Skip to main content Accessibility help
×
Hostname: page-component-848d4c4894-p2v8j Total loading time: 0.001 Render date: 2024-06-02T14:43:32.003Z Has data issue: false hasContentIssue false

2 - Evolution of bacterial pathogens

from Part I - Introduction to the host and bacterial pathogens

Published online by Cambridge University Press:  12 August 2009

Anthony T. Maurelli
Affiliation:
Department of Microbiology and Immunology, F. Hébert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda MD 20814-4799, USA
Beth A. McCormick
Affiliation:
Harvard University, Massachusetts
Get access

Summary

INTRODUCTION

The evolution of bacterial pathogens is essentially the story of how all life evolves. It is a story of mutation and selection, of adaptation and survival, of incremental genetic changes and quantum leaps in genome content. All organisms evolve, but the evolution of microbes is the best studied. The short generation times of microbes and the ability to grow individual populations to large numbers allow researchers to study rare events over many generations – something that is next to impossible with larger, more complex organisms such as fruit flies, mice, and humans.

This chapter begins with a brief overview of the principles of mutation and selection in bacteria. This background will prepare the reader for the subsequent sections that will discuss the various forms of horizontal gene transfer (HGT) and how they each contribute to bacterial evolution. Specific examples are presented to give the reader insight into the enormous power of genetic selection as well as the great diversity of pathways that bacteria take in adapting to their environment. We also highlight some recurrent themes in bacterial pathogenesis. The chapter concludes with a discussion of a new paradigm of bacterial pathogen evolution that involves the loss of gene function as an adaptation to colonization of the host. The concept of pathoadaptation is introduced and expanded to include selection for gene loss as the pathogen improves its fitness within the host niche.

Type
Chapter
Information
Bacterial-Epithelial Cell Cross-Talk
Molecular Mechanisms in Pathogenesis
, pp. 30 - 56
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

