Helicobacter pylori Strain 51 (Korean Isolate): Ordered Overlapping BAC Library, Combined Physical and Genetic Map, and Comparative Analysis with H. pylori Strain 26695 and Strain J99

  • KANG HYUNG-LYUN (Department of Microbiology, Gyeongsang National University College of Medicine, Department of Gyeongsang Institute of Health Sciences, Gyeongsang National University College of Medicine) ;
  • LEE WOO-KON (Department of Microbiology, Gyeongsang National University College of Medicine, Research Institute of Life Science and Central Laboratory, Gyeongsang National University) ;
  • SONG JAE-YOUNG (Department of Microbiology, Gyeongsang National University College of Medicine, Department of Gyeongsang Institute of Health Sciences, Gyeongsang National University College of Medicine) ;
  • CHOI SANG-HAENG (Korea Research Institute for Bioscience and Biotechnology) ;
  • PARK SEONG-GYU (Department of Microbiology, Gyeongsang National University College of Medicine) ;
  • RYU BOK-DEOK (Department of Microbiology, Gyeongsang National University College of Medicine) ;
  • LEE EUN-JOO (Department of Microbiology, Gyeongsang National University College of Medicine) ;
  • KIM JI-SUN (Korea Research Institute for Bioscience and Biotechnology) ;
  • PARK JEONG-UCK (Department of Microbiology, Gyeongsang National University College of Medicine, Department of Gyeongsang Institute of Health Sciences, Gyeongsang National University College of Medicine) ;
  • BAIK SEUNG-CHUL (Department of Microbiology, Gyeongsang National University College of Medicine, Department of Gyeongsang Institute of Health Sciences, Gyeongsang National University College of Medicine) ;
  • CHOI MYOUNG-BUM (Department of Pediatrics, and Gyeongsang National University College of Medicine) ;
  • YOUN HEE-SHANG (Department of Pediatrics, and Gyeongsang National University College of Medicine) ;
  • KO GYUNG-HYUCK (Department of Pathology, and Gyeongsang National University College of Medicine)
  • Published : 2005.08.01

Abstract

We constructed a defined physical and genetic map of H. pylori strain 51, previously isolated from a Korean patient with a duodenal ulcer, by combining a restriction analysis by pulse-field gel electrophoresis with the construction of a BAC library. A Notl-digest of H. pylori strain 51 genome yielded seven fragments, from which the genomic size was estimated to be 1,698$\pm$24 kb. The BAC library was constructed from 50 to 200 kb fragments of HindIII-digested genomic DNA. From 700 BAC clones, an ordered overlapping maxi-set of 82 BAC clones was assembled that covered the entire genome. The positions of 15 genes were localized in the strain 51 genome with 4-22 kb of resolution and were compared with their orthologues in strain 26695 and strain J99. The arrangement of the 15 genes was identical in strain 51 and strain J99, except for flaA and hpaA. The plasticity zone of strain 51, like that of strain J99, was located in the single region, and was shorter than those of strain 26695 and strain J99. The strain 51 plasticity zone consisted of ORFs common only to strain 51 and J99 or to strain 51 and 26695, as well as strain 51-specific ORFs. Three genetic translocations and/or inversions were found between orthologue ORFs in strain 51 and strain J99. These results show that the chromosomal organization of strain 51 differs from Western strains such as strain 26695 and strain J99.

