Abstract
Three species of bacteria in the genus Yersinia are pathogenic for humans. Yersinia enterocolitica and Yersinia pseudotuberculosis cause enteric diseases. Yersinia pestis causes the disease known as plague. Studies utilizing DNA hybridization and multilocus DNA sequencing show that Y. pestis and Y. pseudotuberculosis are closely related at the genetic level, while Y. enterocolitica represents a distinct evolutionary lineage. It has been known for some time that Y. pestis, Y. pseudotuberculosis, and Y. enterocolitica encode homologous type III secretion system (TTSS) gene clusters on a common virulence plasmid. More recently, genome scale sequence analysis has revealed that Y. pestis and Y. pseudotuberculosis also encode homologous TTSS gene clusters on their chromosomes. In this chapter, we describe the genetic organization of TTSSs in Y. pestis and Y. pseudotuberculosis. We also describe several genetic changes in these TTSSs that have occurred during the evolution of Y. pseudotuberculosis and Y. pestis, and discuss the implications of these changes on our understanding of TTSS function during Yersinia pathogenesis.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Preview
Unable to display preview. Download preview PDF.
References
Brubaker, R. R. (1991) Factors promoting acute and chronic diseases caused by yersiniae. Clin. Microbiol. Rev. 4, 309–324.
Skurnik, M., Peippo, A., and Ervela, E. (2000) Characterization of the O-antigen gene clusters of Yersinia pseudotuberculosis and the cryptic O-antigen gene cluster of Yersinia pestis shows that the plague bacillus is most closely related to and has evolved from Y. pseudotuberculosis serotype O:1b. Mol. Microbiol. 37, 316–330.
Perry, R. D. and Fetherston, J. D. (1997) Yersinia pestis-etiologic agent of plague. Clin. Microbiol. Rev. 10, 35–66.
Zhou, D., Tong, Z., Song, Y., et al. (2004) Genetics of metabolic variations between Yersinia pestis biovars and the proposal of a new biovar, Microtus. J. Bacteriol. 186, 5147–5152.
Bottone, E. J. (1997) Yersinia enterocolitica: the charisma continues. Clin. Microbiol. Rev. 10, 257–276.
Clark, M. A., Hirst, B. H., and Jepson, M. A. (1998) M-cell surface beta1 integrin expression and invasin-mediated targeting of Yersinia pseudotuberculosis to mouse Peyer’s patch M cells. Infect. Immun. 66, 1237–1243.
Marra, A. and Isberg, R. R. (1997) Invasin-dependent and invasin-independent pathways for translocation of Yersinia pseudotuberculosis across the Peyer’s patch intestinal epithelium. Infect. Immun. 65, 3412–3421.
Pepe, J. and Miller, V. L. (1993) Yersinia enterocolitica invasin: a primary role in the initiation of infection. Proc. Natl. Acad. Sci. USA 90, 6473–6477.
Cavanaugh, D. C. and Randall, R. (1959) The role of multiplication of Pasteurella pestis in mononuclear phagocytes in the pathogenesis of fleaborne plague. J. Immunol. 85, 348–363.
Achtman, M., Zurth, K., Morelli, G., Torrea, G., Guiyoule, A., and Carniel, E. (1999) Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. USA 96, 14,043–14,048.
Pujol, C. and Bliska, J. B. (2005) Turning Yersinia pathogenesis outside in: subversion of macrophage function by intracellular yersiniae. Clin. Immunol. 114, 216–226.
Carniel, E. (1999) The Yersinia high-pathogenicity island. Int. Microbiol. 2, 161–167.
Wren, B. W. (2003) The yersiniae-a model genus to study the rapid evolution of bacterial pathogens. Nat. Rev. Microbiol. 1, 55–64.
Carniel, E. (2002) Plasmids and pathogenicity islands of Yersinia. Curr. Top. Microbiol. Immunol. 264, 89–108.
Song, Y., Tong, Z., Wang, J., et al. (2004) Complete genome sequence of Yersinia pestis strain 91001, an isolate avirulent to humans. DNA Res. 11, 179–197.
Chain, P. S., Carniel, E., Larimer, F. W., et al. (2004) Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc. Natl. Acad. Sci. USA 101, 13,826–13,831.
Deng, W., Burland, V., Plunkett, G. 3rd, et al. (2002) Genome sequence of Yersinia pestis KIM. J. Bacteriol. 184, 4601–4611.
Parkhill, J., Wren, B. W., Thomson, N. R., et al. (2001) Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413, 523–527.
Zhou, D., Han, Y., Song, Y., et al. (2004) DNA microarray analysis of genome dynamics in Yersinia pestis: insights into bacterial genome microevolution and niche adaptation. J. Bacteriol. 186, 5138–5146.
Une, T. and Brubaker, R. R. (1984) In vivo comparison of avirulent Vwa- and Pgm- or Pstr phenotypes of yersiniae. Infect. Immun. 43, 895–900.
Hueck, C. J. (1998) Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62, 379–433.
Young, G. M., Schmiel, D. H., and Miller, V. L. (1999) A new pathway for the secretion of virulence factors by bacteria: the flagellar export apparatus functions as a protein-secretion system. Proc. Natl. Acad. Sci. USA 96, 6456–6461.
Lee, S. H. and Galan, J. E. (2004) Salmonella type III secretion-associated chaperones confer secretion-pathway specificity. Mol. Microbiol. 51, 483–495.
Macnab, R. M. (1999) The bacterial flagellum: reversible rotary propellor and type III export apparatus. J. Bacteriol. 181, 7149–7153.
Blocker, A., Komoriya, K., and Aizawa, S. (2003) Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc. Natl. Acad. Sci. USA 100, 3027–3030.
