Phase variation and adaptation in bacteria: A 'Red Queen's Race'

Current Science

Volumn 100, Issue 8, 2011, Pages 1163-1171

  Jayaraman, R ^a  

^a NONE   (India)

Author keywords

Adaptation; Contingency genes; Phase variation; Phasevarions; Red Queen's Race

Indexed keywords

BACTERIA (MICROORGANISMS);

EID: 79955458970     PISSN: 00113891     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (68)

1. Hengge-Aronis, R., The general stress response in Escherichia coli. In Bacterial Stress Response (eds Storz, G. and Hengge-Aronis, R.), ASM Press, Washington DC, USA, 2000, pp. 161-178.
2. Hengge-Aronis, R., Signal transductions and regulatory mechanisms involved in the control of sigma(S) (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev., 2002, 66, 373-395.
3. Weber, H., Polen, T., Hueveling, J., Wendisch, V. F. and Hengge, R., Genome-wide analysis of the general stress-response network in Escherichia coli: σ S-dependent genes, promoters, and sigma factor selectivity. J. Bacteriol., 2005, 187, 1591-1603.
4. Hengge, R., The two-component network and the general stress sigma factor RpoS in Escherichia coli. Adv. Exp. Biol. Med., 2008, 631, 41-63.
5. Hengge, R., Proteolysis of RpoS and the general stress response in Escherichia coli. Res. Microbiol., 2009, 160, 667-676.
6. Ron, E. Z., Editorial: An update on bacterial stress response. Res. Microbiol., 2009, 160, 243-244.
7. Galhardo, R. S., Hastings, P. J. and Rosenberg, S. M., Mutation as a stress response and regulation of evolvability. Crit. Rev. Biochem. Mol. Biol., 2007, 42, 399-435.
8. Foster, P. L., Stress induced mutagenesis in bacteria. Crit. Rev. Biochem. Mol. Biol., 2007, 42, 373-397.
9. de Visser, J. A. G. M., The fate of microbial mutators. Microbiology, 2002, 148, 1247-1252.
10. Oliver, A., Hypermutation in natural bacterial populations: consequences for medical microbiology. Rev. Med. Microbiol., 2005, 16, 1-25.
11. Labat, F., Pradillon, O., Gary, L., Peuchmaur, M., Fantin, B. and Denamur, E., Mutator phenotype confers advantage in Escherichia coli chronic urinary tract infection. FEMS Immunol. Med. Microbiol., 2005, 44, 317.
12. Denamur, E. and Matic, I., Evolution of mutation rates in bacteria. Mol. Microbiol., 2006, 60, 820-827.
13. Jayaraman, R., Mutators and hypermutability in bacteria: the Escherichia coli paradigm. J. Genet., 2009, 88, 379-391.
14. Kibota, T. T. and Lynch, M., Estimate of the genomic mutation rate deleterious to overall fitness in E. coli. Nature, 1996, 331, 694-696.
15. Boe, L., Danielsen, M., Knudsen, S., Petersen, J. B., Maymann, J. B. and Jensen, P. R., The frequency of mutations in populations of Escherichia coli. Mutat. Res., 2000, 448, 47-55.
16. Imhoff, M. and Schlotterer, C., Fitness effects of advantageous mutations in evolving Escherichia coli populations. Nature, 2001, 381, 694-696.
17. Wright, B. E., Stress directed mutations and evolution. Mol. Microbiol., 2004, 52, 643-650.
18. Roth, J. R., Kugelberg, E., Reams, A. B., Kofoid, E. and Andersson, D. I., Origin of mutations under selection: the adaptive mutation controversy. Annu. Rev. Microbiol., 2006, 60, 477-501.
19. Galhardo, R. S., Do, R., Yamada, M., Friedberg, E. C., Hastings, P. J., Nohmi, T. and Rosenberg, S. M., DinB up regulation is the sole role of the SOS response in stress-induced mutagenesis in Escherichia coli. Genetics, 2009, 182, 55-68.
20. Hastings, P. J., Adaptive amplification. Crit. Rev. Biochem. Mol. Biol., 2007, 42, 271-283.
21. Gonzalez, C., Hadany, L., Ponder, R. C., Price, M., Hastings, P. J. and Rosenberg, S. M., Mutabilty and importance of a hypermutable cell subpopulation that produces stress induced mutations in Escherichia coli. PLoS Genet., 2007, 4, e1000208.
22. Andersson, D., Hughes, D. and Roth, J., The origin of mutants under selection: interaction of mutation, growth and selection. In Eco Sal: Escherichia coli and Salmonella, Cellular and Molecular Biology (eds Bock, A. et al.), ASM Press, Washington DC, USA, 2009.
23. Roth, J., Genetic adaptation: a new piece for a very old puzzle. Curr. Biol., 2010, 20, R15-R17.
