Identification of New Helicobacter pylori Subpopulations in Native Americans and Mestizos From Peru

Region-specific Helicobacter pylori subpopulations have been identified. It is proposed that the hspAmerind subpopulation is being displaced from the Americans by an hpEurope population following the conquest. Our study aimed to describe the genomes and methylomes of H. pylori isolates from distinct...

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Main Authors: Andrés Julián Gutiérrez-Escobar, Billie Velapatiño, Victor Borda, Charles S. Rabkin, Eduardo Tarazona-Santos, Lilia Cabrera, Jaime Cok, Catherine C. Hooper, Helena Jahuira-Arias, Phabiola Herrera, Mehwish Noureen, Difei Wang, Judith Romero-Gallo, Bao Tran, Richard M. Peek, Douglas E. Berg, Robert H. Gilman, M. Constanza Camargo
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-12-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2020.601839/full
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author Andrés Julián Gutiérrez-Escobar
Billie Velapatiño
Billie Velapatiño
Victor Borda
Charles S. Rabkin
Eduardo Tarazona-Santos
Eduardo Tarazona-Santos
Lilia Cabrera
Jaime Cok
Catherine C. Hooper
Helena Jahuira-Arias
Phabiola Herrera
Mehwish Noureen
Mehwish Noureen
Difei Wang
Judith Romero-Gallo
Bao Tran
Richard M. Peek
Douglas E. Berg
Robert H. Gilman
M. Constanza Camargo
author_facet Andrés Julián Gutiérrez-Escobar
Billie Velapatiño
Billie Velapatiño
Victor Borda
Charles S. Rabkin
Eduardo Tarazona-Santos
Eduardo Tarazona-Santos
Lilia Cabrera
Jaime Cok
Catherine C. Hooper
Helena Jahuira-Arias
Phabiola Herrera
Mehwish Noureen
Mehwish Noureen
Difei Wang
Judith Romero-Gallo
Bao Tran
Richard M. Peek
Douglas E. Berg
Robert H. Gilman
M. Constanza Camargo
author_sort Andrés Julián Gutiérrez-Escobar
collection DOAJ
description Region-specific Helicobacter pylori subpopulations have been identified. It is proposed that the hspAmerind subpopulation is being displaced from the Americans by an hpEurope population following the conquest. Our study aimed to describe the genomes and methylomes of H. pylori isolates from distinct Peruvian communities: 23 strains collected from three groups of Native Americans (Asháninkas [ASHA, n = 9], Shimaas [SHIM, n = 5] from Amazonas, and Punos from the Andean highlands [PUNO, n = 9]) and 9 modern mestizos from Lima (LIM). Closed genomes and DNA modification calls were obtained using SMRT/PacBio sequencing. We performed evolutionary analyses and evaluated genomic/epigenomic differences among strain groups. We also evaluated human genome-wide data from 74 individuals from the selected Native communities (including the 23 H. pylori strains donors) to compare host and bacterial backgrounds. There were varying degrees of hspAmerind ancestry in all strains, ranging from 7% in LIM to 99% in SHIM. We identified three H. pylori subpopulations corresponding to each of the Native groups and a novel hspEuropePeru which evolved in the modern mestizos. The divergence of the indigenous H. pylori strains recapitulated the genetic structure of Native Americans. Phylogenetic profiling showed that Orthogroups in the indigenous strains seem to have evolved differentially toward epigenomic regulation and chromosome maintenance, whereas OGs in the modern mestizo (LIM) seem to have evolved toward virulence and adherence. The prevalence of cagA+/vacA s1i1m1 genotype was similar across populations (p = 0.32): 89% in ASHA, 67% in PUNO, 56% in LIM and 40% in SHIM. Both cagA and vacA sequences showed that LIM strains were genetically differentiated (p < 0.001) as compared to indigenous strains. We identified 642 R-M systems with 39% of the associated genes located in the core genome. We found 692 methylation motifs, including 254 population-specific sequences not previously described. In Peru, hspAmerind is not extinct, with traces found even in a heavily admixed mestizo population. Notably, our study identified three new hspAmerind subpopulations, one per Native group; and a new subpopulation among mestizos that we named hspEuropePeru. This subpopulation seems to have more virulence-related elements than hspAmerind. Purifying selection driven by variable host immune response may have shaped the evolution of Peruvian subpopulations, potentially impacting disease outcomes.