Keywords

References

  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 Doom. 1999. Recombination and clonal groupings within Helicobacter pylori from different geographical regions. Mol. Microbiol. 32: 459-470 https://doi.org/10.1046/j.1365-2958.1999.01382.x
  2. Akopyanz, N., N. O. Bukanov, T. U. Westblom, S. Kresovich, and D. E. Berg. 1992. DNA diversity among clinical isolates of Helicobacter pylori detected by PCR-based RAPD fingerprinting. Nucleic Acids Res. 20: 5137-5142 https://doi.org/10.1093/nar/20.19.5137
  3. Aim, R. A., L. S. Ling, D. T. Moir, B. L. King, E. D. Brown, P. C. Doig, D. R. Smith, B. Noonan, B. C. Guild, B. L. deJonge, G. Carmel, P. J. Tummino, A. Caruso, M. Uria-Nickelsen, D. M. Mills, C. Ives, R. Gibson, D. Merberg, S. D. Mills, Q. Jiang, D. E. Taylor, G. F. Vovis, and T. J. Trust. 1999. Genomic sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397: 176-180 https://doi.org/10.1038/16495
  4. Aim, R. A. and T. J. Trust. 1999. Analysis of the genetic diversity ofHelicobacter pylori: The tale of two genomes. J. Mol. Med. 77: 834-846 https://doi.org/10.1007/s001099900067
  5. Anonymous. 1994. Schistosomes, liver flukes and Helicobacter pylori. IARC Monogr. Eval. Carcinog. Risks Hum. 61: 1241
  6. Baik, S.-C., J.-B. Kim, M.-1. Cho, Y.-c. Kim, C.-G. Park, H.-H. Rhou, H.-J. Choi, and K.-H. Rhee. 1990. Prevalence of Helicobacter pylori infection among normal Korean adults. J. Korean Soc. Microbiol. 25: 455-462
  7. Baik, S.-C., H.-S. Youn, M.-H. Chung, W.-K. Lee, M.-1. Cho, G.-H. Ko, C.-G. Park, H. Kasai, and K.-H. Rhee. 1996. Increased oxidative DNA damage in Helicobacter pylori-infected human gastric mucosa. Cancer Res. 56: 1279-1282
  8. Blaser, M. J. 1987. Gastric Campylobacter-like organisms, gastritis and peptic ulcer disease. Gastroenterology 93: 371-383 https://doi.org/10.1016/0016-5085(87)91028-6
  9. Blaser, M. J. 1990. Helicobacter pylori and the pathogenesis of gastroduodenal inflammation. J. Infect. Dis. 161: 626-633 https://doi.org/10.1093/infdis/161.4.626
  10. Blaser, M. J. 1992. Hypotheses on the pathogenesis and natural history of Helicobacter pylori-induced inflammation. Gastroenterology 102: 720- 727 https://doi.org/10.1016/0016-5085(92)90126-J
  11. Blaser, M. J. 1998. Helicobacter pylori and gastric diseases. Br. Med. J. 316: 1507-1510 https://doi.org/10.1136/bmj.316.7143.1507
  12. Bukanov, N. O. and D. E. Berg. 1994. Ordered cosmid library and high-resolution physical-genetic map of Helicobacter pylori strain NCTCI1638. Mol. Microbiol. 11: 509-523 https://doi.org/10.1111/j.1365-2958.1994.tb00332.x
  13. Cave, D. R. 1997. Section I: Epidemiology and transmission of Helicobacter pylori infection - how is Helicobacter pylori transmitted? Gastroenterology 113: S9-14 https://doi.org/10.1016/S0016-5085(97)80004-2
  14. Chakravarti, D. N., M. J. Fiske, L. D. Fletcher, and R. J. Zagursky. 2000. Application of genomics and proteomics for identification of bacterial gene products as potential vaccine candidates. Vaccine 19: 601-612 https://doi.org/10.1016/S0264-410X(00)00256-5
  15. Choi, K. M., J. K. Park, and S. Y. Hwang. 2003. Pathogenetic impact of vacuolar degeneration by accelerated transport of Helicobacter pylori VacA. J. Microbiol. Biotechnol. 13: 666-672
  16. 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
  17. Feinberg, A. and B. Vogelstein. 1983. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132: 6-13 https://doi.org/10.1016/0003-2697(83)90418-9
