Abstract
Helicobacter pylori is a spiral-shaped Gram-negative bacterium, which has infected more than half of the human population. Besides its colonisation capability, the genetic diversity of H. pylori is exceptionally well structured and belongs to several distinct genetic populations, depicting various prehistorical human migration events. The evolutionary relationship of H. pylori with its host had been started at least ~100,000 years ago. In addition, the discovery of the ancient H. pylori genome from a European Copper Age glacier mummy, “The Iceman”, gave the idea that the second out of Africa migration resulted in the recombinant population of hpEurope at least about 5300 years ago. The advancement of next-generation genome sequencing discovered the prophage of H. pylori and could discriminate the big population of hpEurope into two different subpopulations. In addition, the implementation of the chromopainter/fineSTRUCTURE algorithm to the whole genome analysis of H. pylori provides a finer resolution population genetics of H. pylori; therefore it could also depict the recent migrations within the past 500 years after colonial expansion. This discovery shows that the genetic recombination of H. pylori strains is far more dynamic compared to its human host, but still maintains the similarity to its host, suggesting that H. pylori is a handy tool to reconstruct the human migration both in the past and the recent.
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References
Achtman M, Azuma T, Berg DE, Ito Y, Morelli G, Pan ZJ, Suerbaum S, Thompson SA, van der Ende A, van Doorn LJ (1999) Recombination and clonal groupings within Helicobacter pylori from different geographical regions. Mol Microbiol 32(3):459–470
Aftab H, Miftahussurur M, Subsomwong P, Ahmed F, Khan AKA, Matsumoto T, Suzuki R, Yamaoka Y (2017) Two populations of less-virulent Helicobacter pylori genotypes in Bangladesh. PLoS One 12(8):e0182947. https://doi.org/10.1371/journal.pone.0182947
Allen J, O’Connell J (2014) Both half right: updating the evidence for dating first human arrivals in Sahul. Aust Archaeol 79(1):86–108. https://doi.org/10.1080/03122417.2014.11682025
Backert S, Selbach M (2008) Role of type IV secretion in Helicobacter pylori pathogenesis. Cell Microbiol 10(8):1573–1581. https://doi.org/10.1111/j.1462-5822.2008.01156.x
Backert S, Tegtmeyer N, Selbach M (2010) The versatility of Helicobacter pylori CagA effector protein functions: the master key hypothesis. Helicobacter 15(3):163–176. https://doi.org/10.1111/j.1523-5378.2010.00759.x
Backert S, Tegtmeyer N, Fischer W (2015) Composition, structure and function of the Helicobacter pylori cag pathogenicity island encoded type IV secretion system. Future Microbiol 10(6):955–965. https://doi.org/10.2217/fmb.15.32
Bae CJ, Douka K, Petraglia MD (2017) On the origin of modern humans: Asian perspectives. Science 358(6368):eaai9067. https://doi.org/10.1126/science.aai9067
Björkholm B, Sjölund M, Falk PG, Berg OG, Engstrand L, Andersson DI (2001) Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori. Proc Natl Acad Sci 98(25):14607–14612
Breurec S, Guillard B, Hem S, Brisse S, Dieye FB, Huerre M, Oung C, Raymond J, Tan TS, Thiberge JM, Vong S, Monchy D, Linz B (2011a) Evolutionary history of Helicobacter pylori sequences reflect past human migrations in Southeast Asia. PLoS One 6(7):e22058. https://doi.org/10.1371/journal.pone.0022058
Breurec S, Guillard B, Hem S, Papadakos KS, Brisse S, Huerre M, Monchy D, Oung C, Sgouras DN, Tan TS, Thiberge JM, Vong S, Raymond J, Linz B (2011b) Expansion of European vacA and cagA alleles to East-Asian Helicobacter pylori strains in Cambodia. Infect Genet Evol 11(8):1899–1905. https://doi.org/10.1016/j.meegid.2011.08.007
