1887

Abstract

Pathogens of the complex (MTBC) are considered to be monomorphic, with little gene content variation between strains. Nevertheless, several genotypic and phenotypic factors separate strains of the different MTBC lineages (L), especially L5 and L6 (traditionally termed ) strains, from each other. However, this genome variability and gene content, especially of L5 strains, has not been fully explored and may be important for pathobiology and current approaches for genomic analysis of MTBC strains, including transmission studies. By comparing the genomes of 355 L5 clinical strains (including 3 complete genomes and 352 Illumina whole-genome sequenced isolates) to each other and to H37Rv, we identified multiple genes that were differentially present or absent between H37Rv and L5 strains. Additionally, considerable gene content variability was found across L5 strains, including a split in the L5.3 sub-lineage into L5.3.1 and L5.3.2. These gene content differences had a small knock-on effect on transmission cluster estimation, with clustering rates influenced by the selected reference genome, and with potential overestimation of recent transmission when using H37Rv as the reference genome. We conclude that full capture of the gene diversity, especially high-resolution outbreak analysis, requires a variation of the single H37Rv-centric reference genome mapping approach currently used in most whole-genome sequencing data analysis pipelines. Moreover, the high within-lineage gene content variability suggests that the pan-genome of is at least several kilobases larger than previously thought, implying that a concatenated or reference-free genome assembly () approach may be needed for particular questions.

Funding
This study was supported by the:
  • H2020 European Research Council (Award 883582)
    • Principle Award Recipient: SebastienGagneux
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (Award 310030_188888, IZRJZ3_164171, IZLSZ3_170834 and CRSII5_177163)
    • Principle Award Recipient: SebastienGagneux
  • Generalitat Valenciana (Award SEJI/2019/011)
    • Principle Award Recipient: MireiaCoscolla
  • Ministerio de Ciencia, Innovación y Universidades (ESCMID) (Award RYC-2015-18213 and RTI2018-094399-A-I00)
    • Principle Award Recipient: CoscollaMireia
  • H2020 European Research Council (Award 311725)
    • Principle Award Recipient: BoukeC. de Jong
  • Directorate General for Development (DGD), Belgium (Award FA4)
    • Principle Award Recipient: N'Dira SanoussiC.
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2024-04-19
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References

  1. Phelan J, Sessions PFD, Tientcheu L, Perdigao J, Machado D. Methylation in mycobacterium tuberculosis is lineage specific with associated mutations present globally. Scientific Reports 2018; 8:1–7 [View Article]
    [Google Scholar]
  2. Meehan CJ. Mycobacterium Tuberculosis L5 Complete Genomes with Annonations 2020 [View Article]
    [Google Scholar]
  3. Brites D, Loiseau C, Menardo F, Borrell S, Boniotti MB et al. A New Phylogenetic Framework for the Animal-Adapted Mycobacterium Tuberculosis Complex. In Frontiers in Microbiology 9 (NOV Vol 9 2018 [View Article]
    [Google Scholar]
  4. Ngabonziza CS, Jean CL, Marceau M, Jouet A, Menardo F et al. A sister lineage of the Mycobacterium Tuberculosis complex discovered in the african great lakes region. Nature Communications 2020; 11:2917
    [Google Scholar]
  5. Coscolla M, Gagneux S. Consequences of genomic diversity in Mycobacterium Tuberculosis. Semin Immunol 2014; 26:431–444 [View Article] [PubMed]
    [Google Scholar]
  6. Coscolla M, Gagneux S, Menardo F, Loiseau C, Ruiz-Rodriguez P et al. Phylogenomics of Mycobacterium Africanum Reveals a new lineage and a complex evolutionary history. Microbial Genomics 2021; 7:477
    [Google Scholar]
  7. Boritsch EC, Khanna V, Pawlik A, Honoré N, Navas VH et al. Key experimental evidence of chromosomal DNA transfer among selected tuberculosiscausing mycobacteria. Proc Natl Acad Sci USA 2016; 113:9876–9881 [View Article] [PubMed]
    [Google Scholar]
  8. Chiner-Oms L, Sánchez-Busó J, Corander S, Gagneux SR, Harris D et al. Genomic determinants of speciation and spread of the Mycobacterium Tuberculosis complex. Science Advances 2019; 5: [View Article]
    [Google Scholar]
  9. Bottai D, Frigui W, Sayes F, Luca MD, Spadoni D et al. TbD1 Deletion as a driver of the evolutionary success of modern epidemic Mycobacterium Tuberculosis lineages. Nature Communications 2020; 11:1
    [Google Scholar]
  10. Gagneux S, DeRiemer K, Van T, Kato-Maeda M, de Jong BC et al. Variable Host-Pathogen comen Compatibility in Mycobacterium Tuberculosis. Proc Natl Acad Sci USA 2006; 103:2869–2873
    [Google Scholar]
  11. Behr MA, Wilson MA, Gill WP, Salamon H, Schoolnik GK et al. Comparative genomics of BCG Vaccines by Whole-Genome DNA Microarray. Science 1999; 284:1520–1523 [View Article] [PubMed]
    [Google Scholar]
  12. Brosch R, Gordon SV, Marmiesse M, Brodin P, Buchrieser C et al. A new evolutionary scenario for the Mycobacterium Tuberculosis Complex. PNAS 2002; 99:3684–3689 [View Article]
    [Google Scholar]
  13. Gordon S, Brosch R, Billault A, Garnier T, Eiglmeier K et al. Identification of Variable Regions in the Genomes of Tubercle Bacilli Using Bacterial Artificial Chromosome Arrays. Mol Microbiol 1999; 32:643–655 [View Article] [PubMed]
    [Google Scholar]
  14. 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]
  15. Mostowy S, Cousins D, Brinkman J, Aranaz A, Behr MA. Genomic deletions suggest a phylogeny for the mycobacterium tuberculosis complex. JID 2002
    [Google Scholar]
  16. Firdessa R, Berg S, Hailu E, Schelling E, Gumi B et al. Mycobacterial lineages causing pulmonary and extrapulmonary Tuberculosis, Ethiopia. Emerg Infect Dis 2013; 19:460–463 [View Article] [PubMed]
    [Google Scholar]
  17. Nebenzahl-Guimaraes H, Yimer SA, Holm-Hansen C, Beer JD, Brosch R et al. Genomic characterization of Mycobacterium Tuberculosis Lineage 7 and a Proposed Name: ‘Aethiops Vetus. Microbial Genomics 2016; 2:
    [Google Scholar]
  18. Niemann S, Kubica T, Bange FC, Adjei O, Browne EN et al. The species mycobacterium Africanum in the light of new molecular markers. J Clin Microbiol 2004; 42:3958–3962 [View Article] [PubMed]
    [Google Scholar]
  19. Riojas MA, Mcgough KJ, Rider-Riojas CJ, Rastogi N, Hazbón MH. Phylogenomic Analysis of the Species of the Mycobacterium Tuberculosis Complex Demonstrates That Mycobacterium Africanum, Mycobacterium Bovis, Mycobacterium Caprae, Mycobacterium Microti and Mycobacterium Pinnipedii Are Later Heterotypic Synonyms of Mycob 2018
    [Google Scholar]
  20. de Jong BC, Hill PC, Aiken A, Awine T, Antonio M et al. Progression to active tuberculosis, but not transmission, varssion to Active Tuberculosis, but Not Transmission, Varies by M. Tuberculosis lineage in the gamLineage in The Gambia”. J Infect Dis 2008; 198:1037–1043
    [Google Scholar]
