The Impact of Horizontal Genetic Exchange on Bacterial Population Structure: Insights from the Genera Neisseria and Campylobacter

Martin C. J. Maiden

doi:10.1128/9781555817114.ch3

Chapter 3 : The Impact of Horizontal Genetic Exchange on Bacterial Population Structure: Insights from the Genera Neisseria and Campylobacter

Author: Martin C. J. Maiden¹

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Department of Zoology, University of Oxford, Oxford, OX1 3PS, United Kingdom

Content Type: Monograph

Publication Year: 2011

Category: Bacterial Pathogenesis

Book DOI: 10.1128/9781555817114

Chapter DOI: 10.1128/9781555817114.ch3

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

The Impact of Horizontal Genetic Exchange on Bacterial Population Structure: Insights from the Genera Neisseria and Campylobacter, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555817114/9781555819354_Chap03-1.gif /docserver/preview/fulltext/10.1128/9781555817114/9781555819354_Chap03-2.gif

Abstract:

The concept of clone is fundamental to the study of prokaryotic evolution and is the essential starting point for any discussion on horizontal genetic exchange. Neisseria and Campylobacter share the property of being accidental pathogens—in that they cause human disease as a consequence of dysfunctional or accidental associations with humans—but the disease syndromes that they cause are very different. Neisseria and Campylobacter populations are, however, similarly structured, both exhibiting extensive evidence of frequent horizontal genetic exchange. In the case of Neisseria, the phenotype of interest is the proclivity of certain genotypes to cause invasive disease, which is apparently paradoxical in organisms that have evolved to colonize humans asymptomatically. In the case of Campylobacter, the question relates to the genetic bases of the association of particular genotypes with different animal species. This chapter talks about the impact that studies of the population biology of these genera have had on our understanding of the bacterial species concept. Horizontal genetic exchange has recently become central to discussion of bacterial species and speciation, although there remains much argument concerning the nature of bacterial species and the means whereby they arise and are maintained. In many species, including N. meningitidis and C. coli, bacterial populations show structuring, with evidence for some clonal signal notwithstanding high rates of recombination. Multilocus sequence typing (MLST) studies have substantially advanced our understanding of the population biology and evolution of many pathogenic bacteria and an increasing number of bacteria that are not pathogens of humans.

Citation: Maiden M. 2011. The Impact of Horizontal Genetic Exchange on Bacterial Population Structure: Insights from the Genera Neisseria and Campylobacter, p 15-30. In Walk S, Feng P (ed), Population Genetics of Bacteria. ASM Press, Washington, DC. doi: 10.1128/9781555817114.ch3

Key Concept Ranking

Meningococcal Conjugate Vaccine: 0.5033887
Neisseria gonorrhoeae: 0.4699593
Neisseria meningitidis: 0.4699593
Neisseria gonorrhoeae: 0.4699593
Neisseria meningitidis: 0.4699593

0.5033887

Highlighted Text: Show | Hide

Full text loading...

References

/content/book/10.1128/9781555817114.ch03

1. Achtman, M. 2008. Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens. Annu. Rev. Microbiol. 62: 53– 70.

2. Andam, C. P.,, D. Williams, and, J. P. Gogarten. 2010. Biased gene transfer mimics patterns created through shared ancestry. Proc. Natl. Acad. Sci. USA 107: 10679– 10684.

3. Baldo, L.,, J. C. Dunning Hotopp,, K. A. Jolley,, S. R. Bordenstein,, S. A. Biber,, R. R. Choudhury,, C. Hayashi,, M. C. Maiden,, H. Tettelin, and, J. H. Werren. 2006. Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl. Environ. Microbiol. 72: 7098– 7110.

4. Baumberg, S.,, J. P. W. Young,, E. M. H. Wellington, and, J. R. Saunders (ed.). 1995. Population Genetics of Bacteria. Cambridge University Press, Cambridge, United Kingdom.

5. Bennett, J. S.,, D. T. Griffiths,, N. D. McCarthy,, K. L. Sleeman,, K. A. Jolley,, D. W. Crook, and, M. C. Maiden. 2005. Genetic diversity and carriage dynamics of Neisseria lactamica in infants. Infect. Immun. 73: 2424– 2432.

