Helicobacter pylori genome plasticity

Genome Dynamics

Volumn 6, Issue , 2009, Pages 75-90

  Baltrus, D A ^a   Blaser, M J ^b   Guillemin, K ^c  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF OREGON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAGA PROTEIN; CLARITHROMYCIN; FUCOSYLTRANSFERASE; METRONIDAZOLE;

ALLELE; BACTERIAL CHROMOSOME; BACTERIAL COLONIZATION; BACTERIAL GENOME; BACTERIAL PHENOMENA AND FUNCTIONS; BACTERIAL STRAIN; BACTERIUM CULTURE; BACTERIUM TRANSFORMATION; CELL DEATH; CYTOLYSIS; DNA POLYMORPHISM; DNA REPAIR; DNA REPLICATION; FRAMESHIFT MUTATION; GENE CONVERSION; GENE FUNCTION; GENE INACTIVATION; GENE MUTATION; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOME PLASTICITY; GENOME SIZE; GENOTYPE; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HOST; HUMAN; MICROBIOME; NEISSERIA GONORRHOEAE; NONHUMAN; PATHOGENESIS; PATHOGENICITY ISLAND; POINT MUTATION; POPULATION STRUCTURE; PRIORITY JOURNAL; REVIEW; SEQUENCE HOMOLOGY; STOMACH; TYPE IV SECRETION SYSTEM; ANIMAL; GASTRITIS; GENETIC VARIATION; GENETICS; GENOME; MUTATION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HELICOBACTER PYLORI; NEGIBACTERIA; PRIMATES; PROKARYOTA; SALMONELLA;

ANIMALS; GASTRITIS; GENETIC VARIATION; GENOME; GENOME, BACTERIAL; HELICOBACTER PYLORI; HUMANS; MUTATION;

EID: 77955862437     PISSN: 16609263     EISSN: None     Source Type: Book Series    
DOI: 10.1159/000235764     Document Type: Review

References (109)

1. Linz B, Balloux F, Moodley Y, Manica A, Liu H, et al: An African origin for the intimate association between humans and Helicobacter pylori. Nature 2007;445:915-918.
2. Kang J, Blaser MJ: Bacterial populations as perfect gases: genomic integrity and diversification tensions in Helicobacter pylori. Nat Rev Microbiol 2006;4: 826-836.
3. Cooke CL, Huff JL, Solnick JV: The role of genome diversity and immune evasion in persistent infection with Helicobacter pylori. FEMS Immunol Med Microbiol 2005;45:11-23.
4. Smeets LC, Kusters JG: Natural transformation in Helicobacter pylori: DNA transport in an unexpected way. Trends Microbiol 2002;10:159-162; discussion 162.
5. Suerbaum S, Achtman M: Evolution of Helicobacter pylori: the role of recombination. Trends Microbiol 1999;7:182-184.
6. Wang G, Humayun MZ, Taylor DE: Mutation as an origin of genetic variability in Helicobacter pylori. Trends Microbiol 1999;7:488-493.
7. Kraft C, Suerbaum S: Mutation and recombination in Helicobacter pylori: mechanisms and role in generating strain diversity. Int J Med Microbiol 2005; 295:299-305.
8. Suerbaum S, Josenhans C: Helicobacter pylori evolution and phenotypic diversification in a changing host. Nat Rev Microbiol 2007;5:441-452.
9. de Visser JA, Elena SF: The evolution of sex: empirical insights into the roles of epistasis and drift. Nat Rev Genet 2007;8:139-149.
10. Moxon R, Bayliss C, Hood D: Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu Rev Genet 2006;40:307-333.
11. Otto SP, Gerstein AC: Why have sex? The population genetics of sex and recombination. Biochem Soc Trans 2006;34:519-522.
12. Redfield RJ: Do bacteria have sex? Nat Rev Genet 2001;2:634-639.
13. Sniegowski PD, Gerrish PJ, Johnson T, Shaver A: The evolution of mutation rates: separating causes from consequences. Bioessays 2000;22:1057-1066.
