1887

Microbiology

Volume 147, Issue 6

Population genetics of in the southern part of Switzerland analysed by sequencing of four housekeeping genes (, , and ), and by , , and IS genotyping

The GenBank accession numbers for the sequences reported in this paper are AY004351–AY004662

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Abstract

The population biology of 78 strains (71 from Swiss Italian, 4 from East Asian and 3 from South African patients) was investigated by sequence analysis of four housekeeping genes: , , and . The genotype, the presence of and IS, the allelic type, and the resistance to metronidazole, clarithromycin and amoxycillin were determined. A high percentage of DNA polymorphic sites (198% for , 213% for , 237% for and 203% for ) was found. The phylogenetic trees based on the nucleotide sequences of the four gene fragments showed different topologies and were incongruent. The virulence-associated markers were distributed over the dendrograms and no association was found with phylogenetic clusters or clinical manifestations (chronic gastritis, gastric or duodenal ulcer, MALT lymphoma). Moreover, the ratios (calculated with the homoplasy test) ranged from 0742 to 0799, depending on the gene fragment examined. All these observations suggest that exists as a recombinant population. The clustering of the strains according to their geographical origin (USA/Europe, East Asia, South Africa) that has recently been demonstrated elsewhere could only be confirmed for the East Asian s1c strains. In contrast, the South African strains clustered together only in the tree. Presumably, recombination at the different loci has masked the evolutionary relationship among the strains.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): antibiotic resistance , H. pylori , housekeeping genes and MALT lymphoma, gastric mucosa-associated lymphoid tissue lymphoma
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2001-06-01
2021-03-07
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References