6. Bennett, J. S.,, K. A. Jolley,, P. F. Sparling,, N. J. Saunders,, C. A. Hart,, I. M. Feavers, and, M. C. Maiden. 2007. Species status of Neisseria gonorrhoeae: evolutionary and epidemiological inferences from multilocus sequence typing. BMC Biol. 5: 35.

7. Bennett, J. S.,, E. A. Thompson,, P. Kriz,, K. A. Jolley, and, M. C. Maiden. 2009. A common gene pool for the Neisseria FetA antigen. Int. J. Med. Microbiol. 299: 133– 139.

8. Bentley, S. D.,, and J. Parkhill. 2004. Comparative genomic structure of prokaryotes. Annu. Rev. Genet. 38: 771– 792.

9. Bille, E.,, J. R. Zahar,, A. Perrin,, S. Morelle,, P. Kriz,, K. A. Jolley,, M. C. Maiden,, C. Dervin,, X. Nassif, and, C. R. Tinsley. 2005. A chromosomally integrated bacteriophage in invasive meningococci. J. Exp. Med. 201: 1905– 1913.

10. Bisharat, N.,, D. I. Cohen,, R. M. Harding,, D. Falush,, D. W. Crook,, T. Peto, and, M. C. Maiden. 2005. Hybrid Vibrio vulnificus. Emerg. Infect. Dis. 11: 30– 35.

11. Buckee, C. O.,, K. Jolley,, M. Recker,, B. Penman,, P. Kriz,, S. Gupta, and, M. C. Maiden. 2008. Role of selection in the emergence of lineages and the evolution of virulence in Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 105: 15082– 15087.

12. Caugant, D. A. 1998. Population genetics and molecular epidemiology of Neisseria meningitidis. APMIS 106: 505– 525.

13. Caugant, D. A.,, and M. C. Maiden. 2009. Meningococcal carriage and disease—population biology and evolution. Vaccine 27 (Suppl. 2): B64– B70.

14. Caugant, D. A.,, L. F. Mocca,, C. E. Frasch,, L. O. Frøholm,, W. D. Zollinger, and, R. K. Selander. 1987. Genetic structure of Neisseria meningitidis populations in relation to serogroup, serotype, and outer membrane protein pattern. J. Bacteriol. 169: 2781– 2792.

15. Cody, A. J.,, F. M. Colles,, S. K. Sheppard, and, M. C. J. Maiden. 2010. Where does Campylobacter come from? A molecular odyssey. Adv. Exp. Med. Biol. 659: 47– 56.

16. Cohan, F. M.,, and A. F. Koeppel. 2008. The origins of ecological diversity in prokaryotes. Curr. Biol. 18: R1024– R1034.

17. Didelot, X.,, M. Achtman,, J. Parkhill,, N. R. Thomson, and, D. Falush. 2007. A bimodal pattern of relatedness between the Salmonella Paratyphi A and Typhi genomes: convergence or divergence by homologous recombination? Genome Res. 17: 61– 68.

18. Didelot, X.,, and D. Falush. 2007. Inference of bacterial microevolution using multilocus sequence data. Genetics 175: 1251– 1266.

19. Didelot, X.,, and M. C. Maiden. 2010. Impact of recombination on bacterial evolution. Trends Microbiol. 18: 315– 322.

20. Didelot, X.,, R. Urwin,, M. C. Maiden, and, D. Falush. 2009. Genealogical typing of Neisseria meningitidis. Microbiology 155: 3176– 3186.

21. Dingle, K. E.,, F. M. Colles,, D. Falush, and, M. C. Maiden. 2005. Sequence typing and comparison of population biology of Campylobacter coli and Campylobacter jejuni. J. Clin. Microbiol. 43: 340– 347.

22. Dingle, K. E.,, F. M. Colles,, R. Ure,, J. Wagenaar,, B. Duim,, F. J. Bolton,, A. J. Fox,, D. R. A. Wareing, and, M. C. J. Maiden. 2002. Molecular characterisation of Campylobacter jejuni clones: a rational basis for epidemiological investigations. Emerg. Infect. Dis. 8: 949– 955.