Akiba, T., Koyama, K., Ishiki, Y., Kimura, S., and Fukushima, T. (1960). On the mechanism of the development of multiple-drug resistant clones of Shigella. Jpn. J. Microbiol. 4, 219–227.CrossRefGoogle ScholarPubMed
Andersson, S. G., Zomorodipour, A., Andersson, J. O., et al. (1998). The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396, 133–140.CrossRefGoogle ScholarPubMed
Barbour, A. G. and Restrepo, B. I. (2000). Antigenic variation in vector-borne pathogens. Emerg. Infect. Dis. 6, 449–457.CrossRefGoogle ScholarPubMed
Barksdale, W. L. and Pappenheimer, A. M. Jr (1954). Phage–host relationships in nontoxigenic and toxigenic diphtheria bacilli. J. Bacteriol. 67, 220–232.Google Scholar
Berg, C. M., Berg, D. E., and Groisman, E. A. (1989). Transposable elements and the genetic engineering of bacteria. In Mobile DNA, ed. Berg, D. E. and Howe, M. M.. Washington, DC: American Society for Microbiology, pp. 879–925.Google Scholar
Bertin, P., Benhabiles, N., Krin, E., et al. (1999). The structural and functional organization of H-NS-like proteins is evolutionarily conserved in gram-negative bacteria. Mol. Microbiol. 31, 319–329.CrossRefGoogle ScholarPubMed
Bille, E., Zahar, J. R., Perrin, A., et al. (2005). A chromosomally integrated bacteriophage in invasive meningococci. J. Exp. Med. 201, 1905–1913.CrossRefGoogle ScholarPubMed
Brussow, 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
Casjens, S. (2003). Prophages and bacterial genomics: what have we learned so far?Mol. Microbiol. 49, 277–300.CrossRefGoogle ScholarPubMed
Cole, S. T., Eiglmeier, K., Parkhill, J., et al. (2001). Massive gene decay in the leprosy bacillus. Nature 409, 1007–1011.CrossRefGoogle ScholarPubMed
Cornelis, G. R., Boland, A., Boyd, A. P., et al. (1998). The virulence plasmid of Yersinia, an antihost genome. Microbiol. Mol. Biol. Rev. 62, 1315–1352.Google ScholarPubMed
Day, W. A. Jr, Fernandez, R. E., and Maurelli, A. T. (2001). Pathoadaptive mutations that enhance virulence: genetic organization of the cadA regions of Shigella spp. Infect. Immun. 69, 7471–7480.CrossRefGoogle ScholarPubMed
Dorman, C. J. and Porter, M. E. (1998). The Shigella virulence gene regulatory cascade: a paradigm of bacterial gene control mechanisms. Mol. Microbiol. 29, 677–684.CrossRefGoogle ScholarPubMed
Echeverria, P., Seriwatana, J., Taylor, D. N., et al. (1986). Plasmids coding for colonization factor antigens I and II, heat-labile enterotoxin, and heat-stable enterotoxin A2 in Escherichia coli. Infect. Immun. 51, 626–630.Google ScholarPubMed
Elliott, S. J., Sperandio, V., Giron, J. A., et al. (2000). The locus of enterocyte effacement (LEE)-encoded regulator controls expression of both LEE- and non-LEE-encoded virulence factors in enteropathogenic and enterohemorrhagic Escherichia coli. Infect. Immun. 68, 6115–6126.CrossRefGoogle Scholar
Feng, P., Lampel, K. A., Karch, H., and Whittam, T. S. (1998). Genotypic and phenotypic changes in the emergence of Escherichia coli O157:H7. J. Infect. Dis. 177, 1750–1753.CrossRefGoogle ScholarPubMed
Fernandez, I. M., Silva, M., Schuch, R., et al. (2001). Cadaverine prevents the escape of Shigella flexneri from the phagolysosome: a connection between bacterial dissemination and neutrophil transepithelial signaling. J. Infect. Dis. 184, 743–753.CrossRefGoogle ScholarPubMed
Freeman, V. J. (1951). Studies on the virulence of bacteriophage-infected strains of Corynebacterium diphtheriae. J. Bacteriol. 61, 675–688.Google ScholarPubMed
Grodberg, J. and Dunn, J. J. (1988). ompT encodes the Escherichia coli outer membrane protease that cleaves T7 RNA polymerase during purification. J. Bacteriol. 170, 1245–1253.CrossRefGoogle ScholarPubMed
Groisman, E. A. and Ochman, H. (1996). Pathogenicity islands: bacterial evolution in quantum leaps. Cell 87, 791–794.CrossRefGoogle ScholarPubMed
Groman, N. B. (1953). The relation of bacteriophage to the change of Corynebacterium diphtheriae from avirulence to virulence. Science 117, 297–299.CrossRefGoogle ScholarPubMed
Hacker, J. and Kaper, J. B. (2000). Pathogenicity islands and the evolution of microbes. Annu. Rev. Microbiol. 54, 641–679.CrossRefGoogle ScholarPubMed
Hedges, R. W. and Jacob, A. E. (1974). Transposition of ampicillin resistance from RP4 to other replicons. Mol. Gen. Genet. 132, 31–40.CrossRefGoogle ScholarPubMed
Hromockyj, A. E., Tucker, S. C., and Maurelli, A. T. (1992). Temperature regulation of Shigella virulence: identification of the repressor gene virR, an analogue of hns, and partial complementation by tyrosyl transfer RNA (tRNA1(Tyr)). Mol. Microbiol. 6, 2113–2124.CrossRefGoogle Scholar
Huan, P. T., Bastin, D. A., Whittle, B. L., Lindberg, A. A., and Verma, N. K. (1997). Molecular characterization of the genes involved in O-antigen modification, attachment, integration and excision in Shigella flexneri bacteriophage SfV. Gene 195, 217–227.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
Jin, Q., Yuan, Z., Xu, J., et al. (2002). Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. Nucleic Acids Res. 30, 4432–4441.CrossRefGoogle ScholarPubMed
Lan, R. and Reeves, P. R. (2002). Escherichia coli in disguise: molecular origins of Shigella. Microbes Infect. 4, 1125–1132.CrossRefGoogle ScholarPubMed
Lee, C. H., Hu, S. T., Swiatek, P. J., et al. (1985). Isolation of a novel transposon which carries the Escherichia coli enterotoxin STII gene. J. Bacteriol. 162, 615–620.Google ScholarPubMed
Lindsey, D. F., Mullin, D. A., and Walker, J. R. (1989). Characterization of the cryptic lambdoid prophage DLP12 of Escherichia coli and overlap of the DLP12 integrase gene with the tRNA gene argU. J. Bacteriol. 171, 6197–6205.CrossRefGoogle ScholarPubMed
Makino, S., Uchida, I., Terakado, N., Sasakawa, C., and Yoshikawa, M. (1989). Molecular characterization and protein analysis of the cap region, which is essential for encapsulation in Bacillus anthracis. J. Bacteriol. 171, 722–730.CrossRefGoogle ScholarPubMed
Maurelli, A. T. and Sansonetti, P. J. (1988). Identification of a chromosomal gene controlling temperature-regulated expression of Shigella virulence. Proc. Natl. Acad. Sci. U. S. A. 85, 2820–2824.CrossRefGoogle ScholarPubMed
Maurelli, A. T., Blackmon, B., and Curtiss, R. III (1984). Temperature-dependent expression of virulence genes in Shigella species. Infect. Immun. 43, 195–201.Google ScholarPubMed
