Pantoea ananatis utilizes a type VI secretion system for pathogenesis and bacterial competition

Molecular Plant-Microbe Interactions

Volumn 28, Issue 4, 2015, Pages 420-431

  Shyntum, Divine Y ^a   Theron, Jacques ^a   Venter, Stephanus N ^a   Moleleki, Lucy N ^a   Toth, Ian K ^a,b   Coutinho, Teresa A ^a  

^a UNIVERSITY OF PRETORIA   (South Africa)

^b SCOTTISH CROP RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALLIUM CEPA; ANANAS COMOSUS; BACTERIA (MICROORGANISMS); NEGIBACTERIA; PANTOEA ANANATIS;

BACTERIAL GENE; BACTERIAL SECRETION SYSTEM; GENE INACTIVATION; GENETICS; HOST PATHOGEN INTERACTION; MICROBIOLOGY; MULTIGENE FAMILY; MUTATION; ONION; PANTOEA; PATHOGENICITY; PHYSIOLOGY; PLANT DISEASE; VIRULENCE;

BACTERIAL SECRETION SYSTEMS; GENE KNOCKOUT TECHNIQUES; GENES, BACTERIAL; HOST-PATHOGEN INTERACTIONS; MULTIGENE FAMILY; MUTATION; ONIONS; PANTOEA; PLANT DISEASES; VIRULENCE;

EID: 84927640424     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-07-14-0219-R     Document Type: Article

References (93)

1. Aschtgen, M. S., Bernard, C. S., De Bentzmann, S., Lloubés, R., and Cascales, E. 2008. SciN is an outer membrane lipoprotein required for type VI secretion in enteroaggregative Escherichia coli. J. Bacteriol. 190:7523-7531.
2. Backert, S., and Meyer, T. F. 2006. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr. Opin. Microbiol. 9:207-217.
3. Ballister, E. R., Lai, A. H., Zuckermann, R. N., Cheng, Y., and Mougous, J. D. 2008. In vitro self-assembly of tailorable nanotubes from a simple protein building block. Proc. Natl. Acad. Sci. U. S. A. 105:3733-3738.
4. Basler, M., Pilhofer, M., Henderson, G. P., Jensen, G. J., and Mekalanos, J. J. 2012. Type VI secretion requires a dynamic contractile phage taillike structure. Nature 483:182-186.
5. Bingle, L. E. H., Bailey, C. M., and Pallen, M. J. 2008. Type VI secretion: A beginner's guide. Curr. Opin. Microbiol. 11:3-8.
6. Blondel, C. J., Yang, H.-J., Castro, B., Chiang, S., Toro, C. S., Zaldívar, M., Contreras, I., Andrews-Polymenis, H. L., and Santiviago, C. A. 2010. Contribution of the type VI secretion system encoded in SPI-19 to chicken colonization by Salmonella enterica serotypes Gallinarum and Enteritidis. PLoS One 5:e11724.
7. Bönemann, G., Pietrosiuk, A., Diemand, A., Zentgraf, H., and Mogk, A. 2009. Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO (Eur. Mol. Biol. Organ.) J. 28:315-325.
8. Boyer, F., Fichant, G., Berthod, J., Vandenbrouck, Y., and 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.
9. Carruthers, M. D., Nicholson, P. A., Tracy, E. N., and Munson, R. S., Jr. 2013. Acinetobacter baumannii utilizes a type VI secretion system for bacterial competition. PLoS One 8:e59388.
10. Cascales, E. 2008. The type VI secretion toolkit. EMBO (Eur. Mol. Biol. Organ.) Rep. 9:735-741.
11. Cascales, E., and Cambillau, C. 2012. Structural biology of type VI secretion systems. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367:1102-1111.
12. Chaudhuri, R. R., Morgan, E., Peters, S. E., Pleasance, S. J., Hudson, D. L., Davies, H. M., Wang, J., Van Diemen, P. M., Buckley, A. M., Bowen, A. J., Pullinger, G. D., Turner, D. J., Langridge, G. C., Turner, A. K., Parkhill, J., Charles, I. G., Maskell, D. J., and Stevens, M. P. 2013. Comprehensive assignment of roles for Salmonella typhimurium genes in intestinal colonization of food-producing animals. PLoS Genet. 9:e1003456.
13. Chou, S., Bui, N. K., Russell, A. B., Lexa, K. W., Gardiner, T. E., LeRoux, M., Vollmer, W., and Mougous, J. D. 2012. Structure of a peptidoglycan amidase effector targeted to gram-negative bacteria by the type VI secretion system. Cell Reports 1:656-664.
14. Cianciotto, N. P. 2005. Type II secretion: A protein secretion system for all seasons. Trends Microbiol. 13:581-588.
15. Cohen, S. N., Chang, A. C. Y., and Hsu, L. 1972. Nonchromosomal antibiotic resistance in bacteria: Genetic transformation of Escherichia coli by R-factor DNA. Proc. Natl. Acad. Sci. U. S. A. 69:2110-2114.
16. Cornelis, G. R. 2006. The type III secretion injectisome. Nat. Rev. Microbiol. 4:811-825.
17. Coulthurst, S. J. 2013. The Type VI secretion system - a widespread and versatile cell targeting system. Res. Microbiol. 164:640-654.
18. Coutinho, T. A., and Venter, S. N. 2009. Pantoea ananatis: An unconventional plant pathogen. Mol. Plant Pathol. 10:325-335.
19. Datsenko, K. A., and Wanner, B. L. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
20. De Maayer, P., Venter, S. N., Kamber, T., Duffy, B., Coutinho, T. A., and Smits, T. H. 2011. 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.
21. De Pace, F., Nakazato, G., Pacheco, A., De Paiva, J. B., Sperandio, V., and Da Silveira, W. D. 2010. The type VI secretion system plays a role in type 1 fimbria expression and pathogenesis of an avian pathogenic Escherichia coli strain. Infect. Immun. 78:4990-4998.
22. Decoin, V., Barbey, C., Bergeau, D., Latour, X., Feuilloley, M. G. J., Orange, N., and Merieau, A. 2014. A type VI secretion system is involved in Pseudomonas fluorescens bacterial competition. PLoS One 9:e89411.
23. Dong, T. G., Ho, B. T., Yoder-Himes, D. R., and Mekalanos, J. J. 2013. Identification of T6SS-dependent effector and immunity proteins by Tn-seq in Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A. 110:2623-2628.
24. Durand, E., Zoued, A., Spinelli, S., Watson, P. J., Aschtgen, M. S., Journet, L., Cambillau, C., and Cascales, E. 2012. Structural characterization and oligomerization of the TssL protein, a component shared by bacterial type VI and type IVb secretion systems. J. Biol. Chem. 287:14157-14168.
25. Economou, A., Christie, P. J., Fernandez, R. C., Palmer, T., Plano, G. V., and Pugsley, A. P. 2006. Secretion by numbers: Protein traffic in prokaryotes. Mol. Microbiol. 62:308-319.
26. English, G., Trunk, K., Rao, V. A., Srikannathasan, V., Hunter, W. N., and Coulthurst, S. J. 2012. New secreted toxins and immunity proteins encoded within the type VI secretion system gene cluster of Serratia marcescens. Mol. Microbiol. 86:921-936.
27. Felisberto-Rodrigues, C., Durand, E., Aschtgen, M. S., Blangy, S., Ortiz-Lombardia, M., Douzi, B., Cambillau, C., and Cascales, E. 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.
28. Filloux, A., Hachani, A., and Bleves, S. 2008. The bacterial type VI secretion machine: Yet another player for protein transport across membranes. Microbiology 154:1570-1583.
29. Fritsch, M. J., Trunk, K., Diniz, J. A., Guo, M., Trost, M., and Coulthurst, S. J. 2013. Proteomic identification of novel secreted antibacterial toxins of the Serratia marcescens type VI secretion system. Mol. Cell. Proteomics 12:2735-2749.
30. Gallegos-Robles, M. A., Morales-Loredo, A., Alvarez-Ojeda, G., Vega-P, A., Chew-M, Y., Velarde, S., and Fratamico, P. 2008. Identification of Salmonella serotypes isolated from cantaloupe and chile pepper production systems in Mexico by PCR-restriction fragment length polymorphism. J. Food Prot. 71:2217-2222.
31. Gerlach, R. G., and Hensel, M. 2007. Protein secretion systems and adhesins: The molecular armory of gram-negative pathogens. Int. J. Med. Microbiol. 297:401-415.
32. Gitaitis, R. D., and Gay, J. D. 1997. First report of a leaf blight seed stalk rot, and bulb decay of onion by Pantoea ananas in Georgia. Plant Dis. 81:1096.
33. Goszczynska, T., Moloto, V. M., Venter, S. N., and Coutinho, T. A. 2006. Isolation and identification of Pantoea ananatis from onion seed in South Africa. Seed Sci. Technol. 34:655-668.
34. Goszczynska, T., Botha, W. J., Venter, S. N., and Coutinho, T. A. 2007. Isolation and identification of the causal agent of brown stalk rot, a new disease of maize in South Africa. Plant Dis. 91:711-718.
35. Gu, G., Hu, J., Cevallos-Cevallos, J. M., Richardson, S. M., Bartz, J. A., and Van Bruggen, A. H. C. 2011. Internal colonization of Salmonella enterica serovar Typhimurium in tomato plants. PLoS One 6:e27340.
36. Haapalainen, M., Mosorin, H., Dorati, F., Wu, R.-F., Roine, E., Taira, S., Nissinen, R., Mattinen, L., Jackson, R., Pirhonen, M., and Lin, N. C. 2012. 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.
37. Holland, I. B. 2010. The extraordinary diversity of bacterial protein secretion mechanisms. Methods Mol. Biol. 619:1-20.
38. Hood, R. D., Singh, P., Hsu, F., Güvener, T., Carl, M. A., Trinidad, R. R., Silverman, J. M., Ohlson, B. B., Hicks, K. G., Plemel, R. L., Li, M., Schwarz, S., Wang, W. Y., Merz, A. J., Goodlett, D. R., and Mougous, J. D. 2010. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7:25-37.
39. Hueck, C. J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol. Mol. Biol. Rev. 62:379-433.
40. Jobichen, C., Chakraborty, S., Li, M., Zheng, J., Joseph, L., Mok, Y.-K., Leung, K. Y., and Sivaraman, J. 2010. Structural basis for the secretion of EvpC: A key type VI secretion system protein from Edwardsiella tarda. PLoS One 5:e12910.
41. Kanamaru, S. 2009. Structural similarity of tailed phages and pathogenic bacterial secretion systems. Proc. Natl. Acad. Sci. U. S. A. 106:4067-4068.
42. Kapitein, N., and Mogk, A. 2013. Deadly syringes: Type VI secretion system activities in pathogenicity and interbacterial competition. Curr. Opin. Microbiol. 16:52-58.
43. Kapitein, N., Bönemann, G., Pietrosiuk, A., Seyffer, F., Hausser, I., Locker, J. K., and Mogk, A. 2013. ClpV recycles VipA/VipB tubules and prevents non-productive tubule formation to ensure efficient type VI protein secretion. Mol. Microbiol. 87:1013-1028.
44. Katashkina, J. I., Hara, Y., Golubeva, L. I., Andreeva, I. G., Kuvaeva, T. M., and Mashko, S. V. 2009. Use of the l Red-recombineering method for genetic engineering of Pantoea ananatis. BMC Mol. Biol. 10:34.
45. Koskiniemi, S., Lamoureux, J. G., Nikolakakis, K. C., T'Kint De Roodenbeke, C., Kaplan, M. D., Low, D. A., and Hayes, C. S. 2013. Rhs proteins from diverse bacteria mediate intercellular competition. Proc. Natl. Acad. Sci. U. S. A. 110:7032-7037.
46. Kovach, M. E., Elzer, P. H., Hill, D. S., Robertson, G. T., Farris, M. A., Roop, R. M., 2nd, and Peterson, K. M. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
47. Kung, V. L., Khare, S., Stehlik, C., Bacon, E. M., Hughes, A. J., and Hauser, A. R. 2012. An rhs gene of Pseudomonas aeruginosa encodes a virulence protein that activates the inflammasome. Proc. Natl. Acad. Sci. U. S. A. 109:1275-1280.
48. Lagendijk, E. L., Validov, S., Lamers, G. E. M., De Weert, S., and Bloemberg, G. V. 2010. Genetic tools for tagging gram-negative bacteria with mCherry for visualization in vitro and in natural habitats, biofilm and pathogenicity studies. FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Lett. 305:81-90.
49. Leiman, P. G., Basler, M., Ramagopal, U. A., Bonanno, J. B., Sauder, J. M., Pukatzki, S., Burley, S. K., Almo, S. C., and 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.
50. Lin, J.-S., Ma, L.-S., and Lai, E.-M. 2013. Systematic dissection of the Agrobacterium type VI secretion system reveals machinery and secreted components for subcomplex formation. PLoS One 8:e67647.
51. Liu, H., Coulthurst, S. J., Pritchard, L., Hedley, P. E., Ravensdale, M., Humphris, S., Burr, T., Takle, G., Brurberg, M. B., Birch, P. R., Salmond, G. P. C., and Toth, I. K. 2008. Quorum sensing coordinates brute force and stealth modes of infection in the plant pathogen Pectobacterium atrosepticum. PLoS Pathog. 4:e1000093.
52. Lossi, N. S., Dajani, R., Freemont, P., and Filloux, A. 2011. Structurefunction analysis of HsiF, a gp25-like component of the type VI secretion system, in Pseudomonas aeruginosa. Microbiology 157:3292-3305.
53. Lossi, N. S., Manoli, E., Förster, A., Dajani, R., Pape, T., Freemont, P., and Filloux, A. 2013. The HsiB1C1 (TssB-TssC) complex of the Pseudomonas aeruginosa type VI secretion system forms a bacteriophage tail sheathlike structure. J. Biol. Chem. 288:7536-7548.
54. Ma, A. T., and 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.
55. Ma, L. S., Narberhaus, F., and Lai, E. M. 2012. IcmF family protein TssM exhibits ATPase activity and energizes type VI secretion. J. Biol. Chem. 287:15610-15621.
56. MacIntyre, D. L., Miyata, S. T., Kitaoka, M., and Pukatzki, S. 2010. The Vibrio cholerae type VI secretion system displays antimicrobial properties. Proc. Natl. Acad. Sci. U. S. A. 107:19520-19524.
57. Mergaert, J., Verdonck, L., and Kersters, K. 1993. Transfer of Erwinia ananas (synonym, Erwinia uredovora) and Erwinia stewartii to the genus Pantoea emend. as Pantoea ananas (Serrano 1928) comb. nov., and Pantoea stewartii (Smith 1898) comb. nov., respectively, and description of Pantoea stewartii subsp. indologenes subsp. nov. Int. J. Syst. Bacteriol. 43:162-173.
58. Miyata, S. T., Kitaoka, M., Brooks, T. M., McAuley, S. B., and Pukatzki, S. 2011. Vibrio cholerae requires the type VI secretion system virulence factor VasX to kill Dictyostelium discoideum. Infect. Immun. 79:2941-2949.
59. Morohoshi, T., Nakamura, Y., Yamazaki, G., Ishida, A., Kato, N., and Ikeda, T. 2007. The plant pathogen Pantoea ananatis produces N-acylhomoserine lactone and causes center rot disease of onion by quorum sensing. J. Bacteriol. 189:8333-8338.
60. Morohoshi, T., Ogata, Y., and Ikeda, T. 2011a. Cell aggregation is negatively regulated by N-acylhomoserine lactone-mediated quorum sensing in Pantoea ananatis SK-1. J. Biosci. Bioeng. 112:566-569.
61. Morohoshi, T., Oseki, K., and Ikeda, T. 2011b. Exopolysaccharide production is influenced by sugars, N-acylhomoserine lactone, and transcriptional regulators RcsA and RcsB, but does not affect pathogenicity in the plant pathogen Pantoea ananatis. Biosci. Biotechnol. Biochem. 75:997-999.
62. Mougous, J. D., Cuff, M. E., Raunser, S., Shen, A., Zhou, M., Gifford, C. A., Goodman, A. L., Joachimiak, G., Ordoñez, C. L., Lory, S., Walz, T., Joachimiak, A., and Mekalanos, J. J. 2006. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312:1526-1530.
63. Mougous, J. D., Gifford, C. A., Ramsdell, T. L., and Mekalanos, J. J. 2007. Threonine phosphorylation post-translationally regulates protein secretion in Pseudomonas aeruginosa. Nat. Cell Biol. 9:797-803.
64. Murdoch, S. L., Trunk, K., English, G., Fritsch, M. J., Pourkarimi, E., and Coulthurst, S. J. 2011. The opportunistic pathogen Serratia marcescens utilizes type VI secretion to target bacterial competitors. J. Bacteriol. 193:6057-6069.
65. Pukatzki, S., Ma, A. T., Sturtevant, D., Krastins, B., Sarracino, D., Nelson, W. C., Heidelberg, J. F., and 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.
66. Pukatzki, S., Ma, A. T., Revel, A. T., Sturtevant, D., and 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.
67. Records, A. R. 2011. The type VI secretion system: A multipurpose delivery system with a phage-like machinery. Mol. Plant-Microbe Interact. 24:751-757.
68. Russell, A. B., Hood, R. D., Bui, N. K., LeRoux, M., Vollmer, W., and Mougous, J. D. 2011. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475:343-347.
69. Russell, A. B., Singh, P., Brittnacher, M., Bui, N. K., Hood, R. D., Carl, M. A., Agnello, D. M. K., Schwarz, S., Goodlett, D. R., Vollmer, W., and Mougous, J. D. 2012. A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach. Cell Host Microbe 11:538-549.
70. Sambrook, J., and Russell, D. W. 2001. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, U. S. A.
71. Sandkvist, M. 2001. Biology of type II secretion. Mol. Microbiol. 40:271-283.
72. Sarris, P. F., Trantas, E. A., Skandalis, N., Tampakaki, A. P., Kapanidou, M., Kokkinidis, M., and Panopoulos, N. J. 2012. Phytobacterial type VI secretion system-Gene distribution, phylogeny, structure and biological functions. Pages 53-84 in: Plant Pathology. C. J. Cumagun, ed. InTech, Croatia.
73. Schell, M. A., Ulrich, R. L., Ribot, W. J., Brueggemann, E. E., Hines, H. B., Chen, D., Lipscomb, L., Kim, H. S., Mrazek, J., Nierman, W. C., and Deshazer, D. 2007. Type VI secretion is a major virulence determinant in Burkholderia mallei. Mol. Microbiol. 64:1466-1485.
74. Schwarz, S., Hood, R. D., and Mougous, J. D. 2010a. What is type VI secretion doing in all those bugs? Trends Microbiol. 18:531-537.
75. Schwarz, S., West, T. E., Boyer, F., Chiang, W. C., Carl, M. A., Hood, R. D., Rohmer, L., Tolker-Nielsen, T., Skerrett, S. J., and Mougous, J. D. 2010b. Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog. 6:e1001068.
