Type VI secretion system effectors: Poisons with a purpose

Nature Reviews Microbiology

Volumn 12, Issue 2, 2014, Pages 137-148

  Russell, Alistair B ^a   Peterson, S Brook ^a   Mougous, Joseph D ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; NUCLEIC ACID; POISON;

BACTERIAL CELL WALL; BACTERIAL PHENOMENA AND FUNCTIONS; CELL MEMBRANE; CELL WALL; COMMUNITY STRUCTURE; ENVIRONMENTAL HEALTH; HUMAN; INFECTION; MICROBIAL COMMUNITY; ORGANISMAL INTERACTION; PRIORITY JOURNAL; PROTEOBACTERIA; REVIEW; SOCIAL BEHAVIOR; TYPE IV SECRETION SYSTEM; TYPE VI SECRETION SYSTEM;

BACTERIA (MICROORGANISMS); NEGIBACTERIA;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; GRAM-NEGATIVE BACTERIA; HUMANS; MICROBIAL INTERACTIONS; VIRULENCE FACTORS;

EID: 84892670882     PISSN: 17401526     EISSN: 17401534     Source Type: Journal    
DOI: 10.1038/nrmicro3185     Document Type: Review

References (146)

1. Roesch, L. F. et al. Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J. 1, 283-290 (2007).
2. Kostic, A. D., Howitt, M. R. & Garrett, W. S. Exploring host-microbiota interactions in animal models and humans. Genes Dev. 27, 701-718 (2013).
3. Overmann, J. The phototrophic consortium "Chlorochromatium aggregatum"-a model for bacterial heterologous multicellularity. Adv. Exp. Med. Biol. 675, 15-29 (2010).
4. Baker, B. J. & Banfield, J. F. Microbial communities in acid mine drainage. FEMS Microbiol. Ecol. 44, 139-152 (2003).
5. Dekas, A. E., Poretsky, R. S. & Orphan, V. J. Deep-sea archaea fix and share nitrogen in methane-consuming microbial consortia. Science 326, 422-426 (2009).
6. Boetius, A. et al. A marine microbial consortium apparently mediating anaerobic oxidation of methane. Nature 407, 623-626 (2000).
7. Strom, S. L. Microbial ecology of ocean biogeochemistry: a community perspective. Science 320, 1043-1045 (2008).
8. Belda-Ferre, P. et al. The oral metagenome in health and disease. ISME J. 6, 46-56 (2012).
9. Nielsen, P. H., Saunders, A. M., Hansen, A. A., Larsen, P. & Nielsen, J. L. Microbial communities involved in enhanced biological phosphorus removal from wastewater-a model system in environmental biotechnology. Curr. Opin. Biotechnol. 23, 452-459 (2012).
10. Hood, R. D. et al. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7, 25-37 (2010).
11. Schwarz, S., Hood, R. D. & Mougous, J. D. What is type VI secretion doing in all those bugs? Trends Microbiol. 18, 531-537 (2010).
12. 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 10, 104 (2009).
13. Shalom, G., Shaw, J. G. & Thomas, M. S. 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 (2007).
14. Schwarz, S. et al. Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog. 6, e1001068 (2010).
15. Russell, A. B. et al. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475, 343-347 (2011).
16. English, G. et al. New secreted toxins and immunity proteins encoded within the Type VI secretion system gene cluster of Serratia marcescens. Mol. Microbiol. 86, 921-936 (2012).
17. Dong, T. G., Ho, B. T., Yoder-Himes, D. R. & Mekalanos, J. J. Identification of T6SS-dependent effector and immunity proteins by Tn-seq in Vibrio cholerae. Proc. Natl Acad. Sci. USA 110, 2623-2628 (2013).
18. Brooks, T. M., Unterweger, D., Bachmann, V., Kostiuk, B. & Pukatzki, S. Lytic activity of the Vibrio cholerae type VI secretion toxin VgrG-3 is inhibited by the antitoxin TsaB. J. Biol. Chem. 288, 7618-7625 (2013).
