1887
No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.

Mycobacterial Pathogenomics and Evolution

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.
  • XML
    192.37 Kb
  • HTML
    198.32 Kb
  • PDF
    521.65 Kb
  • Authors: Daria Bottai1, Timothy P. Stinear2, Philip Supply3, Roland Brosch4
  • Editors: Graham F. Hatfull5, William R. Jacobs Jr.6
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Dipartimento di Ricerca Traslazionale e delle Nuove Tecnologie in Medicina e Chirurgia, Università di Pisa, Pisa, Italy; 2: Department of Microbiology and Immunology, University of Melbourne, Parkville, Australia; 3: CNRS UMR 8204; INSERM, U1019; Center for Infection and Immunity of Lille, Institut Pasteur de Lille; and Université Lille Nord de France, Lille, France; 4: Institut Pasteur, Unit for Integrated Mycobacterial Pathogenomics, Paris, France; 5: University of Pittsburgh, Pittsburgh, PA 15260; 6: Howard Hughes Medical Institute, Albert Einstein College of Medicine, Bronx, NY 10461
    • Source: microbiolspec January 2014 vol. 2 no. 1 doi:10.1128/microbiolspec.MGM2-0025-2013
  • Received 03 September 2013 Accepted 12 September 2013 Published 31 January 2014
  • Roland Brosch, [email protected]
image of Mycobacterial Pathogenomics and Evolution
    Preview this microbiology spectrum article:
    Preview Magnify
    Zoom in
    Zoomout

    Mycobacterial Pathogenomics and Evolution, Page 1 of 2

    | /docserver/preview/fulltext/microbiolspec/2/1/MGM2-0025-2013-1.gif /docserver/preview/fulltext/microbiolspec/2/1/MGM2-0025-2013-2.gif

  • Abstract:

    Most mycobacterial species are harmless saprophytes, often found in aquatic environments. A few species seem to have evolved from this pool of environmental mycobacteria into major human pathogens, such as , the agent of tuberculosis, , the leprosy bacillus, and , the agent of Buruli ulcer. While the pathogenicity of relates to the acquisition of a large plasmid encoding a polyketide-derived toxin, the molecular mechanisms by which or have evolved to cause disease are complex and involve the interaction between the pathogen and the host.

    Here we focus on and closely related mycobacteria and discuss insights gained from recent genomic and functional studies. Comparison of genome data with sequences from nontuberculous mycobacteria, such as or , provides a perception of the more distant evolution of , while the recently accomplished genome sequences of multiple tubercle bacilli with smooth colony morphology, named , have allowed the ancestral gene pool of tubercle bacilli to be estimated. The resulting findings are instrumental for our understanding of the pathogenomic evolution of tuberculosis-causing mycobacteria. Comparison of virulent and attenuated members of the complex has further contributed to identification of a specific secretion pathway, named ESX or Type VII secretion. The molecular machines involved are key elements for mycobacterial pathogenicity, strongly influencing the ability of to cope with the immune defense mounted by the host.

  • Citation: Bottai D, Stinear T, Supply P, Brosch R. 2014. Mycobacterial Pathogenomics and Evolution. Microbiol Spectrum 2(1):MGM2-0025-2013. doi:10.1128/microbiolspec.MGM2-0025-2013.

