Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1991 Aug;173(15):4757–4764. doi: 10.1128/jb.173.15.4757-4764.1991

Role of two flagellin genes in Campylobacter motility.

P Guerry 1, R A Alm 1, M E Power 1, S M Logan 1, T J Trust 1
PMCID: PMC208154  PMID: 1856171

Abstract

Campylobacter coli VC167 T2 has two flagellin genes, flaA and flaB, which share 91.9% sequence identity. The flaA gene is transcribed from a o-28 promoter, and the flaB gene from a o-54 promoter. Gene replacement mutagenesis techniques were used to generate flaA+ flaB and flaA flaB+ mutants. Both gene products are capable of assembling independently into functional filaments. A flagellar filament composed exclusively of the flaA gene product is indistinguishable in length from that of the wild type and shows a slight reduction in motility. The flagellar filament composed exclusively of the flaB gene product is severely truncated in length and greatly reduced in motility. Thus, while both flagellins are not necessary for motility, both products are required for a fully active flagellar filament. Although the wild-type flagellar filament is a heteropolymer of the flaA and flaB gene products, immunogold electron microscopy suggests that flaB epitopes are poorly surface exposed along the length of the wild-type filament.

Full text

PDF

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Abimiku A. G., Dolby J. M., Borriello S. P. Comparison of different vaccines and induced immune response against Campylobacter jejuni colonization in the infant mouse. Epidemiol Infect. 1989 Apr;102(2):271–280. doi: 10.1017/s0950268800029940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Abimiku A. G., Dolby J. M. Cross-protection of infant mice against intestinal colonisation by Campylobacter jejuni: importance of heat-labile serotyping (Lior) antigens. J Med Microbiol. 1988 Aug;26(4):265–268. doi: 10.1099/00222615-26-4-265. [DOI] [PubMed] [Google Scholar]
  3. 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]
  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. Butzler J. P., Skirrow M. B. Campylobacter enteritis. Clin Gastroenterol. 1979 Sep;8(3):737–765. [PubMed] [Google Scholar]
  6. 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]
  7. Chowdhury M. N. Campylobacter jejuni enteritis; a review. Trop Geogr Med. 1984 Sep;36(3):215–222. [PubMed] [Google Scholar]
  8. 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]
  9. Gerl L., Sumper M. Halobacterial flagellins are encoded by a multigene family. Characterization of five flagellin genes. J Biol Chem. 1988 Sep 15;263(26):13246–13251. [PubMed] [Google Scholar]
  10. Guerry P., Logan S. M., Thornton S., Trust T. J. Genomic organization and expression of Campylobacter flagellin genes. J Bacteriol. 1990 Apr;172(4):1853–1860. doi: 10.1128/jb.172.4.1853-1860.1990. [DOI] [PMC free article] [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. DNA sequence analysis suggests that expression of flagellar and chemotaxis genes in Escherichia coli and Salmonella typhimurium is controlled by an alternative sigma factor. Proc Natl Acad Sci U S A. 1987 Sep;84(18):6422–6424. doi: 10.1073/pnas.84.18.6422. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  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. Kostrzynska M., Betts J. D., Austin J. W., Trust T. J. Identification, characterization, and spatial localization of two flagellin species in Helicobacter pylori flagella. J Bacteriol. 1991 Feb;173(3):937–946. doi: 10.1128/jb.173.3.937-946.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kranz R. G., Foster-Hartnett D. Transcriptional regulatory cascade of nitrogen-fixation genes in anoxygenic photosynthetic bacteria: oxygen- and nitrogen-responsive factors. Mol Microbiol. 1990 Nov;4(11):1793–1800. doi: 10.1111/j.1365-2958.1990.tb02027.x. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. LeGendre N., Matsudaira P. Direct protein microsequencing from Immobilon-P Transfer Membrane. Biotechniques. 1988 Feb;6(2):154–159. [PubMed] [Google Scholar]
  21. 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]
  22. 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]
  23. 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]
  24. Logan S. M., Trust T. J. Molecular identification of surface protein antigens of Campylobacter jejuni. Infect Immun. 1983 Nov;42(2):675–682. doi: 10.1128/iai.42.2.675-682.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Minnich S. A., Newton A. Promoter mapping and cell cycle regulation of flagellin gene transcription in Caulobacter crescentus. Proc Natl Acad Sci U S A. 1987 Mar;84(5):1142–1146. doi: 10.1073/pnas.84.5.1142. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. 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]
  27. 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]
  28. 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]
  29. Mullin D. A., Newton A. Ntr-like promoters and upstream regulatory sequence ftr are required for transcription of a developmentally regulated Caulobacter crescentus flagellar gene. J Bacteriol. 1989 Jun;171(6):3218–3227. doi: 10.1128/jb.171.6.3218-3227.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Ninfa A. J., Mullin D. A., Ramakrishnan G., Newton A. Escherichia coli sigma 54 RNA polymerase recognizes Caulobacter crescentus flbG and flaN flagellar gene promoters in vitro. J Bacteriol. 1989 Jan;171(1):383–391. doi: 10.1128/jb.171.1.383-391.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Nuijten P. J., van Asten F. J., Gaastra W., van der Zeijst B. A. Structural and functional analysis of two Campylobacter jejuni flagellin genes. J Biol Chem. 1990 Oct 15;265(29):17798–17804. [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. Sasse-Dwight S., Gralla J. D. Role of eukaryotic-type functional domains found in the prokaryotic enhancer receptor factor sigma 54. Cell. 1990 Sep 7;62(5):945–954. doi: 10.1016/0092-8674(90)90269-k. [DOI] [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. 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]
  36. Stragier P., Losick R. Cascades of sigma factors revisited. Mol Microbiol. 1990 Nov;4(11):1801–1806. doi: 10.1111/j.1365-2958.1990.tb02028.x. [DOI] [PubMed] [Google Scholar]
  37. Thornton S. A., Logan S. M., Trust T. J., Guerry P. Polynucleotide sequence relationships among flagellin genes of Campylobacter jejuni and Campylobacter coli. Infect Immun. 1990 Aug;58(8):2686–2689. doi: 10.1128/iai.58.8.2686-2689.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Totten P. A., Lory S. Characterization of the type a flagellin gene from Pseudomonas aeruginosa PAK. J Bacteriol. 1990 Dec;172(12):7188–7199. doi: 10.1128/jb.172.12.7188-7199.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ueki Y., Umeda A., Fujimoto S., Mitsuyama M., Amako K. Protection against Campylobacter jejuni infection in suckling mice by anti-flagellar antibody. Microbiol Immunol. 1987;31(12):1161–1171. doi: 10.1111/j.1348-0421.1987.tb01350.x. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES