Significance of the Identification in the Horn of Africa of an Exceptionally Deep Branching Mycobacterium tuberculosis Clade

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Blouin, Yann ^a,b   Hauck, Yolande ^a,b   Soler, Charles ^c   Fabre, Michel ^c   Vong, Rithy ^c   Dehan, Céline ^d   Cazajous, Géraldine ^d   Massoure, Pierre Laurent ^e   Kraemer, Philippe ^e   Jenkins, Akinbowale ^f   Garnotel, Eric ^e   Pourcel, Christine ^a,b   Vergnaud, Gilles ^a,b,g  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b CNRS   (France)

^c PERCY MILITARY HOSPITAL   (France)

^d Hôpital Militaire Bouffard   (Djibouti)

^e LAVERAN MILITARY TEACHING HOSPITAL   (France)

^f UNIVERSITY OF PRETORIA   (South Africa)

^g DGA/MRIS Mission Pour la Recherche et L'Innovation Scientifique   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AFRICA; ARTICLE; BACTERIAL GENETICS; BACTERIAL GENOME; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; CLADISTICS; CONTROLLED STUDY; DEEP BRANCHING LINEAGE; GENE DELETION; GENE MUTATION; GENETIC DISTANCE; GENETIC VARIABILITY; GENOTYPE; GENOTYPING TECHNIQUE; MULTIPLE LOCUS VARIABLE NUMBER OF TANDEM REPEAT ANALYSIS; MYCOBACTERIUM AFRICANUM; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; SPOLIGOTYPING;

ANIMALS; CLUSTER ANALYSIS; DJIBOUTI; GENES, BACTERIAL; GENOTYPE; HUMANS; KENYA; MINISATELLITE REPEATS; MODELS, GENETIC; MULTILOCUS SEQUENCE TYPING; MUTATION; MYCOBACTERIUM TUBERCULOSIS; PHYLOGENY; PHYLOGEOGRAPHY; POLYMORPHISM, SINGLE NUCLEOTIDE; SOMALIA; SUDAN; TUBERCULOSIS;

MYCOBACTERIUM TUBERCULOSIS; MYCOBACTERIUM TUBERCULOSIS COMPLEX;

EID: 84871652718     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0052841     Document Type: Article

References (76)

1. Rothschild BM, Martin LD, Lev G, Bercovier H, Bar-Gal GK, et al. (2001) Mycobacterium tuberculosis complex DNA from an extinct bison dated 17,000 years before the present. Clin Infect Dis 33: 305-311.
2. Hershkovitz I, Donoghue HD, Minnikin DE, Besra GS, Lee OY, et al. (2008) Detection and molecular characterization of 9,000-year-old Mycobacterium tuberculosis from a Neolithic settlement in the Eastern Mediterranean. PLoS One 3: e3426.
3. Crubezy E, Ludes B, Poveda JD, Clayton J, Crouau-Roy B, et al. (1998) Identification of Mycobacterium DNA in an Egyptian Pott's disease of 5,400 years old. C R Acad Sci III 321: 941-951.
4. Salo WL, Aufderheide AC, Buikstra J, Holcomb TA, (1994) Identification of Mycobacterium tuberculosis DNA in a pre-Columbian Peruvian mummy. Proc Natl Acad Sci U S A 91: 2091-2094.
5. Zink AR, Sola C, Reischl U, Grabner W, Rastogi N, et al. (2003) Characterization of Mycobacterium tuberculosis complex DNAs from Egyptian mummies by spoligotyping. J Clin Microbiol 41: 359-367.
6. Nerlich AG, Haas CJ, Zink A, Szeimies U, Hagedorn HG, (1997) Molecular evidence for tuberculosis in an ancient Egyptian mummy. Lancet 350: 1404.
7. Taylor GM, Goyal M, Legge AJ, Shaw RJ, Young D, (1999) Genotypic analysis of Mycobacterium tuberculosis from medieval human remains. Microbiology 145 (Pt 4):: 899-904.
8. Mays S, Taylor GM, Legge AJ, Young DB, Turner-Walker G, (2001) Paleopathological and biomolecular study of tuberculosis in a medieval skeletal collection from England. Am J Phys Anthropol 114: 298-311.
9. Wilbur AK, Bouwman AS, Stone AC, Roberts CA, Pfister LA, et al. (2009) Deficiencies and challenges in the study of ancient tuberculosis DNA. Journal of Archaeological Science 36: 1990-1997.
10. Brosch R, Gordon SV, Marmiesse M, Brodin P, Buchrieser C, et al. (2002) A new evolutionary scenario for the Mycobacterium tuberculosis complex. Proc Natl Acad Sci U S A 99: 3684-3689.
11. Fabre M, Koeck JL, Le Fleche P, Simon F, Herve V, et al. (2004) High genetic diversity revealed by variable-number tandem repeat genotyping and analysis of hsp65 gene polymorphism in a large collection of "Mycobacterium canettii" strains indicates that the M. tuberculosis complex is a recently emerged clone of "M. canettii". J Clin Microbiol 42: 3248-3255.
12. Gutierrez MC, Brisse S, Brosch R, Fabre M, Omais B, et al. (2005) Ancient origin and gene mosaicism of the progenitor of Mycobacterium tuberculosis. PLoS Pathog 1: e5.
13. Fabre M, Hauck Y, Soler C, Koeck JL, van Ingen J, et al. (2010) Molecular characteristics of "Mycobacterium canettii" the smooth Mycobacterium tuberculosis bacilli. Infect Genet Evol 10: 1165-1173.
14. Comas I, Chakravartti J, Small PM, Galagan J, Niemann S, et al. (2010) Human T cell epitopes of Mycobacterium tuberculosis are evolutionarily hyperconserved. Nat Genet 42: 498-503.
15. 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.
16. Veyrier FJ, Dufort A, Behr MA, (2011) The rise and fall of the Mycobacterium tuberculosis genome. Trends Microbiol 19: 156-161.
17. Koeck JL, Fabre M, Simon F, Daffe M, Garnotel E, et al. (2010) Clinical characteristics of the smooth tubercle bacilli 'Mycobacterium canettii' infection suggest the existence of an environmental reservoir. Clin Microbiol Infect.
18. Smith NH, Kremer K, Inwald J, Dale J, Driscoll JR, et al. (2006) Ecotypes of the Mycobacterium tuberculosis complex. J Theor Biol 239: 220-225.
19. Namouchi A, Didelot X, Schock U, Gicquel B, Rocha EP, (2012) After the bottleneck: Genome-wide diversification of the Mycobacterium tuberculosis complex by mutation, recombination, and natural selection. Genome Res.
20. Kamerbeek J, Schouls L, Kolk A, van Agterveld M, van Soolingen D, et al. (1997) Simultaneous detection and strain differentiation of Mycobacterium tuberculosis for diagnosis and epidemiology. J Clin Microbiol 35: 907-914.
21. Kremer K, van Soolingen D, Frothingham R, Haas WH, Hermans PW, et al. (1999) Comparison of methods based on different molecular epidemiological markers for typing of Mycobacterium tuberculosis complex strains: interlaboratory study of discriminatory power and reproducibility. J Clin Microbiol 37: 2607-2618.
22. Supply P, Allix C, Lesjean S, Cardoso-Oelemann M, Rusch-Gerdes S, et al. (2006) Proposal for standardization of optimized mycobacterial interspersed repetitive unit-variable-number tandem repeat typing of Mycobacterium tuberculosis. J Clin Microbiol 44: 4498-4510.
23. Filliol I, Motiwala AS, Cavatore M, Qi W, Hernando Hazbon M, et al. (2006) Global Phylogeny of Mycobacterium tuberculosis Based on Single Nucleotide Polymorphism (SNP) Analysis: Insights into Tuberculosis Evolution, Phylogenetic Accuracy of Other DNA Fingerprinting Systems, and Recommendations for a Minimal Standard SNP Set. J Bacteriol 188: 759-772.
24. Hershberg R, Lipatov M, Small PM, Sheffer H, Niemann S, et al. (2008) High functional diversity in Mycobacterium tuberculosis driven by genetic drift and human demography. PLoS Biol 6: e311.
25. 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.
26. Marmiesse M, Brodin P, Buchrieser C, Gutierrez C, Simoes N, et al. (2004) Macro-array and bioinformatic analyses reveal mycobacterial 'core' genes, variation in the ESAT-6 gene family and new phylogenetic markers for the Mycobacterium tuberculosis complex. Microbiology 150: 483-496.
27. Smith NH, Upton P, (2011) Naming spoligotype patterns for the RD9-deleted lineage of the Mycobacterium tuberculosis complex;Infect Genet Evolwww.Mbovis.org.
28. Shabbeer A, Cowan LS, Ozcaglar C, Rastogi N, Vandenberg SL, et al. (2012) TB-Lineage: An online tool for classification and analysis of strains of Mycobacterium tuberculosis complex. Infect Genet Evol 12: 789-797.
29. Ledru S, Cauchoix B, Yameogo M, Zoubga A, Lamande-Chiron J, et al. (1996) Impact of short-course therapy on tuberculosis drug resistance in South-West Burkina Faso. Tuber Lung Dis 77: 429-436.
30. Intemann CD, Thye T, Niemann S, Browne EN, Amanua Chinbuah M, et al. (2009) Autophagy gene variant IRGM-261T contributes to protection from tuberculosis caused by Mycobacterium tuberculosis but not by M. africanum strains. PLoS Pathog 5: e1000577.
31. Gomgnimbou MK, Refregier G, Diagbouga SP, Adama S, Kabore A, et al. (2012) Spoligotyping of Mycobacterium africanum, Burkina Faso. Emerg Infect Dis 18: 117-119.
32. Bentley SD, Comas I, Bryant JM, Walker D, Smith NH, et al. (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.
33. van Ingen J, Rahim Z, Mulder A, Boeree MJ, Simeone R, et al. (2012) Characterization of Mycobacterium orygis as M. tuberculosis Complex Subspecies. Emerg Infect Dis 18: 653-655.
34. Kapur V, Whittam TS, Musser JM, (1994) Is Mycobacterium tuberculosis 15,000 years old? J Infect Dis 170: 1348-1349.
35. Sreevatsan S, Pan X, Stockbauer KE, Connell ND, Kreiswirth BN, et al. (1997) Restricted structural gene polymorphism in the Mycobacterium tuberculosis complex indicates evolutionarily recent global dissemination. Proc Natl Acad Sci U S A 94: 9869-9874.
36. Wirth T, Hildebrand F, Allix-Beguec C, Wolbeling F, Kubica T, et al. (2008) Origin, spread and demography of the Mycobacterium tuberculosis complex. PLoS Pathog 4: e1000160.
37. Fagundes NJ, Ray N, Beaumont M, Neuenschwander S, Salzano FM, et al. (2007) Statistical evaluation of alternative models of human evolution. Proc Natl Acad Sci U S A 104: 17614-17619.
38. Li JZ, Absher DM, Tang H, Southwick AM, Casto AM, et al. (2008) Worldwide human relationships inferred from genome-wide patterns of variation. Science 319: 1100-1104.
39. Schlebusch CM, Skoglund P, Sjodin P, Gattepaille LM, Hernandez D, et al. (2012) Genomic variation in seven Khoe-San groups reveals adaptation and complex African history. Science 338: 374-379.
40. Mellars P, (2006) Going east: new genetic and archaeological perspectives on the modern human colonization of Eurasia. Science 313: 796-800.
41. Cohan FM, (2002) What are bacterial species? Annu Rev Microbiol 56: 457-487.
42. Cohan FM, Koeppel AF, (2008) The origins of ecological diversity in prokaryotes. Curr Biol 18: R1024-1034.
43. Godreuil S, Renaud F, Choisy M, Depina JJ, Garnotel E, et al. (2009) Highly structured genetic diversity of the Mycobacterium tuberculosis population in Djibouti. Clin Microbiol Infect.
44. Demay C, Liens B, Burguiere T, Hill V, Couvin D, et al. (2012) SITVITWEB- A publicly available international multimarker database for studying Mycobacterium tuberculosis genetic diversity and molecular epidemiology. Infect Genet Evol 12: 755-766.
45. 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.
46. Helal ZH, Ashour MS, Eissa SA, Abd-Elatef G, Zozio T, et al. (2009) Unexpectedly high proportion of ancestral Manu genotype Mycobacterium tuberculosis strains cultured from tuberculosis patients in Egypt. J Clin Microbiol 47: 2794-2801.
47. Viana-Niero C, Gutierrez C, Sola C, Filliol I, Boulahbal F, et al. (2001) Genetic diversity of Mycobacterium africanum clinical isolates based on IS6110-restriction fragment length polymorphism analysis, spoligotyping, and variable number of tandem DNA repeats. J Clin Microbiol 39: 57-65.
48. Le Flèche P, Fabre M, Denoeud F, Koeck JL, Vergnaud G, (2002) High resolution, on-line identification of strains from the Mycobacterium tuberculosis complex based on tandem repeat typing. BMC Microbiol 2: 37.
49. Thomas SK, Iravatham CC, Moni BH, Kumar A, Archana BV, et al. (2011) Modern and ancestral genotypes of Mycobacterium tuberculosis from Andhra Pradesh, India. PLoS One 6: e27584.
50. Wan K, Liu J, Hauck Y, Zhang Y, Zhao X, et al. (2011) Investigation on Mycobacterium tuberculosis diversity in China and the origin of the Beijing clade. PLoS One 6: e29190.
51. Deshayes C, Perrodou E, Euphrasie D, Frapy E, Poch O, et al. (2008) Detecting the molecular scars of evolution in the Mycobacterium tuberculosis complex by analyzing interrupted coding sequences. BMC Evol Biol 8: 78.
52. Gardy JL, Johnston JC, Ho Sui SJ, Cook VJ, Shah L, et al. (2011) Whole-genome sequencing and social-network analysis of a tuberculosis outbreak. N Engl J Med 364: 730-739.
53. Zumarraga M, Bigi F, Alito A, Romano MI, Cataldi A, (1999) A 12.7 kb fragment of the Mycobacterium tuberculosis genome is not present in Mycobacterium bovis. Microbiology 145 (Pt 4):: 893-897.
54. Ford CB, Lin PL, Chase MR, Shah RR, Iartchouk O, et al. (2011) Use of whole genome sequencing to estimate the mutation rate of Mycobacterium tuberculosis during latent infection. Nat Genet 43: 482-486.
55. Kibiki GS, Mulder B, Dolmans WM, de Beer JL, Boeree M, et al. (2007) M. tuberculosis genotypic diversity and drug susceptibility pattern in HIV-infected and non-HIV-infected patients in northern Tanzania. BMC Microbiol 7: 51.
56. Al-Hajoj SA, Zozio T, Al-Rabiah F, Mohammad V, Al-Nasser M, et al. (2007) First insight into the population structure of Mycobacterium tuberculosis in Saudi Arabia. J Clin Microbiol 45: 2467-2473.
57. Brudey K, Driscoll JR, Rigouts L, Prodinger WM, Gori A, et al. (2006) Mycobacterium tuberculosis complex genetic diversity: mining the fourth international spoligotyping database (SpolDB4) for classification, population genetics and epidemiology. BMC Microbiol 6: 23.