14. Go MF: Review article: natural history and epidemiology of Helicobacter pylori infection. Aliment Pharmacol Ther 2002;16(suppl 1):3-15.
15. Brown LM: Helicobacter pylori: epidemiology and routes of transmission. Epidemiol Rev 2000;22:283-297.
16. Marshall DG, Dundon WG, Beesley SM, Smyth CJ: Helicobacter pylori - a conundrum of genetic diversity. Microbiology 1998;144:2925-2939.
17. Alm RA, Ling LS, Moir DT, King BL, Brown ED, et al: Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 1999;397:176-180.
18. Tomb JF, White O, Kerlavage AR, Clayton RA, Sutton GG, et al: The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 1997;388:539-547.
19. Gressmann H, Linz B, Ghai R, Pleissner KP, Schlapbach R, et al: Gain and loss of multiple genes during the evolution of Helicobacter pylori. PLoS Genet 2005;1:e43.
20. Salama N, Guillemin K, McDaniel TK, Sherlock G, Tompkins L, Falkow S: A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. Proc Natl Acad Sci USA 2000;97:14668-14673.
21. Kivi M, Rodin S, Kupershmidt I, Lundin A, Tindberg Y, et al: Helicobacter pylori genome variability in a framework of familial transmission. BMC Microbiol 2007;7:54.
22. Salama NR, Gonzalez-Valencia G, Deatherage B, Aviles-Jimenez F, Atherton JC, et al: Genetic analysis of Helicobacter pylori strain populations colonizing the stomach at different times postinfection. J Bacteriol 2007;189:3834-3845.
23. Kraft C, Stack A, Josenhans C, Niehus E, Dietrich G, et al: Genomic changes during chronic Helicobacter pylori infection. J Bacteriol 2006;188:249-254.
24. Baltrus DA, Amieva MR, Covacci A, Lowe TM, Merrell DS, et al: The complete genome sequence of Helicobacter pylori strain G27. J Bacteriol 2009; 191:447-448.
25. Oh JD, Kling-Bkhed H, Giannakis M, Xu J, Fulton RS, et al: The complete genome sequence of a chronic atrophic gastritis Helicobacter pylori strain: evolution during disease progression. Proc Natl Acad Sci USA 2006;103:9999-10004.
26. Giannakis M, Chen SL, Karam SM, Engstrand L, Gordon JI: Helicobacter pylori evolution during progression from chronic atrophic gastritis to gastric cancer and its impact on gastric stem cells. Proc Natl Acad Sci USA2008;105:4358-4363.
27. Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R: The microbial pan-genome. Curr Opin Genet Dev 2005;15:589-594.
28. Linz B, Schuster SC: Genomic diversity in Helicobacter and related organisms. Res Microbiol 2007;158:737-744.
29. Saunders NJ, Boonmee P, Peden JF, Jarvis SA: Interspecies horizontal transfer resulting in core-genome and niche-adaptive variation within Helicobacter pylori. BMC Genomics 2005;6:9.
30. Janssen PJ, Audit B, Ouzounis CA: Strain-specific genes of Helicobacter pylori: distribution, function and dynamics. Nucleic Acids Res 2001;29:4395-4404.
31. Sheppard SK, McCarthy ND, Falush D, Maiden MC: Convergence of Campylobacter species: implications for bacterial evolution. Science 2008;320:237-239.
32. Bik EM, Eckburg PB, Gill SR, Nelson KE, Purdom EA, et al: Molecular analysis of the bacterial microbiota in the human stomach. Proc Natl Acad Sci USA 2006;103:732-737.
33. Levine SM, Lin EA, Emara W, Kang J, DiBenedetto M, et al: Plastic cells and populations: DNA substrate characteristics in Helicobacter pylori transformation define a flexible but conservative system for genomic variation. FASEB J 2007;21:3458-3467.