23. Dingle, K. E.,, F. M. Colles,, D. R. A. Wareing,, R. Ure,, A. J. Fox,, F. J. Bolton,, H. J. Bootsma,, R. J. L. Willems,, R. Urwin, and, M. C. J. Maiden. 2001. Multilocus sequence typing system for Campylobacter jejuni. J. Clin. Microbiol. 39: 14– 23.

24. Dingle, K. E.,, and M. C. Maiden. 2005. Population genetics of Campylobacter jejuni, p. 43–58. In J. M. Ketley and, M. E. Konkel (ed.), Campylobacter Molecular and Cellular Biology. Horizon Bioscience, Wymondham, United Kingdom.

25. Doolittle, W. F. 2008. Microbial evolution: stalking the wild bacterial species. Curr. Biol. 18: R565– R567.

26. Dykhuizen, D. E.,, D. S. Polin,, J. J. Dunn,, B. Wilske,, V. Preac Mursic,, R. J. Dattwyler, and, B. J. Luft. 1993. Borrelia burgdorferi is clonal: implications for taxonomy and vaccine development. Proc. Natl. Acad. Sci. USA 90: 10163– 10167.

27. Enright, M. C.,, D. A. Robinson,, G. Randle,, E. J. Feil,, H. Grundmann, and, B. G. Spratt. 2002. The evolutionary history of methicillin-resistant Staphylococcus aureus (MRSA). Proc. Natl. Acad. Sci. USA 99: 7687– 7692.

28. Eppinger, M.,, P. L. Worsham,, M. P. Nikolich,, D. R. Riley,, Y. Sebastian,, S. Mou,, M. Achtman,, L. E. Lindler, and, J. Ravel. 2010. Genome sequence of the deep-rooted Yersinia pestis strain Angola reveals new insights into the evolution and pangenome of the plague bacterium. J. Bacteriol. 192: 1685– 1699.

29. Falush, D.,, C. Kraft,, N. S. Taylor,, P. Correa,, J. G. Fox,, M. Achtman, and, S. Suerbaum. 2001. Recombination and mutation during long-term gastric colonization by Helicobacter pylori: estimates of clock rates, recombination size, and minimal age. Proc. Natl. Acad. Sci. USA 98: 15056– 15061.

30. Feil, E.,, G. Carpenter, and, B. G. Spratt. 1995. Electrophoretic variation in adenylate kinase of Neisseria meningitidis is due to inter- and intraspecies recombination. Proc. Natl. Acad. Sci. USA 92: 10535– 10539.

31. Feil, E. J.,, E. C. Holmes,, D. E. Bessen,, M. S. Chan,, N. P. Day,, M. C. Enright,, R. Goldstein,, D. W. Hood,, A. Kalia,, C. E. Moore,, J. Zhou, and, B. G. Spratt. 2001. Recombination within natural populations of pathogenic bacteria: short-term empirical estimates and long-term phylogenetic consequences. Proc. Natl. Acad. Sci. USA 98: 182– 187.

32. Fraser, C.,, E. J. Alm,, M. F. Polz,, B. G. Spratt, and, W. P. Hanage. 2009. The bacterial species challenge: making sense of genetic and ecological diversity. Science 323: 741– 746.

33. Fraser, C.,, W. P. Hanage, and, B. G. Spratt. 2005. Neutral microepidemic evolution of bacterial pathogens. Proc. Natl. Acad. Sci. USA 102: 1968– 1973.

34. Fraser, C.,, W. P. Hanage, and, B. G. Spratt. 2007. Recombination and the nature of bacterial speciation. Science 315: 476– 480.

35. French, N.,, M. Barrigas,, P. Brown,, P. Ribiero,, N. Williams,, H. Leatherbarrow,, R. Birtles,, E. Bolton,, P. Fearnhead, and, A. Fox. 2005. Spatial epidemiology and natural population structure of Campylobacter jejuni colonizing a farmland ecosystem. Environ. Microbiol. 7: 1116– 1126.