  18. Fleischmann, R. D., M. D. Adams, O. White, R. A. Clayton, E. F. Kirkness, A. R. Kerlavage, C. J. Bult, J. F. Tomb, B. A. Dougherty, J. M. Merrick, K. Mckenny, G. Sutton, W. Fitzhugh, C. Fields, J. D. Gocayne, J. Scott, R. Shirley, L. Liu, A. Glodek, J. M. Kelly, J. F. Weidman, C. A. Philips, T. Spriggs, E. Hedblom, M. D. Cotton, T. R. Utterback, M. C. Hanna, D. T. Nguyen, D. M. Saudek, R. C. Brandon, L. D. Fine, J. L. Fritchman, J. L. Fuhrmann, C. M. Fraser, H. O. Smith, and J. C. Venter. 1995. Whole-genome random sequencing and assembly of Haemophilus injluenzae Rd. Science 269: 496-512 https://doi.org/10.1126/science.7542800
  19. Forman, D., D. G. Newell, F. Fullerton, J. W. Yarnell, A. R. Stacey, N. Wald, and F. Sitas. 1991. Association between infection with Helicobacter pylori and risk of gastric cancer: Evidence from a prospective investigation. Br. Med. J. 302: 1302-1305 https://doi.org/10.1136/bmj.302.6788.1302
  20. 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 https://doi.org/10.1111/j.1523-5378.1998.08011.x
  21. Hua, J., H. C. Ng, K. G. Yeoh, and B. Ho. 1999. Predominance of a single strain of Helicobacter pylori in gastric antrum. Helicobacter 4: 28-32 https://doi.org/10.1046/j.1523-5378.1999.09043.x
  22. Ito, Y., T. Azuma, S. Ito, H. Suto, H. Miyaji, Y. Yamazaki, Y. Kohli, and M. Kuriyama. 1998. Full-length sequence analysis of the vacA gene from cytotoxic and noncytotoxic Helicobacter pylori. J. Infect. Dis. 178: 1391-1398 https://doi.org/10.1086/314435
  23. Jiang, Q., K. Hiratsuka, and D. E. Taylor. 1996. Variability of gene order in different Helicobacter pylori strains contributes to genome diversity. Mol. Microbiol. 20: 833-842 https://doi.org/10.1111/j.1365-2958.1996.tb02521.x
  24. Jungblut, P. R., D. Bumann, G. Haas, U. Zimny-Arndt, P. Holland, S. Lamer, F. Siejak, A. Aebischer, and T. F. Meyer. 2000. Comparative proteome analysis of Helicobacter pylori. Mol. Microbiol. 36: 710-725 https://doi.org/10.1046/j.1365-2958.2000.01896.x
  25. Kersulyte, D., H. Chalkauskas, and D. E. Berg. 1999. Emergence of recombinant strains of Helicobacter pylori during human infection. Mol. Microbiol. 31: 31-43 https://doi.org/10.1046/j.1365-2958.1999.01140.x
  26. Kim, J. M., J. E. Shin, M. J. Han, S. H. Park, and D. H. Kim. 2003. Inhibitory effect of Ginseng saponins and polysaccharides on infection and vacuolation of Helicobacter pylori. J. Microbiol. Biotechnol. 13: 706- 709
  27. Kim, S. M., K. H. Lee, N. K. Lee, C. J. Kim, C. H. Kim, and H. D. Paik. 2004. Antagonistic activity of polyfermenticin SCD against Helicobacter pylori KCTC 2948. J. Microbiol. Biotechnol. 14: 148-152
  28. Majumder, R., S. Sengupta, G Khetawat, R. K. Bhadra, S. Roychoudhury, and J. Das. 1996. Physical map of the genome of Vibrio cholerae 569B and localization of genetic markers. J. Bacteriol. 178: 1105 -1112 https://doi.org/10.1128/jb.178.4.1105-1112.1996
  29. Marshall, D. G., W. G Dundon, S. M. Beesley, and C. J. Smyth. 1998. Helicobacter pylori - a conundrum of genetic diversity. Microbiology 144: 2925-2939 https://doi.org/10.1099/00221287-144-11-2925
  30. Nedenskov-Sorensen, P., G. Bukholm, and K. Bovre. 1990. Natural competence for genetic transformation in Campylobacter pylori. J. Infect. Dis. 161: 365-366 https://doi.org/10.1093/infdis/161.2.365
  31. Parsonnet, J., S. Hansen, L. Rodriguez, A. B. Gelb, R. A. Warnke, E. Jellum, N. Orentreich, J. H. Vogelman, and G. D. Friedman. 1994. Helicobacter pylori infection and lymphoma. N. Engl. J. Med. 330: 1132-1136
  32. Peterson, W. 1991. Helicobacter pylori and peptic ulcer disease. N. Engl. J. Med. 324: 1043-1048 https://doi.org/10.1056/NEJM199104113241507
  33. Rhee, K.-H., M.-J. Cho, J.-B. Kim, S.-K. Choi, C.-K. Park, Y.-C. Kim, J.-H. Choi, and K. J. Choe. 1988. A prospective study on the Campylobacter pylori isolated from patients of gastroduodenal inflammatory conditions. J. Korean Soc. Microbiol. 23: 9-16
