1887

Abstract

The biosynthesis, assembly and regulation of the flagellar apparatus has been the subject of extensive studies over many decades, with considerable attention devoted to the peritrichous flagella of and . The characterization of flagellar systems from many other bacterial species has revealed subtle yet distinct differences in composition, regulation and mode of assembly of this important subcellular structure. Glycosylation of the major structural protein, the flagellin, has been shown most recently to be an important component of numerous flagellar systems in both Archaea and Bacteria, playing either an integral role in assembly or for a number of bacterial pathogens a role in virulence. This review focuses on the structural diversity in flagellar glycosylation systems and demonstrates that as a consequence of the unique assembly processes, the type of glycosidic linkage found on archaeal and bacterial flagellins is distinctive.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28735-0
2006-05-01
2019-10-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/5/1249.html?itemId=/content/journal/micro/10.1099/mic.0.28735-0&mimeType=html&fmt=ahah

References

  1. Aldridge, P. & Hughes, K. T. ( 2002; ). Regulation of flagellar assembly. Curr Opin Microbiol 5, 160–165.[CrossRef]
    [Google Scholar]
  2. Alm, R. A., Guerry, P., Power, M. E. & Trust, T. J. ( 1992; ). Variation in antigenicity and molecular weight of Campylobacter coli VC167 flagellin in different genetic backgrounds. J Bacteriol 174, 4230–4238.
    [Google Scholar]
  3. Alm, R. A., Ling, L. S., Moir, D. T. & 20 other authors ( 1999; ). Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397, 176–180.[CrossRef]
    [Google Scholar]
  4. Andrutis, K. A., Fox, J. G., Schauer, D. B., Marini, R. P., Li, X., Yan, L., Josenhans, C. & Suerbaum, S. ( 1997; ). Infection of the ferret stomach by isogenic flagellar mutant strains of Helicobacter mustelae. Infect Immun 65, 1962–1966.
    [Google Scholar]
  5. Arnold, F., Bedouet, L., Batina, P., Robreau, G., Talbot, F., Lecher, P. & Malcoste, R. ( 1998; ). Biochemical and immunological analyses of the flagellin of Clostridium tyrobutyricum ATCC 25755. Microbiol Immunol 42, 23–31.[CrossRef]
    [Google Scholar]
  6. Arora, S. K., Wolfgang, M. C., Lory, S. & Ramphal, R. ( 2004; ). Sequence polymorphism in the glycosylation island and flagellins of Pseudomonas aeruginosa. J Bacteriol 186, 2115–2122.[CrossRef]
    [Google Scholar]
  7. Arora, S. K., Neely, A. N., Blair, B., Lory, S. & Ramphal, R. ( 2005; ). Role of motility and flagellin glycosylation in the pathogenesis of Pseudomonas aeruginosa burn wound infections. Infect Immun 73, 4395–4398.[CrossRef]
    [Google Scholar]
  8. Bardy, S. L., Ng, S. Y. & Jarrell, K. F. ( 2003; ). Prokaryotic motility structures. Microbiology 149, 295–304.[CrossRef]
    [Google Scholar]
  9. Bardy, S. L., Ng, S. Y. & Jarrell, K. F. ( 2004; ). Recent advances in the structure and assembly of the archaeal flagellum. J Mol Microbiol Biotechnol 7, 41–51.[CrossRef]
    [Google Scholar]
  10. Bedouet, L., Arnold, F., Robreau, G., Batina, P., Talbot, F. & Binet, A. (1998; ). Evidence for an heterogeneous glycosylation of the Clostridium tyrobutyricum ATCC 25755 flagellin. Microbios 94, 183–192.
    [Google Scholar]
  11. Black, R. E., Levine, M. M., Clements, M. L., Hughes, T. P. & Blaser, M. J. ( 1988; ). Experimental Campylobacter jejuni infection in humans. J Infect Dis 157, 472–479.[CrossRef]
    [Google Scholar]
  12. Bodenmiller, D., Toh, E. & Brun, Y. V. ( 2004; ). Development of surface adhesion in Caulobacter crescentus. J Bacteriol 186, 1438–1447.[CrossRef]
    [Google Scholar]
  13. Brahamsha, B. & Greenberg, E. P. ( 1988; ). Biochemical and cytological analysis of the complex periplasmic flagella from Spirochaeta aurantia. J Bacteriol 170, 4023–4032.