34. Delport W, Cunningham M, Olivier B, Preisig O, Van Der Merwe SW: A population genetics pedigree perspective on the transmission of Helicobacter pylori. Genetics 2006;174:2107-2118.
35. Fraser C, Hanage WP, Spratt BG: Recombination and the nature of bacterial speciation. Science 2007;315:476-480.
36. Hler C, Fischer W, Hofreuter D, Haas R: Cryptic plasmids in Helicobacter pylori: putative functions in conjugative transfer and microcin production. Int J Med Microbiol 2004;294:141-148.
37. Hofreuter D, Haas R: Characterization of two cryptic Helicobacter pylori plasmids: a putative source for horizontal gene transfer and gene shuffling. J Bacteriol 2002;184:2755-2766.
38. Hosaka Y, Okamoto R, Irinoda K, Kaieda S, Koizumi W, et al: Characterization of pKU701, a 2.5-kb plasmid, in a Japanese Helicobacter pylori isolate. Plasmid 2002;47:193-200.
39. Minnis JA, Taylor TE, Knesek JE, Peterson WL, McIntire SA: Characterization of a 3.5-kbp plasmid from Helicobacter pylori. Plasmid 1995;34:22-36.
40. Heuermann D, Haas R: Genetic organization of a small cryptic plasmid of Helicobacter pylori. Gene 1995;165:17-24.
41. Kleanthous H, Clayton CL, Tabaqchali S: Characterization of a plasmid from Helicobacter pylori encoding a replication protein common to plasmids in gram-positive bacteria. Mol Microbiol 1991;5:2377-2389.
42. Kuipers EJ, Israel DA, Kusters JG, Blaser MJ: Evidence for a conjugation-like mechanism of DNA transfer in Helicobacter pylori. J Bacteriol 1998;180: 2901-2905.
43. Backert S, Kwok T, Konig W: Conjugative plasmid DNA transfer in Helicobacter pylori mediated by chromosomally encoded relaxase and TraG-like proteins. Microbiology 2005;151:3493-3503.
44. Ando T, Xu Q, Torres M, Kusugami K, Israel DA, Blaser MJ: Restriction-modification system differences in Helicobacter pylori are a barrier to interstrain plasmid transfer. Mol Microbiol 2000;37: 1052-1065.
45. Donahue JP, Israel DA, Peek RM, Blaser MJ, Miller GG: Overcoming the restriction barrier to plasmid transformation of Helicobacter pylori. Mol Microbiol 2000;37:1066-1074.
46. Heintschel von Heinegg E, Nalik HP, Schmid EN: Characterisation of a Helicobacter pylori phage (HP1). J Med Microbiol 1993;38:245-249.
47. Welch RA, Burland V, Plunkett G 3rd, Redford P, Roesch P, et al: Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci USA 2002;99: 17020-17024.
48. Bjkholm B, Sjund M, Falk PG, Berg OG, Engstrand L, Andersson DI: Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori. Proc Natl Acad Sci USA 2001, 98:14607-14612.
49. Huang S, Kang J, Blaser MJ: Antimutator role of the DNA glycosylase mutY gene in Helicobacter pylori. J Bacteriol 2006;188:6224-6234.
50. Kang J, Huang S, Blaser MJ: Structural and functional divergence of MutS2 from bacterial MutS1 and eukaryotic MSH4-MSH5 homologs. J Bacteriol 2005;187:3528-3537.
51. Kang J, Blaser MJ: Repair and antirepair DNA helicases in Helicobacter pylori. J Bacteriol 2008;190: 4218-4224.
52. O'Rourke EJ, Chevalier C, Pinto AV, Thiberge JM, Ielpi L, et al: Pathogen DNA as target for host-generated oxidative stress: role for repair of bacterial DNA damage in Helicobacter pylori colonization. Proc Natl Acad Sci USA 2003;100:2789-2794.
53. Loewe L, Textor V, Scherer S: High deleterious genomic mutation rate in stationary phase of Escherichia coli. Science 2003;302:1558-1560.
