1887

Abstract

The Type VI secretion system (T6SS) is a protein nanomachine that is widespread in Gram-negative bacteria and is used to translocate effector proteins directly into neighbouring cells. It represents a versatile bacterial weapon that can deliver effectors into distinct classes of target cells, playing key roles in inter-bacterial competition and bacterial interactions with eukaryotic cells. This versatility is underpinned by the ability of the T6SS to deliver a vast array of effector proteins, with many distinct activities and modes of interaction with the secretion machinery. Recent work has highlighted the importance and diversity of interactions mediated by T6SSs within polymicrobial communities, and offers new molecular insights into effector delivery and action in target cells.

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2019-05-01
2024-05-16
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References

  1. Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M et al. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 2006; 312:1526–1530 [View Article][PubMed]
    [Google Scholar]
  2. Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D et al. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci 2006; 103:1528–1533 [View Article][PubMed]
    [Google Scholar]
  3. Bingle LE, Bailey CM, Pallen MJ. Type VI secretion: a beginner's guide. Curr Opin Microbiol 2008; 11:3–8 [View Article][PubMed]
    [Google Scholar]
  4. Barret M, Egan F, Fargier E, Morrissey JP, O'Gara F. Genomic analysis of the Type VI secretion systems in Pseudomonas spp.: novel clusters and putative effectors uncovered. Microbiology 2011; 157:1726–1739 [View Article][PubMed]
    [Google Scholar]
  5. Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I. Dissecting the bacterial Type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources?. BMC Genomics 2009; 10:104 [View Article][PubMed]
    [Google Scholar]
  6. Clemens DL, Ge P, Lee BY, Horwitz MA, Zhou ZH. Atomic structure of T6SS reveals interlaced array essential to function. Cell 2015; 160:940–951 [View Article][PubMed]
    [Google Scholar]
  7. Russell AB, Wexler AG, Harding BN, Whitney JC, Bohn AJ et al. A Type VI secretion-related pathway in Bacteroidetes mediates interbacterial antagonism. Cell Host Microbe 2014; 16:227–236 [View Article][PubMed]
    [Google Scholar]
  8. MacIntyre DL, Miyata ST, Kitaoka M, Pukatzki S. The Vibrio cholerae Type VI secretion system displays antimicrobial properties. Proc Natl Acad Sci 2010; 107:19520–19524 [View Article][PubMed]
    [Google Scholar]
  9. Schwarz S, West TE, Boyer F, Chiang WC, Carl MA et al. Burkholderia Type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog 2010; 6:e1001068 [View Article][PubMed]
    [Google Scholar]
  10. Leroux M, Kirkpatrick RL, Montauti EI, Tran BQ, Peterson SB et al. Kin cell lysis is a danger signal that activates antibacterial pathways of Pseudomonas aeruginosa . elife 2015; 4: [View Article][PubMed]
    [Google Scholar]
  11. Schell MA, Ulrich RL, Ribot WJ, Brueggemann EE, Hines HB et al. Type VI secretion is a major virulence determinant in Burkholderia mallei . Mol Microbiol 2007; 64:1466–1485 [View Article][PubMed]
    [Google Scholar]
  12. Brackmann M, Nazarov S, Wang J, Basler M. Using force to punch holes: mechanics of contractile nanomachines. Trends Cell Biol 2017; 27:623–632 [View Article][PubMed]
    [Google Scholar]
  13. Cianfanelli FR, Monlezun L, Coulthurst SJ. Aim, load, fire: the Type VI secretion system, a bacterial nanoweapon. Trends Microbiol 2016; 24:51–62 [View Article][PubMed]
    [Google Scholar]
  14. Clemens DL, Lee BY, Horwitz MA. The Francisella Type VI secretion system. Front Cell Infect Microbiol 2018; 8:121 [View Article][PubMed]
    [Google Scholar]
  15. Nguyen VS, Douzi B, Durand E, Roussel A, Cascales E et al. Towards a complete structural deciphering of Type VI secretion system. Curr Opin Struct Biol 2018; 49:77–84 [View Article][PubMed]
    [Google Scholar]
  16. Durand E, Nguyen VS, Zoued A, Logger L, Péhau-Arnaudet G et al. Biogenesis and structure of a Type VI secretion membrane core complex. Nature 2015; 523:555–560 [View Article][PubMed]
    [Google Scholar]
  17. Cherrak Y, Rapisarda C, Pellarin R, Bouvier G, Bardiaux B et al. Biogenesis and structure of a Type VI secretion baseplate. Nat Microbiol 2018; 3:1404–1416 [View Article][PubMed]
    [Google Scholar]
  18. Nazarov S, Schneider JP, Brackmann M, Goldie KN, Stahlberg H et al. Cryo-EM reconstruction of Type VI secretion system baseplate and sheath distal end. Embo J 2018; 37:e97103 [View Article][PubMed]
    [Google Scholar]
  19. Kudryashev M, Wang RY-R, Brackmann M, Scherer S, Maier T et al. Structure of the Type VI secretion system contractile sheath. Cell 2015; 160:952–962 [View Article]
    [Google Scholar]
  20. Renault MG, Zamarreno Beas J, Douzi B, Chabalier M, Zoued A et al. The gp27-like hub of VgrG serves as adaptor to promote Hcp tube assembly. J Mol Biol 2018; 430:3143–3156 [View Article][PubMed]
    [Google Scholar]
  21. Wang J, Brackmann M, Castaño-Díez D, Kudryashev M, Goldie KN et al. Cryo-EM structure of the extended type VI secretion system sheath-tube complex. Nat Microbiol 2017; 2:1507–1512 [View Article][PubMed]
    [Google Scholar]
  22. Basler M. Type VI secretion system: secretion by a contractile nanomachine. Philos Trans R Soc Lond B Biol Sci 2015; 370:20150021 [View Article][PubMed]
    [Google Scholar]
  23. Vettiger A, Winter J, Lin L, Basler M. The Type VI secretion system sheath assembles at the end distal from the membrane anchor. Nat Commun 2017; 8:16088 [View Article][PubMed]
    [Google Scholar]
  24. Dix SR, Owen HJ, Sun R, Ahmad A, Shastri S et al. Structural insights into the function of Type VI secretion system TssA subunits. Nat Commun 2018; 9:4765 [View Article][PubMed]
    [Google Scholar]
  25. Zoued A, Durand E, Brunet YR, Spinelli S, Douzi B et al. Priming and polymerization of a bacterial contractile tail structure. Nature 2016; 531:59–63 [View Article][PubMed]
    [Google Scholar]
  26. Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 2012; 483:182–186 [View Article][PubMed]
    [Google Scholar]
  27. Basler M, Ho BT, Mekalanos JJ. Tit-for-tat: Type VI secretion system counterattack during bacterial cell-cell interactions. Cell 2013; 152:884–894 [View Article][PubMed]
    [Google Scholar]
  28. Ostrowski A, Cianfanelli FR, Porter M, Mariano G, Peltier J et al. Killing with proficiency: integrated post-translational regulation of an offensive Type VI secretion system. PLoS Pathog 2018; 14:e1007230 [View Article][PubMed]
    [Google Scholar]
  29. Aschtgen MS, Gavioli M, Dessen A, Lloubès R, Cascales E. The SciZ protein anchors the enteroaggregative Escherichia coli Type VI secretion system to the cell wall. Mol Microbiol 2010; 75:886–899 [View Article][PubMed]
    [Google Scholar]
  30. Santin YG, Cascales E. Domestication of a housekeeping transglycosylase for assembly of a Type VI secretion system. EMBO Rep 2017; 18:138–149 [View Article][PubMed]
    [Google Scholar]
  31. Weber BS, Hennon SW, Wright MS, Scott NE, de Berardinis V et al. Genetic dissection of the Type VI secretion system in Acinetobacter and identification of a novel peptidoglycan hydrolase, TagX, required for Its biogenesis. mBio 2016; 7:e0125316 [View Article][PubMed]
    [Google Scholar]
  32. Santin YG, Doan T, Lebrun R, Espinosa L, Journet L et al. In vivo TssA proximity labelling during Type VI secretion biogenesis reveals TagA as a protein that stops and holds the sheath. Nat Microbiol 2018; 3:1304–1313 [View Article]
    [Google Scholar]
  33. Förster A, Planamente S, Manoli E, Lossi NS, Freemont PS et al. 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 2014; 289:33032–33043 [View Article][PubMed]
    [Google Scholar]
  34. Lin JS, Wu HH, Hsu PH, Ma LS, Pang YY et al. Fha interaction with phosphothreonine of TssL activates Type VI secretion in Agrobacterium tumefaciens . PLoS Pathog 2014; 10:e1003991 [View Article][PubMed]
    [Google Scholar]
  35. Durand E, Cambillau C, Cascales E, Journet L. VgrG, Tae, Tle, and beyond: the versatile arsenal of Type VI secretion effectors. Trends Microbiol 2014; 22:498–507 [View Article][PubMed]
    [Google Scholar]
  36. Silverman JM, Agnello DM, Zheng H, Andrews BT, Li M et al. Haemolysin coregulated protein is an exported receptor and chaperone of Type VI secretion substrates. Mol Cell 2013; 51:584–593 [View Article][PubMed]
    [Google Scholar]
  37. Flaugnatti N, Le TT, Canaan S, Aschtgen MS, Nguyen VS et al. A phospholipase A1 antibacterial Type VI secretion effector interacts directly with the C-terminal domain of the VgrG spike protein for delivery. Mol Microbiol 2016; 99:1099–1118 [View Article][PubMed]
    [Google Scholar]
  38. Burkinshaw BJ, Liang X, Wong M, Le ANH, Lam L et al. A Type VI secretion system effector delivery mechanism dependent on PAAR and a chaperone-co-chaperone complex. Nat Microbiol 2018; 3:632–640 [View Article][PubMed]
    [Google Scholar]
  39. Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci 2007; 104:15508–15513 [View Article][PubMed]
    [Google Scholar]
  40. Alcoforado Diniz J, Coulthurst SJ. Intraspecies competition in Serratia marcescens Is mediated by Type VI-Secreted Rhs effectors and a conserved effector-associated accessory protein. J Bacteriol 2015; 197:2350–2360 [View Article][PubMed]
    [Google Scholar]
  41. Hachani A, Allsopp LP, Oduko Y, Filloux A. The VgrG proteins are "à la carte" delivery systems for bacterial Type VI effectors. J Biol Chem 2014; 289:17872–17884 [View Article][PubMed]
    [Google Scholar]
  42. Whitney JC, Beck CM, Goo YA, Russell AB, Harding BN et al. Genetically distinct pathways guide effector export through the Type VI secretion system. Mol Microbiol 2014; 92:529–542 [View Article][PubMed]
    [Google Scholar]
  43. Zhang D, de Souza RF, Anantharaman V, Iyer LM, Aravind L. Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol Direct 2012; 7:18 [View Article][PubMed]
    [Google Scholar]
  44. Shneider MM, Buth SA, Ho BT, Basler M, Mekalanos JJ et al. PAAR-repeat proteins sharpen and diversify the Type VI secretion system spike. Nature 2013; 500:350–353 [View Article][PubMed]
    [Google Scholar]
  45. Ma J, Pan Z, Huang J, Sun M, Lu C et al. The Hcp proteins fused with diverse extended-toxin domains represent a novel pattern of antibacterial effectors in Type VI secretion systems. Virulence 2017; 8:1189–1202 [View Article][PubMed]
    [Google Scholar]
  46. Cianfanelli FR, Alcoforado Diniz J, Guo M, de Cesare V, Trost M et al. VgrG and PAAR proteins define distinct versions of a functional Type VI secretion system. PLoS Pathog 2016; 12:e1005735 [View Article][PubMed]
    [Google Scholar]
  47. Quentin D, Ahmad S, Shanthamoorthy P, Mougous JD, Whitney JC et al. Mechanism of loading and translocation of Type VI secretion system effector Tse6. Nat Microbiol 2018; 3:1142–1152 [View Article][PubMed]
    [Google Scholar]
  48. Ma LS, Hachani A, Lin JS, Filloux A, Lai EM. Agrobacterium tumefaciens deploys a superfamily of Type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell Host Microbe 2014; 16:94–104 [View Article][PubMed]
    [Google Scholar]
  49. Unterweger D, Kostiuk B, Ötjengerdes R, Wilton A, Diaz-Satizabal L et al. Chimeric adaptor proteins translocate diverse Type VI secretion system effectors in Vibrio cholerae . Embo J 2015; 34:2198–2210 [View Article][PubMed]
    [Google Scholar]
  50. Salomon D, Kinch LN, Trudgian DC, Guo X, Klimko JA et al. Marker for Type VI secretion system effectors. Proc Natl Acad Sci 2014; 111:9271–9276 [View Article][PubMed]
    [Google Scholar]
  51. Brooks TM, Unterweger D, Bachmann V, Kostiuk B, Pukatzki S. Lytic activity of the Vibrio cholerae Type VI secretion toxin VgrG-3 is inhibited by the antitoxin TsaB. J Biol Chem 2013; 288:7618–7625 [View Article][PubMed]
    [Google Scholar]
  52. Ma J, Sun M, Pan Z, Lu C, Yao H. Diverse toxic effectors are harbored by vgrG islands for interbacterial antagonism in Type VI secretion system. Biochim Biophys Acta Gen Subj 2018; 1862:1635–1643 [View Article][PubMed]
    [Google Scholar]
  53. Russell AB, Singh P, Brittnacher M, Bui NK, Hood RD et al. A widespread bacterial Type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe 2012; 11:538–549 [View Article][PubMed]
    [Google Scholar]
  54. Whitney JC, Chou S, Russell AB, Biboy J, Gardiner TE et al. Identification, structure, and function of a novel Type VI secretion peptidoglycan glycoside hydrolase effector-immunity pair. J Biol Chem 2013; 288:26616–26624 [View Article][PubMed]
    [Google Scholar]
  55. Russell AB, Leroux M, Hathazi K, Agnello DM, Ishikawa T et al. Diverse Type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 2013; 496:508–512 [View Article][PubMed]
    [Google Scholar]
  56. Lacourse KD, Peterson SB, Kulasekara HD, Radey MC, Kim J et al. Conditional toxicity and synergy drive diversity among antibacterial effectors. Nat Microbiol 2018; 3:440–446 [View Article][PubMed]
    [Google Scholar]
  57. Miyata ST, Unterweger D, Rudko SP, Pukatzki S. Dual expression profile of Type VI secretion system immunity genes protects pandemic Vibrio cholerae. PLoS Pathog 2013; 9:e1003752 [View Article][PubMed]
    [Google Scholar]
  58. Mariano G, Monlezun L, Coulthurst SJ. Dual role for DsbA in attacking and targeted bacterial cells during Type VI secretion system-mediated competition. Cell Rep 2018; 22:774–785 [View Article][PubMed]
    [Google Scholar]
  59. Koskiniemi S, Lamoureux JG, Nikolakakis KC, T'kint de Roodenbeke C, Kaplan MD et al. Rhs proteins from diverse bacteria mediate intercellular competition. Proc Natl Acad Sci 2013; 110:7032–7037 [View Article][PubMed]
    [Google Scholar]
  60. Ma J, Sun M, Dong W, Pan Z, Lu C et al. PAAR-Rhs proteins harbor various C-terminal toxins to diversify the antibacterial pathways of Type VI secretion systems. Environ Microbiol 2017; 19:345–360 [View Article][PubMed]
    [Google Scholar]