References

1. Stackebrandt E, Rainey FA, WardRainey NL. 1997. Proposal for a new hierarchic classification system, Actinobacteria classis nov. Int J Syst Bacteriol 47:479–491.
2. Ripoll F, Pasek S, Schenowitz C, Dossat C, Barbe V, Rottman M, Macheras E, Heym B, Herrmann JL, Daffe M, Brosch R, Risler JL, Gaillard JL. 2009. Non mycobacterial virulence genes in the genome of the emerging pathogen Mycobacterium abscessus. PLoS One 4:e5660. [PubMed][CrossRef]
3. Bryant JM, Grogono DM, Greaves D, Foweraker J, Roddick I, Inns T, Reacher M, Haworth CS, Curran MD, Harris SR, Peacock SJ, Parkhill J, Floto RA. 2013. Whole-genome sequencing to identify transmission of Mycobacterium abscessus between patients with cystic fibrosis: a retrospective cohort study. Lancet 381:1551–1560. [PubMed][CrossRef]
4. Pawlik A, Garnier G, Orgeur M, Tong P, Lohan AJ, Le Chevalier F, Sapriel G, Roux AL, Conlon K, Honoré N, Dillies MA, Ma L, Bouchier C, Coppée JY, Gaillard JL, Gordon SV, Loftus B, Brosch R, Herrmann JL. 2013. Identification and characterization of the genetic changes responsible for the characteristic smooth-to-rough morphotype alterations of clinically persistent Mycobacterium abscessus. Mol Microbiol 90:612–629.
5. Springer B, Stockman L, Teschner K, Roberts GD, Bottger EC. 1996. Two-laboratory collaborative study on identification of mycobacteria: molecular versus phenotypic methods. J Clin Microbiol 34:296–303. [PubMed]
6. Philipp WJ, Poulet S, Eiglmeier K, Pascopella L, Balasubramanian V, Heym B, Bergh S, Bloom BR, Jacobs WR, Jr, Cole ST. 1996. An integrated map of the genome of the tubercle bacillus, Mycobacterium tuberculosis H37Rv, and comparison with Mycobacterium leprae. Proc Natl Acad Sci USA 93:3132–3137. [PubMed]
7. Brosch R, Gordon SV, Billault A, Garnier T, Eiglmeier K, Soravito C, Barrell BG, Cole ST. 1998. Use of a Mycobacterium tuberculosis H37Rv bacterial artificial chromosome library for genome mapping, sequencing, and comparative genomics. Infect Immun 66:2221–2229. [PubMed]
8. Pym AS, Brodin P, Brosch R, Huerre M, Cole ST. 2002. Loss of RD1 contributed to the attenuation of the live tuberculosis vaccines Mycobacterium bovis BCG and Mycobacterium microti. Mol Microbiol 46:709–717. [PubMed]
9. 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. [PubMed]
10. 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, Krogh A, McLean J, Moule S, Murphy L, Oliver K, Osborne J, Quail MA, Rajandream MA, Rogers J, Rutter S, Seeger K, Skelton J, Squares R, Squares S, Sulston JE, Taylor K, Whitehead S, Barrell BG. 1998. Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393:537–544. [PubMed][CrossRef]
11. Cole ST, Eiglmeier K, Parkhill J, James KD, Thomson NR, Wheeler PR, Honore N, Garnier T, Churcher C, Harris D, Mungall K, Basham D, Brown D, Chillingworth T, Connor R, Davies RM, Devlin K, Duthoy S, Feltwell T, Fraser A, Hamlin N, Holroyd S, Hornsby T, Jagels K, Lacroix C, Maclean J, Moule S, Murphy L, Oliver K, Quail MA, Rajandream MA, Rutherford KM, Rutter S, Seeger K, Simon S, Simmonds M, Skelton J, Squares R, Squares S, Stevens K, Taylor K, Whitehead S, Woodward JR, Barrell BG. 2001. Massive gene decay in the leprosy bacillus. Nature 409:1007–1011. [PubMed][CrossRef]
12. 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. [PubMed][CrossRef]
13. Stinear TP, Seemann T, Pidot S, Frigui W, Reysset G, Garnier T, Meurice G, Simon D, Bouchier C, Ma L, Tichit M, Porter JL, Ryan J, Johnson PD, Davies JK, Jenkin GA, Small PL, Jones LM, Tekaia F, Laval F, Daffe M, Parkhill J, Cole ST. 2007. Reductive evolution and niche adaptation inferred from the genome of Mycobacterium ulcerans, the causative agent of Buruli ulcer. Genome Res 17:192–200. [PubMed][CrossRef]
14. 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, Garcia JN, Hewinson GR, Behr MA, Quail MA, Churcher C, Barrell BG, Parhill J, Cole ST. 2007. Genome plasticity of BCG and impact on vaccine efficacy. Proc Natl Acad Sci USA 104:5596–5601. [PubMed][CrossRef]
15. Stinear TP, Seemann T, Harrison PF, Jenkin GA, Davies JK, Johnson PD, Abdellah Z, Arrowsmith C, Chillingworth T, Churcher C, Clarke K, Cronin A, Davis P, Goodhead I, Holroyd N, Jagels K, Lord A, Moule S, Mungall K, Norbertczak H, Quail MA, Rabbinowitsch E, Walker D, White B, Whitehead S, Small PL, Brosch R, Ramakrishnan L, Fischbach MA, Parkhill J, Cole ST. 2008. Insights from the complete genome sequence of Mycobacterium marinum on the evolution of Mycobacterium tuberculosis. Genome Res 18:729–741. [PubMed][CrossRef]
16. Hoffmann C, Leis A, Niederweis M, Plitzko JM, Engelhardt H. 2008. Disclosure of the mycobacterial outer membrane: cryo-electron tomography and vitreous sections reveal the lipid bilayer structure. Proc Natl Acad Sci USA 105:3963–3967. [PubMed][CrossRef]
17. Zuber B, Chami M, Houssin C, Dubochet J, Griffiths G, Daffe M. 2008. Direct visualization of the outer membrane of mycobacteria and corynebacteria in their native state. J Bacteriol 190:5672–5680. [PubMed][CrossRef]
18. Kaur D, Guerin ME, Skovierova H, Brennan PJ, Jackson M. 2009. Chapter 2: biogenesis of the cell wall and other glycoconjugates of Mycobacterium tuberculosis. Adv Appl Microbiol 69:23–78. [PubMed][CrossRef]
19. Chopra T, Gokhale RS. 2009. Polyketide versatility in the biosynthesis of complex mycobacterial cell wall lipids. Methods Enzymol 459:259–294. [PubMed][CrossRef]
20. Cotes K, Bakala N’goma JC, Dhouib R, Douchet I, Maurin D, Carriere F, Canaan S. 2008. Lipolytic enzymes in Mycobacterium tuberculosis. Appl Microbiol Biotechnol 78:741–749. [PubMed][CrossRef]
21. Layre E, Moody DB. 2013. Lipidomic profiling of model organisms and the world’s major pathogens. Biochimie 95:109–115. [PubMed][CrossRef]
22. Gordon SV, Heym B, Parkhill J, Barrell B, Cole ST. 1999. New insertion sequences and a novel repeated sequence in the genome of Mycobacterium tuberculosis H37Rv. Microbiology 145:881–892. [PubMed]
23. Bottai D, Brosch R. 2009. Mycobacterial PE, PPE and ESX clusters: novel insights into the secretion of these most unusual protein families. Mol Microbiol 73:325–328. [PubMed][CrossRef]
24. Sampson SL, Lukey P, Warren RM, van Helden PD, Richardson M, Everett MJ. 2001. Expression, characterization and subcellular localization of the Mycobacterium tuberculosis PPE gene Rv1917c. Tuberculosis (Edinb) 81:305–317. [PubMed][CrossRef]
25. Delogu G, Brennan MJ. 2001. Comparative immune response to PE and PE_PGRS antigens of Mycobacterium tuberculosis. Infect Immun 69:5606–5611. [PubMed]
26. 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. [PubMed]
27. Cascioferro A, Delogu G, Colone M, Sali M, Stringaro A, Arancia G, Fadda G, Palu G, Manganelli R. 2007. PE is a functional domain responsible for protein translocation and localization on mycobacterial cell wall. Mol Microbiol 66:1536–1547. [PubMed][CrossRef]
