Chapter 8 : Prophage Arsenal of Serovar Typhimurium

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The emergence in the last two decades of new epidemic strains with enhanced virulence traits is indicative of the fast pace of the evolutionary process. This chapter reviews the evidence pointing to a central role played by temperate phages in the dissemination of virulence determinants in the complex. The lysogenic condition of most strains was recognized prior to an understanding of the genetic bases of lysogeny. Early studies also indicated that some genes of certain prophages escape lysogenic repression and express functions that modify the host bacterium. Since phage and chromosomal sequences near the attachment sites of most prophages are conserved, PCR can be used to assess the phage occupancy of these sites. This approach is particularly attractive because the reaction can be designed in such a way as to always give a signal, and the presence or absence of the prophage can be deduced from the size of the amplified fragment. Preliminary analyses confirmed that the sequences of the three prophages diverge considerably in the portion corresponding to the immunity module. serovar Typhimurium expresses a second periplasmic [Cu, Zn] superoxide dismutase, SodC2, which is encoded by a chromosomal gene. A disruption of the locus was shown to render serovar Typhimurium more virulent in mice.

Citation: Bossi L, Figueroa-Bossi N. 2005. Prophage Arsenal of Serovar Typhimurium, p 165-186. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch8

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Type III Secretion System
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Image of FIGURE 1

Schematic diagram showing the prophages in the serovar Typhimurium chromosome.The prophage left-right orientation (L/R) is shown according to the convention used for the prophage map of bacteriophage lambda ( ). Genetic symbols specify the genes flanking the insertion sites, with arrows indicating their orientations. An asterisk on the left or right side of the symbol indicates that the gene is truncated at its 5′ end or its 3′ end, respectively.

Citation: Bossi L, Figueroa-Bossi N. 2005. Prophage Arsenal of Serovar Typhimurium, p 165-186. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch8
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Image of FIGURE 2

Immunity relationships among Gifsy phages from three representative strains of serovar Typhimurium. Phages isolated from the indicated strains were used to infect strains that carried or lacked their resident Gifsy prophages. Open circles, phage forms plaques on the strain carrying the specified prophage; closed circles, phage does not form plaques unless the strain is cured of the specified prophage. Phage Gifsy-2 could not be obtained from strains LT2 and SL1344.

Citation: Bossi L, Figueroa-Bossi N. 2005. Prophage Arsenal of Serovar Typhimurium, p 165-186. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch8
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1. Ackermann, H.W. 1998.Tailed bacteriophages: the order Caudovirales. Adv.Virus Res. 51:135201.
2. Alonso, A. M. G. Pucciarelli,, N. Figueroa-Bossi, and F. García del Portillo. Increased excision of the Salmonella defective prophage ST64B caused by a deficiency in Dam methylase. Submitted for publication.
3. Ammendola, S.,, N. Figueroa-Bossi,, A. Battistoni,, and L. Bossi. Unpublished data.
4. Anderson, E. S.,, L.R. Ward,, M. J. de Saxe,, and J. D. de Sa. 1977. Bacteriophage-typing designations of Salmonella typhimurium. J.Hyg. 78:297300.
5. Bacciu, D.,, G. Falchi,, A. Spazziani,, L. Bossi,, G. Marogna,, G. S. Leori,, S. Rubino,, and S. Uzzau. 2004.Transposition of the heat-stable toxin astA gene into a gifsy-2-related prophage of Salmonella enterica serovar Abortusovis. J. Bacteriol. 186:45684574.
6. Bakshi, C. S.,, V. P. Singh,, M.W. Wood,, P.W. Jones,, T. S. Wallis,, and E. E. Galyov. 2000. Identification of SopE2, a Salmonella secreted protein which is highly homologous to SopE and involved in bacterial invasion of epithelial cells. J. Bacteriol. 182:23412344.
7. Bäumler, A. J. 1997. The record of horizontal gene transfer in Salmonella.Trends Microbiol. 5:318322.
8. Bäumler, A. J.,, R. M. Tsolis,, T. A. Ficht,, and L. G. Adams. 1998. Evolution of host adaptation in Salmonella enterica. Infect. Immun. 66:45794587.
9. Beltran, P.,, S. A. Plock,, N. H. Smith,, T. S. Whittam,, D.C. Old,, and R. K. Selander. 1991. Reference collections of strains of the Salmonella typhimurium complex from natural sources. J. Gen. Microbiol. 137:601606.
10. Blanc-Potard, A. B.,, and E. A. Groisman. 1997.The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J. 16:53765385.
11. Blattner, F. R.,, G. Plunkett III,, C. A. Bloch,, N.T. Perna,, V. Burland,, M. Riley,, J. Collado-Vides,, J.D. Glasner,, C.K. Rode,, G. F. Mayhew,, J. Gregor,, N. W. Davis,, H. A. Kirkpatrick,, M.A. Goeden,, D. J. Rose,, B. Mau,, and Y. Shao. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:14531474.
