1887

Abstract

The type VI secretion system (T6SS) is a mechanism evolved by Gram-negative bacteria to negotiate interactions with eukaryotic and prokaryotic competitors. T6SSs are encoded by a diverse array of bacteria and include plant, animal, human and fish pathogens, as well as environmental isolates. As such, the regulatory mechanisms governing T6SS gene expression vary widely from species to species, and even from strain to strain within a given species. This review concentrates on the four bacterial genera that the majority of recent T6SS regulatory studies have been focused on: , , and .

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2013-05-01
2019-10-18
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References

  1. Alarcón-Chaidez F. J. , Keith L. , Zhao Y. , Bender C. L. . ( 2003; ). RpoN (σ54) is required for plasmid-encoded coronatine biosynthesis in Pseudomonas syringae . . Plasmid 49:, 106–117. [CrossRef] [PubMed]
    [Google Scholar]
  2. Aubert D. F. , Flannagan R. S. , Valvano M. A. . ( 2008; ). A novel sensor kinase–response regulator hybrid controls biofilm formation and type VI secretion system activity in Burkholderia cenocepacia . . Infect Immun 76:, 1979–1991. [CrossRef] [PubMed]
    [Google Scholar]
  3. Aubert D. , MacDonald D. K. , Valvano M. A. . ( 2010; ). BcsKC is an essential protein for the type VI secretion system activity in Burkholderia cenocepacia that forms an outer membrane complex with BcsLB. . J Biol Chem 285:, 35988–35998. [CrossRef] [PubMed]
    [Google Scholar]
  4. Babujee L. , Apodaca J. , Balakrishnan V. , Liss P. , Kiley P. J. , Charkowski A. O. , Glasner J. D. , Perna N. T. . ( 2012; ). Evolution of the metabolic and regulatory networks associated with oxygen availability in two phytopathogenic enterobacteria. . BMC Genomics 13:, 110. [CrossRef] [PubMed]
    [Google Scholar]
  5. Barret M. , Egan F. , Fargier E. , Morrissey J. P. , O’Gara F. . ( 2011; ). Genomic analysis of the type VI secretion systems in Pseudomonas spp.: novel clusters and putative effectors uncovered. . Microbiology 157:, 1726–1739. [CrossRef] [PubMed]
    [Google Scholar]
  6. Basler M. , Mekalanos J. J. . ( 2012; ). Type 6 secretion dynamics within and between bacterial cells. . Science 337:, 815. [CrossRef] [PubMed]
    [Google Scholar]
  7. Basler M. , Pilhofer M. , Henderson G. P. , Jensen G. J. , Mekalanos J. J. . ( 2012; ). Type VI secretion requires a dynamic contractile phage tail-like structure. . Nature 483:, 182–186. [CrossRef] [PubMed]
    [Google Scholar]
  8. Bernard C. S. , Brunet Y. R. , Gueguen E. , Cascales E. . ( 2010; ). Nooks and crannies in type VI secretion regulation. . J Bacteriol 192:, 3850–3860. [CrossRef] [PubMed]
    [Google Scholar]
  9. Bernard C. S. , Brunet Y. R. , Gavioli M. , Lloubès R. , Cascales E. . ( 2011; ). Regulation of type VI secretion gene clusters by σ54 and cognate enhancer binding proteins. . J Bacteriol 193:, 2158–2167. [CrossRef] [PubMed]
    [Google Scholar]
  10. Bladergroen M. R. , Badelt K. , Spaink H. P. . ( 2003; ). Infection-blocking genes of a symbiotic Rhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. . Mol Plant Microbe Interact 16:, 53–64. [CrossRef] [PubMed]
    [Google Scholar]
  11. Bleves S. , Viarre V. , Salacha R. , Michel G. P. , Filloux A. , Voulhoux R. . ( 2010; ). Protein secretion systems in Pseudomonas aeruginosa: a wealth of pathogenic weapons. . Int J Med Microbiol 300:, 534–543. [CrossRef] [PubMed]
    [Google Scholar]
  12. Bönemann G. , Pietrosiuk A. , Diemand A. , Zentgraf H. , Mogk A. . ( 2009; ). Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. . EMBO J 28:, 315–325. [CrossRef] [PubMed]
    [Google Scholar]
  13. Bordi C. , Lamy M. C. , Ventre I. , Termine E. , Hachani A. , Fillet S. , Roche B. , Bleves S. , Méjean V. et al. ( 2010; ). Regulatory RNAs and the HptB/RetS signalling pathways fine-tune Pseudomonas aeruginosa pathogenesis. . Mol Microbiol 76:, 1427–1443. [CrossRef] [PubMed]
    [Google Scholar]
  14. Boyer F. , Fichant G. , Berthod J. , Vandenbrouck Y. , Attree I. . ( 2009; ). Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources?. BMC Genomics 10:, 104. [CrossRef] [PubMed]
    [Google Scholar]
  15. Brunet Y. R. , Bernard C. S. , Gavioli M. , Lloubès R. , Cascales E. . ( 2011; ). An epigenetic switch involving overlapping fur and DNA methylation optimizes expression of a type VI secretion gene cluster. . PLoS Genet 7:, e1002205. [CrossRef] [PubMed]
