1932

Abstract

Bacteria need to deliver large molecules out of the cytosol to the extracellular space or even across membranes of neighboring cells to influence their environment, prevent predation, defeat competitors, or communicate. A variety of protein-secretion systems have evolved to make this process highly regulated and efficient. The type VI secretion system (T6SS) is one of the largest dynamic assemblies in gram-negative bacteria and allows for delivery of toxins into both bacterial and eukaryotic cells. The recent progress in structural biology and live-cell imaging shows the T6SS as a long contractile sheath assembled around a rigid tube with associated toxins anchored to a cell envelope by a baseplate and membrane complex. Rapid sheath contraction releases a large amount of energy used to push the tube and toxins through the membranes of neighboring target cells. Because reach of the T6SS is limited, some bacteria dynamically regulate its subcellular localization to precisely aim at their targets and thus increase efficiency of toxin translocation.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-020518-115420
2019-09-08
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/micro/73/1/annurev-micro-020518-115420.html?itemId=/content/journals/10.1146/annurev-micro-020518-115420&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Alcoforado Diniz J, Liu Y, Coulthurst SJ 2015. Molecular weaponry: diverse effectors delivered by the Type VI secretion system. Cell. Microbiol. 17121742–51
  2. 2. 
    Arisaka F, Yap ML, Kanamaru S, Rossmann MG 2016. Molecular assembly and structure of the bacteriophage T4 tail. Biophys. Rev. 84385–96
  3. 3. 
    Aschtgen M-S, Bernard CS, Bentzmann SD, Lloubès R, Cascales E 2008. SciN is an outer membrane lipoprotein required for type VI secretion in enteroaggregative Escherichia coli. J. Bacteriol 190227523–31
  4. 4. 
    Aschtgen M-S, Gavioli M, Dessen A, Lloubès R, Cascales E 2010. The SciZ protein anchors the enteroaggregative Escherichia coli Type VI secretion system to the cell wall. Mol. Microbiol. 754886–99
  5. 5. 
    Basler M, Ho BT, Mekalanos JJ 2013. Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions. Cell 1524884–94
  6. 6. 
    Basler M, Mekalanos JJ. 2012. Type 6 secretion dynamics within and between bacterial cells. Science 3376096815
  7. 7. 
    Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ 2012. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 4837388182–86
  8. 8. 
    Böck D, Medeiros JM, Tsao H-F, Penz T, Weiss GL et al. 2017. In situ architecture, function, and evolution of a contractile injection system. Science 3576352713–17
  9. 9. 
    Bondage DD, Lin JS, Ma LS, Kuo CH, Lai EM 2016. VgrG C terminus confers the type VI effector transport specificity and is required for binding with PAAR and adaptor-effector complex. PNAS 113E3931–40
  10. 10. 
    Bönemann G, Pietrosiuk A, Diemand A, Zentgraf H, Mogk A 2009. Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J 284315–25
  11. 11. 
    Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I 2009. Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources. ? BMC Genom 10104
  12. 12. 
    Brackmann M, Nazarov S, Wang J, Basler M 2017. Using force to punch holes: mechanics of contractile nanomachines. Trends Cell Biol 279623–32
  13. 13. 
    Brackmann M, Wang J, Basler M 2018. Type VI secretion system sheath inter‐subunit interactions modulate its contraction. EMBO Rep 192225–33
  14. 14. 
    Brodmann M, Dreier RF, Broz P, Basler M 2017. Francisella requires dynamic type VI secretion system and ClpB to deliver effectors for phagosomal escape. Nat. Commun. 815853
  15. 15. 
    Bröms JE, Sjöstedt A, Lavander M 2010. The role of the Francisella tularensis pathogenicity island in type VI secretion, intracellular survival, and modulation of host cell signaling. Front. Microbiol. 1136
  16. 16. 
    Burkinshaw BJ, Liang X, Wong M, Le ANH, Lam L, Dong TG 2018. A type VI secretion system effector delivery mechanism dependent on PAAR and a chaperone-co-chaperone complex. Nat. Microbiol. 3632–40
  17. 17. 
    Carlsson F, Joshi SA, Rangell L, Brown EJ 2009. Polar localization of virulence-related Esx-1 secretion in mycobacteria. PLOS Pathog 51e1000285
  18. 18. 