    [Google Scholar]
  14. Carrillo, C. D., Taboada, E., Nash, J. H. & 15 other authors ( 2004; ). Genome-wide expression analyses of Campylobacter jejuni NCTC11168 reveals coordinate regulation of motility and virulence by flhA. J Biol Chem 279, 20327–20338.[CrossRef]
    [Google Scholar]
  15. Castric, P., Cassels, F. J. & Carlson, R. W. ( 2001; ). Structural characterization of the Pseudomonas aeruginosa 1244 pilin glycan. J Biol Chem 276, 26479–26485.[CrossRef]
    [Google Scholar]
  16. Cattozzo, E. M., Stocker, B. A., Radaelli, A., De Giuli, M. C. & Tognon, M. ( 1997; ). Expression and immunogenicity of V3 loop epitopes of HIV-1, isolates SC and WMJ2, inserted in Salmonella flagellin. J Biotechnol 56, 191–203.[CrossRef]
    [Google Scholar]
  17. Champion, O. L., Gaunt, M. W., Gundogdu, O., Elmi, A., Witney, A. A., Hinds, J., Dorrell, N. & Wren, B. W. ( 2005; ). Comparative phylogenomics of the food-borne pathogen Campylobacter jejuni reveals genetic markers predictive of infection source. Proc Natl Acad Sci U S A 102, 16043–16048.[CrossRef]
    [Google Scholar]
  18. Charon, N. W. & Goldstein, S. F. ( 2002; ). Genetics of motility and chemotaxis of a fascinating group of bacteria: the spirochetes. Annu Rev Genet 36, 47–73.[CrossRef]
    [Google Scholar]
  19. Chou, W. K., Dick, S., Wakarchuk, W. W. & Tanner, M. E. ( 2005; ). Identification and characterization of NeuB3 from Campylobacter jejuni as a pseudaminic acid synthase. J Biol Chem 43, 35922–35928.
    [Google Scholar]
  20. Craig, L., Pique, M. E. & Tainer, J. A. ( 2004; ). Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2, 363–378.[CrossRef]
    [Google Scholar]
  21. Creuzenet, C. ( 2004; ). Characterization of CJ1293, a new UDP-GlcNAc C6 dehydratase from Campylobacter jejuni. FEBS Lett 559, 136–140.[CrossRef]
    [Google Scholar]
  22. Creuzenet, C., Schur, M. J., Li, J., Wakarchuk, W. W. & Lam, J. S. ( 2000; ). FlaA1, a new bifunctional UDP-GlcNAc C6 Dehydratase/C4 reductase from Helicobacter pylori. J Biol Chem 275, 34873–34880.[CrossRef]
    [Google Scholar]
  23. Croes, C. L., Moens, S., Van Bastelaere, E., Vanderleyden, J. & Michiels, K. W. ( 2004; ). The polar flagellum mediates Azospirillum brasilense adsorption to wheat roots. J Gen Microbiol 139, 960–967.
    [Google Scholar]
  24. Deakin, W. J., Parker, V. E., Wright, E. L., Ashcroft, K. J., Loake, G. J. & Shaw, C. H. ( 1999; ). Agrobacterium tumefaciens possesses a fourth flagellin gene located in a large gene cluster concerned with flagellar structure, assembly and motility. Microbiology 145, 1397–1407.[CrossRef]
    [Google Scholar]
  25. Dell, A. & Morris, H. R. ( 2001; ). Glycoprotein structure determination by mass spectrometry. Science 291, 2351–2356.[CrossRef]
    [Google Scholar]
  26. Doig, P. & Trust, T. J. ( 1994; ). Identification of surface-exposed outer membrane antigens of Helicobacter pylori. Infect Immun 62, 4526–4533.
    [Google Scholar]
  27. Doig, P., Kinsella, N., Guerry, P. & Trust, T. J. ( 1996; ). Characterization of a post-translational modification of Campylobacter flagellin: identification of a sero-specific glycosyl moiety. Mol Microbiol 19, 379–387.[CrossRef]
    [Google Scholar]
  28. Dons, L., Rasmussen, O. F. & Olsen, J. E. ( 1992; ). Cloning and characterization of a gene encoding flagellin of Listeria monocytogenes. Mol Microbiol 6, 2919–2929.[CrossRef]
    [Google Scholar]
  29. Driks, A., Bryan, R., Shapiro, L. & DeRosier, D. J. ( 1989; ). The organization of the Caulobacter crescentus flagellar filament. J Mol Biol 206, 627–636.[CrossRef]
    [Google Scholar]
  30. Eaton, K. A., Suerbaum, S., Josenhans, C. & Krakowka, S. ( 1996; ). Colonization of gnotobiotic piglets by Helicobacter pylori deficient in two flagellin genes. Infect Immun 64, 2445–2448.
    [Google Scholar]
  31. Engelhardt, H., Schuster, S. C. & Baeuerlein, E. ( 1993; ). An archimedian spiral: the basal disk of the Wolinella flagellar motor. Science 262, 1046–1048.[CrossRef]
    [Google Scholar]
  32. Evdokimov, A. G., Phan, J., Tropea, J. E., Routzahn, K. M., Peters, H. K., Pokross, M. & Waugh, D. S. ( 2003; ). Similar modes of polypeptide recognition by export chaperones in flagellar biosynthesis and type III secretion. Nat Struct Biol 10, 789–793.[CrossRef]
    [Google Scholar]
  33. Feldman, M. F., Wacker, M., Hernandez, M. & 7 other authors ( 2005; ). Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli. Proc Natl Acad Sci U S A 102, 3016–3021.[CrossRef]
    [Google Scholar]
  34. Ferris, F. G., Beveridge, T. J., Marceau-Day, M. L. & Larson, A. D. ( 1984; ). Structure and cell envelope associations of flagellar basal complexes of Vibrio cholerae and Campylobacter fetus. Can J Microbiol 30, 322–333.[CrossRef]
    [Google Scholar]
  35. Fox, J. G. ( 2002; ). The non-H. pylori helicobacters: their expanding role in gastrointestinal and systemic diseases. Gut 50, 273–283.[CrossRef]
    [Google Scholar]
  36. Fuerst, J. A. ( 1980; ). Bacterial sheathed flagella and the rotary motor model for the mechanism of bacterial motility. J Theor Biol 84, 761–774.[CrossRef]
    [Google Scholar]
  37. Gavin, R., Rabaan, A. A., Merino, S., Tomas, J. M., Gryllos, I. & Shaw, J. G. ( 2002; ). Lateral flagella of Aeromonas species are essential for epithelial cell adherence and biofilm formation. Mol Microbiol 43, 383–397.[CrossRef]
    [Google Scholar]
  38. Ge, Y., Li, C., Corum, L., Slaughter, C. A. & Charon, N. W. ( 1998; ). Structure and expression of the FlaA periplasmic flagellar protein of Borrelia burgdorferi. J Bacteriol 180, 2418–2425.
    [Google Scholar]
  39. Geis, G., Suerbaum, S., Forsthoff, B., Leying, H. & Opferkuch, W. ( 1993; ). Ultrastructure and biochemical studies of the flagellar sheath of Helicobacter pylori. J Med Microbiol 38, 371–377.[CrossRef]
    [Google Scholar]
  40. Gober, J. W. & Marques, M. V. ( 1995; ). Regulation of cellular differentiation in Caulobacter crescentus. Microbiol Rev 59, 31–47.
    [Google Scholar]
  41. Goon, S., Kelly, J. F., Logan, S. M., Ewing, C. P. & Guerry, P. ( 2003; ). Pseudaminic acid, the major modification on Campylobacter flagellin, is synthesized via the Cj1293 gene. Mol Microbiol 50, 659–671.[CrossRef]
    [Google Scholar]
  42. Gryllos, I., Shaw, J. G., Gavin, R., Merino, S. & Tomas, J. M. ( 2001; ). Role of flm locus in mesophilic Aeromonas species adherence. Infect Immun 69, 65–74.[CrossRef]
    [Google Scholar]
  43. Guerry, P., Doig, P., Alm, R. A., Burr, D. H., Kinsella, N. & Trust, T. J. ( 1996; ). Identification and characterization of genes required for post-translational modification of Campylobacter coli VC167 flagellin. Mol Microbiol 19, 369–378.[CrossRef]
    [Google Scholar]
  44. Horzempa, J., Comer, J. E., Davis, S. A. & Castric, P. ( 2005; ). Glycosylation substrate specificity of Pseudomonas aeruginosa 1244 Pilin. J Biol Chem 281, 1128–1136.
