A sister lineage of the Mycobacterium tuberculosis complex discovered in the African Great Lakes region.
Aged
DNA, Bacterial
/ genetics
Evolution, Molecular
Genetic Variation
Genome, Bacterial
Genomics
Genotype
Humans
Likelihood Functions
Limit of Detection
Male
Mutation
Mycobacterium tuberculosis
/ classification
Phenotype
Phylogeny
Rifampin
/ pharmacology
Rwanda
Tuberculosis, Multidrug-Resistant
/ microbiology
Uganda
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
09 06 2020
09 06 2020
Historique:
received:
21
01
2020
accepted:
13
05
2020
entrez:
11
6
2020
pubmed:
11
6
2020
medline:
28
8
2020
Statut:
epublish
Résumé
The human- and animal-adapted lineages of the Mycobacterium tuberculosis complex (MTBC) are thought to have expanded from a common progenitor in Africa. However, the molecular events that accompanied this emergence remain largely unknown. Here, we describe two MTBC strains isolated from patients with multidrug resistant tuberculosis, representing an as-yet-unknown lineage, named Lineage 8 (L8), seemingly restricted to the African Great Lakes region. Using genome-based phylogenetic reconstruction, we show that L8 is a sister clade to the known MTBC lineages. Comparison with other complete mycobacterial genomes indicate that the divergence of L8 preceded the loss of the cobF genome region - involved in the cobalamin/vitamin B12 synthesis - and gene interruptions in a subsequent common ancestor shared by all other known MTBC lineages. This discovery further supports an East African origin for the MTBC and provides additional molecular clues on the ancestral genome reduction associated with adaptation to a pathogenic lifestyle.
Identifiants
pubmed: 32518235
doi: 10.1038/s41467-020-16626-6
pii: 10.1038/s41467-020-16626-6
pmc: PMC7283319
doi:
Substances chimiques
DNA, Bacterial
0
Rifampin
VJT6J7R4TR
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2917Références
Gagneux, S. Ecology and evolution of Mycobacterium tuberculosis. Nat. Rev. Microbiol. 16, 202–213 (2018).
pubmed: 29456241
doi: 10.1038/nrmicro.2018.8
World Health Organization. Global Tuberculosis Report 2018 (WHO, 2018).
Comas, I. et al. Out-of-Africa migration and Neolithic coexpansion of Mycobacterium tuberculosis with modern humans. Nat. Genet. 45, 1176–1182 (2013).
pubmed: 23995134
pmcid: 3800747
doi: 10.1038/ng.2744
Supply, P. et al. Genomic analysis of smooth tubercle bacilli provides insights into ancestry and pathoadaptation of Mycobacterium tuberculosis. Nat. Genet. 45, 172–179 (2013).
pubmed: 23291586
doi: 10.1038/ng.2517
Bos, K. I. et al. Pre-Columbian mycobacterial genomes reveal seals as a source of New World human tuberculosis. Nature 514, 494–497 (2014).
pubmed: 25141181
pmcid: 4550673
doi: 10.1038/nature13591
Brites, D. et al. A new phylogenetic framework for the animal-adapted Mycobacterium tuberculosis complex. Front. Microbiol. 9, 2820 (2018).
pubmed: 30538680
pmcid: 6277475
doi: 10.3389/fmicb.2018.02820
Rutaihwa, L. K. et al. Multiple introductions of Mycobacterium tuberculosis lineage 2-Beijing into Africa over centuries. Front. Ecol. Evolution 7, 112 (2019).
doi: 10.3389/fevo.2019.00112
O’Neill, M. B. et al. Lineage specific histories of Mycobacterium tuberculosis dispersal in Africa and Eurasia. Mol. Ecol. 28, 3241–3256 (2019).
pubmed: 31066139
pmcid: 6660993
Wirth, T. et al. Origin, spread and demography of the Mycobacterium tuberculosis complex. PLoS Pathog. 4, e1000160 (2008).
pubmed: 18802459
pmcid: 2528947
doi: 10.1371/journal.ppat.1000160
Gagneux, S. et al. Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 103, 2869–2873 (2006).
pubmed: 16477032
doi: 10.1073/pnas.0511240103
Gutierrez, M. C. et al. Ancient origin and gene mosaicism of the progenitor of Mycobacterium tuberculosis. PLoS Pathog. 1, e5 (2005).
pubmed: 16201017
pmcid: 1238740
doi: 10.1371/journal.ppat.0010005
Blouin, Y. et al. Progenitor “Mycobacterium canettii” clone responsible for lymph node tuberculosis epidemic, Djibouti. Emerg. Infect. Dis. 20, 21–28 (2014).
pubmed: 24520560
pmcid: 3884719
doi: 10.3201/eid2001.130652
Coscolla, M. & Gagneux, S. Consequences of genomic diversity in Mycobacterium tuberculosis. Semin. Immunol. 26, 431–444 (2014).
pubmed: 25453224
pmcid: 4314449
doi: 10.1016/j.smim.2014.09.012
Boritsch, E. C. et al. Key experimental evidence of chromosomal DNA transfer among selected tuberculosis-causing mycobacteria. Proc. Natl Acad. Sci. USA 113, 9876–9881 (2016).
pubmed: 27528665
doi: 10.1073/pnas.1604921113
Boritsch, E. C. et al. pks5-recombination-mediated surface remodelling in Mycobacterium tuberculosis emergence. Nat. Microbiol. 1, 15019 (2016).
pubmed: 27571976
doi: 10.1038/nmicrobiol.2015.19
Mortimer, T. D. & Pepperell, C. S. Genomic signatures of distributive conjugal transfer among mycobacteria. Genome Biol. Evol. 6, 2489–2500 (2014).
pubmed: 25173757
pmcid: 4202316
doi: 10.1093/gbe/evu175
Helb, D. et al. Rapid detection of Mycobacterium tuberculosis and rifampin resistance by use of on-demand, near-patient technology. J. Clin. Microbiol. 48, 229–237 (2010).
pubmed: 19864480
doi: 10.1128/JCM.01463-09
Ng, K. C. S. et al. Automated algorithm for early identification of rifampicin-resistant tuberculosis transmission hotspots in Rwanda [abstract]. Int. J. Tuberc. Lung Dis. 22, 605 (2018).
Torrea, G. et al. Variable ability of rapid tests to detect Mycobacterium tuberculosis rpoB mutations conferring phenotypically occult rifampicin resistance. Sci. Rep. 9, 11826 (2019).
pubmed: 31413308
pmcid: 6694172
doi: 10.1038/s41598-019-48401-z
Trébucq, A. et al. Treatment outcome with a short multidrug-resistant tuberculosis regimen in nine African countries. Int. J. Tuberc. Lung Dis. 22, 17–25 (2018).
pubmed: 29149917
doi: 10.5588/ijtld.17.0498
Coll, F. et al. A robust SNP barcode for typing Mycobacterium tuberculosis complex strains. Nat. Commun. 5, 4812 (2014).
pubmed: 25176035
pmcid: 4166679
doi: 10.1038/ncomms5812
Couvin, D., David, A., Zozio, T. & Rastogi, N. Macro-geographical specificities of the prevailing tuberculosis epidemic as seen through SITVIT2, an updated version of the Mycobacterium tuberculosis genotyping database. Infect. Genet. Evol. https://doi.org/10.1016/j.meegid.2018.12.030 (2018).
doi: 10.1016/j.meegid.2018.12.030
pubmed: 30593925
Wanzala, S. I. et al. Retrospective analysis of archived pyrazinamide resistant Mycobacterium tuberculosis complex isolates from Uganda-evidence of interspecies transmission. Microorganisms 7, 221 (2019).
pmcid: 6723201
doi: 10.3390/microorganisms7080221
Stinear, T. P. et al. Insights from the complete genome sequence of Mycobacterium marinum on the evolution of Mycobacterium tuberculosis. Genome Res. 18, 729–741 (2008).
pubmed: 18403782
pmcid: 2336800
doi: 10.1101/gr.075069.107
Wang, J. et al. Insights on the emergence of Mycobacterium tuberculosis from the analysis of Mycobacterium kansasii. Genome Biol. Evol. 7, 856–870 (2015).
pubmed: 25716827
pmcid: 5322544
doi: 10.1093/gbe/evv035
Ssengooba, W. et al. Whole genome sequencing to complement tuberculosis drug resistance surveys in Uganda. Infect. Genet. Evol. 40, 8–16 (2016).
pubmed: 26917365
pmcid: 4856735
doi: 10.1016/j.meegid.2016.02.019
Carpels, G. et al. Drug resistant tuberculosis in sub-Saharan Africa: an estimation of incidence and cost for the year 2000. Tuber. Lung Dis. 76, 480–486 (1995).
pubmed: 8593367
doi: 10.1016/0962-8479(95)90522-7
Umubyeyi, A. N. et al. Results of a national survey on drug resistance among pulmonary tuberculosis patients in Rwanda. Int. J. Tuberc. Lung Dis. 11, 189–194 (2007).
pubmed: 17263290
World Health Organization. WHO | Global tuberculosis report 2016 (WHO, 2019).
Yang, T. et al. Pan-genomic study of Mycobacterium tuberculosis reflecting the primary/secondary genes, generality/individuality, and the interconversion through copy number variations. Front. Microbiol. 9, 1886 (2018).
pubmed: 30177918
pmcid: 6109687
doi: 10.3389/fmicb.2018.01886
Brosch, R. et al. A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc. Natl Acad. Sci. USA 99, 3684–3689 (2002).
pubmed: 11891304
doi: 10.1073/pnas.052548299
Tsolaki, A. G. et al. Functional and evolutionary genomics of Mycobacterium tuberculosis: Insights from genomic deletions in 100 strains. Proc. Natl Acad. Sci. USA 101, 4865–4870 (2004).
pubmed: 15024109
doi: 10.1073/pnas.0305634101
Brosch, R. et al. Genomic analysis reveals variation between Mycobacterium tuberculosis H37Rv and the attenuated M. tuberculosis H37Ra strain. Infect. Immun. 67, 5768–5774 (1999).
pubmed: 10531227
pmcid: 96953
doi: 10.1128/IAI.67.11.5768-5774.1999
Hirsh, A. E., Tsolaki, A. G., DeRiemer, K., Feldman, M. W. & Small, P. M. Stable association between strains of Mycobacterium tuberculosis and their human host populations. Proc. Natl Acad. Sci. USA 101, 4871–4876 (2004).
pubmed: 15041743
doi: 10.1073/pnas.0305627101
Chiner-Oms, Á. Genomic determinants of speciation and spread of the Mycobacterium tuberculosis complex. Sci. Adv. 5, eaaw3307 (2019).
pubmed: 31448322
pmcid: 6691555
doi: 10.1126/sciadv.aaw3307
Deshayes, C. et al. Detecting the molecular scars of evolution in the Mycobacterium tuberculosis complex by analyzing interrupted coding sequences. BMC Evol. Biol. 8, 78 (2008).
pubmed: 18325090
pmcid: 2277376
doi: 10.1186/1471-2148-8-78
Smith, N. H., Hewinson, R. G., Kremer, K., Brosch, R. & Gordon, S. V. Myths and misconceptions: the origin and evolution of Mycobacterium tuberculosis. Nat. Rev. Microbiol. 7, 537–544 (2009).
pubmed: 19483712
doi: 10.1038/nrmicro2165
Etienne, G. et al. Identification of the polyketide synthase involved in the biosynthesis of the surface-exposed lipooligosaccharides in mycobacteria. J. Bacteriol. 191, 2613–2621 (2009).
pubmed: 19181796
pmcid: 2668396
doi: 10.1128/JB.01235-08
Boritsch, E. C. & Brosch, R. in Tuberculosis and the Tubercle Bacillus 2nd edn, Vol. 4 495–515 (American Society of Microbiology, 2016).
Didelot, X. & Wilson, D. J. ClonalFrameML: efficient inference of recombination in whole bacterial genomes. PLoS Comput. Biol. 11, e1004041 (2015).
pubmed: 25675341
pmcid: 4326465
doi: 10.1371/journal.pcbi.1004041
Hershberg, R. et al. High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol. 6, e311 (2008).
pubmed: 19090620
pmcid: 2602723
doi: 10.1371/journal.pbio.0060311
Supply, P. et al. Linkage disequilibrium between minisatellite loci supports clonal evolution of Mycobacterium tuberculosis in a high tuberculosis incidence area. Mol. Microbiol. 47, 529–538 (2003).
