Structure and regulation of the type VI secretion system

Annual Review of Microbiology

Volumn 66, Issue , 2012, Pages 453-472

  Silverman, Julie M ^a   Brunet, Yannick R ^b   Cascales, Eric ^b   Mougous, Joseph D ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b CNRS and Aix Marseille University   (France)

Author keywords

bacteriophage; host cell interactions; interbacterial interactions; macromolecular; regulation

Indexed keywords

BACTERIOPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PROTEIN STRUCTURE; QUORUM SENSING; REVIEW;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; GRAM-NEGATIVE BACTERIA; MEMBRANE TRANSPORT PROTEINS; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; PROTEIN MULTIMERIZATION;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 84867899841     PISSN: 00664227     EISSN: 15453251     Source Type: Book Series    
DOI: 10.1146/annurev-micro-121809-151619     Document Type: Review

References (122)

1. Abuladze NK, Gingery M, Tsai J, Eiserling FA. 1994. Tail length determination in bacteriophage T4. Virology 199:301-10
2. Aksyuk AA, Leiman PG, Kurochkina LP, Shneider MM, Kostyuchenko VA, et al. 2009. The tail sheath structure of bacteriophage T4: a molecular machine for infecting bacteria. EMBO J. 28:821-29
3. Alvarez-Martinez CE, Christie PJ. 2009. Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. Rev. 73:775-808
4. Aschtgen MS, Bernard CS, De Bentzmann S, Lloubes R, Cascales E. 2008. SciN is an outer membrane lipoprotein required for type VI secretion in enteroaggregative Escherichia coli. J. Bacteriol. 190:7523-31
5. Aschtgen MS, Gavioli M, Dessen A, Lloubes R, Cascales E. 2010. The SciZ protein anchors the enteroaggregative Escherichia coli type VI secretion system to the cell wall. Mol. Microbiol. 75:886-99
6. Aschtgen MS, Thomas MS, Cascales E. 2010. Anchoring the type VI secretion system to the peptidoglycan: TssL, TagL, TagP. .. what else? Virulence 1:535-40
7. Aschtgen MS, Zoued A, Lloub̀es R, Journet L, Cascales E. 2012. The C-tail anchored TssL subunit, an essential protein of the enteroaggregative Escherichia coli Sci-1 Type VI secretion system, is inserted by YidC. Microbiol. Open 1:71-82
8. Aubert D, MacDonald DK, Valvano MA. 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. 285:35988-98
9. Ballister ER, Lai AH, Zuckermann RN, Cheng Y, Mougous JD. 2008. In vitro self-assembly of tailorable nanotubes from a simple protein building block. Proc. Natl. Acad. Sci. USA 105:3733-38
10. Basler M, PilhoferM, Henderson GP, JensenGJ, Mekalanos JJ. 2012. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483:182-86
11. Bernard CS, Brunet YR, Gavioli M, Lloubes R, Cascales E. 2011. Regulation of type VI secretion gene clusters by σ54 and cognate enhancer binding proteins. J. Bacteriol. 193:2158-67
12. Bernard CS, Brunet YR, Gueguen E, Cascales E. 2010. Nooks and crannies in type VI secretion regulation. J. Bacteriol. 192:3850-60
13. Bingle LE, Bailey CM, Pallen MJ. 2008. Type VI secretion: a beginner's guide. Curr. Opin. Microbiol. 11:3-8
14. Bonemann G, Pietrosiuk A, Diemand A, ZentgrafH, Mogk A. 2009. Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J. 28:315-25
15. Bonemann G, Pietrosiuk A, Mogk A. 2010. Tubules and donuts: a type VI secretion story. Mol. Microbiol. 76:815-21
16. Boyer F, FichantG, Berthod J, Vandenbrouck Y, Attree I. 2009. Dissecting the bacterial typeVI secretion system by a genome wide in silico analysis: What can be learned from available microbial genomic resources? BMC Genomics 10:104
