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7 - Prophage Contribution to Salmonella Virulence and Diversity

from PART III - Paradigms of Bacterial Evolution

Published online by Cambridge University Press:  16 September 2009

By
Sébastien Lemire ,
Nara Figueroa-Bossi  and
Lionello Bossi
Edited by
Michael Hensel  and
Herbert Schmidt
Michael Hensel
Affiliation:
Friedrich-Alexander-Universität Erlangen-Nürnberg, Germany
Herbert Schmidt
Affiliation:
Universität Hohenheim, Stuttgart
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Summary

INTRODUCTION

Salmonellae are enteric pathogenic bacteria that infect a vast spectrum of animal species from reptiles to mammals. The genus is highly diversified, comprising more than 2,500 serovars. An even greater diversity exists at the strain level as a result of countless combinations of genomic differences in individual isolates. Strain-specific variations are likely to influence aspects of the organism biology, such as the adaptation to specific hosts or environments, the tropism for certain organs or tissues, and the degree of pathogenicity. The emergence in recent years of epidemic clones that have become predominant, displacing pre-existing strains, confirms that strain diversification is an ongoing process. A leading mechanism promoting diversity in Salmonella genomes is lysogenization by temperate phages. Most strains harbor multiple prophages in variable numbers and combinations. Prophages modify the properties of the host bacterium in various ways, from expressing functions that directly influence pathogenicity, to improving the bacterium's ability to outgrow competitors or to resist killing by superinfecting phages. Unlike toxin-producing phages of other bacterial species, most Salmonella prophages contribute to virulence through the synergistic action of multiple factors playing subtle, often redundant roles. The scope of this chapter is to review the various facets of phage-mediated modification of Salmonella, as well as recent advances in the characterization of phage-borne virulence determinants.

SALMONELLA DIVERSITY

Current classification divides the genus Salmonella into two species, Salmonella bongori and Salmonella enterica.

Type
Chapter
Information
Horizontal Gene Transfer in the Evolution of Pathogenesis , pp. 159 - 192
Publisher: Cambridge University Press
Print publication year: 2008

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References

Aizawa, S. I. (2001). Bacterial flagella and type III secretion systems. FEMS Microbiol Lett, 202, 157–64.CrossRefGoogle ScholarPubMed
Alonso, A., Pucciarelli, M. G., Figueroa-Bossi, N., and Portillo, Garcia-Del, F, . (2005). Increased excision of the Salmonella prophage ST64B caused by a deficiency in Dam methylase. J Bacteriol, 187, 7901–11.CrossRefGoogle ScholarPubMed
Altier, C. (2005). Genetic and environmental control of Salmonella invasion. J Microbiol, 43, 85–92.Google ScholarPubMed
Amavisit, P., Lightfoot, D., Browning, G. F., and Markham, P. F. (2003). Variation between pathogenic serovars within Salmonella pathogenicity islands. J Bacteriol, 185, 3624–35.CrossRefGoogle ScholarPubMed
Anderson, E. S., Ward, L. R., Saxe, M. J., and Sa, J. D. (1977). Bacteriophage-typing designations of Salmonella typhimurium. J Hyg (Lond), 78, 297–300.CrossRefGoogle ScholarPubMed
Bacciu, D., Falchi, G., Spazziani, A., et al. (2004). Transposition of the heat-stable toxin astA gene into a gifsy-2-related prophage of Salmonella enterica serovar Abortusovis. J Bacteriol, 186, 4568–74.CrossRefGoogle ScholarPubMed
