Evolutionary dynamics of insertion sequences in Helicobacter pylori

Journal of Bacteriology

Volumn 186, Issue 22, 2004, Pages 7508-7520

  Kalia, Awdhesh ^a   Mukhopadhyay, Asish K ^a,d   Dailide, Giedrius ^a   Ito, Yoshiyki ^a,b   Azuma, Takeshi ^b   Wong, Benjamin C Y ^c   Berg, Douglas E ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF FUKUI   (Japan)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

^d NATIONAL INSTITUTE OF CHOLERA AND ENTERIC DISEASES   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; PROTEIN ORFA; PROTEIN ORFB; TRANSPOSASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; CODON; EVOLUTION; GENE INSERTION SEQUENCE; GENE SEQUENCE; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; HELICOBACTER PYLORI; HOMOLOGOUS RECOMBINATION; HOMOPLASY; HUMAN; MICROBIAL GENETICS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; PRIORITY JOURNAL; PROKARYOTE; PROTEIN INTERACTION; SALMONELLA; SCREENING; SEQUENCE ANALYSIS;

DNA TRANSPOSABLE ELEMENTS; EUROPE; EVOLUTION, MOLECULAR; FAR EAST; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; IMMUNOBLOTTING; INDIA; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PHYLOGENY; POLYMERASE CHAIN REACTION; RECOMBINATION, GENETIC; SELECTION (GENETICS); SEQUENCE ANALYSIS, DNA; VARIATION (GENETICS);

BACTERIA (MICROORGANISMS); HELICOBACTER; HELICOBACTER PYLORI; INSERTION SEQUENCES; NEGIBACTERIA; PROKARYOTA; SALMONELLA; TRANSPOSONS; UNIDENTIFIED INSERTION SEQUENCE;

EID: 7744220354     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.22.7508-7520.2004     Document Type: Article

References (68)