19. Russell, A. B. et al. A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe 11, 538-549 (2012).
20. Benz, J., Sendlmeier, C., Barends, T. R. & Meinhart, A. Structural insights into the effector-immunity system Tse1/Tsi1 from Pseudomonas aeruginosa. PLoS ONE 7, e40453 (2012).
21. Zhang, H. et al. Structure of the type VI effector-immunity complex (Tae4-Tai4) provides novel insights into the inhibition mechanism of the effector by its immunity protein. J. Biol. Chem. 288, 5928-5939 (2013).
22. Vollmer, W., Pilsl, H., Hantke, K., Holtje, J. V. & Braun, V. Pesticin displays muramidase activity. J. Bacteriol. 179, 1580-1583 (1997).
23. Browder, H. P., Zygmunt, W. A., Young, J. R. & Tavormina, P. A. Lysostaphin: enzymatic mode of action. Biochem. Biophys. Res. Commun. 19, 383-389 (1965).
24. El Ghachi, M. et al. Colicin M exerts its bacteriolytic effect via enzymatic degradation of undecaprenyl phosphate-linked peptidoglycan precursors. J. Biol. Chem. 281, 22761-22772 (2006).
25. Kong, K. F., Schneper, L. & Mathee, K. Beta-lactam antibiotics: from antibiosis to resistance and bacteriology. APMIS 118, 1-36 (2010).
26. Reynolds, P. E. Structure, biochemistry and mechanism of action of glycopeptide antibiotics. Eur. J. Clin. Microbiol. Infect. Dis. 8, 943-950 (1989).
27. Chou, S. et al. Structure of a peptidoglycan amidase effector targeted to Gram-negative bacteria by the type VI secretion system. Cell Rep. 1, 656-664 (2012).
28. Ding, J., Wang, W., Feng, H., Zhang, Y. & Wang, D. C. Structural insights into the Pseudomonas aeruginosa type VI virulence effector Tse1 bacteriolysis and self-protection mechanisms. J. Biol. Chem. 287, 26911-26920 (2012).
29. Zhang, H., Gao, Z.-Q., Su, X.-D. & Dong, Y.-H. Crystal structure of type VI effector Tse1 from Pseudomonas aeruginosa. FEBS Lett. 586, 3193-3199 (2012).
30. LeRoux, M. et al. Quantitative single-cell characterization of bacterial interactions reveals type VI secretion is a double-edged sword. Proc. Natl Acad. Sci. USA 109, 19804-19809 (2012).
31. Srikannathasan, V. et al. Structural basis for type VI secreted peptidoglycan DL-endopeptidase function, specificity and neutralization in Serratia marcescens. Acta Crystallogr. D Biol. Crystallogr. 69, 2468-2482 (2013).
32. Fischetti, V. A. Bacteriophage lysins as effective antibacterials. Curr. Opin. Microbiol. 11, 393-400 (2008).
33. Whitney, J. C. et al. Identification, structure and function of a novel type VI secretion peptidoglycan glycoside hydrolase effector-immunity pair. J. Biol. Chem. 288, 26616-26624 (2013).
34. Pukatzki, S., Ma, A. T., Revel, A. T., Sturtevant, D. & Mekalanos, J. J. 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, 15508-15513 (2007).
35. Suarez, G. et al. A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. J. Bacteriol. 192, 155-168 (2010).
36. Russell, A. B. et al. Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 496, 508-512 (2013).
37. Wilderman, P. J., Vasil, A. I., Johnson, Z. & Vasil, M. L. Genetic and biochemical analyses of a eukaryotic-like phospholipase D of Pseudomonas aeruginosa suggest horizontal acquisition and a role for persistence in a chronic pulmonary infection model. Mol. Microbiol. 39, 291-303 (2001).
38. Cascales, E. et al. Colicin biology. Microbiol. Mol. Biol. Rev. 71, 158-229 (2007).
39. Zheng, J., Ho, B. & Mekalanos, J. J. Genetic analysis of anti-amoebae and anti-bacterial activities of the type VI secretion system in Vibrio cholerae. PLoS ONE 6, e23876 (2011).