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spelling doaj.art-b6b76ee877c3446495f39bc0a03974102022-12-21T22:21:04ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-12-011110.3389/fmicb.2020.601839601839Identification of New Helicobacter pylori Subpopulations in Native Americans and Mestizos From PeruAndrés Julián Gutiérrez-Escobar0Billie Velapatiño1Billie Velapatiño2Victor Borda3Charles S. Rabkin4Eduardo Tarazona-Santos5Eduardo Tarazona-Santos6Lilia Cabrera7Jaime Cok8Catherine C. Hooper9Helena Jahuira-Arias10Phabiola Herrera11Mehwish Noureen12Mehwish Noureen13Difei Wang14Judith Romero-Gallo15Bao Tran16Richard M. Peek17Douglas E. Berg18Robert H. Gilman19M. Constanza Camargo20Division of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, United StatesDepartment of Pathology and Laboratory Medicine, Faculty of Medicine, The University of British Columbia, Vancouver, BC, CanadaUniversidad Peruana Cayetano Heredia, Lima, PeruLaboratório de Bioinformática, Laboratório Nacional de Computação Científica (LNCC/MCTIC), Petrópolis, BrazilDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, United StatesUniversidad Peruana Cayetano Heredia, Lima, PeruDepartment of Genetics, Ecology and Evolution, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte, BrazilAsociación Benéfica PRISMA, Lima, PeruUniversidad Peruana Cayetano Heredia, Lima, PeruUniversidad Peruana Cayetano Heredia, Lima, PeruUniversidad Peruana Cayetano Heredia, Lima, PeruUniversidad Peruana Cayetano Heredia, Lima, PeruNational Institute of Genetics, Mishima, JapanDepartment of Genetics, Graduate School of Life Sciences, The Graduate University for Advanced Studies (SOKENDAI), Mishima, JapanDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, United StatesDivision of Gastroenterology, Hepatology and Nutrition, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, United States0Frederick National Laboratory for Cancer Research, National Cancer Institute, Frederick, MD, United StatesDivision of Gastroenterology, Hepatology and Nutrition, Department of Medicine, Vanderbilt University Medical Center, Nashville, TN, United States1Department of Molecular Microbiology, Washington University School of Medicine in St. Louis, St. Louis, MO, United States2Department of International Health, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MD, United StatesDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, United StatesRegion-specific Helicobacter pylori subpopulations have been identified. It is proposed that the hspAmerind subpopulation is being displaced from the Americans by an hpEurope population following the conquest. Our study aimed to describe the genomes and methylomes of H. pylori isolates from distinct Peruvian communities: 23 strains collected from three groups of Native Americans (Asháninkas [ASHA, n = 9], Shimaas [SHIM, n = 5] from Amazonas, and Punos from the Andean highlands [PUNO, n = 9]) and 9 modern mestizos from Lima (LIM). Closed genomes and DNA modification calls were obtained using SMRT/PacBio sequencing. We performed evolutionary analyses and evaluated genomic/epigenomic differences among strain groups. We also evaluated human genome-wide data from 74 individuals from the selected Native communities (including the 23 H. pylori strains donors) to compare host and bacterial backgrounds. There were varying degrees of hspAmerind ancestry in all strains, ranging from 7% in LIM to 99% in SHIM. We identified three H. pylori subpopulations corresponding to each of the Native groups and a novel hspEuropePeru which evolved in the modern mestizos. The divergence of the indigenous H. pylori strains recapitulated the genetic structure of Native Americans. Phylogenetic profiling showed that Orthogroups in the indigenous strains seem to have evolved differentially toward epigenomic regulation and chromosome maintenance, whereas OGs in the modern mestizo (LIM) seem to have evolved toward virulence and adherence. The prevalence of cagA+/vacA s1i1m1 genotype was similar across populations (p = 0.32): 89% in ASHA, 67% in PUNO, 56% in LIM and 40% in SHIM. Both cagA and vacA sequences showed that LIM strains were genetically differentiated (p < 0.001) as compared to indigenous strains. We identified 642 R-M systems with 39% of the associated genes located in the core genome. We found 692 methylation motifs, including 254 population-specific sequences not previously described. In Peru, hspAmerind is not extinct, with traces found even in a heavily admixed mestizo population. Notably, our study identified three new hspAmerind subpopulations, one per Native group; and a new subpopulation among mestizos that we named hspEuropePeru. This subpopulation seems to have more virulence-related elements than hspAmerind. Purifying selection driven by variable host immune response may have shaped the evolution of Peruvian subpopulations, potentially impacting disease outcomes.https://www.frontiersin.org/articles/10.3389/fmicb.2020.601839/fullAmerindiansancestryindigenoushspAmerindmestizoPeru
spellingShingle Andrés Julián Gutiérrez-Escobar
Billie Velapatiño
Billie Velapatiño
Victor Borda
Charles S. Rabkin
Eduardo Tarazona-Santos
Eduardo Tarazona-Santos
Lilia Cabrera
Jaime Cok
Catherine C. Hooper
Helena Jahuira-Arias
Phabiola Herrera
Mehwish Noureen
Mehwish Noureen
Difei Wang
Judith Romero-Gallo
Bao Tran
Richard M. Peek
Douglas E. Berg
Robert H. Gilman
M. Constanza Camargo
Identification of New Helicobacter pylori Subpopulations in Native Americans and Mestizos From Peru
Frontiers in Microbiology
Amerindians
ancestry
indigenous
hspAmerind
mestizo
Peru
title Identification of New Helicobacter pylori Subpopulations in Native Americans and Mestizos From Peru
title_full Identification of New Helicobacter pylori Subpopulations in Native Americans and Mestizos From Peru
title_fullStr Identification of New Helicobacter pylori Subpopulations in Native Americans and Mestizos From Peru
title_full_unstemmed Identification of New Helicobacter pylori Subpopulations in Native Americans and Mestizos From Peru
title_short Identification of New Helicobacter pylori Subpopulations in Native Americans and Mestizos From Peru
title_sort identification of new helicobacter pylori subpopulations in native americans and mestizos from peru
topic Amerindians
ancestry
indigenous
hspAmerind
mestizo
Peru
url https://www.frontiersin.org/articles/10.3389/fmicb.2020.601839/full
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