36. Frost, L. S.,, R. Leplae,, A. O. Summers, and, A. Toussaint. 2005. Mobile genetic elements: the agents of open source evolution. Nat. Rev. Microbiol. 3: 722– 732.

37. Guibourdenche, M.,, M. Y. Popoff, and, J. Y. Riou. 1986. Deoxyribonucleic acid relatedness among Neisseria gonorrhoeae, N. meningitidis, N. lactamica, N. cinerea and “ Neisseria polysaccharea.” Ann. Inst. Pasteur Microbiol. 137B: 177– 185.

38. Gupta, S.,, M. C. J. Maiden,, I. M. Feavers,, S. Nee,, R. M. May, and, R. M. Anderson. 1996. The maintenance of strain structure in populations of recombining infectious agents. Nat. Med. 2: 437– 442.

39. Hanage, W. P.,, C. Fraser, and, B. G. Spratt. 2005. Fuzzy species among recombinogenic bacteria. BMC Biol. 3: 6.

40. Harrison, O. B.,, N. J. Evans,, J. M. Blair,, H. S. Grimes,, C. R. Tinsley,, X. Nassif,, P. Kriz,, R. Ure,, S. J. Gray,, J. P. Derrick,, M. C. Maiden, and, I. M. Feavers. 2009. Epidemiological evidence for the role of the hemoglobin receptor, HmbR, in meningococcal virulence. J. Infect. Dis. 200: 94– 98.

41. Holmes, E. C.,, R. Urwin, and, M. C. J. Maiden. 1999. The influence of recombination on the population structure and evolution of the human pathogen Neisseria meningitidis. Mol. Biol. Evol. 16: 741– 749.

42. Jolley, K. A.,, J. Kalmusova,, E. J. Feil,, S. Gupta,, M. Musilek,, P. Kriz, and, M. C. Maiden. 2000. Carried meningococci in the Czech Republic: a diverse recombining population. J. Clin. Microbiol. 38: 4492– 4498.

43. Jolley, K. A.,, D. J. Wilson,, P. Kriz,, G. McVean, and, M. C. Maiden. 2005. The influence of mutation, recombination, population history, and selection on patterns of genetic diversity in Neisseria meningitidis. Mol. Biol. Evol. 22: 562– 569.

44. Kingman, J. F. 2000. Origins of the coalescent: 1974–1982. Genetics 156: 1461– 1463.

45. Levin, B. R. 1981. Periodic selection, infectious gene exchange and the genetic structure of E. coli populations. Genetics 99: 1– 23.

46. Lorenz, M. G.,, and W. Wackernagel. 1994. Bacterial gene transfer by natural genetic transformation in the environment. Microbiol. Rev. 58: 563– 602.

47. Maiden, M. C. 2004. Dynamics of bacterial carriage and disease: lessons from the meningococcus. Adv. Exp. Med. Biol. 549: 23– 29.

48. Maiden, M. C. 2006. Multilocus sequence typing of bacteria. Annu. Rev. Microbiol. 60: 561– 588.

49. Maiden, M. C.,, A. B. Ibarz-Pavon,, R. Urwin,, S. J. Gray,, N. J. Andrews,, S. C. Clarke,, A. M. Walker,, M. R. Evans,, J. S. Kroll,, K. R. Neal,, D. A. Ala’aldeen,, D. W. Crook,, K. Cann,, S. Harrison,, R. Cunningham,, D. Baxter,, E. Kaczmarski,, J. Maclennan,, J. C. Cameron, and, J. M. Stuart. 2008. Impact of meningococcal serogroup C conjugate vaccines on carriage and herd immunity. J. Infect. Dis. 197: 737– 743.

50. Maiden, M. C. J. 1998. The impact of molecular techniques on the study of meningococcal disease, p. 265–291. In N. Woodford and, A. P. Johnson (ed.), Molecular Bacteriology: Protocols and Clinical Applications. Humana Press, Totowa, NJ.

51. Maiden, M. C. J. 1993. Population genetics of a transformable bacterium: the influence of horizontal genetical exchange on the biology of Neisseria meningitidis. FEMS Microbiol. Lett. 112: 243– 250.

52. Maiden, M. C. J.,, J. A. Bygraves,, E. Feil,, G. Morelli,, J. E. Russell,, R. Urwin,, Q. Zhang,, J. Zhou,, K. Zurth,, D. A. Caugant,, I. M. Feavers,, M. Achtman, and, B. G. Spratt. 1998. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc. Natl. Acad. Sci. USA 95: 3140– 3145.

53. Maynard Smith, J.,, C. G. Dowson, and, B. G. Spratt. 1991. Localized sex in bacteria. Nature 349: 29– 31.

54. Maynard Smith, J.,, N. H. Smith,, M. O’Rourke, and, B. G. Spratt. 1993. How clonal are bacteria? Proc. Natl. Acad. Sci. USA 90: 4384– 4388.

55. McCarthy, N. D.,, F. M. Colles,, K. E. Dingle,, M. C. Bagnall,, G. Manning,, M. C. Maiden, and, D. Falush. 2007. Host-associated genetic import in Campylobacter jejuni. Emerg. Infect. Dis. 13: 267– 272.

56. Medini, D.,, D. Serruto,, J. Parkhill,, D. A. Relman,, C. Donati,, R. Moxon,, S. Falkow, and, R. Rappuoli. 2008. Microbiology in the post-genomic era. Nat. Rev. Microbiol. 6: 419– 430.

57. Morse, S. A.,, and J. S. Knapp. 1992. The genus Neisseria, p. 2495–2559. In A. Balows,, H. G. Trüper,, M. Dworkin,, W. Harder, and, K.-H. Schleifer (ed.), The Prokaryotes, 2nd ed. Springer-Verlag, New York, NY.

58. Mullner, P.,, S. E. Spencer,, D. J. Wilson,, G. Jones,, A. D. Noble,, A. C. Midwinter,, J. M. Collins-Emerson,, P. Carter,, S. Hathaway, and, N. P. French. 2009. Assigning the source of human campylobacteriosis in New Zealand: a comparative genetic and epidemiological approach. Infect. Genet. Evol. 9: 1311– 1319.

59. Parker, C. T.,, W. G. Miller,, S. T. Horn, and, A. J. Lastovica. 2007. Common genomic features of Campylobacter jejuni subsp. doylei strains distinguish them from C. jejuni subsp. jejuni. BMC Microbiol. 7: 50.

60. Priest, F. G.,, M. Barker,, L. W. Baillie,, E. C. Holmes, and, M. C. Maiden. 2004. Population structure and evolution of the Bacillus cereus group. J. Bacteriol. 186: 7959– 7970.

61. Selander, R. K.,, D. A. Caugant,, H. Ochman,, J. M. Musser,, M. N. Gilmour, and, T. S. Whittam. 1986. Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl. Environ. Microbiol. 51: 837– 884.

62. Sheppard, S. K.,, J. F. Dallas,, N. J. Strachan,, M. MacRae,, N. D. McCarthy,, D. J. Wilson,, F. J. Gormley,, D. Falush,, I. D. Ogden,, M. C. Maiden, and, K. J. Forbes. 2009. Campylobacter genotyping to determine the source of human infection. Clin. Infect. Dis. 48: 1072– 1078.

63. Sheppard, S. K.,, N. D. McCarthy,, D. Falush, and, M. C. Maiden. 2008. Convergence of Campylobacter species: implications for bacterial evolution. Science 320: 237– 239.

64. Snape, M. D.,, D. F. Kelly,, B. Green,, E. R. Moxon,, R. Borrow, and, A. J. Pollard. 2005. Lack of serum bactericidal activity in preschool children two years after a single dose of serogroup C meningococcal polysaccharide-protein conjugate vaccine. Pediatr. Infect. Dis. J. 24: 128– 131.

65. Spratt, B. G. 1988. Hybrid penicillin-binding proteins in penicillin-resistant strains of Neisseria gonorrhoeae. Nature 332: 173– 176.

66. Spratt, B. G.,, and M. C. J. Maiden. 1999. Bacterial population genetics, evolution and epidemiology. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354: 701– 710.

67. Stackebrandt, E.,, W. Frederiksen,, G. M. Garrity,, P. A. Grimont,, P. Kämpfer,, M. C. Maiden,, X. Nesme,, R. Rossello-Mora,, J. Swings,, H. G. Truper,, L. Vauterin,, A. C. Ward, and, W. B. Whitman. 2002. Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int. J. Syst. Evol. Bacteriol. 52: 1043– 1047.

68. Urwin, R.,, J. E. Russell,, E. A. Thompson,, E. C. Holmes,, I. M. Feavers, and, M. C. Maiden. 2004. Distribution of surface protein variants among hyperinvasive meningococci: implications for vaccine design. Infect. Immun. 72: 5955– 5962.

69. Vázquez, J. A.,, L. de la Fuente,, S. Berron,, M. O’Rourke,, N. H. Smith,, J. Zhou, and, B. G. Spratt. 1993. Ecological separation and genetic isolation of Neisseria gonorrheae and Neisseria meningitidis. Curr. Biol. 3: 567– 572.

70. Wassenaar, T. M.,, and D. G. Newell. 2000. Genotyping of Campylobacter species. Appl. Environ. Microbiol. 66: 1– 9.

71. Wilson, D. J.,, E. Gabriel,, A. J. Leatherbarrow,, J. Cheesbrough,, S. Gee,, E. Bolton,, A. Fox,, C. A. Hart,, P. J. Diggle, and, P. Fearnhead. 2009. Rapid evolution and the importance of recombination to the gastroenteric pathogen Campylobacter jejuni. Mol. Biol. Evol. 26: 385– 397.

72. Wilson, D. J.,, E. Gabriel,, A. J. H. Leatherbarrow,, J. Cheesbrough,, S. Gee,, E. Bolton,, A. Fox,, P. Fearnhead,, A. Hart, and, P. J. Diggle. 2008. Tracing the source of campylobacteriosis. PLoS Genet. 26: e1000203.

73. Wirth, T.,, D. Falush,, R. Lan,, F. Colles,, P. Mensa,, L. H. Wieler,, H. Karch,, P. R. Reeves,, M. C. Maiden,, H. Ochman, and, M. Achtman. 2006. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol. Microbiol. 60: 1136– 1151.

74. Wright, S. 1932. The roles of mutation, inbreeding, crossbreeding and selection in evolution, p. 356–366. In D. F. Jones (ed.), Proceedings of the Sixth International Congress on Genetics, vol. 1. Brooklyn Botanic Garden, Brooklyn, NY.

75. Yazdankhah, S. P.,, P. Kriz,, G. Tzanakaki,, J. Kremastinou,, J. Kalmusova,, M. Musilek,, T. Alvestad,, K. A. Jolley,, D. J. Wilson,, N. D. McCarthy,, D. A. Caugant, and, M. C. Maiden. 2004. Distribution of serogroups and genotypes among disease-associated and carried isolates of Neisseria meningitidis from the Czech Republic, Greece, and Norway. J. Clin. Microbiol. 42: 5146– 5153.

76. Young, K. T.,, L. M. Davis, and, V. J. Dirita. 2007. Campylobacter jejuni: molecular biology and pathogenesis. Nat. Rev. Microbiol. 5: 665– 679.

77. Zhou, J.,, and B. G. Spratt. 1992. Sequence diversity within the argF, fbp and recA genes of natural isolates of Neisseria meningitidis: interspecies recombination within the argF gene. Mol. Microbiol. 6: 2135– 2146.

78. Zhu, P.,, A. van der Ende,, D. Falush,, N. Brieske,, G. Morelli,, B. Linz,, T. Popovic,, I. G. Schuurman,, R. A. Adegbola,, K. Zurth,, S. Gagneux,, A. E. Platonov,, J. Y. Riou,, D. A. Caugant,, P. Nicolas, and, M. Achtman. 2001. Fit genotypes and escape variants of subgroup III Neisseria meningitidis during three pandemics of epidemic meningitis. Proc. Natl. Acad. Sci. USA 98: 5234– 5239.