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Selection and evolution of virulence in bacteria: an ecumenical excursion and modest suggestion

Published online by Cambridge University Press:  06 April 2009

B.R. Levin  and
C. Svanborg Edén
B.R. Levin
Affiliation:
Department of Zoology, University of Massachusetts, Amherst 01003, USA
C. Svanborg Edén
Affiliation:
Department of Microbiology and Clinical Immunology, University of Lund, Sweden
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Summary

Why do parasites kill their hosts? During this past decade, research in three different areas; evolutionary ecology, medical microbiology, and population genetics has provided theory and data that address this and related questions of selection and the evolution and maintenance of parasite virulence. A general theory of parasite–host coevolution and the conditions for selection to favour parasite virulence has been put forth. Considerable advances have been made in elucidating the mechanisms of pathogenicity and inheritance of virulence in bacteria. The population genetic structure and the relation ship between pathogenic and non-pathogenic forms has been determined for a number of species of bacteria. We critically review these developments and their implications for questions of selection and the evolution and maintenance of virulence in bacteria. We postulate how selection may operate on specific types of bacterial virulence and present a general protocol to experimentally test hypotheses concerning selection and the evolution of virulence in bacteria.

Keywords

virulencecoevolutionvirulence determinantsbacterial pathogenicitypopulation genetics of bacteria.
Type
Research Article
Information
Parasitology , Volume 100 , Issue S1: Symposia of the British Society for Parasitology Volume 27:The evolutionary biology of parasitism , June 1990 , pp. S103 - S115
Copyright
Copyright © Cambridge University Press 1990

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References

Allison, A. C. (1964). Polymorphism and natural selection in human populations. Cold Spring Harbor Symposium on Quantitative Biology 29, 137–49.CrossRefGoogle ScholarPubMed
Allison, A. C. (1982). Co-evolution between hosts and infectious disease agents and its effects on virulence. In Population Biology of Infectious Diseases (ed. Anderson, R. M. & May, R. M.), pp. 245–267.Dahlem Konferenzen, Berlin, Heidelberg: Springer Verlag.CrossRefGoogle Scholar
Anderson, R. M. (1989). Mathematical and statistical studies of the epidemiology of HIV. AIDS 1989 3, 333–46.Google ScholarPubMed
Anderson, R. M. & May, R. M. (1982). Coevolutoin of hosts and parasites. Parasitology 85, 411–26.CrossRefGoogle ScholarPubMed
Austrian, R. & Gold, J. (1964). Pneumococcal bacteriuria with special reference to bacterial peneumococcal pneumonia. Annals of Internal Medicine 60, 757–76.CrossRefGoogle Scholar
Blyn, L. B., Braaten, B. A., White-Ziegler, C. A., Rolfson, D. H. & Low, D. A. (1989). Phase-variation of pyelonephritis-associated pili in Escherichia coli: Evidence for transcriptional regulation. EMBO Journal 8, 613–20.CrossRefGoogle ScholarPubMed
Brenner, D. J. (1987). Classification of the legionellae. Seminars in Respiratory Infections 2, 190–205.Google ScholarPubMed
Brubaker, R. R. (1985). Mechanisms of bacterial virulence. Annual Reviews of Microbiology 39, 21–50.CrossRefGoogle ScholarPubMed
Burnet, M. & White, D. O. (1972). Natural History of Infectious Disease. Cambridge: Cambridge University Press.Google Scholar
Caugant, D. A., Levin, B. R. & Selander, R. K. (1984). Distribution of multilocus genotypes of Escherichia coli within and between host families. Journal of Hygiene 92, 377–84.CrossRefGoogle ScholarPubMed
Caugant, D. A., Levin, B. R., Lidin-Janson, G., Whittam, T. S., Edén, Svanborg C. & Selander, R. K. (1983). Genetic diversity and relationships among strains of Escherichia coli in the intestine and those causing urinary tract infections. Progress in Allergy 33, 203–27.Google ScholarPubMed