12. Bossi, L.,, J. A. Fuentes,, G. Mora,, and N. Figueroa-Bossi. 2003. Prophage contribution to bacterial population dynamics. J. Bacteriol. 185:64676471.
13. Botstein, D. 1980.A theory of modular evolution for bacteriophages.Ann.N.Y.Acad.Sci.354:484491.
14. Boyd, J. S. 1950.The symbiotic bacteriophages of Salmonella typhi-murium. J. Pathol. Bacteriol. 62:501517.
15. Brody, H.,, and C.W. Hill. 1988.Attachment site of the genetic element e14. J. Bacteriol. 170:20402044.
16. Brumby, A. M.,, I. Lamont,, I. B. Dodd,, and J. B. Egan. 1996. Defining the SOS operon of coliphage 186. Virology 219:105114.
17. Bueno, S. M.,, C.A. Santiviago,, A.A. Murillo,, J. A. Fuentes,, A. N. Trombert,, P. I. Rodas,, P. Youderian,, and G. C. Mora. 2004. Precise excision of the large pathogenicity island, SPI7, in Salmonella enterica serovar Typhi. J. Bacteriol. 186:32023213.
18. Bumann, D. 2002. Examination of Salmonella gene expression in an infected mammalian host using the green fluorescent protein and two-colour flow cytometry. Mol. Microbiol. 43:12691283.
19. Bunny, K.,, J. Liu,, and J. Roth. 2002. Phenotypes of lexA mutations in Salmonella enterica: evidence for a lethal lexA null phenotype due to the Fels-2 prophage. J. Bacteriol. 184:62356249.
20. Casjens, S. Personal communication.
21. Casjens, S.,, G. Hatfull,, and R. Hendrix. 1992. Evolution of the dsDNA tailed-bacteriophage genomes. Semin.Virol. 3:383397.
22. Chai, S.,, L. Bossi,, and F. Heffron. Unpublished data.
23. Collazo, C. M.,, and J. E. Galán. 1997.The invasion- associated type-III protein secretion system in Salmonella. Gene 192:5159.
23a.. Coombes, B. K.,, M. E. Wickham,, N. F. Brown,, S. Lemire,, L. Bossi,, W. W. Hsiao,, F. S. Brinkman,, and B. Finlay. Genetic and molecular analysis of GogB, a phage-encoded type III-secreted substrate in Salmonella enterica serovar Typhimurium with autonomous expression from its associated phage. J. Mol. Biol., in press.
24. Daniels, D. L.,, J. L. Schroeder,, W. Szybalski,, F. Sanger,, and F. R. Blattner,. 1983. A molecular map of coliphage lambda, p. 469676. In R.W. Hendrix,, J.W. Roberts,, F.W. Stahl,, and R.A. Weisberg (ed.), Lambda II. Cold Spring Harbor Laboratory, Cold Spring Harbor,N.Y.
25. Datsenko, K.A.,, and B. L. Wanner. 2000.One-step inactivation of chromosomal genes in Escherichia coli K12 using PCR products. Proc. Natl.Acad. Sci. USA 97:66406645.
26. De Groote, M. A.,, U. A. Ochsner,, M. U. Shiloh,, C. Nathan,, J. M. McCord,, M. C. Dinauer,, S. J. Libby,, A. Vazquez-Torres,, Y. Xu,, and F.C. Fang. 1997.Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. Proc. Natl.Acad. Sci. USA 94:1399714001.
27. Deng, W.,, S.-R. Liou,, G. Plunkett III,, G. F. Mayhew,, D. J. Rose,, V. Burland,, V. Kodoyianni,, D. C. Schwartz,,and F.R. Blattner. 2003.Comparative genomics of Salmonella enterica serovarTyphi strainsTy2 and CT18.J. Bacteriol.185:23302337.
28. Dodd, I. B.,, M.R. Reed,, and J. B. Egan. 1993. The Cro-like repressor of coliphage 186 is required for prophage excision and binds near the phage attachment site. Mol. Microbiol. 10:11391150.
29. Effantin G.,, N. Figueroa-Bossi,, L. Bossi,, and J. Conway. Unpublished data.
30. Fang, F. C.,, M.A. DeGroote,, J.W. Foster,, A. J. Bäumler,, U. Ochsner,, T. Testerman,, S. Bearson,, J. C. Giard,, Y. Xu,, G. Campbell,, and T. Laessig. 1999.Virulent Salmonella typhimurium has two periplasmic Cu, Zn-superoxide dismutases. Proc. Natl.Acad. Sci. USA 96:75027507.
