1932

Abstract

is a globally distributed, lethal pathogen of humans. The virulence armamentarium of appears to have been developed on a scaffold of antiphagocytic defenses found among diverse, mostly free-living species of . Pathoadaptation was further aided by the modularity, flexibility, and interactivity characterizing mycobacterial effectors and their regulators. During emergence of , novel genetic material was acquired, created, and integrated with existing tools. The major mutational mechanisms underlying these adaptations are discussed in this review, with examples. During its evolution, lost the ability and/or opportunity to engage in lateral gene transfer, but despite this it has retained the adaptability that characterizes mycobacteria. exemplifies the evolutionary genomic mechanisms underlying adoption of the pathogenic niche, and studies of its evolution have uncovered a rich array of discoveries about how new pathogens are made.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-121321-093031
2022-09-08
2024-06-13
Loading full text...

Full text loading...

/deliver/fulltext/micro/76/1/annurev-micro-121321-093031.html?itemId=/content/journals/10.1146/annurev-micro-121321-093031&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abdallah AM, Bestebroer J, Savage NDL, de Punder K, von Zon M et al. 2011. Mycobacterial secretion systems ESX-1 and ESX-5 play distinct roles in host cell death and inflammasome activation. J. Immunol. 187:94744–53
    [Google Scholar]
  2. 2.
    Allen AC, Malaga W, Gaudin C, Volle A, Moreau F et al. 2021. Parallel in vivo experimental evolution reveals that increased stress resistance was key for the emergence of persistent tuberculosis bacilli. Nat. Microbiol. 6:81082–93
    [Google Scholar]
  3. 3.
    Ates LS, Brosch R. 2017. Discovery of the type VII ESX-1 secretion needle?. Mol. Microbiol. 103:17–12
    [Google Scholar]
  4. 4.
    Ates LS, Ummels R, Commandeur S, van der Weerd R, Sparrius M et al. 2015. Essential role of the ESX-5 secretion system in outer membrane permeability of pathogenic mycobacteria. PLOS Genet 11:5e1005190
    [Google Scholar]
  5. 5.
    Augenstreich J, Arbues A, Simeone R, Haanappel E, Wegener A et al. 2017. ESX-1 and phthiocerol dimycocerosates of Mycobacterium tuberculosis act in concert to cause phagosomal rupture and host cell apoptosis. Cell. Microbiol. 19:7e12726
    [Google Scholar]
  6. 6.
    Balamayooran G, Pena M, Sharma R, Truman RW. 2015. The armadillo as an animal model and reservoir host for Mycobacterium leprae. Clin. Dermatol. 33:1108–15
    [Google Scholar]
  7. 7.
    Beckwith KS, Beckwith MS, Ullmann S, Sætra RS, Kim H et al. 2020. Plasma membrane damage causes NLRP3 activation and pyroptosis during Mycobacterium tuberculosis infection. Nat. Commun. 11:12270
    [Google Scholar]
  8. 8.
    Becq J, Gutierrez MC, Rosas-Magallanes V, Rauzier J, Gicquel B et al. 2007. Contribution of horizontally acquired genomic islands to the evolution of the tubercle bacilli. Mol. Biol. Evol. 24:1861–71
    [Google Scholar]
  9. 9.
    Belisle JT, Brennan PJ. 1989. Chemical basis of rough and smooth variation in mycobacteria. J. Bacteriol. 171:63465–70
    [Google Scholar]
  10. 10.
    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 Neglected Trop. Dis. 6:e1552
    [Google Scholar]
  11. 11.
    Bohr LL, Youngblom MA, Eldholm V, Pepperell CS. 2021. Genome reorganization during emergence of host-associated Mycobacterium abscessus. Microb. Genom. 7:12000706
    [Google Scholar]
  12. 12.
    Boritsch EC, Frigui W, Cascioferro A, Malaga W, Etienne G et al. 2016. pks5-recombination-mediated surface remodelling in Mycobacterium tuberculosis emergence. Nat. Microbiol. 1:215019
    [Google Scholar]
  13. 13.
    Boritsch EC, Khanna V, Pawlik A, Honoré N, Navas VH et al. 2016. Key experimental evidence of chromosomal DNA transfer among selected tuberculosis-causing mycobacteria. PNAS 113:359876–81
    [Google Scholar]
  14. 14.
