Type IV pilin is glycosylated in Pseudomonas syringae pv. tabaci 6605 and is required for surface motility and virulence

Molecular Plant Pathology

Volumn 13, Issue 7, 2012, Pages 764-774

  Nguyen, Linh Chi ^a   Taguchi, Fumiko ^a   Tran, Quang Minh ^a   Naito, Kana ^a   Yamamoto, Masanobu ^b   Ohnishi Kameyama, Mayumi ^b   Ono, Hiroshi ^b   Yoshida, Mitsuru ^b   Chiku, Kazuhiro ^b   Ishii, Tadashi ^b   Inagaki, Yoshishige ^a   Toyoda, Kazuhiro ^a   Shiraishi, Tomonori ^a   Ichinose, Yuki ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b NATIONAL FOOD RESEARCH INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FIMBRIA PROTEIN; FLAGELLIN;

ARTICLE; BACTERIAL GENE; BACTERIUM ADHERENCE; BIOFILM; CHEMISTRY; GENETICS; GLYCOSYLATION; METABOLISM; MOLECULAR GENETICS; MOVEMENT (PHYSIOLOGY); MUTATION; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PATHOGENICITY; PHYLOGENY; PHYSIOLOGY; PSEUDOMONAS SYRINGAE; TOBACCO; VIROLOGY; VIRULENCE;

BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; FIMBRIAE PROTEINS; FLAGELLIN; GENES, BACTERIAL; GLYCOSYLATION; MOLECULAR SEQUENCE DATA; MOVEMENT; MUTATION; OPEN READING FRAMES; PHYLOGENY; PSEUDOMONAS SYRINGAE; TOBACCO; VIRULENCE;

BACTERIA (MICROORGANISMS); LYCOPERSICON ESCULENTUM; NICOTIANA OBTUSIFOLIA; NICOTIANA TABACUM; PILA; PSEUDOMONAS SYRINGAE; PSEUDOMONAS SYRINGAE PV. TABACI;

EID: 84864379126     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2012.00789.x     Document Type: Article

References (44)