  34. Rhee, K.-H., H.-S. Youn, S.-c. Baik, W.-K. Lee, M.-J. Cho, H.-J. Choi, K.-Y. Maeng, and K.-W. Ko. 1990. Prevalence of Helicobacter pylori infection in Korea. J. Korean Soc. Microbiol. 25: 475-490
  35. Salama, N., K. Guillemin, T. K. McDaniel, G Sherlock, L. Tompkins, and S. Falkow. 2000. A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. Proc. Natl. Acad. Sci. USA 97: 14668-14673
  36. Salama, N., K. Guillemin, T. K. McDaniel, G Sherlock, L. Tompkins, and S. Falkow. 2000. A whole-genome microarray reveals genetic diversity among Helicobacter pylori strains. Proc. Natl. Acad. Sci. USA 97: 14668-14673
  37. Shizuya, H., B. W. Birren, U. J. Kim, V. Mancino, T. Slepak, Y. Tachiiri, and Simon. 1992. Cloning and stable maintenance of 300-kilobase-pair fragments of human DNA in Escherichia coli using an F-factor-based vector. Proc. Natl. Acad. Sci. USA 89: 8794-879
  38. Shizuya, H., B. W. Birren, U. J. Kim, V. Mancino, T. Slepak, Y. Tachiiri, and Simon. 1992. Cloning and stable maintenance of 300-kilobase-pair fragments of human DNA in Escherichia coli using an F-factor-based vector. Proc. Natl. Acad. Sci. USA 89: 8794-879
  39. Taylor, D. N. and M. J. Blaser. 1991. The epidemiology of Helicobacter pylori infection. Epidemiol. Rev. 13: 42-59 https://doi.org/10.1093/oxfordjournals.epirev.a036078
  40. Taylor, D. E., M. Eaton, N. Chang, and S. M. Salama. 1992. Construction of a Helicobacter pylori genome map and demonstration of diversity at the genome level. J. Bacteriol. 174: 6800-6806 https://doi.org/10.1128/jb.174.21.6800-6806.1992
  41. Taylor, N. S., J. G. Fox, N. S. Akopyants, D. E. Berg, N. Thompson, B. Shames, L. Van, E. Fontham, F. Janney, and F. M. Hunter. 1995. Long-term colonization with single and multiple strains of Helicobacter pylori assessed by DNA fngerprinting. J. Clin. Microbiol. 33: 918-923
  42. Tomb, J.-F., O. White, A. R. Kerlavage, R. A. Clayton, G G Sutton, R. D. Fleischmann, K. A. Ketchum, H. P. Klenk, S. Gill, B. A. Dougherty, K. Nelson, J. Quackenbush, L. Zhou, E. F. Kirkness, S. Peterson, B. Loftus, D. Richardson, R. Dodson, H. G Khalak, A. Glodek, E. K. McKenney, L. M. Fitzegerald, N. Lee, M. D. Adams, E. K. Hickey, D. E. Berg, J. D. Gocayne, T. Utterback, I. D. Peterson, J. M. Kelley, M. D. Cotton, J. M. Weidman, C. Fujii, C. Bowman, L. Watthey, E. Wallin, W. S. Hayes, M. Borodovsky, P. D. Karp, H. O. Smith, C. M. Fraser, and J. C. Venter. 1997. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388: 539-547 https://doi.org/10.1038/41483
  43. Van Der Ende, A., Z.-J. Pan, A. Bart, R. W. M. van Der Hulst, M. Feller, S.-D. Xiao, G. N. J. Tytgat, and J. Dankert. 1998. cagA-positive Helicobacter pylori populations in China and The Netherlands are distinct. Infect. Immun. 66: 1822-1826
  44. Wang, G., M. Z. Humayun, and D. E. Taylor. 1999. Mutation as an origin of genetic variability in Helicobacter pylori. Trends Microbiol. 7: 488-493 https://doi.org/10.1016/S0966-842X(99)01632-7
  45. Warren, J. R. and B. Marshall. 1983. Unified curved bacilli on gastric epithelium in active chronic gastritis. Lancet 1: 1273-1275
  46. Watanabe, T., M. Tada, H. Nagai, S. Sasaki, and M. Nakao. 1998. Helicobacter pylori infection induces gastric cancer in Mongolian gerbils. Gastroenterology 115: 642-648 https://doi.org/10.1016/S0016-5085(98)70143-X
  47. Woo, J. S., B. H. Ha, T. G. Kim, Y. Lim, and K. H. Kim. 2003. Inhibition of Helicobacter pylori adhesion by acidic polysaccharide isolated from Artemisia capillaries. J. Microbiol. Biotechnol. 13: 853-858