    Boritsch EC, Supply P, Honoré N, Seeman T, Stinear TP, Brosch R. 2014. A glimpse into the past and predictions for the future: the molecular evolution of the tuberculosis agent. Mol. Microbiol. 93:5835–52
    [Google Scholar]
  15. 15.
    Bottai D, Di Luca M, Majlessi L, Frigui W, Simeone R et al. 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. 83:61195–209
    [Google Scholar]
  16. 16.
    Bouzid F, Brégeon F, Lepidi H, Donoghue HD, Minnikin DE, Drancourt M. 2017. Ready experimental translocation of Mycobacterium canettii yields pulmonary tuberculosis. Infect. Immunity 85:12e00507–17
    [Google Scholar]
  17. 17.
    Brosch R, Gordon SV, Marmiesse M, Brodin P, Buchrieser C et al. 2002. A new evolutionary scenario for the Mycobacterium tuberculosis complex. PNAS 99:63684–89
    [Google Scholar]
  18. 18.
    Bryant JM, Brown KP, Burbaud S, Everall I, Belardinelli JM et al. 2021. Stepwise pathogenic evolution of Mycobacterium abscessus. Science 372:6541eabb8699
    [Google Scholar]
  19. 19.
    Bryant JM, Grogono DM, Rodriguez-Rincon D, Everall I, Brown KP et al. 2016. Emergence and spread of a human-transmissible multidrug-resistant nontuberculous mycobacterium. Science 354:6313751–57
    [Google Scholar]
  20. 20.
    Claeys TA, Robinson RT. 2018. The many lives of nontuberculous mycobacteria. J. Bacteriol. 200:11e00739–17
    [Google Scholar]
  21. 21.
    Constant P, Perez E, Malaga W, Lanéelle M-A, Saurel O et al. 2002. Role of the pks15/1 gene in the biosynthesis of phenolglycolipids in the Mycobacterium tuberculosis complex: evidence that all strains synthesize glycosylated p-hydroxybenzoic methyl esters and that strains devoid of phenolglycolipids harbor a frameshift mutation in the pks15/1 gene. J. Biol. Chem. 277:4138148–58
    [Google Scholar]
  22. 22.
    Coros A, Callahan B, Battaglioli E, Derbyshire KM. 2008. The specialized secretory apparatus ESX-1 is essential for DNA transfer in Mycobacterium smegmatis. Mol. Microbiol. 69:4794–808
    [Google Scholar]
  23. 23.
    Daffé M, Crick DC, Jackson M 2014. Genetics of capsular polysaccharides and cell envelope (glyco)lipids. Microbiol. Spectr. 2:4MGM2–0021-2013
    [Google Scholar]
  24. 24.
    Danilchanka O, Sun J, Pavlenok M, Maueröder C, Speer A et al. 2014. An outer membrane channel protein of Mycobacterium tuberculosis with exotoxin activity. PNAS 111:186750–55
    [Google Scholar]
  25. 25.
    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. 4:9e744
    [Google Scholar]
  26. 26.
    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. 8:178
    [Google Scholar]
  27. 27.
    Dubey VS, Sirakova TD, Cynamon MH, Kolattukudy PE. 2003. Biochemical function of msl5 (pks8 plus pks17) in Mycobacterium tuberculosis H37Rv: biosynthesis of monomethyl branched unsaturated fatty acids. J. Bacteriol. 185:154620–25
    [Google Scholar]
  28. 28.
    Dulberger CL, Rubin EJ, Boutte CC. 2019. The mycobacterial cell envelope—a moving target. Nat. Rev. Microbiol. 18:147
    [Google Scholar]
  29. 29.
    Dumas E, Boritsch EC, Vandenbogaert M, Rodríguez de la Vega RC, Thiberge J-M et al. 2016. Mycobacterial pan-genome analysis suggests important role of plasmids in the radiation of type VII secretion systems. Genome Biol. Evol. 8:2387–401
    [Google Scholar]
  30. 30.
    Eckstein TM, Inamine JM, Lambert ML, Belisle JT. 2000. A genetic mechanism for deletion of the ser2 gene cluster and formation of rough morphological variants of Mycobacterium avium. J. Bacteriol. 182:216177–82
    [Google Scholar]
  31. 31.
