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The Rich Tapestry of Bacterial Protein Translocation Systems

  • Peter J. ChristieEmail author
Article

Abstract

The translocation of proteins across membranes is a fundamental cellular function. Bacteria have evolved a striking array of pathways for delivering proteins into or across cytoplasmic membranes and, when present, outer membranes. Translocated proteins can form part of the membrane landscape, reside in the periplasmic space situated between the inner and outer membranes of Gram-negative bacteria, deposit on the cell surface, or be released to the extracellular milieu or injected directly into target cells. One protein translocation system, the general secretory pathway, is conserved in all domains of life. A second, the twin-arginine translocation pathway, is also phylogenetically distributed among most bacteria and plant chloroplasts. While all cell types have evolved additional systems dedicated to the translocation of protein cargoes, the number of such systems in bacteria is now known to exceed nine. These dedicated protein translocation systems, which include the types 1 through 9 secretion systems (T1SSs–T9SSs), the chaperone–usher pathway, and type IV pilus system, are the subject of this review. Most of these systems were originally identified and have been extensively characterized in Gram-negative or diderm (two-membrane) species. It is now known that several of these systems also have been adapted to function in Gram-positive or monoderm (single-membrane) species, and at least one pathway is found only in monoderms. This review briefly summarizes the distinctive mechanistic and structural features of each dedicated pathway, as well as the shared properties, that together account for the broad biological diversity of protein translocation in bacteria.

Keywords

Protein translocation Pilus Pathogenesis Traffic ATPases 

Notes

Acknowledgements

This work was supported by the National Institute of General Medical Sciences (Grants R01GM48746, R35GM131892).

References

  1. 1.
    Green ER, Mecsas J (2016) Bacterial secretion systems: an overview. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.VMBF-0012-2015 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Gerlach RG, Hensel M (2007) Protein secretion systems and adhesins: the molecular armory of Gram-negative pathogens. Int J Med Microbiol 297:401–415CrossRefPubMedGoogle Scholar
  3. 3.
    Berks BC (2015) The twin-arginine protein translocation pathway. Annu Rev Biochem 84:843–864CrossRefPubMedGoogle Scholar
  4. 4.
    Tsirigotaki A, De Geyter J, Sostaric N, Economou A, Karamanou S (2017) Protein export through the bacterial Sec pathway. Nat Rev Microbiol 15:21–36CrossRefPubMedGoogle Scholar
  5. 5.
    Costa TR, Felisberto-Rodrigues C, Meir A, Prevost MS, Redzej A et al (2015) Secretion systems in Gram-negative bacteria: structural and mechanistic insights. Nat Rev Microbiol 13:343–359CrossRefPubMedGoogle Scholar
  6. 6.
    Galan JE, Waksman G (2018) Protein-injection machines in bacteria. Cell 172:1306–1318CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Oikonomou CM, Jensen GJ (2019) Electron cryotomography of bacterial secretion systems. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.PSIB-0019-2018 CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Bernstein HD (2019) Type V secretion in Gram-negative bacteria. EcoSal Plus.  https://doi.org/10.1128/ecosalplus.ESP-0031-2018 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Fan E, Chauhan N, Udatha DB, Leo JC, Linke D (2016) Type V secretion systems in bacteria. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.VMBF-0009-2015 CrossRefPubMedGoogle Scholar
  10. 10.
    Nash ZM, Cotter PA (2019) Bordetella filamentous hemagglutinin, a model for the two-partner secretion pathway. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.PSIB-0024-2018 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Henderson IR, Nataro JP (2001) Virulence functions of autotransporter proteins. Infect Immun 69:1231–1243CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Oomen CJ, van Ulsen P, van Gelder P, Feijen M, Tommassen J et al (2004) Structure of the translocator domain of a bacterial autotransporter. EMBO J 23:1257–1266CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    van den Berg B (2010) Crystal structure of a full-length autotransporter. J Mol Biol 396:627–633CrossRefPubMedGoogle Scholar
  14. 14.
    Ruiz-Perez F, Henderson IR, Leyton DL, Rossiter AE, Zhang Y et al (2009) Roles of periplasmic chaperone proteins in the biogenesis of serine protease autotransporters of Enterobacteriaceae. J Bacteriol 191:6571–6583CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Ieva R, Bernstein HD (2009) Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane. Proc Natl Acad Sci USA 106:19120–19125CrossRefPubMedGoogle Scholar
  16. 16.
    Pavlova O, Peterson JH, Ieva R, Bernstein HD (2013) Mechanistic link between beta barrel assembly and the initiation of autotransporter secretion. Proc Natl Acad Sci USA 110:E938–E947CrossRefPubMedGoogle Scholar
  17. 17.
    Albenne C, Ieva R (2017) Job contenders: roles of the beta-barrel assembly machinery and the translocation and assembly module in autotransporter secretion. Mol Microbiol 106:505–517CrossRefPubMedGoogle Scholar
  18. 18.
    Kang’ethe W, Bernstein HD (2013) Charge-dependent secretion of an intrinsically disordered protein via the autotransporter pathway. Proc Natl Acad Sci USA 110:E4246–E4255CrossRefPubMedGoogle Scholar
  19. 19.
    Velarde JJ, Nataro JP (2004) Hydrophobic residues of the autotransporter EspP linker domain are important for outer membrane translocation of its passenger. J Biol Chem 279:31495–31504CrossRefPubMedGoogle Scholar
  20. 20.
    Baclayon M, Ulsen P, Mouhib H, Shabestari MH, Verzijden T et al (2016) Mechanical unfolding of an autotransporter passenger protein reveals the secretion starting point and processive transport intermediates. ACS Nano 10:5710–5719CrossRefPubMedGoogle Scholar
  21. 21.
    Besingi RN, Chaney JL, Clark PL (2013) An alternative outer membrane secretion mechanism for an autotransporter protein lacking a C-terminal stable core. Mol Microbiol 90:1028–1045CrossRefPubMedGoogle Scholar
  22. 22.
    Shen HH, Leyton DL, Shiota T, Belousoff MJ, Noinaj N et al (2014) Reconstitution of a nanomachine driving the assembly of proteins into bacterial outer membranes. Nat Commun 5:5078CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Stubenrauch CJ, Lithgow T (2019) The TAM: a translocation and assembly module of the beta-barrel assembly machinery in bacterial outer membranes. EcoSal Plus.  https://doi.org/10.1128/ecosalplus.ESP-0036-2018 CrossRefPubMedGoogle Scholar
  24. 24.
