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BioMed Research International
Volume 2016, Article ID 6106029, 15 pages
http://dx.doi.org/10.1155/2016/6106029
Research Article

Comparative Genomics of H. pylori and Non-Pylori Helicobacter Species to Identify New Regions Associated with Its Pathogenicity and Adaptability

1Center for Scientific Research, Youjiang Medical University for Nationalities, Baise, Guangxi 533000, China
2School of Medical Laboratory Sciences, Youjiang Medical University for Nationalities, Baise, Guangxi 533000, China
3School of Basic Medical Sciences, Youjiang Medical University for Nationalities, Baise, Guangxi 533000, China
4Department of Pathogenic Biology, School of Basic Medical Sciences, Nanjing Medical University, Nanjing, Jiangsu 211166, China

Received 21 July 2016; Revised 17 September 2016; Accepted 11 October 2016

Academic Editor: Wen-Jun Li

Copyright © 2016 De-Min Cao et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. Suerbaum and C. Josenhans, “Helicobacter pylori evolution and phenotypic diversification in a changing host,” Nature Reviews Microbiology, vol. 5, no. 6, pp. 441–452, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. L. Kennemann, X. Didelot, T. Aebischer et al., “Helicobacter pylori genome evolution during human infection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 12, pp. 5033–5038, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. J. G. Kusters, A. H. M. Van Vliet, and E. J. Kuipers, “Pathogenesis of Helicobacter pylori infection,” Clinical Microbiology Reviews, vol. 19, no. 3, pp. 449–490, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Zhang, L. Moise, and S. F. Moss, “H. pylori vaccines: why we still don't have any,” Human Vaccines, vol. 7, no. 11, pp. 1153–1157, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Parsonnet, G. D. Friedman, D. P. Vandersteen et al., “Helicobacter pylori infection and the risk of gastric carcinoma,” New England Journal of Medicine, vol. 325, no. 16, pp. 1127–1131, 1991. View at Publisher · View at Google Scholar · View at Scopus
  6. P. Gueneau and S. Loiseaux-De Goër, “Helicobacter: molecular phylogeny and the origin of gastric colonization in the genus,” Infection, Genetics & Evolution, vol. 1, no. 3, pp. 215–223, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. M. D. Schrenzel, C. L. Witte, J. Bahl et al., “Genetic characterization and epidemiology of helicobacters in non-domestic animals,” Helicobacter, vol. 15, no. 2, pp. 126–142, 2010. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Smet, B. Flahou, I. Mukhopadhya et al., “The other helicobacters,” Helicobacter, vol. 16, no. 1, pp. 70–75, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. Z. Nikin, B. Bogdanovic, B. Kukic, I. Nikolic, and J. Vukojevic, “Helicobacter heilmannii associated gastritis: case report,” Archive of Oncology, vol. 19, no. 3-4, pp. 73–75, 2011. View at Publisher · View at Google Scholar
  10. K. Van Den Bulck, A. Decostere, M. Baele et al., “Identification of non-Helicobacter pylori spiral organisms in gastric samples from humans, dogs, and cats,” Journal of Clinical Microbiology, vol. 43, no. 5, pp. 2256–2260, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. P. L. Melito, C. Munro, P. R. Chipman, D. L. Woodward, T. F. Booth, and F. G. Rodgers, “Helicobacter winghamensis sp. nov., a novel Helicobacter sp. isolated from patients with gastroenteritis,” Journal of Clinical Microbiology, vol. 39, no. 7, pp. 2412–2417, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. A. E. Frick-Cheng, T. M. Pyburn, B. J. Voss, W. H. Mcdonald, M. D. Ohi, and T. L. Cover, “Molecular and structural analysis of the Helicobacter pylori cag Type IV secretion system core complex,” mBio, vol. 7, no. 1, pp. 77–80, 2016. View at Google Scholar
  13. A. Tohidpour, “CagA-mediated pathogenesis of Helicobacter pylori,” Microbial Pathogenesis, vol. 93, pp. 44–55, 2016. View at Publisher · View at Google Scholar