    Casabona MG, Silverman JM, Sall KM, Boyer F, Couté Y et al. 2013. An ABC transporter and an outer membrane lipoprotein participate in posttranslational activation of type VI secretion in Pseudomonas aeruginosa. Environ. Microbiol 152471–86
  19. 19. 
    Cascales E. 2008. The type VI secretion toolkit. EMBO Rep 98735–41
  20. 20. 
    Chakravortty D, Rohde M, Jäger L, Deiwick J, Hensel M 2005. Formation of a novel surface structure encoded by Salmonella Pathogenicity Island 2. EMBO J 24112043–52
  21. 21. 
    Chang Y-W, Rettberg LA, Ortega DR, Jensen GJ 2017. In vivo structures of an intact type VI secretion system revealed by electron cryotomography. EMBO Rep 1871090–99
  22. 22. 
    Charles M, Pérez M, Kobil JH, Goldberg MB 2001. Polar targeting of Shigella virulence factor IcsA in Enterobacteriacae and Vibrio. PNAS 98179871–76
  23. 23. 
    Chen L, Zou Y, She P, Wu Y 2015. Composition, function, and regulation of T6SS in Pseudomonas aeruginosa. Microbiol. Res 17219–25
  24. 24. 
    Cherrak Y, Rapisarda C, Pellarin R, Bouvier G, Bardiaux B et al. 2018. Biogenesis and structure of a type VI secretion baseplate. Nat. Microbiol. 3121404–16
  25. 25. 
    Cianfanelli FR, Alcoforado Diniz J, Guo M, De Cesare V, Trost M, Coulthurst SJ 2016. VgrG and PAAR proteins define distinct versions of a functional Type VI secretion system. PLOS Pathog 126e1005735
  26. 26. 
    Clemens DL, Ge P, Lee B-Y, Horwitz MA, Zhou ZH 2015. Atomic structure of T6SS reveals interlaced array essential to function. Cell 1605940–51
  27. 27. 
    Deville C, Carroni M, Franke KB, Topf M, Bukau B et al. 2017. Structural pathway of regulated substrate transfer and threading through an Hsp100 disaggregase. Sci. Adv. 38e1701726
  28. 28. 
    Dik DA, Marous DR, Fisher JF, Mobashery S 2017. Lytic transglycosylases: concinnity in concision of the bacterial cell wall. Crit. Rev. Biochem. Mol. Biol. 525503–42
  29. 29. 
    Dix SR, Owen HJ, Sun R, Ahmad A, Shastri S et al. 2018. Structural insights into the function of type VI secretion system TssA subunits. Nat Commun 914765
  30. 30. 
    Durand E, Nguyen VS, Zoued A, Logger L, Péhau-Arnaudet G et al. 2015. Biogenesis and structure of a type VI secretion membrane core complex. Nature 5237562555–60
  31. 31. 
    Durand E, Zoued A, Spinelli S, Watson PJH, Aschtgen M-S et al. 2012. Structural characterization and oligomerization of the TssL protein, a component shared by bacterial type VI and type IVb secretion systems. J. Biol. Chem. 2871714157–68
  32. 32. 
    Felisberto-Rodrigues C, Durand E, Aschtgen M-S, Blangy S, Ortiz-Lombardia M et al. 2011. Towards a structural comprehension of bacterial type VI secretion systems: characterization of the TssJ-TssM complex of an Escherichia coli pathovar. PLOS Pathog 711e1002386
  33. 33. 
    Förster A, Planamente S, Manoli E, Lossi NS, Freemont PS, Filloux A 2014. Coevolution of the ATPase ClpV, the sheath proteins TssB and TssC, and the accessory protein TagJ/HsiE1 distinguishes type VI secretion classes. J. Biol. Chem. 2894733032–43
  34. 34. 
    French CT, Toesca IJ, Wu T-H, Teslaa T, Beaty SM et al. 2011. Dissection of the Burkholderia intracellular life cycle using a photothermal nanoblade. PNAS 1082912095–100
  35. 35. 
    Fritsch MJ, Trunk K, Diniz JA, Guo M, Trost M, Coulthurst SJ 2013. Proteomic identification of novel secreted antibacterial toxins of the Serratia marcescens type VI secretion system. Mol. Cell. Proteom. 12102735–49
  36. 36. 