Bakshi, C. S., Singh, V. P., Wood, M. W., et al. (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, 2341–4.CrossRefGoogle ScholarPubMed
Balbontin, R., Rowley, G., Pucciarelli, M. G., et al. (2006). DNA adenine methylation regulates virulence gene expression in Salmonella enterica serovar Typhimurium. J Bacteriol, 188, 8160–8.CrossRefGoogle ScholarPubMed
Bäumler, A. J. (1997). The record of horizontal gene transfer in Salmonella. Trends Microbiol, 5, 318–22.CrossRefGoogle ScholarPubMed
Bäumler, A. J., Tsolis, R., Ficht, T. A., and Adams, L. G. (1998). Evolution of host adaptation in Salmonella enterica. Infect Immun, 66, 4579–87.Google ScholarPubMed
Beltran, P., Musser, J. M., Helmuth, R., et al. (1988). Toward a population genetic analysis of Salmonella: genetic diversity and relationships among strains of serotypes S. choleraesuis, S. derby, S. dublin, S. enteritidis, S. heidelberg, S. infantis, S. newport, and S. typhimurium. Proc Natl Acad Sci USA, 85, 7753–7.CrossRefGoogle Scholar
Beltran, P., Plock, S. A., Smith, N. H., et al. (1991). Reference collection of strains of the Salmonella typhimurium complex from natural populations. J Gen Microbiol, 137, 601–6.CrossRefGoogle ScholarPubMed
Blanc-Potard, A. B., Solomon, F., Kayser, J., and Groisman, E. A. (1999). The SPI-3 pathogenicity island of Salmonella enterica. J Bacteriol, 181, 998–1004.Google ScholarPubMed
Bossi, L., and Figueroa-Bossi, N. (2005). Prophage arsenal of Salmonella enterica serovar Typhimurium. In Waldor, M., Friedman, D., and Adhya, S. (Eds.). Phages: their role in bacterial pathogenesis and biotechnology. Washington, DC: ASM Press.Google Scholar
Bossi, L., Fuentes, J. A., Mora, G., and Figueroa-Bossi, N. (2003). Prophage contribution to bacterial population dynamics. J Bacteriol, 185, 6467–71.CrossRefGoogle ScholarPubMed
Boyd, E. F., Porwollik, S., Blackmer, F., and McClelland, M. (2003). Differences in gene content among Salmonella enterica serovar typhi isolates. J Clin Microbiol, 41, 3823–8.CrossRefGoogle ScholarPubMed
Boyd, J. S. (1950). The symbiotic bacteriophages of Salmonella typhimurium. J Pathol Bacteriol, 62, 501–17.CrossRefGoogle Scholar
Boyle, E. C., Brown, N. F., and Finlay, B. B. (2006). Salmonella enterica serovar Typhimurium effectors SopB, SopE, SopE2 and SipA disrupt tight junction structure and function. Cell Microbiol, 8, 1946–57.CrossRefGoogle ScholarPubMed
Brüssow, H., Canchaya, C., and Hardt, W. D. (2004). Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev, 68, 560–602.CrossRefGoogle ScholarPubMed
Bueno, S. M., Santiviago, C. A., Murillo, A. A., et al. (2004). Precise excision of the large pathogenicity island, SPI7, in Salmonella enterica serovar Typhi. J Bacteriol, 186, 3202–13.CrossRefGoogle ScholarPubMed
Campbell, A. M. (1993). Thirty years ago in Genetics: prophage insertion into bacterial chromosomes. Genetics, 133, 433–7.Google ScholarPubMed
Carlson, S. A., Willson, R. M., Crane, A. J., and Ferris, K. E. (2000). Evaluation of invasion-conferring genotypes and antibiotic-induced hyperinvasive phenotypes in multiple antibiotic resistant Salmonella typhimurium DT104. Microb Pathog, 28, 373–8.CrossRefGoogle ScholarPubMed
Carlson, S. A., Meyerholz, D. K., Stabel, T. J., and Jones, B. D. (2001). Secretion of a putative cytotoxin in multiple antibiotic resistant Salmonella enterica serotype Typhimurium phagetype DT104. Microb Pathog, 31, 201–4.CrossRefGoogle ScholarPubMed
Chiu, C. H., Tang, P., Chu, C., et al. (2005). The genome sequence of Salmonella enterica serovar Choleraesuis, a highly invasive and resistant zoonotic pathogen. Nucleic Acids Res, 33, 1690–8.CrossRefGoogle ScholarPubMed
Collazo, C. M., and Galan, J. E. (1997). The invasion-associated type III system of Salmonella typhimurium directs the translocation of Sip proteins into the host cell. Mol Microbiol, 24, 747–56.CrossRefGoogle ScholarPubMed
Coombes, B. K., Wickham, M. E., Brown, N. F., et al. (2005). 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, 348, 817–30.CrossRefGoogle ScholarPubMed
Crosa, J. H., Brenner, D. J., Ewing, W. H., and Falkow, S. (1973). Molecular relationships among the Salmonellae. J Bacteriol, 115, 307–15.Google Scholar
Crowl, R. M., Boyce, R. P., and Echols, H. (1981). Repressor cleavage as a prophage induction mechanism: hypersensitivity of a mutant lambda cI protein to recA-mediated proteolysis. J Mol Biol, 152, 815–9.CrossRefGoogle ScholarPubMed
Groote, M.Ochsner, A., Shiloh, U. A., , M. U., et al. (1997). Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase. Proc Natl Acad Sci USA, 94, 13997–4001.CrossRefGoogle ScholarPubMed
Deng, W., Liou, , Plunkett, S. R., 3rd, G., et al. (2003). Comparative genomics of Salmonella enterica serovar Typhi strains Ty2 and CT18. J Bacteriol, 185, 2330–7.CrossRefGoogle ScholarPubMed
Ehrbar, K., and Hardt, W. D. (2005). Bacteriophage-encoded type III effectors in Salmonella enterica subspecies 1 serovar Typhimurium. Infect Genet Evol, 5, 1–9.Google ScholarPubMed
Fang, F. C., Groote, M. A., Foster, J. W., et al. (1999). Virulent Salmonella typhimurium has two periplasmic Cu, Zn-superoxide dismutases. Proc Natl Acad Sci USA, 96, 7502–7.CrossRefGoogle ScholarPubMed
Fierer, J., and Guiney, D. G. (2001). Diverse virulence traits underlying different clinical outcomes of Salmonella infection. J Clin Invest, 107, 775–80.CrossRefGoogle ScholarPubMed
Figueroa-Bossi, N., and Bossi, L. (1999). Inducible prophages contribute to Salmonella virulence in mice. Mol Microbiol, 33, 167–76.CrossRefGoogle ScholarPubMed
Figueroa-Bossi, N., and Bossi, L. (2004). Resuscitation of a defective prophage in Salmonella cocultures. J Bacteriol, 186, 4038–41.CrossRefGoogle ScholarPubMed
Figueroa-Bossi, N., Coissac, E., Netter, P., and Bossi, L. (1997). Unsuspected prophage-like elements in Salmonella typhimurium. Mol Microbiol, 25, 161–73.CrossRefGoogle ScholarPubMed
Figueroa-Bossi, N., Uzzau, S., Maloriol, D., and Bossi, L. (2001). Variable assortment of prophages provides a transferable repertoire of pathogenic determinants in Salmonella. Mol Microbiol, 39, 260–71.CrossRefGoogle ScholarPubMed
Figueroa-Bossi, N., Ammendola, S., and Bossi, L. (2006). Differences in gene expression levels and in enzymatic qualities account for the uneven contribution of superoxide dismutases SodCI and SodCII to pathogenicity in Salmonella enterica. Microbes Infect, 8, 1569–78.CrossRefGoogle ScholarPubMed
Friebel, A., Ilchmann, H., Aepfelbacher, M., et al. (2001). SopE and SopE2 from Salmonella typhimurium activate different sets of RhoGTPases of the host cell. J Biol Chem, 276, 34035–40.CrossRefGoogle ScholarPubMed
Fukazawa, Y., and Hartman, P. E. (1964). A P22 bacteriophage mutant defective in antigen conversion. Virology, 23, 279–83.Google ScholarPubMed
Gabbianelli, R., D'orazio, M., Pacello, F., et al. (2004). Distinctive functional features in prokaryotic and eukaryotic Cu,Zn superoxide dismutases. Biol Chem, 385, 749–54.CrossRefGoogle ScholarPubMed
Galan, J. E., and Curtiss, R. (1989). Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci USA, 86, 6383–7.CrossRefGoogle ScholarPubMed
Glynn, M. K., Bopp, C., Dewitt, W., et al. (1998). Emergence of multidrug-resistant Salmonella enterica serotype typhimurium DT104 infections in the United States. N Engl J Med, 338, 1333–8.CrossRefGoogle ScholarPubMed
Golubeva, Y. A., and Slauch, J. M. (2006). Salmonella enterica serovar Typhimurium periplasmic superoxide dismutase SodCI is a member of the PhoPQ regulon and is induced in macrophages. J Bacteriol, 188, 7853–61.CrossRefGoogle ScholarPubMed
Groisman, E. A. (2001). The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol, 183, 1835–42.CrossRefGoogle ScholarPubMed
Groisman, E. A., and Mouslim, C. (2006). Sensing by bacterial regulatory systems in host and non-host environments. Nat Rev Microbiol, 4, 705–9.CrossRefGoogle ScholarPubMed
Groisman, E. A., and Ochman, H. (1996). Pathogenicity islands: bacterial evolution in quantum leaps. Cell, 87, 791–4.CrossRefGoogle ScholarPubMed
Gunn, J. S., Belden, W. J., and Miller, S. I. (1998). Identification of PhoP-PhoQ activated genes within a duplicated region of the Salmonella typhimurium chromosome. Microb Pathog, 25, 77–90.CrossRefGoogle ScholarPubMed
Hapfelmeier, S., Ehrbar, K., Stecher, B., et al. (2004). Role of the Salmonella pathogenicity island 1 effector proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica subspecies 1 serovar Typhimurium colitis in streptomycin-pretreated mice. Infect Immun, 72, 795–809.CrossRefGoogle ScholarPubMed
Haraga, A., and Miller, S. I. (2003). A Salmonella enterica serovar Typhimurium translocated leucine-rich repeat effector protein inhibits NF-kappa B-dependent gene expression. Infect Immun, 71, 4052–8.CrossRefGoogle ScholarPubMed
Haraga, A., and Miller, S. I. (2006). A Salmonella type III secretion effector interacts with the mammalian serine/threonine protein kinase PKN1. Cell Microbiol, 8, 837–46.CrossRefGoogle ScholarPubMed
Hardt, W. D., Urlaub, H., and Galan, J. E. (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, 2574–9.CrossRefGoogle ScholarPubMed
Hensel, M. (2004). Evolution of pathogenicity islands of Salmonella enterica. Int J Med Microbiol, 294, 95–102.CrossRefGoogle ScholarPubMed
Hermans, A. P., Abee, T., Zwietering, M. H., and Aarts, H. J. (2005). Identification of novel Salmonella enterica serovar Typhimurium DT104-specific prophage and nonprophage chromosomal sequences among serovar Typhimurium isolates by genomic subtractive hybridization. Appl Environ Microbiol, 71, 4979–85.CrossRefGoogle ScholarPubMed
Hermans, A. P., Beuling, A. M., Hoek, A. H., et al. (2006). Distribution of prophages and SGI-1 antibiotic-resistance genes among different Salmonella enterica serovar Typhimurium isolates. Microbiology, 152, 2137–47.CrossRefGoogle ScholarPubMed
Ho, T. D., Figueroa-Bossi, N., Wang, M., et al. (2002). Identification of GtgE, a novel virulence factor encoded on the Gifsy-2 bacteriophage of Salmonella enterica serovar Typhimurium. J Bacteriol, 184, 5234–9.CrossRefGoogle ScholarPubMed
Hoyer, L. L., Hamilton, A. C., Steenbergen, S. M., and Vimr, E. R. (1992). Cloning, sequencing and distribution of the Salmonella typhimurium LT2 sialidase gene, nanH, provides evidence for interspecies gene transfer. Mol Microbiol, 6, 873–84.CrossRefGoogle ScholarPubMed
Kingsley, R. A., and Bäumler, A. J. (2000). Host adaptation and the emergence of infectious disease: the Salmonella paradigm. Mol Microbiol, 36, 1006–14.CrossRefGoogle ScholarPubMed
Klumpp, J., and Fuchs, T. M. (2007). Identification of novel genes in genomic islands that contribute to Salmonella typhimurium replication in macrophages. Microbiology, 153, 1207–20.CrossRefGoogle ScholarPubMed
Kourilsky, P. (1973). Lysogenization by bacteriophage lambda. I. Multiple infection and the lysogenic response. Mol Gen Genet, 122, 183–95.CrossRefGoogle ScholarPubMed
Krishnakumar, R., Craig, M., Imlay, J. A., and Slauch, J. M. (2004). Differences in enzymatic properties allow SodCI but not SodCII to contribute to virulence in Salmonella enterica serovar Typhimurium strain 14028. J Bacteriol, 186, 5230–8.CrossRefGoogle Scholar
Krishnakumar, R., Kim, B., Mollo, E. A., Imlay, J. A., and Slauch, J. M. (2007). Structural properties of periplasmic SodCI that correlate with virulence in Salmonella enterica serovar Typhimurium. J Bacteriol, 189, 4343–52.CrossRefGoogle ScholarPubMed
Ku, Y. W., McDonough, S. P., Palaniappan, R. U., Chang, C. F., and Chang, Y. F. (2005). Novel attenuated Salmonella enterica serovar Choleraesuis strains as live vaccine candidates generated by signature-tagged mutagenesis. Infect Immun, 73, 8194–203.CrossRefGoogle ScholarPubMed
Kutsukake, K., Nakashima, H., Tominaga, A., and Abo, T. (2006). Two DNA invertases contribute to flagellar phase variation in Salmonella enterica serovar Typhimurium strain LT2. J Bacteriol, 188, 950–7.CrossRefGoogle ScholarPubMed
Lawley, T. D., Chan, K., Thompson, L. J., et al. (2006). Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog, 2, e11.CrossRefGoogle ScholarPubMed
Minor, L. (1984). Salmonella lignieres. In Kreig, N. R., and Holt, J. G. (Eds.). Bergey's manual of systematic bacteriology. Baltimore: Williams & Wilkins.Google Scholar
Lemire, S. (2006). Les prophages de Salmonella typhimurium: Régulation lysogénique et contribution à la pathogénicité. PhD thesis. Paris-Sud 11 University.
Leong, J. M., Nunes-Duby, S., Lesser, C. F., et al. (1985). The phi 80 and P22 attachment sites. Primary structure and interaction with Escherichia coli integration host factor. J Biol Chem, 260, 4468–77.Google ScholarPubMed
Matsushiro, A., Sato, K., Miyamoto, H., Yamamura, T., and Honda, T. (1999). Induction of prophages of enterohemorrhagic Escherichia coli O157:H7 with norfloxacin. J Bacteriol, 181, 2257–60.Google ScholarPubMed
McClelland, M., Sanderson, K. E., Spieth, J., et al. (2001). Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature, 413, 852–6.CrossRefGoogle ScholarPubMed
McClelland, M., Sanderson, K. E., Clifton, S. W., et al. (2004). Comparison of genome degradation in Paratyphi A and Typhi, human-restricted serovars of Salmonella enterica that cause typhoid. Nat Genet, 36, 1268–74.CrossRefGoogle ScholarPubMed
Miao, E. A., and Miller, S. I. (2000). A conserved amino acid sequence directing intracellular type III secretion by Salmonella typhimurium. Proc Natl Acad Sci USA, 97, 7539–44.CrossRefGoogle ScholarPubMed
Miao, E. A., Scherer, C. A., Tsolis, R. M., et al. (1999). Salmonella typhimurium leucine-rich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol Microbiol, 34, 850–64.CrossRefGoogle ScholarPubMed
Miao, E. A., Brittnacher, M., Haraga, A., et al. (2003). Salmonella effectors translocated across the vacuolar membrane interact with the actin cytoskeleton. Mol Microbiol, 48, 401–15.CrossRefGoogle ScholarPubMed
Mirold, S., Rabsch, W., Rohde, M., et al. (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, 9845–50.CrossRefGoogle ScholarPubMed
Mirold, S., Ehrbar, K., Weissmüller, A., et al. (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, 2348–58.CrossRefGoogle Scholar
Mmolawa, P. T., Schmieger, H., and Heuzenroeder, M. W. (2003a). Bacteriophage ST64B, a genetic mosaic of genes from diverse sources isolated from Salmonella enterica serovar typhimurium DT 64. J Bacteriol, 185, 6481–5.CrossRefGoogle ScholarPubMed
Mmolawa, P. T., Schmieger, H., Tucker, C. P., and Heuzenroeder, M. W. (2003b). Genomic structure of the Salmonella enterica serovar Typhimurium DT 64 bacteriophage ST64T: evidence for modular genetic architecture. J Bacteriol, 185, 3473–5.CrossRefGoogle ScholarPubMed
Ochman, H., Soncini, F. C., Solomon, F., and Groisman, E. A. (1996). Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci USA, 93, 7800–4.CrossRefGoogle ScholarPubMed
Ohl, M. E., and Miller, S. I. (2001). Salmonella: a model for bacterial pathogenesis. Annu Rev Med, 52, 259–74.CrossRefGoogle ScholarPubMed
Parkhill, J., Dougan, G., James, K. D., et al. (2001). Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature, 413, 848–52.CrossRefGoogle ScholarPubMed
Pascopella, L., Raupach, B., Ghori, N., et al. (1995). Host restriction phenotypes of Salmonella typhi and Salmonella gallinarum. Infect Immun, 63, 4329–35.Google ScholarPubMed
Patel, J. C., and Galan, J. E. (2006). Differential activation and function of Rho GTPases during Salmonella-host cell interactions. J Cell Biol, 175, 453–63.CrossRefGoogle ScholarPubMed
Pelludat, C., Mirold, S., and Hardt, W. D. (2003). The SopEPhi phage integrates into the ssrA gene of Salmonella enterica serovar Typhimurium A36 and is closely related to the Fels-2 prophage. J Bacteriol, 185, 5182–91.CrossRefGoogle ScholarPubMed
Perna, N. T., Plunkett, G. 3rd, Burland, V., et al. (2001). Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature, 409, 529–33.CrossRefGoogle ScholarPubMed
Plunkett, G. 3rd, Rose, D. J., Durfee, T. J., and Blattner, F. R. (1999). Sequence of Shiga toxin 2 phage 933W from Escherichia coli O157:H7: Shiga toxin as a phage late-gene product. J Bacteriol, 181, 1767–78.Google ScholarPubMed
Popoff, M. Y., Bockemühl, J., and Gheesling, L. L. (2004). Supplement 2002 (no. 46) to the Kauffmann-White scheme. Res Microbiol, 155, 568–70.CrossRefGoogle Scholar
Porwollik, S., Boyd, E. F., Choy, C., et al. (2004). Characterization of Salmonella enterica subspecies I genovars by use of microarrays. J Bacteriol, 186, 5883–98.CrossRefGoogle ScholarPubMed
Prager, R., Mirold, S., Tietze, E., et al. (2000). Prevalence and polymorphism of genes encoding translocated effector proteins among clinical isolates of Salmonella enterica. Int J Med Microbiol, 290, 605–17.CrossRefGoogle ScholarPubMed
Rabsch, W., Andrews, H. L., Kingsley, R. A., et al. (2002). Salmonella enterica serotype Typhimurium and its host-adapted variants. Infect Immun, 70, 2249–55.CrossRefGoogle ScholarPubMed
Reen, F. J., Boyd, E. F., Porwollik, S., et al. (2005). Genomic comparisons of Salmonella enterica serovar Dublin, Agona, and Typhimurium strains recently isolated from milk filters and bovine samples from Ireland, using a Salmonella microarray. Appl Environ Microbiol, 71, 1616–25.CrossRefGoogle ScholarPubMed
Reeves, M. W., Evins, G. M., Heiba, A. A., Plikaytis, B. D., and Farmer, J. J. D. (1989). Clonal nature of Salmonella typhi and its genetic relatedness to other salmonellae as shown by multilocus enzyme electrophoresis, and proposal of Salmonella bongori comb. nov. J Clin Microbiol, 27, 313–20.Google ScholarPubMed
Roberts, J. W., and Roberts, C. W. (1975). Proteolytic cleavage of bacteriophage lambda repressor in induction. Proc Natl Acad Sci USA, 72, 147–51.CrossRefGoogle ScholarPubMed
Saitoh, M., Tanaka, K., Nishimori, K., et al. (2005). The artAB genes encode a putative ADP-ribosyltransferase toxin homologue associated with Salmonella enterica serovar Typhimurium DT104. Microbiology, 151, 3089–96.CrossRefGoogle ScholarPubMed
Santos, R. L., Zhang, S., Tsolis, R. M., Bäumler, A. J., and Adams, L. G. (2002). Morphologic and molecular characterization of Salmonella typhimurium infection in neonatal calves. Vet Pathol, 39, 200–15.CrossRefGoogle ScholarPubMed
Schicklmaier, P., and Schmieger, H. (1995). Frequency of generalized transducing phages in natural isolates of the Salmonella typhimurium complex. Appl Environ Microbiol, 61, 1637–40.Google ScholarPubMed
Schicklmaier, P., Moser, E., Wieland, T., Rabsch, W., and Schmieger, H. (1998). A comparative study on the frequency of prophages among natural isolates of Salmonella and Escherichia coli with emphasis on generalized transducers. Antonie Van Leeuwenhoek, 73, 49–54.CrossRefGoogle ScholarPubMed
Schicklmaier, P., Wieland, T., and Schmieger, H. (1999). Molecular characterization and module composition of P22-related Salmonella phage genomes. J Biotechnol, 73, 185–94.CrossRefGoogle ScholarPubMed
Shea, J. E., Hensel, M., Gleeson, C., and Holden, D. W. (1996). Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc Natl Acad Sci USA, 93, 2593–7.CrossRefGoogle ScholarPubMed
Stanley, T. L., Ellermeier, C. D., and Slauch, J. M. (2000). Tissue-specific gene expression identifies a gene in the lysogenic phage Gifsy-1 that affects Salmonella enterica serovar typhimurium survival in Peyer's patches. J Bacteriol, 182, 4406–13.CrossRefGoogle ScholarPubMed
Stender, S., Friebel, A., Linder, S., et al. (2000). Identification of SopE2 from Salmonella typhimurium, a conserved guanine nucleotide exchange factor for Cdc42 of the host cell. Mol Microbiol, 36.Google ScholarPubMed
Susskind, M. M., and Botstein, D. (1978). Molecular genetics of bacteriophage P22. Microbiol Rev, 42, 385–413.Google ScholarPubMed
Tanaka, K., Nishimori, K., Makino, S., et al. (2004). Molecular characterization of a prophage of Salmonella enterica serotype Typhimurium DT104. J Clin Microbiol, 42, 1807–12.CrossRefGoogle ScholarPubMed
Thomson, N., Baker, S., Pickard, D., et al. (2004). The role of prophage-like elements in the diversity of Salmonella enterica serovars. J Mol Biol, 339, 279–300.CrossRefGoogle ScholarPubMed
Threlfall, E. J., Frost, J. A., Ward, L. R., and Rowe, B. (1994). Epidemic in cattle and humans of Salmonella typhimurium DT 104 with chromosomally integrated multiple drug resistance. Vet Rec, 134, 577.CrossRefGoogle ScholarPubMed
Threlfall, E. J., Frost, J. A., Ward, L. R., and Rowe, B. (1996). Increasing spectrum of resistance in multiresistant Salmonella typhimurium. Lancet, 347, 1053–4.CrossRefGoogle ScholarPubMed
Tsolis, R. M., Townsend, S. M., Miao, E. A., et al. (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, 6385–93.Google ScholarPubMed
Tyler, J. S., Mills, M. J., and Friedman, D. I. (2004). The operator and early promoter region of the Shiga toxin type 2-encoding bacteriophage 933W and control of toxin expression. J Bacteriol, 186, 7670–9.CrossRefGoogle ScholarPubMed
Uzzau, S., Brown, D. J., Wallis, T., et al. (2000). Host adapted serotypes of Salmonella enterica. Epidemiol Infect, 125, 229–55.CrossRefGoogle ScholarPubMed
Uzzau, S., Figueroa-Bossi, N., Rubino, S., and Bossi, L. (2001). Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci USA, 98, 15264–9.CrossRefGoogle ScholarPubMed
Uzzau, S., Bossi, L., and Figueroa-Bossi, N. (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, 147–56.CrossRefGoogle ScholarPubMed
Valdivia, R. H., and Falkow, S. (1997). Fluorescence-based isolation of bacterial genes expressed within host cells. Science, 277, 2007–11.CrossRefGoogle ScholarPubMed
Vander Byl, C., and Kropinski, A. M. (2000). Sequence of the genome of Salmonella bacteriophage P22. J Bacteriol, 182, 6472–81.Google ScholarPubMed
Vazquez-Torres, A., and Fang, F. C. (2001). Salmonella evasion of the NADPH phagocyte oxidase. Microbes Infect, 3, 1313–20.CrossRefGoogle ScholarPubMed
Vlisidou, I., Marches, O., Dziva, F., et al. (2006). Identification and characterization of EspK, a type III secreted effector protein of enterohaemorrhagic Escherichia coli O157:H7. FEMS Microbiol Lett, 263, 32–40.CrossRefGoogle ScholarPubMed
Wagner, P. L., Neely, M. N., Zhang, X., et al. (2001). Role for a phage promoter in Shiga toxin 2 expression from a pathogenic Escherichia coli strain. J Bacteriol, 183, 2081–5.CrossRefGoogle ScholarPubMed
Wagner, P. L., Livny, J., Neely, M. N., et al. (2002). Bacteriophage control of Shiga toxin 1 production and release by Escherichia coli. Mol Microbiol, 44, 957–70.CrossRefGoogle ScholarPubMed
Waldor, M. K., and Friedman, D. I. (2005). Phage regulatory circuits and virulence gene expression. Curr Opin Microbiol, 8, 459–65.CrossRefGoogle ScholarPubMed
Wallis, T. S., and Galyov, E. E. (2000). Molecular basis of Salmonella-induced enteritis. Mol Microbiol, 36, 997–1005.CrossRefGoogle ScholarPubMed
Ward, L. R., Sa, J. D., and Rowe, B. (1987). A phage-typing scheme for Salmonella enteritidis. Epidemiol Infect, 99, 291–4.CrossRefGoogle ScholarPubMed
Wong, K. K., McClelland, M., Stillwell, L. C., et al. (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, 3365–71.Google ScholarPubMed
Wood, M. W., Rosqvist, R., Mullan, P. B., Edwards, M. H., and Galyov, E. E. (1996). SopE, a secreted protein of Salmonella dublin, is translocated into the target eukaryotic cell via a sip-dependent mechanism and promotes bacterial entry. Mol Microbiol, 22, 327–38.CrossRefGoogle Scholar
Wood, M. W., Jones, M. A., Watson, P. R., et al. (1998). Identification of a pathogenicity island required for Salmonella enteropathogenicity. Mol Microbiol, 29, 883–91.CrossRefGoogle ScholarPubMed
Worley, M. J., Ching, K. H., and Heffron, F. (2000). Salmonella SsrB activates a global regulon of horizontally acquired genes. Mol Microbiol, 36, 749–61.CrossRefGoogle ScholarPubMed
Worley, M. J., Nieman, G. S., Geddes, K., and Heffron, F. (2006). Salmonella typhimurium disseminates within its host by manipulating the motility of infected cells. Proc Natl Acad Sci USA, 103, 17915–20.CrossRefGoogle ScholarPubMed
Zhang, S., Santos, R. L., Tsolis, R. M., et al. (2002). Phage mediated horizontal transfer of the sopE1 gene increases enteropathogenicity of Salmonella enterica serotype Typhimurium for calves. FEMS Microbiol Lett, 217, 243–7.CrossRefGoogle ScholarPubMed
Zhang, S., Kingsley, R. A., Santos, R. L., et al. (2003). Molecular pathogenesis of Salmonella enterica serotype Typhimurium-induced diarrhea. Infect Immun, 71, 1–12.CrossRefGoogle ScholarPubMed
Zhang, X., McDaniel, A. D., Wolf, L. E., et al. (2000). Quinolone antibiotics induce Shiga toxin-encoding bacteriophages, toxin production, and death in mice. J Infect Dis, 181, 664–70.CrossRefGoogle ScholarPubMed
Zinder, N. D., and Lederberg, J. (1952). Genetic exchange in Salmonella. J Bacteriol, 64, 679–99.Google ScholarPubMed

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