Genetic diversity in Mycobacterium tuberculosis

Current Topics in Microbiology and Immunology

Volumn 374, Issue , 2013, Pages 1-25

  Gagneux, Sebastien ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; DNA SEQUENCE; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOTYPE PHENOTYPE CORRELATION; GENOTYPING TECHNIQUE; HORIZONTAL GENE TRANSFER; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOGENICITY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; POPULATION STRUCTURE; PRIORITY JOURNAL; TUBERCULOSIS;

GENES, BACTERIAL; GENETIC VARIATION; GENOME, BACTERIAL; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HOST-PATHOGEN INTERACTIONS; HUMANS; MYCOBACTERIUM TUBERCULOSIS; PHYLOGENY; PHYLOGEOGRAPHY; TUBERCULOSIS, PULMONARY; VIRULENCE;

EID: 84884286461     PISSN: 0070217X     EISSN: None     Source Type: Book Series    
DOI: 10.1007/82-2013-329     Document Type: Article

References (136)

1. Achtman M (2008) Evolution, population structure, and phylogeography of genetically monomorphic bacterial pathogens. Annu Rev Microbiol 62:53-70
2. Alexander KA, Laver PN, Michel AL, Williams M, van Helden PD, Warren RM, Gey van Pittius NC (2010) Novel Mycobacterium tuberculosis complex pathogen, M. mungi. Emerg Infect Dis 16:1296-1299
3. Alland D, Whittam TS, Murray MB, Cave MD, Hazbon MH, Dix K, Kokoris M, Duesterhoeft A, Eisen JA, Fraser CM, Fleischmann RD (2003) Modelling bacterial evolution with comparative-genome-based marker systems: Application to Mycobacterium tuberculosis evolution and pathogenesis. J Bacteriol 185:3392-3399
4. Allix-Beguec C, Harmsen D, Weniger T, Supply P, Niemann S (2008) Evaluation and strategy for use of MIRU-VNTRplus, a multifunctional database for online analysis of genotyping data and phylogenetic identification of mycobacterium tuberculosis complex isolates. J Clin Microbiol 46:2692-2699
5. Andersson DI, Hughes D (2010) Antibiotic resistance and its cost: Is it possible to reverse resistance? Nat Rev Microbiol 8:260-271
6. Andersson DI, Levin BR (1999) The biological cost of antibiotic resistance. Curr Opin Microbiol 2:489-493
7. Arnvig KB, Young D (2012) Non-coding RNA and its potential role in mycobacterium tuberculosis pathogenesis. RNA Biol 9:427-436
8. Arnvig KB, Comas I, Thomson NR, Houghton J, Boshoff HI, Croucher NJ, Rose G, Perkins TT, Parkhill J, Dougan G, Young DB (2011) Sequence-based analysis uncovers an abundance of non-coding RNA in the total transcriptome of mycobacterium tuberculosis. PLoS Pathog 7:e1002342
9. Baker L, Brown T, Maiden MC, Drobniewski F (2004) Silent nucleotide polymorphisms and a phylogeny for Mycobacterium tuberculosis. Emerg Infect Dis 10:1568-1577
10. Banu S, Honore N, Saint-Joanis B, Philpott D, Prevost MC, Cole ST (2002) Are the PE-PGRS proteins of mycobacterium tuberculosis variable surface antigens? Mol Microbiol 44:9-19
11. Becq J, Gutierrez MC, Rosas-Magallanes V, Rauzier J, Gicquel B, Neyrolles O, Deschavanne P (2007) Contribution of horizontally acquired genomic islands to the evolution of the tubercle bacilli. Mol Biol Evol 24:1861-1871
12. Behr M, Gagneux S (2011) The rise and fall of the mycobacterium tuberculosis complex. In: Tibayrenc M (ed) Genetics and evolution of infectious diseases. Elsevier, London, pp 651-667
13. Behr MA, Wilson MA, Gill WP, Salamon H, Schoolnik GK, Rane S, Small PM (1999) Comparative genomics of BCG vaccines by whole-genome DNA microarray. Science 284:1520-1523
14. Bentley SD, Comas I, Bryant JM, Walker D, Smith NH, Harris SR, Thurston S, Gagneux S, Wood J, Antonio M, Quail MA, Gehre F, Adegbola RA, Parkhill J, de Jong BC (2012) The genome of mycobacterium africanum West African 2 reveals a lineage-specific locus and genome erosion common to the M tuberculosis complex. PLoS Negl Trop Dis 6:e1552
15. Bifani PJ, Mathema B, Kurepina NE, Kreiswirth BN (2002) Global dissemination of the mycobacterium tuberculosis W-Beijing family strains. Trends Microbiol 10:45-52
16. Bold TD, Davis DC, Penberthy KK, Cox LM, Ernst JD, de Jong BC (2012) Impaired fitness of mycobacterium africanum despite secretion of ESAT-6. J Infect Dis 205:984-990
17. Borrell S, Gagneux S (2009) Infectiousness, reproductive fitness and evolution of drug-resistant mycobacterium tuberculosis. Int J Tuberc Lung Dis 13:1456-1466
18. Borrell S, Gagneux S (2011) Strain diversity, epistasis and the evolution of drug resistance in mycobacterium tuberculosis. Clin Microbiol Infect 17:815-820
19. Brandis G, Wrande M, Liljas L, Hughes D (2012) Fitness-compensatory mutations in rifampicinresistant RNA polymerase. Mol Microbiol 85:142-151
20. Brennan MJ, Delogu G (2002) The PE multigene family: A 'molecular mantra' for mycobacteria. Trends Microbiol 10:246-249
21. Brites D, Gagneux S (2011) Old and new selective pressures on mycobacterium tuberculosis. Infect Genet Evol 12:678-685
22. Brosch R, Gordon SV, Buchrieser C, Pym AS, Garnier T, Cole ST (2000) Comparative genomics uncovers large tandem chromosomal duplications in mycobacterium bovis BCG Pasteur. Yeast 17:111-123
23. Brosch R, Gordon SV, Marmiesse M, Brodin P, Buchrieser C, Eiglmeier K, Garnier T, Gutierrez C, Hewinson G, Kremer K, Parsons LM, Pym AS, Samper S, van Soolingen D, Cole ST (2002) A new evolutionary scenario for the mycobacterium tuberculosis complex. Proc Natl Acad Sci USA 99:3684-3689
24. Brosch R, Gordon SV, Garnier T, Eiglmeier K, Frigui W, Valenti P, Dos Santos S, Duthoy S, Lacroix C, Garcia-Pelayo C, Inwald JK, Golby P, Nunez Garcia J, Hewinson RG, Behr MA, Quail MA, Churcher C, Barrell BG, Parkhill J, Cole ST (2007) Genome plasticity of BCG and impact on vaccine efficacy. Proc Natl Acad Sci USA
25. Brudey K, Driscoll JR, Rigouts L, Prodinger WM, Gori A, Al-Hajoj SA, Allix C, Aristimuno L, Arora J, Baumanis V, Binder L, Cafrune P, Cataldi A, Cheong S, Diel R, Ellermeier C, Evans JT, Fauville-Dufaux M, Ferdinand S, Garcia de Viedma D, Garzelli C, Gazzola L, Gomes HM, Gutierrez MC, Hawkey PM, van Helden PD, Kadival GV, Kreiswirth BN, Kremer K, Kubin M, Kulkarni SP, Liens B, Lillebaek T, Ly HM, Martin C, Mokrousov I, Narvskaia O, Ngeow YF, Naumann L, Niemann S, Parwati I, Rahim MZ, Rasolofo-Razanamparany V, Rasolonavalona T, Rossetti ML, Rusch-Gerdes S, Sajduda A, Samper S, Shemyakin I, Singh UB, Somoskovi A, Skuce R, van Soolingen D, Streicher EM, Suffys PN, Tortoli E, Tracevska T, Vincent V, Victor TC, Warren R, Yap SF, Zaman K, Portaels F, Rastogi N, Sola C (2006) Mycobacterium tuberculosis complex genetic diversity: Mining the fourth international spoligotyping database (SpolDB4) for classification, population genetics and epidemiology. BMC Microbiol 6:23
26. Casali N, Nikolayevskyy V, Balabanova Y, Ignatyeva O, Kontsevaya I, Harris SR, Bentley SD, Parkhill J, Nejentsev S, Hoffner SE, Horstmann RD, Brown T, Drobniewski F (2012) Microevolution of extensively drug-resistant tuberculosis in Russia. Genome Res 22:735-745
27. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, Harris D, Gordon SV, Eiglmeier K, Gas S, Barry CE 3rd, Tekaia F, Badcock K, Basham D, Brown D, Chillingworth T, Connor R, Davies R, Devlin K, Feltwell T, Gentles S, Hamlin N, Holroyd S, Hornsby T, Jagels K, Barrell BG et al (1998) Deciphering the biology of mycobacterium tuberculosis from the complete genome sequence. Nature 393:537-544
28. Comas I, Gagneux S (2009) The past and future of tuberculosis research. PLoS Pathog 5:e1000600
29. Comas I, Gagneux S (2011) A role for systems epidemiology in tuberculosis research. Trends Microbiol 19:492-500
30. Comas I, Homolka S, Niemann S, Gagneux S (2009) Genotyping of genetically monomorphic bacteria: DNA sequencing in mycobacterium tuberculosis highlights the limitations of current methodologies. PLoS ONE 4:e7815
31. Comas I, Chakravartti J, Small PM, Galagan J, Niemann S, Kremer K, Ernst JD, Gagneux S (2010) Human T cell epitopes of mycobacterium tuberculosis are evolutionarily hyperconserved. Nat Genet 42:498-503
32. Comas I, Borrell S, Roetzer A, Rose G, Malla B, Kato-Maeda M, Galagan J, Niemann S, Gagneux S (2012) Whole-genome sequencing of rifampicin-resistant mycobacterium tuberculosis strains identifies compensatory mutations in RNA polymerase genes. Nat Genet 44:106-110
33. Coscolla M, Gagneux S (2010) Does M tuberculosis genomic diversity explain disease diversity? Drug Discov Today Dis Mech 7:e43-e59
34. Cousins DV, Bastida R, Cataldi A, Quse V, Redrobe S, Dow S, Duignan P, Murray A, Dupont C, Ahmed N, Collins DM, Butler WR, Dawson D, Rodriguez D, Loureiro J, Romano MI, Alito A, Zumarraga M, Bernardelli A (2003) Tuberculosis in seals caused by a novel member of the mycobacterium tuberculosis complex: Mycobacterium pinnipedii sp. nov. Int J Syst Evol Microbiol 53:1305-1314
35. Cruciani M, Malena M, Bosco O, Gatti G, Serpelloni G (2001) The impact of human immunodeficiency virus type 1 on infectiousness of tuberculosis: A meta-analysis. Clin Infect Dis 33:1922-1930
36. de Jong BC, Hill PC, Brookes RH, Otu JK, Peterson KL, Small PM, Adegbola RA (2005) Mycobacterium africanum: A new opportunistic pathogen in HIV infection? Aids 19:1714-1715
37. de Jong BC, Hill PC, Aiken A, Awine T, Antonio M, Adetifa IM, Jackson-Sillah DJ, Fox A, Deriemer K, Gagneux S, Borgdorff MW, McAdam KP, Corrah T, Small PM, Adegbola RA (2008) Progression to active tuberculosis, but not transmission, varies by mycobacterium tuberculosis lineage in The Gambia. J Infect Dis 198:1037-1043
38. de Jong BC, Antonio M, Gagneux S (2010) Mycobacterium africanum-review of an important cause of human tuberculosis in West Africa. PLoS Negl Trop Dis 4:e744
39. de Steenwinkel JE, ten Kate MT, de Knegt GJ, Kremer K, Aarnoutse RE, Boeree MJ, Verbrugh HA, van Soolingen D, Bakker-Woudenberg IA (2012) Drug susceptibility of mycobacterium tuberculosis Beijing genotype and association with MDR TB. Emerg Infect Dis 18:660-663
40. Deitsch KW, Lukehart SA, Stringer JR (2009) Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens. Nat Rev Microbiol 7:493-503
41. Demay C, Liens B, Burguiere T, Hill V, Couvin D, Millet J, Mokrousov I, Sola C, Zozio T, Rastogi N (2012) SITVITWEB -a publicly available international multimarker database for studying Mycobacterium tuberculosis genetic diversity and molecular epidemiology. Infect Genet Evol 12:755-766
42. Didelot X, Lawson D, Darling A, Falush D (2010) Inference of homologous recombination in bacteria using whole-genome sequences. Genetics 186:1435-1449
43. Domenech P, Kolly GS, Leon-Solis L, Fallow A, Reed MB (2010) A massive gene duplication event amongst clinical isolates of the mycobacterium tuberculosis W/Beijing family. J Bacteriol 192:4562-4570
44. Dos Vultos T, Mestre O, Rauzier J, Golec M, Rastogi N, Rasolofo V, Tonjum T, Sola C, Matic I, Gicquel B (2008) Evolution and diversity of clonal bacteria: The paradigm of mycobacterium tuberculosis. PLoS ONE 3:e1538
45. Esterhuyse MM, Linhart HG, Kaufmann SH (2012) Can the battle against tuberculosis gain from epigenetic research? Trends Microbiol 20:220-226
46. Fabre M, Hauck Y, Soler C, Koeck JL, van Ingen J, van Soolingen D, Vergnaud G, Pourcel C (2010) Molecular characteristics of ''Mycobacterium canettii'' the smooth Mycobacterium tuberculosis bacilli. Infect Genet Evol 10:1165-1173
47. Fenner L, Malla B, Ninet B, Dubuis O, Stucki D, Borrell S, Huna T, Bodmer T, Egger M, Gagneux S (2011) ''Pseudo-Beijing'': Evidence for convergent evolution in the direct repeat region of mycobacterium tuberculosis. PLoS One 6:e24737
48. Fenner L, Egger M, Bodmer T, Altpeter E, Zwahlen M, Jaton K, Pfyffer GE, Borrell S, Dubuis O, Bruderer T, Siegrist HH, Furrer H, Calmy A, Fehr J, Stalder JM, Ninet B, Bottger EC, Gagneux S (2012) Effect of mutation and genetic background on drug resistance in mycobacterium tuberculosis. Antimicrob Agents Chemother 56:3047-3053
49. Filliol I, Motiwala AS, Cavatore M, Qi W, Hernando Hazbon M, Bobadilla Del Valle M, Fyfe J, Garcia-Garcia L, Rastogi N, Sola C, Zozio T, Guerrero MI, Leon CI, Crabtree J, Angiuoli S, Eisenach KD, Durmaz R, Joloba ML, Rendon A, Sifuentes-Osornio J, Ponce de Leon A, Cave MD, Fleischmann R, Whittam TS, Alland D (2006) Global phylogeny of mycobacterium tuberculosis based on single nucleotide polymorphism (SNP) analysis: Insights into tuberculosis evolution, phylogenetic accuracy of oher DNA fingerprinting systems, and recommendations for a minimal standard SNP set. J Bacteriol 188:759-772