40. Miyata, S. T., Kitaoka, M., Brooks, T. M., McAuley, S. B. & Pukatzki, S. Vibrio cholerae requires the type VI secretion system virulence factor VasX to kill Dictyostelium discoideum. Infect. Immun. 79, 2941-2949 (2011).
41. Miyata, S.T., Unterweger, D., Rudko, S.P. & Pukatzki, S. Dual expression profile of type VI secretion system immunity genes protects pandemic Vibrio cholerae. PLoS Pathog. 9, e1003752 (2013).
42. Geli, V., Baty, D., Pattus, F. & Lazdunski, C. Topology and function of the integral membrane protein conferring immunity to colicin A. Mol. Microbiol. 3, 679-687 (1989).
43. Poole, S. J. et al. Identification of functional toxin/immunity genes linked to contact-dependent growth inhibition (CDI) and rearrangement hotspot (Rhs) systems. PLoS Genet. 7, e1002217 (2011).
44. Koskiniemi, S. et al. Rhs proteins from diverse bacteria mediate intercellular competition. Proc. Natl Acad. Sci. USA 110, 7032-7037 (2013).
45. Wenren, L. M., Sullivan, N. L., Cardarelli, L., Septer, A. N. & Gibbs, K. A. Two independent pathways for self-recognition in Proteus mirabilis are linked by type VI-dependent export. mBio 4, e00374-00313 (2013).
46. Fritsch, M. J. et al. Proteomic identification of novel secreted anti-bacterial toxins of the Serratia marcescens Type VI secretion system. Mol. Cell Proteom. 12, 2735-2749 (2013).
47. MacIntyre, D. L., Miyata, S. T., Kitaoka, M. & Pukatzki, S. The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc. Natl Acad. Sci. USA 107, 19520-19524 (2010).
48. Murdoch, S. L. et al. The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. J. Bacteriol. 193, 6057-6069 (2011).
49. Salomon, D., Gonzalez, H., Updegraff, B. L. & 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 8, e61086 (2013).
50. Gueguen, E. & Cascales, E. Promoter swapping unveils the role of the Citrobacter rodentium CTS1 type VI secretion system in interbacterial competition. Appl. Environ. Microbiol. 79, 32-38 (2013).
51. Haapalainen, M. et al. Hcp2, a secreted protein of the phytopathogen Pseudomonas syringae pv. tomato DC3000, is required for fitness for competition against bacteria and yeasts. J. Bacteriol. 194, 4810-4822 (2012).
52. Carruthers, M. D., Nicholson, P. A., Tracy, E. N. & Munson, R. S. Jr. Acinetobacter baumannii utilizes a type VI secretion system for bacterial competition. PLoS ONE 8, e59388 (2013).
53. Dong, C. et al. Structural insights into the inhibition of type VI effector Tae3 by its immunity protein Tai3. Biochem. J. 454, 59-68 (2013).
54. Cornforth, D. M. & Foster, K. R. Competition sensing: the social side of bacterial stress responses. Nature Rev. Microbiol. 11, 285-293 (2013).
55. Basler, M. & Mekalanos, J. J. Type 6 secretion dynamics within and between bacterial cells. Science 337, 815 (2012).
56. Lesic, B., Starkey, M., He, J., Hazan, R. & Rahme, L. G. 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 (2009).
57. Ishikawa, T., Rompikuntal, P. K., Lindmark, B., Milton, D. L. & Wai, S. N. Quorum sensing regulation of the two hcp alleles in Vibrio cholerae O1 strains. PLoS ONE 4, e6734 (2009).
58. Wu, C. F., Lin, J. S., Shaw, G. C. & Lai, E. M. Acidinduced type VI secretion system is regulated by ExoRChvG/ChvI signaling cascade in Agrobacterium tumefaciens. PLoS Pathog. 8, e1002938 (2012).
