Spontaneous and transient defence against bacteriophage by phase-variable glucosylation of O-antigen in Salmonella enterica serovar Typhimurium

Molecular Microbiology

Volumn 86, Issue 2, 2012, Pages 411-425

  Kim, Minsik ^a,b   Ryu, Sangryeol ^a,b  

^a Seoul National University   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; GALACTOSE; O ANTIGEN;

AMINO ACID SUBSTITUTION; ANTIGEN EXPRESSION; ANTIGEN FUNCTION; ANTIGENIC MODULATION; ANTIGENIC VARIATION; ARTICLE; BACTERIAL GENE; BACTERIOPHAGE; BTUB GENE; CONTROLLED STUDY; GENE MUTATION; GLYCOSYLATION; HOST RESISTANCE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA TYPHIMURIUM;

ANIMALS; BACTERIAL PROTEINS; BACTERIOPHAGES; GLYCOSYLATION; O ANTIGENS; RECEPTORS, VIRUS; SALMONELLA TYPHIMURIUM; VIRUS ATTACHMENT;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 84867461986     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08202.x     Document Type: Article

References (62)

1. Allison, G.E., and Verma, N.K. (2000) Serotype-converting bacteriophages and O-antigen modification in Shigella flexneri Trends Microbiol 8: 17-23.
2. Andrews, F.W. (1922) Studies in group agglutination I. The Salmonella group and its antigenic structure. J Pathol Bacteriol 25: 505-521.
3. Bogomolnaya, L.M., Santiviago, C.A., Yang, H.J., Baumler, A.J., and Andrews-Polymenis, H.L. (2008) 'Form variation' of the O12 antigen is critical for persistence of Salmonella Typhimurium in the murine intestine. Mol Microbiol 70: 1105-1119.
4. Broadbent, S.E., Davies, M.R., and van der Woude, M.W. (2010) Phase variation controls expression of Salmonella lipopolysaccharide modification genes by a DNA methylation-dependent mechanism. Mol Microbiol 77: 337-353.
5. Brussow, H., and Hendrix, R.W. (2002) Phage genomics: small is beautiful. Cell 108: 13-16.
6. Carey-Smith, G.V., Billington, C., Cornelius, A.J., Hudson, J.A., and Heinemann, J.A. (2006) Isolation and characterization of bacteriophages infecting Salmonella spp. FEMS Microbiol Lett 258: 182-186.
7. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
8. Ellermeier, C.D., Janakiraman, A., and Slauch, J.M. (2002) Construction of targeted single copy lac fusions using lambda Red and FLP-mediated site-specific recombination in bacteria. Gene 290: 153-161.
9. Erickson, M., Newman, D., Helm, R.A., Dino, A., Calcutt, M., French, W., and Eisenstark, A. (2009) Competition among isolates of Salmonella enterica ssp. enterica serovar Typhimurium: role of prophage/phage in archived cultures. FEMS Microbiol Lett 294: 37-44.
10. Fineran, P.C., Blower, T.R., Foulds, I.J., Humphreys, D.P., Lilley, K.S., and Salmond, G.P. (2009) The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc Natl Acad Sci USA 106: 894-899.
11. Fischer, C.R., Yoichi, M., Unno, H., and Tanji, Y. (2004) The coexistence of Escherichia coli serotype O157:H7 and its specific bacteriophage in continuous culture. FEMS Microbiol Lett 241: 171-177.
12. Guerrero-Ferreira, R.C., Viollier, P.H., Ely, B., Poindexter, J.S., Georgieva, M., Jensen, G.J., and Wright, E.R. (2011) Alternative mechanism for bacteriophage adsorption to the motile bacterium Caulobacter crescentus Proc Natl Acad Sci USA 108: 9963-9968.
13. Hantke, K. (1978) Major outer membrane proteins of E. coli K12 serve as receptors for the phages T2 (protein Ia) and 434 (protein Ib). Mol Gen Genet 164: 131-135.
14. Heller, K., and Braun, V. (1979) Accelerated adsorption of bacteriophage T5 to Escherichia coli F, resulting from reversible tail fiber-lipopolysaccharide binding. J Bacteriol 139: 32-38.
15. + via the L-shaped tail fibers. J Virol 41: 222-227.
16. Henderson, I.R., Owen, P., and Nataro, J.P. (1999) Molecular switches-the ON and OFF of bacterial phase variation. Mol Microbiol 33: 919-932.
17. Hyman, P., and Abedon, S.T. (2010) Bacteriophage host range and bacterial resistance. Adv Appl Microbiol 70: 217-248.
18. Kim, B.S., Hwang, J., Kim, M.H., and Choi, S.H. (2011) Cooperative regulation of the Vibrio vulnificus nan gene cluster by NanR protein, cAMP receptor protein, and N-acetylmannosamine 6-phosphate. J Biol Chem 286: 40889-40899.
