1887

Abstract

The life of bacteria is challenging, to endure bacteria employ a range of mechanisms to optimize their environment, including deploying the type VI secretion system (T6SS). Acting as a bacterial crossbow, this system delivers effectors responsible for subverting host cells, killing competitors and facilitating general secretion to access common goods. Due to its importance, this lethal machine has been evolutionarily maintained, disseminated and specialized to fulfil these vital functions. In fact, T6SS structural clusters are present in over 25 % of Gram-negative bacteria, varying in number from one to six different genetic clusters per organism. Since its discovery in 2006, research on the T6SS has rapidly progressed, yielding remarkable breakthroughs. The identification and characterization of novel components of the T6SS, combined with biochemical and structural studies, have revealed fascinating mechanisms governing its assembly, loading, firing and disassembly processes. Recent findings have also demonstrated the efficacy of this system against fungal and Gram-positive cells, expanding its scope. Ongoing research continues to uncover an extensive and expanding repertoire of T6SS effectors, the genuine mediators of T6SS function. These studies are shedding light on new aspects of the biology of prokaryotic and eukaryotic organisms. This review provides a comprehensive overview of the T6SS, highlighting recent discoveries of its structure and the diversity of its effectors. Additionally, it injects a personal perspective on avenues for future research, aiming to deepen our understanding of this combative system.

Funding
This study was supported by the:
  • Proyecto de Excelencia Junta de Andalucia (Award ProyExcel_00450)
    • Principle Award Recipient: PatriciaBernal
  • Proyectos Estratégicos Orientados a la Transición Ecológica y a la Transición Digital (Award TED2021-130357B-I00)
    • Principle Award Recipient: PatriciaBernal
  • Subprograma Estatal de Generación de Conocimiento de la Ministerio de Ciencia e Innovación (Award PID2021-123000OB-I00)
    • Principle Award Recipient: PatriciaBernal
  • Academy of Medical Sciences (Award SBF006\1,161)
    • Principle Award Recipient: LukeP Allsopp
  • European Society of Clinical Microbiology and Infectious Diseases (Award Research Grant 2020)
    • Principle Award Recipient: LukeP Allsopp
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.001367
2023-07-25
2024-05-08
Loading full text...

Full text loading...

/deliver/fulltext/micro/169/7/mic001367.html?itemId=/content/journal/micro/10.1099/mic.0.001367&mimeType=html&fmt=ahah

References

  1. 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]
  2. Trunk K, Peltier J, Liu Y-C, 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]
  3. Yang X, Liu H, Zhang Y, Shen X. Roles of type VI secretion system in transport of metal ions. Front Microbiol 2021; 12:756136 [View Article]
    [Google Scholar]
  4. 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]
  5. Hernandez RE, Gallegos-Monterrosa R, Coulthurst SJ. Type VI secretion system effector proteins: effective weapons for bacterial competitiveness. Cell Microbiol 2020; 22:e13241 [View Article] [PubMed]
    [Google Scholar]
  6. Jurėnas D, Journet L. Activity, delivery, and diversity of Type VI secretion effectors. Mol Microbiol 2021; 115:383–394 [View Article] [PubMed]
    [Google Scholar]
  7. Monjarás Feria J, Valvano MA. An overview of anti-eukaryotic T6SS effectors. Front Cell Infect Microbiol 2020; 10:584751 [View Article] [PubMed]
    [Google Scholar]
  8. 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]
  9. Bingle LEH, Bailey CM, Pallen MJ. Type VI secretion: a beginner’s guide. Curr Opin Microbiol 2008; 11:3–8 [View Article] [PubMed]
    [Google Scholar]
  10. 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; 10:104–114 [View Article] [PubMed]
    [Google Scholar]
  11. Cherrak Y, Flaugnatti N, Durand E, Journet L, Cascales E. Structure and activity of the Type VI secretion system. Microbiol Spectr 2019; 7:7 [View Article] [PubMed]
    [Google Scholar]
  12. 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]
    [Google Scholar]
  13. 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]
    [Google Scholar]
  14. 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]
  15. 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]
  16. Bröms JE, Sjöstedt A, Lavander M. The role of the Francisella tularensis pathogenicity island in type VI secretion, intracellular survival, and modulation of host cell signaling. Front Microbio 2010; 1: [View Article]
