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Volume 8, Issue 2

Genomic differentiation within East Asian Open Access

Abstract

The East Asian region, including China, Japan and Korea, accounts for half of gastric cancer deaths. However, different areas have contrasting gastric cancer incidences and the population structure of in this ethnically diverse region is yet unknown. We aimed to investigate genomic differences in between these areas to identify sequence polymorphisms associated with increased cancer risk. We analysed 381 . genomes collected from different areas of the three countries using phylogenetic and population genetic tools to characterize population differentiation. The functional consequences of SNPs with a highest fixation index (Fst) between subpopulations were examined by mapping amino acid changes on 3D protein structure, solved or modelled. Overall, 329/381 genomes belonged to the previously identified hspEAsia population indicating that import of bacteria from other regions of the world has been uncommon. Seven subregional clusters were found within hspEAsia, related to subpopulations with various ethnicities, geographies and gastric cancer risks. Subpopulation-specific amino acid changes were found in multidrug exporters (), transporters (), outer membrane proteins () and several genes involved in host interaction, such as a catalase site, involved in HO entrance, and a flagellin site mimicking host glycosylation. Several of the top hits, including , , / and have been found to be differentiated within the Americas in previous studies, indicating that a handful of genes may be key to local geographic adaptation. within East Asia are not homogeneous but have become differentiated geographically at multiple loci that might have facilitated adaptation to local conditions and hosts. This has important implications for further evaluation of these changes in relation to the varying gastric cancer incidence between geographical areas in this region.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): bacterial pathogenesis , fixation index , flagellin glycosylation , gastric cancer , multidrug efflux pump , outer membrane protein and population genomics
Funding
This study was supported by the:
  • Shanghai Municipal Science and Technology Major Project (Award 2019SHZDZX02)
    • Principle Award Recipient: DanielFalush
  • Ministry of Education, Culture, Sports, Science and Technology (Award 19K22543)
    • Principle Award Recipient: IchizoKobayashi
  • Swedish Research Council (Award 2018-05973)
    • Principle Award Recipient: KaisaThorell
  • National Major Science and Technology Projects of China (Award 2018ZX10712-001)
    • Principle Award Recipient: JianzhongZhang
  • Chinese Center for Disease Control and Prevention (Award 2014SKLID102)
    • Principle Award Recipient: JianzhongZhang
© 2022 The Authors
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2022-02-21
2024-05-12
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References

  1. Moodley Y, Linz B, Bond RP, Nieuwoudt M, Soodyall H et al. Age of the association between Helicobacter pylori and man. PLoS Pathog 2012; 8:5 [View Article] [PubMed]
     [Google Scholar]
  2. Falush D, Wirth T, Linz B, Pritchard JK, Stephens M et al. Traces of human migrations in Helicobacter pylori populations. Science 2003; 299:1582–1585 [View Article] [PubMed]
     [Google Scholar]
  3. Munoz-Ramirez ZY, Pascoe B, Mendez-Tenorio A, Mourkas E, Sandoval-Motta S et al. A 500-year tale of co-evolution, adaptation, and virulence: Helicobacter pylori in the Americas. ISME J 2021; 15:78–92 [View Article] [PubMed]
     [Google Scholar]
  4. GBD 2017 Stomach Cancer Collaborators The global, regional, and national burden of stomach cancer in 195 countries, 1990-2017: a systematic analysis for the Global Burden of Disease study 2017. Lancet Gastroenterol Hepatol 2020; 5:42–54 [View Article] [PubMed]
     [Google Scholar]
  5. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA et al. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68:394–424 [View Article] [PubMed]
     [Google Scholar]
  6. Kawai M, Furuta Y, Yahara K, Tsuru T, Oshima K et al. Evolution in an oncogenic bacterial species with extreme genome plasticity: Helicobacter pylori East Asian genomes. BMC Microbiol 2011; 11:104 [View Article] [PubMed]
     [Google Scholar]
  7. Furuta Y, Yahara K, Hatakeyama M, Kobayashi I. Evolution of cagA oncogene of Helicobacter pylori through recombination. Plos One 2011; 6:e23499 [View Article] [PubMed]
     [Google Scholar]
  8. Wong BC, Lam SK, Wong WM, Chen JS, Zheng TT et al. Helicobacter pylori eradication to prevent gastric cancer in a high-risk region of China: a randomized controlled trial. JAMA 2004; 291:187–194 [View Article] [PubMed]
     [Google Scholar]
  9. Chen W, Sun K, Zheng R, Zeng H, Zhang S et al. Cancer incidence and mortality in China, 2014. Chin J Cancer Res 2018; 30:1–12 [View Article] [PubMed]
     [Google Scholar]
  10. He J, Chen W. Annual Report of Cancer Registration in China National Cancer Center, China: 2017
     [Google Scholar]
  11. Jung KW, Won YJ, Kong HJ, CM O, Lee DH et al. Cancer statistics in Korea: incidence, mortality, survival, and prevalence in 2011. Cancer Res Treat 2014; 46:109–123 [View Article] [PubMed]
     [Google Scholar]
  12. Eom BW, Jung KW, Won YJ, Yang H, Kim YW. Trends in Gastric Cancer Incidence According to the Clinicopathological Characteristics in Korea, 1999-2014. Cancer Res Treat 2018; 50:1343–1350 [View Article] [PubMed]
     [Google Scholar]
  13. Bray FC, Mery L, Piñeros M, Znaor A, Zanetti R et al. CI5PLUS: Cancer Incidence in Five Continents Time Trends; 2017 http://ci5.iarc.fr/CI5plus
  14. National Cancer Center Cancer Control Information Cente Graph database: Center for Cancer Control and Information Services, National Cancer Center Japan. http://gdb.ganjoho.jp
  15. Guo Y, ZX L, Zhang JY, JL M, Zhang L et al. Association Between Lifestyle Factors, Vitamin and Garlic Supplementation, and Gastric Cancer Outcomes: A Secondary Analysis of a Randomized Clinical Trial. JAMA Netw Open 2020; 3:e206628 [View Article] [PubMed]
     [Google Scholar]
  16. Seemann T. Snippy: fast bacterial variant calling from NGS reads. github.com/tseemann/snippy 2015
     [Google Scholar]
  17. Lawson DJ, Hellenthal G, Myers S, Falush D. Inference of population structure using dense haplotype data. PLoS Genet 2012; 8:e1002453 [View Article] [PubMed]
     [Google Scholar]
  18. Yahara K, Furuta Y, Oshima K, Yoshida M, Azuma T et al. Chromosome painting in silico in a bacterial species reveals fine population structure. Mol Biol Evol 2013; 30:1454–1464 [View Article]
     [Google Scholar]
  19. Price MN, Dehal PS, Arkin AP. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 2009; 26:1641–1650 [View Article]
     [Google Scholar]
  20. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article]
     [Google Scholar]
  21. Pfeifer B, Wittelsbürger U, Ramos-Onsins SE, Lercher MJ. PopGenome: an efficient Swiss army knife for population genomic analyses in R. Mol Biol Evol 2014; 31:1929–1936 [View Article] [PubMed]
     [Google Scholar]
  22. The pymol molecular Graphics system. Schrłdinger, LLC; 2000 [PubMed]
