Functional characterization of WaaL, a ligase associated with linking O-antigen polysaccharide to the core of Pseudomonas aeruginosa lipopolysaccharide

Journal of Bacteriology

Volumn 187, Issue 9, 2005, Pages 3002-3012

  Abeyrathne, Priyanka D ^a   Daniels, Craig ^a,b   Poon, Karen K H ^a   Matewish, Mauricia J ^a   Lam, Joseph S ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; GLYCOSYLTRANSFERASE; LIGASE; LIPID A; O ANTIGEN;

AMINO ACID SEQUENCE; ANTIGEN STRUCTURE; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIUM MUTANT; CARBOHYDRATE SYNTHESIS; CELL MOTILITY; COVALENT BOND; CYTOPLASM; ENZYME ANALYSIS; GENE AMPLIFICATION; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERIZATION; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; WILD TYPE;

BACTERIAL PROTEINS; CARBON-OXYGEN LIGASES; CELL WALL; CLONING, MOLECULAR; GENE DELETION; GENETIC COMPLEMENTATION TEST; MUTATION; O ANTIGENS; POLYMERASE CHAIN REACTION; PSEUDOMONAS AERUGINOSA;

PSEUDOMONAS; PSEUDOMONAS AERUGINOSA; SALMONELLA ENTERICA;

EID: 17644381899     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.9.3002-3012.2005     Document Type: Article

References (64)