    [Google Scholar]
  17. Spidlova P, Stulik J. Francisella tularensis type VI secretion system comes of age. Virulence 2017; 8:628–631 [View Article] [PubMed]
    [Google Scholar]
  18. Böck D, Medeiros JM, Tsao H-F, Penz T, Weiss GL et al. In situ architecture, function, and evolution of a contractile injection system. Science 2017; 357:713–717 [View Article]
    [Google Scholar]
  19. Leiman PG, Basler M, Ramagopal UA, Bonanno JB, Sauder JM et al. Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci 2009; 106:4154–4159 [View Article] [PubMed]
    [Google Scholar]
  20. Silverman JM, Brunet YR, Cascales E, Mougous JD. Structure and regulation of the type VI secretion system. Annu Rev Microbiol 2012; 66:453–472 [View Article] [PubMed]
    [Google Scholar]
  21. Rapisarda C, Cherrak Y, Kooger R, Schmidt V, Pellarin R et al. In situ and high-resolution cryo-EM structure of a bacterial type VI secretion system membrane complex. EMBO J 2019; 38:e100886 [View Article] [PubMed]
    [Google Scholar]
  22. 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]
  23. 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]
  24. 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] [PubMed]
    [Google Scholar]
  25. 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]
  26. Aschtgen M-S, Bernard CS, De Bentzmann S, Lloubès R, Cascales E. SciN is an outer membrane lipoprotein required for type VI secretion in enteroaggregative Escherichia coli. J Bacteriol 2008; 190:7523–7531 [View Article] [PubMed]
    [Google Scholar]
  27. Felisberto-Rodrigues C, Durand E, Aschtgen M-S, Blangy S, Ortiz-Lombardia M et al. Towards a structural comprehension of bacterial type VI secretion systems: characterization of the TssJ-TssM complex of an Escherichia coli pathovar. PLoS Pathog 2011; 7:e1002386 [View Article]
    [Google Scholar]
  28. 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]
  29. Kapitein N, Bönemann G, Pietrosiuk A, Seyffer F, Hausser I et al. ClpV recycles VipA/VipB tubules and prevents non-productive tubule formation to ensure efficient type VI protein secretion. Mol Microbiol 2013; 87:1013–1028 [View Article] [PubMed]
    [Google Scholar]
  30. Bernal P, Furniss RCD, Fecht S, Leung RCY, Spiga L et al. A novel stabilization mechanism for the type VI secretion system sheath. Proc Natl Acad Sci 2021; 118:e2008500118 [View Article] [PubMed]
    [Google Scholar]
  31. Aschtgen MS, Thomas MS, Cascales E. Anchoring the type VI secretion system to the peptidoglycan: TssL, TagL, TagP what else?. Virulence 2010; 1:535–540 [View Article]
    [Google Scholar]
  32. 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]
  33. Santin YG, Camy CE, Zoued A, Doan T, Aschtgen M-S et al. Role and recruitment of the TagL peptidoglycan-binding protein during type VI secretion system biogenesis. J Bacteriol 2019; 201:e00173-19 [View Article] [PubMed]
    [Google Scholar]
  34. 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]
  35. Reglinski M, Monlezun L, Coulthurst SJ. The accessory protein TagV is required for full Type VI secretion system activity in Serratia marcescens. Mol Microbiol 2023; 119:326–339 [View Article] [PubMed]
    [Google Scholar]
  36. 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:e01253-16 [View Article] [PubMed]
    [Google Scholar]
  37. 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]
  38. Scheurwater EM, Burrows LL. Maintaining network security: how macromolecular structures cross the peptidoglycan layer. FEMS Microbiol Lett 2011; 318:1–9 [View Article] [PubMed]
    [Google Scholar]
  39. Planamente S, Salih O, Manoli E, Albesa-Jové D, Freemont PS et al. TssA forms a gp6-like ring attached to the type VI secretion sheath. EMBO J 2016; 35:1613–1627 [View Article] [PubMed]
    [Google Scholar]
  40. 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]
    [Google Scholar]
  41. Schneider JP, Nazarov S, Adaixo R, Liuzzo M, Ringel PD et al. Diverse roles of TssA-like proteins in the assembly of bacterial type VI secretion systems. EMBO J 2019; 38:e100825 [View Article] [PubMed]
    [Google Scholar]
  42. 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] [PubMed]
    [Google Scholar]
  43. Brunet YR, Zoued A, Boyer F, Douzi B, Cascales E. 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 2015; 11:e1005545 [View Article] [PubMed]
    [Google Scholar]
  44. Park Y-J, Lacourse KD, Cambillau C, DiMaio F, Mougous JD et al. Structure of the type VI secretion system TssK-TssF-TssG baseplate subcomplex revealed by cryo-electron microscopy. Nat Commun 2018; 9:5385 [View Article] [PubMed]
    [Google Scholar]
  45. 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]
  46. Vanlioğlu E, Santin YG, Filella-Merce I, Pellarin R, Cascales E. Coevolution-guided mapping of the type VI secretion membrane complex-baseplate interface. J Mol Biol 2023; 435:167918 [View Article] [PubMed]
    [Google Scholar]
  47. Nguyen VS, Logger L, Spinelli S, Legrand P, Huyen Pham TT et al. Type VI secretion TssK baseplate protein exhibits structural similarity with phage receptor-binding proteins and evolved to bind the membrane complex. Nat Microbiol 2017; 2:17103 [View Article] [PubMed]
    [Google Scholar]
  48. English G, Byron O, Cianfanelli FR, Prescott AR, Coulthurst SJ. Biochemical analysis of TssK, a core component of the bacterial Type VI secretion system, reveals distinct oligomeric states of TssK and identifies a TssK-TssFG subcomplex. Biochem J 2014; 461:291–304 [View Article] [PubMed]
    [Google Scholar]
  49. Liebl D, Robert-Genthon M, Job V, Cogoni V, Attrée I. Baseplate component TssK and spatio-temporal assembly of T6SS in Pseudomonas aeruginosa. Front Microbiol 2019; 10:1615 [View Article] [PubMed]
    [Google Scholar]
  50. Zoued A, Cassaro CJ, Durand E, Douzi B, España AP et al. Structure-function analysis of the TssL cytoplasmic domain reveals a new interaction between the type VI secretion baseplate and membrane complexes. J Mol Biol 2016; 428:4413–4423 [View Article] [PubMed]
    [Google Scholar]
  51. Douzi B, Logger L, Spinelli S, Blangy S, Cambillau C et al. Structure-function analysis of the C-terminal domain of the type VI secretion TssB tail sheath subunit. J Mol Biol 2018; 430:297–309 [View Article] [PubMed]
    [Google Scholar]
  52. Mougous JD, Gifford CA, Ramsdell TL, Mekalanos JJ. Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat Cell Biol 2007; 9:797–803 [View Article] [PubMed]
    [Google Scholar]
  53. Lin J-S, Pissaridou P, Wu H-H, Tsai M-D, Filloux A et al. TagF-mediated repression of bacterial type VI secretion systems involves a direct interaction with the cytoplasmic protein Fha. J Biol Chem 2018; 293:8829–8842 [View Article] [PubMed]
    [Google Scholar]
  54. Silverman JM, Austin LS, Hsu F, Hicks KG, Hood RD et al. Separate inputs modulate phosphorylation-dependent and -independent type VI secretion activation. Mol Microbiol 2011; 82:1277–1290 [View Article] [PubMed]
    [Google Scholar]
  55. 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]
  56. Casabona MG, Silverman JM, Sall KM, Boyer F, Couté Y et al. An ABC transporter and an outer membrane lipoprotein participate in posttranslational activation of type VI secretion in Pseudomonas aeruginosa. Environ Microbiol 2013; 15:471–486 [View Article] [PubMed]
    [Google Scholar]
  57. Hsu F, Schwarz S, Mougous JD. TagR promotes PpkA-catalysed type VI secretion activation in Pseudomonas aeruginosa. Mol Microbiol 2009; 72:1111–1125 [View Article] [PubMed]
    [Google Scholar]
  58. Lin J-S, Wu H-H, Hsu P-H, Ma L-S, Pang Y-Y 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]
  59. 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]
  60. Ziveri J, Chhuon C, Jamet A, Rytter H, Prigent G et al. Critical role of a sheath phosphorylation site on the assembly and function of an atypical type VI secretion system. Mol Cell Proteomics 2019; 18:2418–2432 [View Article] [PubMed]
    [Google Scholar]
  61. Brunet YR, Hénin J, Celia H, Cascales E. Type VI secretion and bacteriophage tail tubes share a common assembly pathway. EMBO Rep 2014; 15:315–321 [View Article] [PubMed]
    [Google Scholar]
  62. Zoued A, Durand E, Santin YG, Journet L, Roussel A et al. TssA: The cap protein of the Type VI secretion system tail. Bioessays 2017; 39:1600262 [View Article] [PubMed]
    [Google Scholar]
  63. 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]
  64. Spínola-Amilibia M, Davó-Siguero I, Ruiz FM, Santillana E, Medrano FJ et al. The structure of VgrG1 from Pseudomonas aeruginosa, the needle tip of the bacterial type VI secretion system. Acta Crystallogr D Struct Biol 2016; 72:22–33 [View Article] [PubMed]
    [Google Scholar]
  65. Uchida K, Leiman PG, Arisaka F, Kanamaru S. Structure and properties of the C-terminal β-helical domain of VgrG protein from Escherichia coli O157. J Biochem 2014; 155:173–182 [View Article] [PubMed]
    [Google Scholar]
  66. 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]
  67. 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]
  68. Unterweger D, Kostiuk B, Pukatzki S. Adaptor proteins of Type VI secretion system effectors. Trends Microbiol 2017; 25:8–10 [View Article] [PubMed]
    [Google Scholar]
  69. Bondage DD, Lin JS, Ma LS, Kuo CH, Lai EM. VgrG C terminus confers the type VI effector transport specificity and is required for binding with PAAR and adaptor–effector complex. Proc Natl Acad Sci 2016; 113:E3931–E3940 [View Article]
    [Google Scholar]
  70. 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]
    [Google Scholar]
  71. Ballister ER, Lai AH, Zuckermann RN, Cheng Y, Mougous JD. In vitro self-assembly of tailorable nanotubes from a simple protein building block. Proc Natl Acad Sci 2008; 105:3733–3738 [View Article]
    [Google Scholar]
  72. 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]
    [Google Scholar]
  73. Clemens DL, Ge P, Lee B-Y, Horwitz MA, Zhou ZH. Atomic structure of T6SS reveals interlaced array essential to function. Cell 2015; 160:940–951 [View Article] [PubMed]
    [Google Scholar]
  74. Salih O, He S, Planamente S, Stach L, MacDonald JT et al. Atomic structure of type VI contractile sheath from Pseudomonas aeruginosa. Structure 2018; 26:329–336 [View Article] [PubMed]
    [Google Scholar]
  75. Basler M. Type VI secretion system: secretion by a contractile nanomachine. Phil Trans R Soc B 2015; 370:20150021 [View Article]
    [Google Scholar]
  76. Chang Y-W, Rettberg LA, Ortega DR, Jensen GJ. In vivo structures of an intact type VI secretion system revealed by electron cryotomography. EMBO Rep 2017; 18:1090–1099 [View Article] [PubMed]
    [Google Scholar]
  77. Ge P, Scholl D, Leiman PG, Yu X, Miller JF et al. Atomic structures of a bactericidal contractile nanotube in its pre- and postcontraction states. Nat Struct Mol Biol 2015; 22:377–382 [View Article] [PubMed]
    [Google Scholar]
  78. Bönemann G, Pietrosiuk A, Diemand A, Zentgraf H, Mogk A. Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J 2009; 28:315–325 [View Article]
    [Google Scholar]
  79. Schlieker C, Zentgraf H, Dersch P, Mogk A. ClpV, a unique Hsp100/Clp member of pathogenic proteobacteria. Biol Chem 2005; 386:1115–1127 [View Article] [PubMed]
    [Google Scholar]
  80. Pietrosiuk A, Lenherr ED, Falk S, Bönemann G, Kopp J et al. Molecular basis for the unique role of the AAA+ chaperone ClpV in type VI protein secretion. J Biol Chem 2011; 286:30010–30021 [View Article] [PubMed]
    [Google Scholar]
  81. Kube S, Kapitein N, Zimniak T, Herzog F, Mogk A et al. Structure of the VipA/B type VI secretion complex suggests a contraction-state-specific recycling mechanism. Cell Rep 2014; 8:20–30 [View Article] [PubMed]
    [Google Scholar]
  82. 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]
  83. Hachani A, Lossi NS, Hamilton A, Jones C, Bleves S et al. Type VI secretion system in Pseudomonas aeruginosa: secretion and multimerization of VgrG proteins. J Biol Chem 2011; 286:12317–12327 [View Article] [PubMed]
    [Google Scholar]
  84. 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]
  85. Heisler DB, Kudryashova E, Grinevich DO, Suarez C, Winkelman JD et al. ACTIN-DIRECTED TOXIN. ACD toxin-produced actin oligomers poison formin-controlled actin polymerization. Science 2015; 349:535–539 [View Article] [PubMed]
    [Google Scholar]
  86. 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:E5044–51 [View Article] [PubMed]
    [Google Scholar]
  87. Allsopp LP, Bernal P, Nolan LM, Filloux A. Causalities of war: the connection between type VI secretion system and microbiota. Cell Microbiol 2020; 22:e13153 [View Article] [PubMed]
    [Google Scholar]
  88. Speare L, Jackson A, Septer AN. Calcium promotes T6SS-mediated killing and aggregation between competing symbionts. Microbiol Spectr 2022; 10:e0139722 [View Article] [PubMed]
    [Google Scholar]
  89. Yang Y, Pan D, Tang Y, Li J, Zhu K et al. H3-T6SS of Pseudomonas aeruginosa PA14 contributes to environmental adaptation via secretion of a biofilm-promoting effector. Stress Biol 2022; 2:55 [View Article]
    [Google Scholar]
  90. 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]
  91. Storey D, McNally A, Åstrand M, Sa-Pessoa Graca Santos J, Rodriguez-Escudero I et al. Klebsiella pneumoniae type VI secretion system-mediated microbial competition is PhoPQ controlled and reactive oxygen species dependent. PLoS Pathog 2020; 16:e1007969 [View Article] [PubMed]
    [Google Scholar]
  92. Trunk K, Coulthurst SJ, Quinn J. A new front in microbial warfare-delivery of antifungal effectors by the Type VI secretion system. J Fungi 2019; 5:50 [View Article]
    [Google Scholar]
  93. Yang X, Clemens DL, Lee B-Y, Cui Y, Zhou ZH et al. Atomic structure of the Francisella T6SS central spike reveals a unique α-Helical Lid and a putative cargo. Structure 2019; 27:1811–1819 [View Article]
    [Google Scholar]
  94. Brodmann M, Schnider ST, Basler M, Monack D. Type VI secretion system and its effectors PdpC, PdpD, and OpiA contribute to Francisella virulence in Galleria mellonella larvae. Infect Immun 2021; 89:e0057920 [View Article] [PubMed]
    [Google Scholar]
  95. Long ME, Lindemann SR, Rasmussen JA, Jones BD, Allen L-AH. Disruption of Francisella tularensis Schu S4 iglI, iglJ, and pdpC genes results in attenuation for growth in human macrophages and in vivo virulence in mice and reveals a unique phenotype for pdpC. Infect Immun 2013; 81:850–861 [View Article] [PubMed]
    [Google Scholar]
  96. Cantlay S, Kaftanic C, Horzempa J. PdpC, a secreted effector protein of the type six secretion system, is required for erythrocyte invasion by Francisella tularensis LVS. Front Cell Infect Microbiol 2022; 12:979693 [View Article] [PubMed]
    [Google Scholar]
  97. Ren A, Jia M, Liu J, Zhou T, Wu L et al. Acquisition of T6SS effector TseL contributes to the emerging of novel epidemic strains of Pseudomonas aeruginosa. Microbiol Spectr 2023; 11:03308–03322 [View Article]
    [Google Scholar]
  98. Robinson LA, Collins ACZ, Murphy RA, Davies JC, Allsopp LP. Diversity and prevalence of type VI secretion system effectors in clinical Pseudomonas aeruginosa isolates. Front Microbiol 2022; 13:1042505 [View Article] [PubMed]
    [Google Scholar]
  99. Sá-Pessoa J, López-Montesino S, Przybyszewska K, Rodríguez-Escudero I, Marshall H et al. A trans-kingdom T6SS effector induces the fragmentation of the mitochondrial network and activates innate immune receptor NLRX1 to promote infection. Nat Commun 2023; 14:871 [View Article] [PubMed]
    [Google Scholar]
  100. Salinero-Lanzarote A, Pacheco-Moreno A, Domingo-Serrano L, Durán D, Ormeño-Orrillo E et al. The Type VI secretion system of Rhizobium etli Mim1 has a positive effect in symbiosis. FEMS Microbiol Ecol 2019; 95:fiz054 [View Article] [PubMed]
    [Google Scholar]
  101. Bladergroen MR, Badelt K, Spaink HP. Infection-blocking genes of a symbiotic Rhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. Mol Plant Microbe Interact 2003; 16:53–64 [View Article] [PubMed]
    [Google Scholar]
  102. Ma L-S, Hachani A, Lin J-S, Filloux A, Lai E-M. 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]
  103. Pissaridou P, Allsopp LP, Wettstadt S, Howard SA, Mavridou DAI et al. The Pseudomonas aeruginosa T6SS-VgrG1b spike is topped by a PAAR protein eliciting DNA damage to bacterial competitors. Proc Natl Acad Sci 2018; 115:12519–12524 [View Article] [PubMed]
    [Google Scholar]
  104. 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]
  105. 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]
  106. Nolan LM, Cain AK, Clamens T, Furniss RCD, Manoli E et al. Identification of Tse8 as a Type VI secretion system toxin from Pseudomonas aeruginosa that targets the bacterial transamidosome to inhibit protein synthesis in prey cells. Nat Microbiol 2021; 6:1199–1210 [View Article] [PubMed]
    [Google Scholar]
  107. 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]
  108. Ahmad S, Wang B, Walker MD, Tran H-KR, Stogios PJ et al. An interbacterial toxin inhibits target cell growth by synthesizing (p)ppApp. Nature 2019; 575:674–678 [View Article] [PubMed]
    [Google Scholar]
  109. 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]
  110. de Moraes MH, Hsu F, Huang D, Bosch DE, Zeng J et al. An interbacterial DNA deaminase toxin directly mutagenizes surviving target populations. Elife 2021; 10:1–78 [View Article] [PubMed]
    [Google Scholar]
  111. González-Magaña A, Altuna J, Queralt-Martín M, Largo E, Velázquez C et al. The P. aeruginosa effector Tse5 forms membrane pores disrupting the membrane potential of intoxicated bacteria. Commun Biol 2022; 5:1189 [View Article] [PubMed]
    [Google Scholar]
  112. Mok BY, de Moraes MH, Zeng J, Bosch DE, Kotrys AV et al. A bacterial cytidine deaminase toxin enables CRISPR-free mitochondrial base editing. Nature 2020; 583:631–637 [View Article] [PubMed]
    [Google Scholar]
  113. 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]
  114. Ting S-Y, 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]
  115. Molina-Santiago C, Pearson JR, Navarro Y, Berlanga-Clavero MV, Caraballo-Rodriguez AM et al. The extracellular matrix protects Bacillus subtilis colonies from Pseudomonas invasion and modulates plant co-colonization. Nat Commun 2019; 10:1919–15 [View Article]
    [Google Scholar]
  116. Le N-H, Pinedo V, Lopez J, Cava F, Feldman MF. Killing of Gram-negative and Gram-positive bacteria by a bifunctional cell wall-targeting T6SS effector. Proc Natl Acad Sci 2021; 118:e2106555118–6 [View Article] [PubMed]
    [Google Scholar]
  117. Pei T, Kan Y, Wang Z, Tang M, Li H et al. Delivery of an Rhs‐family nuclease effector reveals direct penetration of the gram‐positive cell envelope by a type VI secretion system in Acidovorax citrulli. mLife 2022; 1:66–78 [View Article]
    [Google Scholar]
  118. 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]
  119. Li C, Zhu L, Wang D, Wei Z, Hao X et al. T6SS secretes an LPS-binding effector to recruit OMVs for exploitative competition and horizontal gene transfer. ISME J 2022; 16:500–510 [View Article] [PubMed]
    [Google Scholar]
  120. Garcia EC, Perault AI, Marlatt SA, Cotter PA. Interbacterial signaling via Burkholderia contact-dependent growth inhibition system proteins. Proc Natl Acad Sci 2016; 113:8296–8301 [View Article] [PubMed]
    [Google Scholar]
  121. Song L, Pan J, Yang Y, Zhang Z, Cui R et al. Contact-independent killing mediated by a T6SS effector with intrinsic cell-entry properties. Nat Commun 2021; 12:423 [View Article] [PubMed]
    [Google Scholar]
  122. Wang D, Zhu L, Zhen X, Yang D, Li C et al. A secreted effector with a dual role as a toxin and as a transcriptional factor. Nat Commun 2022; 13:7779 [View Article]
    [Google Scholar]
  123. Nikolic N, Bergmiller T, Vandervelde A, Albanese TG, Gelens L et al. Autoregulation of mazEF expression underlies growth heterogeneity in bacterial populations. Nucleic Acids Res 2018; 46:2918–2931 [View Article] [PubMed]
    [Google Scholar]
  124. 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]
  125. Han Y, Wang T, Chen G, Pu Q, Liu Q et al. A Pseudomonas aeruginosa type VI secretion system regulated by CueR facilitates copper acquisition. PLoS Pathog 2019; 15:e1008198 [View Article] [PubMed]
    [Google Scholar]
  126. 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:E2233–E2242 [View Article] [PubMed]
    [Google Scholar]
  127. Zhu L, Xu L, Wang C, Li C, Li M et al. T6SS translocates a micropeptide to suppress STING-mediated innate immunity by sequestering manganese. Proc Natl Acad Sci 2021; 118:e2103526118 [View Article] [PubMed]
    [Google Scholar]
  128. Lin RJ, Capage M, Hill CW. A repetitive DNA sequence, rhs, responsible for duplications within the Escherichia coli K-12 chromosome. J Mol Biol 1984; 177:1–18 [View Article] [PubMed]
    [Google Scholar]
  129. Jackson AP, Thomas GH, Parkhill J, Thomson NR. Evolutionary diversification of an ancient gene family (rhs) through C-terminal displacement. BMC Genomics 2009; 10:584–600 [View Article] [PubMed]
    [Google Scholar]
  130. 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]
  131. 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]
  132. Pei T-T, Li H, Liang X, Wang Z-H, Liu G et al. Intramolecular chaperone-mediated secretion of an Rhs effector toxin by a type VI secretion system. Nat Commun 2020; 11:1865 [View Article] [PubMed]
    [Google Scholar]
  133. 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]
    [Google Scholar]
  134. 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]
  135. 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]
  136. 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]
  137. 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]
  138. Busby JN, Panjikar S, Landsberg MJ, Hurst MRH, Lott JS. The BC component of ABC toxins is an RHS-repeat-containing protein encapsulation device. Nature 2013; 501:547–550 [View Article] [PubMed]
    [Google Scholar]
  139. Günther P, Quentin D, Ahmad S, Sachar K, Gatsogiannis C et al. Structure of a bacterial Rhs effector exported by the type VI secretion system. PLoS Pathog 2022; 18:e1010182 [View Article]
    [Google Scholar]
  140. Jurėnas D, Rosa LT, Rey M, Chamot-Rooke J, Fronzes R et al. Mounting, structure and autocleavage of a type VI secretion-associated Rhs polymorphic toxin. Nat Commun 2021; 12:6998 [View Article] [PubMed]
    [Google Scholar]
  141. Tang L, Dong S, Rasheed N, Wu HW, Zhou N et al. Vibrio parahaemolyticus prey targeting requires autoproteolysis-triggered dimerization of the type VI secretion system effector RhsP. Cell Reports 2022; 41:111732 [View Article]
    [Google Scholar]
  142. 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]
  143. 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]
    [Google Scholar]
  144. Liang X, Moore R, Wilton M, Wong MJQ, Lam L et al. Identification of divergent type VI secretion effectors using a conserved chaperone domain. Proc Natl Acad Sci 2015; 112:9106–9111 [View Article]
    [Google Scholar]
  145. 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]
  146. 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]
  147. Liu Y, Zhang Z, Wang F, Li D-D, Li Y-Z. Identification of type VI secretion system toxic effectors using adaptors as markers. Comput Struct Biotechnol J 2020; 18:3723–3733 [View Article] [PubMed]
    [Google Scholar]
  148. Filloux A. Bacterial protein secretion systems: game of types. Microbiology 2022; 168: [View Article] [PubMed]
    [Google Scholar]
  149. Dar Y, Jana B, Bosis E, Salomon D. A binary effector module secreted by a type VI secretion system. EMBO Rep 2022; 23:e53981 [View Article] [PubMed]
    [Google Scholar]
  150. Flaugnatti N, Le TTH, Canaan S, Aschtgen M-S, 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]
  151. Flaugnatti N, Rapisarda C, Rey M, Beauvois SG, Nguyen VA et al. Structural basis for loading and inhibition of a bacterial T6SS phospholipase effector by the VgrG spike. EMBO J 2020; 39:e104129 [View Article] [PubMed]
    [Google Scholar]
  152. Liang X, Kamal F, Pei T-T, Xu P, Mekalanos JJ et al. An onboard checking mechanism ensures effector delivery of the type VI secretion system in Vibrio cholerae. Proc Natl Acad Sci 2019; 116:23292–23298 [View Article] [PubMed]
    [Google Scholar]
  153. Wu C, Lien Y, Bondage D, Lin J, Pilhofer M et al. Effector loading onto the VgrG carrier activates type VI secretion system assembly. EMBO Reports 2020; 21: [View Article]
    [Google Scholar]
  154. Tchelet D, Keppel K, Bosis E, Salomon D. Vibrio parahaemolyticus T6SS2 effector repertoires. Gut Microbes 2023; 15:2178795 [View Article] [PubMed]
    [Google Scholar]
  155. Lopez J, Ly PM, Feldman MF, Stephen Trent M. The tip of the VgrG spike is essential to functional type VI secretion system assembly in Acinetobacter baumannii. mBio 2020; 11:e02761-19 [View Article] [PubMed]
    [Google Scholar]
  156. Ruhe ZC, Low DA, Hayes CS. Polymorphic toxins and their immunity proteins: diversity, evolution, and mechanisms of delivery. Annu Rev Microbiol 2020; 74:497–520 [View Article] [PubMed]
    [Google Scholar]
  157. Speare L, Woo M, Dunn AK, Septer AN, Dubilier N. A putative lipoprotein mediates cell-cell contact for type VI secretion system-dependent killing of specific competitors. mBio 2022; 13: [View Article]
    [Google Scholar]
  158. Ting S-Y, Martínez-García E, Huang S, Bertolli SK, Kelly KA et al. Targeted depletion of bacteria from mixed populations by programmable adhesion with antagonistic competitor cells. Cell Host Microbe 2020; 28:313–321 [View Article]
    [Google Scholar]
  159. Wettstadt S, Filloux A. Manipulating the type VI secretion system spike to shuttle passenger proteins. PLoS One 2020; 15:e0228941 [View Article] [PubMed]
    [Google Scholar]
  160. 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]
    [Google Scholar]
  161. Durán D, Bernal P, Vazquez-Arias D, Blanco-Romero E, Garrido-Sanz D et al. Pseudomonas fluorescens F113 type VI secretion systems mediate bacterial killing and adaption to the rhizosphere microbiome. Sci Rep 2021; 11:5772 [View Article]
    [Google Scholar]
  162. Fridman CM, Keppel K, Gerlic M, Bosis E, Salomon D. A comparative genomics methodology reveals a widespread family of membrane-disrupting T6SS effectors. Nat Commun 2020; 11:1085 [View Article]
    [Google Scholar]
  163. Jana B, Keppel K, Fridman CM, Bosis E, Salomon D et al. Multiple T6SSs, mobile auxiliary modules, and effectors revealed in a systematic analysis of the Vibrio parahaemolyticus pan-genome. mSystems 2022; 7: [View Article]
    [Google Scholar]
  164. Geller AM, Zlotkin D, Levy A. Large-scale discovery of candidate type VI secretion effectors with antibacterial activity. Microbiology 2021; 2021 [View Article]
    [Google Scholar]
  165. Unterweger D, Miyata ST, Bachmann V, Brooks TM, Mullins T et al. The Vibrio cholerae type VI secretion system employs diverse effector modules for intraspecific competition. Nat Commun 2014; 5:3549 [View Article] [PubMed]
    [Google Scholar]