  21. de Jong BC, Antonio M, Gagneux S. Mycobacterium africanum--review of an important cause of human tuberculosis in West Africa. PLoS Negl Trop Dis 2010; 4:e744 [View Article]
    [Google Scholar]
  22. 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. Nature Genetics 2013; 45:10
    [Google Scholar]
  23. Intemann CD, Thye T, Niemann S, Browne ENL, Chinbuah MA et al. Autophagy Gene Variant IRGM −261T contributes to protection from tuberculosis caused by Mycobacterium Tuberculosis but Not by M. Africanum strains. Edited by William Bishai PLoS Pathogens 2009; 5:e1000577
    [Google Scholar]
  24. Thye T, Niemann S, Walter K, Homolka S, Intemann CD et al. Variant G57E of mannose binding lectin associated with protection against tuberculosis caused by mycobacterium africanum but not by M. Tuberculosis” PLoS ONE 2011; 6:6
    [Google Scholar]
  25. Ofori-Anyinam B, Kanuteh F, Agbla SC, Adetifa I, Okoi C. Impact of the mycoBaterium africanum West Africa 2 lineage on tb diagnostics in West Africa: Decreased sensitivity of rapid identification tests in the Gambia. PLOS Neglected Tropical Diseases 2016; 10:1–12 [View Article]
    [Google Scholar]
  26. Sanoussi CN, de Jong BC, Odoun M, Arekpa K, Ligali MA et al. Low Sensitivity of the MPT64 Identification Test to Detect Lineage 5 of the Mycobacterium Tuberculosis Complex 2018
    [Google Scholar]
  27. Sanoussi CN, Affolabi D, Rigouts L, Anagonou S, de Jong B. Genotypic characterization directly applied to sputum improves the detection of mycobacterium Africanum west African 1, under-represented in positive cultures. PLOS Neglected Tropical Diseases 2017; 11:e0005900
    [Google Scholar]
  28. Leao S, Martin A, Mejia GI, Portaels F, Por- Taels F Leao SC. Practical handbook for the phenotypic and genotypic identification of mycobacteria 2004 pp 77–126
    [Google Scholar]
  29. Pattyn SR, Portaels F, Spanoghe L, Magos J. Further studies on african strains of mycobacterium tuberculosis. Ann Soc belge Méd Trop 1970 [PubMed]
    [Google Scholar]
  30. Gehre F, Otu J, DeRiemer K, Sessions PF de, Hibberd ML et al. Deciphering the growth behaviour of Mycobacterium Africanum. PLoS Neglected Tropical Diseases 2013; 7: [View Article]
    [Google Scholar]
  31. Magnus K. Epidemiological basis of tuberculosis eradication 3. Risk of pulmonary tuberculosis after human and bovine infection. Bull Org Mond Sante 1966; Vol. 35: [PubMed]
    [Google Scholar]
  32. Reiling N, Homolka S, Walter K, Brandenburg J, Niwinski L et al. Clade-specific virulence patterns of mycobacterium tuberculosis complex strains in human primary macrophages and aerogenically infected mice. MBio 2013; 4: [View Article]
    [Google Scholar]
  33. Gonzalo-Asensio J, Malaga W, Pawlik A, Astarie-Dequeker C, Passemar C et al. Evolutionary History of Tuberculosis Shaped by Conserved Mutations in the PhoPR Virulence Regulator. Proc Natl Acad Sci USA 2014; 111:11491–11496 [View Article] [PubMed]
    [Google Scholar]
  34. Ofori-Anyinam B, Riley AJ, Jobarteh T, Gitteh E, Sarr B et al. Comparative genomics shows differences in the electron transport and carbon metabolic pathways of mycobacterium Africanum relative to mycobacterium tuberculosis and suggests an adaptation to low oxygen tension. Tuberculosis 2020 p 101899101899 [View Article]
    [Google Scholar]
  35. Ates LS, Dippenaar A, Sayes F, Pawlik A, Bouchier C et al. Unexpected genomic and phenotypic diversity of Mycobacterium Africanum lineage 5 affects drug resistance, protein secretion, and immunogenicity. Genome Biol Evol 2018; 10:1858–1874 [View Article] [PubMed]
    [Google Scholar]
  36. Otchere D, Isaac MC, Sánchez-Busó L, Asante-Poku A, Brites D et al. Comparative genomics parative Genomics of Mycobacterium Africanum Lineage 5 and Lineage 6 from ghana suggests distinct ecological nm Ghana Suggests Distinct Ecological Niches. Scientific RepoRtS | 2018; 8:11269
    [Google Scholar]
  37. Otchere ID, Harris SR, Busso SL, Asante-Poku A, Osei-Wusu S. The first population structure and comparative genomics analysis of mycobacterium africanum strains from Ghana reveals higher diversity of lineage 5. Int J Mycobact 2016; 5:81S80 [View Article]
    [Google Scholar]
  38. Meehan CJ, Goig GA, Kohl TA, Verboven L, Dippenaar A et al. Whole genome sequencing of mycobacterium tuberculosis: Current standards and open issues. Nat Rev Microbiol 2019; 17:533–545 [View Article]
    [Google Scholar]
  39. Camus J-C, Pryor MJ, Me C, Cole ST. Re-Annotation of the Genome Sequence of Mycobacterium Tuberculosis H37Rv 2019
    [Google Scholar]
  40. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C et al. Deciphering the biology of Mycobacterium Tuberculosis from the complete genome sequence. Nature 1998; 393:537–544 [View Article] [PubMed]
    [Google Scholar]
  41. Goig GA, Blanco S, Garcia-Basteiro AL, Comas I. Contaminant DNA in Bacterial Sequencing Experiments Is a Major Source of False Genetic Variability. BioRxiv 2019
    [Google Scholar]
  42. Goig GA, Blanco S, Garcia-Basteiro AL, Comas I. Contaminant DNA in Bacterial Sequencing Experiments Is a Major Source of False Genetic Variability. BMC Biol 2020; 18:24 [View Article] [PubMed]
    [Google Scholar]
  43. Gagneux S. Ecology and evoology and Evolution of Mycobacterium Tuberculosis. Na Rev Microbiol 2018
    [Google Scholar]
  44. Bifani P, Moghazeh S, Shopsin B, Driscoll J, Ravikovitch A et al. Molecular characterization of Mycobacterium Tuberculosis H37Rv/Ra Variants: distinguishing the mycobacterial laboratory strain. J Clin Microbiol 2000; 38:3200–3204 [View Article] [PubMed]
    [Google Scholar]
  45. Kato-Maeda M, Rhee JT, Gingeras TR, Salamon H, Drenkow J et al. Comparing Genomes within the Species Mycobacterium Tuberculosis 2001
    [Google Scholar]
  46. O’Toole RF, Gautam SS. Limitations of the mycobacterium tuberculosis reference genome h37rv in the detection of virulence-related loci. Genomics 2017; 109:471–474
    [Google Scholar]
  47. Periwal V, Patowary A, Vellarikkal SK, Gupta A, Singh M et al. Comparative Whole-Genome Analysis of Clinical Isolates Reveals Characteristic Architecture of Mycobacterium Tuberculosis Pangenome 2015
    [Google Scholar]
  48. Tsolaki AG, Gagneux S, Pym AS, Yves Olivier L, Kreiswirth BN et al. Genomic deletions classify the beijing/w strains as a distinct genetic lineage of mycobacterium tuberculosis. JClin Microbiol 2005; 43:3185–3191
    [Google Scholar]
  49. Lew JM, Kapopoulou A, Jones LM, Cole ST. TubercuList - 10 Years After. Tuberculosis (Edinb) 2011; 91:1–7 [View Article] [PubMed]
    [Google Scholar]
  50. Bentley SD, Comas I, Bryant JM, Walker D, Smith NH et al. The genome of Mycobacterium Africanum West african 2 reveals a Lineage-Specific locus and genome erosion common to the M. Tuberculosis Complex.” Edited by Pamela L. C Small PLoS Neglected Tropical Diseases 2012; 6:e1552
    [Google Scholar]
  51. Malone KM, Farrell D, Stuber TP, Schubert OT, Aebersold R. Updated reference genome sequence and annotation of Mycobacterium bovis af2122/97. Genome Announcements 2017; 5:17–e00157
    [Google Scholar]
  52. Belisle JT, Sonnenberg MG. Isolation of Genomic DNA from Mycobacteria. In In Mycobacteria Protocols New Jersey: Humana Press; 1998 pp 31–44 https://doi.org/10.1385/0-89603-471-2:31
    [Google Scholar]
  53. Chin CS, Alexander DH, Marks P, Klammer AA, Drake J et al. Nonhybrid, finished microbial genome assemblies from Long-Read SMRT sequencing data. Nat Methods 2013; 10:563–569 [View Article] [PubMed]
    [Google Scholar]
  54. Seemann T. Prokka: Rapid prokaryotic genome annotation. Bioinformatics 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  55. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article] [PubMed]
    [Google Scholar]
  56. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J et al. BLAST+: Architecture and Applications. BMC Bioinformatics 2009; 10:421 [View Article] [PubMed]
    [Google Scholar]
  57. Darling ACE, Mau B, Blattner FR, Perna NT. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 2004; 14:1394–1403 [View Article] [PubMed]
    [Google Scholar]
  58. Kohl TA, Utpatel C, Schleusener V, Filippo MRD, Beckert P et al. MTBseq: A Comprehensive Pipeline for Whole Genome Sequence Analysis of Mycobacterium Tuberculosis Complex Isolates 2018
    [Google Scholar]
  59. Meehan CJ, Moris P, Kohl TA, Pečerska J, Akter S et al. The Relationship between Transmission Time and Clustering Methods in Mycobacterium Tuberculosis Epidemiology. EBioMedicine 2018; 37:410–416 [View Article] [PubMed]
    [Google Scholar]
  60. 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]
  61. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 1997; Vol. 25: [PubMed]
    [Google Scholar]
  62. Kapopoulou A, Lew JM, Cole ST. The Mycobrowser portal: A comprehensive and manually annotated resource for mycobacterial genomes. Tuberculosis (Edinb) 2011; 91:8–13 [View Article] [PubMed]
    [Google Scholar]
  63. Tatusov RL, Galperin MY, Natale DA, Koonin EV. The COG Database: A tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Research 2000; Vol. 28: [PubMed]
    [Google Scholar]
  64. Kavanagh KL, Jçrnvall H, Persson B, Oppermann U. The SDR Superfamily: Functional and Structural Diversity within a Family of Metabolic and Regulatory Enzymes 2008 p 77
    [Google Scholar]
  65. Vidal S, Lara CLK, Mordaka PM, Heap JT. Review of NAD(P)H-Dependent Oxidoreductases: Properties, Engineering and Application. In Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics 1866 Vol 2 2018 pp 327–347 https://doi.org/10.1016/j.bbapap.2017.11.005
    [Google Scholar]
  66. Ahmed FH, Elaaf Mohamed A, Carr PD, Lee BM, Condic-Jurkic K et al. Rv2074 Is a Novel F 420 H 2-Dependent Biliverdin Reductase in Mycobacterium Tuberculosis; 2016 https://doi.org/10.1002/pro.2975
  67. Selengut JD, Haft DH. Unexpected Abundance of Coenzyme F 420-Dependent enzymes in mycobacterium tuberculosis and other actinobacteria †. J Bacteriol 2010; 192:5788–5798 [View Article] [PubMed]
    [Google Scholar]
  68. Dick T, Manjunatha U, Kappes B, Gengenbacher M. Vitamin B6 biosynthesis is essential for survival and virulence of Mycobacterium Tuberculosis. Mol Microbiol 2010; 78:980–988 [View Article] [PubMed]
    [Google Scholar]
  69. Grinter R, Ney B, Brammananth R, Barlow CK, Cordero PRF et al. Cellular and structural basis of synthesis of the unique intermediate Dehydro-F420-0 in Mycobacteria. BioRxiv 2020 [View Article]
    [Google Scholar]
  70. Ghodousi A, Rizvi AH, Baloch AQ, Ghafoor A, Masood F et al. Acquisition of Cross-Resistance to Bedaquiline and Clofazimine Following Treatment for Tuberculosis in 2 Pakistan 2019
    [Google Scholar]
  71. Zhang S, Chen J, Cui P, Shi W, Zhang W et al. Identification of Novel Mutations Associated with Clofazimine Resistance in Mycobacterium Tuberculosis 2015
    [Google Scholar]
  72. WHO WHO Consolidated Guidelines on Drug-Resistant Tuberculosis Treatment 2019
    [Google Scholar]
  73. WHO The shorter mdr-tb regimen features of the shorter mdr-tb regimen regimen composition 4-6; 2016
  74. Merker M, Kohl TA, Barilar I, Andres S, Fowler PW et al. Phylogenetically informative mutations in genes implicated in antibiotic resistance in mycobacterium tuberculosis complex. Genome Med 2020; 12:27 [View Article]
    [Google Scholar]
  75. Rengarajan J, Bloom BR, Rubin EJ. Genome-wide requirements for mycobacterium tuberculosis adaptation and survival in macrophages. PNAS June 2005; Vol. 7:
    [Google Scholar]
  76. Cavet JS, Graham AI, Meng W, Robinson NJ. A cadmium-lead-sensing ARSR-SMTB repressor with novel sensory sites. Complementary metal discrimination by NMTR and CMTR in a common cytosol. J Bio Chem 2003; 278:44560–44566
    [Google Scholar]
  77. Marcus SA, Sidiropoulos SW, Steinberg H, Talaat AM. CsoR Is Essential for Maintaining Copper Homeostasis in Mycobacterium Tuberculosis 2016
    [Google Scholar]
  78. Rowland JL, Niederweis M. Resistance Mechanisms of Mycobacterium Tuberculosis against Phagosomal Copper Overload 2012
    [Google Scholar]
  79. Samanovic M, Ding C, Thiele DJ, Heran Darwin K. Copper in microbial pathogenesis: Meddling with the metal. Cell Host & Microbe 2012; 11:106–115
    [Google Scholar]
  80. Ward SK, Hoye EA, Talaat AM. The global responses of Mycobacterium tuberculosis to physiological levels of copper. J Bacteriol 2008; 190:2939–2946 [View Article] [PubMed]
    [Google Scholar]
  81. Parsons LM, Brosch R, Cole ST, Somoskövi A, Loder A et al. Rapid and simple approach for identification of mycobacterium tuberculosis complex isolates by pcr-based genomic deletion analysis. J Clin Microbiol 2002; 40:2339–2345 [View Article]
    [Google Scholar]
  82. Mostowy S, Onipede A, Gagneux S, Niemann S, Kremer K et al. Genomic analysis distinguishes mycobacterium africanum. J Clin Microbiol 2004; 42:3594–3599 [View Article] [PubMed]
    [Google Scholar]
  83. Lee RS, Proulx JF, McIntosh F, Behr MA, Hanage WP. Previously undetected super-spreading of mycobacterium tuberculosis revealed by deep sequencing. ELife 9 2020
    [Google Scholar]
  84. Norman A, Folkvardsen DB, Overballe-Petersen S, Lillebaek T. Complete Genome Sequence of Mycobacterium Tuberculosis DKC2, the Predominant Danish Outbreak Strain 2019
    [Google Scholar]
  85. Lee RS, Behr MA. Does choice matter? Reference-based alignment for molecular epidemiology of tuberculosis. J Clin Microbiol 2016; 54:1891–1895 [View Article] [PubMed]
    [Google Scholar]
  86. McInerney JO, Whelan FJ, Domingo-Sananes MR, McNally A, O’Connell MJ. Pangenomes and Selection: The Public Goods Hypothesis. In In The Pangenome Springer International Publishing; 2020 pp 151–167 https://doi.org/10.1007/978-3-030-38281-0_7
    [Google Scholar]
  87. Church DM, Schneider VA, Steinberg KM, Schatz MC, Quinlan AR et al. Extending reference assembly models. Genome Biology 2015; 16:1–5
    [Google Scholar]
  88. Colquhoun RM, Hall MB, Lima L, Roberts LW, Hunt M et al. Nucleotide-Resolution bacterial pan-genomics with reference graphs. BioRxiv, 2020 202011.12.380378
    [Google Scholar]
  89. Marschall T, Marz M, Abeel T, Dijkstra L, Dutilh BE. Computational Pan-genomics: Status, promises and challenges. Briefings in Bioinformatics 2018; 19:118–135
    [Google Scholar]
  90. Martiniano R, Garrison E, Jones ER, Manica A, Durbin R. Removing reference bias in ancient DNA data analysis by mapping to a sequence variation graph. BioRxiv 2019; 782755:
    [Google Scholar]
  91. Paten B, Novak AM, Eizenga JM, Garrison E. Genome Graphs and the Evolution of Genome Inference. In Genome Research Cold Spring Harbor Laboratory Press; 2017 https://doi.org/10.1101/gr.214155.116
    [Google Scholar]
  92. Rakocevic G, Semenyuk V, Lee WP, Spencer J, Browning J et al. Fast and accurate genomic analyses using genome graphs. Nat Genet 2019; 51:354–362 [View Article] [PubMed]
    [Google Scholar]
  93. Ingen J van, Kohl TA, Kranzer K, Hasse B, Keller PM et al. Global outbreak of severe Mycobacterium Chimaera disease after cardiac surgery: a molecular epidemiological study. The Lancet Infect Dis 2017; 17:1033–1041
    [Google Scholar]
  94. Garimella K, Iqbal Z, Krause MA, Campino S, Kekre M et al. Detection of simple and complex de novo mutations without, with, or with multiple reference sequences. BioRxiv 2019; 698910:
    [Google Scholar]
  95. Ballouz S, Dobin A, Gillis JA. Is it time to change the reference genome?” Genome Biology. BioMed Central Ltd 2019 [View Article]
    [Google Scholar]
  96. Li R, Li Y, Zheng H, Luo R, Zhu H et al. Building the sequence map of the human pan-genome. Nat Biotechnol 2010; 28:57–63 [View Article] [PubMed]
    [Google Scholar]
  97. Sherman RM, Forman J, Antonescu V, Puiu D, Daya M et al. Assembly of a Pan-Genome from Deep Sequencing of 910 Humans of African Descent. Nature Genetics Nature Publishing Group 2019
    [Google Scholar]
  98. Jandrasits C, Kröger S, Haas W, Renard BY. Computational pan-genome mapping and pairwise SNP-distance improve detection of Mycobacterium tuberculosis transmission clusters. PLoS Comput Biol 2019; 15:e1007527e1007527 [View Article]
    [Google Scholar]
  99. Medini D, Donati C, Tettelin H, Masignani V, Rappuoli R. The Microbial Pan-Genome. In Current Opinion in Genetics and Development. Elsevier Current Trends 2005 https://doi.org/10.1016/j.gde.2005.09.006
    [Google Scholar]
  100. Tettelin H, Masignani V, Cieslewicz MJ, Donati C, Medini D et al. Genome analysis of multiple pathogenic isolates of streptococcus agalactiae: implications for the microbial ‘Pan-Genome. Proc Natl Acad Sci USA 2005; 102:13950–13955 [View Article] [PubMed]
    [Google Scholar]
  101. Goig GA, Blanco S, Garcia-Basteiro AL, Comas I. Pervasive Contaminations in Sequencing Experiments Are a Major Source of False Genetic Variability: A Mycobacterium Tuberculosis Meta-Analysis 2018
    [Google Scholar]
  102. Iqbal Z, Caccamo M, Turner I, Flicek P, Mcvean G. De Novo Assembly and Genotyping of Variants Using Colored de Bruijn Graphs. In Nature Genetics Vol 44 2012 pp 226–232 [View Article]
    [Google Scholar]
  103. Maretty L, Jensen JM, Petersen B, Jonas andreas sibbesen, Liu siyang. Sequencing and de novo assembly of 150 genomes from Denmark as a population reference. Nature Publishing Group 2017; 548:
    [Google Scholar]
  104. Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH et al. MASH: Fast genome and metagenome distance estimation using minhash. Genome Biol 2016; 17:132 [View Article] [PubMed]
    [Google Scholar]
  105. Merle CSC, Sismanidis C, Sow OB, Gninafon M, Horton J. A pivotal registration phase III, multicenter, randomized tuberculosis controlled trial: Design issues and lessons learnt from the gatifloxacin for TB (OFLOTUB) project. Trials 13 (May) 2012
    [Google Scholar]
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