Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2025-01-03T16:16:44.631Z Has data issue: false hasContentIssue false

6 - Pathogenicity islands and virulence of Salmonella enterica

Published online by Cambridge University Press:  04 December 2009

Duncan Maskell
By
Michael Hensel
Edited by
Pietro Mastroeni
Duncan Maskell
Affiliation:
University of Cambridge
Michael Hensel
Affiliation:
Institut für Klinische Mikrobiologie, Immunologie und Hygiene, Universität Erlangen-Nuemberg, Wasserturmstr. 3-5, D-91054 Erlangen, Germany
Pietro Mastroeni
Affiliation:
University of Cambridge
Get access

Summary

INTRODUCTION

Horizontal gene transfer and bacterial virulence

Bacteria show a remarkable ability to adapt rapidly to new habitats. This observation also applies to pathogenic bacteria that have evolved strategies to colonize various anatomical niches of their multi-cellular hosts. The acquisition of genetic material by a process termed horizontal gene transfer is considered to be a driving force for the rapid evolution of bacteria as pathogens. Extrachromosomal DNA such as plasmids conferring resistance to antibiotics were the first horizontally transferred DNA elements to be identified, but later it became obvious that there are also mechanisms that allow the horizontal transfer of chromosomal DNA elements. The observation that certain virulence functions are clustered in distinct regions of the chromosome and that these regions are genetically unstable and were deleted with high frequencies gave the first clue about the existence of the new form of genetic elements. The term ‘Pathogenicity Island’ (PAI) was first introduced in 1983 by Hacker and colleagues who observed genetic instability of genes associated with the haemolytic activity of uropathogenic strains of Escherichia coli (Hacker et al., 1983). PAI were initially defined as large, unstable regions of the chromosome. With the identification of a large number of additional PAIs in various groups of bacterial pathogens, further common features were found.

Definition of pathogenicity islands

The following common characteristics were defined for PAIs:

  • They are large, distinct genetic entities on the bacterial chromosome.

  • They harbor one or more virulence genes.

  • They are often genetically unstable. This feature correlates with the presence of genetic elements involved in DNA-mobility, such as direct repeats, integrases, transposases and bacteriophage genes.

  • […]

Type
Chapter
Information
Salmonella Infections
Clinical, Immunological and Molecular Aspects
 , pp. 146 - 172
Publisher: Cambridge University Press
Print publication year: 2006

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmer, B. M., Reeuwijk, J., Watson, P. R., Wallis, T. S. and Heffron, F. (1999). Salmonella SirA is a global regulator of genes mediating enteropathogenesis. Mol Microbiol, 31, 971–82.CrossRefGoogle 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
Bäumler, A. J. (1997). The record of horizontal gene transfer in Salmonella. Trends Microbiol, 5, 318–22.CrossRefGoogle ScholarPubMed
Bäumler, A. J., Tsolis, R. M., Velden, A. W.et al. (1996). Identification of a new iron regulated locus of Salmonella typhi. Gene, 183, 207–13.CrossRefGoogle ScholarPubMed
Beuzon, C. R., Meresse, S., Unsworth, K. E.et al. (2000). Salmonella maintains the integrity of its intracellular vacuole through the action of sifA. EMBO J, 19, 3235–49.CrossRefGoogle ScholarPubMed
Blanc-Potard, A. B. and Groisman, E. A. (1997). The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J, 16, 5376–85.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
Boyd, D., Peters, G. A., Cloeckaert, A.et al. (2001). Complete nucleotide sequence of a 43-kilobase genomic island associated with the multidrug resistance region of Salmonella enterica serovar Typhimurium DT104 and its identification in phage type DT120 and serovar Agona. J Bacteriol, 183, 5725–32.CrossRefGoogle Scholar
Carniel, E. (2001). The Yersinia high-pathogenicity island: an iron-uptake island. Microbes Infect, 3, 561–9.CrossRefGoogle Scholar
Chakravortty, D., Hansen-Wester, I. and Hensel, M. (2002). Salmonella pathogenicity island 2 mediates protection of intracellular Salmonella from reactive nitrogen intermediates. J Exp Med, 195, 1155–66.CrossRefGoogle ScholarPubMed
Cirillo, D. M., Valdivia, R. H., Monack, D. M. and Falkow, S. (1998). Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol Microbiol, 30, 175–88.CrossRefGoogle ScholarPubMed
Deiwick, J., Nikolaus, T., Erdogan, S. and Hensel, M. (1999). Environmental regulation of Salmonella Pathogenicity Island 2 gene expression. Mol Microbiol, 31, 1759–73.CrossRefGoogle ScholarPubMed
Doublet, B., Lailler, R., Meunier, D.et al. (2003). Variant Salmonella genomic island 1 antibiotic resistance gene cluster in Salmonella enterica serovar Albany. Emerg Infect Dis, 9, 585–91.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
Folkesson, A., Lofdahl, S. and Normark, S. (2002). The Salmonella enterica subspecies I specific centisome 7 genomic island encodes novel protein families present in bacteria living in close contact with eukaryotic cells. Res Microbiol, 153, 537–45.CrossRefGoogle ScholarPubMed
Foultier, B., Troisfontaines, P., Muller, S., Opperdoes, F. R. and Cornelis, G. R. (2002). Characterization of the ysa pathogenicity locus in the chromosome of Yersinia enterocolitica and phylogeny analysis of type III secretion systems. J Mol Evol, 55, 37–51.CrossRefGoogle ScholarPubMed
Freeman, J. A., Rappl, C., Kuhle, V., Hensel, M. and Miller, S. I. (2002). SpiC is required for translocation of Salmonella Pathogenicity Island 2 effectors and secretion of translocon proteins SseB and SseC. J Bacteriol, 184, 4971–80.CrossRefGoogle ScholarPubMed
Fu, Y. and Galan, J. E. (1999). A Salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature, 401, 293–7.CrossRefGoogle ScholarPubMed
Galan, J. E. (2001). Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol, 17, 53–86.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
Garcia-del Portillo, F., Zwick, M. B., Leung, K. Y. and Finlay, B. B. (1993). Salmonella induces the formation of filamentous structures containing lysosomal membrane glycoproteins in epithelial cells. Proc Natl Acad Sci USA, 90, 10544–8.CrossRefGoogle ScholarPubMed
Ginocchio, C. C., Rahn, K., Clarke, R. C. and Galan, J. E. (1997). Naturally occurring deletions in the centisome 63 pathogenicity island of environmental isolates of Salmonella spp. Infect Immun, 65, 1267–72.Google ScholarPubMed
Groisman, E. A. and Ochman, H. (1993). Cognate gene clusters govern invasion of host epithelial cells by Salmonella typhimurium and Shigella flexneri. EMBO J, 12, 3779–87.Google ScholarPubMed
Groisman, E. A. and Ochman, H. (1997). How Salmonella became a pathogen. Trends Microbiol, 5, 343–9.CrossRefGoogle ScholarPubMed
Hacker, J., Knapp, S. and Goebel, W. (1983). Spontaneous deletions and flanking regions of the chromosomally inherited hemolysin determinant of an Escherichia coli O6 strain. J Bacteriol, 154, 1145–52.Google ScholarPubMed
Hansen-Wester, I. and Hensel, M. (2002). Genome-based identification of chromosomal regions specific for Salmonella spp. Infect Immun, 70, 2351–60.CrossRefGoogle ScholarPubMed
Hansen-Wester, I., Stecher, B. and Hensel, M. (2002). Analyses of the evolutionary distribution of Salmonella translocated effectors. Infect Immun, 70, 1619–22.CrossRefGoogle ScholarPubMed
Hardt, W. D., Chen, L. M., Schuebel, K. E., Bustelo, X. R. and Galan, J. E. (1998). S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell, 93, 815–26.CrossRefGoogle ScholarPubMed
Hensel, M., Hinsley, A. P., Nikolaus, T., Sawers, G. and Berks, B. C. (1999a). The genetic basis of tetrathionate respiration in Salmonella typhimurium. Mol Microbiol, 32, 275–88.CrossRefGoogle Scholar
Hensel, M., Nikolaus, T. and Egelseer, C. (1999b). Molecular and functional analysis indicates a mosaic structure of Salmonella Pathogenicity Island 2. Mol Microbiol, 31, 489–98.CrossRefGoogle Scholar
Hensel, M., Shea, J. E., Bäumler, A. J.et al. (1997). Analysis of the boundaries of Salmonella pathogenicity island 2 and the corresponding chromosomal region of Escherichia coli K-12. J Bacteriol, 179, 1105–11.CrossRefGoogle ScholarPubMed
Hensel, M., Shea, J. E., Gleeson, C.et al. (1995). Simultaneous identification of bacterial virulence genes by negative selection. Science, 269, 400–3.CrossRefGoogle ScholarPubMed
Hersh, D., Monack, D. M., Smith, M. R.et al. (1999). The Salmonella invasin SipB induces macrophage apoptosis by binding to Caspase-1. Proc Natl Acad Sci USA, 96, 2396–401.CrossRefGoogle ScholarPubMed
Hindle, Z., Chatfield, S. N., Phillimore, J.et al. (2002). Characterization of Salmonella enterica derivatives harboring defined aroC and Salmonella Pathogenicity Island 2 type III secretion system (ssaV) mutations by immunization of healthy volunteers. Infect Immun, 70, 3457–67.CrossRefGoogle ScholarPubMed
Hueck, C. J. (1998). Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev, 62, 379–433.Google ScholarPubMed
Jones, M. A., Wood, M. W., Mullan, P. B.et al. (1998). Secreted effector proteins of Salmonella dublin act in concert to induce enteritis. Infect Immun, 66, 5799–804.Google ScholarPubMed
Knodler, L. A. and Finlay, B. B. (2001). Salmonella and apoptosis: to live or let die? Microbes Infect, 3, 1321–6.CrossRefGoogle ScholarPubMed
Knodler, L. A., Celli, J., Hardt, W. D.et al. (2002). Salmonella effectors within a single pathogenicity island are differentially expressed and translocated by separate type III secretion systems. Mol Microbiol, 43, 1089–103.CrossRefGoogle ScholarPubMed
Kubori, T., Matsushima, Y., Nakamura, D., Galan, J. E. and Aizawa, S. I. (1998). Supramolecular structure of the Salmonella typhimurium type III protein secretion system. Science, 280, 602–5.CrossRefGoogle ScholarPubMed
Kuhle, V. and Hensel, M. (2002). SseF and SseG are translocated effectors of the type III secretion system of Salmonella pathogenicity island 2 that modulate aggregation of endosomal compartments. Cell Microbiol, 4, 813–24.CrossRefGoogle ScholarPubMed
Lee, A. K., Detweiler, C. S. and Falkow, S. (2000). OmpR regulates the two-component system SsrA-SsrB in Salmonella pathogenicity island 2. J. Bacteriol, 182, 771–81.CrossRefGoogle ScholarPubMed
Lucas, R. L. and Lee, C. A. (2000). Unravelling the mysteries of virulence gene regulation in Salmonella typhimurium. Mol Microbiol, 36, 1024–33.CrossRefGoogle ScholarPubMed
Medina, E., Paglia, P., Nikolaus, T.et al. (1999). Pathogenicity Island 2 mutants of Salmonella typhimurium are efficient carriers for heterologous antigens and enable modulation of immune responses. Infect Immun, 67, 1093–9.Google 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
Mills, D. M., Bajaj, V. and Lee, C. A. (1995). A 40 kb chromosomal fragment encoding Salmonella typhimurium invasion genes is absent from the corresponding region of the Escherichia coli K-12 chromosome. Mol Microbiol, 15, 749–59.CrossRefGoogle Scholar
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 (SPI-1), SPI-5, and sopE2. J Bacteriol, 183, 2348–58.CrossRefGoogle Scholar
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
Monack, D. M., Detweiler, C. S. and Falkow, S. (2001). Salmonella pathogenicity island 2-dependent macrophage death is mediated in part by the host cysteine protease Caspase-1. Cell Microbiol, 3, 825–37.CrossRefGoogle ScholarPubMed
Monack, D. M., Hersh, D., Ghori, N.et al. (2000). Salmonella exploits Caspase-1 to colonize Peyer's patches in a murine typhoid model. J Exp Med, 192, 249–58.CrossRefGoogle Scholar
Moncrief, M. B. and Maguire, M. E. (1998). Magnesium and the role of MgtC in growth of Salmonella typhimurium. Infect Immun, 66, 3802–9.Google ScholarPubMed