54. Hudson RE, Bergthorsson U, Ochman H: Transcription increases multiple spontaneous point mutations in Salmonella enterica. Nucleic Acids Res 2003;31:4517-4522.
55. Hudson RE, Bergthorsson U, Roth JR, Ochman H: Effect of chromosome location on bacterial mutation rates. Mol Biol Evol 2002;19:85-92.
56. Kang JM, Iovine NM, Blaser MJ: A paradigm for direct stress-induced mutation in prokaryotes. FASEB J 2006;20:2476-2485.
57. Gonzalez C, Hadany L, Ponder RG, Price M, Hastings PJ, Rosenberg SM: Mutability and importance of a hypermutable cell subpopulation that produces stress-induced mutants in Escherichia coli. PLoS Genet 2008;4:e1000208.
58. Foster PL: Stress-induced mutagenesis in bacteria. Crit Rev Biochem Mol Biol 2007;42:373-397.
59. Sundin GW, Weigand MR: The microbiology of mutability. FEMS Microbiol Lett 2007;277:11-20.
60. Amundsen SK, Fero J, Hansen LM, Cromie GA, Solnick JV, et al: Helicobacter pylori AddAB helicase- nuclease and RecA promote recombinationrelated DNA repair and survival during stomach colonization. Mol Microbiol 2008;69:994-1007.
61. SalǎL, Linz B, Suerbaum S, Saunders NJ: The diversity within an expanded and redefined repertoire of phase-variable genes in Helicobacter pylori. Microbiology 2004;150:817-830.
62. Sanabria-Valentin E, Colbert MT, Blaser MJ: Role of futC slipped strand mispairing in Helicobacter pylori Lewisy phase variation. Microbes Infect 2007;9: 1553-1560.
63. de Vries N, Duinsbergen D, Kuipers EJ, Pot RG, Wiesenekker P, et al: Transcriptional phase variation of a type III restriction-modification system in Helicobacter pylori. J Bacteriol 2002;184:6615-6623.
64. Wirth HP, Yang M, Sanabria-ValenT E, Berg DE, Dubois A, Blaser MJ: Host Lewis phenotype-dependent Helicobacter pylori Lewis antigen expression in rhesus monkeys. FASEB J 2006;20:1534-1536.
65. Tannaes T, Dekker N, Bukholm G, Bijlsma JJ, Appelmelk BJ: Phase variation in the Helicobacter pylori phospholipase A gene and its role in acid adaptation. Infect Immun 2001;69:7334-7340.
66. Kudo T, Nurgalieva ZZ, Conner ME, Crawford S, Odenbreit S, et al: Correlation between Helicobacter pylori OipA protein expression and oipA gene switch status. J Clin Microbiol 2004;42:2279-2281.
67. Aras RA, Kang J, Tschumi AI, Harasaki Y, Blaser MJ: Extensive repetitive DNA facilitates prokaryotic genome plasticity. Proc Natl Acad Sci USA 2003; 100:13579-13584.
68. Aras RA, Fischer W, Perez-Perez GI, Crosatti M, Ando T, et al: Plasticity of repetitive DNA sequences within a bacterial (Type IV) secretion system component. J Exp Med 2003;198:1349-1360.
69. Ayraud S, Janvier B, Salaun L, Fauche JL: Modification in the ppk gene of Helicobacter pylori during single and multiple experimental murine infections. Infect Immun 2003;71:1733-1739.
70. Aras RA, Lee Y, Kim SK, Israel D, Peek RM Jr, Blaser MJ: Natural variation in populations of persistently colonizing bacteria affect human host cell phenotype. J Infect Dis 2003;188:486-496.
71. Aras RA, Takata T, Ando T, Van Der Ende A, Blaser MJ: Regulation of the HpyII restriction-modification system of Helicobacter pylori by gene deletion and horizontal reconstitution. Mol Microbiol 2001; 42:369-382.
