Phylogenetic structure of the global population of Helicobacter Pylori

Cover Page

Cite item

Full Text

Abstract

Helicobacter pylori (H. pylori) is widely considered to be one of the oldest bacteria in the human microbiome. During the co-evolutionary relationships between humans and H. pylori bacterium, spanning at least 100 000 years, a high rate of mutation and recombination events led to extremely high genomic polymorphism of the H. pylori species. Despite this, the large diversity of H. pylori genomes is very well structured, allowing to divide it into different populations associated with the geographic location of H. pylori strains. To date, seven modern H. pylori populations have been determined globally: hpAfrica1, hpAfrica2, hpEastAsia, hpEurope, hpAsia2, hpNEAfrica and hspSahul originated from at least six ancestral populations (ancestral European 1, ancestral European 2, ancestral EastAsia, ancestral Africa1, ancestral Africa2, ancestral Sahul). The global phylogenetic analysis showed that H. pylori is organized into two superlineages: one containing hpAfrica2 and the other containing all other populations in a single monophyletic clade. This indicates that, hpAfrica2 is the most ancient of all H. pylori populations, while the others continued evolutionary development along as mankind spread beyond the African continent. Thus, the H. pylori species populational diversification, which occurred in parallel with paired hosts, allowed us to use H. pylori genetic variants as biological markers, reflecting ethnogeographic migration processes in human history. Moreover, the rapid and dynamic evolution of H. pylori informs about ongoing recombination events enabling use H. pylori as a model both for the co-evolution of pathogenic bacteria and humans as well as for within-individual host pathogen microevolution. This review summarized developments from numerous studies on coevolution process and phylogenetic pattern of the global H. pylori population. The relationships between currently known bacterial populations and subpopulations, related geographical distribution, reconstruction of evolutionary pathway for ancestral and recent populations are detailed. New data on the H. pylori strain populational pattern in Russia, as well as strains circulating in the Northern, Central and South America, are presented. Phylogenetic analysis of the H. pylori population pattern permitted to reconstruct both prehistoric and recent human migrations, demographic processes as well as multilayered evolutionary pathways of H. pylori population.

About the authors

Daria A. Starkova

St. Petersburg Pasteur Institute

Email: dariastarkova13@gmail.com
ORCID iD: 0000-0003-3199-8689

PhD (Biology), Senior Researcher of the Pathogens Identification Laboratory, Senior Researcher of the Laboratory of Molecular Epidemiology and Evolutionary Genetics

Russian Federation, 197101, St. Petersburg, Mira str., 14

A. V. Svarval

St. Petersburg Pasteur Institute

Author for correspondence.
Email: alena.svarval@mail.ru
ORCID iD: 0000-0001-9340-4132

PhD (Medicine), Senior Researcher, Head of the Pathogens Identification Laboratory

Russian Federation, 197101, St. Petersburg, Mira str., 14

References

  1. Борисова Т.В., Готовцев Н.Н., Барашков Н.А., Пак М.В., Алексеева М.П., Иннокентьева Н.Н., Морозов И.В., Бондарь А.А., Лоскутова К.С., Соловьев А.В., Пшенникова В.Г., Рафаилов А.М., Леханова С.Н., Федорова С.А. Филогенетический анализ штаммов Helicobacter pylori, циркулирующих в Якутии, по данным трех генов домашнего хозяйства atpA, mutY, ppa // Вестник Северо-Восточного федерального университета имени М.К. Аммосова. 2018. № 5. C. 15–24. [Borisova T.V., Gotovtsev N.N., Barashkov N.A., Pak M.V., Alekseyeva M.P., Innokent’yeva N.N., Morozov I.V., Bondar’ A.A., Loskutova K.S., Solov’yev A.V., Pshennikova V.G., Rafailov A.M., Lekhanova S.N., Fedorova S.A. Phylogenetic analysis of Helicobacter pylori strains circulating in Yakutia by three housekeeping genes atpA, mutY, ppa. Vestnik Severo-Vostochnogo federal’nogo universiteta imeni M.K. Ammosova = Vestnik of North-Eastern Federal University, 2018, no. 5, pp. 15–24. (In Russ.)] doi: 10.25587/SVFU.2018.67.18653
  2. Сорокин В.М., Сварваль А.В., Водопьянов А.С., Писанов Р.В. Географическое разнообразие штаммов Helicobacter pylori, циркулирующих в европейской части РФ // Инфекция и иммунитет. 2021. Т. 11, № 4. C. 701–706. [Sorokin V.M., Svarval A.V., Vodop’janov A.S., Pisanov R.V. Geographical diversity of Helicobacter pylori strains circulating in the European Part of the Russian Federation. Infektsiya i immunitet = Russian Journal of Infection and Immunity, 2021, vol. 11, no. 4, pp. 701–706. (In Russ.)] doi: 10.15789/2220-7619-GDO-1590
  3. Achtman M., Azuma T., Berg D.E., Ito Y., Morelli G., Pan Z.J., Suerbaum S., Thompson S.A., van der Ende A., van Doorn L.J. Recombination and clonal groupings within Helicobacter pylori from different geographical regions. Mol. Microbiol., 1999, vol. 32, no. 3, pp. 459–470. doi: 10.1046/j.1365-2958.1999.01382.x
  4. Adhikari K., Chacón-Duque J.C., Mendoza-Revilla J., Fuentes-Guajardo M., Ruiz-Linares A. The genetic diversity of the Americas. Annu. Rev. Genomics Hum. Genet., 2017, no. 18, pp. 277–296. doi: 10.1146/annurev-genom-083115-022331
  5. Alexander S.M., Retnakumar R.J., Chouhan D., Devi T.N.B., Dharmaseelan S., Devadas K., Thapa N., Tamang J.P., Lamtha S.C., Chattopadhyay S. Helicobacter pylori in human stomach: the inconsistencies in clinical outcomes and the probable causes. Front. Microbiol., 2021, no. 12: e713955. doi: 10.3389/fmicb.2021.713955
  6. Allen J., O’Connell J. Both half right: updating the evidence for dating first human arrivals in Sahul. Aust. Archaeol., 2014, vol. 78, no. 1, pp. 86–108. doi: 10.1080/03122417.2014.11682025
  7. Baj J., Forma A., Sitarz M., Portincasa P., Garruti G., Krasowska D., Maciejewski R. Helicobacter pylori virulence factors — mechanisms of bacterial pathogenicity in the gastric microenvironment. Cells, 2020, vol. 10, no. 1: 27. doi: 10.3390/cells10010027
  8. Breurec S., Guillard B., Hem S., Brisse S., Dieye F.B., Huerre M., Oung C., Raymond J., Tan T.S., Thiberge J.M., Vong S., Monchy D., Linz B. Evolutionary history of Helicobacter pylori sequences reflect past human migrations in Southeast Asia. PLoS One, 2011, vol. 6, no. 7: e22058. doi: 10.1371/journal.pone.0022058
  9. Falush D., Wirth T., Linz B., Pritchard J.K., Stephens M., Kidd M., Blaser M.J., Graham D.Y., Vacher S., Perez-Perez G.I., Yamaoka Y., Mégraud F., Otto K., Reichard U., Katzowitsch E., Wang X., Achtman M., Suerbaum S. Traces of human migrations in Helicobacter pylori populations. Science, 2003, vol. 299, no. 5612, pp. 1582–1585. doi: 10.1126/science.1080857
  10. Guevara A.A., Torres R.C., Castro-Valencia F.L., Suárez J.J., Criollo-Rayo A., Bravo M.M., Carmona L.C., Echeverry de Polanco M.M., Bohórquez M.E., Torres J. Selective pressure on membrane proteins drives the evolution of Helicobacter pylori Colombian subpopulations. bioRxiv, 2021: 12.14.472690. doi: 10.1101/2021.12.14.472690
  11. Guevara T.A.A. A systematic review of genetic coevolution of homo sapiens and helicobacter pylori: implications for development of gastric cancer. Revista Colombiana de Gastroenterol., 2017, no. 31, pp. 376–390. doi: 10.22516/25007440.113
