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Abstract

Bacteria live in complex polymicrobial communities and are constantly competing for resources. The type VI secretion system (T6SS) is a widespread antagonistic mechanism used by Gram-negative bacteria to gain an advantage over competitors. T6SSs translocate toxic effector proteins inside target prokaryotic cells in a contact-dependent manner. In addition, some T6SS effectors can be secreted extracellularly and contribute to the scavenging scarce metal ions. Bacteria deploy their T6SSs in different situations, categorizing these systems into offensive, defensive and exploitative. The great variety of bacterial species and environments occupied by such species reflect the complexity of regulatory signals and networks that control the expression and activation of the T6SSs. Such regulation is tightly controlled at the transcriptional, posttranscriptional and posttranslational level by abiotic (e.g. pH, iron) or biotic (e.g. quorum-sensing) cues. In this review, we provide an update on the current knowledge about the regulatory networks that modulate the expression and activity of T6SSs across several species, focusing on systems used for interbacterial competition.

Funding
This study was supported by the:
  • Fundação de Amparo à Pesquisa do Estado de São Paulo (Award 2017/02178-2)
    • Principle Award Recipient: EthelBayer-Santos
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. The Microbiology Society waived the open access fees for this article.
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2023-08-08
2024-06-16
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References

  1. Peterson SB, Bertolli SK, Mougous JD. The central role of interbacterial antagonism in bacterial life. Curr Biol 2020; 30:R1203–R1214 [View Article] [PubMed]
    [Google Scholar]
  2. Coulthurst S. The type VI secretion system: a versatile bacterial weapon. Microbiology 2019; 165:503–515 [View Article] [PubMed]
    [Google Scholar]
  3. 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; 10:1–14 [View Article] [PubMed]
    [Google Scholar]
  4. 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]
  5. Kierek-Pearson K, Karatan E. Biofilm development in bacteria. Adv Appl Microbiol 2005; 57:79–111 [View Article] [PubMed]
    [Google Scholar]
  6. 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 U S A 2009; 106:4154–4159 [View Article] [PubMed]
    [Google Scholar]
  7. 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]
  8. 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]
  9. 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]
  10. 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]
  11. 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]
  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] [PubMed]
    [Google Scholar]
  13. 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] [PubMed]
    [Google Scholar]
  14. 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]
  15. 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]
  16. 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]
  17. 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] [PubMed]
    [Google Scholar]
  18. 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]
  19. Jana B, Salomon D. Type VI secretion system: a modular toolkit for bacterial dominance. Future Microbiol 2019; 14:1451–1463 [View Article] [PubMed]
    [Google Scholar]
  20. Jurėnas D, Journet L. Activity, delivery, and diversity of type VI secretion effectors. Mol Microbiol 2021; 115:383–394 [View Article] [PubMed]
    [Google Scholar]
  21. 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]
  22. 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]
  23. Monjarás Feria J, Valvano MA. An overview of anti-eukaryotic T6SS effectors. Front Cell Infect Microbiol 2020; 10:584751 [View Article] [PubMed]
    [Google Scholar]
  24. 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] [PubMed]
    [Google Scholar]
  25. Blondel CJ, Jiménez JC, Contreras I, Santiviago CA. Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genomics 2009; 10:1–17 [View Article] [PubMed]
    [Google Scholar]
  26. Miyata ST, Kitaoka M, Wieteska L, Frech C, Chen N et al. The Vibrio cholerae type VI secretion system: evaluating its role in the human disease cholera. Front Microbiol 2010; 1:117 [View Article] [PubMed]
    [Google Scholar]
  27. 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]
  28. 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]
  29. 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]
  30. 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]
  31. 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]
  32. Stubbendieck RM, Straight PD. Multifaceted interfaces of bacterial competition. J Bacteriol 2016; 198:2145–2155 [View Article] [PubMed]
    [Google Scholar]
  33. 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]
  34. Basler M, Mekalanos JJ. Type 6 secretion dynamics within and between bacterial cells. Science 2012; 337:815 [View Article] [PubMed]
    [Google Scholar]
  35. Stolle A-S, Meader BT, Toska J, Mekalanos JJ. Endogenous membrane stress induces T6SS activity in Pseudomonas aeruginosa. Proc Natl Acad Sci 2021; 118:e2018365118 [View Article] [PubMed]
    [Google Scholar]