    Gates SN, Yokom AL, Lin J, Jackrel ME, Rizo AN et al. 2017. Ratchet-like polypeptide translocation mechanism of the AAA+ disaggregase Hsp104. Science 3576348273–79
  37. 37. 
    Geiger T, Pazos M, Lara-Tejero M, Vollmer W, Galán JE 2018. Peptidoglycan editing by a specific LD-transpeptidase controls the muramidase-dependent secretion of typhoid toxin. Nat. Microbiol. 3111243–54
  38. 38. 
    Gerc AJ, Diepold A, Trunk K, Porter M, Rickman C et al. 2015. Visualization of the Serratia Type VI secretion system reveals unprovoked attacks and dynamic assembly. Cell Rep 12122131–42
  39. 39. 
    Ghosal D, Jeong KC, Chang Y-W, Gyore J, Teng L et al. 2019. Molecular architecture, polar targeting and biogenesis of the Legionella Dot/Icm T4SS. Nat. Microbiol. 41173–82
  40. 40. 
    Ho BT, Basler M, Mekalanos JJ 2013. Type 6 secretion system-mediated immunity to type 4 secretion system-mediated horizontal gene transfer. Science 3426155250–53
  41. 41. 
    Ho BT, Dong TG, Mekalanos JJ 2014. A view to a kill: the bacterial type VI secretion system. Cell Host Microbe 1519–21
  42. 42. 
    Hsu F, Schwarz S, Mougous JD 2009. TagR promotes PpkA-catalyzed type VI secretion activation in Pseudomonas aeruginosa. Mol. Microbiol 7251111–25
  43. 43. 
    Jain S, van Ulsen P, Benz I, Schmidt MA, Fernandez R et al. 2006. Polar localization of the autotransporter family of large bacterial virulence proteins. J. Bacteriol. 188134841–50
  44. 44. 
    Jeong KC, Ghosal D, Chang Y-W, Jensen GJ, Vogel JP 2017. Polar delivery of Legionella type IV secretion system substrates is essential for virulence. PNAS 114308077–82
  45. 45. 
    Jiang F, Li N, Wang X, Cheng J, Huang Y et al. 2019. Cryo-EM structure and assembly of an extracellular contractile injection system. Cell 1772370–83.e15
  46. 46. 
    Joshi A, Kostiuk B, Rogers A, Teschler J, Pukatzki S, Yildiz FH 2017. Rules of engagement: the type VI secretion system in Vibrio cholerae. Trends Microbiol 25426–79
  47. 47. 
    Kudryashev M, Wang RY-R, Brackmann M, Scherer S, Maier T et al. 2015. Structure of the type VI secretion system contractile sheath. Cell 1605952–62
  48. 48. 
    Laloux G, Jacobs-Wagner C. 2014. How do bacteria localize proteins to the cell pole. ? J. Cell Sci. 127Part 111–19
  49. 49. 
    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. PNAS 106114154–59
  50. 50. 
    Leiman PG, Shneider MM. 2012. Contractile tail machines of bacteriophages. Adv. Exp. Med. Biol. 72693–114
  51. 51. 
    Leung KY, Siame BA, Snowball H, Mok Y-K 2011. Type VI secretion regulation: crosstalk and intracellular communication. Host-Microbe Interact 1419–15
  52. 52. 
    Liang X, Moore R, Wilton M, Wong MJ, Lam L, Dong TG 2015. Identification of divergent type VI secretion effectors using a conserved chaperone domain. PNAS 1129106–11
  53. 53. 
    Lien Y-W, Lai E-M. 2017. Type VI secretion effectors: methodologies and biology. Front. Cell. Infect. Microbiol. 7254
  54. 54. 
    Lin J-S, Pissaridou P, Wu H-H, Tsai M-D, Filloux A, Lai E-M 2018. TagF-mediated repression of bacterial type VI secretion systems involves a direct interaction with the cytoplasmic protein Fha. J. Biol. Chem. 2938829–42
  55. 55. 
    Lin J-S, Wu H-H, Hsu P-H, Ma L-S, Pang Y-Y et al. 2014. Fha interaction with phosphothreonine of TssL activates type VI secretion in Agrobacterium tumefaciens. PLOS Pathog 103e1003991
  56. 56. 