Cavalli-Sforza LL, Menozzi P, Piazza A (1994) The history and geography of human genes. Princeton University Press, Princeton
Chomvarin C, Phusri K, Sawadpanich K, Mairiang P, Namwat W, Wongkham C, Hahnvajanawong C (2012) Prevalence of cagA EPIYA motifs in Helicobacter pylori among dyspeptic patients in northeast Thailand. Southeast Asian J Trop Med Public Health 43(1):105–115
Correa P, Piazuelo MB (2012) Evolutionary history of the Helicobacter pylori genome: implications for gastric carcinogenesis. Gut Liver 6(1):21–28. https://doi.org/10.5009/gnl.2012.6.1.21
Dominguez-Bello MG, Perez ME, Bortolini MC, Salzano FM, Pericchi LR, Zambrano-Guzman O, Linz B (2008) Amerindian Helicobacter pylori strains go extinct, as european strains expand their host range. PLoS One 3(10):e3307. https://doi.org/10.1371/journal.pone.0003307
Falush D, Kraft C, Taylor NS, Correa P, Fox JG, Achtman M, Suerbaum S (2001) Recombination and mutation during long-term gastric colonization by Helicobacter pylori: estimates of clock rates, recombination size, and minimal age. Proc Natl Acad Sci U S A 98(26):15056–15061. https://doi.org/10.1073/pnas.251396098
Falush D, Stephens M, Pritchard JK (2003a) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164(4):1567–1587
Falush D, Wirth T, Linz B, Pritchard JK, Stephens M, Kidd M, Blaser MJ, Graham DY, Vacher S, Perez-Perez GI, Yamaoka Y, Megraud F, Otto K, Reichard U, Katzowitsch E, Wang X, Achtman M, Suerbaum S (2003b) Traces of human migrations in Helicobacter pylori populations. Science 299(5612):1582–1585. https://doi.org/10.1126/science.1080857
Fischer W, Windhager L, Rohrer S, Zeiller M, Karnholz A, Hoffmann R, Zimmer R, Haas R (2010) Strain-specific genes of Helicobacter pylori: genome evolution driven by a novel type IV secretion system and genomic island transfer. Nucleic Acids Res 38(18):6089–6101. https://doi.org/10.1093/nar/gkq378
Furuta Y, Yahara K, Hatakeyama M, Kobayashi I (2011) Evolution of cagA oncogene of Helicobacter pylori through recombination. PLoS One 6(8):e23499. https://doi.org/10.1371/journal.pone.0023499
Gillespie R (2002) Dating the first Australians. Radiocarbon 44(2):455–472
Gressmann H, Linz B, Ghai R, Pleissner KP, Schlapbach R, Yamaoka Y, Kraft C, Suerbaum S, Meyer TF, Achtman M (2005) Gain and loss of multiple genes during the evolution of Helicobacter pylori. PLoS Genet 1(4):e43. https://doi.org/10.1371/journal.pgen.0010043
Honarmand-Jahromy S, Siavoshi F, Malekzadeh R, Sattari TN, Latifi-Navid S (2015) Multiple repeats of Helicobacter pylori CagA EPIYA-C phosphorylation sites predict risk of gastric ulcer in Iran. Microb Pathog 89:87–92. https://doi.org/10.1016/j.micpath.2015.09.005
Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, Malfertheiner P, Graham DY, Wong VWS, Wu JCY, Chan FKL, Sung JJY, Kaplan GG, Ng SC (2017) Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology 153(2):420–429. https://doi.org/10.1053/j.gastro.2017.04.022
Hudjashov G, Kivisild T, Underhill PA, Endicott P, Sanchez JJ, Lin AA, Shen P, Oefner P, Renfrew C, Villems R, Forster P (2007) Revealing the prehistoric settlement of Australia by Y chromosome and mtDNA analysis. Proc Natl Acad Sci U S A 104(21):8726–8730. https://doi.org/10.1073/pnas.0702928104
Kivi M, Tindberg Y, Sorberg M, Casswall TH, Befrits R, Hellstrom PM, Bengtsson C, Engstrand L, Granstrom M (2003) Concordance of Helicobacter pylori strains within families. J Clin Microbiol 41(12):5604–5608
Kocazeybek BS, Caliskan R, Erdamar Cetin S, Ergin S, Kuskucu M, Kepil N, Oyku Dinc H, Ziya Erzin Y, Saribas S, Bahar Tokman H, Kalayci F, Akgul O, Yuksel P, Karakullukcu A, Ziver T, Sirekbasan S, Caglar E, Bal K (2015) Patterns of EPIYA motifs among cagA-positive Helicobacter pylori strains: a case-control study in a Turkish population with Eurasian geographical features. J Med Microbiol 64(10):1117–1123. https://doi.org/10.1099/jmm.0.000141
Lawson DJ, Hellenthal G, Myers S, Falush D (2012) Inference of population structure using dense haplotype data. PLoS Genet 8(1):e1002453. https://doi.org/10.1371/journal.pgen.1002453
Li WH, Sadler LA (1991) Low nucleotide diversity in man. Genetics 129(2):513–523
Linz B, Balloux F, Moodley Y, Manica A, Liu H, Roumagnac P, Falush D, Stamer C, Prugnolle F, van der Merwe SW, Yamaoka Y, Graham DY, Perez-Trallero E, Wadstrom T, Suerbaum S, Achtman M (2007) An African origin for the intimate association between humans and Helicobacter pylori. Nature 445(7130):915–918. https://doi.org/10.1038/nature05562
Linz B, Vololonantenainab CR, Seck A, Carod JF, Dia D, Garin B, Ramanampamonjy RM, Thiberge JM, Raymond J, Breurec S (2014) Population genetic structure and isolation by distance of Helicobacter pylori in Senegal and Madagascar. PLoS One 9(1):e87355. https://doi.org/10.1371/journal.pone.0087355
Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, Zhang Q, Zhou J, Zurth K, Caugant DA, Feavers IM, Achtman M, Spratt BG (1998) Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 95(6):3140–3145
Maixner F, Krause-Kyora B, Turaev D, Herbig A, Hoopmann MR, Hallows JL, Kusebauch U, Vigl EE, Malfertheiner P, Megraud F, O’Sullivan N, Cipollini G, Coia V, Samadelli M, Engstrand L, Linz B, Moritz RL, Grimm R, Krause J, Nebel A, Moodley Y, Rattei T, Zink A (2016) The 5300-year-old Helicobacter pylori genome of the Iceman. Science 351(6269):162–165. https://doi.org/10.1126/science.aad2545
Matsunari O, Miftahussurur M, Shiota S, Suzuki R, Vilaichone RK, Uchida T, Ratanachu-ek T, Tshering L, Mahachai V, Yamaoka Y (2016) Rare Helicobacter pylori virulence genotypes in Bhutan. Sci Rep 6:22584. https://doi.org/10.1038/srep22584
Miftahussurur M, Sharma RP, Shrestha PK, Suzuki R, Uchida T, Yamaoka Y (2015a) Molecular epidemiology of Helicobacter pylori infection in Nepal: specific ancestor root. PLoS One 10(7):e0134216. https://doi.org/10.1371/journal.pone.0134216
Miftahussurur M, Shiota S, Suzuki R, Matsuda M, Uchida T, Kido Y, Kawamoto F, Maimunah U, Adi P, Rezkitha Y, Nasronudin NI, Yamaoka Y (2015b) Identification of Helicobacter pylori infection in symptomatic patients in Surabaya, Indonesia, using five diagnostic tests. Epidemiol Infect 143(5):986–996. https://doi.org/10.1017/S095026881400154X
Miftahussurur M, Syam AF, Makmun D, Nusi IA, Zein LH, Zulkhairi AF, Uswan WB, Simanjuntak D, Uchida T, Adi P, Utari AP, Rezkitha YA, Subsomwong P, Nasronudin YY (2015c) Helicobacter pylori virulence genes in the five largest islands of Indonesia. Gut Pathogens 7:26. https://doi.org/10.1186/s13099-015-0072-2
Montano V, Didelot X, Foll M, Linz B, Reinhardt R, Suerbaum S, Moodley Y, Jensen JD (2015) Worldwide population structure, long-term demography, and local adaptation of Helicobacter pylori. Genetics 200(3):947–963. https://doi.org/10.1534/genetics.115.176404
Moodley Y (2016) Helicobacter pylori: genetics, recombination, population structure, and human migrations. In: Backert S, Yamaoka Y (eds) Helicobacter pylori research: from bench to bedside. Springer, Tokyo, pp 3–27. https://doi.org/10.1007/978-4-431-55936-8_1
Moodley Y, Linz B, Yamaoka Y, Windsor HM, Breurec S, Wu JY, Maady A, Bernhoft S, Thiberge JM, Phuanukoonnon S, Jobb G, Siba P, Graham DY, Marshall BJ, Achtman M (2009) The peopling of the Pacific from a bacterial perspective. Science 323(5913):527–530. https://doi.org/10.1126/science.1166083
Moodley Y, Linz B, Bond RP, Nieuwoudt M, Soodyall H, Schlebusch CM, Bernhoft S, Hale J, Suerbaum S, Mugisha L, van der Merwe SW, Achtman M (2012) Age of the association between Helicobacter pylori and man. PLoS Pathog 8(5):e1002693. https://doi.org/10.1371/journal.ppat.1002693
Munoz-Ramirez ZY, Mendez-Tenorio A, Kato I, Bravo MM, Rizzato C, Thorell K, Torres R, Aviles-Jimenez F, Camorlinga M, Canzian F, Torres J (2017) Whole genome sequence and phylogenetic analysis show Helicobacter pylori strains from Latin America have followed a unique evolution pathway. Front Cell Infect Microbiol 7:50. https://doi.org/10.3389/fcimb.2017.00050
Naumann M, Sokolova O, Tegtmeyer N, Backert S (2017) Helicobacter pylori: a paradigm pathogen for subverting host cell signal transmission. Trends Microbiol 25(4):316–328. https://doi.org/10.1016/j.tim.2016.12.004
Nell S, Eibach D, Montano V, Maady A, Nkwescheu A, Siri J, Elamin WF, Falush D, Linz B, Achtman M, Moodley Y, Suerbaum S (2013) Recent acquisition of Helicobacter pylori by Baka pygmies. PLoS Genet 9(9):e1003775. https://doi.org/10.1371/journal.pgen.1003775
Olbermann P, Josenhans C, Moodley Y, Uhr M, Stamer C, Vauterin M, Suerbaum S, Achtman M, Linz B (2010) A global overview of the genetic and functional diversity in the Helicobacter pylori cag pathogenicity island. PLoS Genet 6(8):e1001069. https://doi.org/10.1371/journal.pgen.1001069
Oleastro M, Rocha R, Vale FF (2017) Population genetic structure of Helicobacter pylori strains from Portuguese-speaking countries. Helicobacter 22(4). https://doi.org/10.1111/hel.12382
Pope KO, Terrell JE (2008) Environmental setting of human migrations in the circum-Pacific region. J Biogeogr 35(1):1–21
Posselt G, Backert S, Wessler S (2013) The functional interplay of Helicobacter pylori factors with gastric epithelial cells induces a multi-step process in pathogenesis. Cell Commun Signal 11:77. https://doi.org/10.1186/1478-811X-11-77
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155(2):945–959
Rahim AA, Lee YY, Majid NA, Choo KE, Raj SM, Derakhshan MH, Graham DY (2010) Helicobacter pylori infection among Aborigines (the Orang Asli) in the northeastern region of Peninsular Malaysia. Am J Trop Med Hyg 83(5):1119–1122. https://doi.org/10.4269/ajtmh.2010.10-0226
Schmidt HM, Goh KL, Fock KM, Hilmi I, Dhamodaran S, Forman D, Mitchell H (2009) Distinct cagA EPIYA motifs are associated with ethnic diversity in Malaysia and Singapore. Helicobacter 14(4):256–263. https://doi.org/10.1111/j.1523-5378.2009.00684.x
Subsomwong P, Miftahussurur M, Vilaichone RK, Ratanachu-Ek T, Suzuki R, Akada J, Uchida T, Mahachai V, Yamaoka Y (2017) Helicobacter pylori virulence genes of minor ethnic groups in North Thailand. Gut Pathogens 9:56. https://doi.org/10.1186/s13099-017-0205-x
Suerbaum S, Smith JM, Bapumia K, Morelli G, Smith NH, Kunstmann E, Dyrek I, Achtman M (1998) Free recombination within Helicobacter pylori. Proc Natl Acad Sci 95(21):12619–12624
Syam AF, Miftahussurur M, Makmun D, Nusi IA, Zain LH, Zulkhairi AF, Uswan WB, Simanjuntak D, Uchida T, Adi P, Utari AP, Rezkitha YA, Subsomwong P, Nasronudin SR, Yamaoka Y (2015) Risk factors and prevalence of Helicobacter pylori in five largest Islands of Indonesia: a preliminary study. PLoS One 10(11):e0140186. https://doi.org/10.1371/journal.pone.0140186
Tay CY, Mitchell H, Dong Q, Goh KL, Dawes IW, Lan R (2009) Population structure of Helicobacter pylori among ethnic groups in Malaysia: recent acquisition of the bacterium by the Malay population. BMC Microbiol 9:126. https://doi.org/10.1186/1471-2180-9-126
Thorell K, Yahara K, Berthenet E, Lawson DJ, Mikhail J, Kato I, Mendez A, Rizzato C, Bravo MM, Suzuki R, Yamaoka Y, Torres J, Sheppard SK, Falush D (2017) Rapid evolution of distinct Helicobacter pylori subpopulations in the Americas. PLoS Genet 13(2):e1006546. https://doi.org/10.1371/journal.pgen.1006546
Uchida T, Nguyen LT, Takayama A, Okimoto T, Kodama M, Murakami K, Matsuhisa T, Trinh TD, Ta L, Ho DQ, Hoang HH, Kishida T, Fujioka T, Moriyama M, Yamaoka Y (2009) Analysis of virulence factors of Helicobacter pylori isolated from a Vietnamese population. BMC Microbiol 9:175. https://doi.org/10.1186/1471-2180-9-175
Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, Taniyama K, Sasaki N, Schlemper RJ (2001) Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 345(11):784–789. https://doi.org/10.1056/NEJMoa001999
Vale FF, Vadivelu J, Oleastro M, Breurec S, Engstrand L, Perets TT, Megraud F, Lehours P (2015) Dormant phages of Helicobacter pylori reveal distinct populations in Europe. Sci Rep 5:14333. https://doi.org/10.1038/srep14333
Vale FF, Nunes A, Oleastro M, Gomes JP, Sampaio DA, Rocha R, Vitor JM, Engstrand L, Pascoe B, Berthenet E, Sheppard SK, Hitchings MD, Megraud F, Vadivelu J, Lehours P (2017) Genomic structure and insertion sites of Helicobacter pylori prophages from various geographical origins. Sci Rep 7:42471. https://doi.org/10.1038/srep42471
Wirth T, Wang X, Linz B, Novick RP, Lum JK, Blaser M, Morelli G, Falush D, Achtman M (2004) Distinguishing human ethnic groups by means of sequences from Helicobacter pylori: lessons from Ladakh. Proc Natl Acad Sci U S A 101(14):4746–4751. https://doi.org/10.1073/pnas.0306629101
Yahara K, Furuta Y, Oshima K, Yoshida M, Azuma T, Hattori M, Uchiyama I, Kobayashi I (2013) Chromosome painting in silico in a bacterial species reveals fine population structure. Mol Biol Evol 30(6):1454–1464. https://doi.org/10.1093/molbev/mst055
Yamaoka Y (2010) Mechanisms of disease: Helicobacter pylori virulence factors. Nat Rev Gastroenterol Hepatol 7(11):629–641. https://doi.org/10.1038/nrgastro.2010.154
Yamaoka Y, Kodama T, Kashima K, Graham DY, Sepulveda AR (1998) Variants of the 3′ region of the cagA gene in Helicobacter pylori isolates from patients with different H. pylori-associated diseases. J Clin Microbiol 36(8):2258–2263
Yamaoka Y, El-Zimaity HM, Gutierrez O, Figura N, Kim JG, Kodama T, Kashima K, Graham DY (1999) Relationship between the cagA 3′ repeat region of Helicobacter pylori, gastric histology, and susceptibility to low pH. Gastroenterology 117(2):342–349
Yamaoka Y, Osato MS, Sepulveda AR, Gutierrez O, Figura N, Kim JG, Kodama T, Kashima K, Graham DY (2000) Molecular epidemiology of Helicobacter pylori: separation of H. pylori from East Asian and non-Asian countries. Epidemiol Infect 124(1):91–96
Yamaoka Y, Orito E, Mizokami M, Gutierrez O, Saitou N, Kodama T, Osato MS, Kim JG, Ramirez FC, Mahachai V, Graham DY (2002) Helicobacter pylori in North and South America before Columbus. FEBS Lett 517(1–3):180–184
Zhang XS, Tegtmeyer N, Traube L, Jindal S, Perez-Perez G, Sticht H, Backert S, Blaser MJ (2015) A specific A/T polymorphism in Western tyrosine phosphorylation B-motifs regulates Helicobacter pylori CagA epithelial cell interaction. PLoS Pathog 11:e1004621. https://doi.org/10.1371/journal.ppat.1004621
Acknowledgements
This work was supported in part by grants from the National Institutes of Health (DK62813) and the Grants-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science, and Technology (MEXT) of Japan (221S0002, 16H06279, 15H02657 and 16H05191) (YY). It was also supported by the Japan Society for the Promotion of Science (JSPS) Institutional Program for Core-to-Core Program; B. Africa-Asia Science Platform (YY). LAW is a doctoral students supported by the Japanese Government (The Ministry of Education, Culture, Sports, Science and Technology [MEXT]) Scholarship Program for 2015.
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Waskito, L.A., Yamaoka, Y. (2019). The Story of Helicobacter pylori: Depicting Human Migrations from the Phylogeography. In: Kamiya, S., Backert, S. (eds) Helicobacter pylori in Human Diseases. Advances in Experimental Medicine and Biology(), vol 1149. Springer, Cham. https://doi.org/10.1007/5584_2019_356
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