  23. Matsunari O, Shiota S, Suzuki R, Watada M, Kinjo N et al. Association between Helicobacter pylori virulence factors and gastroduodenal diseases in Okinawa, Japan. J Clin Microbiol 2012; 50:876–883 [View Article] [PubMed]
     [Google Scholar]
  24. Japanese Archipelago Human Population Genetics Consortium Jinam T, Nishida N, Hirai M, Kawamura S et al. The history of human populations in the Japanese Archipelago inferred from genome-wide SNP data with a special reference to the Ainu and the ryukyuan populations. J Hum Genet 2012; 57:787–795 [View Article] [PubMed]
     [Google Scholar]
  25. van Amsterdam K, Bart A, van der Ende A. A Helicobacter pylori TolC efflux pump confers resistance to metronidazole. Antimicrob Agents Chemother 2005; 49:1477–1482 [View Article] [PubMed]
     [Google Scholar]
  26. Trainor EA, Horton KE, Savage PB, Testerman TL, McGee DJ. Role of the HefC efflux pump in Helicobacter pylori cholesterol-dependent resistance to ceragenins and bile salts. Infect Immun 2011; 79:88–97 [View Article] [PubMed]
     [Google Scholar]
  27. Kutschke A, de Jonge BL. Compound efflux in Helicobacter pylori . Antimicrob Agents Chemother 2005; 49:3009–3010 [View Article] [PubMed]
     [Google Scholar]
  28. Zwama M, Yamasaki S, Nakashima R, Sakurai K, Nishino K et al. Multiple entry pathways within the efflux transporter AcrB contribute to multidrug recognition. Nat Commun 2018; 9:124 [View Article] [PubMed]
     [Google Scholar]
  29. Fischer F, Robbe-Saule M, Turlin E, Mancuso F, Michel V et al. Characterization in Helicobacter pylori of a nickel transporter essential for colonization that was acquired during evolution by gastric Helicobacter species. PLoS Pathog 2016; 12:e1006018 [View Article] [PubMed]
     [Google Scholar]
  30. Maki-Yonekura S, Matsuoka R, Yamashita Y, Shimizu H, Tanaka M et al. Hexameric and pentameric complexes of the ExbBD energizer in the Ton system. Elife 2018; 7:e35419 [View Article]
     [Google Scholar]
  31. Thorell K, Yahara K, Berthenet E, Lawson DJ, Mikhail J et al. Rapid evolution of distinct Helicobacter pylori subpopulations in the Americas. PLoS Genet 2017; 13: [View Article] [PubMed]
     [Google Scholar]
  32. Hawtin PR, Delves HT, Newell DG. The demonstration of nickel in the urease of Helicobacter pylori by atomic absorption spectroscopy. FEMS Microbiol Lett 1991; 61:51–54 [View Article] [PubMed]
     [Google Scholar]
  33. Alm RA, Bina J, Andrews BM, Doig P, Hancock RE et al. Comparative genomics of Helicobacter pylori: analysis of the outer membrane protein families. Infect Immun 2000; 68:4155–4168 [View Article] [PubMed]
     [Google Scholar]
  34. Page WJ, Huyer G, Huyer M, Worobec EA. Characterization of the porins of Campylobacter jejuni and Campylobacter coli and implications for antibiotic susceptibility. Antimicrob Agents Chemother 1989; 33:297–303 [View Article] [PubMed]
     [Google Scholar]
  35. Bauwens E, Joosten M, Taganna J, Rossi M, Debraekeleer A et al. In silico proteomic and phylogenetic analysis of the outer membrane protein repertoire of gastric Helicobacter species. Sci Rep 2018; 8:15453 [View Article] [PubMed]
     [Google Scholar]
  36. De E, Jullien M, Labesse G, Pages JM, Molle G et al. MOMP (major outer membrane protein) of Campylobacter jejuni; a versatile pore-forming protein. FEBS Lett 2000; 469:93–97 [View Article] [PubMed]
     [Google Scholar]
  37. Kavermann H, Burns BP, Angermuller K, Odenbreit S, Fischer W et al. Identification and characterization of Helicobacter pylori genes essential for gastric colonization. J Exp Med 2003; 197:813–822 [View Article] [PubMed]
