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. 1990 Apr;172(4):1853–1860. doi: 10.1128/jb.172.4.1853-1860.1990

Genomic organization and expression of Campylobacter flagellin genes.

P Guerry 1, S M Logan 1, S Thornton 1, T J Trust 1
PMCID: PMC208679  PMID: 2318805

Abstract

Campylobacter coli VC167, which undergoes an antigenic flagellar variation, contains two full-length flagellin genes, flaA and flaB, that are located adjacent to one another in a tandem orientation and are 91.5% homologous. The gene product of flaB, which has an Mr of 58,946, has 93% sequence homology to the gene product of flaA, which has an Mr of 58,916 (S. M. Logan, T. J. Trust, and P. Guerry, J. Bacteriol. 171:3031-3038, 1989). Mutational analyses and primer extension experiments indicated that the two genes are transcribed under the control of distinct promoters but that they are expressed concomitantly in the same cell, regardless of the antigenic phase of flagella being produced. The flaA gene, which was expressed at higher levels than the flaB gene in both phases, was transcribed from a typical sigma 28-type promoter, whereas the flaB promoter was unusual. A mutant producing only the flaB gene product did not synthesize a flagellar filament and was nonmotile. Southern blot analysis indicated that flagellar antigenic variation involves a rearrangement of flagellin sequence information rather than the alternate expression of the two distinct genes.