    Bamert RS, Lundquist K, Hwang H, Webb CT, Shiota T et al (2017) Structural basis for substrate selection by the translocation and assembly module of the beta-barrel assembly machinery. Mol Microbiol 106:142–156CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Hospenthal MK, Waksman G (2019) The remarkable biomechanical properties of the Type 1 chaperone-usher pilus: a structural and molecular perspective. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.PSIB-0010-2018 CrossRefPubMedGoogle Scholar
  26. 26.
    Wright KJ, Seed PC, Hultgren SJ (2007) Development of intracellular bacterial communities of uropathogenic Escherichia coli depends on type 1 pili. Cell Microbiol 9:2230–2241CrossRefPubMedGoogle Scholar
  27. 27.
    Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ (2015) Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 13:269–284CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Psonis JJ, Thanassi DG (2019) Therapeutic approaches targeting the assembly and function of chaperone-usher pili. EcoSal Plus.  https://doi.org/10.1128/ecosalplus.ESP-0033-2018 CrossRefPubMedGoogle Scholar
  29. 29.
    Thomas WE, Nilsson LM, Forero M, Sokurenko EV, Vogel V (2004) Shear-dependent ‘stick-and-roll’ adhesion of type 1 fimbriated Escherichia coli. Mol Microbiol 53:1545–1557CrossRefPubMedGoogle Scholar
  30. 30.
    Hung CS, Bouckaert J, Hung D, Pinkner J, Widberg C et al (2002) Structural basis of tropism of Escherichia coli to the bladder during urinary tract infection. Mol Microbiol 44:903–915CrossRefPubMedGoogle Scholar
  31. 31.
    Jacob-Dubuisson F, Striker R, Hultgren SJ (1994) Chaperone-assisted self-assembly of pili independent of cellular energy. J Biol Chem 269:12447–12455PubMedGoogle Scholar
  32. 32.
    Sauer FG, Futterer K, Pinkner JS, Dodson KW, Hultgren SJ et al (1999) Structural basis of chaperone function and pilus biogenesis. Science 285:1058–1061CrossRefPubMedGoogle Scholar
  33. 33.
    Choudhury D, Thompson A, Stojanoff V, Langermann S, Pinkner J et al (1999) X-ray structure of the FimC-FimH chaperone-adhesin complex from uropathogenic Escherichia coli. Science 285:1061–1066CrossRefPubMedGoogle Scholar
  34. 34.
    Nishiyama M, Horst R, Eidam O, Herrmann T, Ignatov O et al (2005) Structural basis of chaperone-subunit complex recognition by the type 1 pilus assembly platform FimD. EMBO J 24:2075–2086CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Remaut H, Tang C, Henderson NS, Pinkner JS, Wang T et al (2008) Fiber formation across the bacterial outer membrane by the chaperone/usher pathway. Cell 133:640–652CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Remaut H, Rose RJ, Hannan TJ, Hultgren SJ, Radford SE et al (2006) Donor-strand exchange in chaperone-assisted pilus assembly proceeds through a concerted beta strand displacement mechanism. Mol Cell 22:831–842CrossRefPubMedGoogle Scholar
  37. 37.
    Allen WJ, Phan G, Waksman G (2012) Pilus biogenesis at the outer membrane of Gram-negative bacterial pathogens. Curr Opin Struct Biol.  https://doi.org/10.1016/j.sbi.2012.02.001 CrossRefPubMedGoogle Scholar
  38. 38.
    Morrissey B, Leney AC, Toste Rego A, Phan G, Allen WJ et al (2012) The role of chaperone-subunit usher domain interactions in the mechanism of bacterial pilus biogenesis revealed by ESI-MS. Molec Cell Proteom 11(M111):015289Google Scholar
  39. 39.
    Huang Y, Smith BS, Chen LX, Baxter RH, Deisenhofer J (2009) Insights into pilus assembly and secretion from the structure and functional characterization of usher PapC. Proc Natl Acad Sci USA 106:7403–7407CrossRefPubMedGoogle Scholar
  40. 40.
    Phan G, Remaut H, Wang T, Allen WJ, Pirker KF et al (2011) Crystal structure of the FimD usher bound to its cognate FimC-FimH substrate. Nature 474:49–53CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Werneburg GT, Henderson NS, Portnoy EB, Sarowar S, Hultgren SJ et al (2015) The pilus usher controls protein interactions via domain masking and is functional as an oligomer. Nat Struct Mol Biol 22:540–546CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Li Q, Ng TW, Dodson KW, So SS, Bayle KM et al (2010) The differential affinity of the usher for chaperone-subunit complexes is required for assembly of complete pili. Mol Microbiol 76:159–172CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Labigne-Roussel A, Schmidt MA, Walz W, Falkow S (1985) Genetic organization of the afimbrial adhesin operon and nucleotide sequence from a uropathogenic Escherichia coli gene encoding an afimbrial adhesin. J Bacteriol 162:1285–1292PubMedPubMedCentralGoogle Scholar
  44. 44.
    Gaastra W, Svennerholm AM (1996) Colonization factors of human enterotoxigenic Escherichia coli (ETEC). Trends Microbiol 4:444–452CrossRefPubMedGoogle Scholar
  45. 45.
    Titball RW, Howells AM, Oyston PC, Williamson ED (1997) Expression of the Yersinia pestis capsular antigen (F1 antigen) on the surface of an aroA mutant of Salmonella typhimurium induces high levels of protection against plague. Infect Immun 65:1926–1930PubMedPubMedCentralGoogle Scholar
  46. 46.
    Stubenrauch C, Belousoff MJ, Hay ID, Shen HH, Lillington J et al (2016) Effective assembly of fimbriae in Escherichia coli depends on the translocation assembly module nanomachine. Nat Microbiol 1:16064CrossRefPubMedGoogle Scholar
  47. 47.
    Bhoite S, van Gerven N, Chapman MR, Remaut H (2019) Curli biogenesis: bacterial amyloid assembly by the Type VIII secretion pathway. EcoSal Plus.  https://doi.org/10.1128/ecosalplus.ESP-0037-2018 CrossRefPubMedGoogle Scholar
  48. 48.
    Dueholm MS, Albertsen M, Otzen D, Nielsen PH (2012) Curli functional amyloid systems are phylogenetically widespread and display large diversity in operon and protein structure. PLoS ONE 7:e51274CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Kikuchi T, Mizunoe Y, Takade A, Naito S, Yoshida S (2005) Curli fibers are required for development of biofilm architecture in Escherichia coli K-12 and enhance bacterial adherence to human uroepithelial cells. Microbiol Immunol 49:875–884CrossRefPubMedGoogle Scholar
  50. 50.