1. Aas, F.E., Vik, A., Vedde, J., Koomey, M. and Egge-Jacobsen, W. (2007) Neisseria gonorrhoeae O-linked pilin glycosylation: functional analyses define both the biosynthetic pathway and glycan structure. Mol. Microbiol. 65, 607-624.
2. Alexeyev, M.F., Shokolenko, I.N. and Croughan, T.P. (1995) New mini-Tn5 derivatives for insertion mutagenesis and genetic engineering in gram-negative bacteria. Can. J. Microbiol. 41, 1053-1055.
3. Bahar, O., Goffer, T. and Burdman, S. (2009) Type IV pili are required for virulence, twitching motility, and biofilm formation of Acidovorax avenae subsp. citrulli. Mol. Plant-Microbe Interact. 22, 909-920.
4. Benz, I. and Schmidt, M.A. (2002) Never say never again: protein glycosylation in pathogenic bacteria. Mol. Microbiol. 45, 267-276.
5. Burdman, S., Bahar, O., Parker, J.K. and Fuente, L. (2011) Involvement of type IV pili in pathogenicity of plant pathogenic bacteria. Genes 2, 706-735.
6. Castric, P. (1995) pilO, a gene required for glycosylation of Pseudomonas aeruginosa 1244 pilin. Microbiology, 141, 1247-1254.
7. Castric, P., Cassels, F.J. and Carlson, R.W. (2001) Structural characterization of the Pseudomonas aeruginosa 1244 pilin glycan. J. Biol. Chem. 276, 26479-26485; correction: 38, 36058.
8. Chiang, P. and Burrows, L.L. (2003) Biofilm formation by hyperpiliated mutants of Pseudomonas aeruginosa. J. Bacteriol. 185, 2374-2378.
9. Comer, J.E., Marshall, M.A., Blanch, V.J., Deal, C.D. and Castric, P. (2002) Identification of the Pseudomonas aeruginosa 1244 pilin glycosylation site. Infect. Immun. 70, 2837-2845.
10. DiGiandomenico, A., Matewish, M.J., Bisaillon, A., Stehle, J.R., Lam, J.S. and Castric, P. (2002) Glycosylation of Pseudomonas aeruginosa 1244 pilin: specificity of glycan substrate. Mol. Microbiol. 46, 519-530.
11. Harvey, H., Kus, J.V., Tessier, L., Kelly, J. and Burrows, L.L. (2011) Pseudomonas aeruginosad-arabinofuranose biosynthetic pathway and its role in type IV pilus assembly. J. Biol. Chem. 286, 28128-28137.
12. Ichinose, Y., Shimizu, R., Ikeda, Y., Taguchi, F., Marutani, M., Mukaihara, T., Inagaki, Y., Toyoda, K. and Shiraishi, T. (2003) Need for flagella for complete virulence of Pseudomonas syringae pv. tabaci: genetic analysis with flagella-defective mutants ΔfliC and ΔfliD in host tobacco plants. J. Gen. Plant Pathol. 69, 244-249.
13. Ichinose, Y., Taguchi, F., Nguyen, L.C., Naito, K., Suzuki, T., Inagaki, Y., Toyoda, K. and Shiraishi, T. (2011) Glycosylation of bacterial flagellins and its role in motility and virulence. In: Genome-Enabled Analysis of Plant-Pathogen Interactions (Wolpert, T., Shiraishi, T., Collmer, A., Glazebrook, J. and Akimitsu, K., eds), pp. 215-224. St. Paul, MN: APS Press.
14. Kus, J.V., Tullis, E., Cvitkovitch, D.G. and Burrows, L.L. (2004) Significant differences in type IV pilin allele distribution among Pseudomonas aeruginosa isolates from cystic fibrosis (CF) versus non-CF patients. Microbiology, 150, 1315-1326.
15. Kus, J.V., Kelly, J., Tessier, L., Harvey, H., Cvitkovitch, D.G. and Burrows, L.L. (2008) Modification of Pseudomonas aeruginosa Pa5196 type IV pilins at multiple sites with D-Araf by a novel GT-C family arabinosyltransferase, TfpW. J. Bacteriol. 190, 7464-7478.
16. Logan, S.M. (2006) Flagellar glycosylation-a new component of the motility repertoire? Microbiology, 152, 1249-1262.
17. Marceau, M. and Nassif, X. (1999) Role of glycosylation at Ser63 in production of soluble pilin in pathogenic Neisseria. J. Bacteriol. 181, 656-661.
18. Marceau, M., Forest, K., Beretti, J.L., Tainer, J. and Nassif, X. (1998) Consequences of the loss of O-linked glycosylation of meningococcal type IV pilin on piliation and pilus-mediated adhesion. Mol. Microbiol. 27, 705-715.
19. Mattick, J.S. (2002) Type IV pili and twitching motility. Annu. Rev. Microbiol. 56, 289-314.
20. Nguyen, L.C., Yamamoto, M., Ohnishi-Kameyama, M., Andi, S., Taguchi, F., Iwaki, M., Yoshida, M., Ishii, T., Konishi, T., Tsunemi, K. and Ichinose, Y. (2009) Genetic analysis of the genes involved in the synthesis of modified 4-amino-4, 6-dideoxyglucose in flagellin of Pseudomonas syringae pv. tabaci. Mol. Genet. Genomics, 282, 595-605.
21. Nudleman, E. and Kaiser, D. (2004) Pulling together with type IV pili. J. Mol. Microbiol. Biotechnol. 7, 52-62.
22. Parge, H.E., Forest, K.T., Hickey, M.J., Christensen, D.E., Getzoff, E.D. and Tainer, J.A. (1995) Structure of the fibre-forming protein pilin at 2.6 A resolution. Nature, 378, 32-38.
23. Power, P.M. and Jennings, M.P. (2003) The genetics of glycosylation in Gram-negative bacteria. FEMS Microbiol. Lett. 218, 211-222.
24. Power, P.M., Seib, K.L. and Jennings, M.P. (2006) Pilin glycosylation in Neisseria meningitidis occurs by a similar pathway to wzy-dependent O-antigen biosynthesis in Escherichia coli. Biochem. Biophys. Res. Commun. 347, 904-908.
25. Qutyan, M., Henkel, M., Horzempa, J., Quinn, M. and Castric, P. (2010) Glycosylation of pilin and nonpilin protein constructs by Pseudomonas aeruginosa 1244. J. Bacteriol. 192, 5972-5981.
26. Rico, A. and Preston, G.M. (2008) Pseudomonas syringae pv. tomato DC3000 uses constitutive and apoplast-induced nutrient assimilation pathways to catabolize nutrients that are abundant in the tomato apoplast. Mol. Plant-Microbe Interact. 21, 269-282.
27. Roine, E., Raineri, D.M., Romantschuk, M., Wilson, M. and Nunn, D.N. (1998) Characterization of type IV pilus genes in Pseudomonas syringae pv. tomato DC3000. Mol. Plant-Microbe Interact. 11, 1048-1056.
28. Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
29. Schäfer, A., Tauch, A., Jager, W., Kalinowski, J., Thierbach, G. and Puhler, A. (1994) Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene, 145, 69-73.
30. Simon, R., Priefer, U. and Pühler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Biotechnology, 1, 784-791.
31. Smedley, J.G. III, Jewell, E., Roguskie, J., Horzempa, J., Seyboldt, A., Stolz, D.B. and Castric, P. (2005) Influence of pilin glycosylation on Pseudomonas aeruginosa 1244 pilus function. J. Bacteriol. 73, 7922-7931.
32. Stimson, E., Virji, M., Makepeace, K., Dell, A., Morris, H.R., Payne, G., Saunders, J.R., Jennings, M.P., Barker, S. and Panico, M. (1995) Meningococcal pilin: a glycoprotein substituted with digalactosyl 2, 4-diacetamido-2, 4, 6-trideoxyhexose. Mol. Microbiol. 17, 1201-1214.
33. Strom, M.S. and Lory, S. (1993) Structure-function and biogenesis of the type IV pili. Annu. Rev. Microbiol. 47, 565-596.
34. Strom, M.S., Nunn, D.N. and Lory, S. (1993) A single bifunctional enzyme, PilD, catalyzes cleavage and N-methylation of proteins belonging to the type IV pilin family. Proc. Natl. Acad. Sci. USA, 90, 2404-2408.
35. Studholme, D.J. (2011) Application of high-throughput genome sequencing to intrapathovar variation in Pseudomonas syringae. Mol. Plant Pathol. 12, 829-838.
36. Taguchi, F. and Ichinose, Y. (2011) Role of type IV pili in virulence of Pseudomonas syringae pv. tabaci 6605: correlation of motility, multidrug resistance, and HR-inducing activity on a nonhost plant. Mol. Plant-Microbe Interact. 24, 1001-1011.
37. Psta from Pseudomonas syringae pv. tabaci is defective and deficient in its expression and HR-inducing activity. J. Gen. Plant Pathol. 67, 116-123.
38. Taguchi, F., Takeuchi, K., Katoh, E., Murata, K., Suzuki, T., Marutani, M., Kawasaki, T., Eguchi, M., Katoh, S., Kaku, H., Yasuda, C., Inagaki, Y., Toyoda, K., Shiraishi, T. and Ichinose, Y. (2006) Identification of glycosylation genes and glycosylated amino acids of flagellin in Pseudomonas syringae pv. tabaci. Cell. Microbiol. 8, 923-938.
39. Taguchi, F., Shibata, S., Suzuki, T., Ogawa, Y., Aizawa, S., Takeuchi, K. and Ichinose, Y. (2008) Effects of glycosylation on swimming ability and flagella polymorphic transformation of Pseudomonas syringae pv. tabaci 6605. J. Bacteriol. 190, 764-768.
40. Taguchi, F., Takeuchi, K., Inagaki, Y., Toyoda, K., Shiraishi, T. and Ichinose, Y. (2009) Glycosylation of flagellin from Pseudomonas syringae pv. tabaci 6605 contributes to evasion of host tobacco plant surveillance system. Physiol. Mol. Plant Pathol. 74, 11-17.
41. Virji, M., Saunders, J.R., Sims, G., Makepeace, K., Maskell, D. and Ferguson, D.J.P. (1993) Pilus-facilitated adherence of Neisseria meningitidis to human epithelial and endothelial cells: modulation of adherence phenotype occurs concurrently with changes in primary amino acid sequence and the glycosylation status of pilin. Mol. Microbiol. 10, 1013-1028.
42. Voisin, S., Kus, J.V., Houliston, S., St-Michael, F., Watson, D., Cvitkovitch, D.G., Kelly, J., Brisson, J.R. and Burrows, L.L. (2007) Glycosylation of Pseudomonas aeruginosa strain Pa5196 type IV pilins with mycobacterium-like α-1, 5-linked D-Araf oligosaccharides. J. Bacteriol. 189, 151-159.
43. Yamamoto, M., Ohnishi-Kameyama, M., Nguyen, L.C., Taguchi, F., Chiku, K., Ishii, T., Ono, H., Yoshida, M. and Ichinose, Y. (2011) Identification of genes involved in the glycosylation of modified viosamine of flagellins in Pseudomonas syringae by mass spectrometry. Genes, 2, 788-803.
44. Zdorovenko, G.M., Solyanik, L.P., Yahovleva, L.M. and Paramonov, N.A. (1997) Characterization of O-antigens from different strains of Pseudomonas syringae pv. tabaci. Biochemistry (Moscow), 62, 28-37.