  166. Rigard M, Bröms JE, Mosnier A, Hologne M, Martin A et al. Francisella tularensis IglG belongs to a novel family of PAAR-like T6SS proteins and harbors a unique N-terminal extension required for virulence. PLoS Pathog 2016; 12:e1005821 [View Article]
    [Google Scholar]
  167. 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]
  168. Jana B, Fridman CM, Bosis E, Salomon D. A modular effector with a DNase domain and a marker for T6SS substrates. Nat Commun 2019; 10:3595 [View Article] [PubMed]
    [Google Scholar]
  169. Kanarek K, Fridman CM, Bosis E, Salomon D. A new class of polymorphic T6SS effectors and tethers. Microbiology 2022; 2022 [View Article]
    [Google Scholar]
  170. Allsopp LP, Collins ACZ, Hawkins E, Wood TE, Filloux A. RpoN/Sfa2-dependent activation of the Pseudomonas aeruginosa H2-T6SS and its cognate arsenal of antibacterial toxins. Nucleic Acids Res 2022; 50:227–243 [View Article] [PubMed]
    [Google Scholar]
  171. Vazquez-Lopez J, Navarro-Garcia F. In silico analyses of core proteins and putative effector and immunity proteins for T6SS in enterohemorrhagic E. coli. Front Cell Infect Microbiol 2020; 10:195 [View Article]
    [Google Scholar]
  172. Habich A, Galeev A, Vargas VC, Vogler O, Ghoul M et al. Core and accessory effectors of type VI secretion systems contribute differently to the intraspecific diversity of Pseudomonas aeruginosa. MicrobiologybioRxiv [View Article]
    [Google Scholar]
  173. 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]
  174. Gallique M, Decoin V, Barbey C, Rosay T, Feuilloley MGJ et al. Contribution of the Pseudomonas fluorescens MFE01 Type VI secretion system to biofilm formation. PLoS One 2017; 12:e0170770 [View Article] [PubMed]
    [Google Scholar]
  175. Decoin V, Barbey C, Bergeau D, Latour X, Feuilloley MGJ et al. A type VI secretion system is involved in Pseudomonas fluorescens bacterial competition. PLoS One 2014; 9:e89411 [View Article] [PubMed]
    [Google Scholar]
  176. Borrero de Acuña JM, Bernal P. Plant holobiont interactions mediated by the type VI secretion system and the membrane vesicles: promising tools for a greener agriculture. Environ Microbiol 2021; 23:1830–1836 [View Article] [PubMed]
    [Google Scholar]
  177. Bernal P, Civantos C, Pacheco-Sánchez D, Quesada JM, Filloux A et al. Transcriptional organization and regulation of the Pseudomonas putida K1 type VI secretion system gene cluster. Microbiology 2023; 169: [View Article]
    [Google Scholar]
  178. Bayer-Santos E, Lima LDP, Ceseti L de M, Ratagami CY, de Santana ES et al. Xanthomonas citri T6SS mediates resistance to Dictyostelium predation and is regulated by an ECF σ factor and cognate Ser/Thr kinase. Environ Microbiol 2018; 20:1562–1575 [View Article] [PubMed]
    [Google Scholar]
  179. Bernal P, Murillo-Torres M, Allsopp LP. Integrating signals to drive type VI secretion system killing. Environ Microbiol 2020; 22:4520–4523 [View Article] [PubMed]
    [Google Scholar]
  180. Jaskólska M, Stutzmann S, Stoudmann C, Blokesch M. QstR-dependent regulation of natural competence and type VI secretion in Vibrio cholerae. Nucleic Acids Res 2018; 46:10619–10634 [View Article] [PubMed]
    [Google Scholar]
  181. Alves JA, Leal FC, Previato-Mello M, da Silva Neto JF. A quorum sensing-regulated type VI secretion system containing multiple nonredundant VgrG proteins is required for interbacterial competition in Chromobacterium violaceum. Microbiol Spectr 2022; 10:e0157622 [View Article] [PubMed]
    [Google Scholar]
  182. Allsopp LP, Wood TE, Howard SA, Maggiorelli F, Nolan LM et al. RsmA and AmrZ orchestrate the assembly of all three type VI secretion systems in Pseudomonas aeruginosa. Proc Natl Acad Sci 2017; 114:7707–7712 [View Article] [PubMed]
    [Google Scholar]
  183. Lin L, Lezan E, Schmidt A, Basler M. Abundance of bacterial Type VI secretion system components measured by targeted proteomics. Nat Commun 2019; 10:2584 [View Article] [PubMed]
    [Google Scholar]
  184. Deng W, Marshall NC, Rowland JL, McCoy JM, Worrall LJ et al. Assembly, structure, function and regulation of type III secretion systems. Nat Rev Microbiol 2017; 15:323–337 [View Article] [PubMed]
    [Google Scholar]
  185. Wanford JJ, Hachani A, Odendall C. Reprogramming of cell death pathways by bacterial effectors as a widespread virulence strategy. Infect Immun 2022; 90:e0061421 [View Article] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001367
Loading
/content/journal/micro/10.1099/mic.0.001367
Loading

Data & Media loading...

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