  12. Gutiérrez-Escobar A.J., Velapatiño B., Borda V., Rabkin C.S., Tarazona-Santos E., Cabrera L., Cok J., Hooper C.C., Jahuira-Arias H., Herrera P., Noureen M., Wang D., Romero-Gallo J., Tran B., Peek R.M. Jr., Berg D.E., Gilman R.H., Camargo M.C. Identification of new Helicobacter pylori subpopulations in native americans and mestizos from Peru. Front. Microbiol., 2020, no. 11: 601839. doi: 10.3389/fmicb.2020.601839
  13. Hanafiah A., Lopes B.S. Genetic diversity and virulence characteristics of Helicobacter pylori isolates in different human ethnic groups. Infect. Genet. Evol., 2020, vol. 78: 104135. doi: 10.1016/j.meegid.2019.104135
  14. Kersulyte D., Kalia A., Gilman R.H., Mendez M., Herrera P., Cabrera L., Velapatiño B., Balqui J., Paredes Puente de la Vega F., Rodriguez Ulloa C.A., Cok J., Hooper C.C., Dailide G., Tamma S., Berg D.E. Helicobacter pylori from Peruvian amerindians: traces of human migrations in strains from remote Amazon, and genome sequence of an Amerind strain. PLoS One, 2010, vol. 5, no. 11: e15076. doi: 10.1371/journal.pone.0015076
  15. Linz B., Balloux F., Moodley Y., Manica A., Liu H., Roumagnac P., Falush D., Stamer C., Prugnolle F., van der Merwe S.W., Yamaoka Y., Graham D.Y., Perez-Trallero E., Wadstrom T., Suerbaum S., Achtman M. An African origin for the intimate association between humans and Helicobacter pylori. Nature, 2007, vol. 445, no. 7130, pp. 915–918. doi: 10.1038/nature05562
  16. Linz B., Vololonantenainab C.R., Seck A., Carod J.F., Dia D., Garin B., Ramanampamonjy R.M., Thiberge J.M., Raymond J., Breurec S. Population genetic structure and isolation by distance of Helicobacter pylori in Senegal and Madagascar. PLoS One, 2014, vol. 9, no. 1: e87355. doi: 10.1371/journal.pone.0087355
  17. Maixner F., Krause-Kyora B., Turaev D., Herbig A., Hoopmann M.R., Hallows J.L., Kusebauch U., Vigl E.E., Malfertheiner P., Megraud F., O’Sullivan N., Cipollini G., Coia V., Samadelli M., Engstrand L., Linz B., Moritz R.L., Grimm R., Krause J., Nebel A., Moodley Y., Rattei T., Zink A. The 5300-year-old Helicobacter pylori genome of the Iceman. Science, 2016, vol. 351, no. 6269, pp. 162–165. doi: 10.1126/science.aad2545
  18. Maixner F., Thorell K., Granehäll L., Linz B., Moodley Y., Rattei T., Engstrand L., Zink A. Helicobacter pylori in ancient human remains. World J. Gastroenterol., 2019, vol. 25, no. 42, pp. 6289–6298. doi: 10.3748/wjg.v25.i42.6289
  19. Marshall B.J., Warren J.R. Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet, 1984, vol. 1, no. 8390, pp. 1311–1315. doi: 10.1016/s0140-6736(84)91816-6
  20. McNeill W.H. Plagues and peoples. New York: Anchor Books, 1976. 365 p.
  21. Mégraud F., Lehours P., Vale F.F. The history of Helicobacter pylori: from phylogeography to paleomicrobiology. Clin. Microbiol. Infect., 2016, vol. 22, no. 11, pp. 922–927. doi: 10.1016/j.cmi.2016.07.013
  22. Moodley Y. Helicobacter pylori: genetics, recombination, population structure, and human migrations. Helicobacter pylori Research. J., 2016, pp. 3–27. doi: 10.1007/978-4-431-55936-8_1
  23. Moodley Y., Brunelli A., Ghirotto S., Klyubin A., Maady A.S., Tyne W., Muñoz-Ramirez Z.Y., Zhou Z., Manica A., Linz B., Achtman M. Helicobacter pylori’s historical journey through Siberia and the Americas. Proc. Natl Acad. Sci. USA, 2021, vol. 118, no. 25: e2015523118. doi: 10.1073/pnas.2015523118
  24. Moodley Y., Linz B. Helicobacter pylori sequences reflect past human migrations. Genome Dyn., 2009, no. 6, pp. 62–74. doi: 10.1159/000235763
  25. Moodley Y., Linz B., Bond R.P., Nieuwoudt M., Soodyall H., Schlebusch C.M., Bernhöft S., Hale J., Suerbaum S., Mugisha L., van der Merwe S.W., Achtman M. Age of the association between Helicobacter pylori and man. PLoS Pathog., 2012, vol. 8, no. 5: e1002693. doi: 10.1371/journal.ppat.1002693
  26. Muñoz-Ramírez Z.Y., Mendez-Tenorio A., Kato I., Bravo M.M., Rizzato C., Thorell K., Torres R., Aviles-Jimenez F., Camorlinga M., Canzian F., Torres J. Whole genome sequence and phylogenetic analysis show helicobacter pylori strains from latin america have followed a unique evolution pathway. Front. Cell. Infect. Microbiol., 2017, no. 7: 50. doi: 10.3389/fcimb.2017.00050