1. Abejrathne, P. D., and R. N. Nazar. 2000. Plasmid-enhanced strategy for PCR-mediated mutagenesis with difficult DNA templates. BioTechniques 29:1172-1176.
2. Alexander, D. C., and M. A. Valvano. 1994. Role of the rfe gene in the biosynthesis of the Escherichia coli O7-specific lipopolysaccharide and other O-specific polysaccharides containing N-acetylglucosamine. J. Bacteriol. 176:7079-7084.
3. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
4. Ausubel, F., R. Brent, R. Kingston, D. Moore, J. seidman, J. Smith, and K. Struhl. 1997. Preparation of genomic DNA from bacteria. In K. Struhl (ed.), Short protocols in molecular biology. John Wiley and Sons, New York, N.Y.
5. Bengoechea, J. A., H. Najdenski, and M. Skurnik. 2004. Lipopolysaccharide O antigen status of Yersinia enterocolitica O:8 is essential for virulence and absence of O antigen affects the expression of other Yersinia virulence factors. Mol. Microbiol. 52:451-469.
6. Bronner, D., B. R. Clarke, and C. Whitfield. 1994. Identification of an ATP-binding cassette transport system required for translocation of lipopolysaccharide O-antigen side-chains across the cytoplasmic membrane of Klebsiella pneumoniae serotype O1. Mol. Microbiol. 14:505-519.
7. Burrows, L. L., D. F. Charter, and J. S. Lam. 1996. Molecular characterization of the Pseudomonas aeruginosa serotype O5 (PAO1) B-band lipopolysaccharide gene cluster. Mol. Microbiol. 22:481-495.
8. Burrows, L. L., and J. S. Lam. 1999. Effect of wzx (rfbX) mutations on A-band and B-band lipopolysaccharide biosynthesis in Pseudomonas aeruginosa O5. J. Bacteriol. 181:973-980.
9. Daniels, C., C. Griffiths, B. Cowles, and J. S. Lam. 2002. Pseudomonas aeruginosa O-antigen chain length is determined before ligation to lipid A core. Environ. Microbiol. 4:883-897.
10. D'Aquila, R. T., L. J. Bechtel, J. A. Videler, J. J. Eron, P. Gorczyca, and J. C. Kaplan. 1991. Maximizing sensitivity and specificity of PCR by pre-amplification heating. Nucleic Acids Res. 19:3749.
11. Darzins, A. 1993. The pilG gene product, required for Pseudomonas aeruginosa pilus production and twitching motility, is homologous to the enteric, single-domain response regulator CheY. J. Bacteriol. 175:5934-5944.
12. de Kievit, T. R., T. Dasgupta, H. Schweizer, and J. S. Lam. 1995. Molecular cloning and characterization of the rfc gene of Pseudomonas aeruginosa (serotype O5). Mol. Microbiol. 16:565-574.
13. DiGiandomenico, A., M. J. Matewish, A. Bisaillon, J. R. Stehle, J. S. Lam, and P. Castric. 2002. Glycosylation of Pseudomonas aeruginosa 1244 pilin: glycan substrate specificity. Mol. Microbiol. 46:519-530.
14. Don, R. H., P. T. Cox, B. J. Wainwright, K. Baker, and J. S. Mattick. 1991. 'Touchdown' PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res. 19:4008.
15. Falt, I. C., E. K. Schweda, A. Weintraub, S. Sturm, K. N. Timmis, and A. A. Lindberg. 1993. Expression of the Shigella dysenteriae type-1 lipopolysaccharide repeating unit in Escherichia coli K12/Shigella dysenteriae type-1 hybrids. Eur. J. Biochem. 213:573-581.
16. Fomsgaard, A., M. A. Freudenberg, and C. Galanos. 1990. Modification of the silver staining technique to detect lipopolysaccharide in polyacrylamide gels. J. Clin. Microbiol. 28:2627-2631.
17. Fuchs-Cleveland, E., and C. Gilvarg. 1976. Oligomeric intermediate in peptidoglycan biosynthesis in Bacillus megaterium. Proc. Natl. Acad. Sci. USA 73:4200-4204.
18. Genevaux, P., P. Bauda, M. S. DuBow, and B. Oudega. 1999. Identification of Tn10 insertions in the rfaG, rfaP, and galU genes involved in lipopolysaccharide core biosynthesis that affect Escherichia coli adhesion. Arch. Microbiol. 172:1-8.
19. Gish, W., and D. J. States. 1993. Identification of protein coding regions by database similarity search. Nat. Genet. 3:266-272.
20. Govan, J. R, and V. Deretic. 1996. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60:539-574.
21. Hancock, R. E., and A. M. Carey. 1979. Outer membrane of Pseudomonas aeruginosa: heat-2-mercaptoethanol-modifiable proteins. J. Bacteriol. 140:902-910.
22. Heinrichs, D. E., M. A. Monteiro, M. B. Perry, and C. Whitfield. 1998. The assembly system for the lipopolysaccharide R2 core-type of Escherichia coli is a hybrid of those found in Escherichia coli K-12 and Salmonella enterica. Structure and function of the R2 WaaK and WaaL homologs. J. Biol. Chem. 273:8849-8859.
