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Volume 169, Issue 2

The type-VI secretion system of the beneficial symbiont Open Access

This article is part of the Environmental Sensing and Cell-Cell Communication collection

An Erratum has been published for this article.

Abstract

The mutualistic symbiosis between the Hawaiian bobtail squid and the marine bacterium is a powerful experimental system for determining how intercellular interactions impact animal–bacterial associations. In nature, this symbiosis features multiple strains of within each adult animal, which indicates that different strains initially colonize each squid. Various studies have demonstrated that certain strains of possess a type-VI secretion system (T6SS), which can inhibit other strains from establishing symbiosis within the same host habitat. The T6SS is a bacterial melee weapon that enables a cell to kill adjacent cells by translocating toxic effectors via a lancet-like apparatus. This review describes the progress that has been made in understanding the factors that govern the structure and expression of the T6SS in and its effect on the symbiosis.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Euprymna scolopes , microbial competition , symbiosis , type VI secretion system and Vibrio fischeri
Funding
This study was supported by the:
  • Division of Intramural Research, National Institute of Allergy and Infectious Diseases (Award F32 AI147543)
    • Principle Award Recipient: KirstenR. Guckes
  • National Institute of General Medical Sciences (Award R01 GM129133)
    • Principle Award Recipient: TimI. Miyashiro
© 2023 The Authors
  • 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.

Erratum

An erratum has been published for this content:
Erratum: The type-VI secretion system of the beneficial symbiont
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References

  1. 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]
  2. Fraune S, Bosch TCG. Why bacteria matter in animal development and evolution. Bioessays 2010; 32:571–580 [View Article] [PubMed]
     [Google Scholar]
  3. Sánchez-Cañizares C, Jorrín B, Poole PS, Tkacz A. Understanding the holobiont: the interdependence of plants and their microbiome. Curr Opin Microbiol 2017; 38:188–196 [View Article] [PubMed]
     [Google Scholar]
  4. Berger D, Rakhamimova A, Pollack A, Loewy Z. Oral biofilms: development, control, and analysis. High Throughput 2018; 7:24 [View Article]
     [Google Scholar]
  5. Byrd AL, Belkaid Y, Segre JA. The human skin microbiome. Nat Rev Microbiol 2018; 16:143–155 [View Article] [PubMed]
     [Google Scholar]
  6. Ghoul M, Mitri S. The ecology and evolution of microbial competition. Trends Microbiol 2016; 24:833–845 [View Article]
     [Google Scholar]
  7. Gonzalez D, Mavridou DAI. Making the best of aggression: the many dimensions of bacterial toxin regulation. Trends Microbiol 2019; 27:897–905 [View Article]
     [Google Scholar]
  8. Coyte KZ, Schluter J, Foster KR. The ecology of the microbiome: networks, competition, and stability. Science 2015; 350:663–666 [View Article]
     [Google Scholar]
  9. Mao J, Blanchard AE, Lu T. Slow and steady wins the race: a bacterial exploitative competition strategy in fluctuating environments. ACS Synth Biol 2015; 4:240–248 [View Article] [PubMed]
     [Google Scholar]
  10. Holdridge EM, Cuellar-Gempeler C, terHorst CP. A shift from exploitation to interference competition with increasing density affects population and community dynamics. Ecol Evol 2016; 6:5333–5341 [View Article]
     [Google Scholar]
  11. Hayes CS, Koskiniemi S, Ruhe ZC, Poole SJ, Low DA. Mechanisms and biological roles of contact-dependent growth inhibition systems. Cold Spring Harb Perspect Med 2014; 4:a010025 [View Article]
     [Google Scholar]
  12. Hassan M, Kjos M, Nes IF, Diep DB, Lotfipour F. Natural antimicrobial peptides from bacteria: characteristics and potential applications to fight against antibiotic resistance. J Appl Microbiol 2012; 113:723–736 [View Article]
     [Google Scholar]
  13. Heilbronner S, Krismer B, Brötz-Oesterhelt H, Peschel A. The microbiome-shaping roles of bacteriocins. Nat Rev Microbiol 2021; 19:726–739 [View Article]
     [Google Scholar]
  14. 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]
  15. 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]
  16. Wood TE, Howard SA, Förster A, Nolan LM, Manoli E et al. The Pseudomonas aeruginosa T6SS delivers a periplasmic toxin that disrupts bacterial cell morphology. Cell Rep 2019; 29:187–201 [View Article]
     [Google Scholar]
  17. Dudley EG, Thomson NR, Parkhill J, Morin NP, Nataro JP. Proteomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity island in enteroaggregative Escherichia coli. Mol Microbiol 2006; 61:1267–1282 [View Article] [PubMed]
     [Google Scholar]
  18. Douzi B, Spinelli S, Blangy S, Roussel A, Durand E et al. Crystal structure and self-interaction of the type VI secretion tail-tube protein from enteroaggregative Escherichia coli. PLoS One 2014; 9:e86918 [View Article]
     [Google Scholar]
  19. 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]
     [Google Scholar]
  20. 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]
     [Google Scholar]
  21. 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]
  22. Altindis E, Dong T, Catalano C, Mekalanos J. Secretome analysis of Vibrio cholerae type VI secretion system reveals a new effector-immunity pair. mBio 2015; 6:e00075 [View Article]
     [Google Scholar]
  23. 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]
  24. Lennings J, Makhlouf M, Olejnik P, Mayer C, Brötz-Oesterhelt H et al. Environmental and cellular factors affecting the localization of T6SS proteins in Burkholderia thailandensis. Int J Med Microbiol 2019; 309:151335 [View Article]
     [Google Scholar]
  25. Yadav SK, Magotra A, Ghosh S, Krishnan A, Pradhan A et al. Immunity proteins of dual nuclease T6SS effectors function as transcriptional repressors. EMBO Rep 2021; 22:e53112 [View Article]
     [Google Scholar]
  26. Nguyen TT, Lee HH, Park I, Seo YS. Genome-wide analysis of type VI system clusters and effectors in Burkholderia species. Plant Pathol J 2018; 34:11–22 [View Article]
     [Google Scholar]
  27. 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]
  28. Morgado S, Vicente AC. Diversity and distribution of type VI secretion system gene clusters in bacterial plasmids. Sci Rep 2022; 12:8249 [View Article]
     [Google Scholar]
  29. 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]
  30. Durand E, Zoued A, Spinelli S, Watson PJH, Aschtgen M-S et al. Structural characterization and oligomerization of the TssL protein, a component shared by bacterial type VI and type IVb secretion systems. J Biol Chem 2012; 287:14157–14168 [View Article] [PubMed]
     [Google Scholar]
  31. 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]
  32. 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]
     [Google Scholar]
  33. Zhang XY, Brunet YR, Logger L, Douzi B, Cambillau C et al. Dissection of the TssB-TssC interface during type VI secretion sheath complex formation. PLoS One 2013; 8:e81074 [View Article] [PubMed]
     [Google Scholar]
  34. Wettstadt S, Wood TE, Fecht S, Filloux A. Delivery of the Pseudomonas aeruginosa Phospholipase Effectors PldA and PldB in a VgrG- and H2-T6SS-Dependent Manner. Front Microbiol 2019; 10:1718 [View Article] [PubMed]
     [Google Scholar]
  35. 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]
     [Google Scholar]
  36. Cherrak Y, Flaugnatti N, Durand E, Journet L, Cascales E. Structure and activity of the Type VI secretion system. Microbiol Spectr 2019; 7: [View Article]
     [Google Scholar]
  37. 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]
  38. 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]
  39. 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]
  40. 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]
     [Google Scholar]
  41. 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]
  42. 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]
     [Google Scholar]
  43. Jurėnas D, Journet L. Activity, delivery, and diversity of Type VI secretion effectors. Mol Microbiol 2021; 115:383–394 [View Article] [PubMed]
     [Google Scholar]
  44. 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]
     [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. English G, Trunk K, Rao VA, Srikannathasan V, Hunter WN et al. New secreted toxins and immunity proteins encoded within the Type VI secretion system gene cluster of Serratia marcescens. Mol Microbiol 2012; 86:921–936 [View Article] [PubMed]
     [Google Scholar]
  47. 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]
  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. 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]
     [Google Scholar]
  50. 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]
     [Google Scholar]
  51. Ma AT, Mekalanos JJ. In vivo actin cross-linking induced by Vibrio cholerae type VI secretion system is associated with intestinal inflammation. Proc Natl Acad Sci 2010; 107:4365–4370 [View Article]
     [Google Scholar]
  52. Gerlach RG, Hensel M. Protein secretion systems and adhesins: the molecular armory of Gram-negative pathogens. Int J Med Microbiol 2007; 297:401–415 [View Article] [PubMed]
     [Google Scholar]
  53. 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]
  54. 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]
  55. 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]
     [Google Scholar]
  56. 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]
     [Google Scholar]
  57. 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]
     [Google Scholar]
  58. Nyholm SV, McFall-Ngai MJ. A lasting symbiosis: how the Hawaiian bobtail squid finds and keeps its bioluminescent bacterial partner. Nat Rev Microbiol 2021; 19:666–679 [View Article] [PubMed]
     [Google Scholar]
  59. Visick KL, Stabb EV, Ruby EG. A lasting symbiosis: how Vibrio fischeri finds a squid partner and persists within its natural host. Nat Rev Microbiol 2021; 19:654–665 [View Article]
     [Google Scholar]
  60. Jones BW, Nishiguchi MK. Counterillumination in the Hawaiian bobtail squid, Euprymna scolopes Berry (Mollusca: Cephalopoda). Marine Biology 2004; 144:1151–1155 [View Article]
     [Google Scholar]
  61. Verma SC, Miyashiro T. Quorum sensing in the squid-Vibrio symbiosis. Int J Mol Sci 2013; 14:16386–16401 [View Article]
     [Google Scholar]
  62. Boettcher KJ, Ruby EG, McFall-Ngai MJ. Bioluminescence in the symbiotic squid Euprymna scolopes is controlled by a daily biological rhythm. J Comp Physiol A 1996; 179:65–73 [View Article]
     [Google Scholar]
  63. Nyholm SV, McFall-Ngai MJ. Sampling the light-organ microenvironment of Euprymna scolopes: description of a population of host cells in association with the bacterial symbiont Vibrio fischeri. Biol Bull 1998; 195:89–97 [View Article]
     [Google Scholar]
  64. Nyholm SV, McFall-Ngai MJ. The winnowing: establishing the squid-vibrio symbiosis. Nat Rev Microbiol 2004; 2:632–642 [View Article] [PubMed]
     [Google Scholar]
  65. McFall-Ngai MJ, Ruby EG. Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterial mutualism. Science 1991; 254:1491–1494 [View Article]
     [Google Scholar]
  66. Wollenberg MS, Ruby EG. Population structure of Vibrio fischeri within the light organs of Euprymna scolopes squid from two Oahu (Hawaii) populations. Appl Environ Microbiol 2009; 75:193–202 [View Article]
     [Google Scholar]
  67. Nyholm SV, Stabb EV, Ruby EG, McFall-Ngai MJ. Establishment of an animal–bacterial association: recruiting symbiotic vibrios from the environment. Proc Natl Acad Sci 2000; 97:10231–10235 [View Article]
     [Google Scholar]
  68. Kremer N, Philipp EER, Carpentier M-C, Brennan CA, Kraemer L et al. Initial symbiont contact orchestrates host-organ-wide transcriptional changes that prime tissue colonization. Cell Host & Microbe 2013; 14:183–194 [View Article]
     [Google Scholar]
  69. McFall-Ngai MJ, Ruby EG. Sepiolids and vibrios: when first they meet: reciprocal interactions between host and symbiont lead to the creation of a complex light-emitting organ. BioScience 1998; 48:257–265
     [Google Scholar]
  70. Essock-Burns T, Bongrand C, Goldman WE, Ruby EG, McFall-Ngai MJ. Interactions of symbiotic partners drive the development of a complex biogeography in the squid-Vibrio symbiosis. mBio 2020; 11:e00853-20 [View Article]
     [Google Scholar]
  71. Graf J, Ruby EG. Host-derived amino acids support the proliferation of symbiotic bacteria. Proc Natl Acad Sci 1998; 95:1818–1822 [View Article]
     [Google Scholar]
  72. Schwartzman JA, Koch E, Heath-Heckman EAC, Zhou L, Kremer N et al. The chemistry of negotiation: rhythmic, glycan-driven acidification in a symbiotic conversation. Proc Natl Acad Sci 2015; 112:566–571 [View Article]
     [Google Scholar]
  73. Wasilko NP, Larios-Valencia J, Steingard CH, Nunez BM, Verma SC et al. Sulfur availability for Vibrio fischeri growth during symbiosis establishment depends on biogeography within the squid light organ. Mol Microbiol 2019; 111:621–636 [View Article]
     [Google Scholar]
  74. Yount TA, Murtha AN, Cecere AG, Miyashiro TI. Quorum sensing facilitates interpopulation signaling by Vibrio fischeri within the light organ of Euprymna scolopes. Isr J Chemist 2022 [View Article]
     [Google Scholar]
  75. Bongrand C, Ruby EG. Achieving a multi-strain symbiosis: strain behavior and infection dynamics. ISME J 2019; 13:698–706 [View Article] [PubMed]
     [Google Scholar]
  76. Sun Y, LaSota ED, Cecere AG, LaPenna KB, Larios-Valencia J et al. Intraspecific competition impacts Vibrio fischeri strain diversity during initial colonization of the squid light organ. Appl Environ Microbiol 2016; 82:3082–3091 [View Article]
     [Google Scholar]
  77. Guckes KR, Cecere AG, Wasilko NP, Williams AL, Bultman KM et al. Incompatibility of Vibrio fischeri strains during symbiosis establishment depends on two functionally redundant hcp genes. J Bacteriol 2019; 201:e00221-19 [View Article]
     [Google Scholar]
  78. Guckes KR, Cecere AG, Williams AL, McNeil AE, Miyashiro T. The bacterial enhancer binding protein VasH promotes expression of a type VI secretion system in Vibrio fischeri during symbiosis. J Bacteriol 2020; 202:e00777-19 [View Article]
     [Google Scholar]
  79. 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:E8528–E8537 [View Article]
     [Google Scholar]
  80. Bultman KM, Cecere AG, Miyashiro T, Septer AN, Mandel MJ. Draft genome sequences of type VI secretion system-encoding Vibrio fischeri strains FQ-A001 and ES401. Microbiol Resour Announc 2019; 8:e00385-19 [View Article]
     [Google Scholar]
  81. Sayers EW, Bolton EE, Brister JR, Canese K, Chan J et al. Database resources of the national center for biotechnology information. Nucleic Acids Res 2022; 50:D20–D26 [View Article] [PubMed]
     [Google Scholar]
  82. Suria AM, Smith S, Speare L, Chen Y, Chien I et al. Prevalence and diversity of type VI secretion systems in a model beneficial symbiosis. Front Microbiol 2022; 13:988044 [View Article]
     [Google Scholar]
  83. Speare L, Septer AN. Coincubation assay for quantifying competitive interactions between Vibrio fischeri isolates. J Vis Exp 2019149 [View Article]
     [Google Scholar]
  84. Speare L, Smith S, Salvato F, Kleiner M, Septer AN. Environmental viscosity modulates interbacterial killing during habitat transition. mBio 2020; 11:e03060-19 [View Article]
     [Google Scholar]
  85. Speare L, Woo M, Bultman KM, Mandel MJ, Wollenberg MS et al. Host-like conditions are required for T6SS-mediated competition among Vibrio fischeri light organ symbionts. mSphere 2021; 6:e0128820 [View Article]
     [Google Scholar]
  86. Speare L, Woo M, Dunn AK, Septer AN. A putative lipoprotein mediates cell-cell contact for type VI secretion system-dependent killing of specific competitors. mBio 2022; 13:e0308521 [View Article]
     [Google Scholar]
  87. Thompson LR, Nikolakakis K, Pan S, Reed J, Knight R et al. Transcriptional characterization of Vibrio fischeri during colonization of juvenile Euprymna scolopes. Environ Microbiol 2017; 19:1845–1856 [View Article] [PubMed]
     [Google Scholar]
  88. 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]
     [Google Scholar]
  89. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 2015; 10:845–858 [View Article] [PubMed]
     [Google Scholar]
  90. 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]
     [Google Scholar]
  91. Huang Y, Du P, Zhao M, Liu W, Du Y et al. Functional characterization and conditional regulation of the type VI secretion system in Vibrio fluvialis. Front Microbiol 2017; 8:528 [View Article]
     [Google Scholar]
  92. 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]
  93. 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]
  94. Smith S, Salvato F, Garikipati A, Kleiner M, Septer AN. Activation of the type VI secretion system in the squid symbiont Vibrio fischeri requires the transcriptional regulator TasR and the structural proteins TssM and TssA. J Bacteriol 2021; 203:e0039921 [View Article]
     [Google Scholar]
  95. Ma LS, Narberhaus F, Lai EM. IcmF family protein TssM exhibits ATPase activity and energizes type VI secretion. J Biol Chem 2012; 287:15610–15621 [View Article] [PubMed]
     [Google Scholar]
  96. Zheng J, Leung KY. Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol 2007; 66:1192–1206 [View Article] [PubMed]
     [Google Scholar]
  97. 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]
  98. 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]
     [Google Scholar]