    Ekiert DC, Cox JS. 2014. Structure of a PE-PPE-EspG complex from Mycobacterium tuberculosis reveals molecular specificity of ESX protein secretion. PNAS 111:4114758–63
    [Google Scholar]
  32. 32.
    Fabre M, Hauck Y, Soler C, Koeck J-L, van Ingen J et al. 2010. Molecular characteristics of “Mycobacterium canettii” the smooth Mycobacterium tuberculosis bacilli. Infect. Genet. Evol. 10:81165–73
    [Google Scholar]
  33. 33.
    Flint JL, Kowalski JC, Karnati PK, Derbyshire KM. 2004. The RD1 virulence locus of Mycobacterium tuberculosis regulates DNA transfer in Mycobacterium smegmatis. PNAS 101:3412598–603
    [Google Scholar]
  34. 34.
    Fortune SM, Jaeger A, Sarracino DA, Chase MR, Sassetti CM et al. 2005. Mutually dependent secretion of proteins required for mycobacterial virulence. PNAS 102:3010676–81
    [Google Scholar]
  35. 35.
    Freeman R, Geier H, Weigel KM, Do J, Ford TE, Cangelosi GA. 2006. Roles for cell wall glycopeptidolipid in surface adherence and planktonic dispersal of Mycobacterium avium. Appl. Environ. Microbiol. 72:127554–58
    [Google Scholar]
  36. 36.
    Garces A, Atmakuri K, Chase MR, Woodworth JS, Krastins B et al. 2010. EspA acts as a critical mediator of ESX1-dependent virulence in Mycobacterium tuberculosis by affecting bacterial cell wall integrity. PLOS Pathog 6:6e1000957
    [Google Scholar]
  37. 37.
    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 2:10research0044.1
    [Google Scholar]
  38. 38.
    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
    [Google Scholar]
  39. 39.
    Godfroid M, Dagan T, Kupczok A. 2018. Recombination signal in Mycobacterium tuberculosis stems from reference-guided assemblies and alignment artefacts. Genome Biol. Evol. 10:81920–26
    [Google Scholar]
  40. 40.
    Gomez-Velasco A, Bach H, Rana AK, Cox LR, Bhatt A et al. 2013. Disruption of the serine/threonine protein kinase H affects phthiocerol dimycocerosates synthesis in Mycobacterium tuberculosis. Microbiology 159:Part 4726–36
    [Google Scholar]
  41. 41.
    Gonzalo-Asensio J, Malaga W, Pawlik A, Astarie-Dequeker C, Passemar C et al. 2014. Evolutionary history of tuberculosis shaped by conserved mutations in the PhoPR virulence regulator. PNAS 111:3111491–96
    [Google Scholar]
  42. 42.
    Gopinath K, Moosa A, Mizrahi V, Warner DF. 2013. Vitamin B12 metabolism in Mycobacterium tuberculosis. Future Microbiol 8:111405–18
    [Google Scholar]
  43. 43.
    Gopinath K, Venclovas Č, Ioerger TR, Sacchettini JC, McKinney JD et al. 2013. A vitamin B12 transporter in Mycobacterium tuberculosis. Open Biol 3:2120175
    [Google Scholar]
  44. 44.
    Goren MB, Brokl O, Schaefer WB. 1974. Lipids of putative relevance to virulence in Mycobacterium tuberculosis: correlation of virulence with elaboration of sulfatides and strongly acidic lipids. Infect. Immun. 9:1142–49
    [Google Scholar]
  45. 45.
    Gray TA, Clark RR, Boucher N, Lapierre P, Smith C, Derbyshire KM. 2016. Intercellular communication and conjugation are mediated by ESX secretion systems in mycobacteria. Science 354:6310347–50
    [Google Scholar]
  46. 46.
    Gray TA, Krywy JA, Harold J, Palumbo MJ, Derbyshire KM. 2013. Distributive conjugal transfer in mycobacteria generates progeny with meiotic-like genome-wide mosaicism, allowing mapping of a mating identity locus. PLOS Biol 11:7e1001602
    [Google Scholar]
  47. 47.
    Griffin JE, Pandey AK, Gilmore SA, Mizrahi V, Mckinney JD et al. 2012. Cholesterol catabolism by Mycobacterium tuberculosis requires transcriptional and metabolic adaptations. Chem. Biol. 19:2218–27
    [Google Scholar]
  48. 48.
    Gutacker MM, Smoot JC, Migliaccio CAL, Ricklefs SM, Hua S et al. 2002. Genome-wide analysis of synonymous single nucleotide polymorphisms in Mycobacterium tuberculosis complex organisms: resolution of genetic relationships among closely related microbial strains. Genetics 162:41533–43
    [Google Scholar]
  49. 49.
    Gutierrez MC, Brisse S, Brosch R, Fabre M, Omaïs B et al. 2005. Ancient origin and gene mosaicism of the progenitor of Mycobacterium tuberculosis. PLOS Pathog 1:1e5
    [Google Scholar]
  50. 50.
    Hagedorn M, Rohde KH, Russell DG, Soldati T. 2009. Infection by tubercular mycobacteria is spread by nonlytic ejection from their amoeba hosts. Science 323:59221729–33
    [Google Scholar]
  51. 51.
    Hirsh AE, Tsolaki AG, DeRiemer K, Feldman MW, Small PM. 2004. Stable association between strains of Mycobacterium tuberculosis and their human host populations. PNAS 101:4871–76
    [Google Scholar]
  52. 52.
    Houben D, Demangel C, van Ingen J, Perez J, Baldeón L et al. 2012. ESX-1-mediated translocation to the cytosol controls virulence of mycobacteria. Cell. Microbiol. 14:81287–98
    [Google Scholar]
  53. 53.
    Howard ST, Rhoades E, Recht J, Pang X, Alsup A et al. 2006. Spontaneous reversion of Mycobacterium abscessus from a smooth to a rough morphotype is associated with reduced expression of glycopeptidolipid and reacquisition of an invasive phenotype. Microbiology 152:61581–90
    [Google Scholar]
  54. 54.
    Huet G, Constant P, Malaga W, Lanéelle M-A, Kremer K et al. 2009. A lipid profile typifies the Beijing strains of Mycobacterium tuberculosis: identification of a mutation responsible for a modification of the structures of phthiocerol dimycocerosates and phenolic glycolipids. J. Biol. Chem. 284:4027101–13
    [Google Scholar]
  55. 55.
    Ignatov DV, Salina EG, Fursov MV, Skvortsov TA, Azhikina TL, Kaprelyants AS. 2015. Dormant non-culturable Mycobacterium tuberculosis retains stable low-abundant mRNA. BMC Genom 16:1954
    [Google Scholar]
  56. 56.
    Izquierdo Lafuente B, Ummels R, Kuijl C, Bitter W, Speer A. 2021. Mycobacterium tuberculosis toxin CpnT is an ESX-5 substrate and requires three type VII secretion systems for intracellular secretion. mBio 12:2e02983–20
    [Google Scholar]
  57. 57.
    Kansal RG, Gomez-Flores R, Mehta RT. 1998. Change in colony morphology influences the virulence as well as the biochemical properties of the complex. Microb. Pathog. 25:4203–14
    [Google Scholar]
  58. 58.
    Khan HS, Nair VR, Ruhl CR, Alvarez-Arguedas S, Galvan Rendiz JL et al. 2020. Identification of scavenger receptor B1 as the airway microfold cell receptor for Mycobacterium tuberculosis. eLife 9:e52551
    [Google Scholar]
  59. 59.
    Kim B-R, Kim B-J, Kook Y-H, Kim B-J. 2019. Phagosome escape of rough Mycobacterium abscessus strains in murine macrophage via phagosomal rupture can lead to type I interferon production and their cell-to-cell spread. Front. Immunol. 10:125
    [Google Scholar]
  60. 60.
    Koeck J-L, Fabre M, Simon F, Daffé M, Garnotel É et al. 2011. Clinical characteristics of the smooth tubercle bacilli ‘Mycobacterium canettii’ infection suggest the existence of an environmental reservoir. Clin. Microbiol. Infect. 17:71013–19
    [Google Scholar]
  61. 61.
    Krishnan N, Malaga W, Constant P, Caws M, Tran TH et al. 2011. Mycobacterium tuberculosis lineage influences innate immune response and virulence and is associated with distinct cell envelope lipid profiles. PLOS ONE 6:e23870
    [Google Scholar]
  62. 62.