50. Fleischmann RD, Alland D, Eisen JA, Carpenter L, White O, Peterson J, DeBoy R, Dodson R, Gwinn M, Haft D, Hickey E, Kolonay JF, Nelson WC, Umayam LA, Ermolaeva M, Salzberg SL, Delcher A, Utterback T, Weidman J, Khouri H, Gill J, Mikula A, Bishai W, Jacobs Jr WR, Venter JC, Fraser CM (2002) Whole-genome comparison of mycobacterium tuberculosis clinical and laboratory strains. J Bacteriol 184:5479-5490
51. Flores L, Van T, Narayanan S, Deriemer K, Kato-Maeda M, Gagneux S (2007) Large sequence polymorphisms classify mycobacterium tuberculosis with ancestral spoligotyping patterns. J Clin Microbiol 45:3393-3395
52. Ford CB, Lin PL, Chase MR, Shah RR, Iartchouk O, Galagan J, Mohaideen N, Ioerger TR, Sacchettini JC, Lipsitch M, Flynn JL, Fortune SM (2011) Use of whole genome sequencing to estimate the mutation rate of mycobacterium tuberculosis during latent infection. Nat Genet 43:482-486
53. Frota CC, Hunt DM, Buxton RS, Rickman L, Hinds J, Kremer K, van Soolingen D, Colston MJ (2004) Genome structure in the vole bacillus, Mycobacterium microti, a member of the mycobacterium tuberculosis complex with a low virulence for humans. Microbiology 150:1519-1527
54. Gagneux S, Small PM (2007) Global phylogeography of mycobacterium tuberculosis and implications for tuberculosis product development. Lancet Infect Dis 7:328-337
55. Gagneux S, Burgos MV, DeRiemer K, Encisco A, Munoz S, Hopewell PC, Small PM, Pym AS (2006a) Impact of bacterial genetics on the transmission of isoniazid-resistant mycobacterium tuberculosis. PLoS Pathog 2:e61
56. Gagneux S, Deriemer K, Van T, Kato-Maeda M, de Jong BC, Narayanan S, Nicol M, Niemann S, Kremer K, Gutierrez MC, Hilty M, Hopewell PC, Small PM (2006b) Variable host-pathogen compatibility in mycobacterium tuberculosis. Proc Natl Acad Sci USA 103:2869-2873
57. Gandhi NR, Nunn P, Dheda K, Schaaf HS, Zignol M, van Soolingen D, Jensen P, Bayona J (2010) Multidrug-resistant and extensively drug-resistant tuberculosis: A threat to global control of tuberculosis. Lancet 375:1830-1843
58. Gao Q, Kripke KE, Saldanha AJ, Yan W, Holmes S, Small PM (2005) Gene expression diversity among Mycobacterium tuberculosis clinical isolates. Microbiology 151:5-14
59. Gardy JL, Johnston JC, Sui SJ, Cook VJ, Shah L, Brodkin E, Rempel S, Moore R, Zhao Y, Holt R, Varhol R, Birol I, Lem M, Sharma MK, Elwood K, Jones SJ, Brinkman FS, Brunham RC, Tang P (2011) Whole-genome sequencing and social-network analysis of a tuberculosis outbreak. N Engl J Med 364:730-739
60. Garnier T, Eiglmeier K, Camus JC, Medina N, Mansoor H, Pryor M, Duthoy S, Grondin S, Lacroix C, Monsempe C, Simon S, Harris B, Atkin R, Doggett J, Mayes R, Keating L, Wheeler PR, Parkhill J, Barrell BG, Cole ST, Gordon SV, Hewinson RG (2003) The complete genome sequence of mycobacterium bovis. Proc Natl Acad Sci USA 100:7877-7882
61. Georghiou SB, Magana M, Garfein RS, Catanzaro DG, Catanzaro A, Rodwell TC (2012) Evaluation of genetic mutations associated with Mycobacterium tuberculosis resistance to amikacin, kanamycin and capreomycin: A systematic review. PLoS One 7:e33275
62. Gordon SV, Brosch R, Billault A, Garnier T, Eiglmeier K, Cole ST (1999) Identification of variable regions in the genomes of tubercle bacilli using bacterial artificial chromosome arrays. Mol Microbiol 32:643-655
63. Gutacker MM, Mathema B, Soini H, Shashkina E, Kreiswirth BN, Graviss EA, Musser JM (2006) Single-nucleotide polymorphism-based population genetic analysis of mycobacterium tuberculosis strains from 4 geographic sites. J Infect Dis 193:121-128
64. Gutierrez C, Brisse S, Brosch R, Fabre M, Omais B, Marmiesse M, Supply P, Vincent V (2005) Ancient origin and gene mosaicism of the progenitor of mycobacterium tuberculosis. PLoS Pathogens 1:1-7