  99. Bourne HR, Sanders DA, McCormick F. The GTPase superfamily: conserved structure and molecular mechanism. Nature 1991; 349:117–127 [View Article] [PubMed]
     [Google Scholar]
  100. Speare L, Jackson A, Septer AN. Calcium promotes T6SS-mediated killing and aggregation between competing symbionts. Microbiol Spectr 2022; 10:e0139722 [View Article]
     [Google Scholar]
  101. Hara T, Matsuyama S, Tokuda H. Mechanism underlying the inner membrane retention of Escherichia coli lipoproteins caused by Lol avoidance signals. J Biol Chem 2003; 278:40408–40414 [View Article] [PubMed]
     [Google Scholar]
  102. Konovalova A, Silhavy TJ. Outer membrane lipoprotein biogenesis: Lol is not the end. Phil Trans R Soc B 2015; 370:20150030 [View Article]
     [Google Scholar]
  103. Miura S, Kamiya S, Saito Y, Wada S, Hayashi R et al. Antiadhesive sites present in the fibronectin type III-like repeats of human plasma fibronectin. Biol Pharm Bull 2007; 30:891–897 [View Article] [PubMed]
     [Google Scholar]
  104. Dial CN, Speare L, Sharpe GC, Gifford SM, Septer AN et al. Para-aminobenzoic acid, calcium, and c-di-GMP induce formation of cohesive, syp-polysaccharide-dependent biofilms in Vibrio fischeri. mBio 2021; 12:e0203421 [View Article]
     [Google Scholar]
  105. Tischler AH, Lie L, Thompson CM, Visick KL. Discovery of calcium as a biofilm-promoting signal for Vibrio fischeri reveals new phenotypes and underlying regulatory complexity. J Bacteriol 2018; 200:15 [View Article]
     [Google Scholar]
  106. Millero FJ. 8.1 - Physico-chemical controls on Seawater. In Holland HD, Turekian KK. eds Treatise on Geochemistry, Second. Oxford: Elsevier; 2014 pp 1–18
     [Google Scholar]
  107. Wolfe AJ, Millikan DS, Campbell JM, Visick KL. Vibrio fischeri sigma54 controls motility, biofilm formation, luminescence, and colonization. Appl Environ Microbiol 2004; 70:2520–2524 [View Article] [PubMed]
     [Google Scholar]
  108. Seibt H, Aung KM, Ishikawa T, Sjöström A, Gullberg M et al. Elevated levels of VCA0117 (VasH) in response to external signals activate the type VI secretion system of Vibrio cholerae O1 El Tor A1552. Environ Microbiol 2020; 22:4409–4423 [View Article] [PubMed]
     [Google Scholar]
  109. 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]
  110. Manera K, Caro F, Li H, Pei T-T, Hersch SJ et al. Sensing of intracellular Hcp levels controls T6SS expression in Vibrio cholerae. Proc Natl Acad Sci 2021; 118:e2104813118 [View Article]
     [Google Scholar]
  111. Bush M, Dixon R. The role of bacterial enhancer binding proteins as specialized activators of σ54-dependent transcription. Microbiol Mol Biol Rev 2012; 76:497–529 [View Article] [PubMed]
     [Google Scholar]
  112. 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]
  113. Aravind L, Ponting CP. The GAF domain: an evolutionary link between diverse phototransducing proteins. Trends Biochem Sci 1997; 22:458–459 [View Article] [PubMed]
     [Google Scholar]
  114. Kitaoka M, Miyata ST, Brooks TM, Unterweger D, Pukatzki S. VasH is a transcriptional regulator of the type VI secretion system functional in endemic and pandemic Vibrio cholerae. J Bacteriol 2011; 193:6471–6482 [View Article]
     [Google Scholar]
  115. Ettema TJG, Brinkman AB, Tani TH, Rafferty JB, Van Der Oost J. A novel ligand-binding domain involved in regulation of amino acid metabolism in prokaryotes. J Biol Chem 2002; 277:37464–37468 [View Article] [PubMed]
     [Google Scholar]
  116. de los Rios S, Perona JJ. Structure of the Escherichia coli leucine-responsive regulatory protein Lrp reveals a novel octameric assembly. J Mol Biol 2007; 366:1589–1602 [View Article] [PubMed]
     [Google Scholar]
  117. Yu Y, Zhang Y, Li J, Yang H, Song H et al. VPA1045 and VPA1049 of Vibrio parahaemolyticus regulate translocation of Hcp2. Wei Sheng Wu Xue Bao 2012; 52:954–961 [PubMed]
     [Google Scholar]
  118. Salomon D, Gonzalez H, Updegraff BL, Orth K. Vibrio parahaemolyticus type VI secretion system 1 is activated in marine conditions to target bacteria, and is differentially regulated from system 2. PLoS One 2013; 8:e61086 [View Article]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001302
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The type-VI secretion system of the beneficial symbiont Vibrio fischeri
Microbiology 169, 001302 (2023); https://doi.org/10.1099/mic.0.001302
/content/journal/micro/10.1099/mic.0.001302
/content/journal/micro/10.1099/mic.0.001302
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