Caugant, D. A., Zollinger, W. D., Mocca, L. F., Frasch, C. E., Whittam, T. S., FrØHolm, L. O., & Selander, R. K. (1987). Genetic relationships and clonal population structure of serotype 2 strains of Neisseria meningitidis.Infection and Immunity 55, 1503–12.CrossRefGoogle ScholarPubMed
Clarke, B. C. (1979). The evolution of genetic diversity. Proceedings of the Royal Society, B 205, 453–74.Google ScholarPubMed
Conway, B. & Ronald, A. (1988). An overview of some mechanisms of bacterial pathogenesis. Canadian Journal of Microbiology 34, 281–6.CrossRefGoogle ScholarPubMed
Davis, B. D., Dulbecco, R., Eisen, H. N. & Ginsberg, H. S. (1980). Microbiology, 3rd Edn.New York City: Harper and Row.Google Scholar
Davis, G. S. & Winn, W. C. Jr, (1987). Legionnaires’ disease: respiratory infections caused by Legionella bacteria. Clinics in Chest Medicine 8, 419–39.CrossRefGoogle ScholarPubMed
Deman, P., Jodal, U., Lincoln, K. & Edén, Svanborg C. (1988). Bacterial attachment and inflammation in the urinary tract. Journal of Infectious Diseases. 158, 29–35.CrossRefGoogle Scholar
Dubos, R. (1965). Man Adapting. New Haven, Connecticut: Yale University Press.Google Scholar
Ecklund, M. E. & Poysky, F. T. (1974). Interconversion of type C and D strains of Clostridium botulinum by specific bacteriophages. Applied Microbiology 27, 251–8.CrossRefGoogle Scholar
Ewald, P. W. (1983). Host–parasite relations, vectors, and the evolution of disease severity. Annual. Reviews of Ecology and Systematics 14, 465–85.CrossRefGoogle Scholar
Ewald, P. W. (1988). Cultural vectors, virulence, and the emergence of evolutionary epidemiology. In Oxford Surveys in Evolutionary Biology, vol. 5, Oxford: Oxford University Press.Google Scholar
Fenner, F. & Ratcliffe, F. N. (1965). Myxomatosis. Cambridge: Cambridge University Press.Google Scholar
Finlay, B. B. & Falkow, S. (1989). Common themes in microbial pathogenicity. Microbiology Reviews 53, 210–30.CrossRefGoogle ScholarPubMed
Fisher, R. A. (1958). The Genetical Theory of Natural Selection. New York City: Dover.Google Scholar
Freeman, V. J. (1951). Studies of bacteriophage infected Corynebacterium diptheriae. Journal of Bacteriology 61, 675.CrossRefGoogle Scholar
Gemski, P., Lazere, J. R. & Casey, T. (1980). Plasmids associated with pathogenicity and calcium dependence in Yersinia enterocolitica. Infection and Immunity 27, 682–5.CrossRefGoogle ScholarPubMed
Gillespie, J. H. (1975). Natural selection for resistance to epidemics. Ecology 56, 493–5.CrossRefGoogle Scholar
Griffith, F. (1928). Significance of Pneumococcal types. Journal of Hygiene 27, 113.CrossRefGoogle ScholarPubMed
Hacker, J., & Hughes, C. (1985). Genetics of Escherichia coli hemolysin. Current Topics in Microbiology and Immunology 118, 139–62.Google ScholarPubMed
Haldane, J. B. S. (1949). Disease and evolution. La Ricerca Science Supplement 19, 68–76.Google Scholar
Hamilton, W. D. (1982). Pathogens as a cause of genetic diversity in their host populations. In Population Biology of Infectious Diseases, (ed. Anderson, R. M. & May, R. M.) pp. 269–296. Dahlem Konferenzem, Berlin, Heidelberg: Springer Verlag.CrossRefGoogle Scholar
Hansson, S., Caugant, D., Jodal, U. & Svanborg-Edén, C. (1989). Untreated asymptomatic bacteriuria in girls: I-Stability of urinary isolates. British Medical Journal. 298, 853–5.CrossRefGoogle ScholarPubMed
Heckles, J. E. (1984). Molecular studies on the pathogenesis of gonorrhoea. Journal of Medical Microbiology 18, 293–306.CrossRefGoogle Scholar
Hull, R. A., Gill, R. E., Hsu, P., Minshaw, B. H. & Falkow, S. (1981). Construction and expression of recombinant plasmids encoding type I or D-mannose resistant pili from a urinary tract infection E. coli isolate. Infection and Immunity 33, 933–8.CrossRefGoogle ScholarPubMed
Jaenike, J. J. (1979). An hypothesis to account for the maintenance of sex within populations. Evolutionary Theory 3, 191–4.Google Scholar