72. Bjkholm B, Lundin A, Sill A, Guillemin K, Salama N: Comparison of genetic divergence and fitness between two subclones of Helicobacter pylori. Infect Immun 2001;69:7832-7838.
73. Lorenz MG, Wackernagel W: Bacterial gene transfer by natural genetic transformation in the environment. Microbiol Rev 1994;58:563-602.
74. Johnsborg O, Eldholm V, Havarstein LS: Natural genetic transformation: prevalence, mechanisms and function. Res Microbiol 2007;158:767-778.
75. Baltrus DA, Guillemin K: Multiple phases of competence occur during the Helicobacter pylori growth cycle. FEMS Microbiol Lett 2006;255:148-155.
76. Israel DA, Lou AS, Blaser MJ: Characteristics of Helicobacter pylori natural transformation. FEMS Microbiol Lett 2000;186:275-280.
77. Hamilton HL, Dillard JP: Natural transformation of Neisseria gonorrhoeae: from DNA donation to homologous recombination. Mol Microbiol 2006; 59:376-385.
78. Suerbaum S, Smith JM, Bapumia K, Morelli G, Smith NH: Free recombination within Helicobacter pylori. Proc Natl Acad Sci USA 1998;95:12619-12624.
79. Falush D, Wirth T, Linz B, Pritchard JK, Stephens M: Traces of human migrations in Helicobacter pylori populations. Science 2003;299:1582-1585.
80. Wirth T, Wang X, Linz B, Novick RP, Lum JK, et al: Distinguishing human ethnic groups by means of sequences from Helicobacter pylori: lessons from Ladakh. Proc Natl Acad Sci USA 2004;101:4746-4751.
81. Lundin A, Bjkholm B, Kupershmidt I, Unemo M, Nilsson P, et al: Slow genetic divergence of Helicobacter pylori strains during long-term colonization. Infect Immun 2005;73:4818-4822.
82. Baltrus DA, Guillemin K, Phillips PC: Natural transformation increases the rate of adaptation in the human pathogen Helicobacter pylori. Evolution 2008;62:39-49.
83. Philpott DJ, Belaid D, Troubadour P, Thiberge JM, Tankovic J, et al: Reduced activation of inflammatory responses in host cells by mouse-adapted Helicobacter pylori isolates. Cell Microbiol 2002;4: 285-296.
84. Sozzi M, Crosatti M, Kim SK, Romero J, Blaser MJ: Heterogeneity of Helicobacter pylori cag genotypes in experimentally infected mice. FEMS Microbiol Lett 2001;203:109-114.
85. Robinson K, Loughlin MF, Potter R, Jenks PJ: Host adaptation and immune modulation are mediated by homologous recombination in Helicobacter pylori. J Infect Dis 2005;191:579-587.
86. Solnick JV, Hansen LM, Salama NR, Boonjakuakul JK, Syvanen M: Modification of Helicobacter pylori outer membrane protein expression during experimental infection of rhesus macaques. Proc Natl Acad Sci USA 2004;101:2106-2111.
87. Van Der Woude MW, Bmler AJ: Phase and antigenic variation in bacteria. Clin Microbiol Rev 2004; 17:581-611.
88. Falush D, Kraft C, Taylor NS, Correa P, Fox JG, et al: 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 2001;98:15056-15061.
89. Israel DA, Salama N, Krishna U, Rieger UM, Atherton Jr JC, et al : Helicobacter pylori genetic diversity within the gastric niche of a single human host. Proc Natl Acad Sci USA 2001;98:14625-14630.
90. Prouzet-Mauln V, Hussain MA, Lamouliatte H, Kauser F, mraud F, Ahmed N: Pathogen evolution in vivo: genome dynamics of two isolates obtained 9 years apart from a duodenal ulcer patient infected with a single Helicobacter pylori strain. J Clin Microbiol 2005;43:4237-4241.
91. Kuipers EJ, Israel DA, Kusters JG, Gerrits MM, Weel J, et al: Quasispecies development of Helicobacter pylori observed in paired isolates obtained years apart from the same host. J Infect Dis 2000;181:273-282.
