A 500-year tale of co-evolution, adaptation, and virulence: Helicobacter pylori in the Americas

Zilia Y Muñoz-Ramirez; Ben Pascoe; Alfonso Mendez-Tenorio; Evangelos Mourkas; Santiago Sandoval-Motta; Guillermo Perez-Perez; Douglas R Morgan; Ricardo Leonel Dominguez; Diana Ortiz-Princz; Maria Eugenia Cavazza; Gifone Rocha; Dulcienne M M Queiroz; Mariana Catalano; Gerardo Zerbetto De Palma; Cinthia G Goldman; Alejandro Venegas; Teresa Alarcon; Monica Oleastro; Filipa F Vale; Karen J Goodman; Roberto C Torres; Elvire Berthenet; Matthew D Hitchings; Martin J Blaser; Samuel K Sheppard; Kaisa Thorell; Javier Torres

doi:10.1038/s41396-020-00758-0

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A 500-year tale of co-evolution, adaptation, and virulence: Helicobacter pylori in the Americas

Journal article

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A 500-year tale of co-evolution, adaptation, and virulence: Helicobacter pylori in the Americas

Zilia Y Muñoz-Ramirez, Ben Pascoe, Alfonso Mendez-Tenorio, Evangelos Mourkas, Santiago Sandoval-Motta, Guillermo Perez-Perez, Douglas R Morgan, Ricardo Leonel Dominguez, Diana Ortiz-Princz, Maria Eugenia Cavazza, …

The ISME Journal, Vol.15(1), pp.78-92

01/2021

DOI: https://doi.org/10.1038/s41396-020-00758-0

PMID: 32879462

Abstract

Americas

Europe

Genetic Variation

Genome, Bacterial

Helicobacter Infections

Helicobacter pylori - genetics

Humans

United States

Virulence - genetics

Helicobacter pylori is a common component of the human stomach microbiota, possibly dating back to the speciation of Homo sapiens. A history of pathogen evolution in allopatry has led to the development of genetically distinct H. pylori subpopulations, associated with different human populations, and more recent admixture among H. pylori subpopulations can provide information about human migrations. However, little is known about the degree to which some H. pylori genes are conserved in the face of admixture, potentially indicating host adaptation, or how virulence genes spread among different populations. We analyzed H. pylori genomes from 14 countries in the Americas, strains from the Iberian Peninsula, and public genomes from Europe, Africa, and Asia, to investigate how admixture varies across different regions and gene families. Whole-genome analyses of 723 H. pylori strains from around the world showed evidence of frequent admixture in the American strains with a complex mosaic of contributions from H. pylori populations originating in the Americas as well as other continents. Despite the complex admixture, distinctive genomic fingerprints were identified for each region, revealing novel American H. pylori subpopulations. A pan-genome Fst analysis showed that variation in virulence genes had the strongest fixation in America, compared with non-American populations, and that much of the variation constituted non-synonymous substitutions in functional domains. Network analyses suggest that these virulence genes have followed unique evolutionary paths in the American populations, spreading into different genetic backgrounds, potentially contributing to the high risk of gastric cancer in the region.