    [Google Scholar]
  16. Buck M. , Gallegos M. T. , Studholme D. J. , Guo Y. , Gralla J. D. . ( 2000; ). The bacterial enhancer-dependent ς54N) transcription factor. . J Bacteriol 182:, 4129–4136. [CrossRef] [PubMed]
    [Google Scholar]
  17. Burtnick M. N. , DeShazer D. , Nair V. , Gherardini F. C. , Brett P. J. . ( 2010; ). Burkholderia mallei cluster 1 type VI secretion mutants exhibit growth and actin polymerization defects in RAW 264.7 murine macrophages. . Infect Immun 78:, 88–99. [CrossRef] [PubMed]
    [Google Scholar]
  18. Burtnick M. N. , Brett P. J. , Harding S. V. , Ngugi S. A. , Ribot W. J. , Chantratita N. , Scorpio A. , Milne T. S. , Dean R. E. et al. ( 2011; ). The cluster 1 type VI secretion system is a major virulence determinant in Burkholderia pseudomallei . . Infect Immun 79:, 1512–1525. [CrossRef] [PubMed]
    [Google Scholar]
  19. Casabona M. G. , Silverman J. M. , Sall K. M. , Boyer F. , Coute Y. , Poirel J. , Grunwald D. , Mougous J. D. , Elsen S. , Attree I. . ( 2012; ). An ABC transporter and an outer membrane lipoprotein participate in posttranslational activation of type VI secretion in Pseudomonas aeruginosa . . Environ Microbiol 15:, 471–486 [PubMed] [CrossRef]
    [Google Scholar]
  20. Castang S. , McManus H. R. , Turner K. H. , Dove S. L. . ( 2008; ). H-NS family members function coordinately in an opportunistic pathogen. . Proc Natl Acad Sci U S A 105:, 18947–18952. [CrossRef] [PubMed]
    [Google Scholar]
  21. Chakraborty S. , Li M. , Chatterjee C. , Sivaraman J. , Leung K. Y. , Mok Y. K. . ( 2010; ). Temperature and Mg2+ sensing by a novel PhoP-PhoQ two-component system for regulation of virulence in Edwardsiella tarda . . J Biol Chem 285:, 38876–38888. [CrossRef] [PubMed]
    [Google Scholar]
  22. Chakraborty S. , Sivaraman J. , Leung K. Y. , Mok Y. K. . ( 2011; ). 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 286:, 39417–39430. [CrossRef] [PubMed]
    [Google Scholar]
  23. Chen Y. , Wong J. , Sun G. W. , Liu Y. , Tan G. Y. , Gan Y. H. . ( 2011; ). Regulation of type VI secretion system during Burkholderia pseudomallei infection. . Infect Immun 79:, 3064–3073. [CrossRef] [PubMed]
    [Google Scholar]
  24. Chow J. , Mazmanian S. K. . ( 2010; ). A pathobiont of the microbiota balances host colonization and intestinal inflammation. . Cell Host Microbe 7:, 265–276. [CrossRef] [PubMed]
    [Google Scholar]
  25. Chugani S. , Greenberg E. P. . ( 2007; ). The influence of human respiratory epithelia on Pseudomonas aeruginosa gene expression. . Microb Pathog 42:, 29–35. [CrossRef] [PubMed]
    [Google Scholar]
  26. Coggan K. A. , Wolfgang M. C. . ( 2012; ). Global regulatory pathways and cross-talk control Pseudomonas aeruginosa environmental lifestyle and virulence phenotype. . Curr Issues Mol Biol 14:, 47–70.[PubMed]
    [Google Scholar]
  27. Cvjetanovic B. , Barua D. . ( 1972; ). The seventh pandemic of cholera. . Nature 239:, 137–138. [CrossRef] [PubMed]
    [Google Scholar]
  28. de Bruin O. M. , Ludu J. S. , Nano F. E. . ( 2007; ). The Francisella pathogenicity island protein IglA localizes to the bacterial cytoplasm and is needed for intracellular growth. . BMC Microbiol 7:, 1. [CrossRef] [PubMed]
    [Google Scholar]
  29. de Pace F. , Boldrin de Paiva J. , Nakazato G. , Lancellotti M. , Sircili M. P. , Guedes Stehling E. , Dias da Silveira W. , Sperandio V. . ( 2011; ). Characterization of IcmF of the type VI secretion system in an avian pathogenic Escherichia coli (APEC) strain. . Microbiology 157:, 2954–2962. [CrossRef] [PubMed]
    [Google Scholar]
  30. Déziel E. , Lépine F. , Milot S. , He J. , Mindrinos M. N. , Tompkins R. G. , Rahme L. G. . ( 2004; ). Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. . Proc Natl Acad Sci U S A 101:, 1339–1344. [CrossRef] [PubMed]
    [Google Scholar]
  31. Déziel E. , Gopalan S. , Tampakaki A. P. , Lépine F. , Padfield K. E. , Saucier M. , Xiao G. , Rahme L. G. . ( 2005; ). The contribution of MvfR to Pseudomonas aeruginosa pathogenesis and quorum sensing circuitry regulation: multiple quorum sensing-regulated genes are modulated without affecting lasRI, rhlRI or the production of N-acyl-L-homoserine lactones. . Mol Microbiol 55:, 998–1014. [CrossRef] [PubMed]
    [Google Scholar]