    [Google Scholar]
  45. Hranitzky, K. W., Mulholland, A., Larson, A. D., Eubanks, E. R. & Hart, L. T. ( 1980; ). Characterization of a flagellar sheath protein of Vibrio cholerae. Infect Immun 27, 597–603.
    [Google Scholar]
  46. Inglis, T. J., Robertson, T., Woods, D. E., Dutton, N. & Chang, B. J. ( 2003; ). Flagellum-mediated adhesion by Burkholderia pseudomallei precedes invasion of Acanthamoeba astronyxis. Infect Immun 71, 2280–2282.[CrossRef]
    [Google Scholar]
  47. Johnson, R. C., Ferber, D. M. & Ely, B. ( 1983; ). Synthesis and assembly of flagellar components by Caulobacter crescentus motility mutants. J Bacteriol 154, 1137–1144.
    [Google Scholar]
  48. Josenhans, C., Ferrero, R. L., Labigne, A. & Suerbaum, S. ( 1999; ). Cloning and allelic exchange mutagenesis of two flagellin genes of Helicobacter felis. Mol Microbiol 33, 350–362.[CrossRef]
    [Google Scholar]
  49. Josenhans, C., Vossebein, L., Friedrich, S. & Suerbaum, S. ( 2002; ). The neuA/flmD gene cluster of Helicobacter pylori is involved in flagellar biosynthesis and flagellin glycosylation. FEMS Microbiol Lett 210, 165–172.[CrossRef]
    [Google Scholar]
  50. Kalmokoff, M. L., Allard, S., Austin, J. W., Whitford, M. F., Hefford, M. A. & Teather, R. M. ( 2000; ). Biochemical and genetic characterisation of the flagellar filaments from the ruman anaerobe Butyrivibrio fibrisolvens OR77. Anaerobe 6, 93–109.[CrossRef]
    [Google Scholar]
  51. Karlyshev, A. V., Linton, D., Gregson, N. A. & Wren, B. W. ( 2002; ). A novel paralogous gene family involved in phase-variable flagella-mediated motility in Campylobacter jejuni. Microbiology 148, 473–480.
    [Google Scholar]
  52. Kauppi, A. M., Nordfelth, R., Uvell, H., Wolf-Watz, H. & Elofsson, M. ( 2003; ). Targeting bacterial virulence: inhibitors of type III secretion in Yersinia. Chem Biol 10, 241–249.[CrossRef]
    [Google Scholar]
  53. Kirov, S. M., Tassell, B. C., Semmler, A. B., O'Donovan, L. A., Rabaan, A. A. & Shaw, J. G. ( 2002; ). Lateral flagella and swarming motility in Aeromonas species. J Bacteriol 184, 547–555.[CrossRef]
    [Google Scholar]
  54. Krupski, G., Gotz, R., Ober, K., Pleier, E. & Schmitt, R. ( 1985; ). Structure of complex flagellar filaments in Rhizobium meliloti. J Bacteriol 162, 361–366.
    [Google Scholar]
  55. Leclerc, G., Wang, S. P. & Ely, B. ( 1998; ). A new class of Caulobacter crescentus flagellar genes. J Bacteriol 180, 5010–5019.
    [Google Scholar]
  56. Li, Z., Dumas, F., Dubreuil, D. & Jacques, M. ( 1993; ). A species-specific periplasmic flagellar protein of Serpulina (Treponema) hyodysenteriae. J Bacteriol 175, 8000–8007.
    [Google Scholar]
  57. Li, C., Motaleb, A., Sal, M., Goldstein, S. F. & Charon, N. W. ( 2000; ). Spirochete periplasmic flagella and motility. J Mol Microbiol Biotechnol 2, 345–354.
    [Google Scholar]
  58. Linton, D., Karlyshev, A. V., Hitchen, P. G., Morris, H. R., Dell, A., Gregson, N. A. & Wren, B. W. ( 2000; ). Multiple N-acetylneuraminic acid synthetase (neuB) genes in Campylobacter jejuni: identification and characterization of the gene involved in sialylation of lipo-oligosaccharide. Mol Microbiol 35, 1120–1134.[CrossRef]
    [Google Scholar]
  59. Logan, S. M., Trust, T. J. & Guerry, P. ( 1989; ). Evidence for posttranslational modification and gene duplication of Campylobacter flagellin. J Bacteriol 171, 3031–3038.
