China’s tuberculosis epidemic stems from historical expansion of four strains of Mycobacterium tuberculosis

Bos, K. I. et al. Pre-Columbian mycobacterial genomes reveal seals as a source of New World human tuberculosis. Nature 514, 494–497 (2014).

Global Tuberculosis Report 2017 (World Health Organization, 2017).

Narain, J. P., Raviglione, M. C. & Kochi, A. HIV-associated tuberculosis in developing countries: epidemiology and strategies for prevention. Tuber. Lung Dis. 73, 311–321 (1992).

Steffen, R., Rickenbach, M., Wilhelm, U., Helminger, A. & Schar, M. Health problems after travel to developing countries. J. Infect. Dis. 156, 84–91 (1987).

Fusegawa, H. et al. Outbreak of tuberculosis in a 2000-year-old Chinese population. Kansenshogaku Zasshi 77, 146–149 (2003).

Prasad, P. V. General medicine in Atharvaveda with special reference to Yaksma (consumption/tuberculosis). Bull. Indian Inst. Hist. Med. Hyderabad 32, 1–14 (2002).

Suzuki, T. & Inoue, T. Earliest evidence of spinal tuberculosis from the Aneolithic Yayoi period in Japan. Int. J. Osteoarchaeol. 17, 392–402 (2007).

Li, X. et al. Archaeological and palaeopathological study on the third/second century bc grave from Turfan, China: individual health history and regional implications. Quat. Int. 290, 335–343 (2013).

Packard, R. M. White Plague, Black Labor: Tuberculosis and the Political Economy of Health and Disease in South Africa (Univ. California Press, Berkeley, 1989).

Dubos, R. J. & Dubos, J. The White Plague: Tuberculosis, Man, and Society (Rutgers Univ. Press, New Brunswick, 1952).

Stead, W. W. The origin and erratic global spread of tuberculosis. How the past explains the present and is the key to the future. Clin. Chest Med. 18, 65–77 (1997).

Zhang, Z. Epidemic Chronology of Ancient China [in Chinese] (Fujian Science and Technology Press, Fuzhou, 2007).

Bates, J. H. & Stead, W. W. The history of tuberculosis as a global epidemic. Med. Clin. North Am. 77, 1205–1217 (1993).

Perry, E. J. & Selden, M. Chinese Society: Change, Conflict and Resistance (Routledge, London, 2003).

Wang, F. & Zuo, X. Inside China’s cities: institutional barriers and opportunities for urban migrants. Am. Econ. Rev. 89, 276–280 (1999).

O’Neill, M. B. et al. Lineage specific histories of Mycobacterium tuberculosis dispersal in Africa and Eurasia. Preprint at https://www.biorxiv.org/content/early/2017/10/27/210161 (2017).

Pepperell, C. S. et al. Dispersal of Mycobacterium tuberculosis via the Canadian fur trade. Proc. Natl Acad. Sci. USA 108, 6526–6531 (2011).

Hershberg, R. et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 6, e311 (2008).

Wirth, T. et al. Origin, spread and demography of the Mycobacterium tuberculosis complex. PLoS. Pathog. 4, e1000160 (2008).

Gagneux, S. & Small, P. M. Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development. Lancet Infect. Dis. 7, 328–337 (2007).

Stucki, D. et al. Mycobacterium tuberculosis lineage 4 comprises globally distributed and geographically restricted sublineages. Nat. Genet. 48, 1535–1543 (2016).

Linz, B. et al. An African origin for the intimate association between humans and Helicobacter pylori. Nature 445, 915–918 (2007).

Pepperell, C. S. et al. The role of selection in shaping diversity of natural M. tuberculosis populations. PLoS Pathog. 9, e1003543 (2013).

Bjorn-Mortensen, K. et al. Tracing Mycobacterium tuberculosis transmission by whole genome sequencing in a high incidence setting: a retrospective population-based study in East Greenland. Sci. Rep. 6, 33180 (2016).

Lee, R. S. et al. Population genomics of Mycobacterium tuberculosis in the Inuit. Proc. Natl Acad. Sci. USA 112, 13609–13614 (2015).

Comas, I. et al. Population genomics of Mycobacterium tuberculosis in Ethiopia contradicts the virgin soil hypothesis for human tuberculosis in Sub-Saharan Africa. Curr. Biol. 25, 3260–3266 (2015).

Holt, K. E. et al. Frequent transmission of the Mycobacterium tuberculosis Beijing lineage and positive selection for the EsxW Beijing variant in Vietnam. Nat. Genet. 50, 849–856 (2018).

Van Soolingen, D. et al. Predominance of a single genotype of Mycobacterium tuberculosis in countries of east Asia. J. Clin. Microbiol. 33, 3234–3238 (1995).

Pang, Y. et al. Spoligotyping and drug resistance analysis of Mycobacterium tuberculosis strains from national survey in China. PLoS ONE 7, e32976 (2012).

Coll, F. et al. A robust SNP barcode for typing Mycobacterium tuberculosis complex strains. Nat. Commun. 5, 4812 (2014).

Comas, I. et al. Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat. Genet. 45, 1176–1182 (2013).

Ge, J. China Population History (Zhongguo Renkou Shi) (Fudan Univ. Press, Shanghai, 2000).

Wang, L. et al. Tuberculosis prevalence in China, 1990–2010; a longitudinal analysis of national survey data. Lancet 383, 2057–2064 (2014).

Neher, R. A. & Hallatschek, O. Genealogies of rapidly adapting populations. Proc. Natl Acad. Sci. USA 110, 437–442 (2013).

Magiorkinis, G. et al. Integrating phylodynamics and epidemiology to estimate transmission diversity in viral epidemics. PLoS Comput. Biol. 9, e1002876 (2013).

Guang-Hui, H. Historical Population Geography of Beijing [in Chinese] (Peking Univ. Press, Beijing, 1996).

Hou Ren-Zhi, T. X.-F. Historical Geography of Beijing City [in Chinese] (Beijing Yanshan Press, Beijing, 2000).

Huang, Q.-S. & Yang, G.-H. The placename of immigration in Sichuan and Huguang people migrate into Sichuan. J. Southwest China Normal Univ. 3, 023 (2005).

Millward, J. A. Eurasian Crossroads: A History of Xinjiang (Columbia Univ. Press, New York, 2007).

Poston, D. L. Jr., Mao, M. X. & Yu, M.-Y. The global distribution of the overseas Chinese around 1990. Popul. Dev. Rev. 20, 631–645 (1994).

Li, P. S. The rise and fall of Chinese immigration to Canada: newcomers from Hong Kong special administrative region of China and mainland China, 1980–2000. Int. Migr. 43, 9–34 (2005).

King, H. & Locke, F. B. Chinese in the United States: a century of occupational transition. Int. Migr. Rev. 14, 15–42 (1980).

Gagneux, S. et al. Variable host–pathogen compatibility in Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 103, 2869–2873 (2006).

McNeill, W. H. Human migration in historical perspective. Popul. Dev. Rev. 10, 1–18 (1984).

Gan, F. Ancient Glass Research Along the Silk Road (World Scientific, Hackensack, 2009).

Kauz, R. Aspects of the Maritime Silk Road: From the Persian Gulf to the East China Sea (Harrassowitz, Wiesbaden, 2010).

McPherson, K. China and the Maritime Silk Route. In Proc. of the UNESCO Quanzhou International Seminar on China and the Maritime Routes of the Silk Roads 55–60 (People’s Publishing House, 1991).

Lin, J. Y. The Needham puzzle: why the industrial revolution did not originate in China. Econ. Dev. Cult. Change 43, 269–292 (1995).

Jones, E. L., Frost, L. & White, C. Coming Full Circle: An Economic History of the Pacific Rim (Westview Press, Colorado, 1993).

Yusuf, S. & Saich, A. China Urbanizes: Consequences, Strategies, and Policies (World Bank, Washington DC, 2008).

Millward, J., Dunnell, R. W., Elliott, M. C. & Forêt, P. New Qing Imperial History. Making of Inner Asian Empire at Qing Chengde (RoutledgeCurzon, New York, 2004).

Mote, F. W., Twitchett, D. & Fairbank, J. K. The Cambridge History of China: Volume 7, The Ming Dynasty, 1368–1644 (Cambridge Univ. Press, London, 1988).

Yang, C. et al. Transmission of Mycobacterium tuberculosis in China: a population-based molecular epidemiologic study. Clin. Infect. Dis. 61, 219–227 (2015).

Ackley, S. F., Liu, F., Porco, T. C. & Pepperell, C. S. Modeling historical tuberculosis epidemics among Canadian First Nations: effects of malnutrition and genetic variation. PeerJ 3, e1237 (2015).

Yang, C. et al. Mycobacterium tuberculosis Beijing strains favor transmission but not drug resistance in China. Clin. Infect. Dis. 55, 1179–1187 (2012).

De Jong, B. C. et al. Progression to active tuberculosis, but not transmission, varies by Mycobacterium tuberculosis lineage in The Gambia. J. Infect. Dis. 198, 1037–1043 (2008).

Liu, Q. et al. Genetic features of Mycobacterium tuberculosis modern Beijing sublineage. Emerg. Microbes Infect. 5, e14 (2016).

Van Laarhoven, A. et al. Low induction of proinflammatory cytokines parallels evolutionary success of modern strains within the Mycobacterium tuberculosis Beijing genotype. Infect. Immun. 81, 3750–3756 (2013).

Ribeiro, S. C. et al. Mycobacterium tuberculosis strains of the modern sublineage of the Beijing family are more likely to display increased virulence than strains of the ancient sublineage. J. Clin. Microbiol. 52, 2615–2624 (2014).

Ates, L. S. et al. Mutations in ppe38 block PE_PGRS secretion and increase virulence of Mycobacterium tuberculosis. Nat. Microbiol. 3, 181–188 (2018).

Kay, G. L. et al. Eighteenth-century genomes show that mixed infections were common at time of peak tuberculosis in Europe. Nat. Commun. 6, 6717 (2015).

Wirth, T. Massive lineage replacements and cryptic outbreaks of Salmonella Typhi in eastern and southern Africa. Nat. Genet. 47, 565–567 (2015).

Wagner, D. M. et al. Yersinia pestis and the plague of Justinian 541–543 ad: a genomic analysis. Lancet Infect. Dis. 14, 319–326 (2014).

Mutreja, A. et al. Evidence for several waves of global transmission in the seventh cholera pandemic. Nature 477, 462–465 (2011).

Vagene, A. J. et al. Salmonella enterica genomes from victims of a major sixteenth-century epidemic in Mexico. Nat. Ecol. Evol. 2, 520–528 (2018).

Zhao, Y. et al. National survey of drug-resistant tuberculosis in China. N. Engl. J. Med. 366, 2161–2170 (2012).

Liu, Q., Luo, T., Li, J., Mei, J. & Gao, Q. Triplex real-time PCR melting curve analysis for detecting Mycobacterium tuberculosis mutations associated with resistance to second-line drugs in a single reaction. J. Antimicrob. Chemother. 68, 1097–1103 (2013).

Farhat, M. R. et al. Genomic analysis identifies targets of convergent positive selection in drug-resistant Mycobacterium tuberculosis. Nat. Genet. 45, 1183–1189 (2013).

Comas, I., Homolka, S., Niemann, S. & Gagneux, S. Genotyping of genetically monomorphic bacteria: DNA sequencing in Mycobacterium tuberculosis highlights the limitations of current methodologies. PLoS ONE 4, e7815 (2009).

Luo, T. et al. Southern East Asian origin and coexpansion of Mycobacterium tuberculosis Beijing family with Han Chinese. Proc. Natl Acad. Sci. USA 112, 8136–8141 (2015).

Merker, M. et al. Evolutionary history and global spread of the Mycobacterium tuberculosis Beijing lineage. Nat. Genet. 47, 242–249 (2015).

Barbier, M. & Wirth, T. The evolutionary history, demography, and spread of the Mycobacterium tuberculosis complex. Microbiol. Spectr. 4, TBTB2-0008-2016 (2016).

Brudey, K. et al. Mycobacterium tuberculosis complex genetic diversity: mining the fourth international spoligotyping database (SpolDB4) for classification, population genetics and epidemiology. BMC Microbiol. 6, 23 (2006).

Viegas, S. O. et al. Molecular diversity of Mycobacterium tuberculosis isolates from patients with pulmonary tuberculosis in Mozambique. BMC Microbiol. 10, 195 (2010).

Zhang, H. et al. Genome sequencing of 161 Mycobacterium tuberculosis isolates from China identifies genes and intergenic regions associated with drug resistance. Nat. Genet. 45, 1255–1260 (2013).

Joshi, N. A. & Fass, J. N. Sickle: A Sliding-Window, Adaptive, Quality-Based Trimming Tool for FastQ Files (2011); https://github.com/najoshi/sickle

Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).

Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).

Koboldt, D. C. et al. VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res. 22, 568–576 (2012).

Gan, M., Liu, Q., Yang, C., Gao, Q. & Luo, T. Deep whole-genome sequencing to detect mixed infection of Mycobacterium tuberculosis. PLoS ONE 11, e0159029 (2016).

Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729 (2013).

Letunic, I. & Bork, P. Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. Nucleic Acids Res. 44, W242–W245 (2016).

RStudio Team RStudio: Integrated Development for R (RStudio, 2015).

Paradis, E. pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26, 419–420 (2010).

Hsieh, T., Ma, K. & Chao, A. iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol. Evol. 7, 1451–1456 (2016).

Yu, Y., Harris, A. J., Blair, C. & He, X. RASP (Reconstruct Ancestral State in Phylogenies): a tool for historical biogeography. Mol. Phylogenet. Evol. 87, 46–49 (2015).

Drummond, A. J., Suchard, M. A., Xie, D. & Rambaut, A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973 (2012).

Gignoux, C. R., Henn, B. M. & Mountain, J. L. Rapid, global demographic expansions after the origins of agriculture. Proc. Natl Acad. Sci. USA 108, 6044–6049 (2011).