  32. Dong T. G. , Mekalanos J. J. . ( 2012; ). Characterization of the RpoN regulon reveals differential regulation of T6SS and new flagellar operons in Vibrio cholerae O37 strain V52. . Nucleic Acids Res 40:, 7766–7775. [CrossRef] [PubMed]
    [Google Scholar]
  33. Dudley E. G. , Thomson N. R. , Parkhill J. , Morin N. P. , Nataro J. P. . ( 2006; ). Proteomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity island in enteroaggregative Escherichia coli . . Mol Microbiol 61:, 1267–1282. [CrossRef] [PubMed]
    [Google Scholar]
  34. Enos-Berlage J. L. , Guvener Z. T. , Keenan C. E. , McCarter L. L. . ( 2005; ). Genetic determinants of biofilm development of opaque and translucent Vibrio parahaemolyticus . . Mol Microbiol 55:, 1160–1182. [CrossRef] [PubMed]
    [Google Scholar]
  35. Euzéby J. P. . ( 1997; ). List of bacterial names with standing in nomenclature: a folder available on the Internet. . Int J Syst Bacteriol 47:, 590–592. [CrossRef] [PubMed]
    [Google Scholar]
  36. Folkesson A. , Löfdahl S. , Normark S. . ( 2002; ). The Salmonella enterica subspecies I specific centisome 7 genomic island encodes novel protein families present in bacteria living in close contact with eukaryotic cells. . Res Microbiol 153:, 537–545. [CrossRef] [PubMed]
    [Google Scholar]
  37. Glass M. B. , Gee J. E. , Steigerwalt A. G. , Cavuoti D. , Barton T. , Hardy R. D. , Godoy D. , Spratt B. G. , Clark T. A. , Wilkins P. P. . ( 2006; ). Pneumonia and septicemia caused by Burkholderia thailandensis in the United States. . J Clin Microbiol 44:, 4601–4604. [CrossRef] [PubMed]
    [Google Scholar]
  38. Gode-Potratz C. J. , McCarter L. L. . ( 2011; ). Quorum sensing and silencing in Vibrio parahaemolyticus . . J Bacteriol 193:, 4224–4237. [CrossRef] [PubMed]
    [Google Scholar]
  39. Goodman A. L. , Kulasekara B. , Rietsch A. , Boyd D. , Smith R. S. , Lory S. . ( 2004; ). A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa . . Dev Cell 7:, 745–754. [CrossRef] [PubMed]
    [Google Scholar]
  40. Haapalainen M. , Mosorin H. , Dorati F. , Wu R. F. , Roine E. , Taira S. , Nissinen R. , Mattinen L. , Jackson R. et al. ( 2012; ). Hcp2, a secreted protein of the phytopathogen Pseudomonas syringae pv. tomato DC3000, is required for competitive fitness against bacteria and yeasts. . J Bacteriol 194:, 4810–4822.[CrossRef]
    [Google Scholar]
  41. Hassan K. A. , Johnson A. , Shaffer B. T. , Ren Q. , Kidarsa T. A. , Elbourne L. D. , Hartney S. , Duboy R. , Goebel N. C. et al. ( 2010; ). Inactivation of the GacA response regulator in Pseudomonas fluorescens Pf-5 has far-reaching transcriptomic consequences. . Environ Microbiol 12:, 899–915. [CrossRef] [PubMed]
    [Google Scholar]
  42. Hendrickson E. L. , Plotnikova J. , Mahajan-Miklos S. , Rahme L. G. , Ausubel F. M. . ( 2001; ). Differential roles of the Pseudomonas aeruginosa PA14 rpoN gene in pathogenicity in plants, nematodes, insects, and mice. . J Bacteriol 183:, 7126–7134. [CrossRef] [PubMed]
    [Google Scholar]
  43. Hood R. D. , Singh P. , Hsu F. , Güvener T. , Carl M. A. , Trinidad R. R. , Silverman J. M. , Ohlson B. B. , Hicks K. G. et al. ( 2010; ). A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. . Cell Host Microbe 7:, 25–37. [CrossRef] [PubMed]
    [Google Scholar]
  44. Hsu F. , Schwarz S. , Mougous J. D. . ( 2009; ). TagR promotes PpkA-catalysed type VI secretion activation in Pseudomonas aeruginosa . . Mol Microbiol 72:, 1111–1125. [CrossRef] [PubMed]
    [Google Scholar]
  45. Hu Y. H. , Dang W. , Liu C. S. , Sun L. . ( 2010; ). Analysis of the effect of copper on the virulence of a pathogenic Edwardsiella tarda strain. . Lett Appl Microbiol 50:, 97–103. [CrossRef] [PubMed]
    [Google Scholar]
  46. Ishikawa T. , Rompikuntal P. K. , Lindmark B. , Milton D. L. , Wai S. N. . ( 2009; ). Quorum sensing regulation of the two hcp alleles in Vibrio cholerae O1 strains. . PLoS ONE 4:, e6734. [CrossRef] [PubMed]
    [Google Scholar]
  47. Ishikawa T. , Sabharwal D. , Bröms J. , Milton D. L. , Sjöstedt A. , Uhlin B. E. , Wai S. N. . ( 2012; ). Pathoadaptive conditional regulation of the type VI secretion system in Vibrio cholerae O1 strains. . Infect Immun 80:, 575–584. [CrossRef] [PubMed]
    [Google Scholar]
  48. Kamal A. M. . ( 1974; ). The seventh pandemic of cholera. In Cholera, pp. . 1–14. Edited by D. Barua & W. Burrows. Philadelphia: Saunders.
    [Google Scholar]
  49. Kang Y. , Nguyen D. T. , Son M. S. , Hoang T. T. . ( 2008; ). The Pseudomonas aeruginosa PsrA responds to long-chain fatty acid signals to regulate the fadBA5 beta-oxidation operon. . Microbiology 154:, 1584–1598. [CrossRef] [PubMed]
    [Google Scholar]
  50. Khajanchi B. K. , Sha J. , Kozlova E. V. , Erova T. E. , Suarez G. , Sierra J. C. , Popov V. L. , Horneman A. J. , Chopra A. K. . ( 2009; ). 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 155:, 3518–3531. [CrossRef] [PubMed]
    [Google Scholar]
  51. Kitaoka M. , Miyata S. T. , Brooks T. M. , Unterweger D. , Pukatzki S. . ( 2011; ). VasH is a transcriptional regulator of the type VI secretion system functional in endemic and pandemic Vibrio cholerae . . J Bacteriol 193:, 6471–6482. [CrossRef] [PubMed]
    [Google Scholar]
  52. Lalaouna D. , Fochesato S. , Sanchez L. , Schmitt-Kopplin P. , Haas D. , Heulin T. , Achouak W. . ( 2012; ). Phenotypic switching in Pseudomonas brassicacearum involves GacS- and GacA-dependent Rsm small RNAs. . Appl Environ Microbiol 78:, 1658–1665. [CrossRef] [PubMed]
    [Google Scholar]
  53. Leiman P. G. , Basler M. , Ramagopal U. A. , Bonanno J. B. , Sauder J. M. , Pukatzki S. , Burley S. K. , Almo S. C. , Mekalanos J. J. . ( 2009; ). Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. . Proc Natl Acad Sci U S A 106:, 4154–4159. [CrossRef] [PubMed]
    [Google Scholar]
  54. Lertpiriyapong K. , Gamazon E. R. , Feng Y. , Park D. S. , Pang J. , Botka G. , Graffam M. E. , Ge Z. , Fox J. G. . ( 2012; ). Campylobacter jejuni type VI secretion system: roles in adaptation to deoxycholic acid, host cell adherence, invasion, and in vivo colonization. . PLoS ONE 7:, e42842. [CrossRef] [PubMed]
    [Google Scholar]
  55. Lesic B. , Starkey M. , He J. , Hazan R. , Rahme L. G. . ( 2009; ). Quorum sensing differentially regulates Pseudomonas aeruginosa type VI secretion locus I and homologous loci II and III, which are required for pathogenesis. . Microbiology 155:, 2845–2855. [CrossRef] [PubMed]
    [Google Scholar]
  56. Leung K. Y. , Siame B. A. , Snowball H. , Mok Y. K. . ( 2011; ). Type VI secretion regulation: crosstalk and intracellular communication. . Curr Opin Microbiol 14:, 9–15. [CrossRef] [PubMed]
    [Google Scholar]
  57. Liu H. , Coulthurst S. J. , Pritchard L. , Hedley P. E. , Ravensdale M. , Humphris S. , Burr T. , Takle G. , Brurberg M. B. et al. ( 2008; ). Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum . . PLoS Pathog 4:, e1000093. [CrossRef] [PubMed]
    [Google Scholar]
  58. Lombardo M. J. , Michalski J. , Martinez-Wilson H. , Morin C. , Hilton T. , Osorio C. G. , Nataro J. P. , Tacket C. O. , Camilli A. , Kaper J. B. . ( 2007; ). An in vivo expression technology screen for Vibrio cholerae genes expressed in human volunteers. . Proc Natl Acad Sci U S A 104:, 18229–18234. [CrossRef] [PubMed]
    [Google Scholar]
  59. Lv Y. , Xiao J. , Liu Q. , Wu H. , Zhang Y. , Wang Q. . ( 2012; ). Systematic mutation analysis of two-component signal transduction systems reveals EsrA-EsrB and PhoP-PhoQ as the major virulence regulators in Edwardsiella tarda . . Vet Microbiol 157:, 190–199. [CrossRef] [PubMed]
    [Google Scholar]
  60. Ma A. T. , Mekalanos J. J. . ( 2010; ). In vivo actin cross-linking induced by Vibrio cholerae type VI secretion system is associated with intestinal inflammation. . Proc Natl Acad Sci U S A 107:, 4365–4370. [CrossRef] [PubMed]
    [Google Scholar]
  61. Ma L. S. , Lin J. S. , Lai E. M. . ( 2009; ). An IcmF family protein, ImpLM, is an integral inner membrane protein interacting with ImpKL, and its walker a motif is required for type VI secretion system-mediated Hcp secretion in Agrobacterium tumefaciens . . J Bacteriol 191:, 4316–4329. [CrossRef] [PubMed]
    [Google Scholar]
  62. Ma L. , Zhang Y. , Yan X. , Guo L. , Wang L. , Qiu J. , Yang R. , Zhou D. . ( 2012; ). Expression of the type VI secretion system 1 component Hcp1 is indirectly repressed by OpaR in Vibrio parahaemolyticus . . ScientificWorldJournal 2012:, 982140. [CrossRef] [PubMed]
    [Google Scholar]
  63. MacIntyre D. L. , Miyata S. T. , Kitaoka M. , Pukatzki S. . ( 2010; ). The Vibrio cholerae type VI secretion system displays antimicrobial properties. . Proc Natl Acad Sci U S A 107:, 19520–19524. [CrossRef] [PubMed]
    [Google Scholar]
  64. Mandlik A. , Livny J. , Robins W. P. , Ritchie J. M. , Mekalanos J. J. , Waldor M. K. . ( 2011; ). RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression. . Cell Host Microbe 10:, 165–174. [CrossRef] [PubMed]
    [Google Scholar]
  65. Mattinen L. , Somervuo P. , Nykyri J. , Nissinen R. , Kouvonen P. , Corthals G. , Auvinen P. , Aittamaa M. , Valkonen J. P. , Pirhonen M. . ( 2008; ). Microarray profiling of host-extract-induced genes and characterization of the type VI secretion cluster in the potato pathogen Pectobacterium atrosepticum . . Microbiology 154:, 2387–2396. [CrossRef] [PubMed]
    [Google Scholar]
  66. Mikkelsen H. , McMullan R. , Filloux A. . ( 2011; ). The Pseudomonas aeruginosa reference strain PA14 displays increased virulence due to a mutation in ladS. . PLoS ONE 6:, e29113. [CrossRef] [PubMed]
    [Google Scholar]
  67. Miyata S. T. , Kitaoka M. , Wieteska L. , Frech C. , Chen N. , Pukatzki S. . ( 2010; ). The Vibrio cholerae type VI secretion system: evaluating its role in the human disease cholera. . Front Microbiol 1:, 117.[PubMed] [CrossRef]
    [Google Scholar]
  68. Miyata S. T. , Kitaoka M. , Brooks T. M. , McAuley S. B. , Pukatzki S. . ( 2011; ). Vibrio cholerae requires the type VI secretion system virulence factor VasX to kill Dictyostelium discoideum . . Infect Immun 79:, 2941–2949. [CrossRef] [PubMed]
    [Google Scholar]
  69. Mojzsis S. J. , Arrhenius G. , McKeegan K. D. , Harrison T. M. , Nutman A. P. , Friend C. R. . ( 1996; ). Evidence for life on Earth before 3,800 million years ago. . Nature 384:, 55–59. [CrossRef] [PubMed]
    [Google Scholar]
  70. Moscoso J. A. , Mikkelsen H. , Heeb S. , Williams P. , Filloux A. . ( 2011; ). The Pseudomonas aeruginosa sensor RetS switches type III and type VI secretion via c-di-GMP signalling. . Environ Microbiol 13:, 3128–3138. [CrossRef] [PubMed]
    [Google Scholar]
  71. Mougous J. D. , Cuff M. E. , Raunser S. , Shen A. , Zhou M. , Gifford C. A. , Goodman A. L. , Joachimiak G. , Ordoñez C. L. et al. ( 2006; ). A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. . Science 312:, 1526–1530. [CrossRef] [PubMed]
    [Google Scholar]
  72. Mougous J. D. , Gifford C. A. , Ramsdell T. L. , Mekalanos J. J. . ( 2007; ). Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa . . Nat Cell Biol 9:, 797–803. [CrossRef] [PubMed]
    [Google Scholar]
  73. Mueller R. S. , Beyhan S. , Saini S. G. , Yildiz F. H. , Bartlett D. H. . ( 2009; ). Indole acts as an extracellular cue regulating gene expression in Vibrio cholerae . . J Bacteriol 191:, 3504–3516. [CrossRef] [PubMed]
    [Google Scholar]
  74. Murdoch S. L. , Trunk K. , English G. , Fritsch M. J. , Pourkarimi E. , Coulthurst S. J. . ( 2011; ). The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. . J Bacteriol 193:, 6057–6069. [CrossRef] [PubMed]
    [Google Scholar]
  75. O’Brien H. E. , Desveaux D. , Guttman D. S. . ( 2011; ). Next-generation genomics of Pseudomonas syringae . . Curr Opin Microbiol 14:, 24–30. [CrossRef] [PubMed]
    [Google Scholar]
  76. Okuda J. , Kiriyama M. , Suzaki E. , Kataoka K. , Nishibuchi M. , Nakai T. . ( 2009; ). Characterization of proteins secreted from a type III secretion system of Edwardsiella tarda and their roles in macrophage infection. . Dis Aquat Organ 84:, 115–121. [CrossRef] [PubMed]
    [Google Scholar]
  77. Palleroni N. J. . ( 1992; ). Introduction to the Pseudomonadaceae. New York:: Springer;.
    [Google Scholar]
  78. Parsons D. A. , Heffron F. . ( 2005; ). sciS, An icmF homolog in Salmonella enterica serovar Typhimurium, limits intracellular replication and decreases virulence. . Infect Immun 73:, 4338–4345. [CrossRef] [PubMed]
    [Google Scholar]
  79. Pieper R. , Huang S. T. , Robinson J. M. , Clark D. J. , Alami H. , Parmar P. P. , Perry R. D. , Fleischmann R. D. , Peterson S. N. . ( 2009; ). Temperature and growth phase influence the outer-membrane proteome and the expression of a type VI secretion system in Yersinia pestis . . Microbiology 155:, 498–512. [CrossRef] [PubMed]
    [Google Scholar]
  80. Podladchikova O. , Antonenka U. , Heesemann J. , Rakin A. . ( 2011; ). Yersinia pestis autoagglutination factor is a component of the type six secretion system. . Int J Med Microbiol 301:, 562–569. [CrossRef] [PubMed]
    [Google Scholar]
  81. Potvin E. , Lehoux D. E. , Kukavica-Ibrulj I. , Richard K. L. , Sanschagrin F. , Lau G. W. , Levesque R. C. . ( 2003; ). In vivo functional genomics of Pseudomonas aeruginosa for high-throughput screening of new virulence factors and antibacterial targets. . Environ Microbiol 5:, 1294–1308. [CrossRef] [PubMed]
    [Google Scholar]
  82. Pukatzki S. , Ma A. T. , Sturtevant D. , Krastins B. , Sarracino D. , Nelson W. C. , Heidelberg J. F. , Mekalanos J. J. . ( 2006; ). Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. . Proc Natl Acad Sci U S A 103:, 1528–1533. [CrossRef] [PubMed]
    [Google Scholar]
  83. Pukatzki S. , Ma A. T. , Revel A. T. , Sturtevant D. , Mekalanos J. J. . ( 2007; ). Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. . Proc Natl Acad Sci U S A 104:, 15508–15513. [CrossRef] [PubMed]
    [Google Scholar]
  84. Rao P. S. , Yamada Y. , Tan Y. P. , Leung K. Y. . ( 2004; ). Use of proteomics to identify novel virulence determinants that are required for Edwardsiella tarda pathogenesis. . Mol Microbiol 53:, 573–586. [CrossRef] [PubMed]
    [Google Scholar]
  85. Records A. R. , Gross D. C. . ( 2010; ). Sensor kinases RetS and LadS regulate Pseudomonas syringae type VI secretion and virulence factors. . J Bacteriol 192:, 3584–3596. [CrossRef] [PubMed]
    [Google Scholar]
  86. Robinson J. B. , Telepnev M. V. , Zudina I. V. , Bouyer D. , Montenieri J. A. , Bearden S. W. , Gage K. L. , Agar S. L. , Foltz S. M. et al. ( 2009; ). Evaluation of a Yersinia pestis mutant impaired in a thermoregulated type VI-like secretion system in flea, macrophage and murine models. . Microb Pathog 47:, 243–251. [CrossRef] [PubMed]
    [Google Scholar]
  87. Rogge M. L. , Thune R. L. . ( 2011; ). Regulation of the Edwardsiella ictaluri type III secretion system by pH and phosphate concentration through EsrA, EsrB, and EsrC. . Appl Environ Microbiol 77:, 4293–4302. [CrossRef] [PubMed]
    [Google Scholar]
  88. Russell A. B. , Hood R. D. , Bui N. K. , LeRoux M. , Vollmer W. , Mougous J. D. . ( 2011; ). Type VI secretion delivers bacteriolytic effectors to target cells. . Nature 475:, 343–347. [CrossRef] [PubMed]
    [Google Scholar]
  89. Russell A. B. , Singh P. , Brittnacher M. , Bui N. K. , Hood R. D. , Carl M. A. , Agnello D. M. , Schwarz S. , Goodlett D. R. et al. ( 2012; ). A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. . Cell Host Microbe 11:, 538–549. [CrossRef] [PubMed]
    [Google Scholar]
  90. Sarris P. F. , Scoulica E. V. . ( 2011; ). Pseudomonas entomophila and Pseudomonas mendocina: potential models for studying the bacterial type VI secretion system. . Infect Genet Evol 11:, 1352–1360. [CrossRef] [PubMed]
    [Google Scholar]
  91. Sarris P. F. , Skandalis N. , Kokkinidis M. , Panopoulos N. J. . ( 2010; ). In silico analysis reveals multiple putative type VI secretion systems and effector proteins in Pseudomonas syringae pathovars. . Mol Plant Pathol 11:, 795–804.[PubMed]
    [Google Scholar]
  92. Schell M. A. , Ulrich R. L. , Ribot W. J. , Brueggemann E. E. , Hines H. B. , Chen D. , Lipscomb L. , Kim H. S. , Mrázek J. et al. ( 2007; ). Type VI secretion is a major virulence determinant in Burkholderia mallei . . Mol Microbiol 64:, 1466–1485. [CrossRef] [PubMed]
    [Google Scholar]
  93. Schwarz S. , West T. E. , Boyer F. , Chiang W. C. , Carl M. A. , Hood R. D. , Rohmer L. , Tolker-Nielsen T. , Skerrett S. J. , Mougous J. D. . ( 2010; ). Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. . PLoS Pathog 6:, e1001068. [CrossRef] [PubMed]
    [Google Scholar]
  94. Shalom G. , Shaw J. G. , Thomas M. S. . ( 2007; ). In vivo expression technology identifies a type VI secretion system locus in Burkholderia pseudomallei that is induced upon invasion of macrophages. . Microbiology 153:, 2689–2699. [CrossRef] [PubMed]
    [Google Scholar]
  95. Shanks J. , Burtnick M. N. , Brett P. J. , Waag D. M. , Spurgers K. B. , Ribot W. J. , Schell M. A. , Panchal R. G. , Gherardini F. C. et al. ( 2009; ). Burkholderia mallei tssM encodes a putative deubiquitinase that is secreted and expressed inside infected RAW 264.7 murine macrophages. . Infect Immun 77:, 1636–1648. [CrossRef] [PubMed]
    [Google Scholar]
  96. Sheng L. , Gu D. , Wang Q. , Liu Q. , Zhang Y. . ( 2012; ). Quorum sensing and alternative sigma factor RpoN regulate type VI secretion system I (T6SSVA1) in fish pathogen Vibrio alginolyticus . . Arch Microbiol 194:, 379–390. [CrossRef] [PubMed]
    [Google Scholar]
  97. Silby M. W. , Winstanley C. , Godfrey S. A. , Levy S. B. , Jackson R. W. . ( 2011; ). Pseudomonas genomes: diverse and adaptable. . FEMS Microbiol Rev 35:, 652–680. [CrossRef] [PubMed]
    [Google Scholar]
  98. Silverman J. M. , Austin L. S. , Hsu F. , Hicks K. G. , Hood R. D. , Mougous J. D. . ( 2011; ). Separate inputs modulate phosphorylation-dependent and -independent type VI secretion activation. . Mol Microbiol 82:, 1277–1290. [CrossRef] [PubMed]
    [Google Scholar]
  99. Sogin M. L. . ( 1991; ). Early evolution and the origin of eukaryotes. . Curr Opin Genet Dev 1:, 457–463. [CrossRef] [PubMed]
    [Google Scholar]
  100. Southey-Pillig C. J. , Davies D. G. , Sauer K. . ( 2005; ). Characterization of temporal protein production in Pseudomonas aeruginosa biofilms. . J Bacteriol 187:, 8114–8126. [CrossRef] [PubMed]
    [Google Scholar]
  101. Srinivasa Rao P. S. , Lim T. M. , Leung K. Y. . ( 2003; ). Functional genomics approach to the identification of virulence genes involved in Edwardsiella tarda pathogenesis. . Infect Immun 71:, 1343–1351. [CrossRef] [PubMed]
    [Google Scholar]
  102. Starkey M. , Rahme L. G. . ( 2009; ). Modeling Pseudomonas aeruginosa pathogenesis in plant hosts. . Nat Protoc 4:, 117–124. [CrossRef] [PubMed]
    [Google Scholar]
  103. Suarez G. , Sierra J. C. , Sha J. , Wang S. , Erova T. E. , Fadl A. A. , Foltz S. M. , Horneman A. J. , Chopra A. K. . ( 2008; ). Molecular characterization of a functional type VI secretion system from a clinical isolate of Aeromonas hydrophila . . Microb Pathog 44:, 344–361. [CrossRef] [PubMed]
    [Google Scholar]
  104. Sun G. W. , Chen Y. , Liu Y. , Tan G. Y. , Ong C. , Tan P. , Gan Y. H. . ( 2010; ). Identification of a regulatory cascade controlling type III secretion system 3 gene expression in Burkholderia pseudomallei . . Mol Microbiol 76:, 677–689. [CrossRef] [PubMed]
    [Google Scholar]
  105. Syed K. A. , Beyhan S. , Correa N. , Queen J. , Liu J. , Peng F. , Satchell K. J. , Yildiz F. , Klose K. E. . ( 2009; ). The Vibrio cholerae flagellar regulatory hierarchy controls expression of virulence factors. . J Bacteriol 191:, 6555–6570. [CrossRef] [PubMed]
    [Google Scholar]
  106. Termine E. , Michel G. P. . ( 2009; ). Transcriptome and secretome analyses of the adaptive response of Pseudomonas aeruginosa to suboptimal growth temperature. . Int Microbiol 12:, 7–12.[PubMed]
    [Google Scholar]
  107. Unterweger D. , Kitaoka M. , Miyata S. T. , Bachmann V. , Brooks T. M. , Moloney J. , Sosa O. , Silva D. , Duran-Gonzalez J. et al. ( 2012; ). Constitutive type VI secretion system expression gives Vibrio cholerae intra- and interspecific competitive advantages. . PLoS ONE 7:, e48320. [CrossRef] [PubMed]
    [Google Scholar]
  108. Veesenmeyer J. L. , Hauser A. R. , Lisboa T. , Rello J. . ( 2009; ). Pseudomonas aeruginosa virulence and therapy: evolving translational strategies. . Crit Care Med 37:, 1777–1786. [CrossRef] [PubMed]
    [Google Scholar]
  109. Ventre I. , Goodman A. L. , Vallet-Gely I. , Vasseur P. , Soscia C. , Molin S. , Bleves S. , Lazdunski A. , Lory S. , Filloux A. . ( 2006; ). Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. . Proc Natl Acad Sci U S A 103:, 171–176. [CrossRef] [PubMed]
    [Google Scholar]