Maurelli, A. T., Fernandez, R. E., Bloch, C. A., Rode, C. K., and Fasano, A. (1998). “Black holes” and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 95, 3943–3948.CrossRefGoogle ScholarPubMed
McCormick, B. A., Fernandez, M. I., Siber, A. M., and Maurelli, A. T. (1999). Inhibition of Shigella flexneri-induced transepithelial migration of polymorphonuclear leucocytes by cadaverine. Cell Microbiol. 1, 143–155.CrossRefGoogle ScholarPubMed
Mellies, J. L., Elliott, S. J., Sperandio, V., Donnenberg, M. S., and Kaper, J. B. (1999). The Per regulon of enteropathogenic Escherichia coli: identification of a regulatory cascade and a novel transcriptional activator, the locus of enterocyte effacement (LEE)-encoded regulator (Ler). Mol. Microbiol. 33, 296–306.CrossRefGoogle Scholar
Mitsuhashi, S., Harada, K., and Hashimoto, H. (1960). Multiple resistance of enteric bacteria and transmission of drug-resistance to other strains by mixed cultivation. Jpn. J. Exp. Med. 30, 179–184.Google ScholarPubMed
Moran, N. A. and Plague, G. R. (2004). Genomic changes following host restriction in bacteria. Curr. Opin. Genet. Dev. 14, 627–633.CrossRefGoogle ScholarPubMed
Nakata, N., Tobe, T., Fukuda, I., et al. (1993). The absence of a surface protease, OmpT, determines the intercellular spreading ability of Shigella: the relationship between the ompT and kcpA loci. Mol. Microbiol. 9, 459–468.CrossRefGoogle ScholarPubMed
Nakaya, R., Nakamura, A., and Murata, Y. (1960). Resistance to transfer agents in Shigella. Biochem. Biophys. Res. Commun. 3, 654–659.CrossRefGoogle ScholarPubMed
Ochman, H., Lawrence, J. G., and Groisman, E. A. (2000). Lateral gene transfer and the nature of bacterial innovation. Nature 405, 299–304.CrossRefGoogle ScholarPubMed
Ohnishi, M., Kurokawa, K., and Hayashi, T. (2001). Diversification of Escherichia coli genomes: are bacteriophages the major contributors?Trends Microbiol. 9, 481–485.CrossRefGoogle ScholarPubMed
Pupo, G. M., Karaolis, D. K., Lan, R., and Reeves, P. R. (1997). Evolutionary relationships among pathogenic and nonpathogenic Escherichia coli strains inferred from multilocus enzyme electrophoresis and mdh sequence studies. Infect. Immun. 65, 2685–2692.Google ScholarPubMed
Pupo, G. M., Lan, R., and Reeves, P. R. (2000). Multiple independent origins of Shigella clones of Escherichia coli and convergent evolution of many of their characteristics. Proc. Natl. Acad. Sci. U. S. A. 97, 10 567–10 572.CrossRefGoogle ScholarPubMed
Purdy, G. E. and Payne, S. M. (2001). The SHI-3 iron transport island of Shigella boydii 0-1392 carries the genes for aerobactin synthesis and transport. J. Bacteriol. 183, 4176–4182.CrossRefGoogle ScholarPubMed
Roth, J. R., Kofoid, E., Roth, F. P., et al. (2003). Regulating general mutation rates: examination of the hypermutable state model for Cairnsian adaptive mutation. Genetics 163, 1483–1496.Google ScholarPubMed
Salyers, A. A., Shoemaker, N. B., Stevens, A. M., and Li, L. Y. (1995). Conjugative transposons: an unusual and diverse set of integrated gene transfer elements. Microbiol. Rev. 59, 579–590.Google ScholarPubMed
Sansonetti, P. J. (1993). Molecular mechanisms of cell and tissue invasion by Shigella flexneri. Infect. Agents Dis. 2, 201–206.Google ScholarPubMed
Sansonetti, P. J., Kopecko, D. J., and Formal, S. B. (1982). Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect. Immun. 35, 852–860.Google ScholarPubMed
Sansonetti, P. J., Arondel, J., Huerre, M., Harada, A., and Matsushima, K. (1999). Interleukin-8 controls bacterial transepithelial translocation at the cost of epithelial destruction in experimental shigellosis. Infect. Immun. 67, 1471–1480.Google ScholarPubMed
Schmidt, H. and Hensel, M. (2004). Pathogenicity islands in bacterial pathogenesis. Clin. Microbiol. Rev. 17, 14–56.CrossRefGoogle ScholarPubMed
Seifert, H. S. (1996). Questions about gonococcal pilus phase- and antigenic variation. Mol. Microbiol. 21, 433–440.CrossRefGoogle ScholarPubMed
Seshadri, R., Paulsen, I. T., Eisen, J. A., et al. (2003). Complete genome sequence of the Q-fever pathogen Coxiella burnetii. Proc. Natl. Acad. Sci. U. S. A. 100, 5455–5460.CrossRefGoogle ScholarPubMed
Silva, R. M., Toledo, M. R., and Trabulsi, L. R. (1980). Biochemical and cultural characteristics of invasive Escherichia coli. J. Clin. Microbiol. 11, 441–444.Google ScholarPubMed
Smith, H. W. and Halls, S. (1967). The transmissible nature of the genetic factor in Escherichia coli that controls haemolysin production. J. Gen. Microbiol. 47, 153–161.CrossRefGoogle ScholarPubMed
Smith, H. W. and Linggood, M. A. (1971a). Observations on the pathogenic properties of the K88, Hly and Ent plasmids of Escherichia coli with particular reference to porcine diarrhoea. J. Med. Microbiol. 4, 467–485.CrossRefGoogle Scholar
Smith, H. W. and Linggood, M. A. (1971b). The transmissible nature of enterotoxin production in a human enteropathogenic strain of Escherichia coli. J. Med. Microbiol. 4, 301–305.CrossRefGoogle Scholar
So, M., Heffron, F., and McCarthy, B. J. (1979). The E. coli gene encoding heat stable toxin is a bacterial transposon flanked by inverted repeats of IS1. Nature 277, 453–456.CrossRefGoogle Scholar
Van, L. N., Engler, G., Holsters, M., et al. (1974). Large plasmid in Agrobacterium tumefaciens essential for crown gall-inducing ability. Nature 252, 169–170.Google Scholar
Venter, J. C., Remington, K., Heidelberg, J. F., et al. (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science 304, 66–74.CrossRefGoogle ScholarPubMed
Wagner, P. L. and Waldor, M. K. (2002). Bacteriophage control of bacterial virulence. Infect. Immun. 70, 3985–3993.CrossRefGoogle ScholarPubMed
Watanabe, T. (1963). Infective heredity of multiple drug resistance in bacteria. Bacteriol. Rev. 27, 87–115.Google ScholarPubMed
West, N. P., Sansonetti, P., Mounier, J., et al. (2005). Optimization of virulence functions through glucosylation of Shigella LPS. Science 307, 1313–1317.CrossRefGoogle ScholarPubMed
Wick, L. M., Qi, W., Lacher, D. W., and Whittam, T. S. (2005). Evolution of genomic content in the stepwise emergence of Escherichia coli O157:H7. J. Bacteriol. 187, 1783–1791.CrossRefGoogle ScholarPubMed
Womble, D. D. and Rownd, R. H. (1988). Genetic and physical map of plasmid NR1: comparison with other IncFII antibiotic resistance plasmids. Microbiol. Rev. 52, 433–451.Google ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org 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.