    Logger L, Aschtgen M-S, Guérin M, Cascales E, Durand E 2016. Molecular dissection of the interface between the type VI secretion TssM cytoplasmic domain and the TssG baseplate component. J. Mol. Biol. 428224424–37
  57. 57. 
    Lossi NS, Dajani R, Freemont P, Filloux A 2011. Structure-function analysis of HsiF, a gp25-like component of the type VI secretion system, in Pseudomonas aeruginosa. Microbiology 1573292–305
  58. 58. 
    Lossi NS, Manoli E, Simpson P, Jones C, Hui K et al. 2012. The archetype Pseudomonas aeruginosa proteins TssB and TagJ form a novel subcomplex in the bacterial type VI secretion system. Mol. Microbiol. 862437–56
  59. 59. 
    Ma L-S, Lin J-S, Lai E-M 2009. An IcmF family protein, ImpLM, is an integral inner membrane protein interacting with ImpKL, and its Walker A motif is required for type VI secretion system-mediated Hcp secretion in Agrobacterium tumefaciens. J. Bacteriol 191134316–29
  60. 60. 
    Ma L-S, Narberhaus F, Lai E-M 2012. IcmF family protein TssM exhibits ATPase activity and energizes type VI secretion. J. Biol. Chem. 2871915610–21
  61. 61. 
    Miyata ST, Bachmann V, Pukatzki S 2013. Type VI secretion system regulation as a consequence of evolutionary pressure. J. Med. Microbiol. 62Part 5663–76
  62. 62. 
    Morgan JK, Luedtke BE, Shaw EI 2010. Polar localization of the Coxiella burnetii type IVB secretion system. FEMS Microbiol. Lett. 3052177–83
  63. 63. 
    Motley ST, Lory S. 1999. Functional characterization of a serine/threonine protein kinase of Pseudomonas aeruginosa. Infect. Immun 67105386–94
  64. 64. 
    Mougous JD, Gifford CA, Ramsdell TL, Mekalanos JJ 2007. Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat. Cell Biol 97797–803
  65. 65. 
    Narita S, Tokuda H. 2006. An ABC transporter mediating the membrane detachment of bacterial lipoproteins depending on their sorting signals. FEBS Lett 58041164–70
  66. 66. 
    Nazarov S, Schneider JP, Brackmann M, Goldie KN, Stahlberg H, Basler M 2018. Cryo-EM reconstruction of Type VI secretion system baseplate and sheath distal end. EMBO J 374e97103
  67. 67. 
    Nguyen VS, Logger L, Spinelli S, Legrand P, Huyen Pham TT et al. 2017. Type VI secretion TssK baseplate protein exhibits structural similarity with phage receptor-binding proteins and evolved to bind the membrane complex. Nat. Microbiol. 2917103
  68. 68. 
    Ostrowski A, Cianfanelli FR, Porter M, Mariano G, Peltier J et al. 2018. Killing with proficiency: integrated post-translational regulation of an offensive Type VI secretion system. PLOS Pathog 147e1007230
  69. 69. 
    Park Y-J, Lacourse KD, Cambillau C, DiMaio F, Mougous JD, Veesler D 2018. Structure of the type VI secretion system TssK-TssF-TssG baseplate subcomplex revealed by cryo-electron microscopy. Nat. Commun. 915385
  70. 70. 
    Pietrosiuk A, Lenherr ED, Falk S, Bönemann G, Kopp J et al. 2011. Molecular basis for the unique role of the AAA+ chaperone ClpV in type VI protein secretion. J. Biol. Chem. 2863430010–21
  71. 71. 
    Planamente S, Salih O, Manoli E, Albesa‐Jové D, Freemont PS, Filloux A 2016. TssA forms a gp6‐like ring attached to the type VI secretion sheath. EMBO J 35151613–27
  72. 72. 
    Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ 2007. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. PNAS 1043915508–13
  73. 73. 
    Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D et al. 2006. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. PNAS 10351528–33
  74. 74. 
    Quentin D, Ahmad S, Shanthamoorthy P, Mougous JD, Whitney JC, Raunser S 2018. Mechanism of loading and translocation of type VI secretion system effector Tse6. Nat. Microbiol. 3101142–52
  75. 75. 
    Rao VA, Shepherd SM, English G, Coulthurst SJ, Hunter WN 2011. The structure of Serratia marcescens Lip, a membrane-bound component of the type VI secretion system. Acta Crystallogr. D Biol. Crystallogr. 67121065–72
  76. 76. 