Gophna, U., Ron, E. Z., and Graur, D. (2003) Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene 312, 151–163.
Aizawa, S. I. (2001) Bacterial flagella and type III secretion systems. FEMS Microbiol. Lett. 202, 157–164.
Nguyen, L., Paulsen, I. T., Tchieu, J., Hueck, C. J., and Saier, M. H. Jr. (2000) Phylogenetic analyses of the constituents of Type III protein secretion systems. J. Mol. Microbiol. Biotechnol. 2, 125–144.
Young, G. M., Badger, J. L., and Miller, V. L. (2000) Motility is required to initiate host cell invasion by Yersinia enterocolitica. Infect. Immun. 68, 4323–4326.
Hinchliffe, S._J., Isherwood, K. E., Stabler, R. A., et al. (2003) Application of DNA microarrays to study the evolutionary genomics of Yersinia pestis and Yersinia pseudotuberculosis. Genome Res. 13, 2018–2029.
Ramamurthi, K. S. and Schneewind, O. (2002) Type III protein secretion in Yersinia species. Annu. Rev. Cell. Dev. Biol. 18, 107–133.
Cornelis, G. R. (2002) Yersinia type III secretion: send in the effectors. J. Cell. Biol. 158, 401–408.
Plano, G. V., Day, J. B., and Ferracci, F. (2001) Type III export: new uses for an old pathway. Mol. Microbiol. 40, 284–293.
Snellings, N. J., Popek, M., and Lindler, L. E. (2001) Complete DNA sequence of Yersinia enterocolitica serotype O:8 low-calcium-response plasmid reveals a new virulence plasmid-associated replicon. Infect. Immun. 69, 4627–4638.
Isberg, R. R. and Van Nhieu, G. T. (1995) The mechanism of phagocytic uptake promoted by invasin-integrin interaction. Trends Cell Biol. 5, 120–124.
Zhang, Y. and Bliska, J. B. (2003) Role of Toll-like receptor signaling in the apoptotic response of macrophages to Yersinia infection. Infect. Immun. 71, 1513–1519.
Haase, R., Kirschning, C. J., Sing, A., et al. (2003) A dominant role of Toll-like receptor 4 in the signaling of apoptosis in bacteria-faced macrophages. J. Immunol. 171, 4294–4303.
Viboud, G. I., So, S. S., Ryndak, M. B., and Bliska, J. B. (2003) Proinflammatory signalling stimulated by the type III translocation factor YopB is counteracted by multiple effectors in epithelial cells infected with Yersinia pseudotuberculosis. Mol. Microbiol. 47, 1305–1315.
Brubaker, R. R. (2003) Interleukin-10 and inhibition of innate immunity to Yersiniae: roles of Yops and LcrV (V antigen). Infect. Immun. 71, 3673–3681.
Boquet, P. (2000) Small GTP binding proteins and bacterial virulence. Microbes Infect. 2, 837–844.
Bishop, A. L. and Hall, A. (2000) Rho GTPases and their effector proteins. Biochem. J. 348(pt 2), 241–255.
Black, D. S. and Bliska, J. B. (2000) The RhoGAP activity of the Yersinia pseudotuberculosis cytotoxin YopE is required for antiphagocytic function and virulence. Mol. Microbiol. 37, 515–527.
Juris, S. J., Shao, F., and Dixon, J. E. (2002) Yersinia effectors target mammalian signalling pathways. Cell. Microbiol. 4, 201–211.
Aepfelbacher, M., Trasak, C., Wilharm, G., et al. (2003) Characterization of YopT effects on Rho GTPases in Yersinia enterocolitica-infected cells. J. Biol. Chem. 278, 33,217–33,223.
Andor, A., Trulzsch, K., Essler, M., et al. (2001) YopE of Yersinia, a GAP for Rho GTPases, selectively modulates Rac-dependent actin structures in endothelial cells. Cell Microbiol. 3, 301–310.
Iriarte, M. and Cornelis, G. (1998) YopT, a new Yersinia Yop effector protein, affects the cytoskeleton of host cells. Mol. Microbiol. 29, 915–929.
Trulzsch, K., et al. (2004) Contribution of the major secreted Yops of Yersinia enterocolitica O:8 to pathogenicity in the mouse infection model. Infect. Immun. 72, 5227–5234.
Shao, F., Merritt, P. M., Bao, Z., Innes, R. W., and Dixon, J. E. (2002) A Yersinia effector and a Pseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109, 575–588.
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.
Miao, E. A., Scherer, C. A., Tsolis, R. M., et al. (1999) Salmonella typhimurium leucinerich repeat proteins are targeted to the SPI1 and SPI2 type III secretion systems. Mol. Microbiol. 34, 850–864.
Waterman, S. R. and Holden, D. W. (2003) Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol. 5, 501–511.
Pujol, C. and Bliska, J. B. (2003) The ability to replicate in macrophages is conserved between Yersinia pestis and Yersinia pseudotuberculosis. Infect. Immun. 71, 5892–5899.
Author information
Authors and Affiliations
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2006 Humana Press Inc., Totowa, NJ
About this chapter
Cite this chapter
Bliska, J.B., Ryndak, M.B., Grabenstein, J.P. (2006). Type III Secretion Systems in Yersinia pestis and Yersinia pseudotuberculosis . In: Chan, V.L., Sherman, P.M., Bourke, B. (eds) Bacterial Genomes and Infectious Diseases. Humana Press. https://doi.org/10.1007/978-1-59745-152-9_12
Download citation
DOI: https://doi.org/10.1007/978-1-59745-152-9_12
Publisher Name: Humana Press
Print ISBN: 978-1-58829-496-8
Online ISBN: 978-1-59745-152-9
eBook Packages: MedicineMedicine (R0)