24. Moxon, R. E., Rainey, P. B., Nowak, M. A. and Lenski, R. E., Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr. Biol., 1994, 4, 24-33.
25. Moxon, R., Bayliss, C. and Hood, D., Bacterial contingency loci: the role of simple sequence repeats in bacterial adaptation. Annu. Rev. Genet., 2006, 40, 307-333.
26. van Belkum, A., Scherer, S., van Alphen, L. and Verbrugh, H., Variable number of tandem repeats in clinical strains of Haemophilus influenzae. Infect. Immunol., 1998, 65, 5017-5027.
27. Moxon, R. E. and Wills, C., DNA microsatellites: agents of evolution? Sci. Am., 1999, 280, 94-99.
28. Metzgar, D. and Willis, C., Evidence for the adaptive evolution of mutation rates. Cell, 2000, 101, 581-584.
29. Bayliss, C. D., Field, D. and Moxon, R. E., The simple sequence contingency loci of Haemophilus influenzae and Neisseria meningiditis. J. Clin. Invest., 2001, 107, 657-662.
30. Salaun, L., Snyder, L. A. and Saunders, N. J., Adaptation by phase variation in pathogenic bacteria. Adv. Appl. Microbiol., 2003, 52, 263-301.
31. Hallet, B., Playing Dr Jekyll and Mr Hyde: combined mechanisms of phase variation in bacteria. Curr. Opin. Microbiol., 2001, 4, 570-581.
32. van der Woude, M. V. and Baumler, A. J., Phase and antigenic variation in bacteria. Clin. Microbiol. Rev., 2004, 17, 581-611.
33. Kline, K., Hechman, E. V., Scaar, E. P. and Seifert, H. S., Recombination, repair and replication in the pathogenic Neisseriae: the 3Rs of molecular genetics of two human-specific bacterial pathogens. Mol. Microbiol., 2003, 50, 3-13.
34. Hernday, A., Krabbe, M., Braatten, B. and Low, D., Selfperpetuating epigenetic pili switches in bacteria. Proc. Natl. Acad. Sci. USA, 2002, 99, 1640-1647.
35. Bayliss, C. D., Determinants of phase variation rates and fitness implications of differing rates for pathogens and commensals. FEMS Microbiol. Rev., 2009, 33, 504-520.
36. van der Woude, M. V., Some types of bacterial phase variations are epigenetic. Microbe, 2008, 3, 21-26.
37. Martin, P. et al., Experimentally revised reportoire of putative contingency loci in Neisseria meningitidis strain MC58: evidence for a novel mechanism of phase variation. Mol. Microbiol., 2003, 50, 245-257.
38. Metruccio, M. M. E. et al., A novel phase variation mechanism in the meningococcus driven by a ligand-responsive repressor and differential spacing of distal promoter elements. PLoS Patho., 2009, 5(12), e1000710.
39. Bayliss, C. D., Callaghan, M. J. and Moxon, R. E., High allelic diversity in methyltransferase gene of a phase variable type III restriction modification system has implications for the fitness of Haemophilus influenzae. Nucleic Acids Res., 2006, 34, 4046-4059.
40. Fox, K. L., Dowideit, S. J., Erwin, A. L., Srikhanta, Y. N., Smith, A. L. and Jennings, M. P., Haemophilus influenzae phasevarions have evolved from type III DNA restriction systems into epigenetic regulators of gene expression. Nucleic Acids Res., 2007, 35, 5242-5252.
41. De Bolle, X. et al., The length of a tetranucleotide repeat tract in Haemophilus influenzae determines the phase variation rate of a gene with homology type III DNA methyltransferases. Mol. Microbiol., 2000, 35, 211-222; Erratum. Mol. Microbiol., 2002, 46, 293.
42. Srikhanta, Y. N., Maquire, T. L., Stacey, K. J., Grimmond, S. M., and Jennings, M. P., The phasevarion: a genetic system controlling coordinated, random switching of expression of multiple genes. Proc. Natl. Acad. Sci. USA, 2005, 102, 5547-5551.
43. Srikhanta, Y. N. et al., Phasevarions mediate random switching of gene expression in pathogenic Neisseriae. PLoS Path.., 2009, 5(5), e1000400.
44. Srikhanta, Y. N., Fox, K. L. and Jennings, M. P., The phasevarion: phase variation of type III DNA methyltransferases controls coordinated switching in multiple genes. Nat. Rev. Microbiol., 2010, 8, 196-206.
45. Glover, S. W. and Piekarowicz, A., Host specificity of DNA in Haemophilus influenzae; restriction and modificatioin in strain Rd. Biochem. Biophys. Res. Commun., 1972, 46, 1610-1617.