17. Brencic A, Lory S. 2009. Determination of the regulon and identification of novel mRNA targets of Pseudomonas aeruginosa RsmA. Mol. Microbiol. 72:612-32
18. Brencic A, McFarland KA, McManus HR, Castang S, Mogno I, et al. 2009. The GacS/GacA signal transduction system of Pseudomonas aeruginosa acts exclusively through its control over the transcription of the RsmY and RsmZ regulatory small RNAs. Mol. Microbiol. 73:434-45
19. Br̈oms JE, Lavander M, Sj ̈ ostedt A. 2009. A conserved α-helix essential for type VI secretion-like system on Francisella tularensis. J. Bacteriol. 8:2431-46
20. Brunet YR, Bernard CS, GavioliM, Lloubes 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
21. Calderwood SB, Mekalanos JJ. 1987. Iron regulation of Shiga-like toxin expression in Escherichia coli is mediated by the fur locus. J. Bacteriol. 169:4759-64
22. Campoy S, Jara M, Busquets N, de Rozas AM, Badiola I, Barbe J. 2002. Intracellular cyclic AMP concentration is decreased in Salmonella typhimurium fur mutants. Microbiology 148:1039-48
23. Carpenter BM, Whitmire JM, Merrell DS. 2009. This is not your mother's repressor: the complex role of fur in pathogenesis. Infect. Immun. 77:2590-601
24. Cascales E. 2008. The type VI secretion toolkit. EMBO Rep. 9:735-41
25. Cascales E, Cambillau C. 2012. Structural biology of type VI secretion systems. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367:1102-11
26. Chakraborty S, Sivaraman J, Leung KY, Mok YK. 2011. Two-component PhoB-PhoR regulatory system and ferric uptake regulator sense phosphate and iron to control virulence genes in type III andVI secretion systems of Edwardsiella tarda. J. Biol. Chem. 286:39417-30
27. Cornelis GR. 2006. The type III secretion injectisome. Nat. Rev. Microbiol. 4:811-25
28. Cornelis GR, Agrain C, Sorg I. 2006. Length control of extended protein structures in bacteria and bacteriophages. Curr. Opin. Microbiol. 9:201-6
29. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-22
30. Cotter P. 2011. Microbiology: Molecular syringes scratch the surface. Nature 475:301-3
31. Das S, Chakrabortty A, Banerjee R, Chaudhuri K. 2002. Involvement of in vivo induced icmF gene of Vibrio cholerae in motility, adherence to epithelial cells, and conjugation frequency. Biochem. Biophys. Res. Commun. 295:922-28
32. de Pace F, Boldrin de Paiva J, Nakazato G, Lancellotti M, Sircili MP, et al. 2011. Characterization of IcmF of the type VI secretion system in an avian pathogenic Escherichia coli (APEC) strain. Microbiology 157:2954-62
33. Dubuis C, Haas D. 2007. Cross-species GacA-controlled induction of antibiosis in pseudomonads. Appl. Environ. Microbiol. 73:650-54
34. Dudley EG, Thomson NR, Parkhill J, Morin NP, Nataro JP. 2006. Proteomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity island in enteroaggregative Escherichia coli. Mol. Microbiol. 61:1267-82
35. Durand E, Zoued A, Spinelli S, Watson PJ, Aschtgen MS, et al. 2012. Structural characterization and oligomerization of the TssL protein, a component shared by bacterial type VI and type IVb secretion systems. J. Biol. Chem. 287:14157-68
36. Ellermeier JR, Slauch JM. 2008. Fur regulates expression of the Salmonella pathogenicity island 1 type III secretion system through HilD. J. Bacteriol. 190:476-86
37. Enos-Berlage JL, Guvener ZT, Keenan CE, McCarter LL. 2005. Genetic determinants of biofilm development of opaque and translucent Vibrio parahaemolyticus. Mol. Microbiol. 55:1160-82
38. Federle MJ, Bassler BL. 2003. Interspecies communication in bacteria. J. Clin. Invest. 112:1291-99
39. Felisberto-Rodrigues C, Durand E, Aschtgen MS, Blangy S, Ortiz-Lombardia M, et al. 2011. Towards a structural comprehension of bacterial type VI secretion systems: characterization of the TssJ-TssM complex of an Escherichia coli pathovar. PLoS Pathog. 7:e1002386
40. Feng J, Atkinson MR, McCleary W, Stock JB, Wanner BL, Ninfa AJ. 1992. Role of phosphorylated metabolic intermediates in the regulation of glutamine synthetase synthesis in Escherichia coli. J. Bacteriol. 174:6061-70
41. Fronzes R, Christie PJ, Waksman G. 2009. The structural biology of type IV secretion systems. Nat. Rev. Microbiol. 7:703-14
42. Fuqua C, Parsek MR, Greenberg EP. 2001. Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu. Rev. Genet. 35:439-68
43. Gode-Potratz CJ, McCarter LL. 2011. Quorum sensing and silencing in Vibrio parahaemolyticus. J. Bacteriol. 193:4224-37
44. Gooderham WJ, Hancock RE. 2009. Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. FEMS Microbiol. Rev. 33:279-94
45. GoodmanAL, KulasekaraB, Rietsch A, Boyd D, SmithRS, Lory S. 2004. Asignaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev. Cell 7:745-54
46. Hachani A, Lossi NS, Hamilton A, JonesC, Bleves S, et al. 2011. TypeVI secretion system in Pseudomonas aeruginosa: secretion and multimerization of VgrG proteins. J. Biol. Chem. 286:12317-27
47. Hall HK, Foster JW. 1996. The role of fur in the acid tolerance response of Salmonella typhimurium is physiologically and genetically separable from its role in iron acquisition. J. Bacteriol. 178:5683-91
48. Harrington SM, Dudley EG, Nataro JP. 2006. Pathogenesis of enteroaggregative Escherichia coli infection. FEMS Microbiol. Lett. 254:12-18
49. Hassan KA, Johnson A, Shaffer BT, Ren Q, Kidarsa TA, et al. 2010. Inactivation of the GacA response regulator in Pseudomonas fluorescens Pf-5 has far-reaching transcriptomic consequences. Environ. Microbiol. 12:899-915
50. Hassett DJ, Sokol PA, Howell ML, Ma JF, Schweizer HT, et al. 1996. Ferric uptake regulator (Fur) mutants of Pseudomonas aeruginosa demonstrate defective siderophore-mediated iron uptake, altered aerobic growth, and decreased superoxide dismutase and catalase activities. J. Bacteriol. 178:3996-4003
51. Hayes CS, Aoki SK, Low DA. 2010. Bacterial contact-dependent delivery systems. Annu. Rev. Genet. 44:71-90
52. Hense BA, Kuttler C, Muller J, Rothballer M, Hartmann A, Kreft JU. 2007. Does efficiency sensing unify diffusion and quorum sensing? Nat. Rev. Microbiol. 5:230-39
53. Hood RD, Singh P, Hsu F, Guvener T, Carl MA, et al. 2010. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7:25-37
54. Hsu F, Schwarz S, Mougous JD. 2009. TagR promotes PpkA-catalysed type VI secretion activation in Pseudomonas aeruginosa. Mol. Microbiol. 72:1111-25
55. Ikeda JS, Janakiraman A, Kehres DG, Maguire ME, Slauch JM. 2005. Transcriptional regulation of sitABCD of Salmonella enterica serovar Typhimurium by MntR and Fur. J. Bacteriol. 187:912-22
56. Ishikawa T, Rompikuntal PK, Lindmark B, Milton DL, Wai SN. 2009. Quorum sensing regulation of the two hcp alleles in Vibrio cholerae O1 strains. PLoS One 4:e6734
57. Ishikawa T, Sabharwal D, Broms J, Milton DL, Sjostedt A, et al. 2012. Pathoadaptive conditional regulation of the type VI secretion system in Vibrio cholerae O1 strains. Infect. Immun. 80:575-84
58. Janakiraman A, Slauch JM. 2000. The putative iron transport system SitABCD encoded on SPI1 is required for full virulence of Salmonella typhimurium. Mol. Microbiol. 35:1146-55
59. Jani AJ, Cotter PA. 2010. Type VI secretion: not just for pathogenesis anymore. Cell Host Microbe 8:2-6
60. Jobichen C, Chakraborty S, Li M, Zheng J, Joseph L, et al. 2010. Structural basis for the secretion of EvpC: a key type VI secretion system protein from Edwardsiella tarda. PLoS One 5:e12910
61. Kanamaru S. 2009. Structural similarity of tailed phages and pathogenic bacterial secretion systems. Proc. Natl. Acad. Sci. USA 106:4067-68
62. Kanamaru S, Leiman PG, Kostyuchenko VA, Chipman PR, Mesyanzhinov VV, et al. 2002. Structure of the cell-puncturing device of bacteriophage T4. Nature 415:553-57
63. Katsura I, Hendrix RW. 1984. Length determination in bacteriophage lambda tails. Cell 39:691-98
64. Khajanchi BK, Sha J, Kozlova EV, Erova TE, SuarezG, et al. 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 155:3518-31
65. King J. 1971. Bacteriophage T4 tail assembly: four steps in core formation. J. Mol. Biol. 58:693-709
66. KitaokaM, Miyata ST, BrooksTM, UnterwegerD, Pukatzki S. 2011. VasH is a transcriptional regulator of the typeVI secretion system functional in endemic and pandemic Vibrio cholerae. J. Bacteriol. 193:6471-82
67. Lapouge K, Schubert M, Allain FH, Haas D. 2008. Gac/Rsm signal transduction pathway of γ-proteobacteria: from RNA recognition to regulation of social behaviour. Mol. Microbiol. 67:241-53
68. Leiman PG, Basler M, Ramagopal UA, Bonanno JB, Sauder JM, et al. 2009. Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc. Natl. Acad. Sci. USA 106:4154-59
69. Lesic B, Starkey M, He J, Hazan R, Rahme LG. 2009. Quorum sensing differentially regulates Pseudomonas aeruginosa type VI secretion locus I and homologous loci II and III, which are required for pathogenesis. Microbiology 155:2845-55
70. Leung KY, Siame BA, Snowball H, Mok YK. 2011. Type VI secretion regulation: crosstalk and intracellular communication. Curr. Opin. Microbiol. 14:9-15
71. Liu H, Coulthurst SJ, Pritchard L, Hedley PE, Ravensdale M, et al. 2008. Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathog. 4:e1000093
72. Lossi NS, Dajani R, Freemont P, Filloux A. 2011. Structure-function analysis of HsiF, a gp25-like component of the type VI secretion system, in Pseudomonas aeruginosa. Microbiology 157:3292-305
73. Ma AT, McAuley S, Pukatzki S, Mekalanos JJ. 2009. Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5:234-43
74. Ma LS, Lin JS, Lai EM. 2009. An IcmF family protein, ImpLM, is an integral inner membrane protein interacting with ImpKL, and itsWalker A motif is required for type VI secretion system-mediated Hcp secretion in Agrobacterium tumefaciens. J. Bacteriol. 191:4316-29
75. Ma LS, Narberhaus F, Lai EM. 2012. IcmF family protein TssM exhibits ATPase activity and energizes type VI secretion. J. Biol. Chem. 287:15610-21
76. MacIntyre DL, Miyata ST, Kitaoka M, Pukatzki S. 2010. The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc. Natl. Acad. Sci. USA 107:19520-24
77. McCleary WR, Stock JB, Ninfa AJ. 1993. Is acetyl phosphate a global signal in Escherichia coli? J. Bacteriol. 175:2793-98
78. Meezan E, Wood WB. 1971. The sequence of gene product interaction in bacteriophage T4 tail core assembly. J. Mol. Biol. 58:685-92
79. Miyata ST, Kitaoka M, Brooks TM, McAuley SB, Pukatzki S. 2011. Vibrio cholerae requires the type VI secretion system virulence factor VasX to kill Dictyostelium discoideum. Infect. Immun. 79:2941-49
80. Moore MM, Fernandez DL, Thune RL. 2002. Cloning and characterization of Edwardsiella ictaluri proteins expressed and recognized by the channel catfish Ictalurus punctatus immune response during infection. Dis. Aquat. Organ. 52:93-107
81. Mougous JD, Cuff ME, Raunser S, Shen A, Zhou M, et al. 2006. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312:1526-30
82. Mougous JD, Gifford CA, Ramsdell TL, Mekalanos JJ. 2007. Threonine phosphorylation posttranslationally regulates protein secretion in Pseudomonas aeruginosa. Nat. Cell Biol. 9:797-803
83. Nagai H, Kubori T. 2011. Type IVB secretion systems of Legionella and other gram-negative bacteria. Front. Microbiol. 2:136
84. Nataro JP, Kaper JB. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201
85. Ng WL, Bassler BL. 2009. Bacterial quorum-sensing network architectures. Annu. Rev. Genet. 43:197-222
86. Osipiuk J, Xu X, Cui H, Savchenko A, Edwards A, Joachimiak A. 2011. Crystal structure of secretory protein Hcp3 from Pseudomonas aeruginosa. J. Struct. Funct. Genomics 12:21-26
87. Parsek MR, Greenberg EP. 2005. Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol. 13:27-33
88. Pell LG, Kanelis V, Donaldson LW, Howell PL, Davidson AR. 2009. The phage lambda major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system. Proc. Natl. Acad. Sci. USA 106:4160-65
89. Pukatzki S, Ma AT, Revel AT, Sturtevant D, Mekalanos JJ. 2007. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc. Natl. Acad. Sci. USA 104:15508-13
90. Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, et al. 2006. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl. Acad. Sci. USA 103:1528-33
91. RaoVA, Shepherd SM, EnglishG, Coulthurst SJ, HunterWN. 2011. The structure of Serratiamarcescens Lip, a membrane-bound component of the type VI secretion system. Acta Crystallogr. D 67:1065-72
92. RappasM, BoseD, Zhang X. 2007. Bacterial enhancer-binding proteins: unlocking σ54-dependent gene transcription. Curr. Opin. Struct. Biol. 17:110-16
93. Rashid RA, Tarr PI, Moseley SL. 2006. Expression of the Escherichia coli IrgA homolog adhesin is regulated by the ferric uptake regulation protein. Microb. Pathog. 41:207-17
94. Records AR. 2011. The type VI secretion system: a multipurpose delivery system with a phage-like machinery. Mol. Plant Microbe Interact. 24:751-57
95. Records AR, Gross DC. 2010. Sensor kinases RetS and LadS regulate Pseudomonas syringae type VI secretion and virulence factors. J. Bacteriol. 192:3584-96
96. Rogge ML, Thune RL. 2011. Regulation of the Edwardsiella ictaluri type III secretion system by pH and phosphate concentration through EsrA, EsrB, and EsrC. Appl. Environ. Microbiol. 77:4293-302
97. Rossmann MG, Mesyanzhinov VV, Arisaka F, Leiman PG. 2004. The bacteriophage T4 DNA injection machine. Curr. Opin. Struct. Biol. 14:171-80
98. Russell AB, Hood RD, Bui NK, LeRoux M, Vollmer W, Mougous JD. 2011. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475:343-47
99. Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG. 2002. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184:1140-54
100. Schlenker C, Surawicz CM. 2009. Emerging infections of the gastrointestinal tract. Best Pract. Res. Clin. Gastroenterol. 23:89-99
101. Schumacher J, Joly N, RappasM, Zhang X, Buck M. 2006. Structures and organisation ofAAA+enhancer binding proteins in transcriptional activation. J. Struct. Biol. 156:190-99
102. Schwarz S, Hood RD, Mougous JD. 2010. What is type VI secretion doing in all those bugs? Trends Microbiol. 18:531-37