    Rapisarda C, Cherrak Y, Kooger R, Schmidt V, Pellarin R 2019. In situ and high-resolution cryo-EM structure of a bacterial type VI secretion system membrane complex. EMBO J 38e100886
  77. 77. 
    Renault MG, Zamarreno Beas J, Douzi B, Chabalier M, Zoued A et al. 2018. The gp27-like hub of VgrG serves as adaptor to promote hcp tube assembly. J. Mol. Biol. 43018 Part B3143–56
  78. 78. 
    Ringel PD, Hu D, Basler M 2017. The role of type VI secretion system effectors in target cell lysis and subsequent horizontal gene transfer. Cell Rep 21133927–40
  79. 79. 
    Robb CS, Nano FE, Boraston AB 2010. Cloning, expression, purification, crystallization and preliminary X-ray diffraction analysis of intracellular growth locus E (IglE) protein from Francisella tularensis subsp. novicida. Acta Crystallograph. F Struct. Biol. Cryst. Commun. 66121596–98
  80. 80. 
    Rosch J, Caparon M. 2004. A microdomain for protein secretion in Gram-positive bacteria. Science 30456761513–15
  81. 81. 
    Salih O, He S, Planamente S, Stach L, MacDonald JT et al. 2018. Atomic structure of type VI contractile sheath from Pseudomonas aeruginosa. Structure 262329–36.e3
  82. 82. 
    Santin YG, Cascales E. 2017. Domestication of a housekeeping transglycosylase for assembly of a Type VI secretion system. EMBO Rep 181138–49
  83. 83. 
    Santin YG, Doan T, Lebrun R, Espinosa L, Journet L, Cascales E 2018. In vivo TssA proximity labelling during type VI secretion biogenesis reveals TagA as a protein that stops and holds the sheath. Nat. Microbiol. 3111304
  84. 84. 
    Scheurwater EM, Burrows LL. 2011. Maintaining network security: how macromolecular structures cross the peptidoglycan layer. FEMS Microbiol. Lett. 31811–9
  85. 85. 
    Schwarz S, Singh P, Robertson JD, LeRoux M, Skerrett SJ et al. 2014. VgrG-5 is a Burkholderia type VI secretion system-exported protein required for multinucleated giant cell formation and virulence. Infect. Immun. 8241445–52
  86. 86. 
    Schwarz S, West TE, Boyer F, Chiang W-C, Carl MA et al. 2010. Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLOS Pathog 68e1001068
  87. 87. 
    Sciara G, Bebeacua C, Bron P, Tremblay D, Ortiz-Lombardia M et al. 2010. Structure of lactococcal phage p2 baseplate and its mechanism of activation. PNAS 107156852–57
  88. 88. 
    Scott ME, Dossani ZY, Sandkvist M 2001. Directed polar secretion of protease from single cells of Vibrio cholerae via the type II secretion pathway. PNAS 982413978–83
  89. 89. 
    Shneider MM, Buth SA, Ho BT, Basler M, Mekalanos JJ, Leiman PG 2013. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 5007462350–53
  90. 90. 
    Silverman JM, Austin LS, Hsu F, Hicks KG, Hood RD, Mougous JD 2011. Separate inputs modulate phosphorylation-dependent and -independent type VI secretion activation. Mol. Microbiol. 8251277–90
  91. 91. 
    Spínola-Amilibia M, Davó-Siguero I, Ruiz FM, Santillana E, Medrano FJ, Romero A 2016. The structure of VgrG1 from Pseudomonas aeruginosa, the needle tip of the bacterial type VI secretion system. Acta Crystallogr. D Struct. Biol. 72Part 122–33
  92. 92. 
    Szwedziak P, Pilhofer M. 2019. Bidirectional contraction of a type six secretion system. Nat. Commun. 101565
  93. 93. 
    Taylor NMI, Prokhorov NS, Guerrero-Ferreira RC, Shneider MM, Browning C et al. 2016. Structure of the T4 baseplate and its function in triggering sheath contraction. Nature 5337603346
  94. 94. 
    Toesca IJ, French CT, Miller JF 2014. The Type VI secretion system spike protein VgrG5 mediates membrane fusion during intercellular spread by pseudomallei group Burkholderia species. Infect. Immun. 8241436–44
  95. 95. 