Johnson, L. P. & Schlievert, P. M. (1984). Group A streptococcal phage T12 carries the structural gene for pyrogeneic endotoxin type A. Molecular and General Genetics 194, 52–6.CrossRefGoogle Scholar
Levin, B. R. (1981). Periodic selection, infectious gene exchange and the genetic structure of E. coli populations. Genetics 99, 1–23.CrossRefGoogle ScholarPubMed
Levin, B. R., Allison, A. C., Bremermann, H. J., Cavali-Sforza, L. L., Clarke, B. C., Frentzel-Beyme, R., Hamilton, W. D., Levin, S. A., May, R. M. & Thieme, H. R. (1982). Evolution of parasites and hosts. In Population Biology of Infectious Diseases (ed. Anderson, R. M. & May, R. M.) pp. 213–243. Berlin, Heidelberg: Springer Verlag.CrossRefGoogle Scholar
Levin, M. H., Weinstein, R. A., Nathan, C., Selander, R. K., Ochman, H. & Kabins, S. A. (1984). Association of infection caused by Pseudomonas aeruginosa serotype 011 with intravenous abuse of pentazocine mixed with tripelennamine. Journal of Clinical of Microbiology 20, 758–62.CrossRefGoogle Scholar
Levin, S. & Pimental, D. (1981). Selection of intermediate rates of virulence in parasite-host systems. American Naturalist 117, 308–15.CrossRefGoogle Scholar
Levins, R. (1966). The strategy of model building in population biology. American Scientist 54, 424.Google Scholar
Linder, H., Engberg, I., Mattsby-Baltzer, I., Jann, K. & Svanborg-Edén, C. (1989). Induction of inflammation by Escherichia coli on the mucosal level: requirement for adherence and endotoxin. Infection and Immunity 56, 10309–13.Google Scholar
Low, D. A., Braaten, B. A., Ling, G. V., Johnson, D. L. & Ruby, A. L. (1988). Isolation and comparison of Escherichia coli strains from canine and human patients with urinary tract infections. Infection and Immunity 56, 2601–9.CrossRefGoogle ScholarPubMed
Lubran, M. M. (1988). Bacterial toxins. Annals of Clinical Laboratory Science 18, 58–71.Google ScholarPubMed
Maruyama, T. & Kimura, M. (1980). Genetic variability and effective population size when local extinction and recolonization of subpopulations are frequent. Proceedings of the National Academy of Sciences, USA 77, 6710–14.CrossRefGoogle ScholarPubMed
Maurelli, A. T. & Sansonetti, P. J. (1988). Genetic determinants of Shigella pathogenicity. Annual Reviews of Microbiology 42, 127–50.CrossRefGoogle ScholarPubMed
May, R. M. & Anderson, H. M. (1983 a). Epidemiology and genetics in the coevolution of parasites and hosts. Proceedings of the Royal Society, B 219, 281–313.Google ScholarPubMed
May, R. M. & Anderson, R. M. (1983 b). Parasite–host coevolution. In Coevolution (ed. Futuyma, D. J. & Slatkin, M.) pp. 186–206. Sunderland: Sinauer Associates.Google ScholarPubMed
Mead-Briggs, A. R. & Vaughan, J. A. (1975). The differential transmissibility of myxoma virus strains of different virulence grade by the rabbit flea Spilopsyllus cuniculi (Dale). Journal of Hygiene 75, 237–47.CrossRefGoogle ScholarPubMed
Mekalanos, J. J. (1985). Cholera toxin: genetic analysis, regulation, and role in pathogenesis. Current Topics in Microbiology and Immunology 118, 97–118.Google ScholarPubMed
Milkman, R. (1973). Electrophoretic variation in Escherichia coli from natural sources. Science 182, 1024–6.CrossRefGoogle ScholarPubMed
Miller, V. L. & Falkow, S. (1988). Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infection and Immunity 56, 1242–8.CrossRefGoogle ScholarPubMed
Moulder, J. (1985). Comparative biology of intracellular parasitism. Microbiology Reviews 49, 298–337.CrossRefGoogle ScholarPubMed
Musser, J. M.Barenkamp, S. J., Granoff, D. M. & Selander, R. K. (1986 a). Genetic relationships of serologically nontypable and serotvpe b strains of Haemophilus influenzae. Infection and Immunity 52, 183–91.CrossRefGoogle ScholarPubMed
Musser, J. M., Bemis, D. A., Ishikawa, H. & Selander, R. K. (1987 a). Clonal diversity and host distribution in Bordetella bronchiseptica. Journal of Bacteriology 169, 2793–803.CrossRefGoogle ScholarPubMed