    [Google Scholar]
  60. Logan, S. M., Kelly, J. F., Thibault, P., Ewing, C. P. & Guerry, P. ( 2002; ). Structural heterogeneity of carbohydrate modifications affects serospecificity of Campylobacter flagellins. Mol Microbiol 46, 587–597.[CrossRef]
    [Google Scholar]
  61. Ly, T. M. & Muller, H. E. ( 1990; ). Ingested Listeria monocytogenes survive and multiply in protozoa. J Med Microbiol 33, 51–54.[CrossRef]
    [Google Scholar]
  62. Lyristis, M., Boynton, Z. L., Petersen, D., Kan, Z., Bennett, G. N. & Rudolph, F. B. ( 2000; ). Cloning, sequencing and characterisation of the gene encoding flagellin, flaC and the posttranslational modification of flagellin, FlaC from Clostridium acetobutylicum ATCC824. Anaerobe 6, 69–79.[CrossRef]
    [Google Scholar]
  63. Macnab, R. M. ( 2003; ). How bacteria assemble flagella. Annu Rev Microbiol 57, 77–100.[CrossRef]
    [Google Scholar]
  64. McCarter, L. L. ( 2001; ). Polar flagellar motility of the Vibrionaceae. Microbiol Mol Biol Rev 65, 445–462.[CrossRef]
    [Google Scholar]
  65. McCarter, L. L. ( 2004; ). Dual flagellar systems enable motility under different circumstances. J Mol Microbiol Biotechnol 7, 18–29.[CrossRef]
    [Google Scholar]
  66. Merkx-Jacques, A., Obhi, R. K., Bethune, G. & Creuzenet, C. ( 2004; ). The Helicobacter pylori flaA1 and wbpB genes control lipopolysaccharide and flagellum synthesis and function. J Bacteriol 186, 2253–2265.[CrossRef]
    [Google Scholar]
  67. Moens, S., Michiels, K. & Vanderleyden, J. ( 1995; ). Glycosylation of the flagellin of the polar flagellum of Azospirillium brazilense Sp7, a Gram-negative nitrogen-fixing bacterium. Microbiology 141, 2651–2657.[CrossRef]
    [Google Scholar]
  68. Newton, S. M., Joys, T. M., Anderson, S. A., Kennedy, R. C., Hovi, M. E. & Stocker, B. A. ( 1995; ). Expression and immunogenicity of an 18-residue epitope of HIV1 gp41 inserted in the flagellar protein of a Salmonella live vaccine. Res Microbiol 146, 203–216.[CrossRef]
    [Google Scholar]
  69. Nordfelth, R., Kauppi, A. M., Norberg, H. A., Wolf-Watz, H. & Elofsson, M. ( 2005; ). Small-molecule inhibitors specifically targeting type III secretion. Infect Immun 73, 3104–3114.[CrossRef]
    [Google Scholar]
  70. Obhi, R. K. & Creuzenet, C. ( 2005; ). Biochemical characterization of the Campylobacter jejuni Cj1294, a novel UDP-4-keto-6-deoxy-GlcNAc aminotransferase that generates UDP-4-amino-4,6-dideoxy-GalNAc. J Biol Chem 280, 20902–20908.[CrossRef]
    [Google Scholar]
  71. Ozin, A. J., Claret, L., Auvray, F. & Hughes, C. ( 2003; ). The FliS chaperone selectively binds the disordered flagellin C-terminal D0 domain central to polymerisation. FEMS Microbiol Lett 219, 219–224.[CrossRef]
    [Google Scholar]
  72. Pallen, M. J., Penn, C. W. & Chaudhuri, R. R. ( 2005; ). Bacterial flagellar diversity in the post-genomic era. Trends Microbiol 13, 143–149.[CrossRef]
    [Google Scholar]
  73. Parkhill, J., Wren, B. W., Mungall, K. & 18 other authors ( 2000; ). The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665–668.[CrossRef]
    [Google Scholar]
  74. Peel, M., Donachie, W. & Shaw, A. ( 1988; ). Physical and antigenic heterogeneity in the flagellins of Listeria monocytogenes and L. ivanovii. J Gen Microbiol 134, 2593–2598.