31. Farrant, J. L.,, A. Sansone,, J. R. Canvin,, M. J. Pallen,, P. R. Langford,, T. S. Wallis,, G. Dougan,, and J. S. Kroll. 1997. Bacterial copper- and zinc-cofactored superoxide dismutase contributes to the pathogenesis of systemic salmonellosis. Mol. Microbiol. 25:785796.
32. Fields, P. I.,, R.V. Swanson,, C.G. Haidaris,, and F. Heffron. 1986. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc. Natl.Acad. Sci.USA 83:51895193.
33. Figueroa-Bossi, N.,, E. Coissac,, P. Netter,, and L. Bossi. 1997. Unsuspected prophage-like elements in Salmonella typhimurium. Mol. Microbiol. 25:161173.
34. Figueroa-Bossi, N.,, and L. Bossi. 1999. Inducible prophages contribute to Salmonella virulence in mice. Mol. Microbiol. 33:167176.
35. Figueroa-Bossi, N.,, S. Uzzau,, D. Maloriol,,and L. Bossi. 2001.Variable assortment of prophages provides a transferable repertoire of pathogenic determinants in Salmonella.Mol.Microbiol.39:260272.
36. Figueroa-Bossi, N.,, and L. Bossi. 2004. Resuscitation of a defective prophage in Salmonella cocultures. J. Bacteriol. 186:40384041.
37. Figueroa-Bossi, N.,, F.-X. Weill,., P. Grimont,, and L. Bossi. Unpublished data.
38. Figueroa-Bossi, N.,, and L. Bossi. Lysogenic relay: dislodgement of the Fels-2 prophage by the SopE_ phage. Submitted for publication.
39. Figueroa-Bossi, N.,, and L. Bossi. Unpublished data.
40. Galán, J. E. 2001. Salmonella interaction with host cells: type III secretion at work. Annu. Rev. Cell. Dev. Biol. 17:5386.
41. Galen, J. E.,, J. M. Ketley,, A. Fasano,, S. H. Richardson,, S. S. Wasserman,, and J. B. Kaper. 1992. Role of Vibrio cholerae neuraminidase in the function of cholera toxin. Infect.Immun. 60:406415.
42. Godoy, V. G.,, M. M. Dallas,, T. A. Russo,, and M. H. Malamy. 1993.A role for Bacteroides fragilis neuraminidase in bacterial growth in two model systems. Infect. Immun. 61:44154426.
43. Groisman, E.A.,, and H. Ochman. 1996.Pathogenicity islands: bacterial evolution in quantum leaps. Cell 87:791794.
44. Groisman, E.A.,, and H. Ochman. 1997.How Salmonella became a pathogen. Trends Microbiol. 5:343349.
45. Gunn, J. S.,, C. M. Alpuche-Aranda,, W. P. Loomis,, W. J. Belden,, and S. I. Miller. 1995. Characterization of the Salmonella typhimurium pagC/pagD chromosomal region. J. Bacteriol. 177:50405047.
46. Gunn, J. S.,, W. J. Belden,, and S. I. Miller. 1998. Identification of PhoP-PhoQ activated genes within a duplicated region of the Salmonella typhimurium chromosome. Microb. Pathog. 25:7790.
47. Hacker, J.,, G. Blum-Oehler,, I. Muhldorfer,, and H. Tschäpe. 1997. Pathogenicity islands of virulent bacteria: structure, function and impact on microbial evolution. Mol. Microbiol. 23:10891097.
48. Harada, K.,, M. Kameda,, M. Suzuki,, and S. Mitsuhashi. 1964. Mutant of Salmonella phage epsilon 34 with loss of converting ability. Jpn. J. Microbiol. 19:125130.
49. Haraga, A.,,and S. I. Miller. 2003.A Salmonella enterica serovarTyphimurium translocated leucine-rich repeat effector protein inhibits NF-κB-dependent gene expression. Infect. Immun. 71:40524058.
50. Hardt, W.-D.,, and J. E. Galan. 1997.A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria. Proc. Natl. Acad. Sci. USA 94:98879892.
51. Hardt, W.-D.,, H. Urlaub,, and J. E. Galán. 1998. A substrate of the centisome 63 type III protein secretion system of Salmonella typhimurium is encoded by a cryptic bacteriophage. Proc. Natl. Acad. Sci. USA 95:25742579.
52. Hardt, W.-D.,, L. M. Chen,, K. E. Schuebel,, X. R. Bustelo,, and J. E. Galan. 1998. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 93:815826.
53. Heffernan, E. J.,, J. Harwood,, J. Fierer,, and D. Guiney. 1992. The Salmonella typhimurium virulence plasmid complement resistance gene rck is homologous to a family of virulence-related outer membrane protein genes, including pagC and ail. J. Bacteriol. 174:8491.
