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8 - Pathogenic Yersinia: Stepwise Gain of Virulence due to Sequential Acquisition of Mobile Genetic Elements

from PART III - Paradigms of Bacterial Evolution

Published online by Cambridge University Press:  16 September 2009

Michael Hensel
Affiliation:
Friedrich-Alexander-Universität Erlangen-Nürnberg, Germany
Herbert Schmidt
Affiliation:
Universität Hohenheim, Stuttgart
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Summary

INTRODUCTION

Acquisition of genetic elements by horizontal transfer has played a major role in the evolution, virulence, and transmission of many bacteria. The genus Yersinia represents a very good example of a bacterial group whose pathogenicity and transmission progressively evolved with the gradual acquisition of foreign genetic elements.

Yersinia are Gram-negative bacteria that belong to the family Enterobacteriaceae. The genus is composed of 12 species that can be differentiated into pathogenic (Y. pseudotuberculosis, Y. enterocolitica, and Y. pestis) and non-pathogenic (Y. intermedia, Y. kristensenii, Y. fredericksenii, Y. aldovae, Y. rohdei, Y. bercovieri, Y. mollaretii, and Y. aleksiciae) species (Figure 8.1; see also color plate after p. 174). Y. ruckeri is not discussed here because the inclusion of this fish pathogen in the genus Yersinia is still controversial. Like several other species of Enterobacteriaceae, Y. enterocolitica and Y. pseudotuberculosis are true enteropathogens, while Y. pestis is the causative agent of plague. This chapter focuses on the evolution and lateral gene transfer in these three pathogenic species.

Y. enterocolitica and Y. pseudotuberculosis are widely spread in countries with temperate climates. They are transmitted by the fecal-oral route and cause intestinal symptoms such as abdominal pain (especially Y. pseudotuberculosis), diarrhea (especially Y. enterocolitica), and fever, usually of moderate intensity.

The species Y. enterocolitica is subdivided into six biotypes (1A, 1B, and 2 to 5). All strains are pathogenic except those of biotype 1A. Pathogenic Y. enterocolitica can be further subdivided into low- and high-pathogenicity strains.

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Publisher: Cambridge University Press
Print publication year: 2008