  1. Achtman M., Azuma T., Berg D. E.. 7 other authors 1999; Recombination and clonal groupings within Helicobacter pylori from different geographical regions. Mol Microbiol32:459–470[CrossRef]
     [Google Scholar]
  2. Akopyanz N., Bukanov N. O., Westblom T. U., Berg D. E.. 1992a; PCR-based RFLP analysis of DNA sequence diversity in the gastric pathogen Helicobacter pylori . Nucleic Acids Res20:6221–6225[CrossRef]
     [Google Scholar]
  3. Akopyanz N., Bukanov N. O., Westblom T. U., Kresovich S., Berg D. E.. 1992b; DNA diversity among clinical isolates of Helicobacter pylori detected by PCR-based RAPD fingerprinting. Nucleic Acids Res20:5137–5142[CrossRef]
     [Google Scholar]
  4. Alm R. A., Ling L. S., Moir D. T.. 20 other authors 1999; Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori . Nature397:176–180[CrossRef]
     [Google Scholar]
  5. Amann R., Ludwig W., Schleifer K. H.. 1988; Beta-subunit of ATP-synthase: a useful marker for studying the phylogenetic relationship of eubacteria. J Gen Microbiol134:2815–2821
     [Google Scholar]
  6. Atherton J. C., Cao P., Tummuru M. K., Blaser M. J., Cover T. L., Peek R. M. Jr. 1995; Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori . Association of specific vacA types with cytotoxin production and peptic ulceration. J Biol Chem270:17771–17777[CrossRef]
     [Google Scholar]
  7. Blaser M. J.. 1997; Ecology of Helicobacter pylori in the human stomach. J Clin Invest100:759–762[CrossRef]
     [Google Scholar]
  8. Blaser M. J., Perez-Perez G. I., Kleanthous H., Cover T. L., Peek R. M., Chyou P. H., Stemmermann G. N., Nomura A.. 1995; Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res55:2111–2115
     [Google Scholar]
  9. Busse H. J., Denner E. B., Lubitz W.. 1996; Classification and identification of bacteria: current approaches to an old problem. Overview of methods used in bacterial systematics. J Biotechnol47:3–38[CrossRef]
     [Google Scholar]
  10. Campbell S., Fraser A., Holliss B., Schmid J., O’Toole P. W.. 1997; Evidence for ethnic tropism of Helicobacter pylori . Infect Immun65:3708–3712
     [Google Scholar]
  11. Censini S., Lange C., Xiang Z., Crabtree J. E., Ghiara P., Borodovsky M., Rappuoli R., Covacci A.. 1996; Cag, a pathogenicity island of Helicobacter pylori , encodes type I-specific and disease-associated virulence factors. Proc Natl Acad Sci USA93:14648–14653[CrossRef]
     [Google Scholar]
  12. Christensen H., Olsen J. E.. 1998; Phylogenetic relationships of Salmonella based on DNA sequence comparison of atpD encoding the beta subunit of ATP synthase. FEMS Microbiol Lett161:89–96
     [Google Scholar]
  13. Corthésy-Theulaz I. E., Bergonzelli G. E., Henry H., Bachmann D., Schorderet D. F., Blum A. L., Ornston L. N.. 1997; Cloning and characterization of Helicobacter pylori succinyl CoA: acetoacetate CoA-transferase, a novel prokaryotic member of the CoA-transferase family. J Biol Chem272:25659–25667[CrossRef]
     [Google Scholar]
  14. Cover T. L., Tummuru M. K., Cao P., Thompson S. A., Blaser M. J.. 1994; Divergence of genetic sequences for the vacuolating cytotoxin among Helicobacter pylori strains. J Biol Chem269:10566–10573
     [Google Scholar]
  15. Doglioni C., Wotherspoon A. C., Moschini A., de Boni M., Isaacson P. G.. 1992; High incidence of primary gastric lymphoma in northeastern Italy. Lancet339:834–835[CrossRef]
     [Google Scholar]
  16. Eisen J. A.. 1995; The RecA protein as a model molecule for molecular systematic studies of bacteria: comparison of trees of RecAs and 16S rRNAs from the same species. J Mol Evol41:1105–1123
     [Google Scholar]
  17. EUROGAST Study Group 1993; An international association between Helicobacter pylori infection and gastric cancer. Lancet341:1359–1362[CrossRef]
     [Google Scholar]
  18. Felsenstein J.. 1988; Phylogenies from molecular sequences: inference and reliability. Annu Rev Genet22:521–565[CrossRef]
     [Google Scholar]
  19. Figueiredo C., Quint W. G., Sanna R.. 7 other authors 2000; Genetic organization and heterogeneity of the ice A locus of Helicobacter pylori . Gene 246:59–68[CrossRef]
     [Google Scholar]
  20. Forbes K. J., Fang Z., Pennington T. H.. 1995; Allelic variation in the Helicobacter pylori flagellin genes flaA and flaB : its consequences for strain typing schemes and population structure. Epidemiol Infect114:257–266[CrossRef]
     [Google Scholar]
  21. Garner R. M., Mobley H. L., Fulkerson J. Jr. 1998; Helicobacter pylori glutamine synthetase lacks features associated with transcriptional and posttranslational regulation. Infect Immun66:1839–1847
     [Google Scholar]
  22. Gibson J. R., Slater E., Xerry J., Tompkins D. S., Owen R. J.. 1998; Use of an amplified-fragment length polymorphism technique to fingerprint and differentiate isolates of Helicobacter pylori . J Clin Microbiol36:2580–2585
     [Google Scholar]