    Laencina L, Dubois V, Moigne VL, Viljoen A, Majlessi L et al. 2018. Identification of genes required for Mycobacterium abscessus growth in vivo with a prominent role of the ESX-4 locus. PNAS 115:5E1002–11
    [Google Scholar]
  63. 63.
    Lee W, VanderVen BC, Fahey RJ, Russell DG. 2013. Intracellular Mycobacterium tuberculosis exploits host-derived fatty acids to limit metabolic stress. J. Biol. Chem. 288:106788–899
    [Google Scholar]
  64. 64.
    Liu X, Gutacker MM, Musser JM, Fu YX. 2006. Evidence for recombination in Mycobacterium tuberculosis. J. Bacteriol. 188:8169–77
    [Google Scholar]
  65. 65.
    Lou Y, Rybniker J, Sala C, Cole ST. 2017. EspC forms a filamentous structure in the cell envelope of Mycobacterium tuberculosis and impacts ESX-1 secretion: filamentous structure formation by EspC. Mol. Microbiol. 103:126–38
    [Google Scholar]
  66. 66.
    Luo T, Xu P, Zhang Y, Porter JL, Ghanem M et al. 2021. Population genomics provides insights into the evolution and adaptation to humans of the waterborne pathogen Mycobacterium kansasii. Nat. Commun. 12:12491
    [Google Scholar]
  67. 67.
    MacGurn JA, Raghavan S, Stanley SA, Cox JS. 2005. A non-RD1 gene cluster is required for Snm secretion in Mycobacterium tuberculosis. Mol. Microbiol. 57:61653–63
    [Google Scholar]
  68. 68.
    Madacki J, Orgeur M, Mas Fiol G, Frigui W, Ma L, Brosch R 2021. ESX-1-independent horizontal gene transfer by Mycobacterium tuberculosis complex strains. mBio 12:3e00965–21
    [Google Scholar]
  69. 69.
    Mehra A, Zahra A, Thompson V, Sirisaengtaksin N, Wells A et al. 2013. Mycobacterium tuberculosis type VII secreted effector EsxH targets host ESCRT to impair trafficking. PLOS Pathog 9:10e1003734
    [Google Scholar]
  70. 70.
    Minias A, Gąsior F, Brzostek A, Jagielski T, Dziadek J. 2021. Cobalamin is present in cells of non-tuberculous mycobacteria, but not in Mycobacterium tuberculosis. Sci. Rep. 11:112267
    [Google Scholar]
  71. 71.
    Minias A, Minias P, Czubat B, Dziadek J. 2018. Purifying selective pressure suggests the functionality of a vitamin B12 biosynthesis pathway in a global population of Mycobacterium tuberculosis. Genome Biol. Evol. 10:92326–37
    [Google Scholar]
  72. 72.
    Mittal E, Skowyra ML, Uwase G, Tinaztepe E, Mehra A et al. 2018. Mycobacterium tuberculosis type VII secretion system effectors differentially impact the ESCRT endomembrane damage response. mBio 9:6e01765–18
    [Google Scholar]
  73. 73.
    Mortimer TD, Pepperell CS. 2014. Genomic signatures of distributive conjugal transfer among mycobacteria. Genome Biol. Evol. 6:92489–500
    [Google Scholar]
  74. 74.
    Mortimer TD, Weber AM, Pepperell CS. 2017. Evolutionary thrift: Mycobacteria repurpose plasmid diversity during adaptation of type VII secretion systems. Genome Biol. Evol. 9:3398–413
    [Google Scholar]
  75. 75.
    Mougous JD, Petzold CJ, Senaratne RH, Lee DH, Akey DL et al. 2004. Identification, function and structure of the mycobacterial sulfotransferase that initiates sulfolipid-1 biosynthesis. Nat. Struct. Mol. Biol. 11:8721–29
    [Google Scholar]
  76. 76.
    Murray GGR, Charlesworth J, Miller EL, Casey MJ, Lloyd CT et al. 2021. Genome reduction is associated with bacterial pathogenicity across different scales of temporal and ecological divergence. Mol. Biol. Evol. 38:41570–79
    [Google Scholar]
  77. 77.
    Newton-Foot M, Warren RM, Sampson SL, van Helden PD, Gey van Pittius NC. 2016. The plasmid-mediated evolution of the mycobacterial ESX (Type VII) secretion systems. BMC Evol. Biol. 16:62
    [Google Scholar]
  78. 78.