65. Hershberg R, Lipatov M, Small PM, Sheffer H, Niemann S, Homolka S, Roach JC, Kremer K, Petrov DA, Feldman MW, Gagneux S (2008) High functional diversity in mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol 6:e311
66. Heym B, Stavropoulos E, Honore N, Domenech P, Saint-Joanis B, Wilson TM, Collins DM, Colston MJ, Cole ST (1997) Effects of overexpression of the alkyl hydroperoxide reductase AhpC on the virulence and isoniazid resistance of mycobacterium tuberculosis. Infect Immun 65:1395-1401
67. Hirsh AE, Tsolaki AG, DeRiemer K, Feldman MW, Small PM (2004) Stable association between strains of mycobacterium tuberculosis and their human host populations. Proc Natl Acad Sci USA 101:4871-4876
68. Homolka S, Meyer CG, Hillemann D, Owusu-Dabo E, Adjei O, Horstmann RD, Browne EN, Chinbuah A, Osei I, Gyapong J, Kubica T, Ruesch-Gerdes S, Niemann S (2010a) Unequal distribution of resistance-conferring mutations among Mycobacterium tuberculosis and mycobacterium africanum strains from Ghana. Int J Med Microbiol 300:489-495
69. Homolka S, Niemann S, Russell DG, Rohde KH (2010b) Functional genetic diversity among Mycobacterium tuberculosis complex clinical isolates: Delineation of conserved core and lineage-specific transcriptomes during intracellular survival. PLoS Pathog 6:e1000988
70. Hughes AL, Friedman R, Murray M (2002) Genomewide pattern of synonymous nucleotide substitution in two complete genomes of mycobacterium tuberculosis. Emerg Infect Dis 8:1342-1346
71. Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, Kuijper S, Bunschoten A, Molhuizen H, Shaw R, Goyal M, van Embden J (1997) Simultaneous detection and strain differentiation of mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol 35:907-914
72. Kato-Maeda M, Bifani PJ, Kreiswirth BN, Small PM (2001a) The nature and consequence of genetic variability within mycobacterium tuberculosis. J Clin Invest 107:533-537
73. Kato-Maeda M, Rhee JT, Gingeras TR, Salamon H, Drenkow J, Smittipat N, Small PM (2001b) Comparing genomes within the species Mycobacterium tuberculosis. Genome Res 11:547-554
74. Kato-Maeda M, Metcalfe JZ, Flores L (2011) Genotyping of mycobacterium tuberculosis: Application in epidemiologic studies. Future Microbiol 6:203-216
75. Koeck JL, Fabre M, Simon F, Daffe M, Garnotel E, Matan AB, Gerome P, Bernatas JJ, Buisson Y, Pourcel C (2010) Clinical characteristics of the smooth tubercle bacilli ''Mycobacterium canettii'' infection suggest the existence of an environmental reservoir. Clin Microbiol Infect 17:1013-1019
76. Kwan CK, Ernst JD (2011) HIV and tuberculosis: A deadly human syndemic. Clin Microbiol Rev 24:351-376
77. Leung AS, Tran V, Wu Z, Yu X, Alexander DC, Gao GF, Zhu B, Liu J (2008) Novel genome polymorphisms in BCG vaccine strains and impact on efficacy. BMC Genomics 9:413
78. Liu X, Gutacker MM, Musser JM, Fu YX (2006) Evidence for recombination in mycobacterium tuberculosis. J Bacteriol 188:8169-8177
79. Malik AN, Godfrey-Faussett P (2005) Effects of genetic variability of mycobacterium tuberculosis strains on the presentation of disease. Lancet Infect Dis 5:174-183
80. Manca C, Tsenova L, Barry CE 3rd, Bergtold A, Freeman S, Haslett PA, Musser JM, Freedman VH, Kaplan G (1999) Mycobacterium tuberculosis CDC1551 induces a more vigorous host response in vivo and in vitro, but is not more virulent than other clinical isolates. J Immunol 162:6740-6746
81. McEvoy C, Cloete R, Muller B, Schurch A, van Helden P, Gagneux S, Warren R, Van Pittius NC (2012) Comparative analysis of mycobacterium tuberculosis PE and PPE genes reveals high sequence variation and an apparent absence of selective constraints. PLoS ONE 7:e30593
82. Mestre O, Luo T, Dos Vultos T, Kremer K, Murray A, Namouchi A, Jackson C, Rauzier J, Bifani P, Warren R, Rasolofo V, Mei J, Gao Q, Gicquel B (2011) Phylogeny of mycobacterium tuberculosis Beijing strains constructed from polymorphisms in genes involved in DNA replication, recombination and repair. PLoS One 6:e16020
83. Meyer CG, Scarisbrick G, Niemann S, Browne EN, Chinbuah MA, Gyapong J, Osei I, Owusu-Dabo E, Kubica T, Rusch-Gerdes S, Thye T, Horstmann RD (2008) Pulmonary tuberculosis: Virulence of mycobacterium africanum and relevance in HIV co-infection. Tuberculosis (Edinb) 88:482-489