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Selected References

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  1. Abraham J. M., Freitag C. S., Clements J. R., Eisenstein B. I. An invertible element of DNA controls phase variation of type 1 fimbriae of Escherichia coli. Proc Natl Acad Sci U S A. 1985 Sep;82(17):5724–5727. doi: 10.1073/pnas.82.17.5724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Arnosti D. N., Chamberlin M. J. Secondary sigma factor controls transcription of flagellar and chemotaxis genes in Escherichia coli. Proc Natl Acad Sci U S A. 1989 Feb;86(3):830–834. doi: 10.1073/pnas.86.3.830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Belland R. J., Trust T. J. Deoxyribonucleic acid sequence relatedness between thermophilic members of the genus Campylobacter. J Gen Microbiol. 1982 Nov;128(11):2515–2522. doi: 10.1099/00221287-128-11-2515. [DOI] [PubMed] [Google Scholar]
  4. Black R. E., Levine M. M., Clements M. L., Hughes T. P., Blaser M. J. Experimental Campylobacter jejuni infection in humans. J Infect Dis. 1988 Mar;157(3):472–479. doi: 10.1093/infdis/157.3.472. [DOI] [PubMed] [Google Scholar]
  5. Borst P., Greaves D. R. Programmed gene rearrangements altering gene expression. Science. 1987 Feb 6;235(4789):658–667. doi: 10.1126/science.3544215. [DOI] [PubMed] [Google Scholar]
  6. Butzler J. P., Skirrow M. B. Campylobacter enteritis. Clin Gastroenterol. 1979 Sep;8(3):737–765. [PubMed] [Google Scholar]
  7. Caldwell M. B., Guerry P., Lee E. C., Burans J. P., Walker R. I. Reversible expression of flagella in Campylobacter jejuni. Infect Immun. 1985 Dec;50(3):941–943. doi: 10.1128/iai.50.3.941-943.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chowdhury M. N. Campylobacter jejuni enteritis; a review. Trop Geogr Med. 1984 Sep;36(3):215–222. [PubMed] [Google Scholar]
  9. Figurski D. H., Helinski D. R. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1648–1652. doi: 10.1073/pnas.76.4.1648. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fouser L. A., Friesen J. D. Mutations in a yeast intron demonstrate the importance of specific conserved nucleotides for the two stages of nuclear mRNA splicing. Cell. 1986 Apr 11;45(1):81–93. doi: 10.1016/0092-8674(86)90540-4. [DOI] [PubMed] [Google Scholar]
  11. Guerry P., Logan S. M., Trust T. J. Genomic rearrangements associated with antigenic variation in Campylobacter coli. J Bacteriol. 1988 Jan;170(1):316–319. doi: 10.1128/jb.170.1.316-319.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Harris L. A., Logan S. M., Guerry P., Trust T. J. Antigenic variation of Campylobacter flagella. J Bacteriol. 1987 Nov;169(11):5066–5071. doi: 10.1128/jb.169.11.5066-5071.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Helmann J. D., Chamberlin M. J. Structure and function of bacterial sigma factors. Annu Rev Biochem. 1988;57:839–872. doi: 10.1146/annurev.bi.57.070188.004203. [DOI] [PubMed] [Google Scholar]
  14. Homma M., Fujita H., Yamaguchi S., Iino T. Regions of Salmonella typhimurium flagellin essential for its polymerization and excretion. J Bacteriol. 1987 Jan;169(1):291–296. doi: 10.1128/jb.169.1.291-296.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hull R. A., Gill R. E., Hsu P., Minshew B. H., Falkow S. Construction and expression of recombinant plasmids encoding type 1 or D-mannose-resistant pili from a urinary tract infection Escherichia coli isolate. Infect Immun. 1981 Sep;33(3):933–938. doi: 10.1128/iai.33.3.933-938.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kuwajima G., Asaka J., Fujiwara T., Fujiwara T., Node K., Kondo E. Nucleotide sequence of the hag gene encoding flagellin of Escherichia coli. J Bacteriol. 1986 Dec;168(3):1479–1483. doi: 10.1128/jb.168.3.1479-1483.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Labigne-Roussel A., Courcoux P., Tompkins L. Gene disruption and replacement as a feasible approach for mutagenesis of Campylobacter jejuni. J Bacteriol. 1988 Apr;170(4):1704–1708. doi: 10.1128/jb.170.4.1704-1708.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  19. Lee A., O'Rourke J. L., Barrington P. J., Trust T. J. Mucus colonization as a determinant of pathogenicity in intestinal infection by Campylobacter jejuni: a mouse cecal model. Infect Immun. 1986 Feb;51(2):536–546. doi: 10.1128/iai.51.2.536-546.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Logan S. M., Guerry P., Rollins D. M., Burr D. H., Trust T. J. In vivo antigenic variation of Campylobacter flagellin. Infect Immun. 1989 Aug;57(8):2583–2585. doi: 10.1128/iai.57.8.2583-2585.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Logan S. M., Harris L. A., Trust T. J. Isolation and characterization of Campylobacter flagellins. J Bacteriol. 1987 Nov;169(11):5072–5077. doi: 10.1128/jb.169.11.5072-5077.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Logan S. M., Trust T. J., Guerry P. Evidence for posttranslational modification and gene duplication of Campylobacter flagellin. J Bacteriol. 1989 Jun;171(6):3031–3038. doi: 10.1128/jb.171.6.3031-3038.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Logan S. M., Trust T. J. Location of epitopes on Campylobacter jejuni flagella. J Bacteriol. 1986 Nov;168(2):739–745. doi: 10.1128/jb.168.2.739-745.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Marrs C. F., Ruehl W. W., Schoolnik G. K., Falkow S. Pilin-gene phase variation of Moraxella bovis is caused by an inversion of the pilin genes. J Bacteriol. 1988 Jul;170(7):3032–3039. doi: 10.1128/jb.170.7.3032-3039.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Meier J. T., Simon M. I., Barbour A. G. Antigenic variation is associated with DNA rearrangements in a relapsing fever Borrelia. Cell. 1985 Jun;41(2):403–409. doi: 10.1016/s0092-8674(85)80013-1. [DOI] [PubMed] [Google Scholar]
  26. Meyer T. F., Mlawer N., So M. Pilus expression in Neisseria gonorrhoeae involves chromosomal rearrangement. Cell. 1982 Aug;30(1):45–52. doi: 10.1016/0092-8674(82)90010-1. [DOI] [PubMed] [Google Scholar]
  27. Minnich S. A., Ohta N., Taylor N., Newton A. Role of the 25-, 27-, and 29-kilodalton flagellins in Caulobacter crescentus cell motility: method for construction of deletion and Tn5 insertion mutants by gene replacement. J Bacteriol. 1988 Sep;170(9):3953–3960. doi: 10.1128/jb.170.9.3953-3960.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Mirel D. B., Chamberlin M. J. The Bacillus subtilis flagellin gene (hag) is transcribed by the sigma 28 form of RNA polymerase. J Bacteriol. 1989 Jun;171(6):3095–3101. doi: 10.1128/jb.171.6.3095-3101.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Morooka T., Umeda A., Amako K. Motility as an intestinal colonization factor for Campylobacter jejuni. J Gen Microbiol. 1985 Aug;131(8):1973–1980. doi: 10.1099/00221287-131-8-1973. [DOI] [PubMed] [Google Scholar]
  30. Newell D. G. Monoclonal antibodies directed against the flagella of Campylobacter jejuni: production, characterization and lack of effect on the colonization of infant mice. J Hyg (Lond) 1986 Apr;96(2):131–141. doi: 10.1017/s0022172400065906. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Plasterk R. H., Simon M. I., Barbour A. G. Transposition of structural genes to an expression sequence on a linear plasmid causes antigenic variation in the bacterium Borrelia hermsii. Nature. 1985 Nov 21;318(6043):257–263. doi: 10.1038/318257a0. [DOI] [PubMed] [Google Scholar]
  32. Pleier E., Schmitt R. Identification and sequence analysis of two related flagellin genes in Rhizobium meliloti. J Bacteriol. 1989 Mar;171(3):1467–1475. doi: 10.1128/jb.171.3.1467-1475.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Segal E., Hagblom P., Seifert H. S., So M. Antigenic variation of gonococcal pilus involves assembly of separated silent gene segments. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2177–2181. doi: 10.1073/pnas.83.7.2177. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sharp P. M., Li W. H. The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 1987 Feb 11;15(3):1281–1295. doi: 10.1093/nar/15.3.1281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Silverman M., Simon M. Phase variation: genetic analysis of switching mutants. Cell. 1980 Apr;19(4):845–854. doi: 10.1016/0092-8674(80)90075-6. [DOI] [PubMed] [Google Scholar]
  36. Silverman M., Zieg J., Hilmen M., Simon M. Phase variation in Salmonella: genetic analysis of a recombinational switch. Proc Natl Acad Sci U S A. 1979 Jan;76(1):391–395. doi: 10.1073/pnas.76.1.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Skirrow M. B. Campylobacter enteritis: a "new" disease. Br Med J. 1977 Jul 2;2(6078):9–11. doi: 10.1136/bmj.2.6078.9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sparling P. F., Cannon J. G., So M. Phase and antigenic variation of pili and outer membrane protein II of Neisseria gonorrhoeae. J Infect Dis. 1986 Feb;153(2):196–201. doi: 10.1093/infdis/153.2.196. [DOI] [PubMed] [Google Scholar]
  39. Stern A., Brown M., Nickel P., Meyer T. F. Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation. Cell. 1986 Oct 10;47(1):61–71. doi: 10.1016/0092-8674(86)90366-1. [DOI] [PubMed] [Google Scholar]
  40. Zieg J., Silverman M., Hilmen M., Simon M. Recombinational switch for gene expression. Science. 1977 Apr 8;196(4286):170–172. doi: 10.1126/science.322276. [DOI] [PubMed] [Google Scholar]

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