58. Flores L, Van T, Narayanan S, Deriemer K, Kato-Maeda M, et al. (2007) Large Sequence Polymorphisms Classify Mycobacterium tuberculosis Strains with Ancestral Spoligotyping Patterns. J Clin Microbiol 45: 3393-3395.
59. Asiimwe BB, Ghebremichael S, Kallenius G, Koivula T, Joloba ML, (2008) Mycobacterium tuberculosis spoligotypes and drug susceptibility pattern of isolates from tuberculosis patients in peri-urban Kampala, Uganda. BMC Infect Dis 8: 101.
60. Eldholm V, Matee M, Mfinanga SG, Heun M, Dahle UR, (2006) A first insight into the genetic diversity of Mycobacterium tuberculosis in Dar es Salaam, Tanzania, assessed by spoligotyping. BMC Microbiol 6: 76.
61. Ferdinand S, Sola C, Chanteau S, Ramarokoto H, Rasolonavalona T, et al. (2005) A study of spoligotyping-defined Mycobacterium tuberculosis clades in relation to the origin of peopling and the demographic history in Madagascar. Infect Genet Evol 5: 340-348.
62. Mulenga C, Shamputa IC, Mwakazanga D, Kapata N, Portaels F, et al. (2010) Diversity of Mycobacterium tuberculosis genotypes circulating in Ndola, Zambia. BMC Infect Dis 10: 177.
63. Viegas SO, Machado A, Groenheit R, Ghebremichael S, Pennhag A, et al. (2010) Molecular diversity of Mycobacterium tuberculosis isolates from patients with pulmonary tuberculosis in Mozambique. BMC Microbiol 10: 195.
64. Stavrum R, Mphahlele M, Ovreas K, Muthivhi T, Fourie PB, et al. (2009) High diversity of Mycobacterium tuberculosis genotypes in South Africa and preponderance of mixed infections among ST53 isolates. J Clin Microbiol 47: 1848-1856.
65. Sharaf Eldin GS, Fadl-Elmula I, Ali MS, Ali AB, Salih AL, et al. (2011) Tuberculosis in Sudan: a study of Mycobacterium tuberculosis strain genotype and susceptibility to anti-tuberculosis drugs. BMC Infect Dis 11: 219.
66. de Jong BC, Antonio M, Awine T, Ogungbemi K, de Jong YP, et al. (2009) Use of spoligotyping and large sequence polymorphisms to study the population structure of the Mycobacterium tuberculosis complex in a cohort study of consecutive smear-positive tuberculosis cases in The Gambia. J Clin Microbiol 47: 994-1001.
67. Weiner B, Gomez J, Victor TC, Warren RM, Sloutsky A, et al. (2012) Independent large scale duplications in multiple M. tuberculosis lineages overlapping the same genomic region. PLoS One 7: e26038.
68. Ford C, Yusim K, Ioerger T, Feng S, Chase M, et al. (2012) Mycobacterium tuberculosis- Heterogeneity revealed through whole genome sequencing. Tuberculosis (Edinb) 92: 194-201.
69. Uplekar S, Heym B, Friocourt V, Rougemont J, Cole ST, (2011) Comparative genomics of esx genes from clinical isolates of Mycobacterium tuberculosis provides evidence for gene conversion and epitope variation. Infect Immun 79: 4042-4049.
70. Buu TN, Huyen MN, Lan NT, Quy HT, Hen NV, et al. (2009) The Beijing genotype is associated with young age and multidrug-resistant tuberculosis in rural Vietnam. Int J Tuberc Lung Dis 13: 900-906.
71. MLVAbank website. Available: http://mlva.u-psud.fr. Accessed 2012 Nov 29.
72. SITVITWEB. Available: http://www.pasteur-guadeloupe.fr:8081/SITVIT_ONLINE/. Accessed 2012 Nov 29.
73. Tsolaki AG, Gagneux S, Pym AS, Goguet de la Salmoniere YO, Kreiswirth BN, et al. (2005) Genomic deletions classify the Beijing/W strains as a distinct genetic lineage of Mycobacterium tuberculosis. J Clin Microbiol 43: 3185-3191.
74. NCBI Sequence Read Archive. Available: http://www.ncbi.nlm.nih.gov/sra. Accessed 2012 Nov 29.
75. The Broad institute website. Available: http://www.broadinstitute.org/. Accessed 2012 Nov 29.
76. ENA project accession ERP001885. Available: http://www.ebi.ac.uk/ena/data/view/ERP001885. Accessed 2012 Nov 29.