Norris, F. A., Wilson, M. P., Wallis, T. S., Galyov, E. E. and Majerus, P. W. (1998). SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc Natl Acad Sci USA, 95, 14057–9.CrossRefGoogle ScholarPubMed
Ochman, H. and Groisman, E. A. (1996). Distribution of pathogenicity islands in Salmonella spp. Infect Immun, 64, 5410–12.Google 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
Oelschlaeger, T. A., Zhang, D., Schubert, S.et al. (2003). The High-Pathogenicity Island is absent in human pathogens of Salmonella enterica subspecies I but present in isolates of subspecies III and VI. J Bacteriol, 185, 1107–11.CrossRefGoogle ScholarPubMed
Parkhill, J., Dougan, G., James, K. D. (2001a). Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature, 413, 848–52.CrossRefGoogle Scholar
Parkhill, J., Wren, B. W., Thomson, N. R. (2001b). Genome sequence of Yersinia pestis, the causative agent of plague. Nature, 413, 523–7.CrossRefGoogle Scholar
Pickard, D., Wain, J., Baker, S.et al. (2003). Composition, acquisition, and distribution of the Vi exopolysaccharide-encoding Salmonella enterica pathogenicity island SPI-7. J Bacteriol, 185, 5055–65.CrossRefGoogle ScholarPubMed
Rappl, C., Deiwick, J. and Hensel, M. (2003). Acidic pH is required for the functional assembly of the type III secretion system encoded by Salmonella pathogenicity island 2. FEMS Microbiol. Lett, 226, 363–72.CrossRefGoogle ScholarPubMed
Rescigno, M., Urbano, M., Valzasina, B.et al. (2001). Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol, 2, 361–7.CrossRefGoogle ScholarPubMed
Schmidt, H. and Hensel, M. (2004). Pathogenicity islands in bacterial pathogenesis. Clin Microbiol. Rev, 17, 14–56.CrossRefGoogle ScholarPubMed
Shea, J. E., Beuzon, C. R., Gleeson, C., Mundy, R. and Holden, D. W. (1999). Influence of the Salmonella typhimurium Pathogenicity Island 2 type III secretion system on bacterial growth in the mouse. Infect Immun, 67, 213–19.Google 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
Snavely, M. D., Miller, C. G. and Maguire, M. E. (1991). The mgtB Mg2+ transport locus of Salmonella typhimurium encodes a P-type ATPase. J Biol Chem, 266, 815–23.Google ScholarPubMed
Stevens, M. P., Wood, M. W., Taylor, L. A.et al. (2002). An Inv/Mxi-Spa-like type III protein secretion system in Burkholderia pseudomallei modulates intracellular behaviour of the pathogen. Mol Microbiol, 46, 649–59.CrossRefGoogle ScholarPubMed
Townsend, S. M., Kramer, N. E., Edwards, R.et al. (2001). Salmonella enterica serovar Typhi possesses a unique repertoire of fimbrial gene sequences. Infect Immun, 69, 2894–901.CrossRefGoogle ScholarPubMed
Uchiya, K., Barbieri, M. A., Funato, K.et al. (1999). A Salmonella virulence protein that inhibits cellular trafficking. EMBO J, 18, 3924–33.CrossRefGoogle ScholarPubMed
Vazquez-Torres, A., Jones-Carson, J., Bäumler, A. J.et al. (1999). Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature, 401, 804–8.Google ScholarPubMed
Vazquez-Torres, A., Xu, Y., Jones-Carson, J.et al. (2000). Salmonella Pathogenicity Island 2-dependent evasion of the phagocyte NADPH oxidase. Science, 287, 1655–8.CrossRefGoogle ScholarPubMed
Wallis, T. S. and Galyov, E. E. (2000). Molecular basis of Salmonella-induced enteritis. Mol Microbiol, 36, 997–1005.CrossRefGoogle ScholarPubMed
Waterman, S. R. and Holden, D. W. (2003). Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol, 5, 501–11.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., 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
Yu, X. J., Ruiz-Albert, J., Unsworth, K. E.et al. (2002). SpiC is required for secretion of Salmonella Pathogenicity Island 2 type III secretion system proteins. Cell Microbiol, 4, 531–40.CrossRefGoogle ScholarPubMed
Zhang, X. L., Morris, C. and Hackett, J. (1997). Molecular cloning, nucleotide sequence, and function of a site-specific recombinase encoded in the major ‘pathogenicity island’ of Salmonella typhi. Gene, 202, 139–46.CrossRefGoogle ScholarPubMed
Zhang, X. L., Tsui, I. S., Yip, C. M.et al. (2000). Salmonella enterica serovar typhi uses type IVB pili to enter human intestinal epithelial cells. Infect Immun, 68, 3067–73.CrossRefGoogle ScholarPubMed
Zhou, D., Hardt, W. D. and Galan, J. E. (1999). Salmonella typhimurium encodes a putative iron transport system within the centisome 63 pathogenicity island. Infect Immun, 67, 1974–81.Google ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure [email protected] is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×