19. Kim, M., and Ryu, S. (2011) Characterization of a T5-like coliphage, SPC35, and differential development of resistance to SPC35 in Salmonella enterica serovar Typhimurium and Escherichia coli Appl Environ Microbiol 77: 2042-2050.
20. Kocharunchitt, C., Ross, T., and McNeil, D.L. (2009) Use of bacteriophages as biocontrol agents to control Salmonella associated with seed sprouts. Int J Food Microbiol 128: 453-459.
21. Kong, Q., Yang, J., Liu, Q., Alamuri, P., Roland, K.L., and Curtiss, R., 3rd (2011) Effect of deletion of genes involved in lipopolysaccharide core and O-antigen synthesis on virulence and immunogenicity of Salmonella enterica serovar typhimurium. Infect Immun 79: 4227-4239.
22. Labrie, S.J., Samson, J.E., and Moineau, S. (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8: 317-327.
23. Lerouge, I., and Vanderleyden, J. (2002) O-antigen structural variation: mechanisms and possible roles in animal/plant-microbe interactions. FEMS Microbiol Rev 26: 17-47.
24. Lindberg, A.A. (1973) Bacteriophage receptors. Annu Rev Microbiol 27: 205-241.
25. Liu, M., Deora, R., Doulatov, S.R., Gingery, M., Eiserling, F.A., Preston, A., etal. (2002) Reverse transcriptase-mediated tropism switching in Bordetella bacteriophage. Science 295: 2091-2094.
26. 2 J Bacteriol 116: 847-856.
27. Marraffini, L.A., and Sontheimer, E.J. (2010) CRISPR interference: RNA-directed adaptive immunity in bacteria and archaea. Nat Rev Genet 11: 181-190.
28. Matic, I., Radman, M., and Rayssiguier, C. (1994) Structure of recombinants from conjugational crosses between Escherichia coli donor and mismatch-repair deficient Salmonella typhimurium recipients. Genetics 136: 17-26.
29. Merighi, M., Ellermeier, C.D., Slauch, J.M., and Gunn, J.S. (2005) Resolvase-in vivo expression technology analysis of the Salmonella enterica serovar Typhimurium PhoP and PmrA regulons in BALB/c mice. J Bacteriol 187: 7407-7416.
30. Miller, J.H. (1972) Assay of β-galactosidase. In Experiments in Molecular Genetics. Miller, J.H. (ed.). New York: Cold Spring Harbor Laboratory Press, pp. 352-355.
31. Nesper, J., Kapfhammer, D., Klose, K.E., Merkert, H., and Reidl, J. (2000) Characterization of Vibrio cholerae O1 antigen as the bacteriophage K139 receptor and identification of IS1004 insertions aborting O1 antigen biosynthesis. J Bacteriol 182: 5097-5104.
32. Nicholson, B., and Low, D. (2000) DNA methylation-dependent regulation of pef expression in Salmonella typhimurium Mol Microbiol 35: 728-742.
33. Nikaido, H., Nikaido, K., Nakae, T., and Makela, P.H. (1971) Glucosylation of lipopolysaccharide in Salmonella: biosynthesis of O antigen factor 12-2. I. Over-all reaction. J Biol Chem 246: 3902-3911.
34. Nikaido, K., and Nikaido, H. (1971) Glucosylation of lipopolysaccharide in Salmonella: biosynthesis of O antigen factor 12-2. II. Structure of the lipid intermediate. J Biol Chem 246: 3912-3919.
35. Nordstrom, K., and Forsgren, A. (1974) Effect of protein A on adsorption of bacteriophages to Staphylococcus aureus J Virol 14: 198-202.
36. Norris, T.L., Kingsley, R.A., and Bumler, A.J. (1998) Expression and transcriptional control of the Salmonella typhimurium Ipf fimbrial operon by phase variation. Mol Microbiol 29: 311-320.
37. Palva, E.T., and Makela, P.H. (1980) Lipopolysaccharide heterogeneity in Salmonella typhimurium analyzed by sodium dodecyl sulfate polyacrylamide gel electrophoresis. Eur J Biochem 107: 137-143.
38. Park, M., Lee, J.H., Shin, H., Kim, M., Choi, J., Kang, D.H., etal. (2012) Characterization and comparative genomic analysis of a novel bacteriophage SFP10 simultaneously inhibiting both Salmonella and Escherichia coli O157:H7. Appl Environ Microbiol 78: 58-69.
39. Pasharawipas, T., Wetchakit, N., and Sriurairatana, S. (2008) The cycle for a Siphoviridae-like phage (VHS1) of Vibrio harveyi is dependent on the physiological state of the host. Virus Res 135: 332-335.