59. Robinson, J. B. et al. 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 (2009).
60. Brunet, Y. R., Bernard, C. S., Gavioli, M., Lloubes, R. & Cascales, E. An epigenetic switch involving overlapping fur and DNA methylation optimizes expression of a type VI secretion gene cluster. PLoS Genet. 7, e1002205 (2011).
61. Ishikawa, T. et al. Pathoadaptive conditional regulation of the type VI secretion system in Vibrio cholerae O1 strains. Infect. Immun. 80, 575-584 (2012).
62. Termine, E. & Michel, G. P. Transcriptome and secretome analyses of the adaptive response of Pseudomonas aeruginosa to suboptimal growth temperature. Int. Microbiol. 12, 7-12 (2009).
63. Tilman, D. Resource competition and community structure. Monogr. Popul. Biol. 17, 1-296 (1982).
64. Hawlena, H., Bashey, F., Mendes-Soares, H. & Lively, C. M. Spiteful interactions in a natural population of the bacterium Xenorhabdus bovienii. Am. Nat. 175, 374-381 (2010).
65. Vos, M. & Velicer, G. J. Social conflict in centimeterand global-scale populations of the bacterium Myxococcus xanthus. Curr. Biol. 19, 1763-1767 (2009).
66. Chantratita, N. et al. Genetic diversity and microevolution of Burkholderia pseudomallei in the environment. PLoS Negl Trop. Dis. 2, e182 (2008).
67. Gibbs, K. A., Urbanowski, M. L. & Greenberg, E. P. Genetic determinants of self identity and social recognition in bacteria. Science 321, 256-259 (2008).
68. Riley, M. A. & Wertz, J. E. Bacteriocins: evolution, ecology, and application. Annu. Rev. Microbiol. 56, 117-137 (2002).
69. Eldar, A. Social conflict drives the evolutionary divergence of quorum sensing. Proc. Natl Acad. Sci. USA 108, 13635-13640 (2011).
70. Strassmann, J. E., Gilbert, O. M. & Queller, D. C. Kin discrimination and cooperation in microbes. Annu. Rev. Microbiol. 65, 349-367 (2011).
71. Ruhe, Z. C., Low, D. A. & Hayes, C. S. Bacterial contact-dependent growth inhibition. Trends Microbiol. 21, 230-237 (2013).
72. Unterweger, D. et al. Constitutive type VI secretion system expression gives Vibrio cholerae intra-and interspecific competitive advantages. PLoS ONE 7, e48320 (2012).
73. Zhang, W. et al. Modulation of a thermoregulated type VI secretion system by AHL-dependent quorum sensing in Yersinia pseudotuberculosis. Arch. Microbiol. 193, 351-363 (2011).
74. Bernard, C. S., Brunet, Y. R., Gueguen, E. & Cascales, E. Nooks and crannies in type VI secretion regulation. J. Bacteriol. 192, 3850-3860 (2010).
75. Nadell, C. D., Foster, K. R. & Xavier, J. B. Emergence of spatial structure in cell groups and the evolution of cooperation. PLoS Comput. Biol. 6, e1000716 (2010).
76. Engelberg-Kulka, H. & Glaser, G. Addiction modules and programmed cell death and antideath in bacterial cultures. Annu. Rev. Microbiol. 53, 43-70 (1999).
77. Yamaguchi, Y., Park, J. H. & Inouye, M. Toxin-antitoxin systems in bacteria and archaea. Annu. Rev. Genet. 45, 61-79 (2011).
78. Li, M. et al. Structural basis for type VI secretion effector recognition by a cognate immunity protein. PLoS Pathog. 8, e1002613 (2012).
79. Van Melderen, L. & Saavedra De Bast, M. Bacterial toxin-antitoxin systems: more than selfish entities? PLoS Genet. 5, e1000437 (2009).
80. Yamaguchi, Y. & Inouye, M. Regulation of growth and death in Escherichia coli by toxin-antitoxin systems. Nature Rev. Microbiol. 9, 779-790 (2011).
