Current Microbiology

, Volume 74, Issue 2, pp 224–229 | Cite as

Characterization of Gastric Microbiota in Twins

  • Quanjiang Dong
  • Yongning Xin
  • Lili Wang
  • Xinying Meng
  • Xinjuan Yu
  • Linlin Lu
  • Shiying Xuan


Contribution of host genetic backgrounds in the development of gastric microbiota has not been clearly defined. This study was aimed to characterize the biodiversity, structure and composition of gastric microbiota among twins. A total of four pairs of twins and eight unrelated individuals were enrolled in the study. Antral biopsies were obtained during endoscopy. The bacterial 16S rRNA gene was amplified and pyrosequenced. Sequences were analyzed for the composition, structure, and α and β diversities of gastric microbiota. Proteobacteria, Firmicutes, Bacteroidetes, Actinobacteria, and Fusobacteria were the most predominant phyla of gastric microbiota. Each individual, twins as well as unrelated individuals, harbored a microbiota of distinct composition. There was no evidence of additional similarity in the richness and evenness of gastric microbiota among co-twins as compared to unrelated individuals. Calculations of θYC and PCoA demonstrated that the structure similarity of gastric microbial community between co-twins did not increase compared to unrelated individuals. In contrast, the structure of microbiota was altered enormously by Helicobacter pylori infection. These results suggest that host genetic backgrounds had little effect in shaping the gastric microbiota. This property of gastric microbiota could facilitate the studies discerning the role of microbiota from genetic grounds in the pathogenesis.


Pylorus Infection Actinobacteria Twin Pair Firmicutes Bacteroidetes 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interests.