1. Achtman, M., T. Azuma, D. E. Berg, Y. Ito, G. Morelli, Z. J. Pan, S. Suerbaum, S. A. Thompson, A. van der Ende, and L. J. van Doorn. 1999. Recombination and clonal groupings within Helicobacter pylori from different geographical regions. Mol. Microbiol. 32:459-470.
2. Bandelt, H. J., and A. W. Dress. 1992. Split decomposition: a new and useful approach to phylogenetic analysis of distance data. Mol. Phylogenet. Evol. 1:242-252.
3. Berg, D. E., and M. M. Howe. 1989. Mobile DNA. ASM Press, Washington, D.C.
4. Bergelson, J., M. Kreitman, E. A. Stahl, and D. Tian. 2001. Evolutionary dynamics of plant R-genes. Science 292:2281-2285.
5. Bisercic, M., and H. Ochman. 1993. The ancestry of insertion sequences common to Escherichia coli and Salmonella typhimurium. J. Bacteriol. 175:7863-7868.
6. Blaser, M. J., and D. E. Berg. 2001. Helicobacter pylori genetic diversity and risk of human disease. J. Clin. Investig. 107:767-773.
7. Burcb, C. L., and L. Chao. 1999. Evolution by small steps and rugged landscapes in the RNA virus phi6. Genetics 151:921-927.
8. Cavalli-Sfroza, L. L., and W. F. Bodmer. 1999. The genetics of human populations. Dover Publications Inc., New York, N.Y.
9. Censini, S., C. Lange, Z. Xiang, J. E. Crabtree, P. Ghiara, M. Borodovsky, R. Rappuoli, and A. Covacci. 1996. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors. Proc. Natl. Acad. Sci. USA 93:14648-14653.
10. Chandler, M., and J. Mahillon. 2002. Insertion sequences revisited, p. 305-367. In N. C. Craig, R. Craigie, M. Gellert, and A. M. Lambowitz (ed.), Mobile DNA II. ASM Press, Washington, D.C.
11. Chao, L., C. Vargas, B. B. Spear, and E. C. Cox. 1983. Transposable elements as mutator genes in evolution. Nature 303:633-635.
12. Cherry, J. L. 2004. Selection, subdivision, and extinction and recolonization. Genetics 166:1105-1114.
13. Cohan, F. M. 2002. Sexual isolation and speciation in bacteria. Genetica 116:359-370.
14. Cover, T. L., D. E. Berg, M. J. Blaser, and H. L. T. Mobely. 2001. Helicobacter pylori pathogenesis, p. 509-558. In E. A. Groisman (ed.), Principles of bacterial pathogenesis. Academic Press, New York, N.Y.
15. Craig, N. C., R. Craigie, M. Gellert, and A. M. Lambowitz (ed.). 2002. Mobile DNA II. ASM Press, Washington, D.C.
16. Curcio, M. J., and K. M. Derbyshire. 2003. The outs and ins of transposition: from mu to kangaroo. Nat. Rev. Mol. Cell Biol. 4:865-877.
17. Derbyshire, K. M., and N. D. Grindley. 1996. cis preference of the IS903 transposase is mediated by a combination of transposase instability and inefficient translation. Mol. Microbiol. 21:1261-1272.
18. Doak, T. G., D. J. Witherspoon, C. L. Jahn, and G. Herrick. 2003. Selection on the genes of Euplotes crassus Tec1 and Tec2 transposons: evolutionary appearance of a programmed frameshift in a Tec2 gene encoding a tyrosine family site-specific recombinase. Eukaryot. Cell 2:95-102.
19. Doolittle, W. F., and C. Sapienza. 1980. Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601-603.
20. Dubois, A., D. E. Berg, E. T. Incecik, N. Fiala, L. M. Heman-Ackah, J. Del Valle, M. Yang, H. P. Wirth, G. I. Perez-Perez, and M. J. Blaser. 1999. Host specificity of Helicobacter pylori strains and host responses in experimentally challenged nonhuman primates. Gastroenterology 116:90-96.
21. Falush, D., C. Kraft, N. S. Taylor, P. Correa, J. G. Fox, M. Achtman, and S. Suerbaum. 2002. 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.
22. Falush, D., T. Wirth, B. Linz, J. K. Pritchard, M. Stephens, M. Kidd, M. J. Blaser, D. Y. Graham, S. Vacher, G. I. Perez-Perez, Y. Yamaoka, F. Megraud, K. Otto, U. Reichard, E. Katzowitsch, X. Wang, M. Achtman, and S. Suerbaum. 2003. Traces of human migrations in Helicobacter pylori populations. Science 299:1582-1585.
23. Ghose, C., G. I. Perez-Perez, M. G. Dominguez-Bello, D. T. Pride, C. M. Bravi, and M. J. Blaser. 2002. East Asian genotypes of Helicobacter pylori strains in Amerindians provide evidence for its ancient human carriage. Proc. Natl. Acad. Sci. USA 99:15107-15111.