81. Frampton, R., Aggio, R. B., Villas-Boas, S. G., Arcus, V. L. & Cook, G. M. Toxin-antitoxin systems of Mycobacterium smegmatis are essential for cell survival. J. Biol. Chem. 287, 5340-5356 (2012).
82. Hazan, R. & Engelberg-Kulka, H. Escherichia coli mazEF-mediated cell death as a defense mechanism that inhibits the spread of phage P1. Mol. Genet. Genom. 272, 227-234 (2004).
83. Gerdes, K. & Maisonneuve, E. Bacterial persistence and toxin-antitoxin loci. Annu. Rev. Microbiol. 66, 103-123 (2012).
84. Maisonneuve, E., Castro-Camargo, M. & Gerdes, K. PPGpp controls bacterial persistence by stochastic induction of toxin-antitoxin activity. Cell 154, 1140-1150 (2013).
85. Stoodley, P., Sauer, K., Davies, D. G. & Costerton, J. W. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56, 187-209 (2002).
86. Parsek, M. R. & Greenberg, E. P. Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol. 13, 27-33 (2005).
87. Blango, M. G. & Mulvey, M. A. Bacterial landlines: contact-dependent signaling in bacterial populations. Curr. Opin. Microbiol. 12, 177-181 (2009).
88. Fagotto, F. & Gumbiner, B. M. Cell contact-dependent signaling. Dev. Biol. 180, 445-454 (1996).
89. Downing, K. J. et al. Mutants of Mycobacterium tuberculosis lacking three of the five rpf-like genes are defective for growth in vivo and for resuscitation in vitro. Infect. Immun. 73, 3038-3043 (2005).
90. Mukamolova, G. V. et al. Muralytic activity of Micrococcus luteus Rpf and its relationship to physiological activity in promoting bacterial growth and resuscitation. Mol. Microbiol. 59, 84-98 (2006).
91. Mukamolova, G. V. et al. The rpf gene of Micrococcus luteus encodes an essential secreted growth factor. Mol. Microbiol. 46, 611-621 (2002).
92. Ravagnani, A., Finan, C. L. & Young, M. A novel firmicute protein family related to the actinobacterial resuscitation-promoting factors by non-orthologous domain displacement. BMC Genomics 6, 39 (2005).
93. West, S. A., Griffin, A. S. & Gardner, A. Evolutionary explanations for cooperation. Curr. Biol. 17, R661-R672 (2007).
94. Diggle, S. P., Griffin, A. S., Campbell, G. S. & West, S. A. Cooperation and conflict in quorum-sensing bacterial populations. Nature 450, 411-414 (2007).
95. Lapouge, K., Schubert, M., Allain, F. H. & Haas, D. Gac/Rsm signal transduction pathway of.-proteobacteria: from RNA recognition to regulation of social behaviour. Mol. Microbiol. 67, 241-253 (2008).
96. Hassan, K. A. et al. Inactivation of the GacA response regulator in Pseudomonas fluorescens Pf-5 has farreaching transcriptomic consequences. Environ. Microbiol. 12, 899-915 (2010).
97. Mougous, J. D. et al. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312, 1526-1530 (2006).
98. Enos-Berlage, J. L., Guvener, Z. T., Keenan, C. E. & McCarter, L. L. Genetic determinants of biofilm development of opaque and translucent Vibrio parahaemolyticus. Mol. Microbiol. 55, 1160-1182 (2005).
99. Aschtgen, M. S., Bernard, C. S., De Bentzmann, S., Lloubes, R. & Cascales, E. SciN is an outer membrane lipoprotein required for type VI secretion in enteroaggregative Escherichia coli. J. Bacteriol. 190, 7523-7531 (2008).
100. Sha, J. et al. Evaluation of the roles played by Hcp and VgrG type 6 secretion system effectors in Aeromonas hydrophila SSU pathogenesis. Microbiology 159, 1120-1135 (2013).
101. Webb, J. S., Givskov, M. & Kjelleberg, S. Bacterial biofilms: prokaryotic adventures in multicellularity. Curr. Opin. Microbiol. 6, 578-585 (2003).