    Typas A, Banzhaf M, Gross CA, Vollmer W 2011. From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat. Rev. Microbiol. 102123–36
  96. 96. 
    Unterweger D, Kostiuk B, Ötjengerdes R, Wilton A, Diaz-Satizabal L, Pukatzki S 2015. Chimeric adaptor proteins translocate diverse type VI secretion system effectors in Vibrio cholerae. EMBO J 342198–210
  97. 97. 
    Veesler D, Spinelli S, Mahony J, Lichière J, Blangy S et al. 2012. Structure of the phage TP901–1 1.8 MDa baseplate suggests an alternative host adhesion mechanism. PNAS 109238954–58
  98. 98. 
    Vettiger A, Basler M. 2016. Type VI secretion system substrates are transferred and reused among sister cells. Cell 167199–110.e12
  99. 99. 
    Vettiger A, Winter J, Lin L, Basler M 2017. The type VI secretion system sheath assembles at the end distal from the membrane anchor. Nat. Commun. 816088
  100. 100. 
    Wang J, Brackmann M, Castaño-Díez D, Kudryashev M, Goldie KN et al. 2017. Cryo-EM structure of the extended type VI secretion system sheath-tube complex. Nat. Microbiol. 2111507–12
  101. 101. 
    Weber BS, Hennon SW, Wright MS, Scott NE, de Berardinis V et al. 2016. Genetic dissection of the type VI secretion system in Acinetobacter and identification of a novel peptidoglycan hydrolase, TagX, required for its biogenesis. mBio 75e01253–16
  102. 102. 
    Wilton M, Wong MJQ, Tang L, Liang X, Moore R et al. 2016. Chelation of membrane-bound cations by extracellular DNA activates the type VI secretion system in Pseudomonas aeruginosa. Infect. Immun 8482355–61
  103. 103. 
    Yang Z, Zhou X, Ma Y, Zhou M, Waldor MK et al. 2018. Serine/threonine kinase PpkA coordinates the interplay between T6SS2 activation and quorum sensing in the marine pathogen Vibrio alginolyticus. Environ. Microbiol 20903–19
  104. 104. 
    Yin M, Yan Z, Li X 2019. Architecture of type VI secretion system membrane core complex. Cell Res 29251–52
  105. 105. 
    Yu H, Lupoli TJ, Kovach A, Meng X, Zhao G et al. 2018. ATP hydrolysis-coupled peptide translocation mechanism of Mycobacterium tuberculosis ClpB. PNAS 11541E9560–69
  106. 106. 
    Zheng J, Ho B, Mekalanos JJ 2011. Genetic analysis of anti-amoebae and anti-bacterial activities of the type VI secretion system in Vibrio cholerae. PLOS ONE 68e23876
  107. 107. 
    Zheng J, Leung KY. 2007. Dissection of a type VI secretion system in Edwardsiella tarda. Mol. Microbiol 6651192–206
  108. 108. 
    Zoued A, Cassaro CJ, Durand E, Douzi B, España AP et al. 2016. Structure-function analysis of the TssL cytoplasmic domain reveals a new interaction between the type VI secretion baseplate and membrane complexes. J. Mol. Biol. 428224413–23
  109. 109. 
    Zoued A, Duneau J-P, Durand E, España AP, Journet L et al. 2018. Tryptophan-mediated dimerization of the TssL transmembrane anchor is required for type VI secretion system activity. J. Mol. Biol. 4307987–1003
  110. 110. 
    Zoued A, Durand E, Bebeacua C, Brunet YR, Douzi B et al. 2013. TssK is a trimeric cytoplasmic protein interacting with components of both phage-like and membrane anchoring complexes of the type VI secretion system. J. Biol. Chem. 2883827031–41
  111. 111. 
    Zoued A, Durand E, Brunet YR, Spinelli S, Douzi B et al. 2016. Priming and polymerization of a bacterial contractile tail structure. Nature 531759259–63
  112. 112. 
    Zoued A, Durand E, Santin YG, Journet L, Roussel A et al. 2017. TssA: the cap protein of the Type VI secretion system tail. BioEssays 39101600262
/content/journals/10.1146/annurev-micro-020518-115420
Loading
/content/journals/10.1146/annurev-micro-020518-115420
Loading

Data & Media loading...

  • 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