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References

Achtman, M., Zurth, K., Morelli, C., et al. (1999). Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis. Proc Natl Acad Sci USA, 96, 14043–8.CrossRefGoogle ScholarPubMed
Achtman, M., Morelli, G., Zhu, P., et al. (2004). Microevolution and history of the plague bacillus, Yersinia pestis. Proc Natl Acad Sci USA, 101, 17837–42.CrossRefGoogle ScholarPubMed
Aepfelbacher, M. (2004). Modulation of Rho GTPases by type III secretion system translocated effectors of Yersinia. Rev Physiol Biochem Pharmacol, 152, 65–77.CrossRefGoogle ScholarPubMed
Aili, M., Hallberg, B., Wolf-Watz, H., and Rosqvist, R. (2002). GAP activity of Yersinia YopE. Methods Enzymol, 359, 359–70.CrossRefGoogle Scholar
Antonenka, U., Nolting, C., Heesemann, J., and Rakin, A. (2005). Horizontal transfer of Yersinia high-pathogenicity island by the conjugative RP4 attB target-presenting shuttle plasmid. Mol Microbiol, 57, 727–34.CrossRefGoogle ScholarPubMed
Bercovier, H., Mollaret, H. H., Alonso, J. M., et al. (1980). Intra- and interspecies relatedness of Yersinia pestis by DNA hybridization and its relationship to Yersinia pseudotuberculosis. Curr Microbiol, 4, 225–9.CrossRefGoogle Scholar
Carniel, E. (2003). Evolution of pathogenic Yersinia, some lights in the dark. Adv Exp Med Biol, 529, 3–12.CrossRefGoogle Scholar
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, 13826–31.CrossRefGoogle ScholarPubMed
Chain, P. S. G., Hu, P., Malfatti, S. A., et al. (2006). Complete genome sequence of Yersinia pestis strains Antiqua and Nepal516: Evidence of gene reduction in an emerging pathogen. J Bacteriol, 188, 4453–63.CrossRefGoogle Scholar
Collyn, F., Marceau, M., and Simonet, M. (2004). YAPI, a new Pathogenicity Island in enteropathogenic yersiniae. In Carniel, E., and Hinnebusch, B. J. (Eds.) Yersinia molecular and cellular biology. Horizon Bioscience.Google Scholar
Collyn, F., Fukushima, H., Carnoy, C., Simonet, M., and Vincent, P. (2005). Linkage of the horizontally acquired ypm and pil genes in Yersinia pseudotuberculosis. Infect Immun, 73, 2556–8.CrossRefGoogle ScholarPubMed
Collyn, F., Guy, L., Marceau, M., Simonet, M., and Roten, C. A. (2006). Describing ancient horizontal gene transfers at the nucleotide and gene levels by comparative pathogenicity island genometrics. Bioinformatics, 22, 1072–9.CrossRefGoogle ScholarPubMed
Darby, C., Ananth, S. L., Tan, L., and Hinnebusch, B. J. (2005). Identification of gmhA, a Yersinia pestis gene required for flea blockage, by using a Caenorhabditis elegans biofilm system. Infect Immun, 73, 7236–42.CrossRefGoogle ScholarPubMed
Deng, W., Burland, V., Plunkett, G., et al. (2002). Genome sequence of Yersinia pestis KIM. J Bacteriol, 184, 4601–11.CrossRefGoogle ScholarPubMed
Derbise, A., Chenal-Francisque, V., Pouillot, F., et al. (2007). A horizontally acquired filamentous phage contributes to the pathogenicity of the plague bacillus. Mol Microbiol, 63, 1145–57.CrossRefGoogle ScholarPubMed
Drancourt, M., Roux, W., Dang, L. V., et al. (2004). Genotyping, orientalis-like Yersinia pestis, and plague pandemics. Emerg Infect Dis, 10, 1585–92.CrossRefGoogle ScholarPubMed
Fallman, M., and Gustavsson, A. (2005). Cellular mechanisms of bacterial internalization counteracted by Yersinia. Int Rev Cytol, 246, 135–88.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
Golubov, A., Neubauer, H., Nolting, C., Heesemann, J., and Rakin, A. (2004). Structural organization of the pFra virulence-associated plasmid of rhamnose-positive Yersinia pestis. Infect Immun, 72, 5613–21.CrossRefGoogle ScholarPubMed
Hacker, J., Blum-Oehler, G., Mühldorfer, I., and Tschäpe, H. (1997). Pathogenicity islands of virulent bacteria: structure, function, and impact on microbial evolution. Mol Microbiol, 23, 1089–97.CrossRefGoogle ScholarPubMed
Heesemann, J., Sing, A., and Trülzsch, K. (2006). Yersinia's stratagem: targeting innate and adaptive immune defense. Curr Opin Microbiol, 9, 55–61.CrossRefGoogle ScholarPubMed
Hinnebusch, B. J. (2004). The evolution of flea-borne transmission in Yersinia pestis. In Carniel, E., and Hinnebusch, B. J. (Eds.). Yersinia molecular and cellular biology. Horizon Bioscience.Google Scholar
Hinnebusch, B. J., Perry, R. D., and Schwan, T. G. (1996). Role of the Yersinia pestis hemin storage (hms) locus in the transmission of plague by fleas. Science, 273, 367–70.CrossRefGoogle ScholarPubMed