    Hufnagel DA, Depas WH, Chapman MR (2015) The biology of the Escherichia coli extracellular matrix. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.MB-0014-2014 CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Tukel C, Raffatellu M, Humphries AD, Wilson RP, Andrews-Polymenis HL et al (2005) CsgA is a pathogen-associated molecular pattern of Salmonella enterica serotype Typhimurium that is recognized by Toll-like receptor 2. Mol Microbiol 58:289–304CrossRefPubMedGoogle Scholar
  52. 52.
    Van Gerven N, Van der Verren SE, Reiter DM, Remaut H (2018) The role of functional amyloids in bacterial virulence. J Mol Biol 430:3657–3684CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Hung C, Zhou Y, Pinkner JS, Dodson KW, Crowley JR et al (2013) Escherichia coli biofilms have an organized and complex extracellular matrix structure. MBio 4:e00645-00613Google Scholar
  54. 54.
    Chapman MR, Robinson LS, Pinkner JS, Roth R, Heuser J et al (2002) Role of Escherichia coli curli operons in directing amyloid fiber formation. Science 295:851–855CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Evans ML, Chorell E, Taylor JD, Aden J, Gotheson A et al (2015) The bacterial curli system possesses a potent and selective inhibitor of amyloid formation. Mol Cell 57:445–455CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Robinson LS, Ashman EM, Hultgren SJ, Chapman MR (2006) Secretion of curli fibre subunits is mediated by the outer membrane-localized CsgG protein. Mol Microbiol 59:870–881CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Goyal P, Krasteva PV, Van Gerven N, Gubellini F, Van den Broeck I et al (2014) Structural and mechanistic insights into the bacterial amyloid secretion channel CsgG. Nature 516:250–253CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Nenninger AA, Robinson LS, Hammer ND, Epstein EA, Badtke MP et al (2011) CsgE is a curli secretion specificity factor that prevents amyloid fibre aggregation. Mol Microbiol 81:486–499CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Van Gerven N, Goyal P, Vandenbussche G, De Kerpel M, Jonckheere W et al (2014) Secretion and functional display of fusion proteins through the curli biogenesis pathway. Mol Microbiol 91:1022–1035CrossRefPubMedGoogle Scholar
  60. 60.
    Hammer ND, McGuffie BA, Zhou Y, Badtke MP, Reinke AA et al (2012) The C-terminal repeating units of CsgB direct bacterial functional amyloid nucleation. J Mol Biol 422:376–389CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Nenninger AA, Robinson LS, Hultgren SJ (2009) Localized and efficient curli nucleation requires the chaperone-like amyloid assembly protein CsgF. Proc Natl Acad Sci USA 106:900–905CrossRefPubMedGoogle Scholar
  62. 62.
    Dunstan RA, Hay ID, Wilksch JJ, Schittenhelm RB, Purcell AW et al (2015) Assembly of the secretion pores GspD, Wza and CsgG into bacterial outer membranes does not require the Omp85 proteins BamA or TamA. Mol Microbiol 97:616–629CrossRefPubMedGoogle Scholar
  63. 63.
    Korotkov KV, Sandkvist M (2019) Architecture, function, and substrates of the Type II secretion system. EcoSal Plus.  https://doi.org/10.1128/ecosalplus.ESP-0034-2018 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Cianciotto NP, White RC (2017) Expanding role of Type II secretion in bacterial pathogenesis and beyond. Infect Immun 85:e00014–e00017.  https://doi.org/10.1128/IAI.00014-17 CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Ferrandez Y, Condemine G (2008) Novel mechanism of outer membrane targeting of proteins in Gram-negative bacteria. Mol Microbiol 69:1349–1357CrossRefPubMedGoogle Scholar
  66. 66.
    East A, Mechaly AE, Huysmans GHM, Bernarde C, Tello-Manigne D et al (2016) Structural basis of pullulanase bembrane binding and secretion revealed by X-ray crystallography, molecular dynamics and biochemical analysis. Structure 24:92–104CrossRefPubMedGoogle Scholar
  67. 67.
    Sauvonnet N, Vignon G, Pugsley AP, Gounon P (2000) Pilus formation and protein secretion by the same machinery in Escherichia coli. EMBO J 19:2221–2228CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Korotkov KV, Sandkvist M, Hol WG (2012) The type II secretion system: biogenesis, molecular architecture and mechanism. Nat Rev Microbiol 10:336–351CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Hay ID, Belousoff MJ, Lithgow T (2017) Structural Basis of Type 2 secretion system engagement between the inner and outer bacterial membranes. MBio.  https://doi.org/10.1128/mBio.01344-17 CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Majewski DD, Worrall LJ, Strynadka NC (2018) Secretins revealed: structural insights into the giant gated outer membrane portals of bacteria. Curr Opin Struct Biol 51:61–72CrossRefPubMedGoogle Scholar
  71. 71.
    Lopez-Castilla A, Thomassin JL, Bardiaux B, Zheng W, Nivaskumar M et al (2017) Structure of the calcium-dependent type 2 secretion pseudopilus. Nat Microbiol 2:1686–1695CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Nouwen N, Ranson N, Saibil H, Wolpensinger B, Engel A et al (1999) Secretin PulD: association with pilot PulS, structure, and ion-conducting channel formation. Proc Natl Acad Sci USA 96:8173–8177CrossRefPubMedGoogle Scholar
  73. 73.
    Hoang HH, Nickerson NN, Lee VT, Kazimirova A, Chami M et al (2011) Outer membrane targeting of Pseudomonas aeruginosa proteins shows variable dependence on the components of Bam and Lol machineries. MBio.  https://doi.org/10.1128/mBio.00246-11 CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Camberg JL, Sandkvist M (2005) Molecular analysis of the Vibrio cholerae type II secretion ATPase EpsE. J Bacteriol 187:249–256CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Sandkvist M (2001) Biology of type II secretion. Mol Microbiol 40:271–283CrossRefPubMedGoogle Scholar
  76. 76.
    McCallum M, Burrows LL, Howell PL (2019) The dynamic structures of the type IV pilus. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.PSIB-0006-2018 CrossRefPubMedGoogle Scholar
  77. 77.
    Craig L, Forest KT, Maier B (2019) Type IV pili: dynamics, biophysics and functional consequences. Nat Rev Microbiol.  https://doi.org/10.1038/s41579-019-0195-4 CrossRefPubMedGoogle Scholar
  78. 78.
    Ellison CK, Dalia TN, Vidal Ceballos A, Wang JC, Biais N et al (2018) Retraction of DNA-bound type IV competence pili initiates DNA uptake during natural transformation in Vibrio cholerae. Nat Microbiol 3:773–780CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Clausen M, Jakovljevic V, Sogaard-Andersen L, Maier B (2009) High-force generation is a conserved property of type IV pilus systems. J Bacteriol 191:4633–4638CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Ellison CK, Kan J, Dillard RS, Kysela DT, Ducret A et al (2017) Obstruction of pilus retraction stimulates bacterial surface sensing. Science 358:535–538CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Zollner R, Cronenberg T, Maier B (2019) Motor properties of PilT-independent type 4 pilus retraction in gonococci. J Bacteriol.  https://doi.org/10.1128/JB.00778-18 CrossRefPubMedGoogle Scholar
  82. 82.
    Muschiol S, Aschtgen MS, Nannapaneni P, Henriques-Normark B (2019) Gram-positive type IV pili and competence. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.PSIB-0011-2018 CrossRefPubMedGoogle Scholar
  83. 83.
    Kirn TJ, Bose N, Taylor RK (2003) Secretion of a soluble colonization factor by the TCP type 4 pilus biogenesis pathway in Vibrio cholerae. Mol Microbiol 49:81–92CrossRefPubMedGoogle Scholar
  84. 84.
    Albers SV, Szabo Z, Driessen AJ (2006) Protein secretion in the archaea: multiple paths towards a unique cell surface. Nat Rev Microbiol 4:537–547CrossRefPubMedGoogle Scholar
  85. 85.
    Chaudhury P, Quax TEF, Albers SV (2018) Versatile cell surface structures of archaea. Mol Microbiol 107:298–311CrossRefPubMedGoogle Scholar
  86. 86.
    Sato K, Naito M, Yukitake H, Hirakawa H, Shoji M et al (2010) A protein secretion system linked to bacteroidete gliding motility and pathogenesis. Proc Natl Acad Sci USA 107:276–281CrossRefPubMedGoogle Scholar
  87. 87.
    McBride MJ (2019) Bacteroidetes gliding motility and the type IX secretion system. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.PSIB-0002-2018 CrossRefPubMedGoogle Scholar
  88. 88.
    Seers CA, Slakeski N, Veith PD, Nikolof T, Chen YY et al (2006) The RgpB C-terminal domain has a role in attachment of RgpB to the outer membrane and belongs to a novel C-terminal-domain family found in Porphyromonas gingivalis. J Bacteriol 188:6376–6386CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    de Diego I, Ksiazek M, Mizgalska D, Koneru L, Golik P et al (2016) The outer-membrane export signal of Porphyromonas gingivalis type IX secretion system (T9SS) is a conserved C-terminal beta-sandwich domain. Sci Rep 6:23123CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Johnston JJ, Shrivastava A, McBride MJ (2018) Untangling Flavobacterium johnsoniae gliding motility and protein secretion. J Bacteriol 200:e00362-17.  https://doi.org/10.1128/JB.00362-17 CrossRefPubMedGoogle Scholar
  91. 91.
    Nakane D, Sato K, Wada H, McBride MJ, Nakayama K (2013) Helical flow of surface protein required for bacterial gliding motility. Proc Natl Acad Sci USA 110:11145–11150CrossRefPubMedGoogle Scholar
  92. 92.
    Lauber F, Deme JC, Lea SM, Berks BC (2018) Type 9 secretion system structures reveal a new protein transport mechanism. Nature 564:77–82CrossRefPubMedGoogle Scholar
  93. 93.
    Glew MD, Veith PD, Chen D, Gorasia DG, Peng B et al (2017) PorV is an outer membrane shuttle protein for the type IX secretion system. Sci Rep 7:8790CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Veith PD, Glew MD, Gorasia DG, Reynolds EC (2017) Type IX secretion: the generation of bacterial cell surface coatings involved in virulence, gliding motility and the degradation of complex biopolymers. Mol Microbiol 106:35–53CrossRefPubMedGoogle Scholar
  95. 95.
    Nelson SS, Bollampalli S, McBride MJ (2008) SprB is a cell surface component of the Flavobacterium johnsoniae gliding motility machinery. J Bacteriol 190:2851–2857CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Shrivastava A, Rhodes RG, Pochiraju S, Nakane D, McBride MJ (2012) Flavobacterium johnsoniae RemA is a mobile cell surface lectin involved in gliding. J Bacteriol 194:3678–3688CrossRefPubMedPubMedCentralGoogle Scholar
  97. 97.
    Shrivastava A, Berg HC (2015) Towards a model for Flavobacterium gliding. Curr Opin Microbiol 28:93–97CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Higgins CF, Hiles ID, Salmond GP, Gill DR, Downie JA et al (1986) A family of related ATP-binding subunits coupled to many distinct biological processes in bacteria. Nature 323:448–450CrossRefPubMedGoogle Scholar
  99. 99.
    Holland IB, Peherstorfer S, Kanonenberg K, Lenders M, Reimann S et al (2016) Type I protein secretion-deceptively simple yet with a wide range of mechanistic variability across the family. EcoSal Plus.  https://doi.org/10.1128/ecosalplus.ESP-0019-2015 CrossRefPubMedGoogle Scholar
  100. 100.
    Spitz O, Erenburg IN, Beer T, Kanonenberg K, Holland IB et al (2019) Type I secretion systems—one mechanism for all? Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.PSIB-0003-2018 CrossRefPubMedGoogle Scholar
  101. 101.
    Letoffe S, Wandersman C (1992) Secretion of CyaA-PrtB and HlyA-PrtB fusion proteins in Escherichia coli: involvement of the glycine-rich repeat domain of Erwinia chrysanthemi protease B. J Bacteriol 174:4920–4927CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Lecher J, Schwarz CK, Stoldt M, Smits SH, Willbold D et al (2012) An RTX transporter tethers its unfolded substrate during secretion via a unique N-terminal domain. Structure 20:1778–1787CrossRefPubMedGoogle Scholar
  103. 103.
    Sanchez-Magraner L, Viguera AR, Garcia-Pacios M, Garcillan MP, Arrondo JL et al (2007) The calcium-binding C-terminal domain of Escherichia coli alpha-hemolysin is a major determinant in the surface-active properties of the protein. J Biol Chem 282:11827–11835CrossRefPubMedGoogle Scholar
  104. 104.
    Thanabalu T, Koronakis E, Hughes C, Koronakis V (1998) Substrate-induced assembly of a contiguous channel for protein export from E.coli: reversible bridging of an inner-membrane translocase to an outer membrane exit pore. EMBO J 17:6487–6496CrossRefPubMedPubMedCentralGoogle Scholar
  105. 105.