pubmed: 12519202
doi: 10.1046/j.1365-2958.2003.03315.x
Mostowy, S., Cousins, D., Brinkman, J., Aranaz, A. & Behr, M. A. Genomic deletions suggest a phylogeny for the Mycobacterium tuberculosis complex. J. Infect. Dis. 186, 74–80 (2002).
pubmed: 12089664
doi: 10.1086/341068
Menardo, F., Duchêne, S., Brites, D. & Gagneux, S. The molecular clock of Mycobacterium tuberculosis. PLoS Pathog. 15, e1008067 (2019).
pubmed: 31513651
pmcid: 6759198
doi: 10.1371/journal.ppat.1008067
Niobe-Eyangoh, S. N. et al. Genetic biodiversity of Mycobacterium tuberculosis complex strains from patients with pulmonary tuberculosis in Cameroon. J. Clin. Microbiol. 41, 2547–2553 (2003).
pubmed: 12791879
pmcid: 156567
doi: 10.1128/JCM.41.6.2547-2553.2003
Godreuil, S. et al. First molecular epidemiology study of Mycobacterium tuberculosis in Burkina Faso. J. Clin. Microbiol. 45, 921–927 (2007).
pubmed: 17251410
pmcid: 1829100
doi: 10.1128/JCM.01918-06
Groenheit, R. et al. The Guinea-Bissau family of Mycobacterium tuberculosis complex revisited. PLoS ONE 6, e18601 (2011).
pubmed: 21533101
pmcid: 3080393
doi: 10.1371/journal.pone.0018601
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).
pubmed: 26687624
pmcid: 4691238
doi: 10.1016/j.cub.2015.10.061
Ates, L. S. et al. Mutations in ppe38 block PE_PGRS secretion and increase virulence of Mycobacterium tuberculosis. Nat. Microbiol. 3, 181–188 (2018).
pubmed: 29335553
doi: 10.1038/s41564-017-0090-6
Boritsch, E. C. et al. A glimpse into the past and predictions for the future: the molecular evolution of the tuberculosis agent. Mol. Microbiol. 93, 835–852 (2014).
pubmed: 25039682
doi: 10.1111/mmi.12720
Martens, J. H., Barg, H., Warren, M. & Jahn, D. Microbial production of vitamin B12. Appl. Microbiol. Biotechnol. 58, 275–B285 (2002).
pubmed: 11935176
doi: 10.1007/s00253-001-0902-7
Gopinath, K. et al. A vitamin B
pubmed: 23407640
pmcid: 3603451
doi: 10.1098/rsob.120175
Minias, A., Minias, P., Czubat, B. & Dziadek, J. Purifying selective pressure suggests the functionality of a vitamin B12 biosynthesis pathway in a global population of Mycobacterium tuberculosis. Genome Biol. Evol. 10, 2326–2337 (2018).
pubmed: 30060031
pmcid: 6363050
doi: 10.1093/gbe/evy153
Bottai, D. et al. TbD1 deletion as a driver of the evolutionary success of modern epidemic Mycobacterium tuberculosis lineages. Nat. Commun. 11, 1–14 (2020).
doi: 10.1038/s41467-020-14508-5
LEÃO, S. C. et al. Practical Handbook for the Phenotypic and Genotypic Identification of Mycobacteria, https://www.scienceopen.com/document?vid=f4807bef-1c8d-431e-be6a-bced8cb452b9 (Vanden Broele, Brugge, Belgium, 2004).
Borrell, S. et al. Reference set of Mycobacterium tuberculosis clinical strains: a tool for research and product development. PLOS ONE 14, e0214088 (2019).
pubmed: 30908506
pmcid: 6433267
doi: 10.1371/journal.pone.0214088
Kent, P. & Kubica, G. Public Health Mycobacteriology: A Guide for the Level III Laboratory (US Department of Health and Human Services, Centres for Disease Control, 1985).