103. Schwarz S, West TE, Boyer F, ChiangWC, Carl MA, et al. 2010. Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog. 6(8):e1001068
104. Shingler V. 1996. Signal sensing by σ54-dependent regulators: derepression as a control mechanism. Mol. Microbiol. 19:409-16
105. Silverman JM, Austin LS, Hsu F, Hicks KG, Hood RD, Mougous JD. 2011. Separate inputs modulate phosphorylation-dependent and-independent type VI secretion activation. Mol. Microbiol. 82:1277-90
106. Suarez G, Sierra JC, Erova TE, Sha J, Horneman AJ, Chopra AK. 2010. A type VI secretion system effector protein VgrG1 from Aeromonas hydrophila that induces host cell toxicity by ADP-ribosylation of actin. J. Bacteriol. 192:155-68
107. Taylor DN, Bourgeois AL, Ericsson CD, Steffen R, Jiang ZD, et al. 2006. A randomized, double-blind, multicenter study of rifaximin compared with placebo andwith ciprofloxacin in the treatment of travelers' diarrhea. Am. J. Trop. Med. Hyg. 74:1060-66
108. Ventre I, GoodmanAL, Vallet-Gely I, Vasseur P, Soscia C, et al. 2006. Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc. Natl. Acad. Sci. USA 103:171-76
109. Waksman G, Fronzes R. 2010. Molecular architecture of bacterial type IV secretion systems. Trends Biochem. Sci. 35:691-98
110. Wang Q, Frye JG, McClelland M, Harshey RM. 2004. Gene expression patterns during swarming in Salmonella typhimurium: genes specific to surface growth and putative new motility and pathogenicity genes. Mol. Microbiol. 52:169-87
111. Wang X, Wang Q, Xiao J, LiuQ, WuH, et al. 2009. Edwardsiella tarda T6SS component evpP is regulated by esrB and iron, and plays essential roles in the invasion of fish. Fish Shellfish Immunol. 27:469-77
112. Weber B, Hasic M, Chen C, Wai SN, Milton DL. 2009. Type VI secretion modulates quorum sensing and stress response in Vibrio anguillarum. Environ. Microbiol. 11:3018-28
113. Weiss V, Magasanik B. 1988. Phosphorylation of nitrogen regulator I (NRI) of Escherichia coli. Proc. Natl. Acad. Sci. USA 85:8919-23
114. Worrall LJ, Lameignere E, Strynadka NC. 2011. Structural overview of the bacterial injectisome. Curr. Opin. Microbiol. 14:3-8
115. Xu H, Hoover TR. 2001. Transcriptional regulation at a distance in bacteria. Curr. Opin. Microbiol. 4:138-44
116. Yahr TL, Greenberg EP. 2004. The genetic basis for the commitment to chronic versus acute infection in Pseudomonas aeruginosa. Mol. Cell 16:497-98
117. YapML, Mio K, Ali S, Minton A, Kanamaru S, Arisaka F. 2010. Sequential assembly of the wedge of the baseplate of phage T4 in the presence and absence of gp11 as monitored by analytical ultracentrifugation. Macromol. Biosci. 10:808-13
118. Zhang L, Hinz AJ, Nadeau JP, Mah TF. 2011. Pseudomonas aeruginosa tssC1 links type VI secretion and biofilm-specific antibiotic resistance. J. Bacteriol. 193:5510-13
119. ZhangW, Xu S, Li J, ShenX, Wang Y, Yuan Z. 2011. Modulation of a thermoregulated typeVI secretion system by AHL-dependent quorum sensing in Yersinia pseudotuberculosis. Arch. Microbiol. 193:351-63
120. Zheng J, Ho B, Mekalanos JJ. 2011. Genetic analysis of anti-amoebae and anti-bacterial activities of the type VI secretion system in Vibrio cholerae. PLoS One 6:e23876
121. Zheng J, Leung KY. 2007. Dissection of a type VI secretion system in Edwardsiella tarda. Mol. Microbiol. 66:1192-206
122. Zheng J, Shin OS, Cameron DE, Mekalanos JJ. 2010. Quorum sensing and a global regulator TsrA control expression of type VI secretion and virulence in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 107:21128-33