    Du D, Wang Z, James NR, Voss JE, Klimont E et al (2014) Structure of the AcrAB-TolC multidrug efflux pump. Nature 509:512–515CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Koronakis V, Sharff A, Koronakis E, Luisi B, Hughes C (2000) Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature 405:914–919CrossRefPubMedGoogle Scholar
  107. 107.
    Balakrishnan L, Hughes C, Koronakis V (2001) Substrate-triggered recruitment of the TolC channel-tunnel during type I export of hemolysin by Escherichia coli. J Mol Biol 313:501–510CrossRefPubMedGoogle Scholar
  108. 108.
    Lenders MH, Weidtkamp-Peters S, Kleinschrodt D, Jaeger KE, Smits SH et al (2015) Directionality of substrate translocation of the hemolysin A type I secretion system. Sci Rep 5:12470CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Smith TJ, Font ME, Kelly CM, Sondermann H, O’Toole GA (2018) An N-terminal retention module anchors the giant adhesin LapA of Pseudomonas fluorescens at the cell surface: a novel subfamily of type I secretion systems. J Bacteriol.  https://doi.org/10.1128/JB.00734-17 CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Guo S, Stevens CA, Vance TDR, Olijve LLC, Graham LA et al (2017) Structure of a 1.5-MDa adhesin that binds its Antarctic bacterium to diatoms and ice. Sci Adv 3:e1701440CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Smith TJ, Sondermann H, O’Toole GA (2018) Type 1 does the two-step: type 1 secretion substrates with a functional periplasmic intermediate. J Bacteriol.  https://doi.org/10.1128/JB.00168-18 CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Deng W, Marshall NC, Rowland JL, McCoy JM, Worrall LJ et al (2017) Assembly, structure, function and regulation of type III secretion systems. Nat Rev Microbiol 15:323–337CrossRefPubMedGoogle Scholar
  113. 113.
    Diepold A, Armitage JP (2015) Type III secretion systems: the bacterial flagellum and the injectisome. Philos Trans R Soc Lond B Biol Sci 370:20150020.  https://doi.org/10.1098/rstb.2015.0020 CrossRefPubMedPubMedCentralGoogle Scholar
  114. 114.
    Lara-Tejero M, Galan JE (2019) The injectisome, a complex nanomachine for protein injection into mammalian cells. EcoSal Plus.  https://doi.org/10.1128/ecosalplus.ESP-0039-2018 CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    McDermott JE, Corrigan A, Peterson E, Oehmen C, Niemann G et al (2011) Computational prediction of type III and IV secreted effectors in gram-negative bacteria. Infect Immun 79:23–32CrossRefPubMedGoogle Scholar
  116. 116.
    Anderson DM, Schneewind O (1997) A mRNA signal for the type III secretion of Yop proteins by Yersinia enterocolitica. Science 278:1140–1143CrossRefPubMedGoogle Scholar
  117. 117.
    Niemann GS, Brown RN, Mushamiri IT, Nguyen NT, Taiwo R et al (2013) RNA type III secretion signals that require Hfq. J Bacteriol 195:2119–2125CrossRefPubMedPubMedCentralGoogle Scholar
  118. 118.
    Lee SH, Galan JE (2004) Salmonella type III secretion-associated chaperones confer secretion-pathway specificity. Mol Microbiol 51:483–495CrossRefPubMedGoogle Scholar
  119. 119.
    Deng W, Yu HB, Li Y, Finlay BB (2015) SepD/SepL-dependent secretion signals of the type III secretion system translocator proteins in enteropathogenic Escherichia coli. J Bacteriol 197:1263–1275CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Radics J, Konigsmaier L, Marlovits TC (2014) Structure of a pathogenic type 3 secretion system in action. Nat Struct Mol Biol 21:82–87CrossRefPubMedGoogle Scholar
  121. 121.
    Hu B, Lara-Tejero M, Kong Q, Galan JE, Liu J (2017) In situ molecular architecture of the Salmonella type III secretion machine. Cell 168(1065–1074):e1010Google Scholar
  122. 122.
    Park D, Lara-Tejero M, Waxham MN, Li W, Hu B et al (2018) Visualization of the type III secretion mediated Salmonella-host cell interface using cryo-electron tomography. Elife.  https://doi.org/10.7554/eLife.39514 CrossRefPubMedPubMedCentralGoogle Scholar
  123. 123.
    Zhu S, Schniederberend M, Zhitnitsky D, Jain R, Galan JE et al (2019) In situ structures of polar and lateral flagella revealed by cryo-electron tomography. J Bacteriol 201:e00117–e00119.  https://doi.org/10.1128/JB.00117-19 CrossRefPubMedGoogle Scholar
  124. 124.
    Lara-Tejero M, Kato J, Wagner S, Liu X, Galan JE (2011) A sorting platform determines the order of protein secretion in bacterial type III systems. Science 331:1188–1191CrossRefPubMedGoogle Scholar
  125. 125.
    Hu B, Morado DR, Margolin W, Rohde JR, Arizmendi O et al (2015) Visualization of the type III secretion sorting platform of Shigella flexneri. Proc Natl Acad Sci USA 112:1047–1052CrossRefPubMedGoogle Scholar
  126. 126.
    Akeda Y, Galan JE (2005) Chaperone release and unfolding of substrates in type III secretion. Nature 437:911–915CrossRefPubMedGoogle Scholar
  127. 127.
    Wagner S, Konigsmaier L, Lara-Tejero M, Lefebre M, Marlovits TC et al (2010) Organization and coordinated assembly of the type III secretion export apparatus. Proc Natl Acad Sci USA 107:17745–17750CrossRefPubMedGoogle Scholar
  128. 128.
    Kuhlen L, Abrusci P, Johnson S, Gault J, Deme J et al (2018) Structure of the core of the type III secretion system export apparatus. Nat Struct Mol Biol 25:583–590CrossRefPubMedPubMedCentralGoogle Scholar
  129. 129.
    Schraidt O, Marlovits TC (2011) Three-dimensional model of Salmonella’s needle complex at subnanometer resolution. Science 331:1192–1195CrossRefPubMedGoogle Scholar
  130. 130.
    Hu J, Worrall LJ, Hong C, Vuckovic M, Atkinson CE et al (2018) Cryo-EM analysis of the T3S injectisome reveals the structure of the needle and open secretin. Nat Commun 9:3840.  https://doi.org/10.1038/s41467-018-06298-8 CrossRefPubMedPubMedCentralGoogle Scholar
  131. 131.