  61. Tang JY, Bullen NP, Ahmad S, Whitney JC. Diverse NADase effector families mediate interbacterial antagonism via the Type VI secretion system. J Biol Chem 2018; 293:1504–1514 [View Article][PubMed]
    [Google Scholar]
  62. Whitney JC, Quentin D, Sawai S, Leroux M, Harding BN et al. An interbacterial NAD(P)(+) glycohydrolase toxin requires elongation factor Tu for delivery to target cells. Cell 2015; 163:607–619 [View Article][PubMed]
    [Google Scholar]
  63. Ting SY, Bosch DE, Mangiameli SM, Radey MC, Huang S et al. Bifunctional immunity proteins protect bacteria against FtsZ-Targeting ADP-ribosylating toxins. Cell 2018; 175:1380–1392 [View Article][PubMed]
    [Google Scholar]
  64. Vettiger A, Basler M. Type VI secretion system substrates are transferred and reused among sister cells. Cell 2016; 167:99–110 [View Article][PubMed]
    [Google Scholar]
  65. Willett JL, Gucinski GC, Fatherree JP, Low DA, Hayes CS. Contact-dependent growth inhibition toxins exploit multiple independent cell-entry pathways. Proc Natl Acad Sci 2015; 112:11341–11346 [View Article][PubMed]
    [Google Scholar]
  66. Russell AB, Hood RD, Bui NK, Leroux M, Vollmer W et al. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 2011; 475:343–347 [View Article][PubMed]
    [Google Scholar]
  67. Srikannathasan V, English G, Bui NK, Trunk K, O'Rourke PE et al. Structural basis for Type VI secreted peptidoglycan DL-endopeptidase function, specificity and neutralization in Serratia marcescens . Acta Crystallogr D Biol Crystallogr 2013; 69:2468–2482 [View Article][PubMed]
    [Google Scholar]
  68. Koskiniemi S, Garza-Sánchez F, Sandegren L, Webb JS, Braaten BA et al. Selection of orphan Rhs toxin expression in evolved Salmonella enterica serovar typhimurium. PLoS Genet 2014; 10:e1004255 [View Article][PubMed]
    [Google Scholar]
  69. Fitzsimons TC, Lewis JM, Wright A, Kleifeld O, Schittenhelm RB et al. Identification of novel acinetobacter baumannii Type VI secretion system antibacterial effector and immunity pairs. Infect Immun 2018; 86: [View Article][PubMed]
    [Google Scholar]
  70. Alcoforado Diniz J, Liu YC, Coulthurst SJ. Molecular weaponry: diverse effectors delivered by the Type VI secretion system. Cell Microbiol 2015; 17:1742–1751 [View Article][PubMed]
    [Google Scholar]
  71. Kirchberger PC, Unterweger D, Provenzano D, Pukatzki S, Boucher Y. Sequential displacement of Type VI secretion system effector genes leads to evolution of diverse immunity gene arrays in Vibrio cholerae . Sci Rep 2017; 7:45133 [View Article][PubMed]
    [Google Scholar]
  72. Batot G, Michalska K, Ekberg G, Irimpan EM, Joachimiak G et al. The CDI toxin of Yersinia kristensenii is a novel bacterial member of the RNase A superfamily. Nucleic Acids Res 2017; 45:5013–5025 [View Article][PubMed]
    [Google Scholar]
  73. Poole SJ, Diner EJ, Aoki SK, Braaten BA, T'kint de Roodenbeke C et al. Identification of functional toxin/immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems. PLoS Genet 2011; 7:e1002217 [View Article][PubMed]
    [Google Scholar]
  74. Hood RD, Singh P, Hsu F, Güvener T, Carl MA et al. A Type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 2010; 7:25–37 [View Article][PubMed]
    [Google Scholar]
  75. Anderson MC, Vonaesch P, Saffarian A, Marteyn BS, Sansonetti PJ. Shigella sonnei encodes a functional T6SS used for interbacterial competition and niche occupancy. Cell Host Microbe 2017; 21:769–776 [View Article][PubMed]
    [Google Scholar]
  76. Sana TG, Flaugnatti N, Lugo KA, Lam LH, Jacobson A et al. Salmonella typhimurium utilizes a T6SS-mediated antibacterial weapon to establish in the host gut. Proc Natl Acad Sci 2016; 113:E5044E5051 [View Article][PubMed]
    [Google Scholar]
  77. Fu Y, Ho BT, Mekalanos JJ. Tracking Vibrio cholerae cell-cell interactions during infection reveals bacterial population dynamics within intestinal microenvironments. Cell Host Microbe 2018; 23:274–281 [View Article][PubMed]
    [Google Scholar]
  78. Zhao W, Caro F, Robins W, Mekalanos JJ. Antagonism toward the intestinal microbiota and its effect on Vibrio cholerae virulence. Science 2018; 359:210–213 [View Article][PubMed]
    [Google Scholar]
  79. Fast D, Kostiuk B, Foley E, Pukatzki S. Commensal pathogen competition impacts host viability. Proc Natl Acad Sci 2018; 115:7099–7104 [View Article][PubMed]
    [Google Scholar]
  80. Logan SL, Thomas J, Yan J, Baker RP, Shields DS et al. The Vibrio cholerae Type VI secretion system can modulate host intestinal mechanics to displace gut bacterial symbionts. Proc Natl Acad Sci 2018; 115:E3779E3787 [View Article][PubMed]
    [Google Scholar]
  81. Coyne MJ, Roelofs KG, Comstock LE. Type VI secretion systems of human gut Bacteroidales segregate into three genetic architectures, two of which are contained on mobile genetic elements. BMC Genomics 2016; 17:58 [View Article][PubMed]
    [Google Scholar]
  82. Chatzidaki-Livanis M, Geva-Zatorsky N, Comstock LE. Bacteroides fragilis Type VI secretion systems use novel effector and immunity proteins to antagonize human gut Bacteroidales species. Proc Natl Acad Sci 2016; 113:3627–3632 [View Article][PubMed]
    [Google Scholar]
  83. Verster AJ, Ross BD, Radey MC, Bao Y, Goodman AL et al. The Landscape of Type VI secretion across human gut microbiomes reveals its role in community composition. Cell Host Microbe 2017; 22:411–419 [View Article][PubMed]
    [Google Scholar]
  84. Wexler AG, Bao Y, Whitney JC, Bobay LM, Xavier JB et al. Human symbionts inject and neutralize antibacterial toxins to persist in the gut. Proc Natl Acad Sci 2016; 113:3639–3644 [View Article][PubMed]
    [Google Scholar]
  85. Hecht AL, Casterline BW, Earley ZM, Goo YA, Goodlett DR et al. Strain competition restricts colonization of an enteric pathogen and prevents colitis. EMBO Rep 2016; 17:1281–1291 [View Article][PubMed]
    [Google Scholar]
  86. Steele MI, Kwong WK, Whiteley M, Moran NA. Diversification of Type VI secretion system toxins reveals ancient antagonism among bee gut microbes. mBio 2017; 8: [View Article][PubMed]
    [Google Scholar]
  87. Bernal P, Llamas MA, Filloux A. Type VI secretion systems in plant-associated bacteria. Environ Microbiol 2018; 20:1–15 [View Article][PubMed]
    [Google Scholar]
  88. Bernal P, Allsopp LP, Filloux A, Llamas MA. The Pseudomonas putida T6SS is a plant warden against phytopathogens. Isme J 2017; 11:972–987 [View Article][PubMed]
    [Google Scholar]
  89. Speare L, Cecere AG, Guckes KR, Smith S, Wollenberg MS et al. Bacterial symbionts use a Type VI secretion system to eliminate competitors in their natural host. Proc Natl Acad Sci 2018; 115:E8528E8537 [View Article][PubMed]
    [Google Scholar]
  90. Toska J, Ho BT, Mekalanos JJ. Exopolysaccharide protects Vibrio cholerae from exogenous attacks by the type 6 secretion system. Proc Natl Acad Sci 2018; 115:7997–8002 [View Article][PubMed]
    [Google Scholar]
  91. Alteri CJ, Himpsl SD, Pickens SR, Lindner JR, Zora JS et al. Multicellular bacteria deploy the Type VI secretion system to preemptively strike neighboring cells. PLoS Pathog 2013; 9:e1003608 [View Article][PubMed]
    [Google Scholar]
  92. Wenren LM, Sullivan NL, Cardarelli L, Septer AN, Gibbs KA. Two independent pathways for self-recognition in Proteus mirabilis are linked by Type VI-dependent export. mBio 2013; 4:e0037413 [View Article][PubMed]
    [Google Scholar]
  93. Gong Y, Zhang Z, Liu Y, Zhou XW, Anwar MN et al. A nuclease-toxin and immunity system for kin discrimination in Myxococcus xanthus . Environ Microbiol 2018; 20:2552–2567 [View Article][PubMed]
    [Google Scholar]
  94. Majerczyk C, Schneider E, Greenberg EP. Quorum sensing control of Type VI secretion factors restricts the proliferation of quorum-sensing mutants. eLife 2016; 5: [View Article][PubMed]
    [Google Scholar]
  95. Troselj V, Treuner-Lange A, Søgaard-Andersen L, Wall D. Physiological heterogeneity triggers sibling conflict mediated by the Type VI secretion system in an aggregative multicellular bacterium. mBio 2018; 9: [View Article][PubMed]
    [Google Scholar]
  96. McNally L, Bernardy E, Thomas J, Kalziqi A, Pentz J et al. Killing by Type VI secretion drives genetic phase separation and correlates with increased cooperation. Nat Commun 2017; 8:14371 [View Article][PubMed]
    [Google Scholar]
  97. Borgeaud S, Metzger LC, Scrignari T, Blokesch M. The Type VI secretion system of Vibrio cholerae fosters horizontal gene transfer. Science 2015; 347:63–67 [View Article][PubMed]
    [Google Scholar]
  98. Thomas J, Watve SS, Ratcliff WC, Hammer BK. Horizontal gene transfer of functional Type VI killing genes by natural transformation. mBio 2017; 8: [View Article][PubMed]
    [Google Scholar]
  99. Cooper RM, Tsimring L, Hasty J. Inter-species population dynamics enhance microbial horizontal gene transfer and spread of antibiotic resistance. elife 2017; 6: [View Article][PubMed]
    [Google Scholar]
  100. Ringel PD, Hu D, Basler M. The role of Type VI secretion system effectors in target Cell lysis and subsequent horizontal gene transfer. Cell Rep 2017; 21:3927–3940 [View Article][PubMed]
    [Google Scholar]
  101. Hachani A, Wood TE, Filloux A. Type VI secretion and anti-host effectors. Curr Opin Microbiol 2016; 29:81–93 [View Article][PubMed]
    [Google Scholar]
  102. Jiang F, Waterfield NR, Yang J, Yang G, Jin Q. A Pseudomonas aeruginosa Type VI secretion phospholipase D effector targets both prokaryotic and eukaryotic cells. Cell Host Microbe 2014; 15:600–610 [View Article][PubMed]
    [Google Scholar]
  103. Brodmann M, Dreier RF, Broz P, Basler M. Francisella requires dynamic Type VI secretion system and ClpB to deliver effectors for phagosomal escape. Nat Commun 2017; 8:15853 [View Article][PubMed]
    [Google Scholar]
  104. Eshraghi A, Kim J, Walls AC, Ledvina HE, Miller CN et al. Secreted effectors encoded within and outside of the Francisella pathogenicity island promote intramacrophage growth. Cell Host Microbe 2016; 20:573–583 [View Article][PubMed]
    [Google Scholar]
  105. Ledvina HE, Kelly KA, Eshraghi A, Plemel RL, Peterson SB et al. A Phosphatidylinositol 3-kinase effector alters phagosomal maturation to promote intracellular growth of Francisella . Cell Host Microbe 2018; 24:285–295 [View Article][PubMed]
    [Google Scholar]
  106. Aubert DF, Xu H, Yang J, Shi X, Gao W et al. A Burkholderia Type VI effector deamidates Rho GTPases to activate the pyrin inflammasome and trigger inflammation. Cell Host Microbe 2016; 19:664–674 [View Article][PubMed]
    [Google Scholar]
  107. Chen H, Yang D, Han F, Tan J, Zhang L et al. The Bacterial T6SS effector EvpP prevents NLRP3 inflammasome activation by inhibiting the Ca(2+)-dependent MAPK-Jnk pathway. Cell Host Microbe 2017; 21:47–58 [View Article][PubMed]
    [Google Scholar]
  108. Jiang F, Wang X, Wang B, Chen L, Zhao Z et al. The Pseudomonas aeruginosa Type VI secretion PGAP1-like effector induces host autophagy by activating endoplasmic reticulum stress. Cell Rep 2016; 16:1502–1509 [View Article][PubMed]
    [Google Scholar]
  109. Ray A, Schwartz N, de Souza Santos M, Zhang J, Orth K et al. Type VI secretion system MIX-effectors carry both antibacterial and anti-eukaryotic activities. EMBO Rep 2017; 18:1978–1990 [View Article][PubMed]
    [Google Scholar]
  110. Wan B, Zhang Q, Ni J, Li S, Wen D et al. Type VI secretion system contributes to Enterohemorrhagic Escherichia coli virulence by secreting catalase against host reactive oxygen species (ROS). PLoS Pathog 2017; 13:e1006246 [View Article][PubMed]
    [Google Scholar]
  111. Peleg AY, Hogan DA, Mylonakis E. Medically important bacterial-fungal interactions. Nat Rev Microbiol 2010; 8:340–349 [View Article][PubMed]
    [Google Scholar]
  112. Haapalainen M, Mosorin H, Dorati F, Wu RF, Roine E et al. Hcp2, a secreted protein of the phytopathogen Pseudomonas syringae pv. tomato DC3000, is required for fitness for competition against bacteria and yeasts. J Bacteriol 2012; 194:4810–4822 [View Article][PubMed]
    [Google Scholar]
  113. Marchi M, Boutin M, Gazengel K, Rispe C, Gauthier JP et al. Genomic analysis of the biocontrol strain Pseudomonas fluorescens Pf29Arp with evidence of T3SS and T6SS gene expression on plant roots. Environ Microbiol Rep 2013; 5:393–403 [View Article][PubMed]
    [Google Scholar]
  114. Trunk K, Peltier J, Liu YC, Dill BD, Walker L et al. The Type VI secretion system deploys antifungal effectors against microbial competitors. Nat Microbiol 2018; 3:920–931 [View Article][PubMed]
    [Google Scholar]
  115. Miyata ST, Kitaoka M, Brooks TM, McAuley SB, Pukatzki S. Vibrio cholerae requires the Type VI secretion system virulence factor VasX to kill Dictyostelium discoideum . Infect Immun 2011; 79:2941–2949 [View Article][PubMed]
    [Google Scholar]
  116. Zheng J, Ho B, Mekalanos JJ. Genetic analysis of anti-amoebae and anti-bacterial activities of the Type VI secretion system in Vibrio cholerae . PLoS One 2011; 6:e23876 [View Article][PubMed]
    [Google Scholar]
  117. Wang T, Si M, Song Y, Zhu W, Gao F et al. Type VI secretion system transports Zn2+ to combat multiple stresses and host immunity. PLoS Pathog 2015; 11:e1005020 [View Article][PubMed]
    [Google Scholar]
  118. Si M, Wang Y, Zhang B, Zhao C, Kang Y et al. The Type VI secretion system engages a redox-regulated Dual-functional heme transporter for zinc acquisition. Cell Rep 2017; 20:949–959 [View Article][PubMed]
    [Google Scholar]
  119. Si M, Zhao C, Burkinshaw B, Zhang B, Wei D et al. Manganese scavenging and oxidative stress response mediated by Type VI secretion system in Burkholderia thailandensis . Proc Natl Acad Sci 2017; 114:E2233E2242 [View Article][PubMed]
    [Google Scholar]
  120. Lin J, Zhang W, Cheng J, Yang X, Zhu K et al. A Pseudomonas T6SS effector recruits PQS-containing outer membrane vesicles for iron acquisition. Nat Commun 2017; 8:14888 [View Article][PubMed]
    [Google Scholar]
  121. Böck D, Medeiros JM, Tsao HF, Penz T, Weiss GL et al. In situ architecture, function, and evolution of a contractile injection system. Science 2017; 357:713–717 [View Article][PubMed]
    [Google Scholar]
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