  14. D. Mora and S. Arioli, “Microbial urease in health and disease,” PLoS Pathogens, vol. 10, no. 12, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. T. L. Cover and S. R. Blanke, “Helicobacter pylori VacA, a paradigm for toxin multifunctionality,” Nature Reviews Microbiology, vol. 3, no. 4, pp. 320–332, 2005. View at Publisher · View at Google Scholar · View at Scopus
  16. K. Yahiro, M. Satoh, M. Nakano et al., “Low-density lipoprotein receptor-related protein-1 (LRP1) mediates autophagy and apoptosis caused by Helicobacter pylori VacA,” Journal of Biological Chemistry, vol. 287, no. 37, pp. 31104–31115, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. E. Lerat and H. Ochman, “Recognizing the pseudogenes in bacterial genomes,” Nucleic Acids Research, vol. 33, no. 10, pp. 3125–3132, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. W. Fischer, U. Breithaupt, B. Kern, S. I. Smith, C. Spicher, and R. Haas, “A comprehensive analysis of Helicobacter pylori plasticity zones reveals that they are integrating conjugative elements with intermediate integration specificity,” BMC Genomics, vol. 15, no. 1, article 310, 2014. View at Publisher · View at Google Scholar · View at Scopus
  19. K. P. Haley and J. A. Gaddy, “Helicobacter pylori: genomic insight into the host-pathogen interaction,” International Journal of Genomics, vol. 2015, Article ID 386905, 8 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  20. D. Medini, C. Donati, H. Tettelin, V. Masignani, and R. Rappuoli, “The microbial pan-genome,” Current Opinion in Genetics & Development, vol. 15, no. 6, pp. 589–594, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. H. Tettelin, V. Masignani, M. J. Cieslewicz et al., “Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial ‘pan-genome’,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 39, pp. 13950–13955, 2005. View at Google Scholar
  22. A. L. Delcher, D. Harmon, S. Kasif, O. White, and S. L. Salzberg, “Improved microbial gene identification with GLIMMER,” Nucleic Acids Research, vol. 27, no. 23, pp. 4636–4641, 1999. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Lagesen, P. Hallin, E. A. Rødland, H.-H. Stærfeldt, T. Rognes, and D. W. Ussery, “RNAmmer: consistent and rapid annotation of ribosomal RNA genes,” Nucleic Acids Research, vol. 35, no. 9, pp. 3100–3108, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. K. Katoh and D. M. Standley, “MAFFT multiple sequence alignment software version 7: improvements in performance and usability,” Molecular Biology and Evolution, vol. 30, no. 4, pp. 772–780, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. N. Saitou and M. Nei, “The neighbor-joining method: a new method for reconstructing phylogenetic trees.,” Molecular biology and evolution, vol. 4, no. 4, pp. 406–425, 1987. View at Google Scholar · View at Scopus
  26. S. Kumar, G. Stecher, and K. Tamura, “MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets,” Molecular Biology and Evolution, vol. 33, no. 7, pp. 1870–1874, 2016. View at Publisher · View at Google Scholar
  27. L. Li, C. J. Stoeckert Jr., and D. S. Roos, “OrthoMCL: identification of ortholog groups for eukaryotic genomes,” Genome Research, vol. 13, no. 9, pp. 2178–2189, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Dongen, “A cluster algorithm for graphs,” in Information Systems [INS], pp. 1–40, 2000. View at Google Scholar
  29. M. Y. Galperin, K. S. Makarova, Y. I. Wolf, and E. V. Koonin, “Expanded Microbial genome coverage and improved protein family annotation in the COG database,” Nucleic Acids Research, vol. 43, no. 1, pp. D261–D269, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. R. L. Tatusov, M. Y. Galperin, D. A. Natale, and E. V. Koonin, “The COG database: a tool for genome-scale analysis of protein functions and evolution,” Nucleic Acids Research, vol. 28, no. 1, pp. 33–36, 2000. View at Publisher · View at Google Scholar · View at Scopus
  31. F. Mao, P. Dam, J. Chou, V. Olman, and Y. Xu, “DOOR: a database for prokaryotic operons,” Nucleic Acids Research, vol. 37, supplement 1, pp. D459–D463, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Lerat and H. Ochman, “Ψ-Φ: Exploring the outer limits of bacterial pseudogenes,” Genome Research, vol. 14, no. 11, pp. 2273–2278, 2004. View at Publisher · View at Google Scholar · View at Scopus
  33. P. Jones, D. Binns, H.-Y. Chang et al., “InterProScan 5: genome-scale protein function classification,” Bioinformatics, vol. 30, no. 9, pp. 1236–1240, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. K. D. Pruitt, T. Tatusova, and D. R. Maglott, “NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins,” Nucleic Acids Research, vol. 35, no. 1, pp. D61–D65, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. R. D. Finn, A. Bateman, J. Clements et al., “Pfam: The protein families database,” Nucleic Acids Research, vol. 42, no. 1, pp. D222–D230, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. H. Ogata, S. Goto, K. Sato, W. Fujibuchi, H. Bono, and M. Kanehisa, “KEGG: kyoto encyclopedia of genes and genomes,” Nucleic Acids Research, vol. 27, no. 1, pp. 29–34, 1999. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Ashburner, C. A. Ball, J. A. Blake et al., “Gene ontology: tool for the unification of biology,” Nature Genetics, vol. 25, no. 1, pp. 25–29, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. E. Camon, M. Magrane, D. Barrell et al., “The Gene Ontology Annotation (GOA) Project: implementation of GO in SWISS-PROT, TrEMBL, and InterPro,” Genome Research, vol. 13, no. 4, pp. 662–672, 2003. View at Publisher · View at Google Scholar
  39. E. Westhof, “The amazing world of bacterial structured RNAs,” Genome Biology, vol. 11, no. 11, pp. 79–82, 2010. View at Publisher · View at Google Scholar
  40. G. Storz and D. Haas, “A guide to small RNAs in microorganisms,” Current Opinion in Microbiology, vol. 10, no. 2, pp. 93–95, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. M.-J. Cros, A. De Monte, J. Mariette et al., “RNAspace.org: an integrated environment for the prediction, annotation, and analysis of ncRNA,” RNA, vol. 17, no. 11, pp. 1947–1956, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. N.-F. Alikhan, N. K. Petty, N. L. Ben Zakour, and S. A. Beatson, “BLAST ring image generator (BRIG): simple prokaryote genome comparisons,” BMC Genomics, vol. 12, article no. 402, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. D. Szklarczyk, A. Franceschini, S. Wyder et al., “STRING v10: protein-protein interaction networks, integrated over the tree of life,” Nucleic Acids Research, vol. 43, no. 1, pp. D447–D452, 2015. View at Publisher · View at Google Scholar · View at Scopus
  44. J. R. Warren and B. Marshall, “Unidentified curved bacilli on gastric epithelium in active chronic gastritis,” The Lancet, vol. 321, no. 8336, pp. 1273–1275, 1983. View at Publisher · View at Google Scholar · View at Scopus
  45. J.-F. Tomb, O. White, A. R. Kerlavage et al., “The complete genome sequence of the gastric pathogen Helicobacter pylori,” Nature, vol. 388, no. 6642, pp. 539–547, 1997. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Bryant, C. Chewapreecha, and S. D. Bentley, “Developing insights into the mechanisms of evolution of bacterial pathogens from whole-genome sequences,” Future Microbiology, vol. 7, no. 11, pp. 1283–1296, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. N. A. Moran, “Microbial minimalism: genome reduction in bacterial pathogens,” Cell, vol. 108, no. 5, pp. 583–586, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. F. E. Dewhirst, C. Seymour, G. J. Fraser, B. J. Paster, and J. G. Fox, “Phylogeny of Helicobacter isolates from bird and swine feces and description of Helicobacter pametensis sp. nov.,” International Journal of Systematic Bacteriology, vol. 44, no. 3, pp. 553–560, 1994. View at Publisher · View at Google Scholar · View at Scopus
  49. J. Waldenström, S. L. W. On, R. Ottvall, D. Hasselquist, C. S. Harrington, and B. Olsen, “Avian reservoirs and zoonotic potential of the emerging human pathogen helicobacter canadensis,” Applied & Environmental Microbiology, vol. 69, no. 12, pp. 7523–7526, 2003. View at Publisher · View at Google Scholar · View at Scopus