    Epler CR, Dickenson NE, Bullitt E, Picking WL (2012) Ultrastructural analysis of IpaD at the tip of the nascent MxiH type III secretion apparatus of Shigella flexneri. J Mol Biol 420:29–39CrossRefPubMedPubMedCentralGoogle Scholar
  132. 132.
    Li YG, Hu B, Christie PJ (2019) Biological and structural diversity of type IV secretion systems. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.PSIB-0012-2018 CrossRefPubMedPubMedCentralGoogle Scholar
  133. 133.
    Lang S, Zechner EL (2012) General requirements for protein secretion by the F-like conjugation system R1. Plasmid.  https://doi.org/10.1016/j.plasmid.2011.12.014 CrossRefPubMedPubMedCentralGoogle Scholar
  134. 134.
    Redzej A, Ilangovan A, Lang S, Gruber CJ, Topf M et al (2013) Structure of a translocation signal domain mediating conjugative transfer by type IV secretion systems. Mol Microbiol 89:324–333CrossRefPubMedPubMedCentralGoogle Scholar
  135. 135.
    de la Cruz F, Frost LS, Meyer RJ, Zechner EL (2010) Conjugative DNA metabolism in Gram-negative bacteria. FEMS Micro Rev 34:18–40CrossRefGoogle Scholar
  136. 136.
    Cascales E, Christie PJ (2003) The versatile bacterial type IV secretion systems. Nat Rev Microbiol 1:137–150CrossRefPubMedGoogle Scholar
  137. 137.
    Gonzalez-Rivera C, Bhatty M, Christie PJ (2016) Mechanism and function of type IV secretion during infection of the human host. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.VMBF-0024-2015 CrossRefPubMedPubMedCentralGoogle Scholar
  138. 138.
    Souza DP, Oka GU, Alvarez-Martinez CE, Bisson-Filho AW, Dunger G et al (2015) Bacterial killing via a type IV secretion system. Nat Commun 6:6453.  https://doi.org/10.1038/ncomms7453 CrossRefPubMedGoogle Scholar
  139. 139.
    Nas MY, White RC, DuMont AL, Lopez AE, Cianciotto NP (2019) Stenotrophomonas maltophilia encodes a VirB/D4 type IV secretion system that modulates apoptosis in human cells and promotes competition against heterologous bacteria including Pseudomonas aeruginosa. Infect Immun.  https://doi.org/10.1128/IAI.00457-19 CrossRefPubMedGoogle Scholar
  140. 140.
    Ghigo JM (2001) Natural conjugative plasmids induce bacterial biofilm development. Nature 412:442–445CrossRefPubMedGoogle Scholar
  141. 141.
    Arutyunov D, Frost LS (2013) F conjugation: back to the beginning. Plasmid 70:18–32CrossRefPubMedGoogle Scholar
  142. 142.
    Christie PJ, Atmakuri K, Krishnamoorthy V, Jakubowski S, Cascales E (2005) Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu Rev Microbiol 59:451–485CrossRefPubMedGoogle Scholar
  143. 143.
    Fronzes R, Schafer E, Wang L, Saibil HR, Orlova EV et al (2009) Structure of a type IV secretion system core complex. Science 323:266–268CrossRefPubMedGoogle Scholar
  144. 144.
    Chandran V, Fronzes R, Duquerroy S, Cronin N, Navaza J et al (2009) Structure of the outer membrane complex of a type IV secretion system. Nature 462:1011–1015CrossRefPubMedPubMedCentralGoogle Scholar
  145. 145.
    Low HH, Gubellini F, Rivera-Calzada A, Braun N, Connery S et al (2014) Structure of a type IV secretion system. Nature 508:550–553CrossRefPubMedPubMedCentralGoogle Scholar
  146. 146.
    Chetrit D, Hu B, Christie PJ, Roy CR, Liu J (2018) A unique cytoplasmic ATPase complex defines the Legionella pneumophila type IV secretion channel. Nat Microbiol 3:678–686CrossRefPubMedPubMedCentralGoogle Scholar
  147. 147.
    Hu B, Khara P, Song L, Lin AS, Frick-Cheng AE et al (2019) In situ molecular architecture of the Helicobacter pylori Cag type IV secretion System. MBio.  https://doi.org/10.1128/mBio.00849-19 CrossRefPubMedPubMedCentralGoogle Scholar
  148. 148.
    Sgro GG, Costa TR, Cenens W, Souza DP, Cassago A et al (2018) CryoEM structure of the core complex of a bacterial killing type IV secretion system. Nat Microbiol 3(12):1429–1440.  https://doi.org/10.1038/s41564-018-0262-z CrossRefPubMedPubMedCentralGoogle Scholar
  149. 149.
    Jakubowski SJ, Kerr JE, Garza I, Krishnamoorthy V, Bayliss R et al (2009) Agrobacterium VirB10 domain requirements for type IV secretion and T pilus biogenesis. Mol Microbiol 71:779–794CrossRefPubMedGoogle Scholar
  150. 150.
    Spudich GM, Fernandez D, Zhou XR, Christie PJ (1996) Intermolecular disulfide bonds stabilize VirB7 homodimers and VirB7/VirB9 heterodimers during biogenesis of the Agrobacterium tumefaciens T-complex transport apparatus. Proc Natl Acad Sci USA 93:7512–7517CrossRefPubMedGoogle Scholar
  151. 151.
    Fernandez D, Spudich GM, Zhou XR, Christie PJ (1996) The Agrobacterium tumefaciens VirB7 lipoprotein is required for stabilization of VirB proteins during assembly of the T-complex transport apparatus. J Bacteriol 178:3168–3176CrossRefPubMedPubMedCentralGoogle Scholar
  152. 152.
    Gonzalez-Rivera C, Khara P, Awad D, Patel R, Li YG et al (2019) Two pKM101-encoded proteins, the pilus-tip protein TraC and Pep, assemble on the Escherichia coli cell surface as adhesins required for efficient conjugative DNA transfer. Mol Microbiol 111:96–117CrossRefPubMedGoogle Scholar
  153. 153.
    Atmakuri K, Cascales E, Christie PJ (2004) Energetic components VirD4, VirB11 and VirB4 mediate early DNA transfer reactions required for bacterial type IV secretion. Mol Microbiol 54:1199–1211CrossRefPubMedGoogle Scholar
  154. 154.
    Cabezon E, Sastre JI, de la Cruz F (1997) Genetic evidence of a coupling role for the TraG protein family in bacterial conjugation. Mol Gen Genet 254:400–406CrossRefPubMedGoogle Scholar
  155. 155.