76. Serrano, F. B. 1928. Bacterial fruitlet brown-rot of pineapple in the Philippines. Philip. J. Sci. 36:271-305.
77. Sessitsch, A., Reiter, B., and Berg, G. 2004. Endophytic bacterial communities of field-grown potato plants and their plant-growth-promoting and antagonistic abilities. Can. J. Microbiol. 50:239-249.
78. Shalom, G., Shaw, J. G., and 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.
79. Shevchuk, N. A., Bryksin, A. V., Nusinovich, Y. A., Cabello, F. C., Sutherland, M., and Ladisch, S. 2004. Construction of long DNA molecules using long PCR-based fusion of several fragments simultaneously. Nucleic Acids Res. 32:e19.
80. Shneider, M. M., Buth, S. A., Ho, B. T., Basler, M., Mekalanos, J. J., and Leiman, P. G. 2013. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500:350-353.
81. Shrivastava, S., and Mande, S. S. 2008. Identification and functional characterization of gene components of Type VI Secretion system in bacterial genomes. PLoS One 3:e2955.
82. Shyntum, D. Y., Venter, S. N., Moleleki, L. N., Toth, I., and Coutinho, T. A. 2014. Comparative genomics of type VI secretion systems in strains of Pantoea ananatis from different environments. BMC Genomics 15:163.
83. Silverman, J. M., Brunet, Y. R., Cascales, E., and Mougous, J. D. 2012. Structure and regulation of the type VI secretion system. Annu. Rev. Microbiol. 66:453-472.
84. Suarez, G., Sierra, J. C., Sha, J., Wang, S., Erova, T. E., Fadl, A. A., Foltz, S. M., Horneman, A. J., and 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.
85. Suarez, G., Sierra, J. C., Erova, T. E., Sha, J., Horneman, A. J., and Chopra, A. K. 2010. A type VI secretion system effector protein, VgrG1, from Aeromonas hydrophila that induces host cell toxicity by ADP ribosylation of actin. J. Bacteriol. 192:155-168.
86. Toth, I. K., Bell, K. S., Holeva, M. C., and Birch, P. R. J. 2003. Soft rot erwiniae: From genes to genomes. Mol. Plant Pathol. 4:17-30.
87. Walcott, R. R., Gitaitis, R. D., Castro, A. C., Sanders, F. H., and Diaz-Perez, J. C. 2002. Natural infestation of onion seed by Pantoea ananatis, causal agent of center rot. Plant Dis. 86:106-111.
88. Weber, B. S., Miyata, S. T., Iwashkiw, J. A., Mortensen, B. L., Skaar, E. P., Pukatzki, S., and Feldman, M. F. 2013. Genomic and functional analysis of the type VI secretion system in Acinetobacter. PLoS One 8:e55142.
89. Wu, H. Y., Chung, P. C., Shih, H. W., Wen, S. R., and Lai, E. M. 2008. Secretome analysis uncovers an Hcp-family protein secreted via a type VI secretion system in Agrobacterium tumefaciens. J. Bacteriol. 190:2841-2850.
90. Zhang, D., De Souza, R. F., Anantharaman, V., Iyer, L. M., and Aravind, L. 2012. Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol. Direct 7:18.
91. Zheng, J., and Leung, K. Y. 2007. Dissection of a type VI secretion system in Edwardsiella tarda. Mol. Microbiol. 66:1192-1206.
92. Zheng, J., Ho, B., and Mekalanos, J. J. 2011. Genetic analysis of antiamoebae and anti-bacterial activities of the type VI secretion system in Vibrio cholerae. PLoS One 6:e23876.
93. Zoued, A., Durand, E., Bebeacua, C., Brunet, Y. R., Douzi, B., Cambillau, C., Cascales, E., and Journet, L. 2013. TssK is a trimeric cytoplasmic protein interacting with components of both phage-like and membrane anchoring complexes of the type VI secretion system. J. Biol. Chem. 288:27031-27041.