica. J Bacteriol 176: 6743-6751.
11. Clouthier, S.C., Muller, K.-H., Doran, J.L., Collinson, S.K., and Kay, W.W. (1993) Characterization of three fimbrial genes, set ABC, of Salmonella enteritidis. J Bacteriol 175: 2523-2533.
12. Clouthier, S.C., Collinson, S.K., and Kay, W.W. (1994) Unique fimbriae-like structures encoded by sefD of the Sef 14 fimbrial gene cluster of Salmonella enteritidis. Mol Microbiol 12: 893-903.
13. Conner, C.P., Heithoff, D.M., Julio, S.M., Sinsheimer, R.L., and Mahan, M.J. (1998) Differential patterns of acquired virulence genes distinguish Salmonella strains. Proc Natl Acad Sci USA 95: 4641-4645.
14. Devereux, J., Haeberli, P., and Smithies, O. (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12: 387-395.
15. Fields, P.I., Swanson, R.V., Haidaris, C.G., and Heffron, F. (1986) Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA 83: 5189-5193.
16. Friedrich, M.J., Kinsey, N.E., Vila, J., and Kadner, R.J. (1993) Nucleotide sequence of a 13.9kb segment of the 90kb virulence plasmid of Salmonella typhimurium: the presence of fimbrial biosynthetic genes. Mol Microbiol 8: 543-556.
17. Froehlich, B.J., Karakashian, A., Melsen, L.R., Wakefield, J.C., and Scott, J.R. (1994) CooC and CooD are required for assembly of CS1 pili. Mol Microbion 12: 387-401.
18. Garcia, M.-I., Gounon, P., Courcoux, P., Labigne, A., and Le Bouguenec, C. (1996) The afimbrial adhesive sheath encoded by the afa-3 gene cluster of pathogenic i Escherichia coli is composed of two adhesins. Mol Microbiol 19: 683-693.
19. de Graaf, F.K., and Gaastra, W. (1994) Fimbriae of enterotoxigenic Escherichia coli. In Fimbriae: Adhesion, Genetics, Biogenesis, and Vaccines. Klemm, P. (ed.). Boca Raton, FL: CRC Press, pp. 58-83.
20. Groisman, E.A., and Ochman, H. (1997) How Salmonella became a pathogen. Trends Microbiol 5: 343-349.
21. Groisman, E.A., Stumorski, M.A., Solomon, F.R., Lin, R., and Ochman, H. (1993) Molecular, functional, and evolutionary analysis of sequences specific to Salmonella. Proc Natl Acad Sci USA 90: 1033-1037.
22. Gulig, P.A., and Curtiss, III, R. (1987) Plasmid-associated virulence of Salmonella typhimurium. Infect Immun 55: 2891-2901.
23. Gunn, J.S., Belden, W.J., and Miller, S.I. (1998) Identification of PhoP-PhoQ activated genes within a duplicated region of the Salmonella typhimurium chromosome. Microb Pathogen 25: 77-90.
24. Heithoff, D.M., Conner, C.P., Hanna, P.C., Julio, S.M., Hentschel, U., and Mahan, M.J. (1997) Bacterial infection as assessed by in vivo gene expression. Proc Natl Acad Sci USA 94: 934-939.
25. Mensel, M., Shea, J.E., Bäumler, A.J., Gleeson, C., Blattner, F., and Holden, D.W. (1997) Analysis of the boundaries of Salmonella pathogenicity island 2 and the corresponding chromosomal region of Escherichia coli K12. J Bacteriol 179: 1105-1111.
26. Hensel, M., Shea, J.E., Gleeson, C., Jones, M.D., Dalton, E., and Holden, D.W. (1995) Simultaneous identification of bacterial virulence genes by negative selection. Science 269: 400-403.
27. Hultgren, S.J., Normark, S., and Abraham, S.N. (1991) Chaperone-assisted assembly and molecular architecture of adhesive pili. Annu Rev Microbiol 45: 383-415.
28. Hung, D.L., Knight, S.D., Woods, R.M., Pinkner, J.S., and Hultgren, S.J. (1996) Molecular basis of two subfamilies of immunoglobulin-like chaperones. EMBO J 15: 3792-3805.
29. Lawrence, J.G., and Ochman, H. (1998) Molecular archaeology of the Escherichia coli genome. Proc Natl Acad Sci USA 95: 9413-9417.
30. Lawrence, J.G., and Roth, J.R. (1996) Selfish operons: horizontal transfer may drive the evolution of gene clusters. Genetics 143: 1843-1860.
31. Low, D., Braaten, B., and van der Woude, M. (1996) Fimbriae. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C., Curtiss, III, R., Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., et al. (eds). Washington, DC: American Society for Microbiology Press, pp. 146-157.
32. McDaniel, T., Jarvis, K.G., Donnenberg, M.S., and Kaper, J.B. (1995) A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci USA 92: 1664-1668.