28. Daleke MH, Cascioferro A, de Punder K, Ummels R, Abdallah AM, van der Wel N, Peters PJ, Luirink J, Manganelli R, Bitter W. 2011. Conserved Pro-Glu (PE) and Pro-Pro-Glu (PPE) protein domains target LipY lipases of pathogenic mycobacteria to the cell surface via the ESX-5 pathway. J Biol Chem 286:19024–19034. [PubMed][CrossRef]
29. Abdallah AM, Verboom T, Hannes F, Safi M, Strong M, Eisenberg D, Musters RJ, Vandenbroucke-Grauls CM, Appelmelk BJ, Luirink J, Bitter W. 2006. A specific secretion system mediates PPE41 transport in pathogenic mycobacteria. Mol Microbiol 62:667–679. [PubMed][CrossRef]
30. Bottai D, Di Luca M, Majlessi L, Frigui W, Simeone R, Sayes F, Bitter W, Brennan MJ, Leclerc C, Batoni G, Campa M, Brosch R, Esin S. 2012. Disruption of the ESX-5 system of Mycobacterium tuberculosis causes loss of PPE protein secretion, reduction of cell wall integrity and strong attenuation. Mol Microbiol 83:1195–1209. [PubMed][CrossRef]
31. Sayes F, Sun L, Di Luca M, Simeone R, Degaiffier N, Fiette L, Esin S, Brosch R, Bottai D, Leclerc C, Majlessi L. 2012. Strong immunogenicity and cross-reactivity of Mycobacterium tuberculosis ESX-5 type VII secretion-encoded PE-PPE proteins predicts vaccine potential. Cell Host Microbe 11:352–363. [PubMed][CrossRef]
32. Gey van Pittius NC, Sampson SL, Lee H, Kim Y, van Helden PD, Warren RM. 2006. Evolution and expansion of the Mycobacterium tuberculosis PE and PPE multigene families and their association with the duplication of the ESAT-6 ( esx) gene cluster regions. BMC Evol Biol 6:95. [PubMed][CrossRef]
33. Dheenadhayalan V, Delogu G, Brennan MJ. 2006. Expression of the PE_PGRS 33 protein in Mycobacterium smegmatis triggers necrosis in macrophages and enhanced mycobacterial survival. Microbes Infect 8:262-272 [Epub Sep 12, 2005]. [PubMed][CrossRef]
34. Cadieux N, Parra M, Cohen H, Maric D, Morris SL, Brennan MJ. 2011. Induction of cell death after localization to the host cell mitochondria by the Mycobacterium tuberculosis PE_PGRS33 protein. Microbiology 157:793–804. [PubMed][CrossRef]
35. Supply P, Marceau M, Mangenot S, Roche D, Rouanet C, Khanna V, Majlessi L, Criscuolo A, Tap J, Pawlik A, Fiette L, Orgeur M, Fabre M, Parmentier C, Frigui W, Simeone R, Boritsch EC, Debrie AS, Willery E, Walker D, Quail MA, Ma L, Bouchier C, Salvignol G, Sayes F, Cascioferro A, Seemann T, Barbe V, Locht C, Gutierrez MC, Leclerc C, Bentley SD, Stinear TP, Brisse S, Médigue C, Parkhill J, Cruveiller S, Brosch R. 2013. Genomic analysis of smooth tubercle bacilli provides insights into ancestry and pathoadaptation of Mycobacterium tuberculosis. Nat. Genet. 45:172–179. [PubMed][CrossRef]
36. Arruda S, Bomfim G, Knights R, Huima-Byron T, Riley LW. 1993. Cloning of an M. tuberculosis DNA fragment associated with entry and survival inside cells. Science 261:1454–1457. [PubMed]
37. Tekaia F, Gordon SV, Garnier T, Brosch R, Barrell BG, Cole ST. 1999. Analysis of the proteome of Mycobacterium tuberculosis in silico. Tuber Lung Dis 79:329–342. [PubMed][CrossRef]
38. Casali N, Riley LW. 2007. A phylogenomic analysis of the Actinomycetales mce operons. BMC Genomics 8:60. [PubMed][CrossRef]
39. 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 32:643–656. [PubMed]
40. 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. [PubMed][CrossRef]
41. Shimono N, Morici L, Casali N, Cantrell S, Sidders B, Ehrt S, Riley LW. 2003. Hypervirulent mutant of Mycobacterium tuberculosis resulting from disruption of the mce1 operon. Proc Natl Acad Sci USA 100:15918–15923. [PubMed][CrossRef]
42. Senaratne RH, Sidders B, Sequeira P, Saunders G, Dunphy K, Marjanovic O, Reader JR, Lima P, Chan S, Kendall S, McFadden J, Riley LW. 2008. Mycobacterium tuberculosis strains disrupted in mce3 and mce4 operons are attenuated in mice. J Med Microbiol 57:164–170. [PubMed][CrossRef]
43. Pandey AK, Sassetti CM. 2008. Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci USA 105:4376–4380. [PubMed][CrossRef]
44. Griffin JE, Gawronski JD, Dejesus MA, Ioerger TR, Akerley BJ, Sassetti CM. 2011. High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog 7:e1002251. [PubMed][CrossRef]
45. Sorensen AL, Nagai S, Houen G, Andersen P, Andersen AB. 1995. Purification and characterization of a low-molecular-mass T-cell antigen secreted by Mycobacterium tuberculosis. Infect Immun 63:1710–1717. [PubMed]
46. Berthet FX, Rasmussen PB, Rosenkrandt I, Andersen P, Gicquel B. 1998. A Mycobacterium tuberculosis operon encoding ESAT-6 and a novel low-molecular-mass culture filtrate protein (CFP-10). Microbiology 144:3195–3203. [PubMed]
47. Gey Van Pittius NC, Gamieldien J, Hide W, Brown GD, Siezen RJ, Beyers AD. 2001. The ESAT-6 gene cluster of Mycobacterium tuberculosis and other high G+C Gram-positive bacteria. Genome Biol 2:RESEARCH0044. [PubMed]
48. Pallen MJ. 2002. The ESAT-6/WXG100 superfamily—and a new Gram-positive secretion system? Trends Microbiol 10:209–212. [PubMed]
49. Gordon SV, Bottai D, Simeone R, Stinear TP, Brosch R. 2009. Pathogenicity in the tubercle bacillus: molecular and evolutionary determinants. Bioessays 31:378–388. [PubMed][CrossRef]
50. Li L, Bannantine JP, Zhang Q, Amonsin A, May BJ, Alt D, Banerji N, Kanjilal S, Kapur V. 2005. The complete genome sequence of Mycobacterium avium subspecies paratuberculosis. Proc Natl Acad Sci USA 102:12344–12349. [PubMed][CrossRef]
51. Ramakrishnan L, Tran HT, Federspiel NA, Falkow S. 1997. A crtB homolog essential for photochromogenicity in Mycobacterium marinum: isolation, characterization, and gene disruption via homologous recombination. J Bacteriol 179:5862–5868. [PubMed]
52. Gao LY, Groger R, Cox JS, Beverley SM, Lawson EH, Brown EJ. 2003. Transposon mutagenesis of Mycobacterium marinum identifies a locus linking pigmentation and intracellular survival. Infect Immun 71:922–929. [PubMed]
53. 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. [PubMed][CrossRef]
54. Veyrier FJ, Dufort A, Behr MA. 2011. The rise and fall of the Mycobacterium tuberculosis genome. Trends Microbiol 19:156–161. [PubMed][CrossRef]
55. Gutierrez MC, 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 Pathog 1:e5. [PubMed][CrossRef]
56. 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. [PubMed][CrossRef]
57. 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. [PubMed][CrossRef]
58. 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. [PubMed][CrossRef]
59. 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 M. tuberculosis driven by genetic drift and human demography. PLoS Biol 6:e311. [PubMed][CrossRef]
60. 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. [PubMed][CrossRef]
61. Smith NH, Crawshaw T, Parry J, Birtles RJ. 2009. Mycobacterium microti: more diverse than previously thought. J Clin Microbiol 47:2551–2559. [PubMed][CrossRef]
62. van Soolingen D, van der Zanden AG, de Haas PE, Noordhoek GT, Kiers A, Foudraine NA, Portaels F, Kolk AH, Kremer K, van Embden JD. 1998. Diagnosis of Mycobacterium microti infections among humans by using novel genetic markers. J Clin Microbiol 36:1840–1845. [PubMed]
63. 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. [PubMed]
64. Aranaz A, Cousins D, Mateos A, Dominguez L. 2003. Elevation of Mycobacterium tuberculosis subsp. caprae Aranaz et al. 1999 to species rank as Mycobacterium caprae comb. nov., sp. nov. Int J Syst Evol Microbiol 53:1785–1789. [PubMed]
65. Domogalla J, Prodinger WM, Blum H, Krebs S, Gellert S, Muller M, Neuendorf E, Sedlmaier F, Buttner M. 2013. Region of difference 4 in alpine Mycobacterium caprae isolates indicates three variants. J Clin Microbiol 51:1381–1388. [PubMed][CrossRef]
66. Berg S, Garcia-Pelayo MC, Muller B, Hailu E, Asiimwe B, Kremer K, Dale J, Boniotti MB, Rodriguez S, Hilty M, Rigouts L, Firdessa R, Machado A, Mucavele C, Ngandolo BN, Bruchfeld J, Boschiroli L, Muller A, Sahraoui N, Pacciarini M, Cadmus S, Joloba M, van Soolingen D, Michel AL, Djonne B, Aranaz A, Zinsstag J, van Helden P, Portaels F, Kazwala R, Kallenius G, Hewinson RG, Aseffa A, Gordon SV, Smith NH. 2011. African 2, a clonal complex of Mycobacterium bovis epidemiologically important in East Africa. J Bacteriol 193:670–678. [PubMed][CrossRef]
67. 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. [PubMed][CrossRef]
68. Cousins DV, Peet RL, Gaynor WT, Williams SN, Gow BL. 1994. Tuberculosis in imported hyrax ( Procavia capensis) caused by an unusual variant belonging to the Mycobacterium tuberculosis complex. Vet Microbiol 42:135–145. [PubMed]
69. Mostowy S, Cousins D, Behr MA. 2004. Genomic interrogation of the dassie bacillus reveals it as a unique RD1 mutant within the Mycobacterium tuberculosis complex. J Bacteriol 186:104–109. [PubMed]
70. Coscolla M, Lewin A, Metzger S, Maetz-Rennsing K, Calvignac-Spencer S, Nitsche A, Dabrowski PW, Radonic A, Niemann S, Parkhill J, Couacy-Hymann E, Feldman J, Comas I, Boesch C, Gagneux S, Leendertz FH. 2013. Novel Mycobacterium tuberculosis complex isolate from a wild chimpanzee. Emerg Infect Dis 19:969–976. [PubMed][CrossRef]
71. Stead WW, Eisenach KD, Cave MD, Beggs ML, Templeton GL, Thoen CO, Bates JH. 1995. When did Mycobacterium tuberculosis infection first occur in the New World? An important question with public health implications. Am J Respir Crit Care Med 151:1267–1268. [PubMed][CrossRef]
72. Donoghue HD, Spigelman M, Greenblatt CL, Lev-Maor G, Bar-Gal GK, Matheson C, Vernon K, Nerlich AG, Zink AR. 2004. Tuberculosis: from prehistory to Robert Koch, as revealed by ancient DNA. Lancet Infect Dis 4:584–592. [PubMed][CrossRef]
73. Taylor GM, Young DB, Mays SA. 2005. Genotypic analysis of the earliest known prehistoric case of tuberculosis in Britain. J Clin Microbiol 43:2236–2240. [PubMed][CrossRef]
74. Domenech P, Reed MB, Barry CE, 3rd. 2005. Contribution of the Mycobacterium tuberculosis MmpL protein family to virulence and drug resistance. Infect Immun 73:3492–3501. [PubMed][CrossRef]
75. Gutierrez MC, Ahmed N, Willery E, Narayanan S, Hasnain SE, Chauhan DS, Katoch VM, Vincent V, Locht C, Supply P. 2006. Predominance of ancestral lineages of Mycobacterium tuberculosis in India. Emerg Infect Dis 12:1367–1374. [PubMed][CrossRef]
76. Banu S, Gordon SV, Palmer S, Islam R, Ahmed S, Alam KM, Cole ST, Brosch R. 2004. Genotypic analysis of Mycobacterium tuberculosis in Bangladesh and prevalence of the Beijing Strain. J Clin Microbiol 42:674–682. [PubMed]
77. 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. [PubMed][CrossRef]
78. 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. [PubMed][CrossRef]
79. 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. 2006 Variable host-pathogen compatibility in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 103:2869–2873. [PubMed][CrossRef]
80. Blouin Y, Hauck Y, Soler C, Fabre M, Vong R, Dehan C, Cazajous G, Massoure PL, Kraemer P, Jenkins A, Garnotel E, Pourcel C, Vergnaud G. 2012. Significance of the identification in the Horn of Africa of an exceptionally deep branching Mycobacterium tuberculosis clade. PLoS One 7:e52841. [PubMed][CrossRef]
81. Firdessa R, Berg S, Hailu E, Schelling E, Gumi B, Erenso G, Gadisa E, Kiros T, Habtamu M, Hussein J, Zinsstag J, Robertson BD, Ameni G, Lohan AJ, Loftus B, Comas I, Gagneux S, Tschopp R, Yamuah L, Hewinson G, Gordon SV, Young DB, Aseffa A. 2013. Mycobacterial lineages causing pulmonary and extrapulmonary tuberculosis, Ethiopia. Emerg Infect Dis 19:460–463. [PubMed][CrossRef]
82. Gagneux S, Small PM. 2007. Global phylogeography of Mycobacterium tuberculosis and implications for tuberculosis product development. Lancet Infect Dis 7:328–337. [PubMed][CrossRef]
83. Chan JZ, Sergeant MJ, Lee OY, Minnikin DE, Besra GS, Pap I, Spigelman M, Donoghue HD, Pallen MJ. 2013. Metagenomic analysis of tuberculosis in a mummy. N Engl J Med 369:289–290. [PubMed][CrossRef]
84. Supply P, Mazars E, Lesjean S, Vincent V, Gicquel B, Locht C. 2000. Variable human minisatellite-like regions in the Mycobacterium tuberculosis genome. Mol Microbiol 36:762–771. [PubMed]
85. 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. [PubMed][CrossRef]
86. Walker TM, Ip CL, Harrell RH, Evans JT, Kapatai G, Dedicoat MJ, Eyre DW, Wilson DJ, Hawkey PM, Crook DW, Parkhill J, Harris D, Walker AS, Bowden R, Monk P, Smith EG, Peto TE. 2013. Whole-genome sequencing to delineate Mycobacterium tuberculosis outbreaks: a retrospective observational study. Lancet Infect Dis 13:137–146. [PubMed][CrossRef]
87. Roetzer A, Diel R, Kohl TA, Ruckert C, Nubel U, Blom J, Wirth T, Jaenicke S, Schuback S, Rusch-Gerdes S, Supply P, Kalinowski J, Niemann S. 2013. Whole genome sequencing versus traditional genotyping for investigation of a Mycobacterium tuberculosis outbreak: a longitudinal molecular epidemiological study. PLoS Med 10:e1001387. [PubMed][CrossRef]
88. 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 22:721–734. [PubMed][CrossRef]
89. Marmiesse M, Brodin P, Buchrieser C, Gutierrez C, Simoes N, Vincent V, Glaser P, Cole ST, Brosch R. 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. [PubMed]
90. 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. [PubMed][CrossRef]
91. Koeck JL, Fabre M, Simon F, Daffe M, Garnotel E, Matan AB, Gerome P, Bernatas JJ, Buisson Y, Pourcel C. 2011. Clinical characteristics of the smooth tubercle bacilli ‘Mycobacterium canettii’ infection suggest the existence of an environmental reservoir. Clin Microbiol Infect 17:1013–1019. [PubMed][CrossRef]
92. 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. [PubMed]
93. Pfyffer GE, Auckenthaler R, van Embden JD, van Soolingen D. 1998. Mycobacterium canettii, the smooth variant of M. tuberculosis, isolated from a Swiss patient exposed in Africa. Emerg Infect Dis 4:631–634. [PubMed][CrossRef]
94. Fabre M, Koeck JL, Le Fleche P, Simon F, Herve V, Vergnaud G, Pourcel C. 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. [PubMed][CrossRef]
95. Brisse S, Supply P, Brosch R, Vincent V, Gutierrez MC. 2006. “A re-evaluation of M. prototuberculosis”: continuing the debate. PLoS Pathog 2:e95. [PubMed][CrossRef]
96. Deshayes C, Perrodou E, Euphrasie D, Frapy E, Poch O, Bifani P, Lecompte O, Reyrat JM. 2008. Detecting the molecular scars of evolution in the Mycobacterium tuberculosis complex by analyzing interrupted coding sequences. BMC Evol Biol 8:78. [PubMed][CrossRef]
97. Cain AK, Boinett CJ. 2013. A CRISPR view of genome sequences. Nat Rev Microbiol 11:226. [PubMed][CrossRef]
98. Gray T, Krywy J, Harold J, Palumbo M, Derbyshire K. 2013. Distributive conjugal transfer in mycobacteria generates progeny with meiotic-like genome-wide mosaicism, allowing mapping of a mating identity locus. PLoS Biol 11:e1001602. [PubMed][CrossRef]
99. Simeone R, Bottai D, Brosch R. 2009. ESX/type VII secretion systems and their role in host-pathogen interaction. Curr Opin Microbiol 12:4–10. [PubMed][CrossRef]
100. Wiker HG, Harboe M. 1992. The antigen 85 complex: a major secretion product of Mycobacterium tuberculosis. Microbiol Rev 56:648–661. [PubMed]
101. Sassetti CM, Boyd DH, Rubin EJ. 2003. Genes required for mycobacterial growth defined by high density mutagenesis. Mol Microbiol 48:77–84. [PubMed]
102. Lamichhane G, Zignol M, Blades NJ, Geiman DE, Dougherty A, Grosset J, Broman KW, Bishai WR. 2003. A postgenomic method for predicting essential genes at subsaturation levels of mutagenesis: application to Mycobacterium tuberculosis. Proc Natl Acad Sci USA 100:7213–7218. [PubMed][CrossRef]
103. Sassetti CM, Rubin EJ. 2003. Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci USA 100:12989–12994. [PubMed][CrossRef]
104. Berthet FX, Lagranderie M, Gounon P, Laurent-Winter C, Ensergueix D, Chavarot P, Thouron F, Maranghi E, Pelicic V, Portnoi D, Marchal G, Gicquel B. 1998. Attenuation of virulence by disruption of the Mycobacterium tuberculosis erp gene. Science 282:759–762. [PubMed]
105. Camacho LR, Ensergueix D, Perez E, Gicquel B, Guilhot C. 1999. Identification of a virulence gene cluster of Mycobacterium tuberculosis by signature-tagged transposon mutagenesis. Mol Microbiol 34:257–267. [PubMed]
106. Cox JS, Chen B, McNeil M, Jacobs WR, Jr. 1999. Complex lipid determines tissue-specific replication of Mycobacterium tuberculosis in mice. Nature 402:79–83. [PubMed][CrossRef]
107. Hingley-Wilson SM, Sambandamurthy VK, Jacobs WR, Jr. 2003. Survival perspectives from the world’s most successful pathogen, Mycobacterium tuberculosis. Nat Immunol 4:949–955. [PubMed][CrossRef]
108. Mahairas GG, Sabo PJ, Hickey MJ, Singh DC, Stover CK. 1996. Molecular analysis of genetic differences between Mycobacterium bovis BCG and virulent M. bovis. J Bacteriol 178:1274–1282. [PubMed]
109. Behr MA, Wilson MA, Gill WP, Salamon H, Schoolnik GK, Rane S, Small PM. 1999. Comparative genomics of BCG vaccines by whole-genome DNA microarrays. Science 284:1520–1523. [PubMed]
110. Brodin P, Eiglmeier K, Marmiesse M, Billault A, Garnier T, Niemann S, Cole ST, Brosch R. 2002. Bacterial artificial chromosome-based comparative genomic analysis identifies Mycobacterium microti as a natural ESAT-6 deletion mutant. Infect Immun 70:5568–5578. [PubMed]
111. Sula L, Radkovsky I. 1976. Protective effects of M. microti vaccine against tuberculosis. J Hyg Epidemiol Microbiol Immunol 20:1–6. [PubMed]
112. Hart PD, Sutherland I. 1977. BCG and vole bacillus vaccines in the prevention of tuberculosis in adolescence and early adult life. BMJ 2:293–295. [PubMed]
113. Pym AS, Brodin P, Majlessi L, Brosch R, Demangel C, Williams A, Griffiths KE, Marchal G, Leclerc C, Cole ST. 2003. Recombinant BCG exporting ESAT-6 confers enhanced protection against tuberculosis. Nat Med 9:533–539. [PubMed][CrossRef]
114. Brodin P, Majlessi L, Marsollier L, de Jonge MI, Bottai D, Demangel C, Hinds J, Neyrolles O, Butcher PD, Leclerc C, Cole ST, Brosch R. 2006. Dissection of ESAT-6 system 1 of Mycobacterium tuberculosis and impact on immunogenicity and virulence. Infect Immun 74:88–98. [PubMed][CrossRef]
115. Hsu T, Hingley-Wilson SM, Chen B, Chen M, Dai AZ, Morin PM, Marks CB, Padiyar J, Goulding C, Gingery M, Eisenberg D, Russell RG, Derrick SC, Collins FM, Morris SL, King CH, Jacobs WR, Jr. 2003. The primary mechanism of attenuation of bacillus Calmette-Guerin is a loss of secreted lytic function required for invasion of lung interstitial tissue. Proc Natl Acad Sci USA 100:12420–12425. [PubMed][CrossRef]
116. Lewis KN, Liao R, Guinn KM, Hickey MJ, Smith S, Behr MA, Sherman DR. 2003. Deletion of RD1 from Mycobacterium tuberculosis mimics bacille Calmette-Guerin attenuation. J Infect Dis 187:117–123. [PubMed][CrossRef]
117. Stanley SA, Raghavan S, Hwang WW, Cox JS. 2003. Acute infection and macrophage subversion by Mycobacterium tuberculosis require a specialized secretion system. Proc Natl Acad Sci USA 100:13001–13006. [PubMed][CrossRef]
118. Young DB. 2003. Building a better tuberculosis vaccine. Nat Med 9:503–504 [Epub Apr 14, 2003]. [PubMed][CrossRef]
119. Brodin P, Rosenkrands I, Andersen P, Cole ST, Brosch R. 2004. ESAT-6 proteins: protective antigens and virulence factors? Trends Microbiol 12:500–508. [PubMed][CrossRef]
120. Abdallah A, Gey van Pittius N, Champion P, Cox J, Luirink J, Vandenbroucke-Grauls C, Appelmelk B, Bitter W. 2007. Type VII secretion—mycobacteria show the way. Nat Rev Microbiol 5:883–891. [PubMed][CrossRef]
121. Bitter W, Houben EN, Bottai D, Brodin P, Brown EJ, Cox JS, Derbyshire K, Fortune SM, Gao LY, Liu J, Gey van Pittius NC, Pym AS, Rubin EJ, Sherman DR, Cole ST, Brosch R. 2009. Systematic genetic nomenclature for type VII secretion systems. PLoS Pathog 5:e1000507. [PubMed][CrossRef]
122. Houben EN, Bestebroer J, Ummels R, Wilson L, Piersma SR, Jimenez CR, Ottenhoff TH, Luirink J, Bitter W. 2012. Composition of the type VII secretion system membrane complex. Mol Microbiol 86:472–484. [PubMed][CrossRef]
123. Brown GD, Dave JA, Gey van Pittius NC, Stevens L, Ehlers MR, Beyers AD. 2000. The mycosins of Mycobacterium tuberculosis H37Rv: a family of subtilisin-like serine proteases. Gene 254:147–155. [PubMed]
124. Dave JA, Gey van Pittius NC, Beyers AD, Ehlers MR, Brown GD. 2002. Mycosin-1, a subtilisin-like serine protease of Mycobacterium tuberculosis, is cell wall-associated and expressed during infection of macrophages. BMC Microbiol 2:30. [PubMed]
125. Ohol YM, Goetz DH, Chan K, Shiloh MU, Craik CS, Cox JS. 2010. Mycobacterium tuberculosis MycP1 protease plays a dual role in regulation of ESX-1 secretion and virulence. Cell Host Microbe 7:210–220. [PubMed][CrossRef]
126. Brodin P, Majlessi L, Brosch R, Smith D, Bancroft G, Clark S, Williams A, Leclerc C, Cole ST. 2004. Enhanced protection against tuberculosis by vaccination with recombinant Mycobacterium microti vaccine that induces T cell immunity against region of difference 1 antigens. J Infect Dis 190:115–122. [PubMed][CrossRef]
127. Champion PA, Cox JS. 2007. Protein secretion systems in mycobacteria. Cell Microbiol 9:1376–1384. [PubMed][CrossRef]
128. Champion PA, Stanley SA, Champion MM, Brown EJ, Cox JS. 2006. C-terminal signal sequence promotes virulence factor secretion in Mycobacterium tuberculosis. Science 313:1632–1636. [PubMed][CrossRef]
129. Daleke MH, Ummels R, Bawono P, Heringa J, Vandenbroucke-Grauls CM, Luirink J, Bitter W. 2012. General secretion signal for the mycobacterial type VII secretion pathway. Proc Natl Acad Sci USA 109:11342–11347. [PubMed][CrossRef]
130. Daleke MH, van der Woude AD, Parret AH, Ummels R, de Groot AM, Watson D, Piersma SR, Jimenez CR, Luirink J, Bitter W, Houben EN. 2012. Specific chaperones for the type VII protein secretion pathway. J Biol Chem 287:31939–31947. [PubMed][CrossRef]
131. Bottai D, Majlessi L, Simeone R, Frigui W, Laurent C, Lenormand P, Chen J, Rosenkrands I, Huerre M, Leclerc C, Cole ST, Brosch R. 2011. ESAT-6 secretion-independent impact of ESX-1 genes espF and espG1 on virulence of Mycobacterium tuberculosis. J Infect Dis 203:1155–1164. [PubMed][CrossRef]
132. Nagai H, Cambronne ED, Kagan JC, Amor JC, Kahn RA, Roy CR. 2005. A C-terminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. Proc Natl Acad Sci USA 102:826–831. [PubMed][CrossRef]
133. MacGurn JA, Raghavan S, Stanley SA, Cox JS. 2005. A non-RD1 gene cluster is required for Snm secretion in Mycobacterium tuberculosis. Mol Microbiol 57:1653–1663. [PubMed][CrossRef]
134. Fortune SM, Jaeger A, Sarracino DA, Chase MR, Sassetti CM, Sherman DR, Bloom BR, Rubin EJ. 2005. Mutually dependent secretion of proteins required for mycobacterial virulence. Proc Natl Acad Sci USA 102:10676–10681. [PubMed][CrossRef]
135. Chen JM, Boy-Rottger S, Dhar N, Sweeney N, Buxton RS, Pojer F, Rosenkrands I, Cole ST. 2012. EspD is critical for the virulence-mediating ESX-1 secretion system in Mycobacterium tuberculosis. J Bacteriol 194:884–893. [PubMed][CrossRef]
136. Chen JM, Zhang M, Rybniker J, Boy-Rottger S, Dhar N, Pojer F, Cole ST. 2013. Mycobacterium tuberculosis EspB binds phospholipids and mediates EsxA-independent virulence. Mol Microbiol 89:1154–1166. [PubMed][CrossRef]
137. Frigui W, Bottai D, Majlessi L, Monot M, Josselin E, Brodin P, Garnier T, Gicquel B, Martin C, Leclerc C, Cole S, Brosch R. 2008. Control of M. tuberculosis ESAT-6 secretion and specific T cell recognition by PhoP. PLoS Pathog 4:e33. [PubMed][CrossRef]
138. Blasco B, Chen JM, Hartkoorn R, Sala C, Uplekar S, Rougemont J, Pojer F, Cole ST. 2012. Virulence regulator EspR of Mycobacterium tuberculosis is a nucleoid-associated protein. PLoS Pathog 8:e1002621. [PubMed][CrossRef]
139. Pang X, Samten B, Cao G, Wang X, Tvinnereim AR, Chen XL, Howard ST. 2013. MprAB regulates the espA operon in Mycobacterium tuberculosis and modulates ESX-1 function and host cytokine response. J Bacteriol 195:66–75. [PubMed][CrossRef]
140. Wang S, Engohang-Ndong J, Smith I. 2007. Structure of the DNA-binding domain of the response regulator PhoP from Mycobacterium tuberculosis. Biochemistry 46:14751–14761. [PubMed][CrossRef]
141. Hunt DM, Sweeney NP, Mori L, Whalan RH, Comas I, Norman L, Cortes T, Arnvig KB, Davis EO, Stapleton MR, Green J, Buxton RS. 2012. Long-range transcriptional control of an operon necessary for virulence-critical ESX-1 secretion in Mycobacterium tuberculosis. J Bacteriol 194:2307–2320. [PubMed][CrossRef]
142. Converse SE, Cox JS. 2005. A protein secretion pathway critical for Mycobacterium tuberculosis virulence is conserved and functional in Mycobacterium smegmatis. J Bacteriol 187:1238–1245. [PubMed][CrossRef]
143. Gao LY, Guo S, McLaughlin B, Morisaki H, Engel JN, Brown EJ. 2004. A mycobacterial virulence gene cluster extending RD1 is required for cytolysis, bacterial spreading and ESAT-6 secretion. Mol Microbiol 53:1677–1693. [PubMed][CrossRef]
144. van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M, Pierson J, Brenner M, Peters PJ. 2007. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129:1287–1298. [PubMed][CrossRef]
145. Simeone R, Bobard A, Lippmann J, Bitter W, Majlessi L, Brosch R, Enninga J. 2012. Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLoS Pathog 8:e1002507. [PubMed][CrossRef]
146. Houben D, Demangel C, van Ingen J, Perez J, Baldeon L, Abdallah AM, Caleechurn L, Bottai D, van Zon M, de Punder K, van der Laan T, Kant A, Bossers-de Vries R, Willemsen P, Bitter W, van Soolingen D, Brosch R, van der Wel N, Peters PJ. 2012. ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cell Microbiol 14:1287–1298. [PubMed][CrossRef]
147. de Jonge MI, Pehau-Arnaudet G, Fretz MM, Romain F, Bottai D, Brodin P, Honore N, Marchal G, Jiskoot W, England P, Cole ST, Brosch R. 2007. ESAT-6 from Mycobacterium tuberculosis dissociates from its putative chaperone CFP-10 under acidic conditions and exhibits membrane-lysing activity. J Bacteriol 189:60286034.
148. Lightbody KL, Ilghari D, Waters LC, Carey G, Bailey MA, Williamson RA, Renshaw PS, Carr MD. 2008. Molecular features governing the stability and specificity of functional complex formation by Mycobacterium tuberculosis CFP-10/ESAT-6 family proteins. J Biol Chem 283:17681–17690. [PubMed][CrossRef]
149. De Leon J, Jiang G, Ma Y, Rubin E, Fortune S, Sun J. 2012. Mycobacterium tuberculosis ESAT-6 exhibits a unique membrane-interacting activity that is not found in its ortholog from non-pathogenic Mycobacterium smegmatis. J Biol Chem 287:44184–44191. [PubMed][CrossRef]
150. Guinn KI, Hickey MJ, Mathur SK, Zakel KL, Grotzke JE, Lewinsohn DM, Smith S, Sherman DR. 2004. Individual RD1-region genes are required for export of ESAT-6/CFP-10 and for virulence of Mycobacterium tuberculosis.Mol Microbiol 51:359–370. [PubMed][CrossRef]
151. Aguilo J, Alonso H, Uranga S, Marinova D, Arbues A, de Martino A, Anel A, Monzon M, Badiola J, Pardo J, Brosch R, Martin C. 2013. ESX-1-induced apoptosis is involved in cell-to-cell spread of Mycobacterium tuberculosis. Cell Microbiol [Epub ahead of print.] doi:10.1111/cmi.12169. [PubMed][CrossRef]
152. Watson RO, Manzanillo PS, Cox JS. 2012. Extracellular M. tuberculosis DNA targets bacteria for autophagy by activating the host DNA-sensing pathway. Cell 150:803–815. [PubMed][CrossRef]
153. Romagnoli A, Etna MP, Giacomini E, Pardini M, Remoli ME, Corazzari M, Falasca L, Goletti D, Gafa V, Simeone R, Delogu G, Piacentini M, Brosch R, Fimia GM, Coccia EM. 2012. ESX-1 dependent impairment of autophagic flux by Mycobacterium tuberculosis in human dendritic cells. Autophagy 8:1357–1370. [PubMed][CrossRef]
154. Mishra BB, Moura-Alves P, Sonawane A, Hacohen N, Griffiths G, Moita LF, Anes E. 2010. Mycobacterium tuberculosis protein ESAT-6 is a potent activator of the NLRP3/ASC inflammasome. Cell Microbiol 12:1046–1063. [PubMed][CrossRef]
155. Wong KW, Jacobs WR, Jr. 2011. Critical role for NLRP3 in necrotic death triggered by Mycobacterium tuberculosis.Cell Microbiol 13:1371–1384. [PubMed][CrossRef]