  • Evolution of bacterial pathogens
    • By Anthony T. Maurelli, Department of Microbiology and Immunology, F. Hébert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda MD 20814-4799, USA
  • Edited by Beth A. McCormick, Harvard University, Massachusetts
  • Book: Bacterial-Epithelial Cell Cross-Talk
  • Online publication: 12 August 2009
  • Chapter DOI: https://doi.org/10.1017/CBO9780511541537.002
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.

  • Evolution of bacterial pathogens
    • By Anthony T. Maurelli, Department of Microbiology and Immunology, F. Hébert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda MD 20814-4799, USA
  • Edited by Beth A. McCormick, Harvard University, Massachusetts
  • Book: Bacterial-Epithelial Cell Cross-Talk
  • Online publication: 12 August 2009
  • Chapter DOI: https://doi.org/10.1017/CBO9780511541537.002
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.

  • Evolution of bacterial pathogens
    • By Anthony T. Maurelli, Department of Microbiology and Immunology, F. Hébert School of Medicine, Uniformed Services University of the Health Sciences, Bethesda MD 20814-4799, USA
  • Edited by Beth A. McCormick, Harvard University, Massachusetts
  • Book: Bacterial-Epithelial Cell Cross-Talk
  • Online publication: 12 August 2009
  • Chapter DOI: https://doi.org/10.1017/CBO9780511541537.002
Available formats
×