  50. V. B. Young, C.-C. Chien, K. A. Knox, N. S. Taylor, D. B. Schauer, and J. G. Fox, “Cytolethal distending toxin in avian and human isolates of Helicobacter pullorum,” Journal of Infectious Diseases, vol. 182, no. 2, pp. 620–623, 2000. View at Publisher · View at Google Scholar · View at Scopus
  51. D. Kersulyte, M. Rossi, and D. E. Berg, “Sequence divergence and conservation in genomes of Helicobacter cetorum strains from a dolphin and a whale,” PLoS ONE, vol. 8, no. 12, Article ID e83177, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. R. P. Marini, S. Muthupalani, Z. Shen et al., “Persistent infection of rhesus monkeys with ‘Helicobacter macacae’ and its isolation from an animal with intestinal adenocarcinoma,” Journal of Medical Microbiology, vol. 59, no. 8, pp. 961–969, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Frank, C. Dingemanse, A. M. Schmitz et al., “The complete genome sequence of the murine pathobiont helicobacter typhlonius,” Frontiers in Microbiology, vol. 6, article 1549, 2016. View at Publisher · View at Google Scholar · View at Scopus
  54. F. Haesebrouck, F. Pasmans, B. Flahou et al., “Gastric helicobacters in domestic animals and nonhuman primates and their significance for human health,” Clinical Microbiology Reviews, vol. 22, no. 2, pp. 202–223, 2009. View at Publisher · View at Google Scholar · View at Scopus
  55. D. Falush, T. Wirth, B. Linz et al., “Traces of human migrations in Helicobacter pylori populations,” Science, vol. 299, no. 5612, pp. 1582–1585, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. T. P. Mikkonen, R. I. Kärenlampi, and M.-L. Hänninen, “Phylogenetic analysis of gastric and enterohepatic Helicobacter species based on partial HSP60 gene sequences,” International Journal of Systematic & Evolutionary Microbiology, vol. 54, no. 3, pp. 753–758, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Ali, A. Naz, S. C. Soares et al., “Pan-genome analysis of human gastric pathogen H. pylori: comparative genomics and pathogenomics approaches to identify regions associated with pathogenicity and prediction of potential core therapeutic targets,” BioMed Research International, vol. 2015, Article ID 139580, 17 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  58. C. H. Schilling, M. W. Covert, I. Famili, G. M. Church, J. S. Edwards, and B. O. Palsson, “Genome-scale metabolic model of Helicobacter pylori 26695,” Journal of Bacteriology, vol. 184, no. 16, pp. 4582–4593, 2002. View at Publisher · View at Google Scholar · View at Scopus
  59. K. J. Guillemin and N. R. Salama, “Helicobacter pylori functional genomics,” Methods in Microbiology, vol. 33, pp. 291–319, 2002. View at Publisher · View at Google Scholar
  60. D. N. Sgouras, T. T. H. Trang, and Y. Yamaoka, “Pathogenesis of Helicobacter pylori infection,” Helicobacter, vol. 20, pp. 8–16, 2015. View at Publisher · View at Google Scholar · View at Scopus
  61. M. So, “Pilus retraction powers bacterial twitching motility,” Nature, vol. 407, no. 6800, p. 98, 2000. View at Publisher · View at Google Scholar
  62. R. K. Aziz, M. Breitbart, and R. A. Edwards, “Transposases are the most abundant, most ubiquitous genes in nature,” Nucleic Acids Research, vol. 38, no. 13, pp. 4207–4217, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. J. Lubelski, W. N. Konings, and A. J. M. Driessen, “Distribution and physiology of ABC-type transporters contributing to multidrug resistance in bacteria,” Microbiology and Molecular Biology Reviews, vol. 71, no. 3, pp. 463–476, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. T. Lefébure and M. J. Stanhope, “Evolution of the core and pan-genome of Streptococcus: positive selection, recombination, and genome composition,” Genome Biology, vol. 8, no. 5, article R71, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. C. M. Sharma, S. Hoffmann, F. Darfeuille et al., “The primary transcriptome of the major human pathogen Helicobacter pylori,” Nature, vol. 464, no. 7286, pp. 250–255, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. D. S. Merrell, M. L. Goodrich, G. Otto, L. S. Tompkins, and S. Falkow, “pH-regulated gene expression of the gastric pathogen Helicobacter pylori,” Infection and Immunity, vol. 71, no. 6, pp. 3529–3539, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. Y. Wen, E. A. Marcus, U. Matrubutham, M. A. Gleeson, D. R. Scott, and G. Sachs, “Acid-adaptive genes of Helicobacter pylori,” Infection and Immunity, vol. 71, no. 10, pp. 5921–5939, 2003. View at Publisher · View at Google Scholar · View at Scopus