Musser, J. M., Granoff, D. M.Pattison, P. E. & Selander, R. K. (1985). A population genetic framework for the study of invasive diseases caused by serotype b strains of Haemophilus influenzae. Proceedings of the National Academy of Sciences, USA 82, 5078–82.CrossRefGoogle Scholar
Musser, J. M., Hewlett, E. L., Peppler, M. S. & Selander, R. K. (1986 b). Genetic diversity and relationships in populations of Bordetella spp. Journal of Bacteriology 166, 230–7.CrossRefGoogle ScholarPubMed
Musser, J. M., Rapp, V. J. & Selander, R. K. (1987 b). Clonal diversity in Haemophilus pleuropneumoniae. Infection and Immunity 55, 1207–15.CrossRefGoogle ScholarPubMed
Ochman, H., Whittam, T. S., Caugant, O. A. & Selander, R. K. (1983). Enzyme polymorphism and genetic population structure in Escherichia coli and Shigella. Journal of General Microbiology 129, 2715–26.Google Scholar
Ørskov, F. & ørskov, I. (1983). Summary of a workshop on the clone concept in epidemiology, taxonomy and evolution of Enterobacteriacae and other bacteria. Journal of Infectious Diseases 148, 346–57.CrossRefGoogle Scholar
Ørskov, F., Ørskov, I., Evans, D. J., Sack, R. B. & Wadstrom, T. (1976). Special Escherichia coli serotypes among enterotoxigenic strains from diarrhoea in adults and children. Medical Microbiology and Immunity 162, 73–83.CrossRefGoogle ScholarPubMed
Pappenheimer, A. M. (1977). Diptheria toxin. Annual Review of Biochemistry 46, 69–94.CrossRefGoogle Scholar
Piffaretti, J. C., Kressebuch, H., Aeschbacher, M., Bille, J., Bannerman, E., Musser, J. M., Selander, R. K. & Rocourt, J. (1989). Genetic characterization of clones of the bacterium Listeria monocytogenes causing epidemic disease. Proceedings of the National Academy of Sciences, USA 86, 3818–22.CrossRefGoogle ScholarPubMed
Pinero, O., Martinez, E. & Selander, R. K. (1988). Genetic diversity and relationships among isolates of Rhizobium legianinosarum biovar phaseoli. Applied Environmental Microbiology 54, 2825–32.CrossRefGoogle ScholarPubMed
Plos, K., Hull, S. & Edén, Svanborg C. (1990). Frequency and organization of pap homologous DNA in relation to clinical origin of uropathogenic Escherichia coli. Journal of Infectious Diseases (in the Press).CrossRefGoogle ScholarPubMed
Plos, K., Hull, S., Hull, H., Levin, B. R., Ørskov, R., Ørskov, F. & Svanborg-Edén, C. (1989). The distribution of the P-associated pili (Pap) region among Escherichia coli from natural sources: Evidence for horizontal gene transfer. Infection and Immunity 57,1604–11.CrossRefGoogle ScholarPubMed
Porras, O., Caugant, D. A., Gray, B., Lagerard, T., Levin, B. R. & Edén, Svanborg C. (1986). Difference in structure between type b and nontypable Haemophilus influenzae populations. Infection and Immunity 53, 79–89.CrossRefGoogle ScholarPubMed
Portony, D. A. & Martinez, R. J. (1985). Role of plasmids in the pathogenicity of Yersinia species. In Current Topics in Microbiology and Immunology 118: Genetic Approaches to Microbial Pathogenicity (ed. Gobel, W.) pp. 29–51. Berlin and Heidelberg: Springer Verlag.Google Scholar
Rastogi, N. & David, H. L.. (1988). Mechanisms of pathogenicitv in Mycobacteria. Biochimie 70, 1101–20.CrossRefGoogle ScholarPubMed
Reid, G. & Sobel, J. D. (1987). Bacterial adherence in the pathogenesis of urinary tract infection: a review. Reviews of Infectious Diseases 9, 470–87.CrossRefGoogle ScholarPubMed
Sansonetti, P. J., Kopecko, D. J. & Formal, S. B. (1981).Shigella sonnei plasmids: evidence that a large plasmid is necessary for virulence. Infection and Immunity 34, 75–83.CrossRefGoogle ScholarPubMed
Sansonetti, P. J., Kopecko, D. J. & Formal, S. B. (1982).Involvement of a plasmid in the invasive ability of Shigella flexneri. Infection and Immunity 35, 852–60.CrossRefGoogle ScholarPubMed
Schultzer, S. E., Fischetti, V. A. & Zabriskie, J. B. (1983). Toxic shock syndrome and lysogeny in Staphylococcus aurens. Science 220, 316–18.CrossRefGoogle Scholar
Selander, R. K. & Levin, B. R. (1980). Genetic diversity and structure in Escherichia coli populations. Science 210, 545–7.CrossRefGoogle ScholarPubMed