  110. Venturi V. . ( 2006; ). Regulation of quorum sensing in Pseudomonas . . FEMS Microbiol Rev 30:, 274–291. [CrossRef] [PubMed]
    [Google Scholar]
  111. Waldor M. K. , Mekalanos J. J. . ( 1996; ). Lysogenic conversion by a filamentous phage encoding cholera toxin. . Science 272:, 1910–1914. [CrossRef] [PubMed]
    [Google Scholar]
  112. Wang Q. , Yang M. , Xiao J. , Wu H. , Wang X. , Lv Y. , Xu L. , Zheng H. , Wang S. et al. ( 2009a; ). Genome sequence of the versatile fish pathogen Edwardsiella tarda provides insights into its adaptation to broad host ranges and intracellular niches. . PLoS ONE 4:, e7646. [CrossRef] [PubMed]
    [Google Scholar]
  113. Wang X. , Wang Q. , Xiao J. , Liu Q. , Wu H. , Xu L. , Zhang Y. . ( 2009b; ). Edwardsiella tarda T6SS component evpP is regulated by esrB and iron, and plays essential roles in the invasion of fish. . Fish Shellfish Immunol 27:, 469–477. [CrossRef] [PubMed]
    [Google Scholar]
  114. Wang X. , Wang Q. , Xiao J. , Liu Q. , Wu H. , Zhang Y. . ( 2010; ). Hemolysin EthA in Edwardsiella tarda is essential for fish invasion in vivo and in vitro and regulated by two-component system EsrA-EsrB and nucleoid protein HhaEt. . Fish Shellfish Immunol 29:, 1082–1091. [CrossRef] [PubMed]
    [Google Scholar]
  115. Wang M. , Luo Z. , Du H. , Xu S. , Ni B. , Zhang H. , Sheng X. , Xu H. , Huang X. . ( 2011; ). Molecular characterization of a functional type VI secretion system in Salmonella enterica serovar Typhi. . Curr Microbiol 63:, 22–31. [CrossRef] [PubMed]
    [Google Scholar]
  116. Weber B. , Hasic M. , Chen C. , Wai S. N. , Milton D. L. . ( 2009; ). Type VI secretion modulates quorum sensing and stress response in Vibrio anguillarum . . Environ Microbiol 11:, 3018–3028. [CrossRef] [PubMed]
    [Google Scholar]
  117. Weber B. , Lindell K. , El Qaidi S. , Hjerde E. , Willassen N. P. , Milton D. L. . ( 2011; ). The phosphotransferase VanU represses expression of four qrr genes antagonizing VanO-mediated quorum-sensing regulation in Vibrio anguillarum . . Microbiology 157:, 3324–3339. [CrossRef] [PubMed]
    [Google Scholar]
  118. Williams S. G. , Varcoe L. T. , Attridge S. R. , Manning P. A. . ( 1996; ). Vibrio cholerae Hcp, a secreted protein coregulated with HlyA. . Infect Immun 64:, 283–289.[PubMed]
    [Google Scholar]
  119. Yuan Z. C. , Liu P. , Saenkham P. , Kerr K. , Nester E. W. . ( 2008; ). 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 190:, 494–507. [CrossRef] [PubMed]
    [Google Scholar]
  120. Zhang W. , Xu S. , Li J. , Shen X. , Wang Y. , Yuan Z. . ( 2011; ). Modulation of a thermoregulated type VI secretion system by AHL-dependent quorum sensing in Yersinia pseudotuberculosis . . Arch Microbiol 193:, 351–363.[PubMed]
    [Google Scholar]
  121. Zheng J. , Leung K. Y. . ( 2007; ). Dissection of a type VI secretion system in Edwardsiella tarda . . Mol Microbiol 66:, 1192–1206. [CrossRef] [PubMed]
    [Google Scholar]
  122. Zheng J. , Tung S. L. , Leung K. Y. . ( 2005; ). Regulation of a type III and a putative secretion system in Edwardsiella tarda by EsrC is under the control of a two-component system, EsrA-EsrB. . Infect Immun 73:, 4127–4137. [CrossRef] [PubMed]
    [Google Scholar]
  123. Zheng J. , Shin O. S. , Cameron D. E. , Mekalanos J. J. . ( 2010; ). Quorum sensing and a global regulator TsrA control expression of type VI secretion and virulence in Vibrio cholerae . . Proc Natl Acad Sci U S A 107:, 21128–21133. [CrossRef] [PubMed]
    [Google Scholar]
  124. Zheng J. , Ho B. , Mekalanos J. J. . ( 2011; ). Genetic analysis of anti-amoebae and anti-bacterial activities of the type VI secretion system in Vibrio cholerae . . PLoS ONE 6:, e23876. [CrossRef] [PubMed]
    [Google Scholar]
  125. Zhou Y. , Tao J. , Yu H. , Ni J. , Zeng L. , Teng Q. , Kim K. S. , Zhao G. P. , Guo X. , Yao Y. . ( 2012; ). Hcp family proteins secreted via the type VI secretion system coordinately regulate Escherichia coli K1 interaction with human brain microvascular endothelial cells. . Infect Immun 80:, 1243–1251. [CrossRef] [PubMed]
    [Google Scholar]
  126. Zhu J. , Miller M. B. , Vance R. E. , Dziejman M. , Bassler B. L. , Mekalanos J. J. . ( 2002; ). Quorum-sensing regulators control virulence gene expression in Vibrio cholerae . . Proc Natl Acad Sci U S A 99:, 3129–3134. [CrossRef] [PubMed]
    [Google Scholar]
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