33. Maloy, S.R., Stewart, V.J., and Taylor, R.K. (1996) Genetic Analysis of Pathogenic Bacteria. A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
34. Marklund, B.I., Tennent, J.M., Garcia, E., Hamers, A., Båga, M., Lindberg, F., et al. (1992) Horizontal gene transfer of the Escherichia coli pap and prs pili operons as a mechanism for the development of tissue-specific adhesive properties. Mol Microbiol 6: 2225-2242.
35. Mills, D.M., Bajaj, V., and Lee, C.A. (1995) 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 15: 749-759.
36. Ochman, H., and Groisman, E.A. (1996) Distribution of pathogenicity islands in Salmonella spp. Infect Immun 64: 5410-5412.
37. Ochman, H., Soncini, F.C., Solomon, F., and Groisman, E.A. (1996) Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci USA 93: 7800-7804.
38. Pier, G.B., Grout, M., Zaidi, T., Meluleni, G., Mueschenborn, S.S., Banting, G., et al. (1998). Salmonella typhi uses CFTR to enter intestinal epithelial cells. Nature 393: 79-82.
39. Popoff, M.Y., and Le Minor, L. (1992) Antigenic Formulae of the Salmonella Serovars, 5th edn. Paris: WHO Collaborating Center for Reference and Research on Salmonella, Institute Pasteur.
40. Priess, H., Kamp, D., Kahmann, R., Bräuer, B., and Delius, H. (1982) Nucleotide sequence of the immunity region of bacteriophage Mu. Mol Gen Genet 186: 315-321.
41. Rajakumar, K., Luo, F., Sasakawa, C., and Adler, B. (1996) Evolutionary perspective on a composite Shigella flexneri 2a virulence plasmid-borne locus comprising three distinct genetic elements. FEMS Microbiol Lett 144: 13-20.
42. Reeves, M.W., Evins, G.M., Heiba, A.A., Plikaytis, B.D., and Farmer, III, J.J. (1989) 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 27: 313-320.
43. Sajjan, U.S., Sun, L., Goldstein, R., and Forstner, J.F. (1995) Cable (cbl) type II pili of cystic fibrosis-associated Burkholderia (Pseudomonas) cepacia: nucleotide sequence of the cbIA major subunit pilin gene and novel morphology of the assembled appendage fibers. J Bacteriol 177: 1030-1038.
44. Salyers, A.A., and Whitt, D.D. (1994) Bacterial Pathogenesis: a Molecular Approach, 1st edn. Washington DC: American Society for Microbiology Press.
45. Sanger, F., Nicklen, S., and Coulson, A.R. (1977). DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463-5467.
46. Schmeiger, H. (1972) Phage P22 mutants with increased or decreased transduction abilities. Mol Gen Genet 119: 75-88.
47. Simon, R., Preifer, U., and Phuler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Biotechnology 1: 785-789.
48. Sokurenko, E.V., Chesnokova, V., Dykhuizen, D.E., Ofek, I., Wu, X.R., Krogfelt, K.A., et al. (1998) Pathogenic adaptation of Escherichia coli by natural variation of the FimH adhesin. Proc Natl Acad Sci USA 95: 8922-8926.
49. Svennerholm, A.-M., Åhren, C., and Jertborn, M. (1997) Vaccines against enterotoxigenic E. coli infections. I. Oral inactivated vaccines against enterotoxigenic E. coli. In New Generation Vaccines. Levine, M.M., Woodrow, G.C., Kaper J.B., and Cobon, G.S. (eds). New York: Marcel Dekker, pp. 865-873.
50. Tacket, C.O., and Levine, M.M. (1997) Vaccines against enterotoxigenic E. coli infections. II. Live oral vaccines and subunit (purified fimbriae and toxin subunit) vaccines. In New Generation Vaccines. Levine, M.M., Woodrow, G.C., Kaper, J.B., and Cobon, G.S. (eds). New York: Marcel Dekker, pp. 875-883.
51. Tobe, T., Schoolnik, G.K., Sohel, I., Bustamante, V.H., and Puente, J. (1996) Cloning and characterization of bfpTVW, genes required for the transcriptional activation of bfpA in enteropathogenic Escherichia coli. Mol Microbiol 21: 963-975.
52. van der Velden, A.W.M., Bäumler, A.J., Tsolis, R.M., and Heffron, F. (1998) Multiple fimbrial adhesins required for full virulence of Salmonella typhimurium in mice. Infect Immun 66: 2803-2808.
53. Wong, K., McClelland, M., Stillwell, L.C., Sisk, E.C., Thurston, S.J., and Saffer, J.D. (1998) Identification and sequence analysis of a 27-kilobase chromosomal fragment containing a Salmonella pathogenicity island located at 92 minutes on the chromosome map of Salmonella enterica serovar Typhimurium LT2. Infect Immun 66: 3365-3371.
54. Wood, M.W., Jones, M.A., Watson, P.R., Hedges, S., Wallis, T.S., and Galyov, E.E. (1998) Identification of a pathogenicity island required for Salmonella enteropathogenicity. Mol Microbiol 29: 883-891.