  36. Kamal F, Liang X, Manera K, Pei T-T, Kim H et al. Differential cellular response to translocated toxic effectors and physical penetration by the type VI secretion system. Cell Rep 2020; 31:107766 [View Article] [PubMed]
    [Google Scholar]
  37. Ho BT, Basler M, Mekalanos JJ. Type 6 secretion system-mediated immunity to type 4 secretion system-mediated gene transfer. Science 2013; 342:250–253 [View Article] [PubMed]
    [Google Scholar]
  38. Wilton M, Wong MJQ, Tang L, Liang X, Moore R et al. Chelation of membrane-bound cations by extracellular DNA activates the type VI secretion system in Pseudomonas aeruginosa. Infect Immun 2016; 84:2355–2361 [View Article] [PubMed]
    [Google Scholar]
  39. Qin S, Xiao W, Zhou C, Pu Q, Deng X et al. Pseudomonas aeruginosa: pathogenesis, virulence factors, antibiotic resistance, interaction with host, technology advances and emerging therapeutics. Signal Transduct Target Ther 2022; 7:199 [View Article] [PubMed]
    [Google Scholar]
  40. Sana TG, Berni B, Bleves S. The T6SSs of Pseudomonas aeruginosa strain PAO1 and their effectors: beyond bacterial-cell targeting. Front Cell Infect Microbiol 2016; 6:61 [View Article] [PubMed]
    [Google Scholar]
  41. Majerczyk C, Schneider E, Greenberg EP. Quorum sensing control of Type VI secretion factors restricts the proliferation of quorum-sensing mutants. Elife 2016; 5:e14712 [View Article] [PubMed]
    [Google Scholar]
  42. Bernard CS, Brunet YR, Gueguen E, Cascales E. Nooks and crannies in type VI secretion regulation. J Bacteriol 2010; 192:3850–3860 [View Article] [PubMed]
    [Google Scholar]
  43. 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]
  44. Ishikawa T, Sabharwal D, Bröms J, Milton DL, Sjöstedt A et al. Pathoadaptive conditional regulation of the type VI secretion system in vibrio cholerae O1 strains. Infect Immun 2012; 80:575–584 [View Article] [PubMed]
    [Google Scholar]
  45. Townsley L, Sison Mangus MP, Mehic S, Yildiz FH. Response of vibrio cholerae to low-temperature shifts: CspV regulation of type VI secretion, biofilm formation, and association with zooplankton. Appl Environ Microbiol 2016; 82:4441–4452 [View Article] [PubMed]
    [Google Scholar]
  46. Joshi A, Kostiuk B, Rogers A, Teschler J, Pukatzki S et al. Rules of engagement: the type VI secretion system in Vibrio cholerae. Trends Microbiol 2017; 25:267–279 [View Article] [PubMed]
    [Google Scholar]
  47. Ben-Yaakov R, Salomon D. The regulatory network of Vibrio parahaemolyticus type VI secretion system 1. Environ Microbiol 2019; 21:2248–2260 [View Article] [PubMed]
    [Google Scholar]
  48. 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] [PubMed]
    [Google Scholar]
  49. Nie H, Xiao Y, Song M, Wu N, Peng Q et al. Wsp system oppositely modulates antibacterial activity and biofilm formation via FleQ-FleN complex in Pseudomonas putida. Environ Microbiol 2022; 24:1543–1559 [View Article] [PubMed]
    [Google Scholar]
  50. 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] [PubMed]
    [Google Scholar]
  51. 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]
  52. Wu C-F, Lin J-S, Shaw G-C, Lai E-M. Acid-induced type VI secretion system is regulated by ExoR-ChvG/ChvI signaling cascade in Agrobacterium tumefaciens. PLoS Pathog 2012; 8:e1002938 [View Article] [PubMed]
    [Google Scholar]
  53. Körner H, Sofia HJ, Zumft WG. Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: exploiting the metabolic spectrum by controlling alternative gene programs. FEMS Microbiol Rev 2003; 27:559–592 [View Article] [PubMed]
    [Google Scholar]
  54. Yoon SS, Karabulut AC, Lipscomb JD, Hennigan RF, Lymar SV et al. Two-pronged survival strategy for the major cystic fibrosis pathogen, Pseudomonas aeruginosa, lacking the capacity to degrade nitric oxide during anaerobic respiration. EMBO J 2007; 26:3662–3672 [View Article] [PubMed]
    [Google Scholar]
  55. Wang T, Du X, Ji L, Han Y, Dang J et al. Pseudomonas aeruginosa T6SS-mediated molybdate transport contributes to bacterial competition during anaerobiosis. Cell Rep 2021; 35:108957 [View Article] [PubMed]
    [Google Scholar]
  56. Dang J, Wang T, Wen J, Liang H. An important role of the type VI secretion system of Pseudomonas aeruginosa regulated by dnr in response to anaerobic environments. Microbiol Spectr 2022; 10:e0153322 [View Article] [PubMed]
    [Google Scholar]
  57. Pomposiello PJ, Demple B. Redox-operated genetic switches: the SoxR and OxyR transcription factors. Trends Biotechnol 2001; 19:109–114 [View Article] [PubMed]
    [Google Scholar]
  58. Troxell B, Hassan HM. Transcriptional regulation by Ferric Uptake Regulator (Fur) in pathogenic bacteria. Front Cell Infect Microbiol 2013; 3:59 [View Article] [PubMed]
    [Google Scholar]
  59. Wang S, Yang D, Wu X, Yi Z, Wang Y et al. The ferric uptake regulator represses type VI secretion system function by binding directly to the clpV promoter in Salmonella enterica serovar Typhimurium. Infect Immun 2019; 87:e00562-19 [View Article] [PubMed]
    [Google Scholar]
  60. Chakraborty S, Sivaraman J, Leung KY, Mok Y-K. Two-component PhoB-PhoR regulatory system and ferric uptake regulator sense phosphate and iron to control virulence genes in type III and VI secretion systems of Edwardsiella tarda. J Biol Chem 2011; 286:39417–39430 [View Article] [PubMed]
    [Google Scholar]