54. Hendrix, R.,, M.C. Smith,, R.N. Burns,, M. E. Ford,, and G. F. Hatfull. 1999. Evolutionary relationships among diverse bacteriophages and prophages: all the world’s a phage. Proc. Natl.Acad. Sci. USA 96:21922197.
55. Hendrix, R.W.,, J. G. Lawrence,, G. F. Hatfull,, and S. Casjens. 2000. The origins and ongoing evolution of viruses. Trends Microbiol. 8:504508.
56. Hill, C.W.,, J. A. Gray,, and H. Brody. 1989. Use of the isocitrate dehydrogenase structural gene for attachment of e14 in Escherichia coli K-12. J. Bacteriol. 171:40834084.
57. Ho, T.D.,, and J. M. Slauch. 2001. OmpC is the receptor for Gifsy-1 and Gifsy-2 bacteriophages of Salmonella. J. Bacteriol. 183:14951498.
58. Ho, T. D.,, and J. M. Slauch. 2001. Characterization of grvA, an antivirulence gene on the Gifsy-2 phage in Salmonella enterica serovar Typhimurium. J. Bacteriol. 183:611620.
59. Ho, T. D.,, N. Figueroa-Bossi,, M. Wang,, S. Uzzau,, L. Bossi,, and J. M. Slauch. 2002. Identification of GtgE, a novel virulence factor encoded on the Gifsy-2 bacteriophage of Salmonella enterica serovar Typhimurium. J. Bacteriol. 184:52345239.
60. Hochhut, B.,, and M. K. Waldor. 1999. Site-specific integration of the conjugal Vibrio cholerae SXT element into prfC. Mol. Microbiol. 32:99110.
61. Hoiseth, S. K.,, and B. A. D. Stocker. 1981. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291:238239.
62. Hoyer, L. L.,, A. C. Hamilton,, S. M. Steenbergen,, and E. R. Vimr. 1992. Cloning, sequencing and distribution of the Salmonella typhimurium LT2 sialidase gene, nanH, provides evidence for interspecies gene transfer. Mol. Microbiol. 6:873884.
63. Iseki, S.,, and K. Kashiwagi. 1955. Induction of somatic antigen 1 by bacteriophage in Salmonella group B. Proc. Jpn.Acad. 31:558564.
64. Jost, B. H.,, J. G. Songer,, and S. J. Billington. 2002. Identification of a second Arcanobacterium pyogenes neuraminidase and involvement of neuraminidase activity in host cell adhesion. Infect. Immun. 70:11061112.
65. Juhala, R. J.,, M. E. Ford,, R. L. Duda,, A. Youlton,, G. F. Hatfull,, and R.W. Hendrix. 2000.Genetic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J. Mol. Biol. 299:2751.
66. Kamp, D.,, R. Kahmann,, D. Zipser,, T.R. Broker,, and L. T. Chow. 1978. Inversion of the G DNA segment of phage Mu controls phage infectivity. Nature 271:577580.
67. Karaolis, D. K.,, J. A. Johnson,, C. C. Bailey,, E. C. Boedeker,, J. B. Kaper,, and P. R. Reeves. 1998.A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. Proc. Natl. Acad. Sci. USA 95:31343139.
68. Kingsley, R. A.,, and A. J. Bäumler. 2000. Host adaptation and the emergence of infectious disease: the Salmonella paradigm. Mol. Microbiol. 36: 10061014.
69. Kingsley, R.A.,, and A. J. Bäumler. 2002.Pathogenicity islands and host adaptation of Salmonella serovars. Curr.Top. Microbiol. Immunol. 264:6787.
70. Kirby, J. E.,, J. E. Trempy,, and S. Gottesman. 1994. Excision of a P4-like cryptic prophage leads to Alp protease expression in Escherichia coli. J. Bacteriol. 176:20682081.
71. Krishnakumar, R.,, M. Craig,, J. A. Imlay,, and J. M. Slauch. 2004. Differences in enzymatic properties allow SodCI but not SodCII to contribute to virulence in Salmonella enterica serovar Typhimurium strain 14028. J. Bacteriol. 186:52305238.
72. Kushner, S. R.,, H. Nagaishi,, and A. J. Clark. 1974. Isolation of exonuclease VIII: the enzyme associated with sbcA indirect suppressor. Proc. Natl. Acad. Sci. USA 71:35933597.
73. Lamont, I.,, A. M. Brumby,, and J. B. Egan. 1989. UV induction of coliphage 186: prophage induction as an SOS function. Proc. Natl.Acad. Sci. USA 86:54925496.
74. Lemire S.,, N. Figueroa-Bossi,, and L. Bossi. Unpublished data.
75. Lemire S.,, N. Figueroa-Bossi,, and L. Bossi. Genetic interactions between the Gifsy-1 and Gifsy-2 prophages of Salmonella enterica serovar Typhimurium. Submitted for publication.