102. Whitchurch, C. B., Tolker-Nielsen, T., Ragas, P. C. & Mattick, J. S. Extracellular DNA required for bacterial biofilm formation. Science 295, 1487 (2002).
103. Stewart, P. S. & Franklin, M. J. Physiological heterogeneity in biofilms. Nature Rev. Microbiol. 6, 199-210 (2008).
104. Otsuka, Y. & Yonesaki, T. Dmd of bacteriophage T4 functions as an antitoxin against Escherichia coli LsoA and RnlA toxins. Mol. Microbiol. 83, 669-681 (2012).
105. Corr, S. C. et al. Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. Proc. Natl Acad. Sci. USA 104, 7617-7621 (2007).
106. Dawid, S., Roche, A. M. & Weiser, J. N. The blp bacteriocins of Streptococcus pneumoniae mediate intraspecies competition both in vitro and in vivo. Infect. Immun. 75, 443-451 (2007).
107. Sekirov, I., Russell, S. L., Antunes, L. C. & Finlay, B. B. Gut microbiota in health and disease. Physiol. Rev. 90, 859-904 (2010).
108. Blondel, C. J., Jimenez, J. C., Contreras, I. & Santiviago, C. A. Comparative genomic analysis uncovers 3 novel loci encoding type six secretion systems differentially distributed in Salmonella serotypes. BMC Genomics 10, 354 (2009).
109. Suarez, G. et al. Molecular characterization of a functional type VI secretion system from a clinical isolate of Aeromonas hydrophila. Microb. Pathog. 44, 344-361 (2008).
110. Brunet, Y. R., Espinosa, L., Harchouni, S., Mignot, T. & Cascales, E. Imaging type VI secretion-mediated bacterial killing. Cell Rep. 3, 36-41 (2013).
111. Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. & Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220-230 (2012).
112. Percival, S. L., Emanuel, C., Cutting, K. F. & Williams, D. W. Microbiology of the skin and the role of biofilms in infection. Int. Wound J. 9, 14-32 (2012).
113. O'Hara, C. M., Brenner, F. W. & Miller, J. M. Classification, identification, and clinical significance of Proteus, Providencia, and Morganella. Clin. Microbiol. Rev. 13, 534-546 (2000).
114. Hejazi, A. & Falkiner, F. R. Serratia marcescens. J. Med. Microbiol. 46, 903-912 (1997).
115. Goddard, A. F. et al. Direct sampling of cystic fibrosis lungs indicates that DNA-based analyses of upper-airway specimens can misrepresent lung microbiota. Proc. Natl Acad. Sci. USA 109, 13769-13774 (2012).
116. Cox, M. J. et al. Airway microbiota and pathogen abundance in age-stratified cystic fibrosis patients. PLoS ONE 5, e11044 (2010).
117. Zhao, J. et al. Decade-long bacterial community dynamics in cystic fibrosis airways. Proc. Natl Acad. Sci. USA 109, 5809-5814 (2012).
118. Davies, J. C. Pseudomonas aeruginosa in cystic fibrosis: pathogenesis and persistence. Paediatr. Respir. Rev. 3, 128-134 (2002).
119. Moscoso, J. A., 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. 13, 3128-3138 (2011).
120. Folkesson, A. et al. Adaptation of Pseudomonas aeruginosa to the cystic fibrosis airway: an evolutionary perspective. Nature Rev. Microbiol. 10, 841-851 (2012).
121. Ehrlich, G. D., Hu, F. Z., Shen, K., Stoodley, P. & Post, J. C. Bacterial plurality as a general mechanism driving persistence in chronic infections. Clin Orthop Relat Res. 437, 20-24 (2005).
122. Vorholt, J. A. Microbial life in the phyllosphere. Nature Rev. Microbiol. 10, 828-840 (2012).
123. Whipps, J. M. Microbial interactions and biocontrol in the rhizosphere. J. Exp. Bot. 52, 487-511 (2001).
124. Sarris, P. F., Skandalis, N., Kokkinidis, M. & Panopoulos, N. J. In silico analysis reveals multiple putative type VI secretion systems and effector proteins in Pseudomonas syringae pathovars. Mol. Plant Pathol. 11, 795-804 (2010).