  61. Brunet YR, Bernard CS, Gavioli M, Lloubès R, Cascales E. An epigenetic switch involving overlapping fur and DNA methylation optimizes expression of a type VI secretion gene cluster. PLoS Genet 2011; 7:e1002205 [View Article] [PubMed]
    [Google Scholar]
  62. Brunet YR, Bernard CS, Cascales E. Fur-Dam regulatory interplay at an internal promoter of the enteroaggregative Escherichia coli type VI secretion sci1 gene cluster. J Bacteriol 2020; 202:e00075-20 [View Article] [PubMed]
    [Google Scholar]
  63. Ma J, Sun M, Pan Z, Song W, Lu C et al. Three Hcp homologs with divergent extended loop regions exhibit different functions in avian pathogenic Escherichia coli. Emerg Microbes Infect 2018; 7:1–13 [View Article] [PubMed]
    [Google Scholar]
  64. Sana TG, Hachani A, Bucior I, Soscia C, Garvis S et al. The second type VI secretion system of Pseudomonas aeruginosa strain PAO1 is regulated by quorum sensing and Fur and modulates internalization in epithelial cells. J Biol Chem 2012; 287:27095–27105 [View Article] [PubMed]
    [Google Scholar]
  65. Zhao X, Xu C, Qu J, Jin Y, Bai F et al. PitA controls the H2- and H3-T6SSs through PhoB in Pseudomonas aeruginosa. Appl Environ Microbiol 2023; 89:e0209422 [View Article] [PubMed]
    [Google Scholar]
  66. 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]
  67. Fu Y, Waldor MK, Mekalanos JJ. Tn-Seq analysis of Vibrio cholerae intestinal colonization reveals a role for T6SS-mediated antibacterial activity in the host. Cell Host Microbe 2013; 14:652–663 [View Article] [PubMed]
    [Google Scholar]
  68. 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–E5051 [View Article] [PubMed]
    [Google Scholar]
  69. 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]
  70. Bachmann V, Kostiuk B, Unterweger D, Diaz-Satizabal L, Ogg S et al. Bile salts modulate the mucin-activated type VI secretion system of pandemic Vibrio cholerae. PLoS Negl Trop Dis 2015; 9:e0004031 [View Article] [PubMed]
    [Google Scholar]
  71. 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]
  72. Winzer K, Williams P. Quorum sensing and the regulation of virulence gene expression in pathogenic bacteria. Int J Med Microbiol 2001; 291:131–143 [View Article] [PubMed]
    [Google Scholar]
  73. Zhang Y, Gao H, Osei-Adjei G, Zhang Y, Yang W et al. Transcriptional regulation of the type VI secretion system 1 genes by quorum sensing and ToxR in Vibrio parahaemolyticus. Front Microbiol 2017; 8:2005 [View Article] [PubMed]
    [Google Scholar]
  74. Zheng J, Shin OS, Cameron DE, Mekalanos JJ. Quorum sensing and a global regulator TsrA control expression of type VI secretion and virulence in Vibrio cholerae. Proc Natl Acad Sci 2010; 107:21128–21133 [View Article] [PubMed]
    [Google Scholar]
  75. Gao X, Wang X, Mao Q, Xu R, Zhou X et al. VqsA, a novel LysR-type transcriptional regulator, coordinates Quorum Sensing (QS) and is controlled by QS to regulate virulence in the pathogen Vibrio alginolyticus. Appl Environ Microbiol 2018; 84:e00444-18 [View Article] [PubMed]
    [Google Scholar]
  76. Khajanchi BK, Sha J, Kozlova EV, Erova TE, Suarez G et al. N-acylhomoserine lactones involved in quorum sensing control the type VI secretion system, biofilm formation, protease production, and in vivo virulence in a clinical isolate of Aeromonas hydrophila. Microbiology 2009; 155:3518–3531 [View Article] [PubMed]
    [Google Scholar]
  77. 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]
  78. Sabag-Daigle A, Dyszel JL, Gonzalez JF, Ali MM, Ahmer BMM. Identification of sdiA-regulated genes in a mouse commensal strain of Enterobacter cloacae. Front Cell Infect Microbiol 2015; 5:47 [View Article] [PubMed]
    [Google Scholar]
  79. Lesic B, Starkey M, He J, Hazan R, Rahme LG. Quorum sensing differentially regulates Pseudomonas aeruginosa type VI secretion locus I and homologous loci II and III, which are required for pathogenesis. Microbiology 2009; 155:2845–2855 [View Article] [PubMed]
    [Google Scholar]
  80. Hu L, Yu F, Liu M, Chen J, Zong B et al. RcsB-dependent regulation of type VI secretion system in porcine extra-intestinal pathogenic Escherichia coli. Gene 2021; 768:145289 [View Article] [PubMed]
    [Google Scholar]
  81. Jones C, Allsopp L, Horlick J, Kulasekara H, Filloux A. Subinhibitory concentration of kanamycin induces the Pseudomonas aeruginosa type VI secretion system. PLoS One 2013; 8:e81132 [View Article] [PubMed]
    [Google Scholar]
  82. Linares JF, Gustafsson I, Baquero F, Martinez JL. Antibiotics as intermicrobial signaling agents instead of weapons. Proc Natl Acad Sci 2006; 103:19484–19489 [View Article] [PubMed]
    [Google Scholar]
  83. Gao R, Mack TR, Stock AM. Bacterial response regulators: versatile regulatory strategies from common domains. Trends Biochem Sci 2007; 32:225–234 [View Article] [PubMed]
    [Google Scholar]
  84. Guo X-P, Sun Y-C. New insights into the non-orthodox two component Rcs phosphorelay System. Front Microbiol 2017; 8:2014 [View Article] [PubMed]
    [Google Scholar]
  85. Wösten M. Eubacterial sigma-factors. FEMS Microbiol Rev 1998; 22:127–150 [View Article] [PubMed]
    [Google Scholar]
  86. Bervoets I, Charlier D. Diversity, versatility and complexity of bacterial gene regulation mechanisms: opportunities and drawbacks for applications in synthetic biology. FEMS Microbiol Rev 2019; 43:304–339 [View Article] [PubMed]
    [Google Scholar]
  87. Axelrod R, Hamilton WD. The evolution of cooperation. Science 1981; 211:1390–1396 [View Article] [PubMed]
    [Google Scholar]
  88. 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]
  89. 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; 169:001295 [View Article] [PubMed]
    [Google Scholar]
  90. Records AR, Gross DC. Sensor kinases RetS and LadS regulate Pseudomonas syringae type VI secretion and virulence factors. J Bacteriol 2010; 192:3584–3596 [View Article] [PubMed]
    [Google Scholar]
  91. Zhou T, Huang J, Liu Z, Lin Q, Xu Z et al. The two-component system FleS/FleR represses H1-T6SS via cyclic di-GMP signaling in Pseudomonas aeruginosa. Appl Environ Microbiol 2022; 88:e0165521 [View Article] [PubMed]
    [Google Scholar]
  92. Xu B, Ju Y, Soukup RJ, Ramsey DM, Fishel R et al. The Pseudomonas aeruginosa AmrZ C-terminal domain mediates tetramerization and is required for its activator and repressor functions. Environ Microbiol Rep 2016; 8:85–90 [View Article] [PubMed]
    [Google Scholar]
  93. Francis VI, Stevenson EC, Porter SL. Two-component systems required for virulence in Pseudomonas aeruginosa. FEMS Microbiol Lett 2017; 364:fnx104 [View Article] [PubMed]
    [Google Scholar]
  94. McCarthy RR, Yu M, Eilers K, Wang Y-C, Lai E-M et al. Cyclic di-GMP inactivates T6SS and T4SS activity in Agrobacterium tumefaciens. Mol Microbiol 2019; 112:632–648 [View Article] [PubMed]
    [Google Scholar]
  95. Yuan Z-C, Liu P, Saenkham P, Kerr K, Nester EW. Transcriptome profiling and functional analysis of Agrobacterium tumefaciens reveals a general conserved response to acidic conditions (pH 5.5) and a complex acid-mediated signaling involved in agrobacterium-plant interactions. J Bacteriol 2008; 190:494–507 [View Article] [PubMed]
    [Google Scholar]
  96. McCarthy RR, Yu M, Eilers K, Wang Y-C, Lai E-M et al. Cyclic di-GMP inactivates T6SS and T4SS activity in Agrobacterium tumefaciens. Mol Microbiol 2019; 112:632–648 [View Article] [PubMed]
    [Google Scholar]
  97. Waldburger CD, Sauer RT. Signal detection by the PhoQ sensor-transmitter. characterization of the sensor domain and a response-impaired mutant that identifies ligand-binding determinants. J Biol Chem 1996; 271:26630–26636 [View Article] [PubMed]
    [Google Scholar]
  98. Aubert DF, Flannagan RS, Valvano MA. A novel sensor kinase-response regulator hybrid controls biofilm formation and type VI secretion system activity in Burkholderia cenocepacia. Infect Immun 2008; 76:1979–1991 [View Article] [PubMed]
    [Google Scholar]
  99. Spiewak HL, Shastri S, Zhang L, Schwager S, Eberl L et al. Burkholderia cenocepacia utilizes a type VI secretion system for bacterial competition. Microbiologyopen 2019; 8:e00774 [View Article] [PubMed]
    [Google Scholar]
  100. Teschler JK, Jiménez-Siebert E, Jeckel H, Singh PK, Park JH et al. VxrB influences antagonism within biofilms by controlling competition through extracellular matrix production and type 6 secretion. mBio 2022; 13:e0188522 [View Article] [PubMed]
    [Google Scholar]
  101. Cheng AT, Ottemann KM, Yildiz FH, Baumler AJ. Vibrio cholerae response regulator VxrB controls Colonization and regulates the type VI secretion system. PLoS Pathog 2015; 11:e1004933 [View Article] [PubMed]
    [Google Scholar]
  102. Meibom KL, Li XB, Nielsen AT, Wu C-Y, Roseman S et al. The Vibrio cholerae chitin utilization program. Proc Natl Acad Sci 2004; 101:2524–2529 [View Article] [PubMed]
    [Google Scholar]
  103. Li X, Roseman S. The chitinolytic cascade in Vibrios is regulated by chitin oligosaccharides and a two-component chitin catabolic sensor/kinase. Proc Natl Acad Sci U S A 2004; 101:627–631 [View Article] [PubMed]
    [Google Scholar]
  104. Dalia AB, Lazinski DW, Camilli A, Taylor R. Identification of a membrane-bound transcriptional regulator that links chitin and natural competence in Vibrio cholerae. mBio 2014; 5:e01028-13 [View Article] [PubMed]
    [Google Scholar]
  105. 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]
  106. Meibom KL, Blokesch M, Dolganov NA, Wu C-Y, Schoolnik GK. Chitin induces natural competence in Vibrio cholerae. Science 2005; 310:1824–1827 [View Article] [PubMed]
    [Google Scholar]
  107. Majdalani N, Gottesman S. The Rcs phosphorelay: a complex signal transduction system. Annu Rev Microbiol 2005; 59:379–405 [View Article] [PubMed]
    [Google Scholar]
  108. Wall E, Majdalani N, Gottesman S. The complex Rcs regulatory cascade. Annu Rev Microbiol 2018; 72:111–139 [View Article] [PubMed]
    [Google Scholar]
  109. Lazzaro M, Feldman MF, García Véscovi E. A transcriptional regulatory mechanism finely tunes the firing of type VI secretion system in response to bacterial enemies. mBio 2017; 8:e00559-17 [View Article] [PubMed]
    [Google Scholar]
  110. Gerc AJ, Diepold A, Trunk K, Porter M, Rickman C et al. Visualization of the serratia type VI secretion system reveals unprovoked attacks and dynamic assembly. Cell Rep 2015; 12:2131–2142 [View Article] [PubMed]
    [Google Scholar]
  111. Ng W-L, Bassler BL. Bacterial quorum-sensing network architectures. Annu Rev Genet 2009; 43:197–222 [View Article] [PubMed]
    [Google Scholar]
  112. O’Grady EP, Viteri DF, Malott RJ, Sokol PA. Reciprocal regulation by the CepIR and CciIR quorum sensing systems in Burkholderia cenocepacia. BMC Genomics 2009; 10:1–20 [View Article] [PubMed]
    [Google Scholar]
  113. Chambers CE, Lutter EI, Visser MB, Law PPY, Sokol PA. Identification of potential CepR regulated genes using a cep box motif-based search of the Burkholderia cenocepacia genome. BMC Microbiol 2006; 6:1–19 [View Article] [PubMed]
    [Google Scholar]
  114. Chen L, Zou Y, Kronfl AA, Wu Y. Type VI secretion system of Pseudomonas aeruginosa is associated with biofilm formation but not environmental adaptation. Microbiologyopen 2020; 9:e991 [View Article] [PubMed]
    [Google Scholar]
  115. Sana TG, Lomas R, Gimenez MR, Laubier A, Soscia C et al. Differential modulation of quorum sensing signaling through QslA in Pseudomonas aeruginosa strains PAO1 and PA14. J Bacteriol 2019; 201:21 [View Article] [PubMed]
    [Google Scholar]
  116. Meng X, Ahator SD, Zhang L-H. Molecular mechanisms of phosphate stress activation of Pseudomonas aeruginosa quorum sensing systems. mSphere 2020; 5:e00119-20 [View Article] [PubMed]
    [Google Scholar]
  117. Filloux A, Bally M, Soscia C, Murgier M, Lazdunski A. Phosphate regulation in Pseudomonas aeruginosa: cloning of the alkaline phosphatase gene and identification of phoB- and phoR-like genes. Mol Gen Genet 1988; 212:510–513 [View Article] [PubMed]
    [Google Scholar]
  118. Miller MB, Skorupski K, Lenz DH, Taylor RK, Bassler BL. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 2002; 110:303–314 [View Article] [PubMed]
    [Google Scholar]
  119. Jung SA, Chapman CA, Ng W-L. Quadruple quorum-sensing inputs control Vibrio cholerae virulence and maintain system robustness. PLoS Pathog 2015; 11:e1004837 [View Article] [PubMed]
    [Google Scholar]
  120. Shao Y, Bassler BL. Quorum regulatory small RNAs repress type VI secretion in Vibrio cholerae. Mol Microbiol 2014; 92:921–930 [View Article] [PubMed]
    [Google Scholar]
  121. Ball AS, Chaparian RR, van Kessel JC. Quorum sensing gene regulation by LuxR/HapR master regulators in Vibrios. J Bacteriol 2017; 199:19 [View Article] [PubMed]
    [Google Scholar]
  122. Ishikawa T, Rompikuntal PK, Lindmark B, Milton DL, Wai SN. Quorum sensing regulation of the two hcp alleles in Vibrio cholerae O1 strains. PLoS One 2009; 4:e6734 [View Article] [PubMed]
    [Google Scholar]
  123. Liu X, Pan J, Gao H, Han Y, Zhang A et al. CqsA/LuxS-HapR quorum sensing circuit modulates type VI secretion system VflT6SS2 in Vibrio fluvialis. Emerg Microbes Infect 2021; 10:589–601 [View Article] [PubMed]
    [Google Scholar]
  124. Han Y, Pan J, Huang Y, Cheng Q, Liu P et al. VfqI-VfqR quorum sensing circuit modulates type VI secretion system VflT6SS2 in Vibrio fluvialis. Biochem Biophys Rep 2022; 31:101282 [View Article] [PubMed]
    [Google Scholar]
  125. Yang Z, Zhou X, Ma Y, Zhou M, Waldor MK et al. Serine/threonine kinase PpkA coordinates the interplay between T6SS2 activation and quorum sensing in the marine pathogen Vibrio alginolyticus. Environ Microbiol 2018; 20:903–919 [View Article] [PubMed]
    [Google Scholar]
  126. Yang Z, Wang X, Xu W, Zhou M, Zhang Y et al. Phosphorylation of PppA at threonine 253 controls T6SS2 expression and bacterial killing capacity in the marine pathogen Vibrio alginolyticus. Microbiol Res 2018; 209:70–78 [View Article] [PubMed]
    [Google Scholar]
  127. 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]
  128. 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] [PubMed]
    [Google Scholar]
  129. Asfahl KL, Schuster M. Social interactions in bacterial cell-cell signaling. FEMS Microbiol Rev 2017; 41:92–107 [View Article] [PubMed]
    [Google Scholar]
  130. Zhang Z, Claessen D, Rozen DE. Understanding microbial divisions of labor. Front Microbiol 2016; 7:2070 [View Article] [PubMed]
    [Google Scholar]
  131. Sandoz KM, Mitzimberg SM, Schuster M. Social cheating in Pseudomonas aeruginosa quorum sensing. Proc Natl Acad Sci 2007; 104:15876–15881 [View Article] [PubMed]
    [Google Scholar]
  132. Katzianer DS, Wang H, Carey RM, Zhu J. “Quorum non-sensing”: social cheating and deception in Vibrio cholerae. Appl Environ Microbiol 2015; 81:3856–3862 [View Article] [PubMed]
    [Google Scholar]
  133. Kimbrough JH, Stabb EV, O’Toole GA. Antisocial luxO mutants provide a stationary-phase survival advantage in Vibrio fischeri ES114. J Bacteriol 2016; 198:673–687 [View Article] [PubMed]
    [Google Scholar]
  134. Mashruwala AA, Qin B, Bassler BL. Quorum-sensing- and type VI secretion-mediated spatiotemporal cell death drives genetic diversity in Vibrio cholerae. Cell 2022; 185:3966–3979 [View Article] [PubMed]
    [Google Scholar]
  135. Toska J, Ho BT, Mekalanos JJ. Exopolysaccharide protects Vibrio cholerae from exogenous attacks by the type 6 secretion system. Proc Natl Acad Sci U S A 2018; 115:7997–8002 [View Article] [PubMed]
    [Google Scholar]
  136. Aravind L, Anantharaman V, Balaji S, Babu MM, Iyer LM. The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiol Rev 2005; 29:231–262 [View Article] [PubMed]
    [Google Scholar]
  137. Molina-Henares AJ, Krell T, Eugenia Guazzaroni M, Segura A, Ramos JL. Members of the IclR family of bacterial transcriptional regulators function as activators and/or repressors. FEMS Microbiol Rev 2006; 30:157–186 [View Article] [PubMed]
    [Google Scholar]
  138. Brinkman AB, Ettema TJG, de Vos WM, van der Oost J. The Lrp family of transcriptional regulators. Mol Microbiol 2003; 48:287–294 [View Article] [PubMed]
    [Google Scholar]
  139. Maddocks SE, Oyston PCF. Structure and function of the LysR-type transcriptional regulator (LTTR) family proteins. Microbiology 2008; 154:3609–3623 [View Article] [PubMed]
    [Google Scholar]
  140. 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] [PubMed]
    [Google Scholar]
  141. Zhang L, Osei-Adjei G, Zhang Y, Gao H, Yang W et al. CalR is required for the expression of T6SS2 and the adhesion of Vibrio parahaemolyticus to HeLa cells. Arch Microbiol 2017; 199:931–938 [View Article] [PubMed]
    [Google Scholar]
  142. 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]
  143. Morin N, Santiago AE, Ernst RK, Guillot SJ, Nataro JP. Characterization of the AggR regulon in enteroaggregative Escherichia coli. Infect Immun 2013; 81:122–132 [View Article] [PubMed]
    [Google Scholar]
  144. Brunet YR, Espinosa L, Harchouni S, Mignot T, Cascales E. Imaging type VI secretion-mediated bacterial killing. Cell Rep 2013; 3:36–41 [View Article] [PubMed]
    [Google Scholar]
  145. Weber BS, Ly PM, Irwin JN, Pukatzki S, Feldman MF. A multidrug resistance plasmid contains the molecular switch for type VI secretion in Acinetobacter baumannii. Proc Natl Acad Sci U S A 2015; 112:9442–9447 [View Article] [PubMed]
    [Google Scholar]
  146. Di Venanzio G, Moon KH, Weber BS, Lopez J, Ly PM et al. Multidrug-resistant plasmids repress chromosomally encoded T6SS to enable their dissemination. Proc Natl Acad Sci U S A 2019; 116:1378–1383 [View Article] [PubMed]
    [Google Scholar]
  147. Di Venanzio G, Flores-Mireles AL, Calix JJ, Haurat MF, Scott NE et al. Urinary tract colonization is enhanced by a plasmid that regulates uropathogenic Acinetobacter baumannii chromosomal genes. Nat Commun 2019; 10:2763 [View Article] [PubMed]
    [Google Scholar]
  148. Cuthbertson L, Nodwell JR. The TetR family of regulators. Microbiol Mol Biol Rev 2013; 77:440–475 [View Article] [PubMed]
    [Google Scholar]
  149. 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]
  150. 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] [PubMed]
    [Google Scholar]
  151. Bernard CS, Brunet YR, Gavioli M, Lloubès R, Cascales E. Regulation of type VI secretion gene clusters by sigma54 and cognate enhancer binding proteins. J Bacteriol 2011; 193:2158–2167 [View Article] [PubMed]
    [Google Scholar]
  152. Suarez G, Sierra JC, Sha J, Wang S, Erova TE et al. Molecular characterization of a functional type VI secretion system from a clinical isolate of Aeromonas hydrophila. Microb Pathog 2008; 44:344–361 [View Article] [PubMed]
    [Google Scholar]
  153. Li J, Wu Z, Wu C, Chen D-D, Zhou Y et al. VasH contributes to virulence of Aeromonas hydrophila and Is necessary to the T6SS-mediated bactericidal effect. Front Vet Sci 2021; 8:793458 [View Article] [PubMed]
    [Google Scholar]
  154. 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] [PubMed]
    [Google Scholar]
  155. 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] [PubMed]
    [Google Scholar]
  156. Yan J, Guo X, Li J, Li Y, Sun H et al. RpoN is required for the motility and contributes to the killing ability of Plesiomonas shigelloides. BMC Microbiol 2022; 22:299 [View Article] [PubMed]
    [Google Scholar]
  157. Wang Y, Li Y, Wang J, Wang X. FleQ regulates both the type VI secretion system and flagella in Pseudomonas putida. Biotechnol Appl Biochem 2018; 65:419–427 [View Article] [PubMed]
    [Google Scholar]
  158. Sana TG, Soscia C, Tonglet CM, Garvis S, Bleves S. Divergent control of two type VI secretion systems by RpoN in Pseudomonas aeruginosa. PLoS One 2013; 8:e76030 [View Article] [PubMed]
    [Google Scholar]
  159. 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 2021; 50:227–243 [View Article] [PubMed]
    [Google Scholar]
  160. Shao X, Zhang X, Zhang Y, Zhu M, Yang P et al. RpoN-dependent direct regulation of quorum sensing and the type VI secretion system in Pseudomonas aeruginosa PAO1. J Bacteriol 2018; 200:e00205-18 [View Article] [PubMed]
    [Google Scholar]
  161. Guan J, Xiao X, Xu S, Gao F, Wang J et al. Roles of RpoS in Yersinia pseudotuberculosis stress survival, motility, biofilm formation and type VI secretion system expression. J Microbiol 2015; 53:633–642 [View Article] [PubMed]
    [Google Scholar]
  162. Zhang Y, Huang Y, Ding H, Ma J, Tong X et al. A σE-mediated temperature gauge orchestrates type VI secretion system, biofilm formation and cell invasion in pathogen Pseudomonas plecoglossicida. Microbiol Res 2023; 266:127220 [View Article] [PubMed]
    [Google Scholar]
  163. Dong TG, Mekalanos JJ. Characterization of the RpoN regulon reveals differential regulation of T6SS and new flagellar operons in Vibrio cholerae O37 strain V52. Nucleic Acids Res 2012; 40:7766–7775 [View Article] [PubMed]
    [Google Scholar]
  164. Grainger DC. Structure and function of bacterial H-NS protein. Biochem Soc Trans 2016; 44:1561–1569 [View Article] [PubMed]
    [Google Scholar]
  165. Eijkelkamp BA, Stroeher UH, Hassan KA, Elbourne LDH, Paulsen IT et al. H-NS plays a role in expression of Acinetobacter baumannii virulence features. Infect Immun 2013; 81:2574–2583 [View Article] [PubMed]
    [Google Scholar]
  166. Brunet YR, Khodr A, Logger L, Aussel L, Mignot T et al. H-NS silencing of the Salmonella pathogenicity island 6-encoded type VI secretion system limits Salmonella enterica serovar Typhimurium interbacterial killing. Infect Immun 2015; 83:2738–2750 [View Article] [PubMed]
    [Google Scholar]
  167. Castang S, McManus HR, Turner KH, Dove SL. H-NS family members function coordinately in an opportunistic pathogen. Proc Natl Acad Sci U S A 2008; 105:18947–18952 [View Article] [PubMed]
    [Google Scholar]
  168. Renzi F, Rescalli E, Galli E, Bertoni G. Identification of genes regulated by the MvaT-like paralogues TurA and TurB of Pseudomonas putida KT2440. Environ Microbiol 2010; 12:254–263 [View Article] [PubMed]
    [Google Scholar]
  169. Haas AL, Zemke AC, Melvin JA, Armbruster CR, Hendricks MR et al. Iron bioavailability regulates Pseudomonas aeruginosa interspecies interactions through type VI secretion expression. Cell Rep 2023; 42:112270 [View Article] [PubMed]
    [Google Scholar]
  170. 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] [PubMed]
    [Google Scholar]
  171. 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:e51857 [View Article] [PubMed]
    [Google Scholar]
  172. Van Assche E, Van Puyvelde S, Vanderleyden J, Steenackers HP. RNA-binding proteins involved in post-transcriptional regulation in bacteria. Front Microbiol 2015; 6:141 [View Article] [PubMed]
    [Google Scholar]
  173. Jørgensen MG, Pettersen JS, Kallipolitis BH. sRNA-mediated control in bacteria: an increasing diversity of regulatory mechanisms. Biochim Biophys Acta Gene Regul Mech 2020; 1863:194504 [View Article] [PubMed]
    [Google Scholar]
  174. Vakulskas CA, Potts AH, Babitzke P, Ahmer BMM, Romeo T. Regulation of bacterial virulence by Csr (Rsm) systems. Microbiol Mol Biol Rev 2015; 79:193–224 [View Article] [PubMed]
    [Google Scholar]
  175. Brencic A, Lory S. Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol Microbiol 2009; 72:612–632 [View Article] [PubMed]
    [Google Scholar]
  176. Romero M, Silistre H, Lovelock L, Wright VJ, Chan K-G et al. Genome-wide mapping of the RNA targets of the Pseudomonas aeruginosa riboregulatory protein RsmN. Nucleic Acids Res 2018; 46:6823–6840 [View Article] [PubMed]
    [Google Scholar]
  177. Willett JW, Crosson S. Atypical modes of bacterial histidine kinase signaling. Mol Microbiol 2017; 103:197–202 [View Article] [PubMed]
    [Google Scholar]
  178. Xia YS, Xu CJ, Wang D, Weng YD, Jin YX et al. YbeY controls the type III and type VI secretion systems and biofilm formation through RetS in Pseudomonas aeruginosa. Appl Environ Microbiol 2021; 87:e02171-20 [View Article] [PubMed]
    [Google Scholar]
  179. Hochschild A, Lewis M. The bacteriophage lambda CI protein finds an asymmetric solution. Curr Opin Struct Biol 2009; 19:79–86 [View Article] [PubMed]
    [Google Scholar]
  180. Jiao H, Li F, Wang T, Yam JKH, Yang L et al. The pyocin regulator PrtR regulates virulence expression of Pseudomonas aeruginosa by modulation of Gac/Rsm system and c-di-GMP signaling pathway. Infect Immun 2021; 89:e00602-20 [View Article] [PubMed]
    [Google Scholar]
  181. Zhang X, Yin L, Liu Q, Wang D, Xu C et al. NrtR mediated regulation of H1-T6SS in Pseudomonas aeruginosa. Microbiol Spectr 2022; 10:e0185821 [View Article] [PubMed]
    [Google Scholar]
  182. Rodionov DA, De Ingeniis J, Mancini C, Cimadamore F, Zhang H et al. Transcriptional regulation of NAD metabolism in bacteria: NrtR family of Nudix-related regulators. Nucleic Acids Res 2008; 36:2047–2059 [View Article] [PubMed]
    [Google Scholar]
  183. Dadashi M, Chen L, Nasimian A, Ghavami S, Duan K. Putative RNA ligase RtcB affects the switch between T6SS and T3SS in Pseudomonas aeruginosa. Int J Mol Sci 2021; 22:12561 [View Article] [PubMed]
    [Google Scholar]
  184. Stacey SD, Williams DA, Pritchett CL. The Pseudomonas aeruginosa two-component regulator AlgR directly activates rsmA expression in a phosphorylation-independent manner. J Bacteriol 2017; 199:e00048-17 [View Article] [PubMed]
    [Google Scholar]
  185. Goodman AL, Merighi M, Hyodo M, Ventre I, Filloux A et al. Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev 2009; 23:249–259 [View Article] [PubMed]
    [Google Scholar]
  186. Chambonnier G, Roux L, Redelberger D, Fadel F, Filloux A et al. The hybrid histidine kinase LadS forms a multicomponent signal transduction system with the GacS/GacA two-component system in Pseudomonas aeruginosa. PLoS Genet 2016; 12:e1006032 [View Article] [PubMed]
    [Google Scholar]
  187. LeRoux M, Peterson SB, Mougous JD. Bacterial danger sensing. J Mol Biol 2015; 427:3744–3753 [View Article] [PubMed]
    [Google Scholar]
  188. Mikkelsen H, Sivaneson M, Filloux A. Key two-component regulatory systems that control biofilm formation in Pseudomonas aeruginosa. Environ Microbiol 2011; 13:1666–1681 [View Article] [PubMed]
    [Google Scholar]
  189. Zhang L, Hinz AJ, Nadeau JP, Mah TF. Pseudomonas aeruginosa tssC1 links type VI secretion and biofilm-specific antibiotic resistance. J Bacteriol 2011; 193:5510–5513 [View Article] [PubMed]
    [Google Scholar]
  190. Sun Z, Shi J, Liu C, Jin Y, Li K et al. PrtR homeostasis contributes to Pseudomonas aeruginosa pathogenesis and resistance against ciprofloxacin. Infect Immun 2014; 82:1638–1647 [View Article] [PubMed]
    [Google Scholar]
  191. Moscoso JA, Mikkelsen H, Heeb S, Williams P, Filloux A. The Pseudomonas aeruginosa sensor RetS switches type III and type VI secretion via c-di-GMP signalling. Environ Microbiol 2011; 13:3128–3138 [View Article] [PubMed]
    [Google Scholar]
  192. Tamayo R, Pratt JT, Camilli A. Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 2007; 61:131–148 [View Article] [PubMed]
    [Google Scholar]
  193. Anantharajah A, Mingeot-Leclercq M-P, Van Bambeke F. Targeting the type three secretion system in Pseudomonas aeruginosa. Trends Pharmacol Sci 2016; 37:734–749 [View Article] [PubMed]
    [Google Scholar]
  194. Ermolenko DN, Makhatadze GI. Bacterial cold-shock proteins. Cell Mol Life Sci 2002; 59:1902–1913 [View Article] [PubMed]
    [Google Scholar]
  195. Coppins RL, Hall KB, Groisman EA. The intricate world of riboswitches. Curr Opin Microbiol 2007; 10:176–181 [View Article] [PubMed]
    [Google Scholar]
  196. Metzger LC, Stutzmann S, Scrignari T, Van der Henst C, Matthey N et al. Independent regulation of Type VI secretion in Vibrio cholerae by TfoX and TfoY. Cell Rep 2016; 15:951–958 [View Article] [PubMed]
    [Google Scholar]
  197. Inuzuka S, Nishimura K-I, Kakizawa H, Fujita Y, Furuta H et al. Mutational analysis of structural elements in a class-I cyclic di-GMP riboswitch to elucidate its regulatory mechanism. J Biochem 2016; 160:153–162 [View Article] [PubMed]
    [Google Scholar]
  198. Inuzuka S, Kakizawa H, Nishimura K-I, Naito T, Miyazaki K et al. Recognition of cyclic-di-GMP by a riboswitch conducts translational repression through masking the ribosome-binding site distant from the aptamer domain. Genes Cells 2018; 23:435–447 [View Article] [PubMed]
    [Google Scholar]
  199. Joshi A, Mahmoud SA, Kim S-K, Ogdahl JL, Lee VT et al. c-di-GMP inhibits LonA-dependent proteolysis of TfoY in Vibrio cholerae. PLoS Genet 2020; 16:e1008897 [View Article] [PubMed]
    [Google Scholar]
  200. Macek B, Forchhammer K, Hardouin J, Weber-Ban E, Grangeasse C et al. Protein post-translational modifications in bacteria. Nat Rev Microbiol 2019; 17:651–664 [View Article] [PubMed]
    [Google Scholar]
  201. Wang J, Brodmann M, Basler M. Assembly and subcellular localization of bacterial type VI secretion systems. Annu Rev Microbiol 2019; 73:621–638 [View Article] [PubMed]
    [Google Scholar]
  202. 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]
  203. Fritsch MJ, Trunk K, Diniz JA, Guo M, Trost M et al. Proteomic identification of novel secreted antibacterial toxins of the Serratia marcescens type VI secretion system. Mol Cell Proteomics 2013; 12:2735–2749 [View Article] [PubMed]
    [Google Scholar]
  204. 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]
  205. 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]
  206. 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]
  207. 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]
  208. Wang G, Fan C, Wang H, Jia C, Li X et al. Type VI secretion system-associated FHA domain protein TagH regulates the hemolytic activity and virulence of Vibrio cholerae. Gut Microbes 2022; 14:2055440 [View Article] [PubMed]
    [Google Scholar]
  209. 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]
  210. 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]
  211. Lin L, Capozzoli R, Ferrand A, Plum M, Vettiger A et al. Subcellular localization of Type VI secretion system assembly in response to cell-cell contact. EMBO J 2022; 41:e108595 [View Article] [PubMed]
    [Google Scholar]
  212. 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]
  213. Stietz MS, Liang X, Li H, Zhang X, Dong TG. TssA-TssM-TagA interaction modulates type VI secretion system sheath-tube assembly in Vibrio cholerae. Nat Commun 2020; 11:5065 [View Article] [PubMed]
    [Google Scholar]
  214. 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]
  215. 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]
  216. Trampari E, Stevenson CEM, Little RH, Wilhelm T, Lawson DM et al. Bacterial rotary export ATPases are allosterically regulated by the nucleotide second messenger cyclic-di-GMP. J Biol Chem 2015; 290:24470–24483 [View Article] [PubMed]
    [Google Scholar]
  217. 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]
  218. 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 U S A 2021; 118:e2104813118 [View Article] [PubMed]
    [Google Scholar]
  219. Smith WPJ, Brodmann M, Unterweger D, Davit Y, Comstock LE et al. The evolution of tit-for-tat in bacteria via the type VI secretion system. Nat Commun 2020; 11:5395 [View Article] [PubMed]
    [Google Scholar]
  220. Zhang C, Ratcliff WC, Hammer BK. Constitutive expression of the Type VI secretion system carries no measurable fitness cost in Vibrio cholerae. bioRxiv 2023 [View Article]
    [Google Scholar]
  221. Chien C-F, Liu C-Y, Lu Y-Y, Sung Y-H, Chen K-Y et al. HSI-II gene cluster of Pseudomonas syringae pv. tomato DC3000 encodes a functional type VI secretion system required for interbacterial competition. Front Microbiol 2020; 11:1118 [View Article] [PubMed]
    [Google Scholar]
  222. Salomon D, Klimko JA, Orth K. H-NS regulates the Vibrio parahaemolyticus type VI secretion system 1. Microbiology 2014; 160:1867–1873 [View Article] [PubMed]
    [Google Scholar]
  223. Gu D, Zhang Y, Wang K, Li M, Jiao X. Characterization of the RpoN regulon reveals the regulation of motility, T6SS2 and metabolism in Vibrio parahaemolyticus. Front Microbiol 2022; 13:1025960 [View Article] [PubMed]
    [Google Scholar]
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