Selander, R. K., Mckinney, R. M.Whittam, T. S., Bibb, W. F., Brenner, D. J., Nolte, F. S. & Pattison, P. E.(1985). Genetic structure of populations of Legionella pneumophila. Journal of Bacteriology 163, 1021–37.CrossRefGoogle ScholarPubMed
So, M., Billyard, E., Deal, C., Getzoff, E., Hagblom, P., Meyer, T. F., Segal, E. & Tainer, J. (1985). Gonococcal pilus: genetics and structure. Current Topics in Microbiology and Immunology 118, 13–28.Google ScholarPubMed
Sodeine, O. A. & Goguen, J. D. (1988). Genetic analysis of the 95 kilobase virulence plasmid of Yersinia pestis. Infection and Immunity 56, 2743–8.CrossRefGoogle Scholar
Stocker, B. A. D. (1949). Measurement of rate of mutation of flagellar antigenic phase in Salmonella typhimurium. Journal of Hygiene 47, 398–413.Google Scholar
Edén, Svanborg C. & Deman, P. (1987). Bacterial virulence in urinary tract infection. Infection Disease Clinics of North America 1, 731–50.CrossRefGoogle Scholar
Edén, Svanborg C., Hagberg, L., Hanson, L. A., Hull, S., Hull, R., Jodal, U., Leffler, H., Lomberg, H. & Straube, E. (1983). Bacterial adherence a pathogenic mechanism in urinary tract infections caused by Escherichia coli. Progress in Allergy 33, 175–88.Google Scholar
Edén, Svanborg C., Erikson, B., Hanson, L. A., Jodal, U., Kaijer, J., Janson, G. L., Lindberg, U. & Olling, S. (1978). Adhesion to normal human uro-epithelial cells of Escherichia coli from children with various forms of urinary tract infection. Journal of Pediatrics 93, 398–403.CrossRefGoogle Scholar
Edén, Svanborg C., Hagberg, L., Hull, R., Hull, S., Magnusson, R. & Ohman, L. (1987). Bacterial virulence versus host resistance in the urinary tract of mice. Infection and Immunity 55, 1224–32.CrossRefGoogle Scholar
Edén, Svanborg C., Hanson, L. A., Jodal, U., Lindberg, u. & Akerlund, s. (1976). Variable adherence to normal urinary tract epithelial cells of Escherichia coli strains associated with various forms of urinary tract infections. Lancet II, 490–2.CrossRefGoogle Scholar
Edén, Svanborg C., Hull, S., Leffler, H., Norgren, S., Plos, K. & Wold, A. (1989) The large intestine as a reservoir for Escherichia coli causing extraintestinal infections. In The Regulatory and Protective Role of the Normal Microflora (ed. Grubb, T., Midtvedt, T. & Noren, E.) Proceedings of a Symposium at the Wenner-gren Center, Stockholm, pp. 47–58.CrossRefGoogle Scholar
Uhlin, B. E., Baga, M., Goransson, M., Lindberg, F. P., Lund, B., Norgren, M. & Normark, S. (1985). Genes determining adhesin formation in uropathogenic Escherichia coli. Current Topics in Microbiology and Immunology 118, 163–78.Google ScholarPubMed
Wallace, B. (1989). Can ‘stepping stones’ for stairways? American Naturalist 133, 578–9.CrossRefGoogle Scholar
Whittam, T. S., Ochman, H. & Selander, R. K. (1983). Geographic components of linkage disequilibrium in natural populations of Escherichia coli. Molecular Biology and Evolution 1, 67–83.Google ScholarPubMed
Wilson, D. S. (1983). The group selection controversy: history and current status. Annual Reviews of Ecology and Systematics 14, 159–187.CrossRefGoogle Scholar
Wold, A. E., Mestecky, J., Tomana, M. & Svanborg-Edén, C. (1990). Secretory IgA2 carries oligosaccharide receptors for bacterial type I fimbrial lectin. Infection and Immunity. (in the Press.)CrossRefGoogle ScholarPubMed
Wold, A. E., Thorsen, M., Hull, S. & Edén, Svanborg C. (1988). Attachment of Escherichia coli via Mannose Galα1- > 4β Gal-containing receptors to human colonic epithelial cells. Infection and Immunity 56, 2531–7.CrossRefGoogle Scholar
Wright, J. & Fathergill, L. (1933). Influenzal meningitis: the relation of age to the bactericidal power of blood against the causal organism. Journal of Immunology 24, 273–86.Google Scholar
Zink, D. J., Feeley, J. C., Wells, J. C., Vickery, J., Rood, W. D. & Donovan, C. A. (1980). Plasmid-mediated tissue invasiveness in Yersinia enterocolitica. Nature, London 238, 224–6.CrossRefGoogle Scholar