76. Leong, J. M.,, S. Nunes-Duby,, C. F. Lesser,, P. Youderian,, M. M. Susskind,, and A. Landy. 1985.The phi 80 and P22 attachment sites. Primary structure and interaction with Escherichia coli integration host factor. J. Biol. Chem. 260:44684477.
77. Lilleengen, K. 1948. Typing of Salmonella typhimurium by means of bacteriophage. Acta Pathol. Microbiol. Scand. 77(Suppl.):2125.
78. Lin-Chao, S.,, C.-L. Wei,, and Y.-T. Lin. 1999. RNase E is required for the maturation of ssrA RNA and normal ssrA RNA peptide-tagging activity. Proc. Natl.Acad. Sci. USA 96:1240612411.
79. Lloyd, R.G.,, and S.D. Barbour. 1974.The genetic location of the sbcA gene of Escherichia coli. Mol. Gen. Genet. 134:157171.
80. Low, K. B. 1973. Restoration by the Rac locus of recombinant-forming ability in recB and recC merozygotes of Escherichia coli. Mol. Gen. Genet. 122:119130.
81. March, P. E.,, and M. Inouye. 1985. Characterization of the lep operon of Escherichia coli.Identification of the promoter and the gene upstream of the signal peptidase I gene.J.Biol.Chem.260:72067213.
82. March, P. E.,, and M. Inouye. 1985. GTP-binding membrane protein of Escherichia coli with sequence homology to initiation factor 2 and elongation factors Tu and G. Proc. Natl. Acad. Sci. USA 82:75007504.
83. McClelland, M.,, K. E. Sanderson,, J. Spieth,, S.W. Clifton,, P. Latreille,, L. Courtney,, S. Porwollik,, J. Ali,, M. Dante,, F. Du,, S. Hou,, D. Layman,, S. Leonard,, C. Nguyen,, K. Scott,, A. Holmes,, N. Grewal,, E. Mulvaney,, E. Ryan,, H. Sun,, L. Florea,, W. Miller,, T. Stoneking,, M. Nhan,, R. Waterston,, and R. K. Wilson. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413:852856.
84. Miao, E. A.,, C.A. Scherer,, R.M. Tsolis,, R.A. Kingsley,, L. G. Adams,, A. J. Baumler,, and S. I. Miller. 1999. Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol. Microbiol. 34:850864.
85. Miao, E. A.,, and S. I. Miller. 2000.A conserved amino acid sequence directing intracellular type III secretion by Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 97:75397544.
86. Miao, E. A.,, M. Brittnacher,, A. Haraga,, R. L. Jeng,, M. D. Welch,, and S. I. Miller. 2003. Salmonella effectors translocated across the vacuolar membrane interact with the actin cytoskeleton. Mol. Microbiol. 48:401415.
87. Miller, V. L.,, and J. J. Mekalanos. 1988.A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J. Bacteriol. 170:25752583.
88. Mirold, S.,, W. Rabsch,, M. Rohde,, S. Stender,, H. Tschäpe,, H. Rüssmann,, E. Igwe,, and W.-D. Hardt. 1999. Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. Proc. Natl.Acad. Sci. USA 96:98459850.
89. Mirold, S.,, W. Rabsch,, H. Tschäpe,, and W.-D. Hardt. 2001.Transfer of the Salmonella type III effector sopE between unrelated phage families. J. Mol. Biol. 312:716.
90. Mirold, S.,, K. Ehrbar,, A. Weissmuller,, R. Prager,, H. Tschäpe,, H. Russmann,, and W.-D. Hardt. 2001. Salmonella host cell invasion emerged by acquisition of a mosaic of separate genetic elements, including Salmonella pathogenicity island 1 (SPI1), SPI5, and sopE2. J. Bacteriol. 183:23482358.
91. Mizan, S.,, A. Henk,, A. Stallings,, M. Maier,, and M. D. Lee. 2000. Cloning and characterization of sialidases with 2-6' and 2-3' sialyl lactose specificity from Pasteurella multocida. J. Bacteriol. 182:68746883.
92. Mmolawa, P.T.,, R. Willmore,, C. J. Thomas,, and M. W. Heuzenroeder. 2002. Temperate phages in Salmonella enterica serovar Typhimurium: implications for epidemiology. Int. J. Med. Microbiol. 291:633644.
93. Mmolawa, P. T.,, H. Schmieger,, and M.W. Heuzenroeder. 2003. Bacteriophage ST64B, a genetic mosaic of genes from diverse sources isolated from Salmonella enterica serovar Typhimurium DT 64. J. Bacteriol. 185:64816485.
94. Mmolawa, P.T.,, H. Schmieger,, C. P. Tucker,, and M.W. Heuzenroeder. 2003. Genomic structure of the Salmonella enterica serovar Typhimurium DT 64 bacteriophage ST64T: evidence for modular genetic architecture. J. Bacteriol. 185:34733475.