23. Heinrichs, D. E., J. A. Yethon, P. A. Amor, and C. Whitfield. 1998. The assembly system for the outer core portion of R1- and R4-type lipopolysaccharides of Escherichia coli. The R1 core-specific beta-glucosyltransferase provides a novel attachment site for O-polysaccharides. J. Biol. Chem. 273:29497-29505.
24. Heinrichs, D. E., J. A. Yethon, and C. Whitfield. 1998. Molecular basis for structural diversity in the core regions of the lipopolysaccharides of Escherichia coli and Salmonella enterica. Mol. Microbiol. 30:221-232.
25. Hitchcock, P. J., and T. M. Brown. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J. Bacteriol. 154:269-277.
26. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
27. Hoang, T. T., R. R. Karkhoff-Schweizer, A. J. Kutchma, and H. P. Schweizer. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
28. Jonsson, A. B., D. Ilver, P. Falk, J. Pepose, and S. Normark. 1994. Sequence changes in the pilus subunit lead to tropism variation of Neisseria gonorrhoeae to human tissue. Mol. Microbiol. 13:403-416.
29. Jonsson, A. B., G. Nyberg, and S. Normark. 1991. Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J. 10:477-488.
30. Kent, J. L., and M. J. Osborn. 1968. Properties of the O-specific hapten formed in vivo by mutant strains of Salmonella typhimurium. Biochemistry 7:4396-4408.
31. Kido, N., N. Morooka, N. Paeng, T. Ohtani, H. Kobayashi, N. Shibata, Y. Okawa, S. Suzuki, T. Sugiyama, and T. Yokochi. 1997. Production of monoclonal antibody discriminating serological difference in Escherichia coli O9 and O9a polysaccharides. Microbiol. Immunol. 41:519-525.
32. Kido, N., V. I. Torgov, T. Sugiyama, K. Uchiya, H. Sugihara, T. Komatsu, N. Kato, and K. Jann. 1995. Expression of the O9 polysaccharide of Escherichia coli: sequencing of the E. coli O9 rfb gene cluster, characterization of mannosyl transferases, and evidence for an ATP-binding cassette transport system. J. Bacteriol. 177:2178-2187.
33. Kielhofner, M., R. L. Atmar, R. J. Hamill, and D. M. Musher. 1992. Life-threatening Pseudomonas aeruginosa infections in patients with human immunodeficiency virus infection. Clin. Infect. Dis. 14:403-411.
34. Kirov, S. M. 2003. Bacteria that express lateral flagella enable dissection of the multifunctional roles of flagella in pathogenesis. FEMS. Microbiol. Lett. 224:151-159.
35. Klena, J. D., E. Pradel, and C. A. Schnaitman. 1992. Comparison of lipopolysaccharide biosynthesis genes rfaK, rfaL, rfaY, and rfaZ of Escherichia coli K-12 and Salmonella typhimurium. J. Bacteriol. 174:4746-4752.
36. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
37. Lightfoot, J., and J. S. Lam. 1993. Chromosomal mapping, expression and synthesis of lipopolysaccharide in Pseudomonas aeruginosa: a role for guanosine diphospho(GDP)-D-mannose. Mol. Microbiol. 8:771-782.
38. Liu, D., R. A. Cole, and P. R. Reeves. 1996. An O-antigen processing function for Wzx (RfbX): a promising candidate for O-unit flippase. J. Bacteriol. 178:2102-2107.
39. Makin, S. A., and T. J. Beveridge. 1996. The influence of A-band and B-band lipopolysaccharide on the surface characteristics and adhesion of Pseudomonas aeruginosa to surfaces. Microbiology 142:299-307.
40. Manning, P. A., M. W. Heuzenroeder, J. Yeadon, D. I. Leavesley, P. R. Reeves, and D. Rowley. 1986. Molecular cloning and expression in Escherichia coli K-12 of the O antigens of the Inaba and Ogawa serotypes of the Vibrio cholerae O1 lipopolysaccharides and their potential for vaccine development. Infect. Immun. 53:272-277.
41. Manning, P. A., U. H. Stroeher, L. E. Karageorgos, and R. Morona. 1995. Putative O-antigen transport genes within the rfb region of Vibrio cholerae O1 are homologous to those for capsule transport. Gene 158:1-7.
42. McMichael, J. C. 1992. Bacterial differentiation within Moraxella bovis colonies growing at the interface of the agar medium with the petri dish. J. Gen. Microbiol. 138:2687-2695.
43. Morona, R., M. H. Brown, J. Yeadon, M. W. Heuzenroeder, and P. A. Manning. 1991. Effect of lipopolysaccharide core synthesis mutations on the production of Vibrio cholerae O-antigen in Escherichia coli K-12. FEMS. Microbiol. Lett. 66:279-285.
44. Mulford, C. A., and M. J. Osborn. 1983. An intermediate step in translocation of lipopolysaccharide to the outer membrane of Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 80:1159-1163.
