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

Liu, Qingyun; Ma, Aijing; Wei, Lan‐Hai; Pang, Yu; Wu, Biao; Luò, Tāo; Zhou, Yang; Zheng, Hou-Feng; Jing, Qi; Gan, Mingyu; Zuo, Tianyu; Liu, Mei; Yang, Chongguang; Jin, Li; Comas, Iñaki; Gagneux, Sébastien; Zhao, Yanlin; Pepperell, Caitlin S.; Gao, Qian

doi:10.1038/s41559-018-0680-6

Cited by 108 publications

(173 citation statements)

References 74 publications

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“…Although L2 is dominant in Eastern Asia, interestingly the region did not appear to have played a prominent role in dispersal of this lineage, except in its exchanges with South Eastern Asia. A recently published study using a range of methods including Bayesian inference on a large regional sample found that the extant M.tb population in China traces to a limited number of introductions (Liu et al, ), which is consistent with our findings of relatively few exchanges of M. tb between Eastern Asia and other regions.…”

Section: Discussionsupporting

confidence: 91%

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Lineage specific histories of Mycobacterium tuberculosis dispersal in Africa and Eurasia

et al. 2019

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Mycobacterium tuberculosis ( M.tb ) is a globally distributed, obligate pathogen of humans that can be divided into seven clearly defined lineages. An emerging consensus places the origin and global dispersal of M.tb within the past 6,000 years: identifying how the ancestral clone of M.tb spread and differentiated within this timeframe is important for identifying the ecological drivers of the current pandemic. We used Bayesian phylogeographic inference to reconstruct the migratory history of M.tb in Africa and Eurasia and to investigate lineage specific patterns of spread from a geographically diverse sample of 552 M.tb genomes. Applying evolutionary rates inferred with ancient M.tb genome calibration, we estimated the timing of major events in the migratory history of the pathogen. Inferred timings contextualize M.tb dispersal within historical phenomena that altered patterns of connectivity throughout Africa and Eurasia: trans‐Indian Ocean trade in spices and other goods, the Silk Road and its predecessors, the expansion of the Roman Empire, and the European Age of Exploration. We found that Eastern Africa and Southeast Asia have been critical in the dispersal of M.tb . Our results further reveal that M.tb populations have grown through range expansion, as well as in situ, and delineate the independent evolutionary trajectories of bacterial subpopulations underlying the current pandemic.

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Section: Discussionsupporting

confidence: 91%

“…We estimate that L2 diversified in South Eastern Asia following migration from Eastern Africa at some point between 697 BCE and 20 BCE (Table 1, Figures 5 and S7). Previously published analyses of L2 phylogeography also inferred a Southeast Asian origin for the lineage (Liu et al, 2018;Luo et al, 2015).…”

Section: Major Events In Mtbs Migratory Historymentioning

confidence: 87%

Lineage specific histories of Mycobacterium tuberculosis dispersal in Africa and Eurasia

et al. 2019

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“…The increase is more gradual in the L4 model, and declines to hovering just above R=1. This roughly coincides with a jump in effective population size estimated by Liu and colleagues for MTBC lineages indigenous to China (61). The decline of R for L4 beginning approximately 350 BP appears surprising, given the historically recorded rise of the White Plague in Europe from the 17 th -19 th century (62).…”

Section: Discussionsupporting

confidence: 86%

A seventeenth-centuryMycobacterium tuberculosisgenome supports a Neolithic emergence of theMycobacterium tuberculosiscomplex

Sabin

Herbig

Vågene‬

et al. 2019

Preprint

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BackgroundAlthough tuberculosis accounts for the highest mortality from a bacterial infection on a global scale, questions persist regarding its origin. One hypothesis based on modernMycobacterium tuberculosiscomplex (MTBC) genomes suggests their most recent common ancestor (MRCA) followed human migrations out of Africa ~70,000 years before present (BP). However, studies using ancient genomes as calibration points have yielded much younger MRCA dates of less than 6,000 years. Here we aim to address this discrepancy through the analysis of the highest-coverage and highest quality ancient MTBC genome available to date, reconstructed from a calcified lung nodule of Bishop Peder Winstrup of Lund (b. 1605 – d. 1697).ResultsA metagenomic approach for taxonomic classification of whole DNA content permitted the identification of abundant DNA belonging to the human host and the MTBC, with few non-TB bacterial taxa comprising the background. Subsequent genomic enrichment enabled the reconstruction of a 141-fold coverageM. tuberculosisgenome. In utilizing this high-quality, high-coverage 17thcenturyM. tuberculosisgenome as a calibration point for dating the MTBC, we employed multiple Bayesian tree models, including birth-death models, which allowed us to model pathogen population dynamics and data sampling strategies more realistically than those based on the coalescent.ConclusionsThe results of our metagenomic analysis demonstrate the unique preservation environment calcified nodules provide for DNA. Importantly, we estimate an MRCA date for the MTBC of 3683 BP (2253-5821 BP) and for Lineage 4 of 1651 BP (946-2575 BP) using multiple models, confirming a Neolithic emergence for the MTBC.

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“…Kingman coalescent. These findings have deep implications for population genetic studies of MTB (also discussed in Morales-Arce et al 2019): 1) in the last five years, at least a dozen studies inferred the demographic history of different MTB populations(Pepperell et al 2013, Comas et al 2013, Bos et al 2014, Lee et al 2015Eldholm et al 2015, Kay et al 2015, Luo et al 2015, Merker et al 2015, Folkvardsen et al 2017, Merker et al 2018, Liu et al 2018, Bainomugisa et al 2018, O'Neill et al 2019.…”

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confidence: 94%

“…For example: 1) The Bayesian Skyline Plot (Drummond et al 2005) has been used to infer past population dynamics in tuberculosis outbreaks, finding evidence for constant population size (Bainomugisa et al 2018), rapid population growth (Eldholm et al 2015, Folkvardsen et al 2017 or slow population decline (Lee et al 2015). 2) Different methods have been used to infer the demographic history of the global MTB population (Pepperell et al 2013, Comas et al 2013, Bos et al 2014) and of single MTB lineages (Kay et al 2015, Luo et al 2015, Merker et al 2015, Merker et al 2018, Liu et al 2018, O'Neill et al 2019, finding evidence for population growth or for complex fluctuations that have been correlated with major events in human history such as the introduction of antibiotic treatment.…”

Section: Introductionmentioning

confidence: 99%

Multiple merger genealogies in outbreaks ofMycobacterium tuberculosis

Menardo

Gagneux

Freund

2019

Preprint

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The Kingman coalescent and its developments are often considered among the most important advances in population genetics of the last decades. Demographic inference based on the coalescent theory has been used to reconstruct the population dynamics and evolutionary history of several species, including Mycobacterium tuberculosis (MTB), an important human pathogen causing tuberculosis. One key assumption of Kingman's coalescent is that the number of descendants of different individuals does not vary strongly, and violating this assumption could lead to severe biases caused by model misspecification. Individual lineages of MTB are expected to vary strongly in reproductive success because 1) MTB is potentially under constant selection due to the pressure of the host immune system, 2) MTB undergoes repeated population bottlenecks when it transmits from one host to another, and 3) some hosts show much higher transmission rates compared to the average ("super-spreaders").Here we used an Approximate Bayesian Computation approach to test whether multiple merger coalescents (MMC), a class of models that allow for large variation in offspring sizes, are more adequate models to study MTB populations. We considered eleven publicly available whole genome sequence data sets sampled from MTB local populations and outbreaks and found that MMC had a better fit compared to the Kingman coalescent for nine of the eleven data sets. These results indicate that the neutral model for analyzing MTB outbreaks, and potentially the outbreaks of other pathogens, should be reassessed, and that past findings based on the Kingman coalescent need to be revisited.

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

Cited by 108 publications

References 74 publications

Lineage specific histories of Mycobacterium tuberculosis dispersal in Africa and Eurasia

Lineage specific histories of Mycobacterium tuberculosis dispersal in Africa and Eurasia

A seventeenth-centuryMycobacterium tuberculosisgenome supports a Neolithic emergence of theMycobacterium tuberculosiscomplex

Multiple merger genealogies in outbreaks ofMycobacterium tuberculosis

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