125. De Maayer, P. et al. Comparative genomics of the Type VI secretion systems of Pantoea and Erwinia species reveals the presence of putative effector islands that may be translocated by the VgrG and Hcp proteins. BMC Genomics 12, 576 (2011).
126. Mattinen, L. et al. 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 (2008).
127. Varivarn, K., Champa, L. A., Silby, M. W. & Robleto, E. A. Colonization strategies of Pseudomonas fluorescens Pf0-1: activation of soil-specific genes important for diverse and specific environments. BMC Microbiol. 13, 92 (2013).
128. Parsek, M. R. & Singh, P. K. Bacterial biofilms: an emerging link to disease pathogenesis. Annu. Rev. Microbiol. 57, 677-701 (2003).
129. Leiman, P. G. et al. Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc. Natl Acad. Sci. USA 106, 4154-4159 (2009).
130. Kanamaru, S. Structural similarity of tailed phages and pathogenic bacterial secretion systems. Proc. Natl Acad. Sci. USA 106, 4067-4068 (2009).
131. Basler, M., Pilhofer, M., Henderson, G. P., Jensen, G. J. & Mekalanos, J. J. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483, 182-186 (2012).
132. Silverman, J. M., Brunet, Y. R., Cascales, E. & Mougous, J. D. Structure and regulation of the type VI secretion system. Annu. Rev. Microbiol. 66, 453-472 (2012).
133. Cascales, E. & Cambillau, C. Structural biology of type VI secretion systems. Phil. Trans. R. Soc. Lond. B Biol. Sci. 367, 1102-1111 (2012).
134. Hachani, A. et al. Type VI secretion system in Pseudomonas aeruginosa: secretion and multimerization of VgrG proteins. J. Biol. Chem. 286, 12317-12327 (2011).
135. Shneider, M. M. et al. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500, 350-353 (2013).
136. Silverman, J. M. et al. Secretion substrates. Mol. Cell 51, 584-593 (2013).
137. Pukatzki, S. et al. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc. Natl Acad. Sci. USA 103, 1528-1533 (2006).
138. Bladergroen, M. R., Badelt, K. & Spaink, H. P. Infection-blocking genes of a symbiotic Rhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. Mol. Plant Microbe Interact. 16, 53-64 (2003).
139. Rao, P. S., Yamada, Y., Tan, Y. P. & Leung, K. Y. Use of proteomics to identify novel virulence determinants that are required for Edwardsiella tarda pathogenesis. Mol. Microbiol. 53, 573-586 (2004).
140. Zheng, J. & Leung, K. Y. Dissection of a type VI secretion system in Edwardsiella tarda. Mol. Microbiol. 66, 1192-1206 (2007).
141. Aoki, S. K. et al. A widespread family of polymorphic contact-dependent toxin delivery systems in bacteria. Nature 468, 439-442 (2010).
142. Nikolakakis, K. et al. The toxin/immunity network of Burkholderia pseudomallei contact-dependent growth inhibition (CDI) systems. Mol. Microbiol. 84, 516-529 (2012).
143. Anderson, M. S., Garcia, E. C. & Cotter, P. A. The Burkholderia bcpAIOB genes define unique classes of two-partner secretion and contact dependent growth inhibition systems. PLoS Genet. 8, e1002877 (2012).
144. Aoki, S. K. et al. Contact-dependent growth inhibition requires the essential outer membrane protein BamA (YaeT) as the receptor and the inner membrane transport protein AcrB. Mol. Microbiol. 70, 323-340 (2008).
145. Aoki, S. K. et al. Contact-dependent inhibition of growth in Escherichia coli. Science 309, 1245-1248 (2005).
146. Webb, J. S. et al. Delivery of CdiA nuclease toxins into target cells during contact-dependent growth inhibition. PLoS ONE 8, e57609 (2013).