    Neyrolles O, Guilhot C. 2011. Recent advances in deciphering the contribution of Mycobacterium tuberculosis lipids to pathogenesis. Tuberculosis 91:3187–95
    [Google Scholar]
  79. 79.
    Ngabonziza JCS, Loiseau C, Marceau M, Jouet A, Menardo F et al. 2020. A sister lineage of the Mycobacterium tuberculosis complex discovered in the African Great Lakes region. Nat. Commun. 11:12917
    [Google Scholar]
  80. 80.
    Nguyen KT, Piastro K, Gray TA, Derbyshire KM. 2010. Mycobacterial biofilms facilitate horizontal DNA transfer between strains of Mycobacterium smegmatis. J. Bacteriol. 192:195134–42
    [Google Scholar]
  81. 81.
    O'Neill MB, Mortimer TD, Pepperell CS. 2015. Diversity of Mycobacterium tuberculosis across evolutionary scales. PLOS Pathog 11:11e1005257
    [Google Scholar]
  82. 82.
    Ortalo-Magné A, Lemassu A, Lanéelle MA, Bardou F, Silve G et al. 1996. Identification of the surface-exposed lipids on the cell envelopes of Mycobacterium tuberculosis and other mycobacterial species. J. Bacteriol. 178:2456–61
    [Google Scholar]
  83. 83.
    Pajuelo D, Gonzalez-Juarbe N, Tak U, Sun J, Orihuela CJ, Niederweis M. 2018. NAD+ depletion triggers macrophage necroptosis, a cell death pathway exploited by Mycobacterium tuberculosis. Cell Rep 24:2429–40
    [Google Scholar]
  84. 84.
    Parsons LM, Jankowski CS, Derbyshire KM. 1998. Conjugal transfer of chromosomal DNA in Mycobacterium smegmatis. Mol. Microbiol. 28:3571–82
    [Google Scholar]
  85. 85.
    Parte AC, Leibniz Inst. DSMZ. 2022. Genus Mycobacterium List of Prokaryotic Names with Standing in Nomenclature Braunschweig, Ger.: accessed Apr. 27. https://lpsn.dsmz.de/genus/mycobacterium
    [Google Scholar]
  86. 86.
    Passemar C, Arbués A, Malaga W, Mercier I, Moreau F et al. 2014. Multiple deletions in the polyketide synthase gene repertoire of Mycobacterium tuberculosis reveal functional overlap of cell envelope lipids in host-pathogen interactions. Cell Microbiol 16:2195–213
    [Google Scholar]
  87. 87.
    Pawełczyk J, Brzostek A, Minias A, Płociński P, Rumijowska-Galewicz A et al. 2021. Cholesterol-dependent transcriptome remodeling reveals new insight into the contribution of cholesterol to Mycobacterium tuberculosis pathogenesis. Sci. Rep. 11:112396
    [Google Scholar]
  88. 88.
    Pawlik A, Garnier G, Orgeur M, Tong P, Lohan A et al. 2013. Identification and characterization of the genetic changes responsible for the characteristic smooth-to-rough morphotype alterations of clinically persistent Mycobacterium abscessus. Mol. Microbiol. 90:3612–29
    [Google Scholar]
  89. 89.
    Pepperell C, Hoeppner VH, Lipatov M, Wobeser W, Schoolnik GK, Feldman MW. 2010. Bacterial genetic signatures of human social phenomena among M. tuberculosis from an Aboriginal Canadian population. Mol. Biol. Evol. 27:427–40
    [Google Scholar]
  90. 90.
    Pepperell CS, Casto AM, Kitchen A, Granka JM, Cornejo OE et al. 2013. The role of selection in shaping diversity of natural M. tuberculosis populations. PLOS Pathog 9:8e1003543
    [Google Scholar]
  91. 91.
    Phelan JE, Coll F, Bergval I, Anthony RM, Warren R et al. 2016. Recombination in pe/ppe genes contributes to genetic variation in Mycobacterium tuberculosis lineages. BMC Genom 17:151
    [Google Scholar]
  92. 92.
    Portal-Celhay C, Tufariello JM, Srivastava S, Zahra A, Klevorn T et al. 2016. Mycobacterium tuberculosis EsxH inhibits ESCRT-dependent CD4+ T-cell activation. Nat. Microbiol. 2:16232
    [Google Scholar]
  93. 93.