95. Nnalue, N. A.,, S. Newton,, and B. A. Stocker. 1990. Lysogenization of Salmonella choleraesuis by phage 14 increases average length of O-antigen chains, serum resistance and intraperitoneal mouse virulence. Microb. Pathog. 8:393402.
96. Ochman, H.,, F. C. Soncini,, F. Solomon,, and E. A. Groisman. 1996. Identification of a pathogenicity island required for Salmonella survival in host cells. Proc. Natl.Acad. Sci.USA 93:78007804.
97. Ochman, H.,, J.G. Lawrence,, and E.A. Groisman. 2000. Lateral gene transfer and the nature of bacterial innovation. Nature 405:299304.
98. Parkhill, J.,, G. Dougan,, K. D. James,, N. R. Thomson,, D. Pickard,, J. Wain,, C. Churcher,, K. L. Mungall,, S. D. Bentley,, M.T. Holden,, M. Sebaihia,, S. Baker,, D. Basham,, K. Brooks,, T. Chillingworth,, P. Connerton,, A. Cronin,, P. Davis,, R. M. Davies,, L. Dowd,, N. White,, J. Farrar,, T. Feltwell,, N. Hamlin,, A. Haque,, T. T. Hien,, S. Holroyd,, K. Jagels,, A. Krogh,, T. S. Larsen,, S. Leather,, S. Moule,, P. O’Gaora,, C. Parry,, M. Quail,, K. Rutherford,, M. Simmonds,, J. Skelton,, K. Stevens,, S. Whitehead,, and B. G. Barrell. 2001. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413:848852.
99. Pascopella, L.,, B. Raupach,, N. Ghori,, D. Monack,, S. Falkow,, and P. L. Small. 1995. Host restriction phenotypes of Salmonella typhi and Salmonella gallinarum. Infect.Immun. 63:43294335.
100. Pedulla, M. L.,, M. E. Ford,, T. Karthikeyan,, J. M. Houtz,, R.W. Hendrix,, G. F. Hatfull,, A. R. Poteete,, E. B. Gilcrease,, D. A. Winn-Stapley,, and S. R. Casjens. 2003. Corrected sequence of the bacteriophage P22 genome. J. Bacteriol. 185:14751477.
101. Pelludat, C.,, S. Mirold,, and W.-D. Hardt. 2003.The SopEϕ phage integrates into the ssrA gene of Salmonella enterica serovar Typhimurium A36 and is closely related to the Fels-2 prophage. J. Bacteriol. 185:51825191.
102. Plasterk, R. H.,, A. Brinkman,, and P. van de Putte. 1983. DNA inversions in the chromosome of Escherichia coli and in bacteriophage Mu: relationship to other site-specific recombination systems. Proc. Natl.Acad. Sci.USA 80:53555358.
103. Plasterk, R. H.,, and P. van de Putte. 1985.The invertible P-DNA segment in the chromosome of Escherichia coli. EMBO J. 4:237242.
104. Popoff, M.Y.,, and L. Le Minor. 1997. Antigenic Formulas of the Salmonella Serovars, 7th revision. WHO Collaborating Centre for Reference and Research on Salmonella. Institut Pasteur, Paris, France.
105. Ptashne, M. 1992. A Genetic Switch, 2nd ed. Blackwell Scientific Publications, Cambridge, Mass.
106. Rabsch, W.,, H. L. Andrews,, R. A. Kingsley,, R. Prager,, H. Tschäpe,, L. G. Adams,, and A. J. Bäumler. 2002. Salmonella enterica serotype Typhimurium and its host-adapted variants. Infect. Immun. 70:22492255.
107. Reed, M. R.,, K. E. Shearwin,, and J. B. Egan. 1997.The dual role of the Cro-like Apl protein in prophage induction of coliphage 186. Mol. Microbiol. 23:669681.
108. Sansone, A.,, P. R. Watson,, T. S. Wallis,, P. R. Langford,, and J. S. Kroll. 2002. The role of two periplasmic copper- and zinc-cofactored superoxide dismutases in the virulence of Salmonella choleraesuis. Microbiology 148:719726.
109. Sauer, R. T.,, M. J. Ross,, and M. Ptashne. 1982. Cleavage of the lambda and P22 repressors by RecA protein. J. Biol. Chem. 257:44584462.
110. Schicklmaier, P.,, and H. Schmieger. 1994. Frequency of generalized transducing phages in natural isolates of the Salmonella typhimurium complex. Appl. Environ. Microbiol. 61:16371640.
111. Schicklmaier, P.,, E. Moser,, T. Wieland,, W. Rabsch,, and H. Schmieger. 1998.A comparative study on the frequency of prophages among natural isolates of Salmonella and Escherichia coli with emphasis on generalized transducers. Antonie Leeuwenhoek 73:4954.