84. Mitchison DA, Wallace JG, Bhatia AL, Selkon JB, Subbaiah TV, Lancaster MC (1960) A comparison of the virulence in guinea-pigs of South Indian and British tubercle bacilli. Tubercle 41:1-22
85. Mostowy S, Cousins D, Brinkman J, Aranaz A, Behr MA (2002) Genomic deletions suggest a phylogeny for the mycobacterium tuberculosis complex. J Infect Dis 186:74-80
86. Mostowy S, Cousins D, Behr MA (2004a) Genomic interrogation of the dassie bacillus reveals it as a unique RD1 mutant within the mycobacterium tuberculosis complex. J Bacteriol 186:104-109
87. Mostowy S, Onipede A, Gagneux S, Niemann S, Kremer K, Desmond EP, Kato-Maeda M, Behr M (2004b) Genomic analysis distinguishes Mycobacterium africanum. J Clin Microbiol 42:3594-3599
88. Mueller B, Borrell S, Rose G, Gagneux S (2012) The heterogeneous evolution of multidrugresistant mycobacterium tuberculosis. Trends Genet (in press
89. Musser JM, Amin A, Ramaswamy S (2000) Negligible genetic diversity of mycobacterium tuberculosis host immune system protein targets: Evidence of limited selective pressure. Genetics 155:7-16
90. Namouchi A, Didelot X, Schock U, Gicquel B, Rocha EP (2012) After the bottleneck: Genomewide diversification of the mycobacterium tuberculosis complex by mutation, recombination, and natural selection. Genome Res 22:721-734
91. Newton SM, Smith RJ, Wilkinson KA, Nicol MP, Garton NJ, Staples KJ, Stewart GR, Wain JR, Martineau AR, Fandrich S, Smallie T, Foxwell B, Al-Obaidi A, Shafi J, Rajakumar K, Kampmann B, Andrew PW, Ziegler-Heitbrock L, Barer MR, Wilkinson RJ (2006) A deletion defining a common Asian lineage of mycobacterium tuberculosis associates with immune subversion. Proc Natl Acad Sci USA 103:15594-15598
92. Nicol MP, Wilkinson RJ (2008) The clinical consequences of strain diversity in mycobacterium tuberculosis. Trans R Soc Trop Med Hyg 102:955-965
93. Niemann S, Richter E, Rusch-Gerdes S (2002) Biochemical and genetic evidence for the transfer of mycobacterium tuberculosis subsp. Caprae Aranaz et al. 1999 to the species Mycobacterium bovis Karlson and Lessel 1970 (approved lists 1980) as Mycobacterium bovis subsp. caprae comb. nov. Int J Syst Evol Microbiol 52:433-436
94. Niemann S, Koser CU, Gagneux S, Plinke C, Homolka S, Bignell H, Carter RJ, Cheetham RK, Cox A, Gormley NA, Kokko-Gonzales P, Murray LJ, Rigatti R, Smith VP, Arends FP, Cox HS, Smith G, Archer JA (2009) Genomic diversity among drug sensitive and multidrug resistant isolates of mycobacterium tuberculosis with identical DNA fingerprints. PLoS ONE 4:e7407
95. Parwati I, van Crevel R, van Soolingen D (2010) Possible underlying mechanisms for successful emergence of the mycobacterium tuberculosis Beijing genotype strains. Lancet Infect Dis 10:103-111
96. Pearson T, Busch JD, Ravel J, Read TD, Rhoton SD, U'Ren JM, Simonson TS, Kachur SM, Leadem RR, Cardon ML, Van Ert MN, Huynh LY, Fraser CM, Keim P (2004) Phylogenetic discovery bias in Bacillus anthracis using single-nucleotide polymorphisms from wholegenome sequencing. Proc Natl Acad Sci USA 101:13536-13541
97. Phillips PC (2008) Epistasis-the essential role of gene interactions in the structure and evolution of genetic systems. Nat Rev Genet 9:855-867
98. Portevin D, Gagneux S, Comas I, Young D (2011) Human macrophage responses to clinical isolates from the mycobacterium tuberculosis complex discriminate between ancient and modern lineages. PLoS Pathog 7:e1001307
99. Rajakumar K, Shafi J, Smith RJ, Stabler RA, Andrew PW, Modha D, Bryant G, Monk P, Hinds J, Butcher PD, Barer MR (2004) Use of genome level-informed PCR as a new investigational approach for analysis of outbreak-associated mycobacterium tuberculosis isolates. J Clin Microbiol 42:1890-1896
100. Reed MB, Domenech P, Manca C, Su H, Barczak AK, Kreiswirth BN, Kaplan G, Barry CE 3rd (2004) A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431:84-87
101. Rodrigo T, Cayla JA, Garcia de Olalla P, Galdos-Tanguis H, Jansa JM, Miranda P, Brugal T (1997) Characteristics of tuberculosis patients who generate secondary cases. Int J Tuberc Lung Dis 1:352-357
102. Rosas-Magallanes V, Deschavanne P, Quintana-Murci L, Brosch R, Gicquel B, Neyrolles O (2006) Horizontal transfer of a virulence operon to the ancestor of mycobacterium tuberculosis. Mol Biol Evol 23:1129-1135
103. Sandegren L, Groenheit R, Koivula T, Ghebremichael S, Advani A, Castro E, Pennhag A, Hoffner S, Mazurek J, Pawlowski A, Kan B, Bruchfeld J, Melefors O, Kallenius G (2011) Genomic Stability over 9 Years of an isoniazid resistant mycobacterium tuberculosis outbreak strain in Sweden. PLoS One 6:e16647
104. Sandgren A, Strong M, Muthukrishnan P, Weiner BK, Church GM, Murray MB (2009) Tuberculosis drug resistance mutation database. PLoS Med 6:e2
105. Saunders NJ, Trivedi UH, Thomson ML, Doig C, Laurenson IF, Blaxter ML (2011) Deep resequencing of serial sputum isolates of mycobacterium tuberculosis during therapeutic failure due to poor compliance reveals stepwise mutation of key resistance genes on an otherwise stable genetic background. J Infect 62:212-217
106. Schurch AC, Kremer K, Kiers A, Daviena O, Boeree MJ, Siezen R, Smith NH, van Soolingen D (2009) The tempo and mode of molecular evolution of mycobacterium tuberculosis at patientto-patient scale. Infect Genet Evol 10:108-114
107. Schurch AC, Kremer K, Daviena O, Kiers A, Boeree MJ, Siezen RJ, van Soolingen D (2010) High resolution typing by integration of genome sequencing data in a large tuberculosis cluster. J Clin Microbiol 48:3403-3406
108. Shcherbakov D, Akbergenov R, Matt T, Sander P, Andersson DI, Bottger EC (2010) Directed mutagenesis of mycobacterium smegmatis 16S rRNA to reconstruct the in vivo evolution of aminoglycoside resistance in mycobacterium tuberculosis. Mol Microbiol 77:830-840
109. Sherman DR, Mdluli K, Hickey MJ, Arain TM, Morris SL, Barry CE 3rd, Stover CK (1996) Compensatory ahpC gene expression in isoniazid-resistant mycobacterium tuberculosis. Science 272:1641-1643
110. Smith NH, Kremer K, Inwald J, Dale J, Driscoll JR, Gordon SV, van Soolingen D, Glyn Hewinson R, Maynard Smith J (2005) Ecotypes of the mycobacterium tuberculosis complex. J Theor Biol 239:220-225
111. Smith NH, Hewinson RG, Kremer K, Brosch R, Gordon SV (2009) Myths and misconceptions: The origin and evolution of mycobacterium tuberculosis. Nat Rev Microbiol 7:537-544
112. Sorek R, Cossart P (2010) Prokaryotic transcriptomics: A new view on regulation, physiology and pathogenicity. Nat Rev Genet 11:9-16
113. Sreevatsan S, Pan X, Stockbauer KE, Connell ND, Kreiswirth BN, Whittam TS, Musser JM (1997) Restricted structural gene polymorphism in the mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc Natl Acad Sci USA 94:9869-9874
114. Stucki D, Malla B, Hostettler S, Huna T, Feldmann J, Yeboah-Manu D, Borrell S, Fenner L, Comas I, Coscolla M, Gagneux S (2012) Two new rapid SNP-typing methods for classifying Mycobacterium tuberculosis complex into the main phylogenetic lineages. PLoS ONE 7:e41253
115. Supply P, Warren RM, Banuls AL, Lesjean S, Van Der Spuy GD, Lewis LA, Tibayrenc M, Van Helden PD, Locht C (2003) Linkage disequilibrium between minisatellite loci supports clonal evolution of mycobacterium tuberculosis in a high tuberculosis incidence area. Mol Microbiol 47:529-538
116. Supply P, Allix C, Lesjean S, Cardoso-Oelemann M, Rusch-Gerdes S, Willery E, Savine E, de Haas P, van Deutekom H, Roring S, Bifani P, Kurepina N, Kreiswirth B, Sola C, Rastogi N, Vatin V, Gutierrez MC, Fauville M, Niemann S, Skuce R, Kremer K, Locht C, van Soolingen D (2006) Proposal for standardization of optimized mycobacterial Interspersed Repetitive Unit-Variable Number Tandem Repeat typing of mycobacterium tuberculosis. J Clin Microbiol 44:4498-4510
117. Talarico S, Cave MD, Marrs CF, Foxman B, Zhang L, Yang Z (2005) Variation of the mycobacterium tuberculosis PE-PGRS 33 gene among clinical isolates. J Clin Microbiol 43:4954-4960
118. Talarico S, Zhang L, Marrs CF, Foxman B, Cave MD, Brennan MJ, Yang Z (2008) Mycobacterium tuberculosis PE-PGRS16 and PE-PGRS26 genetic polymorphism among clinical isolates. Tuberculosis (Edinb) 88:283-294
119. Toprak E, Veres A, Michel JB, Chait R, Hartl DL, Kishony R (2012) Evolutionary paths to antibiotic resistance under dynamically sustained drug selection. Nat Genet 44:101-105
120. Trindade S, Sousa A, Xavier KB, Dionisio F, Ferreira MG, Gordo I (2009) Positive epistasis drives the acquisition of multidrug resistance. PLoS Genet 5:e1000578
121. Tsolaki AG, Hirsh AE, DeRiemer K, Enciso JA, Wong MZ, Hannan M, Goguet de la Salmoniere YO, Aman K, Kato-Maeda M, Small PM (2004) Functional and evolutionary genomics of mycobacterium tuberculosis: Insights from genomic deletions in 100 strains. Proc Natl Acad Sci USA 101:4865-4870
122. Tsolaki AG, Gagneux S, Pym AS, Goguet de la Salmoniere YO, Kreiswirth BN, Van Soolingen D, Small PM (2005) Genomic deletions classify the Beijing/W strains as a distinct genetic lineage of mycobacterium tuberculosis. J Clin Microbiol 43:3185-3191
123. Valway SE, Sanchez MP, Shinnick TF, Orme I, Agerton T, Hoy D, Jones JS, Westmoreland H, Onorato IM (1998) An outbreak involving extensive transmission of a virulent strain of mycobacterium tuberculosis. N Engl J Med 338:633-639
124. van Embden JD, Cave MD, Crawford JT, Dale JW, Eisenach KD, Gicquel B, Hermans P, Martin C, McAdam R, Shinnick TM et al (1993) Strain identification of mycobacterium tuberculosis by DNA fingerprinting: Recommendations for a standardized methodology. J Clin Microbiol 31:406-409
125. van Ingen J, Rahim Z, Mulder A, Boeree MJ, Simeone R, Brosch R, van Soolingen D (2012) Characterization of mycobacterium orygis as M tuberculosis complex subspecies. Emerg Infect Dis 18:653-655
126. van Soolingen D, Qian L, de Haas PE, Douglas JT, Traore H, Portaels F, Qing HZ, Enkhsaikan D, Nymadawa P, van Embden JD (1995) Predominance of a single genotype of mycobacterium tuberculosis in countries of east Asia. J Clin Microbiol 33:3234-3238
127. van Soolingen D, Hoogenboezem T, de Haas PE, Hermans PW, Koedam MA, Teppema KS, Brennan PJ, Besra GS, Portaels F, Top J, Schouls LM, van Embden JD (1997) A novel pathogenic taxon of the mycobacterium tuberculosis complex, Canetti: Characterization of an exceptional isolate from Africa. Int J Syst Bacteriol 47:1236-1245
128. Veyrier F, Pletzer D, Turenne C, Behr MA (2009) Phylogenetic detection of horizontal gene transfer during the step-wise genesis of mycobacterium tuberculosis. BMC Evol Biol 9:196
129. Ward H, Perron GG, Maclean RC (2009) The cost of multiple drug resistance in Pseudomonas aeruginosa. J Evol Biol 22:997-1003
130. Weiner B, Gomez J, Victor TC, Warren RM, Sloutsky A, Plikaytis BB, Posey JE, van Helden PD, Gey van Pittius NC, Koehrsen M, Sisk P, Stolte C, White J, Gagneux S, Birren B, Hung D, Murray M, Galagan J (2012) Independent large scale duplications in multiple M tuberculosis lineages overlapping the same genomic region. PLoS One 7:e26038
131. Weinreich DM, Watson RA, Chao L (2005) Perspective: Sign epistasis and genetic constraint on evolutionary trajectories. Evolution 59:1165-1174
132. Werngren J, Hoffner SE (2003) Drug-susceptible mycobacterium tuberculosis Beijing genotype does not develop mutation-conferred resistance to rifampin at an elevated rate. J Clin Microbiol 41:1520-1524
133. Wirth T, Hildebrand F, Allix-Beguec C, Wolbeling F, Kubica T, Kremer K, van Soolingen D, Rusch-Gerdes S, Locht C, Brisse S, Meyer A, Supply P, Niemann S (2008) Origin, spread and demography of the mycobacterium tuberculosis complex. PLoS Pathog 4:e1000160
134. Young DB, Perkins MD, Duncan K, Barry CE (2008) Confronting the scientific obstacles to global control of tuberculosis. J Clin Invest 118:1255-1265
135. Zhang Y, Yew WW (2009) Mechanisms of drug resistance in mycobacterium tuberculosis. Int J Tuberc Lung Dis 13:1320-1330
136. Zhang M, Gong J, Yang Z, Samten B, Cave MD, Barnes PF (1999) Enhanced capacity of a widespread strain of mycobacterium tuberculosis to grow in human macrophages. J Infect Dis 179:1213-1217