  1. 1.
    Avershina E, Lundgård K, Sekelja M, Dotterud C, Storrø O, Øien T, Johnsen R, Rudi K (2016) Transition from infant- to adult-like gut microbiota. Environ Microbiol. doi: 10.1111/1462-2920.13248 PubMedGoogle Scholar
  2. 2.
    Aviles-Jimenez F, Vazquez-Jimenez F, Medrano-Guzman R, Mantilla A, Torres J (2014) Stomach microbiota composition varies between patients with non-atrophic gastritis and patients with intestinal type of gastric cancer. Sci Rep 4:4202. doi: 10.1038/srep04202 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Belizário JE, Napolitano M (2015) Human microbiomes and their roles in dysbiosis, common diseases, and novel therapeutic approaches. Front Microbiol 6:1050. doi: 10.3389/fmicb.2015.01050 CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Bik EM, Eckburg PB, Gill SR, Nelson KE, Purdom EA, Francois F, Perez-Perez G, Blaser MJ, Relman DA (2006) Molecular analysis of the bacterial microbiota in the human stomach. Proc Natl Acad Sci USA 103:732–737. doi: 10.1073/pnas.0506655103 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. doi: 10.1038/nmeth.f.303 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Collado MC, Rautava S, Aakko J, Isolauri E, Salminen S (2016) Human gut colonization may be initiated in utero by distinct microbial communities in the placenta andamniotic fluid. Sci Rep 6:23129. doi: 10.1038/srep23129 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Del Chierico F, Vernocchi P, Petrucca A, Paci P, Fuentes S, Praticò G, Capuani G, Masotti A, Reddel S, Russo A, Vallone C, Salvatori G, Buffone E, Signore F, Rigon G, Dotta A, Miccheli A, de Vos WM, Dallapiccola B, Putignani L (2015) Phylogenetic and metabolic tracking of gut microbiota during perinatal development. PLoS ONE 10:e0137347. doi: 10.1371/journal.pone.0137347 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. doi: 10.1093/bioinformatics/btr381 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Eun CS, Kim BK, Han DS, Kim SY, Kim KM, Choi BY, Song KS, Kim YS, Kim JF (2014) Differences in gastric mucosal microbiota profiling in patients with chronic gastritis, intestinal metaplasia, and gastric cancer using pyrosequencing methods. Helicobacter 19:407–416. doi: 10.1111/hel.12145 CrossRefPubMedGoogle Scholar
  10. 10.
    Forsythe SJ, Dolby JM, Webster AD, Cole JA (1988) Nitrate- and nitrite-reducing bacteria in the achlorhydric stomach. J Med Microbiol 25:253–259. doi: 10.1099/00222615-25-4-253 CrossRefPubMedGoogle Scholar
  11. 11.
    Grazul H, Kanda LL, Gondek D (2016) Impact of probiotic supplements on microbiome diversity following antibiotic treatment of mice. Gut Microbes 7:101–114. doi: 10.1080/19490976.2016.1138197 CrossRefPubMedGoogle Scholar
  12. 12.
    Hamady M, Lozupone C, Knight R (2010) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4:17–27. doi: 10.1038/ismej.2009.97 CrossRefPubMedGoogle Scholar
  13. 13.
    Hansen R, Scott KP, Khan S, Martin JC, Berry SH, Stevenson M, Okpapi A, Munro MJ, Hold GL (2015) First-pass meconium samples from healthy term vaginally-delivered neonates: an analysis of the microbiota. PLoS ONE 10:e0133320. doi: 10.1371/journal.pone.0133320 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Homan M, Hojsak I, Kolaček S (2012) Helicobacter pylori in pediatrics. Helicobacter 17:43–48. doi: 10.1111/j.1523-5378.2012.00982.x CrossRefPubMedGoogle Scholar
  15. 15.
    Ibarbalz FM, Pérez MV, Figuerola EL, Erijman L (2014) The bias associated with amplicon sequencing does not affect the quantitative assessment of bacterial community dynamics. PLoS One. 9:e99722. doi: 10.1371/journal.pone.0099722 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Kashtanova DA, Popenko AS, Tkacheva ON, Tyakht AB, Alexeev DG, Boytsov SA (2016) Association between the gut microbiota and diet: fetal life, early childhood and further life. Nutrition 32:620–627. doi: 10.1016/j.nut.2015.12.037 CrossRefPubMedGoogle Scholar
  17. 17.
    Khanna S, Pardi DS (2016) Clinical implications of antibiotic impact on gastrointestinal microbiota and Clostridium difficile infection. Expert Rev Gastroenterol Hepatol 16:1–8. doi: 10.1586/17474124.2016.1158097 Google Scholar
  18. 18.
    Kirpich IA, Petrosino J, Ajami N, Feng W, Wang Y, Liu Y, Beier JI, Barve SS, Yin X, Wei X, Zhang X, McClain CJ (2016) Saturated and unsaturated dietary fats differentially modulate ethanol-induced changes in gut microbiome and metabolome in a mouse model of alcoholic liver disease. Am J Pathol 186:765–776. doi: 10.1016/j.ajpath.2015.11.017 CrossRefPubMedGoogle Scholar
  19. 19.
    Lang D, MAL-ED Network Investigators (2015) Opportunities to assess factors contributing to the development of the intestinal microbiota in infants living in developing countries. Microb Ecol Health Dis 26:28316. doi: 10.3402/mehd.v26.28316 PubMedGoogle Scholar
  20. 20.
    Lee JE, Lee S, Lee H, Song YM, Lee K, Han MJ, Sung J, Ko G (2013) Association of the vaginal microbiota with human papillomavirus infection in a Korean twin cohort. PLoS ONE 8:e63514. doi: 10.1371/journal.pone.0063514 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Lee S, Sung J, Lee J, Ko G (2011) Comparison of the gut microbiotas of healthy adult twins living in South Korea and the United States. Appl Environ Microbiol 77:7433–7437. doi: 10.1128/AEM.05490-11 CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Lee SA, Lim JY, Kim BS, Cho SJ, Kim NY, Kim OB, Kim Y (2015) Comparison of the gut microbiota profile in breast-fed and formula-fed Korean infants using pyrosequencing. Nutr Res Pract 9:242–248. doi: 10.4162/nrp.2015.9.3.242 CrossRefPubMedGoogle Scholar
  23. 23.