    Quigley J, Hughitt VK, Velikovsky CA, Mariuzza RA, El-Sayed NM, Briken V. 2017. The cell wall lipid PDIM Contributes to phagosomal escape and host cell exit of Mycobacterium tuberculosis. mBio 8:2e00148–17
    [Google Scholar]
  94. 94.
    Ramage HR, Connolly LE, Cox JS. 2009. Comprehensive functional analysis of Mycobacterium tuberculosis toxin-antitoxin systems: implications for pathogenesis, stress responses, and evolution. PLOS Genet 5:12e1000767
    [Google Scholar]
  95. 95.
    Recht J, Kolter R. 2001. Glycopeptidolipid acetylation affects sliding motility and biofilm formation in Mycobacterium smegmatis. J. Bacteriol. 183:195718–24
    [Google Scholar]
  96. 96.
    Reed MB, Domenech P, Manca C, Su H, Barczak AK et al. 2004. A glycolipid of hypervirulent tuberculosis strains that inhibits the innate immune response. Nature 431:700484–87
    [Google Scholar]
  97. 97.
    Reed MB, Gagneux S, DeRiemer K, Small PM, Barry CE. 2007. The W-Beijing lineage of Mycobacterium tuberculosis overproduces triglycerides and has the DosR dormancy regulon constitutively upregulated. J. Bacteriol. 189:72583–89
    [Google Scholar]
  98. 98.
    Ren H, Dover LG, Islam ST, Alexander DC, Chen JM et al. 2007. Identification of the lipooligosaccharide biosynthetic gene cluster from Mycobacterium marinum. Mol. Microbiol. 63:51345–59
    [Google Scholar]
  99. 99.
    Rhoades ER, Archambault AS, Greendyke R, Hsu F-F, Streeter C, Byrd TF. 2009. Mycobacterium abscessus glycopeptidolipids mask underlying cell wall phosphatidyl-myo-inositol mannosides blocking induction of human macrophage TNF-α by preventing interaction with TLR2. J. Immunol. 183:31997–2007
    [Google Scholar]
  100. 100.
    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. 23:1129–35
    [Google Scholar]
  101. 101.
    Rousseau C, Sirakova TD, Dubey VS, Bordat Y, Kolattukudy PE et al. 2003. Virulence attenuation of two Mas-like polyketide synthase mutants of Mycobacterium tuberculosis. Microbiology 149:71837–47
    [Google Scholar]
  102. 102.
    Rousseau C, Turner OC, Rush E, Bordat Y, Sirakova TD et al. 2003. Sulfolipid deficiency does not affect the virulence of Mycobacterium tuberculosis H37Rv in mice and guinea pigs. Infect. Immunity 71:84684–90
    [Google Scholar]
  103. 103.
    Roux A-L, Viljoen A, Bah A, Simeone R, Bernut A et al. 2016. The distinct fate of smooth and rough Mycobacterium abscessus variants inside macrophages. Open Biol 6:11160185
    [Google Scholar]
  104. 104.
    Ruhl CR, Pasko BL, Khan HS, Kindt LM, Stamm CE et al. 2020. Mycobacterium tuberculosis sulfolipid-1 activates nociceptive neurons and induces cough. Cell 181:2293–305.e11
    [Google Scholar]
  105. 105.
    Sapriel G, Brosch R. 2019. Shared pathogenomic patterns characterize a new phylotype, revealing transition toward host-adaptation long before speciation of Mycobacterium tuberculosis. Genome Biol. Evol. 11:82420–38
    [Google Scholar]
  106. 106.
    Savvi S, Warner DF, Kana BD, McKinney JD, Mizrahi V, Dawes SS. 2008. Functional characterization of a vitamin B12-dependent methylmalonyl pathway in Mycobacterium tuberculosis: implications for propionate metabolism during growth on fatty acids. J. Bacteriol. 190:113886–95
    [Google Scholar]
  107. 107.
    Schrenzel MD. 2012. Molecular epidemiology of mycobacteriosis in wildlife and pet animals. Vet. Clin. Exot. Anim. 15:1–23
    [Google Scholar]
  108. 108.
    Serafini A, Boldrin F, Palù G, Manganelli R. 2009. Characterization of a Mycobacterium tuberculosis ESX-3 conditional mutant: essentiality and rescue by iron and zinc. J. Bacteriol. 191:206340–44
    [Google Scholar]
  109. 109.
