Phase variation: How to create and coordinate population diversity

Current Opinion in Microbiology

Volumn 14, Issue 2, 2011, Pages 205-211

  van der Woude, Marjan W ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE;

BACTERIAL GENOME; CELL GROWTH; DNA METHYLATION; DNA REPLICATION; DNA SEQUENCE; DNA STRUCTURE; GENE CONTROL; GENE SEQUENCE; MISMATCH REPAIR; NONHUMAN; OPERON; PHASE VARIATION; POPULATION GENETICS; PROMOTER REGION; REVIEW; SHORT SEQUENCE REPEAT;

ANTIGENS, BACTERIAL; BACTERIA; BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIAL TYPING TECHNIQUES; GENE EXPRESSION REGULATION, BACTERIAL; PHENOTYPE; SEROTYPING;

EID: 79954596315     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2011.01.002     Document Type: Review

References (51)

1. Bayliss C.D. Determinants of phase variation rate and the fitness implications of differing rates for bacterial pathogens and commensals. FEMS Microbiol Rev 2009, 33:504-520.
2. van der Woude M.W., Baumler A.J. Phase and antigenic variation in bacteria. Clin Microbiol Rev 2004, 17:581-611. (table of contents).
3. van der Woude M.W. Re-examining the role and random nature of phase variation. FEMS Microbiol Lett 2006, 254:190-197.
4. Telford J.L. Bacterial genome variability and its impact on vaccine design. Cell Host Microbe 2008, 3:408-416.
5. van der Woude M.W., Broadbent S.E. Phase variation. Bacterial Stress Responses 2011, 399-411. ASM Press. edn 2. G. Sotrz, R. Hengge (Eds.).
6. Tormo M.A., Ubeda C., Marti M., Maiques E., Cucarella C., Valle J., Foster T.J., Lasa I., Penades J.R. Phase-variable expression of the biofilm-associated protein (Bap) in Staphylococcus aureus. Microbiology 2007, 153:1702-1710.
7. Hoskisson P.A., Smith M.C.M. Hypervariation and phase variation in the bacteriophage 'resistome'. Curr Opin Microbiol 2007, 10:396-400.
8. Srikhanta Y.N., Fox K.L., 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.
9. Power P.M., Sweetman W.A., Gallacher N.J., Woodhall M.R., Kumar G.A., Moxon E.R., Hood D.W. Simple sequence repeats in Haemophilus influenzae. Infect Genet Evol 2009, 9:216-228.
10. Bentley S.D., Vernikos G.S., Snyder L.A., Churcher C., Arrowsmith C., Chillingworth T., Cronin A., Davis P.H., Holroyd N.E., Jagels K., et al. Meningococcal genetic variation mechanisms viewed through comparative analysis of serogroup C strain FAM18. PLoS Genet 2007, 3:e23.
11. Chen Q., Decker K.B., Boucher P.E., Hinton D., Stibitz S. Novel architectural features of Bordetella pertussis fimbrial subunit promoters and their activation by the global virulence regulator BvgA. Mol Microbiol 2010, 11:1326-1340.
12. Willems R., Paul A., van der Heide H.G., ter Avest A.R., Mooi F.R. Fimbrial phase variation in Bordetella pertussis: a novel mechanism for transcriptional regulation. EMBO J 1990, 9:2803-2809.
13. Metruccio M.M., Pigozzi E., Roncarati D., Berlanda Scorza F., Norais N., Hill S.A., Scarlato V., Delany I. A novel phase variation mechanism in the meningococcus driven by a ligand-responsive repressor and differential spacing of distal promoter elements. PLoS Pathog 2009, 5:e1000710.
14. Cerdeno-Tarraga A.M., Patrick S., Crossman L.C., Blakely G., Abratt V., Lennard N., Poxton I., Duerden B., Harris B., Quail M.A., et al. Extensive DNA inversions in the B. fragilis genome control variable gene expression. Science 2005, 307:1463-1465.
