Evolutionary history and global spread of the Mycobacterium tuberculosis Beijing lineage

Matthias Merker, Camille Blin, Stefano Mona, Nicolas Duforet-Frebourg, Sophie Lecher, Eve Willery, Michael G.B. Blum, Sabine Rüsch-Gerdes, Igor Mokrousov, Eman Aleksic, Caroline Allix-Béguec, Annick Antierens, Ewa Augustynowicz-Kopeć, Marie Ballif, Francesca Barletta, Hans Peter Beck, Clifton E. Barry, Maryline Bonnet, Emanuele Borroni, Isolina Campos-HerreroDaniela Cirillo, Helen Cox, Suzanne Crowe, Valeriu Crudu, Roland Diel, Francis Drobniewski, Maryse Fauville-Dufaux, Sébastien Gagneux, Solomon Ghebremichael, Madeleine Hanekom, Sven Hoffner, Wei Wei Jiao, Stobdan Kalon, Thomas A. Kohl, Irina Kontsevaya, Troels Lillebæk, Shinji Maeda, Vladyslav Nikolayevskyy, Michael Rasmussen, Nalin Rastogi, Sofia Samper, Elisabeth Sanchez-Padilla, Branislava Savic, Isdore Chola Shamputa, Adong Shen, Li Hwei Sng, Petras Stakenas, Kadri Toit, Francis Varaine, Dragana Vukovic, Céline Wahl, Robin Warren, Philip Supply, Stefan Niemann*, Thierry Wirth

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

302 Citations (Scopus)

Abstract

Mycobacterium tuberculosis strains of the Beijing lineage are globally distributed and are associated with the massive spread of multidrug-resistant (MDR) tuberculosis in Eurasia. Here we reconstructed the biogeographical structure and evolutionary history of this lineage by genetic analysis of 4,987 isolates from 99 countries and whole-genome sequencing of 110 representative isolates. We show that this lineage initially originated in the Far East, from where it radiated worldwide in several waves. We detected successive increases in population size for this pathogen over the last 200 years, practically coinciding with the Industrial Revolution, the First World War and HIV epidemics. Two MDR clones of this lineage started to spread throughout central Asia and Russia concomitantly with the collapse of the public health system in the former Soviet Union. Mutations identified in genes putatively under positive selection and associated with virulence might have favored the expansion of the most successful branches of the lineage.

Original languageEnglish
Pages (from-to)242-249
Number of pages8
JournalNature Genetics
Volume47
Issue number3
DOIs
Publication statusPublished - Mar 2015

Bibliographical note

Funding Information:
We gratefully acknowledge L. Cowan and J. Posey (US Centers for Disease Control and Prevention) for providing us with significant amounts of genotyping data for M. tuberculosis Beijing isolates. We thank T. Ubben, I. Radzio, T. Struwe-Sonnenschein and J. Zallet (Research Center Borstel) for excellent technical assistance. We acknowledge J. Peh for her assistance and support in the study and I. Comas for statistical advice. Parts of this work have been supported by grants from the European Community's Seventh Framework Programme (FP7/2007-2013) under grant agreement 278864 in the framework of the European Union PathoNGenTrace project and grant agreement 223681 in the framework of the TB-PAN-NET project. We also thank Action Transversale du Mus?um National d'Histoire Naturelle 'Les Microorganismes, Acteurs Cl?s dans les Ecosyst?mes' for financial support. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Funding Information:
14Department of Microbiology, National Tuberculosis and Lung Diseases Research Institute, Warsaw, Poland. 15Institute of Social and Preventive Medicine, University of Bern, Bern, Switzerland. 16Instituto de Medicina Tropical Alexander von Humboldt, Molecular Epidemiology Unit–Tuberculosis, Universidad Peruana Cayetano Heredia, Lima, Peru. 17Department of Medical Parasitology and Infection Biology, Swiss Tropical and Public Health Institute, Basel, Switzerland. 18Tuberculosis Research Section, National Institute of Allergy and Infectious Diseases, US National Institutes of Health, Bethesda, Maryland, USA. 19Clinical Research Department, Epicentre, Paris, France. 20Emerging Bacterial Pathogens Unit, San Raffaele Scientific Institute, Milan, Italy. 21Department of Microbiology, Hospital Universitario de Gran Canaria Dr. Negrín, Las Palmas de Gran Canaria, Spain. 22Division of Medical Microbiology, University of Cape Town, Cape Town, South Africa. 23Department of Infectious Diseases, Alfred Hospital, Melbourne, Victoria, Australia. 24Central Clinical School, Monash University, Melbourne, Victoria, Australia. 25National Tuberculosis Reference Laboratory, Phthysiopneumology Institute, Chisinau, Republic of Moldova. 26Institute for Epidemiology, Schleswig-Holstein University Hospital, Kiel, Germany. 27Public Health England National Mycobacterial Reference Laboratory and Clinical Tuberculosis and Human Immunodeficiency Virus Group, Queen Mary’s School of Medicine and Dentistry, London, UK. 28Department of Infectious Diseases, Imperial College, London, UK. 29Tuberculosis and Mycobacteria, Scientific Institute of Public Health, Brussels, Belgium. 30Department of Microbiology, Public Health Agency of Sweden, Solna, Sweden. 31Department of Science and Technology/National Research Foundation, Centre of Excellence for Biomedical Tuberculosis Research/Medical Research Council, Centre for Tuberculosis Research, Division of Molecular Biology and Human Genetics, Faculty of Medicine and Health Sciences, Stellenbosch University, Cape Town, South Africa. 32Department of Diagnostics and Vaccinology, Swedish Institute for Communicable Disease Control, Solna, Sweden. 33Key Laboratory of Major Diseases in Children and National Key Discipline of Pediatrics (Capital Medical University), Ministry of Education, Beijing Pediatric Research Institute, Beijing Children’s Hospital, Capital Medical University, Beijing, China. 34US Agency for International Development Quality Health Care Project, Bishkek, Kyrgyzstan. 35Samara Oblast Tuberculosis Service, Samara, Russia. 36Statens Serum Institute, International Reference Laboratory of Mycobacteriology, Copenhagen, Denmark. 37Research Institute of Tuberculosis, Japan Anti-Tuberculosis Association, Tokyo, Japan. 38World Health Organization Supranational Tuberculosis Reference Laboratory, Institut Pasteur de la Guadeloupe, Abymes, France. 39Instituto de Investigación Sanitaria Aragón, Hospital Universitario Miguel Servet, Zaragoza, Spain. 40Institute of Microbiology and Immunology, Faculty of Medicine, University of Belgrade, Belgrade, Serbia. 41Central Tuberculosis Laboratory, Department of Pathology, Singapore General Hospital, Singapore. 42Department of Immunology and Cell Biology, Institute of Biotechnology, Vilnius University, Vilnius, Lithuania. 43Tartu University Hospital United Laboratories, Mycobacteriology, Tartu, Estonia. 44Medical Department, Médecins sans Frontières, Paris, France. 45German Center for Infection Research, Borstel Site, Borstel, Germany. 46These authors contributed equally to this work. Correspondence should be addressed to T.W. (wirth@mnhn.fr), P. Supply (philip.supply@ibl.cnrs.fr) or S.N. (sniemann@fz-borstel.de).

Funding Information:
We gratefully acknowledge L. Cowan and J. Posey (US Centers for Disease Control and Prevention) for providing us with significant amounts of genotyping data for M. tuberculosis Beijing isolates. We thank T. Ubben, I. Radzio, T. Struwe-Sonnenschein and J. Zallet (Research Center Borstel) for excellent technical assistance. We acknowledge J. Peh for her assistance and support in the study and I. Comas for statistical advice. Parts of this work have been supported by grants from the European Community’s Seventh Framework Programme (FP7/2007-2013) under grant agreement 278864 in the framework of the European Union PathoNGenTrace project and grant agreement 223681 in the framework of the TB-PAN-NET project. We also thank Action Transversale du Muséum National d’Histoire Naturelle ‘Les Microorganismes, Acteurs Clés dans les Ecosystèmes’ for financial support. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Publisher Copyright:
© 2015 Nature Amrerica, Inc. All rights reserved.

Copyright:
Copyright 2018 Elsevier B.V., All rights reserved.

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