40. Perry, L.L., SanMiguel, P., Minocha, U., Terekhov, A.I., Shroyer, M.L., Farris, L.A., etal. (2009) Sequence analysis of Escherichia coli O157:H7 bacteriophage PhiV10 and identification of a phage-encoded immunity protein that modifies the O157 antigen. FEMS Microbiol Lett 292: 182-186.
41. Philippe, N., Alcaraz, J.P., Coursange, E., Geiselmann, J., and Schneider, D. (2004) Improvement of pCVD442, a suicide plasmid for gene allele exchange in bacteria. Plasmid 51: 246-255.
42. Rakhuba, D.V., Kolomiets, E.I., Dey, E.S., and Novik, G.I. (2010) Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. Pol J Microbiol 59: 145-155.
43. Randall-Hazelbauer, L., and Schwartz, M. (1973) Isolation of the bacteriophage lambda receptor from Escherichia coli J Bacteriol 116: 1436-1446.
44. Reuhs, B.L., Geller, D.P., Kim, J.S., Fox, J.E., Kolli, V.S., and Pueppke, S.G. (1998) Sinorhizobium fredii and Sinorhizobium meliloti produce structurally conserved lipopolysaccharides and strain-specific K antigens. Appl Environ Microbiol 64: 4930-4938.
45. Riede, I., and Eschbach, M.L. (1986) Evidence that TraT interacts with OmpA of Escherichia coli FEBS Lett 205: 241-245.
46. Samuel, A.D., Pitta, T.P., Ryu, W.S., Danese, P.N., Leung, E.C., and Berg, H.C. (1999) Flagellar determinants of bacterial sensitivity to chi-phage. Proc Natl Acad Sci USA 96: 9863-9866.
47. Scholl, D., Adhya, S., and Merril, C. (2005) Escherichia coli K1's capsule is a barrier to bacteriophage T7. Appl Environ Microbiol 71: 4872-4874.
48. Scott, A.E., Timms, A.R., Connerton, P.L., Loc Carrillo, C., Adzfa Radzum, K., and Connerton, I.F. (2007) Genome dynamics of Campylobacter jejuni in response to bacteriophage predation. PLoS Pathog 3: e119.
49. Simon, R., Priefer, U., and Puhler, A. (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Bio-Technology 1: 784-791.
50. Slauch, J.M., Lee, A.A., Mahan, M.J., and Mekalanos, J.J. (1996) Molecular characterization of the oafA locus responsible for acetylation of Salmonella typhimurium O-antigen: oafA is a member of a family of integral membrane trans-acylases. J Bacteriol 178: 5904-5909.
51. Soncini, F.C., Vescovi, E.G., and Groisman, E.A. (1995) Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon. J Bacteriol 177: 4364-4371.
52. Sorek, R., and Stern, A. (2011) The phage-host arms race: Shaping the evolution of microbes. Bioessays 33: 43-51.
53. Sorensen, M.C., van Alphen, L.B., Harboe, A., Li, J., Christensen, B.B., Szymanski, C.M., and Brondsted, L. (2011) Bacteriophage F336 recognizes the capsular phosphoramidate modification of Campylobacter jejuni NCTC11168. J Bacteriol 193: 6742-6749.
54. Vander Byl, C., and Kropinski, A.M. (2000) Sequence of the genome of Salmonella bacteriophage P22. J Bacteriol 182: 6472-6481.
55. Vernikos, G.S., and Parkhill, J. (2006) Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands. Bioinformatics 22: 2196-2203.
56. Wang, L., Wang, Q., and Reeves, P.R. (2010a) The variation of O-antiges in Gram-negative bacteria. In Endotoxins: Structure, Function and Recognition. Wang, X., and Quinn, P.J. (eds). New York: Springer, pp. 123-152.
57. Wang, X., Zhang, C., Shi, F., and Hu, X. (2010b) Purification and characterization of lipopolysaccharides. In Endotoxins: Structure, Function and Recognition. Wang, X., and Quinn, P.J. (eds). New York: Springer, pp. 27-51.
58. van der Woude, M.W. (2006) Re-examining the role and random nature of phase variation. FEMS Microbiol Lett 254: 190-197.
59. van der Woude, M.W. (2011) Phase variation: how to create and coordinate population diversity. Curr Opin Microbiol 14: 205-211.
60. Yun, T.H., Cott, J.E., Tapping, R.I., Slauch, J.M., and Morrissey, J.H. (2009) Proteolytic inactivation of tissue factor pathway inhibitor by bacterial omptins. Blood 113: 1139-1148.
61. Zaleski, P., Wojciechowski, M., and Piekarowicz, A. (2005) The role of Dam methylation in phase variation of Haemophilus influenzae genes involved in defence against phage infection. Microbiology 151: 3361-3369.
62. Zieg, J., Silverman, M., Hilmen, M., and Simon, M. (1977) Recombinational switch for gene expression. Science 196: 170-172.