    Lertpiriyapong K, Whary MT, Muthupalani S, Lofgren JL, Gamazon ER, Feng Y, Wang TC, Ge Z, Fox JG (2014) Gastric colonisation with a restricted commensal microbiota replicates the promotion of neoplastic lesions by diverse intestinal microbiota in the Helicobacter pylori INS-GAS mouse model of gastric carcinogenesis. Gut 63:54–63. doi: 10.1136/gutjnl-2013-305178 CrossRefPubMedGoogle Scholar
  24. 24.
    Lim ES, Zhou Y, Zhao G, Bauer IK, Droit L, Ndao IM, Warner BB, Tarr PI, Wang D, Holtz LR (2015) Early life dynamics of the human gut virome and bacterial microbiome in infants. Nat Med 21:1228–1234. doi: 10.1038/nm.3950 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Maldonado-Contreras A, Goldfarb KC, Godoy-Vitorino F, Karaoz U, Contreras M, Blaser MJ, Brodie EL, Dominguez-Bello MG (2011) Structure of the human gastric bacterial community in relation to Helicobacter pylori status. ISME J 5:574–579. doi: 10.1038/ismej.2010.149 CrossRefPubMedGoogle Scholar
  26. 26.
    McKenna P, Hoffmann C, Minkah N, Aye PP, Lackner A, Liu Z, Lozupone CA, Hamady M, Knight R, Bushman FD (2008) The macaque gut microbiome in health, lentiviral infection, and chronic enterocolitis. PLoS Pathog 4:e20. doi: 10.1371/journal.ppat.0040020 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Martin ME, Bhatnagar S, George MD, Paster BJ, Canfield DR, Eisen JA, Solnick JV (2013) The impact of Helicobacter pylori infection on the gastric microbiota of the rhesus macaque. PLoS ONE 8:e76375. doi: 10.1371/journal.pone.0076375 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Mason KL, Erb Downward JR, Falkowski NR, Young VB, Kao JY, Huffnagle GB (2012) Interplay between the gastric bacterial microbiota and Candida albicans during post antibiotic recolonization and gastritis. Infect Immun 80:150–158. doi: 10.1128/IAI.05162-11 CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Papapostolou A, Kroffke B, Tatakis DN, Nagaraja HN, Kumar PS (2011) Contribution of host genotype to the composition of health-associated supragingival and subgingival microbiomes. J Clin Periodontol 38:517–524. doi: 10.1111/j.1600-051X.2011.01718.x CrossRefPubMedGoogle Scholar
  30. 30.
    Rolig AS, Cech C, Ahler E, Carter JE, Ottemann KM (2013) The degree of Helicobacter pylori-triggered inflammation is manipulated by preinfection host microbiota. Infect Immun 81:1382–1389. doi: 10.1128/IAI.00044-13 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Schanche M, Avershina E, Dotterud C, Øien T, Storrø O, Johnsen R, Rudi K (2015) High-resolution analyses of overlap in the microbiota between mothers and their children. Curr Microbiol 71:283–290. doi: 10.1007/s00284-015-0843-5 CrossRefPubMedGoogle Scholar
  32. 32.
    Schloss PD, Handelsman J (2006) Introducing SONS, a tool for operational taxonomic unit-based comparisons of microbial community memberships and structures. Appl Environ Microbiol 72:6773–6779. doi: 10.1128/AEM.00474-06 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Si J, Lee S, Park JM, Sung J, Ko G (2015) Genetic associations and shared environmental effects on the skin microbiome of Korean twins. BMC Genom 16:992. doi: 10.1186/s12864-015-2131-y CrossRefGoogle Scholar
  34. 34.
    Simões CD, Maukonen J, Kaprio J, Rissanen A, Pietiläinen KH, Saarela M (2013) Habitual dietary intake is associated with stool microbiota composition in monozygotic twins. J Nutr 143:417–423. doi: 10.3945/jn.112.166322 CrossRefPubMedGoogle Scholar
  35. 35.
    Stearns JC, Lynch MD, Senadheera DB, Tenenbaum HC, Goldberg MB, Cvitkovitch DG, Croitoru K, Moreno-Hagelsieb G, Neufeld JD (2011) Bacterial biogeography of the human digestive tract. Sci Rep 1:170. doi: 10.1038/srep00170 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Wang L, Zhou J, Xin Y, Geng C, Tian Z, Yu X, Dong Q (2016) Bacterial overgrowth and diversification of microbiota in gastric cancer. Eur J Gastroenterol Hepatol 28:261–266. doi: 10.1097/MEG.0000000000000542 CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Wang LL, Yu XJ, Zhan SH, Jia SJ, Tian ZB, Dong QJ (2014) Participation of microbiotain the development of gastric cancer. World J Gastroenterol 20:4948–4952. doi: 10.3748/wjg.v20.i17.4948 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267. doi: 10.1128/AEM.00062-0 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Whary MT, Muthupalani S, Ge Z, Feng Y, Lofgren J, Shi HN, Taylor NS, Correa P, Versalovic J, Wang TC, Fox JG (2014) Helminth co-infection in Helicobacter pylori infected INS-GAS mice attenuates gastric premalignant lesions of epithelial dysplasia and glandular atrophy and preserves colonization resistance of the stomach to lower bowel microbiota. Microbes Infect 16:345–355. doi: 10.1016/j.micinf.2014.01.005 CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Yang I, Woltemate S, Piazuelo MB, Bravo LE, Yepez MC, Romero-Gallo J, Delgado AG, Wilson KT, Peek RM, Correa P, Josenhans C, Fox JG, Suerbaum S (2016) Different gastric microbiota compositions in two human populations with high and low gastric cancer risk in Colombia. Sci Rep 6:18594. doi: 10.1038/srep18594 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Zilberstein B, Quintanilha AG, Santos MA, Pajecki D, Moura EG, Alves PR, MalufFilho F, de Souza JA, Gama-Rodrigues J (2007) Digestive tract microbiota in healthy volunteers. Clinics (Sao Paulo) 62:47–54CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Quanjiang Dong
    • 1
  • Yongning Xin
    • 1
  • Lili Wang
    • 1
  • Xinying Meng
    • 1
  • Xinjuan Yu
    • 1
  • Linlin Lu
    • 1
  • Shiying Xuan
    • 1
  1. 1.Central Laboratories and Department of GastroenterologyQingdao Municipal HospitalQingdaoChina

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