45. O'Toole, G., H. B. Kaplan, and R. Kolter. 2000. Biofilm formation as microbial development. Annu. Rev. Microbiol. 54:49-79.
46. O'Toole, G. A., and R. Kolter. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30:295-304.
47. Reeves, P. 1993. Evolution of Salmonella O antigen variation by interspecific gene transfer on a large scale. Trends Genet. 9:17-22.
48. Rick, P. D., G. L. Hubbard, and K. Barr. 1994. Role of the rfe gene in the synthesis of the O8 antigen in Escherichia coli K-12. J. Bacteriol. 176:2877-2884.
49. Rocchetta, H. L., L. L. Burrows, J. C. Pacan, and J. S. Lam. 1998. Three rhamnosyltransferases responsible for assembly of the A-band D-rhamnan polysaccharide in Pseudomonas aeruginosa: a fourth transferase, WbpL, is required for the initiation of both A-band and B-band lipopolysaccharide synthesis. Mol. Microbiol. 28:1103-1119.
50. Rocchetta, H. L., and J. S. Lam. 1997. Identification and functional characterization of an ABC transport system involved in polysaccharide export of A-band lipopolysaccharide in Pseudomonas aeruginosa. J. Bacteriol. 179:4713-4724.
51. Sadovskaya, I., J. R. Brisson, J. S. Lam, J. C. Richards, and E. Altman. 1998. Structural elucidation of the lipopolysaccharide core regions of the wild-type strain PAO1 and O-chain-deficient mutant strains AK1401 and AK1012 from Pseudomonas aeruginosa serotype O5. Eur. J. Biochem. 255:673-684.
52. Schweizer, H. D. 1993. Small broad-host-range gentamycin resistance gene cassettes for site-specific insertion and deletion mutagenesis. BioTechniques 15:831-834.
53. Schweizer, H. P., and T. T. Hoang. 1995. An improved system for gene replacement and xylE fusion analysis in Pseudomonas aeruginosa. Gene 158:15-22.
54. Senanayake, S. D., and D. A. Brian. 1995. Precise large deletions by the PCR-based overlap extension method. Mol. Biotechnol. 4:13-15.
55. Simon, R., U. Priefer, and A. Puhler. 1983. A broad-host-range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio/Technology 1:784-791.
56. Stover, C. K., X. Q. Pham, A. L. Erwin, S. D. Mizoguchi, P. Warrener, M. J. Hickey, F. S. Brinkman, W. O. Hufnagle, D. J. Kowalik, M. Lagrou, R. L. Garber, L. Goltry, E. Tolentino, S. Westbrock-Wadman, Y. Yuan, L. L. Brody, S. N. Coulter, K. R. Folger, A. Kas, K. Larbig, R. Lim, K. Smith, D. Spencer, G. K. Wong, Z. Wu, I. T. Paulsen, J. Reizer, M. H. Saier, R. E. Hancock, S. Lory, and M. V. Olson. 2000. Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Nature 406:959-964.
57. Szabo, M., D. Bronner, and C. Whitfield. 1995. Relationships between rfb gene clusters required for biosynthesis of identical D-galactose-containing O antigens in Klebsiella pneumoniae serotype O1 and Serratia marcescens serotype O16. J. Bacteriol. 177:1544-1553.
58. Toguchi, A., M. Siano, M. Burkart, and R. M. Harshey. 2000. Genetics of swarming motility in Salmonella enterica serovar typhimurium: critical role for lipopolysaccharide. J. Bacteriol. 182:6308-6321.
59. West, S. E., H. P. Schweizer, C. Dall, A. K. Sample, and L. J. Runyen-Janecky. 1994. Construction of improved Escherichia-Pseudomonas shuttle vectors derived from pUC18/19 and sequence of the region required for their replication in Pseudomonas aeruginosa. Gene 148:81-86.
60. Westphal, O., and K. Jann. 1965. Bacterial lipopolysaccharides: extraction with phenol-water and further applications of the procedure. Methods Carbohydr. Chem. 5:83-91.
61. Whitfield, C. 1995. Biosynthesis of lipopolysaccharide O antigens. Trends Microbiol. 3:178-185.
62. Whitfield, C., P. A. Amor, and R. Koplin. 1997. Modulation of the surface architecture of gram-negative bacteria by the action of surface polymer:lipid A-core ligase and by determinants of polymer chain length. Mol. Microbiol. 23:629-638.
63. Wright, A., M. Dankert, P. Fennessey, and P. W. Robbins. 1967. Characterization of a polyisoprenoid compound functional in O-antigen biosynthesis. Proc. Natl. Acad. Sci. USA 57:1798-1803.
64. Zhang, L., A. al-Hendy, P. Toivanen, and M. Skurnik. 1993. Genetic organization and sequence of the rfb gene cluster of Yersinia enterocolilica serotype O:3: similarities to the dTDP-L-rhamnose biosynthesis pathway of Salmonella and to the bacterial polysaccharide transport systems. Mol. Microbiol. 9:309-321.