15. Emerson J.E., Reynolds E., Fagan R.P., Shaw H.A., Goulding D., Fairweather N.F. A novel genetic switch controls phase variable expression of CwpV, a Clostridium difficile cell wall protein. Mol Microbiol 2009, 74:541-556.
16. van der Woude M., Braaten B., Low D. Epigenetic phase variation of the pap operon in Escherichia coli. Trends Microbiol 1996, 4:5-9.
17. van der Woude M.W., Henderson I.R. Regulation and function of Ag43 (flu). Annu Rev Microbiol 2008, 62:153-169.
18. Wallecha A., Munster V., Correnti J., Chan T., van der Woude M.W. Dam- and OxyR-dependent phase variation of agn43: essential elements and evidence for a new role of DNA methylation. J Bacteriol 2002, 184:3338-3347.
19. Low D.A., Casadesus J. Clocks and switches: bacterial gene regulation by DNA adenine methylation. Curr Opin Microbiol 2008, 11:106-112.
20. Broadbent S.E., Davies M.R., van der Woude M.W. Phase variation controls expression of Salmonella lipopolysaccharide modification genes by a DNA methylation-dependent mechanism. Mol Microbiol 2010, 77:337-353.
21. McCusker M.P., Turner E.C., Dorman C.J. DNA sequence heterogeneity in Fim tyrosine-integrase recombinase-binding elements and functional motif asymmetries determine the directionality of the fim genetic switch in Escherichia coli K-12. Mol Microbiol 2008, 67:171-187.
22. Totsika M., Beatson S.A., Holden N., Gally D.L. Regulatory interplay between pap operons in uropathogenic Escherichia coli. Mol Microbiol 2008, 67:996-1011.
23. Peterson S.N., Reich N.O. GATC flanking sequences regulate Dam activity: evidence for how Dam specificity may influence pap expression. J Mol Biol 2006, 355:459-472.
24. Peterson S.N., Reich N.O. Competitive Lrp and Dam assembly at the pap regulatory region: implications for mechanisms of epigenetic regulation. J Mol Biol 2008, 383:92-105.
25. Lindberg S., Xia Y., Sonden B., Goransson M., Hacker J., Uhlin B.E. Regulatory interactions among adhesin gene systems of uropathogenic Escherichia coli. Infect Immun 2008, 76:771-780.
26. Lane M.C., Simms A.N., Mobley H.L. Complex interplay between type 1 fimbrial expression and flagellum-mediated motility of uropathogenic Escherichia coli. J Bacteriol 2007, 189:5523-5533.
27. Simms A.N., Mobley H.L.T. PapX, a P fimbrial operon-encoded inhibitor of motility in uropathogenic Escherichia coli. Infect Immun 2008, 76:4833-4841.
28. Sjostrom A.E., Balsalobre C., Emody L., Westerlund-Wikstrom B., Hacker J., Uhlin B.E. The SfaXII protein from newborn meningitis E. coli is involved in regulation of motility and type 1 fimbriae expression. Microb Pathog 2009, 46:243-252.
29. Simms A.N., Mobley H.L. Multiple genes repress motility in uropathogenic Escherichia coli constitutively expressing type 1 fimbriae. J Bacteriol 2008, 190:3747-3756.
30. Chatzidaki-Livanis M., Coyne M.J., Comstock L.E. A family of transcriptional antitermination factors necessary for synthesis of the capsular polysaccharides of Bacteroides fragilis. J Bacteriol 2009, 191:7288-7295.
31. Chatzidaki-Livanis M., Weinacht K.G., Comstock L.E. Trans locus inhibitors limit concomitant polysaccharide synthesis in the human gut symbiont Bacteroides fragilis. Proc Natl Acad Sci U S A 2010, 107:11976-11980.
32. Kullberg M.C. Immunology: soothing intestinal sugars. Nature 2008, 453:602-604.
33. Mazmanian S.K., Round J.L., Kasper D.L. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 2008, 453:620-625.