  23. Go M. F., Graham D. Y.. 1996; Presence of the cagA gene in the majority of Helicobacter pylori strains is independent of whether the individual has duodenal ulcer or asymptomatic gastritis. Helicobacter1:107–111[CrossRef]
     [Google Scholar]
  24. Go M. F., Kapur V., Graham D. Y., Musser J. M.. 1996; Population genetic analysis of Helicobacter pylori by multilocus enzyme electrophoresis: extensive allelic diversity and recombinational population structure. J Bacteriol178:3934–3938
     [Google Scholar]
  25. Go M. F., Cissell L., Graham D. Y.. 1998; Failure to confirm association of vacA gene mosaicism with duodenal ulcer disease. Scand J Gastroenterol33:132–136[CrossRef]
     [Google Scholar]
  26. Hofreuter D., Odenbreit S., Henke G., Haas R.. 1998; Natural competence for DNA transformation in Helicobacter pylori : identification and genetic characterization of the comB locus. Mol Microbiol28:1027–1038[CrossRef]
     [Google Scholar]
  27. Holcombe C.. 1992; Helicobacter pylori : the African enigma. Gut33:429–431[CrossRef]
     [Google Scholar]
  28. Hook-Nikanne J., Berg D. E., Kersulyte D., Tummuru M. K., Blaser M. J., Peek R. M. Jr. 1998; DNA sequence conservation and diversity in transposable element IS 605 of Helicobacter pylori . Helicobacter3:79–85[CrossRef]
     [Google Scholar]
  29. Kumada Y., Benson D. R., Hillemann D., Hosted T. J., Rochefort D. A., Thompson C. J., Wohlleben W., Tateno Y.. 1993; Evolution of the glutamine synthetase gene, one of the oldest existing and functioning genes. Proc Natl Acad Sci USA90:3009–3013[CrossRef]
     [Google Scholar]
  30. Kumar S., Tamura K., Nei M.. 1993; mega: Molecular Evolutionary Genetics Analysis, version 1.01. University Park, PA: Pennsylvania State University;
     [Google Scholar]
  31. Letley D. P., Lastovica A., Louw J. A., Hawkey C. J., Atherton J. C.. 1999; Allelic diversity of the Helicobacter pylori vacuolating cytotoxin gene in South Africa: rarity of the vacA s1a genotype and natural occurrence of an s2/m1 allele. J Clin Microbiol37:1203–1205
     [Google Scholar]
  32. McGowan C. C., Cover T. L., Blaser M. J.. 1997; Analysis of F1F0-ATPase from Helicobacter pylori . Infect Immun65:2640–2657
     [Google Scholar]
  33. Maeda S., Ogura K., Yoshida H., Kanai F., Ikenoue T., Kato N., Shiratori Y., Omata M.. 1998; Major virulence factors, VacA and CagA, are commonly positive in Helicobacter pylori isolates in Japan. Gut42:338–343[CrossRef]
     [Google Scholar]
  34. Maggi-Solcà N., Valsangiacomo C., Piffaretti J.-C.. 2000; Prevalence of Helicobacter pylori resistant strains in the Southern part of Switzerland. Clin Microbiol Infect6:38–40[CrossRef]
     [Google Scholar]
  35. Maiden M. C., Bygraves J. A., Feil E.. 10 other authors 1998; Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci USA95:3140–3145[CrossRef]
     [Google Scholar]
  36. Maynard Smith J., Smith N. H.. 1998; Detecting recombination from gene trees. Mol Biol Evol15:590–599[CrossRef]
     [Google Scholar]
  37. Miehlke S., Kibler K., Kim J. G., Figura N., Small S. M., Graham D. Y., Go M. F.. 1996; Allelic variation in the cagA gene of Helicobacter pylori obtained from Korea compared to the United States. Am J Gastroenterol91:1322–1325
     [Google Scholar]
  38. Mukhopadhyay A. K., Kersulyte D., Jeong J. Y.. 9 other authors 2000; Distinctiveness of genotypes of Helicobacter pylori in Calcutta, India. J Bacteriol182:3219–3227[CrossRef]
     [Google Scholar]
  39. Musser J. M.. 1996; Molecular population genetic analyses of emerged bacterial pathogens: selected insights . . Emerg Infect Dis 2:1–17[CrossRef]
     [Google Scholar]
  40. Pan Z. J., Berg D. E., Su W. W., Raudonikiene A., Xiao S. D., Dankert J., Tytgat G. N., Van der Hulst R. W., Van der Ende A.. 1998; Prevalence of vacuolating cytotoxin production and distribution of distinct vacA alleles in Helicobacter pylori from China. J Infect Dis178:220–226[CrossRef]
     [Google Scholar]
  41. Peek R. M. Jr, Thompson S. A., Donahue J. P., Tham K. T., Atherton J. C., Blaser M. J., Miller G. G.. 1998; Adherence to gastric epithelial cells induces expression of a Helicobacter pylori gene, iceA , that is associated with clinical outcome. Proc Assoc Am Physicians110:531–544
     [Google Scholar]
  42. Piffaretti J.-C., Kressebuch H., Aeschbacher M., Bille J., Bannerman E., Musser J. M., Selander R. K., Rocourt J.. 1989; Genetic characterization of the bacterium Listeria monocytogenes causing epidemic disease. Proc Natl Acad Sci USA86:3818–3822[CrossRef]
     [Google Scholar]
  43. Pounder R. E.. 1995; The prevalence of Helicobacter pylori in different countries. Aliment. Pharmacol Ther9:suppl 233–44
     [Google Scholar]
  44. Roggero E., Zucca E., Pinotti G.. 7 other authors 1995; Eradication of Helicobacter pylori infection in primary low-grade gastric lymphoma of mucosa-associated lymphoid tissue. Ann Intern Med122:767–769[CrossRef]
     [Google Scholar]
  45. Rozas J., Rozas R.. 1999; DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics15:174–174[CrossRef]