Hu, P., Elliott, J., McCready, P., et al. (1998). Structural organization of virulence-associated plasmids of Yersinia pestis. J Bacteriol, 180, 5192–202.Google ScholarPubMed
Korhonen, T. K., Kukkonen, M., Virkola, R., et al. (2004). The plasminogen activator Pla of Yersinia pestis: localized proteolysis and systemic spread. In Carniel, E., and Hinnebusch, B. J. (Eds.). Yersinia molecular and cellular biology. Horizon Bioscience.Google Scholar
Kutyrev, V., Mehigh, R. J., Motin, V. L., et al. (1999). Expression of the plague plasminogen activator in Yersinia pseudotuberculosis and Escherichia coli. Infect Immun, 67, 1359–67.Google ScholarPubMed
Lesic, B., and Carniel, E. (2004). The High-Pathogenicity Island: a broad-host-range pathogenicity island. In Carniel, E., and Hinnebusch, B. J. (Eds.). Yersinia molecular and cellular biology. Horizon Bioscience.Google Scholar
Lesic, B., and Carniel, E. (2005). Horizontal transfer of the high-pathogenicity island of Yersinia pseudotuberculosis. J Bacteriol, 187, 3352–8.CrossRefGoogle ScholarPubMed
Lindler, L. E. (2004). The Yersinia pestis-specific plasmids pFra and pPla. In Carniel, E., and Hinnebusch, B. J., (Eds.) Yersinia molecular and cellular biology. Horizon Bioscience.Google Scholar
Lorange, E. A., Race, B. L., Sebbane, F., and Hinnebusch, B. J. (2005). Poor vector competence of fleas and the evolution of hypervirulence in Yersinia pestis. J Infect Dis, 191, 1907–12.CrossRefGoogle ScholarPubMed
MacIntyre, S., Knight, S. D., and Fooks, L. J. (2004). Structure, assembly and application of the polymeric F1 antigen of Yersinia pestis. In Carniel, E., and Hinnebusch, B. J. (Eds.). Yersinia molecular and cellular biology. Horizon Bioscience.Google Scholar
Marenne, M.-N., Mota, L. J., and Cornelis, G. R. (2004). The pYV plasmid and the Ysc-Yop type III secretion system. In Carniel, E., and Hinnebusch, B. J. (Eds.). Yersinia molecular and cellular biology. Horizon Bioscience.Google Scholar
Navarro, L., Alto, N. M., and Dixon, J. E. (2005). Functions of the Yersinia effector proteins in inhibiting host immune responses. Curr Opin Microbiol, 8, 21–7.CrossRefGoogle ScholarPubMed
Parkhill, J., Wren, B. W., Thomson, N. R., et al. (2001). Genome sequence of Yersinia pestis, the causative agent of plague. Nature, 413, 523–7.CrossRefGoogle ScholarPubMed
Perry, R. D., Straley, S. C., Fetherston, J. D., et al. (1998). DNA sequencing and analysis of the low-Ca2+-response plasmid pCD1 of Yersinia pestis KIM5. Infect Immun, 66, 4611–23.Google ScholarPubMed
Pouillot, F., Derbise, A., Kukkonen, M., et al. (2005). Evaluation of O-antigen inactivation on Pla activity and virulence of Yersinia pseudotuberculosis harbouring the pPla plasmid. Microbiology, 151, 3759–68.CrossRefGoogle ScholarPubMed
Prentice, M. B., James, K. D., Parkhill, J., et al. (2001). Yersinia pestis pFra shows biovar-specific differences and recent common ancestry with a Salmonella enterica serovar typhi plasmid. J Bacteriol, 183, 2586–94.CrossRefGoogle ScholarPubMed
Ramamurthi, K. S., and Schneewind, O. (2002). Type III protein secretion in Yersinia species. Ann Rev Cell Dev Biol, 18, 107–33.CrossRefGoogle ScholarPubMed
Schubert, S., Dufke, S., Sorsa, J., and Heesemann, J. (2004a). A novel integrative and conjugative element (ICE) of Escherichia coli: the putative progenitor of the Yersinia high-pathogenicity island. Mol Microbiol, 51, 837–48.CrossRefGoogle ScholarPubMed
Schubert, S., Rakin, A., and Heesemann, J. (2004b). The Yersinia high-pathogenicity island (HPI): evolutionary and functional aspects. Int J Med Microbiol, 294, 83–94.CrossRefGoogle ScholarPubMed
Sebbane, F., Jarrett, C. O., Gardner, D., Long, D., and Hinnebusch, B. J. (2006). Role of the Yersinia pestis plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea-borne plague. Proc Natl Acad Sci USA, 103, 5526–30.CrossRefGoogle ScholarPubMed
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 Yersinia pseudotuberculosis serotype O : 1b. Mol Microbiol, 37, 316–30.CrossRefGoogle ScholarPubMed
Sodeinde, O. A., Subrahmanyam, Y. V. B. K., Stark, K., et al. (1992). A surface protease and the invasive character of plague. Science, 258, 1004–7.CrossRefGoogle ScholarPubMed
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, 179–97.CrossRefGoogle Scholar
Viboud, G. I., and Bliska, J. B. (2005).Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu Rev Microbiol, 59, 69–89.CrossRefGoogle ScholarPubMed

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