Makhado, N. A. et al. Outbreak of multidrug-resistant tuberculosis in South Africa undetected by WHO-endorsed commercial tests: an observational study. Lancet Infect. Dis. 18, 1350–1359 (2018).
pubmed: 30342828
doi: 10.1016/S1473-3099(18)30496-1
van der Zanden, A. G. M. et al. Improvement of differentiation and interpretability of spoligotyping for Mycobacterium tuberculosis complex isolates by introduction of new spacer oligonucleotides. J. Clin. Microbiol. 40, 4628–4639 (2002).
pubmed: 12454164
pmcid: 154657
doi: 10.1128/JCM.40.12.4628-4639.2002
Menardo, F. et al. Treemmer: a tool to reduce large phylogenetic datasets with minimal loss of diversity. BMC Bioinformatics 19, 164 (2018).
pubmed: 29716518
pmcid: 5930393
doi: 10.1186/s12859-018-2164-8
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 4103590
pmcid: 4103590
doi: 10.1093/bioinformatics/btu170
Comas, I. et al. Human T cell epitopes of Mycobacterium tuberculosis are evolutionarily hyperconserved. Nat. Genet. 42, 498–503 (2010).
pubmed: 20495566
pmcid: 2883744
doi: 10.1038/ng.590
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 2705234
pmcid: 2705234
doi: 10.1093/bioinformatics/btp324
McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303 (2010).
pubmed: 2928508
pmcid: 2928508
doi: 10.1101/gr.107524.110
Li, H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27, 2987–2993 (2011).
pubmed: 21903627
pmcid: 3198575
doi: 10.1093/bioinformatics/btr509
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).
pubmed: 22300766
pmcid: 3290792
doi: 10.1101/gr.129684.111
Steiner, A., Stucki, D., Coscolla, M., Borrell, S. & Gagneux, S. KvarQ: targeted and direct variant calling from fastq reads of bacterial genomes. BMC Genomics 15, 881 (2014).
pubmed: 25297886
pmcid: 4197298
doi: 10.1186/1471-2164-15-881
Stamatakis, A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30, 1312–1313 (2014).
pubmed: 24451623
pmcid: 3998144
doi: 10.1093/bioinformatics/btu033
Duchene, S. et al. Inferring demographic parameters in bacterial genomic data using Bayesian and hybrid phylogenetic methods. BMC Evolut. Biol. 18, 95 (2018).
doi: 10.1186/s12862-018-1210-5
Koren, S. et al. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 27, 722–736 (2017).
pubmed: 28298431
pmcid: 5411767
doi: 10.1101/gr.215087.116
Hunt, M. et al. Circlator: automated circularization of genome assemblies using long sequencing reads. Genome Biol. 16, 294 (2015).
pubmed: 26714481
pmcid: 4699355
doi: 10.1186/s13059-015-0849-0
Scofield, D. G. GitHub - douglasgscofield/PacBio-utilities: collection of utilities for working with PacBio-based assemblies. https://github.com/douglasgscofield/PacBio-utilities (2015).
Seemann, T. GitHub - tseemann-snippy Rapid bacterial SNP calling and core genome alignments. https://github.com/tseemann/snippy (2015).
Carver, T. et al. Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database. Bioinformatics 24, 2672–2676 (2008).
pubmed: 18845581
pmcid: 2606163
doi: 10.1093/bioinformatics/btn529
Li, H. et al. East-Asian Helicobacter pylori strains synthesize heptan-deficient lipopolysaccharide. PLoS Genet. 15, e1008497 (2019).
pubmed: 31747390
pmcid: 6892558
doi: 10.1371/journal.pgen.1008497
Médigue, C. et al. MicroScope-an integrated resource for community expertise of gene functions and comparative analysis of microbial genomic and metabolic data. Brief. Bioinformatics 20, 1071–1084 (2019).
pubmed: 28968784
doi: 10.1093/bib/bbx113
Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).
pubmed: 25977477
pmcid: 4484387
doi: 10.1101/gr.186072.114
Page, A. J. et al. Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31, 3691–3693 (2015).
pubmed: 26198102
pmcid: 4817141
doi: 10.1093/bioinformatics/btv421
Fedrizzi, T. et al. Genomic characterization of Nontuberculous Mycobacteria. Sci. Rep. 7, 45258 (2017).
pubmed: 28345639
pmcid: 5366915
doi: 10.1038/srep45258
Kozlov, A. M., Darriba, D., Flouri, T., Morel, B. & Stamatakis, A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 35, 4453–4455 (2019).
pubmed: 31070718
pmcid: 6821337
doi: 10.1093/bioinformatics/btz305