112. Schmidt, H.,, and M. Hensel. 2004. Pathogenicity islands in bacterial pathogenesis. Clin. Microbiol. Rev. 17:1456.
113. Schmieger, H. 1972. Phage P22-mutants with increased or decreased transduction abilities. Mol. Gen. Genet. 119:7588.
114. Schmieger, H.,, and P. Schicklmaier. 1999. Transduction of multiple drug resistance of Salmonella enterica serovar Typhimurium DT104. FEMS Microbiol. Lett. 170:251256.
115. Shea, J. E.,, M. Hensel,, C. Gleeson,, and D.W. Holden. 1996. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 93:25932597.
116. Shearwin, K. E.,, A. M. Brumby,, and J. B. Egan. 1998.The Tum protein of coliphage 186 is an antirepressor. J. Biol. Chem. 273:57085715.
117. Stanley, T. L.,, C. D. Ellermeier,, and J. M. Slauch. 2000. Tissue-specific gene expression identifies a gene in the lysogenic phage Gifsy-1 that affects Salmonella enterica serovarTyphimurium survival in Peyer’s patches. J. Bacteriol.182:44064413.
118. Stender, S.,, A. Friebel,, S. Linder,, M. Rohde,, S. Mirold,, and W.-D. Hardt. 2000. Identification of SopE2 from Salmonella typhimurium, a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol. Microbiol. 36:12061221.
119. Susskind, M. M.,, and D. Botstein. 1978.Molecular genetics of bacteriophage P22. Microbiol. Rev. 42:385413.
120. Szybalski, W.,, K. Bøvre,, M. Fiandt,, S. Hayes,, Z. Hradecna,, S. Kumar,, H. A. Lozeron,, H. J. J. Nijkamp,, and W. F. Stevens. 1970. Transcriptional units and their controls in Escherichia coli phage λ: operons and scriptons. Cold Spring Harbor Symp. Quant. Biol. 35:341353.
121. Tanaka, K.,, K. Nishimori,, S. Makino,, T. Nishimori,, T. Kanno,, R. Ishihara,, T. Sameshima,, M. Akiba,, M. Nakazawa,, Y. Yokomizo,, and I. Uchida. 2004. Molecular characterization of a prophage of Salmonella enterica serotype Typhimurium DT104. J. Clin. Microbiol. 42:18071812.
122. Threlfall, E. J.,, L. R. Ward,, J. A. Frost,, and G. A. Willshaw. 2000. Spread of resistance from food animals to man—the UK experience. Acta Vet. Scand. 93(Suppl.):6368.
123. Tsolis, R. M.,, S. M. Townsend,, E. A. Miao,, S. I. Miller,, T. A. Ficht,, L. G. Adams,, and A. J. Bäumler. 1999. Identification of a putative Salmonella enterica serotype Typhimurium host range factor with homology to IpaH and YopM by signature-tagged mutagenesis. Infect. Immun. 67:63856393.
124. Uzzau, S.,, D. J. Brown,, T. Wallis,, S. Rubino,, G. Leori,, S. Bernard,, J. Casadesús,, D. J. Platt,, and J. E. Olsen. 2000. Host adapted serotypes of Salmonella enterica. Epidemiol. Infect. 125:229255.
125. Uzzau, S.,, N. Figueroa-Bossi,, S. Rubino,, and L. Bossi. 2001. Epitope tagging of chromosomal genes in Salmonella. Proc. Natl.Acad. Sci. USA 98:1526415269.
126. Uzzau, S.,, L. Bossi,, and N. Figueroa-Bossi. 2002. Differential accumulation of Salmonella [Cu, Zn] superoxide dismutases SodCI and SodCII in intracellular bacteria: correlation with their relative contribution to pathogenicity. Mol. Microbiol. 46:147156.
127. Uzzau, S.,, N. Figueroa-Bossi,, and L. Bossi. Unpublished data.
128. van de Putte, P.,, S. Cramer,, and M. Giphart-Gassler. 1980. Invertible DNA determines host specificity of bacteriophage Mu. Nature 286:218222.
129. Vander Byl, C.,, and A. M. Kropinski. 2000. Sequence of the genome of Salmonella bacteriophage P22. J. Bacteriol. 182:64726481.
130. van Dijl, J. M.,, R. van den Bergh,, T. Reversma,, H. Smith,, S. Bron,, and G. Venema. 1990. Molecular cloning of the Salmonella typhimurium lep gene in Escherichia coli. Mol. Gen. Genet. 223:233240.
131. Vimr, E. R.,, K. A. Kalivoda,, E. L. Deszo,, and S. M. Steenbergen. 2004. Diversity of microbial sialic acid metabolism. Microbiol. Mol. Biol. Rev. 68:132153.
132. Voloshin, O. N.,, B. E. Ramirez,, A. Bax,, and R. D. Camerini-Otero. 2001.A model for the abrogation of the SOS response by an SOS protein: a negatively charged helix in DinI mimics DNA in its interaction with RecA. Genes Dev. 15:415427.
133. Walker, G., 1996. The SOS response of Escherichia coli, p. 14001416. In F. C. Neidhardt,, R. CurtissIII,, J. L. Ingraham,, E.C.C. Lin,, K.B. Low,, B. Magasanik,, W. S. Reznikoff,, M. Riley,, M. Schaechter,, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: Cellular and Molecular Biology, 2nd ed., vol. 1.ASM Press,Washington,D.C.
134. Wang, H.,, C.-H. Yang,, G. Lee,, F. Chang,, H. Wilson,, A. del Campillo-Campbell,, and A. Campbell. 1997. Integration specificities of two lambdoid phages (21 and e14) that insert at the same attB site. J. Bacteriol. 179:57055711.
135. Williams, K. P. 2003. Traffic at the tmRNA gene. J. Bacteriol. 185:10591070.
136. Withey, J. H.,, and D. I. Friedman. 2003. A salvage pathway for protein structures: tmRNA and trans-translation. Annu. Rev. Microbiol. 57:101123.
137. Wong, K. K.,, M. McClelland,, L. C. Stillwell,, E. C. Sisk,, S. J. Thurston,, and J. D. Saffer. 1998. Identification and sequence analysis of a 27-kilobase chromosomal fragment containing a Salmonella pathogenicity island located at 92 minutes on the chromosome map of Salmonella enterica serovar Typhimurium LT2. Infect. Immun. 66:33653371.
138. Wood, M. W.,, R. Rosqvist,, P. B. Mullan,, M. H. Edwards,, and E. E. Galyov. 1996. SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via a sipdependent mechanism and promotes bacterial entry. Mol. Microbiol. 22:327338.
139. Wood, M.W.,, M. A. Jones,, P. R. Watson,, S. Hedges,, T. S. Wallis,, and E. E. Galyov. 1998. Identification of a pathogenicity island required for Salmonella enteropathogenicity. Mol. Microbiol. 29:883891.
140. Worley, M. J.,, K. H. Ching,, and F. Heffron. 2000. Salmonella SsrB activates a global regulon of horizontally acquired genes. Mol. Microbiol. 36: 749761.
141. Worley, M. J.,, and F. Heffron. Salmonella invades its host by manipulating the motility of infected cells. EMBO J., in press.
142. Wright, A. 1971. Mechanism of conversion of the Salmonella O antigen by bacteriophage epsilon 34. J. Bacteriol. 105:927936.
143. Yamamoto, N.,, and T. F. Anderson. 1961. Genomic masking and recombination between serologically unrelated phages P22 and P221. Virology 14:430439.
144. Yamamoto, N. 1964. Bacteriophage: an unusual hybrid of serologically unrelated phages P22 and P221. Science 143:144145.
145. Yamamoto, N. 1967. The origin of bacteriophage P221. Virology 33:545547.
146. Yamamoto, N. 1969. Genetic evolution of bacteriophage. I. Hybrids between unrelated bacteriophages P22 and Fels 2. Proc. Natl. Acad. Sci. USA 62:6369.
147. Yasuda, T.,, K. Morimatsu,, T. Horii,, T. Nagata,, and H. Ohmori. 1998. Inhibition of Escherichia coli RecA coprotease activites by DinI. EMBO J. 17:32073216.
148. Young, B.G.,, Y. Fukazawa,, and P. Hartman. 1964. A P22 bacteriophage mutant defective in antigen conversion. Virology 23:279283.
149. Zhang, S.,, R. L. Santos,, R. M. Tsolis,, S. Stender,, W.-D. Hardt,, A. J. Bäumler,, and L. G. Adams. 2002. SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves infected with Salmonella enterica serotype Typhimurium. Infect. Immun. 70:38433855.
150. Zhang, S.,, R. L. Santos,, R. M. Tsolis,, S. Mirold,, W.-D. Hardt,, L. G. Adams,, and A. J. Bäumler. 2002. Phage mediated horizontal transfer of the sopE1 gene increases enteropathogenicity of Salmonella enterica serotype Typhimurium for calves. FEMS Microbiol. Lett. 217:243247.
151. Zinder, N.D.,, and J. Lederberg. 1952. Genetic exchange in Salmonella. J. Bacteriol. 64:679699.


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prophage genes that can be linked to pathogenicity

Citation: Bossi L, Figueroa-Bossi N. 2005. Prophage Arsenal of Serovar Typhimurium, p 165-186. In Waldor M, Friedman D, Adhya S (ed), Phages. ASM Press, Washington, DC. doi: 10.1128/9781555816506.ch8

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