    [Google Scholar]
  75. Power, P. & Jennings, M. P. ( 2003; ). The genetics of glycosylation in Gram negative bacteria. FEMS Microbiol Lett 218, 211–222.[CrossRef]
    [Google Scholar]
  76. Rabaan, A. A., Gryllos, I., Tomas, J. M. & Shaw, J. G. ( 2001; ). Motility and the polar flagellum are required for Aeromonas caviae adherence to HEp-2 cells. Infect Immun 69, 4257–4267.[CrossRef]
    [Google Scholar]
  77. Rademaker, G. J. & Thomas-Oates, J. ( 1996; ). Analysis of glycoproteins and glycopeptides using fast-atom bombardment. Methods Mol Biol 61, 231–241.
    [Google Scholar]
  78. Salas, A. P., Zhu, L., Sanchez, C., Brana, A. F., Rohr, J., Mendez, C. & Salas, J. A. ( 2005; ). Deciphering the late steps in the biosynthesis of the anti-tumour indolocarbazole staurosporine: sugar donor substrate flexibility of the StaG glycosyltransferase. Mol Microbiol 58, 17–27.[CrossRef]
    [Google Scholar]
  79. Samatey, F. A., Imada, K., Vonderviszt, F., Shirakihara, Y. & Namba, K. ( 2000; ). Crystallization of the F41 fragment of flagellin and data collection from extremely thin crystals. J Struct Biol 132, 106–111.[CrossRef]
    [Google Scholar]
  80. Schaffer, C. & Messner, P. ( 2004; ). Surface-layer glycoproteins: an example for the diversity of bacterial glycosylation with promising impacts on nanobiotechnology. Glycobiology 14, 31R–42R.[CrossRef]
    [Google Scholar]
  81. Schirm, M., Soo, E. C., Aubry, A. J., Austin, J., Thibault, P. & Logan, S. M. ( 2003; ). Structural, genetic and functional characterization of the flagellin glycosylation process in Helicobacter pylori. Mol Microbiol 48, 1579–1592.[CrossRef]
    [Google Scholar]
  82. Schirm, M., Arora, S. K., Verma, A., Vinogradov, E., Thibault, P., Ramphal, R. & Logan, S. M. ( 2004a; ). Structural and genetic characterization of glycosylation of type a flagellin in Pseudomonas aeruginosa. J Bacteriol 186, 2523–2531.[CrossRef]
    [Google Scholar]
  83. Schirm, M., Kalmokoff, M., Aubry, A., Thibault, P., Sandoz, M. & Logan, S. M. ( 2004b; ). Flagellin from Listeria monocytogenes is glycosylated with beta-O-linked N-acetylglucosamine. J Bacteriol 186, 6721–6727.[CrossRef]
    [Google Scholar]
  84. Schirm, M., Schoenhofen, I. C., Logan, S. M., Waldron, K. C. & Thibault, P. ( 2005; ). Identification of unusual bacterial glycosylation by tandem mass spectrometry analyses of intact proteins. Anal Chem 77, 7774–7782.[CrossRef]
    [Google Scholar]
  85. Schoenhofen, I. C., McNally, D. J., Vinogradov, E., Whitfield, D., Young, M., Dick, S., Wakarchuk, W. W., Brisson, J.-R. & Logan, S. M. ( 2006; ). Functional characterisation of dehydratase/aminotransferase pairs from Helicobacter and Campylobacter: enzymes distinguishing the pseudaminic acid and bacillosamine biosynthetic pathways. J Biol Chem 281, 723–732.[CrossRef]
    [Google Scholar]
  86. Schuster, S. C. & Khan, S. ( 1994; ). The bacterial flagellar motor. Annu Rev Biophys Biomol Struct 23, 509–539.[CrossRef]
    [Google Scholar]
  87. Soo, E. C., Aubry, A. J., Logan, S. M., Guerry, P., Kelly, J. F., Young, N. M. & Thibault, P. ( 2004; ). Selective detection and identification of sugar nucleotides by CE-electrospray-MS and its application to bacterial metabolomics. Anal Chem 76, 619–626.[CrossRef]
    [Google Scholar]
  88. Szymanski, C. M. & Wren, B. W. ( 2005; ). Protein glycosylation in bacterial mucosal pathogens. Nat Rev Microbiol 3, 225–237.[CrossRef]
    [Google Scholar]
  89. Szymanski, C. M., Logan, S. M., Linton, D. & Wren, B. W. ( 2003; ). Campylobacter – a tale of two protein glycosylation systems. Trends Microbiol 11, 233–238.[CrossRef]
    [Google Scholar]
  90. Taguchi, F., Shimizu, R., Ikeda, Y., Inagaki, Y., Toyoda, K., Shiraishi, T. & Ichinose, Y. ( 2003; ). Post-translational modification of flagellin determines the specific induction of HR. Plant Physiol Biochem 44, 342–349.