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Title: A 500-year tale of co-evolution, adaptation, and virulence: Helicobacter pylori in the Americas
Creators: Zilia Y Muñoz-Ramirez - Laboratorio de Bioinformática y Biotecnología Genómica, Escuela Nacional de Ciencias Biológicas, Unidad Profesional Lázaro Cárdenas, Instituto Politécnico Nacional, 11340, Mexico City, Mexico
Ben Pascoe - Department of Biology and Biochemistry, The Milner Centre for Evolution, University of Bath, Claverton Down, Bath, UK
Alfonso Mendez-Tenorio - Laboratorio de Bioinformática y Biotecnología Genómica, Escuela Nacional de Ciencias Biológicas, Unidad Profesional Lázaro Cárdenas, Instituto Politécnico Nacional, 11340, Mexico City, Mexico
Evangelos Mourkas - Department of Biology and Biochemistry, The Milner Centre for Evolution, University of Bath, Claverton Down, Bath, UK
Santiago Sandoval-Motta - Consejo Nacional de Ciencia y Tecnologia, Catedras CONACYT, Ciudad de México, México
Guillermo Perez-Perez - New York University Langone Medical Center, New York, NY, USA
Douglas R Morgan - Division of Gastroenterology, Hepatology, and Nutrition, Vanderbilt University, Nashville, TN, USA
Ricardo Leonel Dominguez - Western Honduras Gastric Cancer Prevention Initiative Hospital de Occidente Santa Rosa de Copan, Santa Rosa de Copan, Honduras
Diana Ortiz-Princz - Laboratorio de Microbiología Molecular, Servicio Instituto de Biomedicina MPPS-UCV, Caracas, Venezuela
Maria Eugenia Cavazza - Laboratorio de Microbiología Molecular, Servicio Instituto de Biomedicina MPPS-UCV, Caracas, Venezuela
Gifone Rocha - Faculdade de Medicina da UFMG, Belo Horizonte, Brazil
Dulcienne M M Queiroz - Faculdade de Medicina da UFMG, Belo Horizonte, Brazil
Mariana Catalano - Facultad de Medicina, Instituto de Microbiología y Parasitología Médica (IMPAM, UBA-CONICET), Universidad de Buenos Aires-Consejo Nacional de Investigaciones Científicas y Técnicas, Santa Rosa de Copan, Honduras
Gerardo Zerbetto De Palma - Instituto de Química y Fisicoquímica Biológicas "Prof. Alejandro C. Paladini", IQUIFIB UBA-CONICET, Santa Rosa de Copan, Honduras
Cinthia G Goldman - National Scientific and Technical Research Council (CONICET), C1425FQB, Buenos Aires, Argentina
Alejandro Venegas - Laboratorio de Patogénesis Microbiana, Centro de Investigación Biomédica, Universidad Diego Portales, Ejército, 141, Santiago, Chile
Teresa Alarcon - Department of Microbiology, Hospital Universitario La Princesa, Instituto de Investigación Sanitaria Princesa, Madrid, Spain
Monica Oleastro - Host-Pathogen Interactions Unit, Faculty of Pharmacy, Research Institute for Medicines (iMed-ULisboa), Universidade de Lisboa, Lisboa, Portugal
Filipa F Vale - Host-Pathogen Interactions Unit, Faculty of Pharmacy, Research Institute for Medicines (iMed-ULisboa), Universidade de Lisboa, Lisboa, Portugal
Karen J Goodman - Division of Gastroenterology, Centre of Excellence for Gastrointestinal Inflammation & Immunity Research, University of Alberta, Edmonton, AB, Canada
Roberto C Torres - Unidad de Investigacion en Enfermedades Infecciosas, UMAE Pediatria, Instituto Mexicano del Seguro Social, Ciudad de México, Mexico
Elvire Berthenet - Swansea University Medical School, Swansea University, Swansea, UK
Matthew D Hitchings - Swansea University Medical School, Swansea University, Swansea, UK
Martin J Blaser - Center for Advanced Biotechnology and Medicine, Rutgers University, New Brunswick, NJ, USA
Samuel K Sheppard - Department of Biology and Biochemistry, The Milner Centre for Evolution, University of Bath, Claverton Down, Bath, UK
Kaisa Thorell - Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet, Stockholm, Sweden. kaisa.thorell@gu.se
Javier Torres - Unidad de Investigacion en Enfermedades Infecciosas, UMAE Pediatria, Instituto Mexicano del Seguro Social, Ciudad de México, Mexico. uimeip@gmail.com
Publication Details: The ISME Journal, Vol.15(1), pp.78-92
Date published: 01/2021
Grant note: R01 CA190612 / NCI NIH HHS P30 CA068485 / NCI NIH HHS MR/L015080/1 / Medical Research Council K07 CA125588 / NCI NIH HHS P01 CA028842 / NCI NIH HHS
Academic Unit: Center for Advanced Biotechnology and Medicine
Language: English
Resource Type: Journal article
Identifiers: 991031665883704646