46. Zaleski, P., Wojciechow, M. and Piekarowicz, A., The role of Dam methylation in phase variation of Haemophilus influenzae genes involved in defence against phage infection. Microbiology, 2005, 151, 3361-3369.
47. Jayaraman, R., Bacterial persistence: some new insights into an old phenomenon. J. Biosci., 2008, 33, 795-805.
48. van der Woude, M. V., Re-examining the role and random nature of phase variation. FEMS Microbiol. Lett., 2006, 254, 190-197.
49. Bayliss, C. D., Hoe, J. C., Makepeace, K., Martin, P., Hood, D. W. and Moxon, R. E., Neisseria meningiditis escape from the bactericidal activity of a monoclonal antibody is mediated by phase variation of lgtG and enhanced by a mutator phenotype. Infect. Immunol., 2008, 76, 5038-5048.
50. Martin, P., Sun, L., Hood, D. W. and Moxon, R. E., Involvement of genes of genome maintenance in the regulation of phase variation frequencies in Neisseria meningitidis. Microbiology, 2004, 150, 3001-3012.
51. Citti, C., Nouvel, L. and Baronowski, E., Phage and antigenic variation in mycoplasma. Future Microbiol., 2010, 5, 1073-1085.
52. Gogol, E. B., Cummings, C. A., Burns, R. C. and Relman, D. A., Phase variation and microevolution at homopolymeric tracts in Bordetella pertussis. BMC Genomics, 2007, 8, 122.
53. Salaun, L., Linz, B., Suerbaum, S. and Saunders, N. J., The diversity within an expanded and redefined repertoire of phase variable genes in Helicobacter pylori. Microbiology, 2004, 150, 817-830.
54. Salaun, L., Ayraud, S. and Saunders, N. J., Phase variation mediated niche adaptation during prolonged experimental murine infection with Helicobacter pylori. Microbiology, 2005, 161, 917-923.
55. Snyder, A. J. et al., Transcriptome of uropathogenic Escherichia coli during urinary tract infection. Infect. Immun., 2004, 72, 6373-6381.
56. Snyder, J. A., Lloyd, A. L., Lockatell, C. V., Johnson, D. E. and Mobley, H. L. T., Role of phase variation of type 1 fimbriae in a uropathogenic Escherichia coli cystitis isolate during urinary tract infection. Infect. Immun., 2006, 74, 1387-1393.
57. Rosen, D. A., Pinker, J. S., Jones, J. M., Walker, J. N., Cleg, S., and Hultgren, S. J., Utilization of an intracellular bacterial community pathway in Klebsiella pneumoniae urinary tract infection and the effects of fimK on type I pilus expression. Infect. Immun., 2008, 76, 3337-3345.
58. Capeechi, B. et al., Neisseria meningitidis NadA is a new invasion which promotes bacterial adhesion and penetration into human epithelial cells. Mol. Microbiol., 2005, 55, 687-698.
59. Dehio, C., Grey-Owen, S. D. and Meyer, T. F., The role of Neisseria Opa proteins in interaction with host cells. Trends Microbiol., 1998, 6, 489-495.
60. Hauck, C. R. and Meyer, T. F., Smal talk: Opa proteins as mediators of Neisseria -host cell communication. Curr. Opin. Microbiol., 2003, 6, 43-49.
61. Marri, P. R. et al., Genome sequencing reveals widespread virulence gene exchange among human Neisseria species. PLoS ONE, 2010, 5, e11835.
62. Schoen, C. et al., Whole-genome comparison of disease and carriage strains provides insights into virulence evolution in Neisseria meningitidis. Proc. Natl. Acad. Sci. USA, 2008, 105, 3475-3478.
63. Hill, D. J., Griffiths, N. J., Borodina, E. and Virji, M., Cellular and molecular biology of Neisseria meningitidis colonization and invasive disease. Clin. Sci., 2010, 118, 547-564.
64. Fox, K. L., Srikhanta, Y. N. and Jennings, M. P., Phase variable type III restriction-modification systems of host-adapted bacterial pathogens. Mol. Microbiol., 2007, 65, 1375-1379.
65. Bille, E. et al., A chromosomally integrated bacteriophage in invasive meningococci. J. Exp. Med., 2005, 201, 1905-1913.
66. Moxon, R. E. and Jansen, V. A., Phage variation: understanding the behaviour of an accidental pathogen. Trends Microbiol., 2005, 13, 563-565.
67. Dryden, D. T., Murray, N. E. and Rao, D. N., Nucleoside triphosphate-dependent restriction enzymes. Nucleic Acids Res., 2001, 29, 3728-3741.
68. Van Valen, A new evolutionary law. Evol. Theory., 1973, 1, 1-30.