     [Google Scholar]
  38. Quandt EM, Gollihar J, Blount ZD, Ellington AD, Georgiou G et al. Fine-tuning citrate synthase flux potentiates and refines metabolic innovation in the Lenski evolution experiment. Elife 2015; 4:e09696 [View Article] [PubMed]
     [Google Scholar]
  39. Richter C, Mukherjee O, Ermert D, Singh B, YC S et al. Moonlighting of Helicobacter pylori catalase protects against complement-mediated killing by utilising the host molecule vitronectin. Sci Rep 2016; 6:24391 [View Article] [PubMed]
     [Google Scholar]
  40. Jha V, Chelikani P, Carpena X, Fita I, Loewen PC. Influence of main channel structure on H2O2 access to the heme cavity of catalase KatE of Escherichia coli . Arch Biochem Biophys 2012; 526:54–59 [View Article] [PubMed]
     [Google Scholar]
  41. Kreutzberger MAB, Ewing C, Poly F, Wang F, Egelman EH. Atomic structure of the Campylobacter jejuni flagellar filament reveals how epsilon Proteobacteria escaped Toll-like receptor 5 surveillance. Proc Natl Acad Sci U S A 2020; 117:16985–16991 [View Article] [PubMed]
     [Google Scholar]
  42. Schirm M, Soo EC, Aubry AJ, Austin J, Thibault P et al. Structural, genetic and functional characterization of the flagellin glycosylation process in Helicobacter pylori . Mol Microbiol 2003; 48:1579–1592 [View Article] [PubMed]
     [Google Scholar]
  43. Wang F, Burrage AM, Postel S, Clark RE, Orlova A et al. A structural model of flagellar filament switching across multiple bacterial species. Nat Commun 2017; 8:960 [View Article] [PubMed]
     [Google Scholar]
  44. Perkins A, Tudorica DA, Amieva MR, Remington SJ, Guillemin K. Helicobacter pylori senses bleach (HOCl) as a chemoattractant using a cytosolic chemoreceptor. PLoS Biol 2019; 17:e3000395 [View Article] [PubMed]
     [Google Scholar]
  45. Higashi H, Tsutsumi R, Fujita A, Yamazaki S, Asaka M et al. Biological activity of the Helicobacter pylori virulence factor CagA is determined by variation in the tyrosine phosphorylation sites. Proc Natl Acad Sci U S A 2002; 99:14428–14433 [View Article] [PubMed]
     [Google Scholar]
  46. Ailloud F, Didelot X, Woltemate S, Pfaffinger G, Overmann J et al. Within-host evolution of Helicobacter pylori shaped by niche-specific adaptation, intragastric migrations and selective sweeps. Nat Commun 2019; 10:2273 [View Article] [PubMed]
     [Google Scholar]
  47. Noto JM, Lee JY, Gaddy JA, Cover TL, Amieva MR et al. Regulation of Helicobacter pylori Virulence Within the Context of Iron Deficiency. J Infect Dis 2015; 211:1790–1794 [View Article] [PubMed]
     [Google Scholar]
  48. Carrizo-Chavez MA, Cruz-Castaneda A, Olivares-Trejo Jde J. The frpB1 gene of Helicobacter pylori is regulated by iron and encodes a membrane protein capable of binding haem and haemoglobin. FEBS Lett 2012; 586:875–879 [View Article] [PubMed]
     [Google Scholar]
  49. Cao Q, Didelot X, Wu Z, Li Z, He L et al. Progressive genomic convergence of two Helicobacter pylori strains during mixed infection of a patient with chronic gastritis. Gut 2015; 64:554–561 [View Article] [PubMed]
     [Google Scholar]
  50. Bubendorfer S, Krebes J, Yang I, Hage E, Schulz TF et al. Genome-wide analysis of chromosomal import patterns after natural transformation of Helicobacter pylori . Nat Commun 2016; 7:11995 [View Article] [PubMed]
     [Google Scholar]
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Genomic differentiation within East Asian Helicobacter pylori
M Gen 8, 000676 (2022); https://doi.org/10.1099/mgen.0.000676
/content/journal/mgen/10.1099/mgen.0.000676
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