    Gomis-Ruth FX, Moncalian G, Perez-Luque R, Gonzalez A, Cabezon E et al (2001) The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase. Nature 409:637–641CrossRefPubMedGoogle Scholar
  156. 156.
    Cascales E, Christie PJ (2004) Definition of a bacterial type IV secretion pathway for a DNA substrate. Science 304:1170–1173CrossRefPubMedGoogle Scholar
  157. 157.
    Bhatty M, Laverde Gomez JA, Christie PJ (2013) The expanding bacterial type IV secretion lexicon. Res Microbiol 164:620–639CrossRefPubMedGoogle Scholar
  158. 158.
    Burns DL (2003) Type IV transporters of pathogenic bacteria. Curr Opin Microbiol 6:29–34CrossRefPubMedGoogle Scholar
  159. 159.
    Locht C, Coutte L, Mielcarek N (2011) The ins and outs of pertussis toxin. FEBS J 278:4668–4682.  https://doi.org/10.1111/j.1742-4658.2011.08237.x CrossRefPubMedGoogle Scholar
  160. 160.
    Grohmann E, Christie PJ, Waksman G, Backert S (2018) Type IV secretion in Gram-negative and Gram-positive bacteria. Mol Microbiol 107:455–471CrossRefPubMedPubMedCentralGoogle Scholar
  161. 161.
    Arends K, Celik EK, Probst I, Goessweiner-Mohr N, Fercher C et al (2013) TraG encoded by the pIP501 type IV secretion system is a two domain peptidoglycan degrading enzyme essential for conjugative transfer. J Bacteriol 195(19):4436–4444.  https://doi.org/10.1128/JB.02263-12 CrossRefPubMedPubMedCentralGoogle Scholar
  162. 162.
    Laverde Gomez JA, Bhatty M, Christie PJ (2014) PrgK, a multidomain peptidoglycan hydrolase, is essential for conjugative transfer of the pheromone-responsive plasmid pCF10. J Bacteriol 196:527–539CrossRefPubMedPubMedCentralGoogle Scholar
  163. 163.
    Bhatty M, Cruz MR, Frank KL, Gomez JA, Andrade F et al (2015) Enterococcus faecalis pCF10-encodes surface proteins PrgA, PrgB (aggregation substance) and PrgC contribute to plasmid transfer, biofilm formation and virulence. Mol Microbiol 95:660–677CrossRefPubMedGoogle Scholar
  164. 164.
    Zoued A, Brunet YR, Durand E, Aschtgen MS, Logger L et al (2014) Architecture and assembly of the type VI secretion system. Biochim Biophys Acta 1843:1664–1673CrossRefPubMedGoogle Scholar
  165. 165.
    Taylor NMI, van Raaij MJ, Leiman PG (2018) Contractile injection systems of bacteriophages and related systems. Mol Microbiol 108:6–15CrossRefPubMedGoogle Scholar
  166. 166.
    Alcoforado Diniz J, Liu YC, Coulthurst SJ (2015) Molecular weaponry: diverse effectors delivered by the Type VI secretion system. Cell Microbiol 17:1742–1751CrossRefPubMedPubMedCentralGoogle Scholar
  167. 167.
    Coyne MJ, Comstock LE (2019) Type VI secretion systems and the gut microbiota. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.PSIB-0009-2018 CrossRefPubMedGoogle Scholar
  168. 168.
    Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W et al (2011) Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475:343–347CrossRefPubMedPubMedCentralGoogle Scholar
  169. 169.
    Sana TG, Flaugnatti N, Lugo KA, Lam LH, Jacobson A et al (2016) Salmonella typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut. Proc Natl Acad Sci USA 113:E5044–E5051CrossRefPubMedGoogle Scholar
  170. 170.
    Durand E, Cambillau C, Cascales E, Journet L (2014) VgrG, Tae, Tle, and beyond: the versatile arsenal of Type VI secretion effectors. Trends Microbiol 22:498–507CrossRefPubMedPubMedCentralGoogle Scholar
  171. 171.
    Russell AB, Peterson SB, Mougous JD (2014) Type VI secretion system effectors: poisons with a purpose. Nat Rev Microbiol 12:137–148CrossRefPubMedPubMedCentralGoogle Scholar
  172. 172.
    Wang T, Si M, Song Y, Zhu W, Gao F et al (2015) Type VI secretion system transports Zn2+ to combat multiple stresses and host immunity. PLoS Pathog 11:e1005020CrossRefPubMedPubMedCentralGoogle Scholar
  173. 173.
    Si M, Zhao C, Burkinshaw B, Zhang B, Wei D et al (2017) Manganese scavenging and oxidative stress response mediated by type VI secretion system in Burkholderia thailandensis. Proc Natl Acad Sci USA 114:E2233–E2242CrossRefPubMedGoogle Scholar
  174. 174.
    Lin J, Zhang W, Cheng J, Yang X, Zhu K et al (2017) A Pseudomonas T6SS effector recruits PQS-containing outer membrane vesicles for iron acquisition. Nat Commun 8:14888.  https://doi.org/10.1038/ncomms14888 CrossRefPubMedPubMedCentralGoogle Scholar
  175. 175.
    Saak CC, Gibbs KA (2016) The self-identity protein IdsD Is communicated between cells in swarming Proteus mirabilis colonies. J Bacteriol 198:3278–3286CrossRefPubMedPubMedCentralGoogle Scholar
  176. 176.
    Cascales E (2008) The type VI secretion toolkit. EMBO Rep 9:735–741CrossRefPubMedPubMedCentralGoogle Scholar
  177. 177.
    Shneider MM, Buth SA, Ho BT, Basler M, Mekalanos JJ et al (2013) PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500:350–353CrossRefPubMedPubMedCentralGoogle Scholar
  178. 178.
    Brunet YR, Zoued A, Boyer F, Douzi B, Cascales E (2015) The type VI secretion TssEFGK-VgrG phage-like baseplate Is recruited to the TssJLM membrane complex via multiple contacts and serves as assembly platform for tail tube/sheath polymerization. PLoS Genet 11:e1005545CrossRefPubMedPubMedCentralGoogle Scholar
  179. 179.
    Leiman PG, Basler M, Ramagopal UA, Bonanno JB, Sauder JM et al (2009) Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci USA 106:4154–4159CrossRefPubMedGoogle Scholar
  180. 180.
    Cherrak Y, Rapisarda C, Pellarin R, Bouvier G, Bardiaux B et al (2018) Biogenesis and structure of a type VI secretion baseplate. Nat Microbiol 3:1404–1416CrossRefPubMedGoogle Scholar
  181. 181.