92. Salaun L, Saunders NJ: Population-associated differences between the phase variable LPS biosynthetic genes of Helicobacter pylori. BMC Microbiol 2006;6:79.
93. Albert TJ, Dailidiene D, Dailide G, Norton JE, Kalia A, et al: Mutation discovery in bacterial genomes: metronidazole resistance in Helicobacter pylori. Nat Methods 2005;2:951-953.
94. Goodwin A, Kersulyte D, Sisson G, Veldhuyzen van Zanten SJ, Berg DE, Hoffman PS: Metronidazole resistance in Helicobacter pylori is due to null mutations in a gene (rdxA) that encodes an oxygeninsensitive NADPH nitroreductase. Mol Microbiol 1998;28:383-393.
95. Smeets LC, Arents NL, van Zwet AA, Vandenbroucke-Grauls CM, Verboom T, et al: Molecular patchwork: Chromosomal recombination between two Helicobacter pylori strains during natural colonization. Infect Immun 2003;71:2907-2910.
96. Kersulyte D, Chalkauskas H, Berg DE: Emergence of recombinant strains of Helicobacter pylori during human infection. Mol Microbiol 1999;31:31-43.
97. Aviles-Jimenez F, Letley DP, Gonzalez-Valencia G, Salama N, Torres J, Atherton JC: Evolution of the Helicobacter pylori vacuolating cytotoxin in a human stomach. J Bacteriol 2004;186:5182-5185.
98. Webb GF, Blaser MJ: Dynamics of bacterial phenotype selection in a colonized host. Proc Natl Acad Sci USA 2002;99:3135-3140.
99. Hartl DL, Clark AG: Principles of Population Genetics. Sunderland, Sinauer Associates, Inc., 2007.
100. Ostrowski EA, Woods RJ, Lenski RE: The genetic basis of parallel and divergent phenotypic responses in evolving populations of Escherichia coli. Proc Biol Sci 2008;275:277-284.
101. Szollosi GJ, Derenyi I, Vellai T: The maintenance of sex in bacteria is ensured by its potential to reload genes. Genetics 2006;174:2173-2180.
102. Matteo MJ, Granados G, Pez CV, Olmos M, Sanchez C, Catalano M: Helicobacter pylori cag pathogenicity island genotype diversity within the gastric niche of a single host. J Med Microbiol 2007; 56:664-669.
103. Wirth HP, Yang M, Peek RM Jr, hk-Nikanne J, Fried M, Blaser MJ: Phenotypic diversity in Lewis expression of Helicobacter pylori isolates from the same host. J Lab Clin Med 1999;133:488-500.
104. Carroll IM, Ahmed N, Beesley SM, Khan AA, Ghousunnissa S: Microevolution between paired antral and paired antrum and corpus Helicobacter pylori isolates recovered from individual patients. J Med Microbiol 2004;53:669-677.
105. Lee YC, Lee SY, Pyo JH, Kwon DH, Rhee JC, Kim JJ: Isogenic variation of Helicobacter pylori strain resulting in heteroresistant antibacterial phenotypes in a single host in vivo. Helicobacter 2005;10:240-248.
106. Akada JK, Ogura K, Dailidiene D, Dailide G, Cheverud JM, Berg DE: Helicobacter pylori tissue tropism: mouse-colonizing strains can target different gastric niches. Microbiology 2003;149:1901-1909.
107. Dubois A, Berg DE, Incecik ET, Fiala N, Heman- Ackah LM, et al: Host specificity of Helicobacter pylori strains and host responses in experimentally challenged nonhuman primates. Gastroenterology 1999;116:90-96.
108. Blaser MJ, Kirschner D: The equilibria that allow bacterial persistence in human hosts. Nature 2007;449:843-849.
109. Schwarz S, Morelli G, Kusecek B, Manica A, Balloux F, et al: Horizontal versus familial transmission of Helicobacter pylori. PLoS Pathog 2008;4:e1000180.