    [Google Scholar]
  91. Takeuchi, K., Taguchi, F., Inagaki, Y., Toyoda, K., Shiraishi, T. & Ichinose, Y. ( 2003; ). Flagellin glycosylation island in Pseudomonas syringae pv glycinea and its role in host specificity. J Bacteriol 185, 6658–6665.[CrossRef]
    [Google Scholar]
  92. Thibault, P., Logan, S. M., Kelly, J. F., Brisson, J. R., Ewing, C. P., Trust, T. J. & Guerry, P. ( 2001; ). Identification of the carbohydrate moieties and glycosylation motifs in Campylobacter jejuni flagellin. J Biol Chem 276, 34862–34870.[CrossRef]
    [Google Scholar]
  93. Thomas, N. A., Bardy, S. L. & Jarrell, K. F. ( 2001; ). The archaeal flagellum: a different kind of prokaryotic motility structure. FEMS Microbiol Rev 25, 147–174.[CrossRef]
    [Google Scholar]
  94. Thomashow, L. S. & Rittenberg, S. C. ( 1985a; ). Isolation and composition of sheathed flagella from Bdellovibrio bacteriovorus 109J. J Bacteriol 163, 1047–1054.
    [Google Scholar]
  95. Thomashow, L. S. & Rittenberg, S. C. ( 1985b; ). Waveform analysis and structure of flagella and basal complexes from Bdellovibrio bacteriovorus 109J. J Bacteriol 163, 1038–1046.
    [Google Scholar]
  96. Thornley, J. P., Shaw, J. G., Gryllos, I. A. & Eley, E. ( 1997; ). Virulence properties of clinically significant Aeromonas species: evidence for pathogenicity. Rev Med Microbiol 8, 61–72.[CrossRef]
    [Google Scholar]
  97. Tomb, J. F., White, O., Kerlavage, A. R. & 22 other authors ( 1997; ). The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388, 539–547.[CrossRef]
    [Google Scholar]
  98. Totten, P. A. & Lory, S. ( 1990; ). Characterization of the type a flagellin gene from Pseudomonas aeruginosa PAK. J Bacteriol 172, 7188–7199.
    [Google Scholar]
  99. Trefzer, A., Salas, J. A. & Bechthold, A. ( 1999; ). Genes and enzymes involved in deoxysugar biosynthesis in bacteria. Nat Prod Rep 16, 283–299.[CrossRef]
    [Google Scholar]
  100. Voisin, S., Houliston, R. S., Kelly, J., Brisson, J. R., Watson, D., Bardy, S. L., Jarrell, K. F. & Logan, S. M. ( 2005; ). Identification and characterization of the unique N-linked glycan common to the flagellins and S-layer glycoprotein of Methanococcus voltae. J Biol Chem 280, 16586–16593.[CrossRef]
    [Google Scholar]
  101. Wieland, F., Paul, G. & Sumper, M. ( 1985; ). Halobacterial flagellins are sulfated glycoproteins. J Biol Chem 260, 15180–15185.
    [Google Scholar]
  102. Wysocki, V. H., Resing, K. A., Zhang, Q. & Cheng, G. ( 2005; ). Mass spectrometry of peptides and proteins. Methods 35, 211–222.[CrossRef]
    [Google Scholar]
  103. Wyss, C. ( 1998; ). Flagellins, but not endoflagellar sheath proteins, of Treponema pallidum and of pathogen-related oral spirochetes are glycosylated. Infect Immun 66, 5751–5754.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28735-0
Loading
/content/journal/micro/10.1099/mic.0.28735-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error