  27. Muñoz-Ramirez Z.Y., Pascoe B., Mendez-Tenorio A., Mourkas E., Sandoval-Motta S., Perez-Perez G., Morgan D.R., Dominguez R.L., Ortiz-Princz D., Cavazza M.E., Rocha G., Queiroz D.M.M., Catalano M., Palma G.Z., Goldman C.G., Venegas A., Alarcon T., Oleastro M., Vale F.F., Goodman K.J., Torres R.C., Berthenet E., Hitchings M.D., Blaser M.J., Sheppard S.K., Thorell K., Torres J. A 500-year tale of co-evolution, adaptation, and virulence: Helicobacter pylori in the Americas. ISME J., 2021, vol. 15, no. 1, pp. 78–92. doi: 10.1038/s41396-020-00758-0
  28. Nell S., Eibach D., Montano V., Maady A., Nkwescheu A., Siri J., Elamin W.F., Falush D., Linz B., Achtman M., Moodley Y., Suerbaum S. Recent acquisition of Helicobacter pylori by Baka pygmies. PLoS Genet., 2013, vol. 9, no. 9: e1003775. doi: 10.1371/journal.pgen.1003775
  29. Oleastro M., Rocha R., Vale F.F. Population genetic structure of Helicobacter pylori strains from portuguese-speaking countries. Helicobacter, 2017, vol. 22, no. 4. doi: 10.1111/hel.12382
  30. Pakendorf B., Bostoen K., de Filippo C. Molecular perspectives on the Bantu expansion: a synthesis. Lang Dyn. Chang., 2011, no. 1, pp. 50–88. doi: 10.1163/221058211X570349
  31. Pugach I., Matveev R., Spitsyn V., Makarov S., Novgorodov I., Osakovsky V., Stoneking M., Pakendorf B. The complex admixture history and recent southern origins of siberian populations. Mol. Biol. Evol., 2016, vol. 33, no. 7, pp. 1777–1195. doi: 10.1093/molbev/msw055
  32. Reshetnyak V.I., Burnistrov A.I., Maev I.V. Helicobacter pylori: commensals, symbiont or pathogens? World J. Gastroenterol., 2021, vol. 27, no. 7, pp. 545–560. doi: 10.3748/wjg.v27.i7.545
  33. Subsomwong P., Miftahussurur M., Vilaichone R.K., Ratanachu-Ek T., Suzuki R., Akada J., Uchida T., Mahachai V., Yamaoka Y. Helicobacter pylori virulence genes of minor ethnic groups in North Thailand. Gut Pathog., 2017, vol. 9, no. 56. doi: 10.1186/s13099-017-0205-x
  34. Suerbaum S., Achtman M. Helicobacter pylori: recombination, population structure and human migrations. Int. J. Med. Microbiol., 2004, no. 294, pp. 133–139. doi: 10.1016/j.ijmm.2004.06.014
  35. Tay C.Y., Mitchell H., Dong Q., Goh K.L., Dawes I.W., Lan R. Population structure of Helicobacter pylori among ethnic groups in Malaysia: recent acquisition of the bacterium by the Malay population. BMC Microbiol., 2009, vol. 9, no. 126, pp. 1–13. doi: 10.1186/1471-2180-9-126
  36. Thorell K., Yahara K., Berthenet E., Lawson D.J., Mikhail J., Kato I., Mendez A., Rizzato C., Bravo M.M., Suzuki R., Yamaoka Y., Torres J., Sheppard S.K., Falush D. Rapid evolution of distinct Helicobacter pylori subpopulations in the Americas. PLoS Genet., 2017, vol. 13, no. 2: e1006546. doi: 10.1371/journal.pgen.1006546
  37. Vale F.F., Vadivelu J., Oleastro M., Breurec S., Engstrand L., Perets T.T., Mégraud F., Lehours P. Dormant phages of Helicobacter pylori reveal distinct populations in Europe. Sci. Rep., 2015, vol. 5: 14333. doi: 10.1038/srep14333
  38. Waskito L.A., Yamaoka Y. The story of Helicobacter pylori: depicting human migrations from the phylogeography. Adv. Exp. Med. Biol., 2019, no. 1149, pp. 1–16. doi: 10.1007/5584_2019_356
  39. Yamaoka Y. Helicobacter pylori typing as a tool for tracking human migration. Clin. Microbiol. Infect., 2009, vol. 15, no. 9, pp. 829–834. doi: 10.1111/j.1469-0691.2009.02967.x
  40. Yunusbayev B., Metspalu M., Metspalu E., Valeev A., Litvinov S., Valiev R., Akhmetova V., Balanovska E., Balanovsky O., Turdikulova S., Dalimova D., Nymadawa P., Bahmanimehr A., Sahakyan H., Tambets K., Fedorova S., Barashkov N., Khidiyatova I., Mihailov E., Khusainova R., Damba L., Derenko M., Malyarchuk B., Osipova L., Voevoda M., Yepiskoposyan L., Kivisild T., Khusnutdinova E., Villems R. The genetic legacy of the expansion of Turkic-speaking nomads across Eurasia. PLoS Genet., 2015, vol. 11, no. 4: e1005068. doi: 10.1371/journal.pgen.1005068

Supplementary files

Supplementary Files
Action
1. JATS XML
2. Figure 1. Structure of the global H. pylori population

Download (117KB)

Copyright (c) 2022 Starkova D.A., Svarval A.V.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies