1887

Abstract

Molecular and genomic studies have revealed that Lineage 4 (L4, Euro-American lineage) emerged in Europe before becoming distributed around the globe by trade routes, colonial migration and other historical connections. Although L4 accounts for tens or hundreds of thousands of tuberculosis (TB) cases in multiple Southeast Asian countries, phylogeographical studies have either focused on a single country or just included Southeast Asia as part of a global analysis. Therefore, we interrogated public genomic data to investigate the historical patterns underlying the distribution of L4 in Southeast Asia and surrounding countries. We downloaded 6037 genomes associated with 29 published studies, focusing on global analyses of L4 and Asian studies of . We identified 2256 L4 genomes including 968 from Asia. We show that 81 % of L4 in Thailand, 51 % of L4 in Vietnam and 9 % of L4 in Indonesia belong to sub-lineages of L4 that are rarely seen outside East and Southeast Asia (L4.2.2, L4.4.2 and L4.5). These sub-lineages have spread between East and Southeast Asian countries, with no recent European ancestor. Although there is considerable uncertainty about the exact direction and order of intra-Asian dispersal, due to differing sampling frames between countries, our analysis suggests that China may be the intermediate location between Europe and Southeast Asia for two of the three predominantly East and Southeast Asian L4 sub-lineages (L4.2.2 and L4.5). This new perspective on L4 in Southeast Asia raises the possibility of investigating host population-specific evolution and highlights the need for more structured sampling from Southeast Asian countries to provide more certainty of the historical and current routes of dispersal.

Funding
This study was supported by the:
  • Wellcome Trust (Award 106680)
    • Principle Award Recipient: GuyE. Thwaites
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/mgen/10.1099/mgen.0.000955
2023-02-02
2024-03-19
Loading full text...

Full text loading...

/deliver/fulltext/mgen/9/2/mgen000955.html?itemId=/content/journal/mgen/10.1099/mgen.0.000955&mimeType=html&fmt=ahah

References

  1. World Health Organization Global tuberculosis report 2021 [Internet]. n.d https://www.who.int/publications-detail-redirect/9789240037021 accessed 18 June 2022
  2. Pai M, Kasaeva T, Swaminathan S. Covid-19’s Devastating Effect on Tuberculosis Care - A Path to Recovery. N Engl J Med 2022; 386:1490–1493 [View Article]
    [Google Scholar]
  3. Gagneux S, Small PM. Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development. Lancet Infect Dis 2007; 7:328–337 [View Article]
    [Google Scholar]
  4. Blouin Y, Hauck Y, Soler C, Fabre M, Vong R et al. Significance of the identification in the Horn of Africa of an exceptionally deep branching Mycobacterium tuberculosis clade. PLoS One 2012; 7:e52841 [View Article] [PubMed]
    [Google Scholar]
  5. Ngabonziza JCS, Loiseau C, Marceau M, Jouet A, Menardo F et al. A sister lineage of the Mycobacterium tuberculosis complex discovered in the African Great Lakes region. Nat Commun 2020; 11:2917 [View Article]
    [Google Scholar]
  6. Demay C, Liens B, Burguière T, Hill V, Couvin D et al. SITVITWEB--A publicly available international multimarker database for studying Mycobacterium tuberculosis genetic diversity and molecular epidemiology. Infect Genet Evol 2012; 12:755–766 [View Article] [PubMed]
    [Google Scholar]
  7. Mokrousov I, Vyazovaya A, Iwamoto T, Skiba Y, Pole I et al. Latin-American-Mediterranean lineage of Mycobacterium tuberculosis: Human traces across pathogen’s phylogeography. Mol Phylogenet Evol 2016; 99:133–143 [View Article] [PubMed]
    [Google Scholar]
  8. Stucki D, Brites D, Jeljeli L, Coscolla M, Liu Q et al. Mycobacterium tuberculosis lineage 4 comprises globally distributed and geographically restricted sublineages. Nat Genet 2016; 48:1535–1543 [View Article] [PubMed]
    [Google Scholar]
  9. Brynildsrud OB, Pepperell CS, Suffys P, Grandjean L, Monteserin J et al. Global expansion of Mycobacterium tuberculosis lineage 4 shaped by colonial migration and local adaptation. Sci Adv 2018; 4:eaat5869 [View Article] [PubMed]
    [Google Scholar]
  10. O’Neill MB, Shockey A, Zarley A, Aylward W, Eldholm V et al. Lineage specific histories of Mycobacterium tuberculosis dispersal in Africa and Eurasia. Mol Ecol 2019; 28:3241–3256 [View Article]
    [Google Scholar]
  11. Sasmono RT, Massi MN, Setianingsih TY, Wahyuni S, Halik H et al. Heterogeneity of Mycobacterium tuberculosis strains in Makassar, Indonesia. Int J Tuberc Lung Dis 2012; 16:1441–1448 [View Article]
    [Google Scholar]
  12. Chaidir L, Sengstake S, de Beer J, Oktavian A, Krismawati H et al. Predominance of modern Mycobacterium tuberculosis strains and active transmission of Beijing sublineage in Jayapura, Indonesia Papua. Infect Genet Evol 2016; 39:187–193 [View Article] [PubMed]
    [Google Scholar]
  13. Lisdawati V, Puspandari N, Rif’ati L, Soekarno T, M M et al. Molecular epidemiology study of Mycobacterium tuberculosis and its susceptibility to anti-tuberculosis drugs in Indonesia. BMC Infect Dis 2015; 15:366 [View Article] [PubMed]
    [Google Scholar]
  14. Parwati I, van Crevel R, Sudiro M, Alisjahbana B, Pakasi T et al. Mycobacterium tuberculosis population structures differ significantly on two Indonesian Islands. J Clin Microbiol 2008; 46:3639–3645 [View Article] [PubMed]
    [Google Scholar]
  15. Liu Q, Ma A, Wei L, Pang Y, Wu B et al. China’s tuberculosis epidemic stems from historical expansion of four strains of Mycobacterium tuberculosis. Nat Ecol Evol 2018; 2:1982–1992 [View Article] [PubMed]
    [Google Scholar]
  16. Nguyen VAT, Choisy M, Nguyen DH, Tran THT, Pham KLT et al. High prevalence of Beijing and EAI4-VNM genotypes among M. tuberculosis isolates in northern Vietnam: sampling effect, rural and urban disparities. PLoS ONE 2012; 7:e45553 [View Article]
    [Google Scholar]
  17. Nguyen VAT, Bañuls A-L, Tran THT, Pham KLT, Nguyen TS et al. Mycobacterium tuberculosis lineages and anti-tuberculosis drug resistance in reference hospitals across Viet Nam. BMC Microbiol 2016; 16: [View Article]
    [Google Scholar]
  18. Phyu S, Stavrum R, Lwin T, Svendsen ØS, Ti T et al. Predominance of Mycobacterium tuberculosis EAI and Beijing lineages in Yangon, Myanmar. J Clin Microbiol 2009; 47:335–344 [View Article] [PubMed]
    [Google Scholar]
  19. Ismail F, Couvin D, Farakhin I, Abdul Rahman Z, Rastogi N et al. Study of Mycobacterium tuberculosis complex genotypic diversity in Malaysia reveals a predominance of ancestral East-African-Indian lineage with a Malaysia-specific signature. PLOS ONE 2014; 9:e114832 [View Article] [PubMed]
    [Google Scholar]
  20. Zhang J, Heng S, Le Moullec S, Refregier G, Gicquel B et al. A first assessment of the genetic diversity of Mycobacterium tuberculosis complex in Cambodia. BMC Infect Dis 2011; 11: [View Article]
    [Google Scholar]
  21. Schopfer K, Rieder HL, Steinlin-Schopfer JF, van Soolingen D, Bodmer T et al. Molecular epidemiology of tuberculosis in Cambodian children. Epidemiol Infect 2015; 143:910–921 [View Article] [PubMed]
    [Google Scholar]
  22. Montoya JC, Murase Y, Ang C, Solon J, Ohkado A. A molecular epidemiologic analysis of Mycobacterium tuberculosis among Filipino patients in a suburban community in the Philippines. Kekkaku 2013; 88:543–552
    [Google Scholar]
  23. Faksri K, Xia E, Ong RT-H, Tan JH, Nonghanphithak D et al. Comparative whole-genome sequence analysis of Mycobacterium tuberculosis isolated from tuberculous meningitis and pulmonary tuberculosis patients. Sci Rep 2018; 8:4910 [View Article] [PubMed]
    [Google Scholar]
  24. Ruesen C, Chaidir L, van Laarhoven A, Dian S, Ganiem AR et al. Large-scale genomic analysis shows association between homoplastic genetic variation in Mycobacterium tuberculosis genes and meningeal or pulmonary tuberculosis. BMC Genomics 2018; 19:122 [View Article] [PubMed]
    [Google Scholar]
  25. Holt KE, McAdam P, Thai PVK, Thuong NTT, Ha DTM et al. Frequent transmission of the Mycobacterium tuberculosis Beijing lineage and positive selection for the EsxW Beijing variant in Vietnam. Nat Genet 2018; 50:849–856 [View Article] [PubMed]
    [Google Scholar]
  26. Phelan JE, Lim DR, Mitarai S, de Sessions PF, Tujan MAA et al. Mycobacterium tuberculosis whole genome sequencing provides insights into the Manila strain and drug-resistance mutations in the Philippines. Sci Rep 2019; 9:9305 [View Article] [PubMed]
    [Google Scholar]
  27. Maeda S, Hijikata M, Hang NTL, Thuong PH, Huan HV et al. Genotyping of Mycobacterium tuberculosis spreading in Hanoi, Vietnam using conventional and whole genome sequencing methods. Infect Genet Evol 2020; 78:104107 [View Article] [PubMed]
    [Google Scholar]
  28. Ajawatanawong P, Yanai H, Smittipat N, Disratthakit A, Yamada N et al. A novel Ancestral Beijing sublineage of Mycobacterium tuberculosis suggests the transition site to Modern Beijing sublineages. Sci Rep 2019; 9:13718 [View Article] [PubMed]
    [Google Scholar]
  29. BBMap [Internet] SourceForge; 2022 https://sourceforge.net/projects/bbmap/ accessed 23 July 2023
  30. Phelan JE, O’Sullivan DM, Machado D, Ramos J, Oppong YEA et al. Integrating informatics tools and portable sequencing technology for rapid detection of resistance to anti-tuberculous drugs. Genome Med 2019; 11:41 [View Article] [PubMed]
    [Google Scholar]
  31. Li H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. ArXiv13033997 Q-Bio [Internet]; 2013 http://arxiv.org/abs/1303.3997 accessed 1 April 2019
  32. Van der Auwera GA, O’Connor BD. Genomics in the cloud: using Docker, GATK, and WDL in Terra, First edition. Sebastopol, CA: O’Reilly Media; 2020
    [Google Scholar]
  33. PHEnix [Internet] PHE Bioinformatics Unit; 2021 https://github.com/phe-bioinformatics/PHEnix accessed 23 July 2023
  34. Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD et al. IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Mol Biol Evol 2020; 37:1530–1534 [View Article] [PubMed]
    [Google Scholar]
  35. Ansari MA, Didelot X. Bayesian Inference of the Evolution of a Phenotype Distribution on a Phylogenetic Tree. Genetics 2016; 204:89–98 [View Article] [PubMed]
    [Google Scholar]
  36. Sukumaran J, Holder MT. DendroPy: a Python library for phylogenetic computing. Bioinformatics 2010; 26:1569–1571 [View Article] [PubMed]
    [Google Scholar]
  37. Bollback JP. SIMMAP: stochastic character mapping of discrete traits on phylogenies. BMC Bioinformatics 2006; 7:88 [View Article] [PubMed]
    [Google Scholar]
  38. Revell LJ. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol 2012; 3:217–223 [View Article]
    [Google Scholar]
  39. R Core Team. R: A Language and Environment for Statistical Computing [Internet]. Vienna, Austria: R Foundation for Statistical Computing; 2020 https://www.R-project.org/
  40. RStudio Team. RStudio: Integrated Development Environment for R [Internet. Boston, MA: RStudio, PBC; 2021 http://www.rstudio.com/
  41. Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res 2019; 47:W256–W259 [View Article]
    [Google Scholar]
  42. Wickham H. Elegant Graphics for Data Analysis [Internet]. Springer-Verlag New York; 2016 https://ggplot2.tidyverse.org
  43. Sagulenko P, Puller V, Neher RA. TreeTime: Maximum-likelihood phylodynamic analysis. Virus Evol 2018; 4:vex042 [View Article] [PubMed]
    [Google Scholar]
  44. Menardo F, Duchêne S, Brites D, Gagneux S. The molecular clock of Mycobacterium tuberculosis. PLOS Pathog 2019; 15:e1008067 [View Article] [PubMed]
    [Google Scholar]
  45. Walker TM, Ip CLC, Harrell RH, Evans JT, Kapatai G et al. Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis 2013; 13:137–146 [View Article] [PubMed]
    [Google Scholar]
  46. Walker TM, Lalor MK, Broda A, Ortega LS, Morgan M et al. Assessment of Mycobacterium tuberculosis transmission in Oxfordshire, UK, 2007-12, with whole pathogen genome sequences: an observational study. Lancet Respir Med 2014; 2:285–292 [View Article] [PubMed]
    [Google Scholar]
  47. Comas I, Coscolla M, Luo T, Borrell S, Holt KE et al. Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat Genet 2013; 45:1176–1182 [View Article] [PubMed]
    [Google Scholar]
  48. Bryant JM, Harris SR, Parkhill J, Dawson R, Diacon AH et al. Whole-genome sequencing to establish relapse or re-infection with Mycobacterium tuberculosis: a retrospective observational study. Lancet Respir Med 2013; 1:786–792 [View Article] [PubMed]
    [Google Scholar]
  49. Zhang H, Li D, Zhao L, Fleming J, Lin N et al. Genome sequencing of 161 Mycobacterium tuberculosis isolates from China identifies genes and intergenic regions associated with drug resistance. Nat Genet 2013; 45:1255–1260 [View Article] [PubMed]
    [Google Scholar]
  50. Advani J, Verma R, Chatterjee O, Pachouri PK, Upadhyay P et al. Whole Genome Sequencing of Mycobacterium tuberculosis Clinical Isolates From India Reveals Genetic Heterogeneity and Region-Specific Variations That Might Affect Drug Susceptibility. Front Microbiol 2019; 10:309 [View Article] [PubMed]
    [Google Scholar]
  51. Chatterjee A, Nilgiriwala K, Saranath D, Rodrigues C, Mistry N. Whole genome sequencing of clinical strains of Mycobacterium tuberculosis from Mumbai, India: a potential tool for determining drug-resistance and strain lineage. Tuberculosis 2017; 107:63–72 [View Article]
    [Google Scholar]
  52. Manson AL, Abeel T, Galagan JE, Sundaramurthi JC, Salazar A et al. Mycobacterium tuberculosis Whole Genome Sequences From Southern India Suggest Novel Resistance Mechanisms and the Need for Region-Specific Diagnostics. Clin Infect Dis 2017; 64:1494–1501 [View Article] [PubMed]
    [Google Scholar]
  53. Shanmugam S, Kumar N, Nair D, Natrajan M, Tripathy SP et al. Genome Sequencing of Polydrug-, Multidrug-, and Extensively Drug-Resistant Mycobacterium tuberculosis Strains from South India. Microbiol Resour Announc 2019; 8:e01388-18 [View Article] [PubMed]
    [Google Scholar]
  54. Aung HL, Tun T, Moradigaravand D, Köser CU, Nyunt WW et al. Whole-genome sequencing of multidrug-resistant Mycobacterium tuberculosis isolates from Myanmar. J Glob Antimicrob Resist 2016; 6:113–117 [View Article] [PubMed]
    [Google Scholar]
  55. Bainomugisa A, Lavu E, Hiashiri S, Majumdar S, Honjepari A et al. Multi-clonal evolution of multi-drug-resistant/extensively drug-resistant Mycobacterium tuberculosis in a high-prevalence setting of Papua New Guinea for over three decades. Microb Genom 2018; 4:e000147 [View Article] [PubMed]
    [Google Scholar]
  56. Palittapongarnpim P, Ajawatanawong P, Viratyosin W, Smittipat N, Disratthakit A et al. Evidence for Host-Bacterial Co-evolution via Genome Sequence Analysis of 480 Thai Mycobacterium tuberculosis Lineage 1 Isolates. Sci Rep 2018; 8:11597 [View Article] [PubMed]
    [Google Scholar]
  57. Ali A, Hasan Z, McNerney R, Mallard K, Hill-Cawthorne G et al. Whole genome sequencing based characterization of extensively drug-resistant Mycobacterium tuberculosis isolates from Pakistan. PLoS One 2015; 10:e0117771 [View Article] [PubMed]
    [Google Scholar]
  58. Lempens P, Meehan CJ, Vandelannoote K, Fissette K, de Rijk P et al. Isoniazid resistance levels of Mycobacterium tuberculosis can largely be predicted by high-confidence resistance-conferring mutations. Sci Rep 2018; 8:3246 [View Article] [PubMed]
    [Google Scholar]
  59. Eldholm V, Monteserin J, Rieux A, Lopez B, Sobkowiak B et al. Four decades of transmission of a multidrug-resistant Mycobacterium tuberculosis outbreak strain. Nat Commun 2015; 6:7119 [View Article] [PubMed]
    [Google Scholar]
  60. Lee RS, Radomski N, Proulx J-F, Levade I, Shapiro BJ et al. Population genomics of Mycobacterium tuberculosis in the Inuit. Proc Natl Acad Sci U S A 2015; 112:13609–13614 [View Article] [PubMed]
    [Google Scholar]
  61. Glynn JR, Guerra-Assunção JA, Houben RMGJ, Sichali L, Mzembe T et al. Whole Genome Sequencing Shows a Low Proportion of Tuberculosis Disease Is Attributable to Known Close Contacts in Rural Malawi. PLoS One 2015; 10:e0132840 [View Article] [PubMed]
    [Google Scholar]
  62. Bryant JM, Schürch AC, van Deutekom H, Harris SR, de Beer JL et al. Inferring patient to patient transmission of Mycobacterium tuberculosis from whole genome sequencing data. BMC Infect Dis 2013; 13:110 [View Article] [PubMed]
    [Google Scholar]
  63. Perdigão J, Silva H, Machado D, Macedo R, Maltez F et al. Unraveling Mycobacterium tuberculosis genomic diversity and evolution in Lisbon, Portugal, a highly drug resistant setting. BMC Genomics 2014; 15:991 [View Article] [PubMed]
    [Google Scholar]
  64. Lillebaek T, Norman A, Rasmussen EM, Marvig RL, Folkvardsen DB et al. Substantial molecular evolution and mutation rates in prolonged latent Mycobacterium tuberculosis infection in humans. Int J Med Microbiol 2016; 306:580–585 [View Article] [PubMed]
    [Google Scholar]
  65. Guerra-Assunção JA, Crampin AC, Houben RMGJ, Mzembe T, Mallard K et al. Large-scale whole genome sequencing of M. tuberculosis provides insights into transmission in a high prevalence area. eLife 2015; 4:e05166 [View Article] [PubMed]
    [Google Scholar]
  66. Coll F, McNerney R, Guerra-Assunção JA, Glynn JR, Perdigão J et al. A robust SNP barcode for typing Mycobacterium tuberculosis complex strains. Nat Commun 2014; 5:4812 [View Article] [PubMed]
    [Google Scholar]
  67. Gagneux S. Host-pathogen coevolution in human tuberculosis. Philos Trans R Soc Lond B Biol Sci 2012; 367:850–859 [View Article] [PubMed]
    [Google Scholar]
  68. Pepperell CS, Granka JM, Alexander DC, Behr MA, Chui L et al. Dispersal of Mycobacterium tuberculosis via the Canadian fur trade. Proc Natl Acad Sci U S A 2011; 108:6526–6531 [View Article] [PubMed]
    [Google Scholar]
  69. Mulholland CV, Shockey AC, Aung HL, Cursons RT, O’Toole RF et al. Dispersal of Mycobacterium tuberculosis Driven by Historical European Trade in the South Pacific. Front Microbiol 2019; 10:2778 [View Article]
    [Google Scholar]
  70. French and British interregnum in the Dutch East Indies. In: Wikipedia [Internet] 2022 https://en.wikipedia.org/w/index.php?title=French_and_British_interregnum_in_the_Dutch_East_Indies&oldid=1091832267 accessed 23 July 2022
    [Google Scholar]
  71. Gagneux S. Ecology and evolution of Mycobacterium tuberculosis. Nat Rev Microbiol 2018; 16:202–213 [View Article] [PubMed]
    [Google Scholar]
  72. Casali N, Nikolayevskyy V, Balabanova Y, Ignatyeva O, Kontsevaya I et al. Microevolution of extensively drug-resistant tuberculosis in Russia. Genome Research 2012; 22:735–745 [View Article] [PubMed]
    [Google Scholar]
  73. Casali N, Nikolayevskyy V, Balabanova Y, Harris SR, Ignatyeva O et al. Evolution and transmission of drug-resistant tuberculosis in a Russian population. Nature Genetics 2014; 46:279–286 [View Article] [PubMed]
    [Google Scholar]
  74. Grandjean L, Gilman RH, Iwamoto T, Köser CU, Coronel J et al. Convergent evolution and topologically disruptive polymorphisms among multidrug-resistant tuberculosis in Peru. PLoS One 2017; 12:e0189838 [View Article] [PubMed]
    [Google Scholar]
  75. Malm S, Linguissi LSG, Tekwu EM, Vouvoungui JC, Kohl TA et al. New Mycobacterium tuberculosis complex sublineage, Brazzaville, Congo. Emerg Infect Dis 2017; 23:423–429 [View Article]
    [Google Scholar]
  76. Clark TG, Mallard K, Coll F, Preston M, Assefa S et al. Elucidating emergence and transmission of multidrug-resistant tuberculosis in treatment experienced patients by whole genome sequencing. PLoS One 2013; 8:e83012 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/mgen/10.1099/mgen.0.000955
Loading
/content/journal/mgen/10.1099/mgen.0.000955
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

EXCEL
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error