    Rapisarda C, Cherrak Y, Kooger R, Schmidt V, Pellarin R et al (2019) In situ and high-resolution cryo-EM structure of a bacterial type VI secretion system membrane complex. EMBO J 38(10):e100886.  https://doi.org/10.15252/embj.2018100886 CrossRefPubMedPubMedCentralGoogle Scholar
  182. 182.
    Kudryashev M, Wang RY, Brackmann M, Scherer S, Maier T et al (2015) Structure of the type VI secretion system contractile sheath. Cell 160:952–962CrossRefPubMedPubMedCentralGoogle Scholar
  183. 183.
    Wang J, Brackmann M, Castano-Diez D, Kudryashev M, Goldie KN et al (2017) Cryo-EM structure of the extended type VI secretion system sheath-tube complex. Nat Microbiol 2:1507–1512CrossRefPubMedGoogle Scholar
  184. 184.
    Brackmann M, Wang J, Basler M (2018) Type VI secretion system sheath inter-subunit interactions modulate its contraction. EMBO Rep 19:225–233CrossRefPubMedGoogle Scholar
  185. 185.
    Kapitein N, Bonemann G, Pietrosiuk A, Seyffer F, Hausser I et al (2013) ClpV recycles VipA/VipB tubules and prevents non-productive tubule formation to ensure efficient type VI protein secretion. Mol Microbiol 87:1013–1028CrossRefPubMedGoogle Scholar
  186. 186.
    Unterweger D, Kostiuk B, Pukatzki S (2017) Adaptor proteins of type VI secretion system effectors. Trends Microbiol 25:8–10CrossRefPubMedGoogle Scholar
  187. 187.
    Silverman JM, Agnello DM, Zheng H, Andrews BT, Li M et al (2013) Haemolysin coregulated protein is an exported receptor and chaperone of type VI secretion substrates. Mol Cell 51:584–593CrossRefPubMedGoogle Scholar
  188. 188.
    Groschel MI, Sayes F, Simeone R, Majlessi L, Brosch R (2016) ESX secretion systems: mycobacterial evolution to counter host immunity. Nat Rev Microbiol 14:677–691CrossRefPubMedGoogle Scholar
  189. 189.
    Pallen MJ (2002) The ESAT-6/WXG100 superfamily—and a new Gram-positive secretion system? Trends Microbiol 10:209–212CrossRefPubMedGoogle Scholar
  190. 190.
    Renshaw PS, Lightbody KL, Veverka V, Muskett FW, Kelly G et al (2005) Structure and function of the complex formed by the tuberculosis virulence factors CFP-10 and ESAT-6. EMBO J 24:2491–2498CrossRefPubMedPubMedCentralGoogle Scholar
  191. 191.
    Brodin P, de Jonge MI, Majlessi L, Leclerc C, Nilges M et al (2005) Functional analysis of early secreted antigenic target-6, the dominant T-cell antigen of Mycobacterium tuberculosis, reveals key residues involved in secretion, complex formation, virulence, and immunogenicity. J Biol Chem 280:33953–33959CrossRefPubMedGoogle Scholar
  192. 192.
    Poulsen C, Panjikar S, Holton SJ, Wilmanns M, Song YH (2014) WXG100 protein superfamily consists of three subfamilies and exhibits an alpha-helical C-terminal conserved residue pattern. PLoS ONE 9:e89313CrossRefPubMedPubMedCentralGoogle Scholar
  193. 193.
    Fortune SM, Jaeger A, Sarracino DA, Chase MR, Sassetti CM et al (2005) Mutually dependent secretion of proteins required for mycobacterial virulence. Proc Natl Acad Sci USA 102:10676–10681CrossRefPubMedGoogle Scholar
  194. 194.
    Champion PA, Stanley SA, Champion MM, Brown EJ, Cox JS (2006) C-terminal signal sequence promotes virulence factor secretion in Mycobacterium tuberculosis. Science 313:1632–1636CrossRefPubMedGoogle Scholar
  195. 195.
    Daleke MH, Ummels R, Bawono P, Heringa J, Vandenbroucke-Grauls CM et al (2012) General secretion signal for the mycobacterial type VII secretion pathway. Proc Natl Acad Sci USA 109:11342–11347CrossRefPubMedGoogle Scholar
  196. 196.
    Ekiert DC, Cox JS (2014) Structure of a PE-PPE-EspG complex from Mycobacterium tuberculosis reveals molecular specificity of ESX protein secretion. Proc Natl Acad Sci USA 111:14758–14763CrossRefPubMedGoogle Scholar
  197. 197.
    Houben EN, Korotkov KV, Bitter W (2014) Take five—type VII secretion systems of Mycobacteria. Biochim Biophys Acta 1843:1707–1716CrossRefPubMedGoogle Scholar
  198. 198.
    Burton B, Dubnau D (2010) Membrane-associated DNA transport machines. Cold Spring Harb Perspect Biol 2:a000406CrossRefPubMedPubMedCentralGoogle Scholar
  199. 199.
    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 69:794–808PubMedPubMedCentralGoogle Scholar
  200. 200.
    Derbyshire KM, Gray TA (2014) Distributive conjugal transfer: new insights into horizontal gene transfer and genetic exchange in mycobacteria. Microbiol Spectr.  https://doi.org/10.1128/microbiolspec.MGM2-0022-2013 CrossRefPubMedPubMedCentralGoogle Scholar
  201. 201.
    Serafini A, Pisu D, Palu G, Rodriguez GM, Manganelli R (2013) The ESX-3 secretion system is necessary for iron and zinc homeostasis in Mycobacterium tuberculosis. PLoS ONE 8:e78351CrossRefPubMedPubMedCentralGoogle Scholar
  202. 202.
    Siegrist MS, Unnikrishnan M, McConnell MJ, Borowsky M, Cheng TY et al (2009) Mycobacterial Esx-3 is required for mycobactin-mediated iron acquisition. Proc Natl Acad Sci USA 106:18792–18797CrossRefPubMedGoogle Scholar
  203. 203.
    Siegrist MS, Steigedal M, Ahmad R, Mehra A, Dragset MS et al (2014) Mycobacterial Esx-3 requires multiple components for iron acquisition. MBio 5:e01073-01014CrossRefGoogle Scholar
  204. 204.
    Lai LY, Lin TL, Chen YY, Hsieh PF, Wang JT (2018) Role of the Mycobacterium marinum ESX-1 secretion system in sliding motility and biofilm formation. Front Microbiol 9:1160CrossRefPubMedPubMedCentralGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Microbiology and Molecular GeneticsMcGovern Medical SchoolHoustonUSA

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