  68. D. T. Pride, R. J. Meinersmann, and M. J. Blaser, “Allelic variation within Helicobacter pylori babA and babB,” Infection & Immunity, vol. 69, no. 2, pp. 1160–1171, 2001. View at Publisher · View at Google Scholar · View at Scopus
  69. J. Mahdavi, B. Sondén, M. Hurtig et al., “Helicobacter pylori sabA adhesin in persistent infection and chronic inflammation,” Science, vol. 297, no. 5581, pp. 573–578, 2002. View at Publisher · View at Google Scholar · View at Scopus
  70. R. Rad, M. Gerhard, R. Lang et al., “The Helicobacter pylori blood group antigen-binding adhesin facilitates bacterial colonization and augments a nonspecific immune response,” Journal of Immunology, vol. 168, no. 6, pp. 3033–3041, 2002. View at Publisher · View at Google Scholar · View at Scopus
  71. Y. Furuta, H. Namba-Fukuyo, T. F. Shibata et al., “Methylome diversification through changes in DNA methyltransferase sequence specificity,” PLoS Genetics, vol. 10, no. 4, Article ID e1004272, 2014. View at Publisher · View at Google Scholar · View at Scopus
  72. J. K. Hendricks and H. L. T. Mobley, “Helicobacter pylori ABC transporter: effect of allelic exchange mutagenesis on urease activity,” Journal of Bacteriology, vol. 179, no. 18, pp. 5892–5902, 1997. View at Google Scholar · View at Scopus
  73. N. Yan, “Structural advances for the major facilitator superfamily (MFS) transporters,” Trends in Biochemical Sciences, vol. 38, no. 3, pp. 151–159, 2013. View at Publisher · View at Google Scholar · View at Scopus
  74. A. L. Davidson and J. Chen, “ATP-binding cassette transporters in bacteria,” Annual Review of Biochemistry, vol. 73, pp. 241–268, 2004. View at Publisher · View at Google Scholar · View at Scopus
  75. Á. D. Ortega, J. J. Quereda, M. Graciela Pucciarelli, and F. García-del Portillo, “Non-coding RNA regulation in pathogenic bacteria located inside eukaryotic cells,” Frontiers in Cellular and Infection Microbiology, vol. 4, article no. 162, 2014. View at Publisher · View at Google Scholar · View at Scopus
  76. B. Xiao, W. Li, G. Guo et al., “Identification of small noncoding RNAs in Helicobacter pylori by a bioinformatics-based approach,” Current Microbiology, vol. 58, no. 3, pp. 258–263, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. S. Bury-Moné, J.-M. Thiberge, M. Contreras, A. Maitournam, A. Labigne, and H. De Reuse, “Responsiveness to acidity via metal ion regulators mediates virulence in the gastric pathogen Helicobacter pylori,” Molecular Microbiology, vol. 53, no. 2, pp. 623–638, 2004. View at Publisher · View at Google Scholar · View at Scopus
  78. L. Deml, M. Aigner, J. Decker et al., “Characterization of the Helicobacter pylori cysteine-rich protein A as a T-helper cell type 1 polarizing agent,” Infection and Immunity, vol. 73, no. 8, pp. 4732–4742, 2005. View at Publisher · View at Google Scholar · View at Scopus
  79. R. Louwen, R. H. J. Staals, H. P. Endtz, P. Van Baarlen, and J. Van Der Oost, “The role of CRISPR-cas systems in virulence of pathogenic bacteria,” Microbiology and Molecular Biology Reviews, vol. 78, no. 1, pp. 74–88, 2014. View at Publisher · View at Google Scholar · View at Scopus
  80. P. Brahmachary, G. Wang, S. L. Benoit, M. V. Weinberg, R. J. Maier, and T. R. Hoover, “The human gastric pathogen Helicobacter pylori has a potential acetone carboxylase that enhances its ability to colonize mice,” BMC Microbiology, vol. 8, no. 1, article 14, pp. 1–8, 2008. View at Publisher · View at Google Scholar · View at Scopus
  81. M.-J. Zhang, F. Zhao, D. Xiao et al., “Comparative proteomic analysis of passaged Helicobacter pylori,” Journal of Basic Microbiology, vol. 49, no. 5, pp. 482–490, 2009. View at Publisher · View at Google Scholar · View at Scopus