     [Google Scholar]
  46. Saitou N., Nei M.. 1987; The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol4:406–425
     [Google Scholar]
  47. Salaun L., Audibert C., Le Lay G., Burucoa C., Fauchere J. L., Picard B.. 1998; Panmictic structure of Helicobacter pylori demonstrated by the comparative study of six genetic markers. FEMS Microbiol Lett161:231–239[CrossRef]
     [Google Scholar]
  48. Schmitt W., Odenbreit S., Heuermann D., Haas R.. 1995; Cloning of the Helicobacter pylori recA gene and functional characterization of its product. Mol Gen Genet248:563–572[CrossRef]
     [Google Scholar]
  49. Selander R. K., Caugant D. A., Ochman H., Musser J. M., Gilmour M. N., Whittam T. S.. 1986; Methods of multilocus enzyme electrophoresis for bacterial population genetics and systematics. Appl Environ Microbiol51:873–884
     [Google Scholar]
  50. Sreevatsan S., Pan X., Stockbauer K. E., Connell N. D., Kreiswirth B. N., Whittam T. S., Musser J. M.. 1997; Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc Natl Acad Sci USA94:9869–9874[CrossRef]
     [Google Scholar]
  51. Suerbaum S., Smith J. M., Bapumia K., Morelli G., Smith N. H., Kunstmann E., Dyrek I., Achtman M.. 1998; Free recombination within Helicobacter pylori . Proc Natl Acad Sci USA95:12619–12624[CrossRef]
     [Google Scholar]
  52. Taylor N. S., Fox J. G., Akopyants N. S.. 7 other authors 1995; Long-term colonization with single and multiple strains of Helicobacter pylori assessed by DNA fingerprinting. J Clin Microbiol33:918–923
     [Google Scholar]
  53. Tee W., Lambert J., Smallwood R., Schembri M., Ross B. C., Dwyer B.. 1992; Ribotyping of Helicobacter pylori from clinical specimens. J Clin Microbiol30:1562–1567
     [Google Scholar]
  54. Thompson S. A., Blaser M. J.. 1995; Isolation of the Helicobacter pylori recA gene and involvement of the recA region in resistance to low pH. Infect Immun63:2185–2193
     [Google Scholar]
  55. Tomb J. F., White O., Kerlavage A. R.. 39 other authors 1997; The complete genome sequence of the gastric pathogen Helicobacter pylori . Nature388:539–547[CrossRef]
     [Google Scholar]
  56. Valsangiacomo C., Balmelli T., Piffaretti J. C.. 1997; A phylogenetic analysis of Borrelia burgdorferi sensu lato based on sequence information from the hbb gene, coding for a histone-like protein. Int J Syst Bacteriol47:1–10[CrossRef]
     [Google Scholar]
  57. Van der Ende A., Pan Z. J., Bart A., Feller M., Xiao S. D., Tytgat G. N., Dankert J., van der Hulst R. W.. 1998; cagA -positive Helicobacter pylori populations in China and The Netherlands are distinct. Infect Immun66:1822–1826
     [Google Scholar]
  58. Van Doorn L. J., Figueiredo C., Sanna R., Plaisier A., Schneeberger P., Quint W. G., de Boer W.. 1998a; Clinical relevance of the cagA , vacA , and iceA status of Helicobacter pylori . Gastroenterology115:58–66[CrossRef]
     [Google Scholar]
  59. Van Doorn L. J., Figueiredo C., Sanna R., Pena S., Midolo P., Ng E. K., Atherton J. C., Blaser M. J., Quint W. G.. 1998b; Expanding allelic diversity of Helicobacter pylori vacA . J Clin Microbiol36:2597–2603
     [Google Scholar]
  60. Van Doorn L. J., Figueiredo C., Rossau R., Jannes G., Sousa J. C., Carneiro F., Quint W. G., van Asbroek M.. 1998c; Typing of Helicobacter pylori vacA gene and detection of cagA gene by PCR and reverse hybridization. J Clin Microbiol36:1271–1276
     [Google Scholar]
  61. Van Doorn L. J., Figueiredo C.,14 other authors Mégraud F.. 1999a; Geographic distribution of vacA allelic types of Helicobacter pylori . Gastroenterology116:823–830[CrossRef]
     [Google Scholar]
  62. Van Doorn L. J., Figueiredo C., Sanna R., Blaser M. J., Quint W. G.. 1999b; Distinct variants of Helicobacter pylori cagA are associated with vacA subtypes. J Clin Microbiol37:2306–2311
     [Google Scholar]
  63. Yamaoka Y., Kodama T., Kita M., Imanishi J., Kashima K., Graham D. Y.. 1998; Relationship of vacA genotypes of Helicobacter pylori to cagA status, cytotoxin production, and clinical outcome. Helicobacter3:241–253[CrossRef]
     [Google Scholar]
  64. Yamaoka Y., Kodama T., Gutierrez O., Kim J. G., Kashima K., Graham D. Y.. 1999; Relationship between Helicobacter pylori iceA , cagA , and vacA status and clinical outcome: studies in four different countries. J Clin Microbiol37:2274–2279
     [Google Scholar]
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Population genetics of Helicobacter pylori in the southern part of Switzerland analysed by sequencing of four housekeeping genes (atpD, glnA, scoB and recA), and by vacA, cagA, iceA and IS605 genotypingThe GenBank accession numbers for the sequences reported in this paper are AY004351–AY004662
Microbiology 147, 1693 (2001); https://doi.org/10.1099/00221287-147-6-1693
/content/journal/micro/10.1099/00221287-147-6-1693
/content/journal/micro/10.1099/00221287-147-6-1693
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