156. Dorhoi A, Nouailles G, Jorg S, Hagens K, Heinemann E, Pradl L, Oberbeck-Muller D, Duque-Correa MA, Reece ST, Ruland J, Brosch R, Tschopp J, Gross O, Kaufmann SHE. 2012. Activation of the NLRP3 inflammasome by Mycobacterium tuberculosis is uncoupled from susceptibility to active tuberculosis. Eur J of Immunol 42:374–384. [PubMed][CrossRef]
157. Stanley SA, Johndrow JE, Manzanillo P, Cox JS. 2007. The type I IFN response to infection with Mycobacterium tuberculosis requires ESX-1-mediated secretion and contributes to pathogenesis. J Immunol 178:3143–3152. [PubMed]
158. Ryan AA, Nambiar JK, Wozniak TM, Roediger B, Shklovskaya E, Britton WJ, Fazekas de St Groth B, Triccas JA. 2009. Antigen load governs the differential priming of CD8 T cells in response to the bacille Calmette Guerin vaccine or Mycobacterium tuberculosis infection. J Immunol 182:7172–7177. [PubMed][CrossRef]
159. Abdallah AM, Verboom T, Weerdenburg EM, Gey van Pittius NC, Mahasha PW, Jimenez C, Parra M, Cadieux N, Brennan MJ, Appelmelk BJ, Bitter W. 2009. PPE and PE_PGRS proteins of Mycobacterium marinum are transported via the type VII secretion system ESX-5. Mol Microbiol 73:329–340. [PubMed][CrossRef]
160. Di Luca M, Bottai D, Batoni G, Orgeur M, Aulicino A, Counoupas C, Campa M, Brosch R, Esin S. 2012. The ESX-5 associated eccB-eccC locus is essential for Mycobacterium tuberculosis viability. PLoS One 7:e52059. [PubMed][CrossRef]
161. Deb C, Daniel J, Sirakova TD, Abomoelak B, Dubey VS, Kolattukudy PE. 2006. A novel lipase belonging to the hormone-sensitive lipase family induced under starvation to utilize stored triacylglycerol in Mycobacterium tuberculosis. J Biol Chem 281:3866–3875. [PubMed][CrossRef]
162. Russell DG, Mwandumba HC, Rhoades EE. 2002. Mycobacterium and the coat of many lipids. J Cell Biol 158:421–426. [PubMed][CrossRef]
163. Guilhot C, Chalut C, Daffe M. 2008. Biosynthesis and roles of phenolic glycolipids and related molecules in Mycobacterium tuberculosis, p 273–289 . In Daffe M, Reyrat JM (ed), The Mycobacterial Cell Envelope. ASM Press, Washington, DC.
164. Joshi SM, Pandey AK, Capite N, Fortune SM, Rubin EJ, Sassetti CM. 2006. Characterization of mycobacterial virulence genes through genetic interaction mapping. Proc Natl Acad Sci USA 103:11760–11765. [PubMed][CrossRef]
165. Schnappinger D, Ehrt S, Voskuil MI, Liu Y, Mangan JA, Monahan IM, Dolganov G, Efron B, Butcher PD, Nathan C, Schoolnik GK. 2003. Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the phagosomal environment. J Exp Med 198:693–704. [PubMed][CrossRef]
166. Voskuil MI, Schnappinger D, Visconti KC, Harrell MI, Dolganov GM, Sherman DR, Schoolnik GK. 2003. Inhibition of respiration by nitric oxide induces a Mycobacterium tuberculosis dormancy program. J Exp Med 198:705–713. [PubMed][CrossRef]
167. Kana BD, Gordhan BG, Downing KJ, Sung N, Vostroktunova G, Machowski EE, Tsenova L, Young M, Kaprelyants A, Kaplan G, Mizrahi V. 2008. The resuscitation-promoting factors of Mycobacterium tuberculosis are required for virulence and resuscitation from dormancy but are collectively dispensable for growth in vitro. Mol Microbiol 67:672–684. [PubMed][CrossRef]
168. Zwerling A, Behr MA, Verma A, Brewer TF, Menzies D, Pai M. 2011. The BCG World Atlas: a database of global BCG vaccination policies and practices. PLoS Med 8:e1001012. [PubMed][CrossRef]
169. Asensio JA, Arbues A, Perez E, Gicquel B, Martin C. 2008. Live tuberculosis vaccines based on phoP mutants: a step towards clinical trials. Expert Opin Biol Ther 8:201–211. [PubMed][CrossRef]
170. Grode L, Seiler P, Baumann S, Hess J, Brinkmann V, Nasser Eddine A, Mann P, Goosmann C, Bandermann S, Smith D, Bancroft GJ, Reyrat JM, van Soolingen D, Raupach B, Kaufmann SH. 2005. Increased vaccine efficacy against tuberculosis of recombinant Mycobacterium bovis bacille Calmette-Guerin mutants that secrete listeriolysin. J Clin Invest 115:2472–2479. [PubMed][CrossRef]
171. Stover CK, Warrener P, VanDevanter DR, Sherman DR, Arain TM, Langhorne MH, Anderson SW, Towell JA, Yuan Y, McMurray DN, Kreiswirth BN, Barry CE, Baker WR. 2000. A small-molecule nitroimidazopyran drug candidate for the treatment of tuberculosis. Nature 405:962–966. [PubMed][CrossRef]
172. Andries K, Verhasselt P, Guillemont J, Gohlmann HW, Neefs JM, Winkler H, Van Gestel J, Timmerman P, Zhu M, Lee E, Williams P, de Chaffoy D, Huitric E, Hoffner S, Cambau E, Truffot-Pernot C, Lounis N, Jarlier V. 2005. A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis. Science 307:223–227. [PubMed][CrossRef]
173. Lee M, Lee J, Carroll MW, Choi H, Min S, Song T, Via LE, Goldfeder LC, Kang E, Jin B, Park H, Kwak H, Kim H, Jeon HS, Jeong I, Joh JS, Chen RY, Olivier KN, Shaw PA, Follmann D, Song SD, Lee JK, Lee D, Kim CT, Dartois V, Park SK, Cho SN, Barry CE, 3rd. 2012. Linezolid for treatment of chronic extensively drug-resistant tuberculosis. N Engl J Med 367:1508–1518. [PubMed][CrossRef]
174. Makarov V, Manina G, Mikusova K, Mollmann U, Ryabova O, Saint-Joanis B, Dhar N, Pasca MR, Buroni S, Lucarelli AP, Milano A, De Rossi E, Belanova M, Bobovska A, Dianiskova P, Kordulakova J, Sala C, Fullam E, Schneider P, McKinney JD, Brodin P, Christophe T, Waddell S, Butcher P, Albrethsen J, Rosenkrands I, Brosch R, Nandi V, Bharath S, Gaonkar S, Shandil RK, Balasubramanian V, Balganesh T, Tyagi S, Grosset J, Riccardi G, Cole ST. 2009. Benzothiazinones kill Mycobacterium tuberculosis by blocking arabinan synthesis. Science 324:801–804. [PubMed][CrossRef]
175. Christophe T, Jackson M, Jeon HK, Fenistein D, Contreras-Dominguez M, Kim J, Genovesio A, Carralot JP, Ewann F, Kim EH, Lee SY, Kang S, Seo MJ, Park EJ, Skovierova H, Pham H, Riccardi G, Nam JY, Marsollier L, Kempf M, Joly-Guillou ML, Oh T, Shin WK, No Z, Nehrbass U, Brosch R, Cole ST, Brodin P. 2009. High content screening identifies decaprenyl-phosphoribose 2′ epimerase as a target for intracellular antimycobacterial inhibitors. PLoS Pathog 5:e1000645. [PubMed][CrossRef]
176. Hartkoorn RC, Sala C, Neres J, Pojer F, Magnet S, Mukherjee R, Uplekar S, Boy-Rottger S, Altmann KH, Cole ST. 2012. Towards a new tuberculosis drug: pyridomycin: nature's isoniazid. EMBO Mol Med 4:1032–1042. [PubMed][CrossRef]
177. Shi W, Zhang X, Jiang X, Yuan H, Lee JS, Barry CE, 3rd, Wang H, Zhang W, Zhang Y. 2011. Pyrazinamide inhibits trans-translation in Mycobacterium tuberculosis. Science 333:1630–1632. [PubMed][CrossRef]
178. Zumla A, Nahid P, Cole ST. 2013. Advances in the development of new tuberculosis drugs and treatment regimens. Nat Rev Drug Discov 12:388–404. [PubMed][CrossRef]
179. Diacon AH, Pym A, Grobusch M, Patientia R, Rustomjee R, Page-Shipp L, Pistorius C, Krause R, Bogoshi M, Churchyard G, Venter A, Allen J, Palomino JC, De Marez T, van Heeswijk RP, Lounis N, Meyvisch P, Verbeeck J, Parys W, de Beule K, Andries K, McNeeley DF. 2009. The diarylquinoline TMC207 for multidrug-resistant tuberculosis. N Engl J Med 360:2397–2405. [PubMed][CrossRef]
Loading