24. Guedon, G., F. Bourgoin, M. Pebay, Y. Roussel, C. Colmin, J. M. Simonet, and B. Decaris. 1995. Characterization and distribution of two insertion sequences, IS1191 and iso-IS981, in Streptococcus thermophilus: does intergeneric transfer of insertion sequences occur in lactic acid bacteria cocultures? Mol. Microbiol. 16:69-78.
25. Hartl, D. L., D. E. Dykhuizen, R, D. Miller, L. Green, and J. de Framond. 1983. Transposable element IS50 improves growth rate of E. coli cells without transposition. Cell 35:503-510.
26. Hartl, D. L., and S, A. Sawyer. 1988. Why do unrelated insertion sequences occur together in the genome of Eschenchia coli. Genetics 118:537-541.
27. Hartl, D. L., and A. G. Clark. 1997. Principles of population genetics. Sinauer Associates Inc., Sunderland, Mass.
28. Hey, J. 1991. The structure of genealogies and the distribution of fixed differences between DNA sequence samples from natural populations. Genetics 128:831-840.
29. Hook-Nikanne, J., D. E. Berg, R. M. Peek, Jr., D. Kersulyte, M. K. Tummuru, and M. J. Blaser. 1998. DNA sequence conservation and diversity in transposable element IS605 of Helicobacter pylori. Helicobacter 3:79-85.
30. Hudson, R. R., D. D. Boos, and N. L. Kaplan. 1992. A statistical test for detecting geographic subdivision. Mol. Biol. Evol. 9:138-151.
31. Hudson, R. R. 2000. A new statistic for detecting genetic differentiation. Genetics 155:2011-2014.
32. Huelsenbeck, J. P., and B. Rannala. 1997. Phylogenetic methods come of age: testing hypotheses in an evolutionary context. Science 276:227-232.
33. Huson, D. H. 1998. SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 14:68-73.
34. Kersulyte, D., N. S. Akopyants, S. W. Clifton, B. A. Roe, and D. E. Berg. 1998. Novel sequence organization and insertion specificity of IS605 and IS606: chimaeric transposable elements of Helicobacter pylori. Gene 223:175-186.
35. Kersulyte, D., A. K. Mukhopadhyay, M. Shirai, T. Nakazawa, and D. E. Berg. 2000. Functional organization and insertion specificity of IS607, a chimeric element of Helicobacter pylori. J. Bacteriol. 182:5300-5308.
36. Kersulyte, D., A. K. Mukhopadhyay, B. Velapatino, W. Su, Z. Pan, C. Garcia, V. Hernandez, Y. Valdez, R. S. Mistry, R. H. Gilman, Y. Yuan, H. Gao, T. Alarcon, M. Lopez-Brea, G. Balakrish Nair, A. Chowdhury, S. Datta, M. Shirai, T. Nakazawa, R. Ally, I. Segal, B. C. Wong, S. K. Lam, F. O. Olfat, T. Boren, L. Engstrand, O. Torres, R. Schneider, J. E. Thomas, S. Czinn, and D. E. Berg. 2000. Differences in genotypes of Helicobacter pylori from different human populations. J. Bacteriol. 182:3210-3218.
37. Kersulyte, D., B. Velapatino, G. Dailide, A. K. Mukhopadhyay, Y. Ito, L. Cahuayme, A. J. Parkinson, R. H. Gilman, and D. E. Berg. 2002. Transposable element IShp608 of Helicobacter pylori: nonrandom geographic distribution, functional organization, and insertion specificity. J. Bacteriol. 184:992-1002.
38. Kidwell, M. G., and D. R. Lisch. 2002. Perspective: transposable elements, parasitic DNA, and genome evolution. Evol. Int. J. Org. Evol. 55:1-24.
39. Kiss, J., M. Szabo, and F. Olasz. 2003. Site-specific recombination by the DDE family member mobile element IS30 transposase. Proc. Natl. Acad. Sci. USA 100:15000-15005.
40. Lampe, D. J., D. J. Witherspoon, F. N. Soto-Adames, and H. M. Robertson. 2003. Recent horizontal transfer of mellifera subfamily mariner transposons into insect lineages representing four different orders shows that selection acts only during horizontal transfer. Mol. Biol. Evol. 20:554-562.
41. Lawrence, J. G., H. Ochman, and D. L. Hartl. 1992. The evolution of insertion sequences within enteric bacteria. Genetics 131:9-20.
42. Leon, O., and M. Roth. 2000. Zinc fingers: DNA binding and protein-protein interactions. Biol. Res. 33:21-30.
43. Levin, B. R. 1993. The accessory genetic elements of bacteria: existence conditions and (co)evolution. Curr. Opin. Genet. Dev. 3:849-854.