    Shapiro JW, Putonti C. 2018. Gene co-occurrence networks reflect bacteriophage ecology and evolution. mBio 9:2e01870–17
    [Google Scholar]
  110. 110.
    Shi M, Lin X-D, Chen X, Tian J-H, Chen L-J et al. 2018. The evolutionary history of vertebrate RNA viruses. Nature 556:7700197–202
    [Google Scholar]
  111. 111.
    Siegrist MS, Unnikrishnan M, McConnell MJ, Borowsky M, Cheng T-Y et al. 2009. Mycobacterial Esx-3 is required for mycobactin-mediated iron acquisition. PNAS 106:4418792–97
    [Google Scholar]
  112. 112.
    Simeone R, Bobard A, Lippmann J, Bitter W, Majlessi L et al. 2012. Phagosomal rupture by Mycobacterium tuberculosis results in toxicity and host cell death. PLOS Pathog 8:2e1002507
    [Google Scholar]
  113. 113.
    Simeone R, Sayes F, Song O, Gröschel MI, Brodin P et al. 2015. Cytosolic access of Mycobacterium tuberculosis: critical impact of phagosomal acidification control and demonstration of occurrence in vivo. PLOS Pathog 11:2e1004650
    [Google Scholar]
  114. 114.
    Smith TM, Youngblom MA, Kernien JF, Mohamed MA, Fry SS et al. 2022. Rapid adaptation of a complex trait during experimental evolution of Mycobacterium tuberculosis. eLife 11:e78454
    [Google Scholar]
  115. 115.
    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. PNAS 94:9869–74
    [Google Scholar]
  116. 116.
    Sun J, Siroy A, Lokareddy RK, Speer A, Doornbos KS et al. 2015. The tuberculosis necrotizing toxin kills macrophages by hydrolyzing NAD. Nat. Struct. Mol. Biol. 22:9672–78
    [Google Scholar]
  117. 117.
    Supply P, Marceau M, Mangenot S, Roche D, Rouanet C et al. 2013. Genomic analysis of smooth tubercle bacilli provides insights into ancestry and pathoadaptation of Mycobacterium tuberculosis. Nat. Genet. 45:2172–79
    [Google Scholar]
  118. 118.
    Tak U, Dokland T, Niederweis M. 2021. Pore-forming Esx proteins mediate toxin secretion by Mycobacterium tuberculosis. Nat. Commun. 12:1394
    [Google Scholar]
  119. 119.
    Tufariello JM, Chapman JR, Kerantzas CA, Wong K-W, Vilchèze C et al. 2016. Separable roles for Mycobacterium tuberculosis ESX-3 effectors in iron acquisition and virulence. PNAS 113:3E348–57
    [Google Scholar]
  120. 120.
    Ummels R, Abdallah AM, Kuiper V, Aâjoud A, Sparrius M et al. 2014. Identification of a novel conjugative plasmid in mycobacteria that requires both type IV and type VII secretion. mBio 5:5e01744–14
    [Google Scholar]
  121. 121.
    van der Wel N, Hava D, Houben D, Fluitsma D, van Zon M et al. 2007. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129:71287–98
    [Google Scholar]
  122. 122.
    van der Woude AD, Sarkar D, Bhatt A, Sparrius M, Raadsen SA et al. 2012. Unexpected link between lipooligosaccharide biosynthesis and surface protein release in Mycobacterium marinum. J. Biol. Chem. 287:2420417–29
    [Google Scholar]
  123. 123.
    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
    [Google Scholar]
  124. 124.
    Wang J, Behr MA. 2014. Building a better bacillus: the emergence of Mycobacterium tuberculosis. Front. Microbiol. 5:139
    [Google Scholar]
  125. 125.
    World Health Organ 2020. Global tuberculosis report 2020 Rep. World Health Organ. Geneva:
    [Google Scholar]
  126. 126.
    Young DB, Comas I, de Carvalho LPS. 2015. Phylogenetic analysis of vitamin B12-related metabolism in Mycobacterium tuberculosis. Front. Mol. Biosci. 2:6
    [Google Scholar]
/content/journals/10.1146/annurev-micro-121321-093031
Loading
/content/journals/10.1146/annurev-micro-121321-093031
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error