Article metrics loading...

/content/journal/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013
2014-01-31
2019-08-22

Abstract:

Most mycobacterial species are harmless saprophytes, often found in aquatic environments. A few species seem to have evolved from this pool of environmental mycobacteria into major human pathogens, such as , the agent of tuberculosis, , the leprosy bacillus, and , the agent of Buruli ulcer. While the pathogenicity of relates to the acquisition of a large plasmid encoding a polyketide-derived toxin, the molecular mechanisms by which or have evolved to cause disease are complex and involve the interaction between the pathogen and the host.

Here we focus on and closely related mycobacteria and discuss insights gained from recent genomic and functional studies. Comparison of genome data with sequences from nontuberculous mycobacteria, such as or , provides a perception of the more distant evolution of , while the recently accomplished genome sequences of multiple tubercle bacilli with smooth colony morphology, named , have allowed the ancestral gene pool of tubercle bacilli to be estimated. The resulting findings are instrumental for our understanding of the pathogenomic evolution of tuberculosis-causing mycobacteria. Comparison of virulent and attenuated members of the complex has further contributed to identification of a specific secretion pathway, named ESX or Type VII secretion. The molecular machines involved are key elements for mycobacterial pathogenicity, strongly influencing the ability of to cope with the immune defense mounted by the host.

Highlighted Text: Show | Hide
Loading full text...

Full text loading...

/deliver/fulltext/microbiolspec/2/1/MGM2-0025-2013.html?itemId=/content/journal/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013&mimeType=html&fmt=ahah

Figures

Mycobacterial Pathogenomics and Evolution
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-1,properties={foaf_givenname=Daria, foaf_name=Daria Bottai, foaf_surname=Bottai, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-2,properties={foaf_givenname=Timothy P., foaf_name=Timothy P. Stinear, foaf_surname=Stinear, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-3,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-3,properties={foaf_givenname=Philip, foaf_name=Philip Supply, foaf_surname=Supply, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-aff3]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-4,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-4,properties={foaf_givenname=Roland, foaf_name=Roland Brosch, foaf_surname=Brosch, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-aff4]]}]]
Citation: Bottai D, Stinear T, Supply P, Brosch R. 2014. Mycobacterial pathogenomics and evolution. microbiolspec 2(1): doi:10.1128/microbiolspec.MGM2-0025-2013
/content/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013.fig1
FIGURE 1
Proposed scenario of pathoadaptation of tubercle bacilli from a hypothetical mycobacterial common ancestor (most recent common ancestor, MRCA), adapted from reference 49 . In the proposed evolutionary pathway strains gain specific functions (via horizontal gene transfer, recombination, mutation and/or gene loss, etc.), which allow them to better replicate and persist under the environment and temperature conditions of a niche such as human macrophages. It is plausible that the pathogenomic adaptation at some stage involved smooth tubercle bacilli/, which show a broader environmental adaptability and a genetically much larger diversity than the strains ( 35 ).
microbiolspec/2/1/MGM2-0025-2013-fig1_thmb.gif
microbiolspec/2/1/MGM2-0025-2013-fig1.gif
Image of FIGURE 1

Click to view

FIGURE 1

Proposed scenario of pathoadaptation of tubercle bacilli from a hypothetical mycobacterial common ancestor (most recent common ancestor, MRCA), adapted from reference 49 . In the proposed evolutionary pathway strains gain specific functions (via horizontal gene transfer, recombination, mutation and/or gene loss, etc.), which allow them to better replicate and persist under the environment and temperature conditions of a niche such as human macrophages. It is plausible that the pathogenomic adaptation at some stage involved smooth tubercle bacilli/, which show a broader environmental adaptability and a genetically much larger diversity than the strains ( 35 ).

Source: microbiolspec January 2014 vol. 2 no. 1 doi:10.1128/microbiolspec.MGM2-0025-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013.fig2
FIGURE 2
Network phylogeny inferred among the five strains subjected to complete genome sequence analysis and 39 selected genome sequences from members of the classical complex by NeighborNet analysis, based on pairwise alignments of whole-genome SNP data, which in part are also listed in the lower right portion of the figure. The color code and the naming of different phylogenetic lineages within the complex refer to the nomenclature used in reference 59 .
microbiolspec/2/1/MGM2-0025-2013-fig2_thmb.gif
microbiolspec/2/1/MGM2-0025-2013-fig2.gif
Image of FIGURE 2

Click to view

FIGURE 2

Network phylogeny inferred among the five strains subjected to complete genome sequence analysis and 39 selected genome sequences from members of the classical complex by NeighborNet analysis, based on pairwise alignments of whole-genome SNP data, which in part are also listed in the lower right portion of the figure. The color code and the naming of different phylogenetic lineages within the complex refer to the nomenclature used in reference 59 .

Source: microbiolspec January 2014 vol. 2 no. 1 doi:10.1128/microbiolspec.MGM2-0025-2013
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013.fig3
FIGURE 3
Working model of the type VII secretion apparatus adapted from reference 121 . Schematic representation of the core components and their interactions. Various ESX components belonging to different protein families are represented by different colors: orange, amino-terminal transmembrane protein; violet, amino-terminal transmembrane ATPase; green, integral membrane protein; red, mycosin (subtilisin-like serine protease); pink, AAA+ ATPase. Esx secreted substrates, PE and PPE proteins, as well as ESX-1-associated Esp proteins are also represented. Note that the channel drawn in the mycomembrane refers to a hypothetical protein, whose existence has not been experimentally demonstrated, and that the drawing of the mycomembrane follows a schematic representation of reference 17 .
microbiolspec/2/1/MGM2-0025-2013-fig3_thmb.gif
microbiolspec/2/1/MGM2-0025-2013-fig3.gif
Image of FIGURE 3

Click to view

FIGURE 3

Working model of the type VII secretion apparatus adapted from reference 121 . Schematic representation of the core components and their interactions. Various ESX components belonging to different protein families are represented by different colors: orange, amino-terminal transmembrane protein; violet, amino-terminal transmembrane ATPase; green, integral membrane protein; red, mycosin (subtilisin-like serine protease); pink, AAA+ ATPase. Esx secreted substrates, PE and PPE proteins, as well as ESX-1-associated Esp proteins are also represented. Note that the channel drawn in the mycomembrane refers to a hypothetical protein, whose existence has not been experimentally demonstrated, and that the drawing of the mycomembrane follows a schematic representation of reference 17 .

Source: microbiolspec January 2014 vol. 2 no. 1 doi:10.1128/microbiolspec.MGM2-0025-2013
Permissions and Reprints Request Permissions
Download as Powerpoint

Tables

Mycobacterial Pathogenomics and Evolution
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-1,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-1,properties={foaf_givenname=Daria, foaf_name=Daria Bottai, foaf_surname=Bottai, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-2,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-2,properties={foaf_givenname=Timothy P., foaf_name=Timothy P. Stinear, foaf_surname=Stinear, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-aff2]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-3,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-3,properties={foaf_givenname=Philip, foaf_name=Philip Supply, foaf_surname=Supply, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-aff3]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-4,webId=/content/author/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-4,properties={foaf_givenname=Roland, foaf_name=Roland Brosch, foaf_surname=Brosch, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013-aff4]]}]]
Citation: Bottai D, Stinear T, Supply P, Brosch R. 2014. Mycobacterial pathogenomics and evolution. microbiolspec 2(1): doi:10.1128/microbiolspec.MGM2-0025-2013
/content/microbiolspec/10.1128/microbiolspec.MGM2-0025-2013.T1
TABLE 1
Ratios of nonsynonymous versus synonymous SNPs in gene categories
Generic image for table

Click to view

TABLE 1

Ratios of nonsynonymous versus synonymous SNPs in gene categories

Source: microbiolspec January 2014 vol. 2 no. 1 doi:10.1128/microbiolspec.MGM2-0025-2013

Supplemental Material

No supplementary material available for this content.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error