44. Maynard Smith, J., and N. H. Smith. 1998. Detecting recombination from gene trees. Mol. Biol. Evol. 15:590-599.
45. Modi, R. I., L. H. Castilla, S. Puskas-Rozsa, R. B. Helling, and J. Adams. 1992. Genetic changes accompanying increased fitness in evolving populations of Escherichia coli. Genetics 130:241-249.
46. Mukhopadhyay, A. K., D. Kersulyte, J. Y. Jeong, S. Datta, Y. Ito, A. Chowdhury, S. Chowdhury, A. Santra, S. K. Bhattacharya, T. Azuma, G. B. Nair, and D. E. Berg. 2000. Distinctiveness of genotypes of Helicobacter pylori in Calcutta, India. J. Bacteriol. 182:3219-3227.
47. Mukhopadhyay, A. K., J. Y. Jeong, D. Dailidiene, P. S. Hoffman, and D. E. Berg. 2003. The fdxA ferredoxin gene can down-regulate frxA nitroreductase gene expression and is essential in many strains of Helicobacter pylori. J. Bacteriol. 185:2927-2935.
48. Naas, T., M. Blot, W. M. Fitch, and W. Arber. 1995. Dynamics of IS-related genetic rearrangements in resting Escherichia coli K-12. Mol. Biol. Evol. 12:198-207.
49. Page, R. D. M. 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
50. Page, R. D. M., and E. C. Holmes. 1998. Molecular evolution: a phylogenetic approach. Blackwell Science Inc., Maiden, Mass.
51. Palys, T., L. K. Nakamura, and F. M. Cohan. 1997. Discovery and classification of ecological diversity in the bacterial world: the role of DNA sequence data. Int. J. Syst. Bacteriol. 47:1145-1156.
52. Pan, Z. J., D. E. Berg, R. W. van der Hulst, W. W. Su, A. Raudonikiene, S. D. Xiao, J. Dankert, G. N. Tytgat, and A, van der Ende. 1998. Prevalence of vacuolating cytotoxin production and distribution of distinct vacA alleles in Helicobacter pylori from China. J. Infect. Dis. 178:220-226.
53. Papadopoulos, D., D. Schneider, J. Meier-Eiss, W. Arber, R. E. Lenski, and M. Blot. 1999. Genomic evolution during a 10,000-generation experiment with bacteria. Proc. Natl. Acad. Sci. USA 96:3807-3812.
54. Picardeau, M., T. J, Bull, and V. Vincent. 1997. Identification and characterization of IS-like elements in Mycobacterium gordonae. FEMS Microbiol. Lett. 154:95-102.
55. Posada, D., and K. A. Crandall. 1998. MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817-818.
56. Reynolds, A. E., J. Felton, and A. Wright. 1981. Insertion of DNA activates the cryptic bgl operon in E. coli K12. Nature 293:625-629.
57. Reznikoff, W. S. 2003. Tn5 as a model for understanding DNA transposition. Mol. Microbiol. 47:1199-1206.
58. Rozas, J., and R. Rozas. 1999. DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174-175.
59. Smith, M. C., and H. M. Thorpe. 2002. Diversity in the serine recombinases. Mol. Microbiol. 44:299-307.
60. Stanley, T. L., C. D. Ellermeier, and J. M. Slauch. 2000. Tissue-specific gene expression identifies a gene in the lysogenic phage Gifsy-1 that affects Salmonella enterica serovar Typhimurium survival in Peyer's patches. J. Bacteriol. 182:4406-4413.
61. Suerbaum, S., J. M. Smith, K, Bapumia, G. Morelli, N. H. Smith, E. Kunstmann, I. Dyrek, and M. Achtman. 1998. Free recombination in Helicobacter pylori. Proc. Natl. Acad. Sci. USA 95:12619-12624.
62. Swofford, D. L., G. J. Olsen, P. J. Wadell, and D. M. Hillis. 1996. Phylogenetic inference, p. 407-514. In D. M. Hillis, C. Moritc, and B. K. Mable (ed.), Molecular systematics. Sinauer Associates Inc., Sunderland, Mass.
63. Swofford, D. L. 2003. PAUP. Phylogenetic analysis using parsimony (and other methods), version 4. Sinauer Associates, Sunderland, Mass.
64. Wakeley, J., and J. Hey. 1997. Estimating ancestral population parameters. Genetics 145:847-855.
65. Witherspoon, D. J. 1999. Selective constraints on P element evolution. Mol. Biol. Evol. 16:472-478.
66. Woolhouse, M. E., J. P. Webster, E. Domingo, B. Charlesworth, and B. R. Levin. 2003. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat. Genet. 32:569-577.
67. Yang, Z. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput. Appl. Biosci. 13:555-556.
68. Yang, Z., R. Nielsen, N. Goldman, and A. M. Pedersen. 2000. Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431-449.