34. Patrick S., Blakely G.W., Houston S., Moore J., Abratt V.R., Bertalan M., Cerdeno-Tarraga A.M., Quail M.A., Corton N., Corton C., et al. Twenty-eight divergent polysaccharide loci specifying within- and amongst-strain capsule diversity in three strains of Bacteroides fragilis. Microbiology 2010, 156:3255-3269.
35. Srikhanta Y.N., Dowideit S.J., Edwards J.L., Falsetta M.L., Wu H.J., Harrison O.B., Fox K.L., Seib K.L., Maguire T.L., Wang A.H., et al. Phasevarions mediate random switching of gene expression in pathogenic Neisseria. PLoS Pathog 2009, 5:e1000400.
36. Lane M.C., Li X., Pearson M.M., Simms A.N., Mobley H.L. Oxygen-limiting conditions enrich for fimbriate cells of uropathogenic Proteus mirabilis and Escherichia coli. J Bacteriol 2009, 191:1382-1392.
37. Sohanpal B.K., Friar S., Roobol J., Plumbridge J.A., Blomfield I.C. Multiple co-regulatory elements and IHF are necessary for the control of fimB expression in response to sialic acid and N-acetylglucosamine in Escherichia coli K-12. Mol Microbiol 2007, 63:1223-1236.
38. Hernday A., Krabbe M., Braaten B., Low D. Self-perpetuating epigenetic pili switches in bacteria. Proc Natl Acad Sci U S A 2002, 29:29.
39. Murphy G.L., Connell T.D., Barritt D.S., Koomey M., Cannon J.G. Phase variation of gonococcal protein II: regulation of gene expression by slipped-strand mispairing of a repetitive DNA sequence. Cell 1989, 56:539-547.
40. Adiciptaningrum A.M., Blomfield I.C., Tans S.J. Direct observation of type 1 fimbrial switching. EMBO Rep 2009, 10:527-532.
41. Kaminska R., van der Woude M.W. Establishing and maintaining sequestration of Dam target sites for phase variation of agn43 in Escherichia coli. J Bacteriol 2010, 192:1937-1945.
42. Criss A.K., Bonney K.M., Chang R.A., Duffin P.M., Lecuyer B.E., Seifert H.S. Mismatch correction modulates mutation frequency and pilus phase and antigenic variation in Neisseria gonorrhoeae. J Bacteriol 2009, 192:316-325.
43. Bayliss C.D., Hoe J.C., Makepeace K., Martin P., Hood D.W., Moxon E.R. Neisseria meningitidis escape from the bactericidal activity of a monoclonal antibody is mediated by phase variation of lgtG and enhanced by a mutator phenotype. Infect Immun 2008, 76:5038-5048.
44. Davidson C.J., Surette M.G. Individuality in bacteria. Annu Rev Genet 2008, 42:253-268.
45. Ackermann M., Stecher B., Freed N.E., Songhet P., Hardt W.D., Doebeli M. Self-destructive cooperation mediated by phenotypic noise. Nature 2008, 454:987-990.
46. Veening J.W., Stewart E.J., Berngruber T.W., Taddei F., Kuipers O.P., Hamoen L.W. Bet-hedging and epigenetic inheritance in bacterial cell development. Proc Natl Acad Sci U S A 2008, 105:4393-4398.
47. Rando O.J., Verstrepen K.J. Timescales of genetic and epigenetic inheritance. Cell 2007, 128:655-668.
48. Gaal B., Pitchford J.W., Wood A.J. Exact results for the evolution of stochastic switching in variable asymmetric environments. Genetics 2010, 184:1113-1119.
49. Hill S.A., Davies J.K. Pilin gene variation in Neisseria gonorrhoeae: reassessing the old paradigms. FEMS Microbiol Rev 2009, 33:521-530.
50. Cahoon L.A., Seifert H.S. An alternative DNA structure is necessary for pilin antigenic variation in Neisseria gonorrhoeae. Science 2009, 325:764-767.
51. Vial L., Groleau M.-C., Lamarche M.G., Filion G., Castonguay-Vanier J., Dekimpe V., Daigle F., Charette S.J., Deziel E. Phase variation has a role in Burkholderia ambifaria niche adaptation. ISME J 2009, 4:49-60.