Chimeric adaptor proteins translocate diverse type VI secretion system effectors in Vibrio cholerae

EMBO Journal

Volumn 34, Issue 16, 2015, Pages 2198-2210

  Unterweger, Daniel ^a   Kostiuk, Benjamin ^a   Ötjengerdes, Rina ^a   Wilton, Ashley ^a   Diaz Satizabal, Laura ^a   Pukatzki, Stefan ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

adaptor protein; compatibility groups; T6SS; type VI secretion system; Vibrio cholerae

Indexed keywords

ADAPTOR PROTEIN; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1; BACTERIAL PROTEIN; BACTERIAL SECRETION SYSTEM; BACTERIAL TOXIN; CARRIER PROTEIN; VIRULENCE FACTOR;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL CELL; DIVERSIFYING SELECTION; GENE CLUSTER; IMMUNOPRECIPITATION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TYPE VI SECRETION SYSTEM; VIBRIO CHOLERAE; WESTERN BLOTTING; BACTERIAL SECRETION SYSTEM; BIOLOGICAL MODEL; GENETICS; INTERSPERSED REPEAT; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

BACTERIA (MICROORGANISMS); EUKARYOTA; NEGIBACTERIA; PROKARYOTA; VIBRIO CHOLERAE;

BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BACTERIAL TOXINS; BIOLOGICAL TRANSPORT; INTERSPERSED REPETITIVE SEQUENCES; MEMBRANE TRANSPORT PROTEINS; MODELS, BIOLOGICAL; VIBRIO CHOLERAE; VIRULENCE FACTORS;

EID: 84939272605     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201591163     Document Type: Article

References (41)

1. Altindis E, Dong T, Catalano C, Mekalanos J, (2015) Secretome analysis of Vibrio cholerae type VI secretion system reveals a new effector-immunity pair. mBio 6: e00075
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, (1990) Basic local alignment search tool. J Mol Biol 215: 403-410
3. Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ, (2012) Type VI secretion requires a dynamic contractile phage tail-like structure. Nature 483: 182-186
4. Borgeaud S, Metzger LC, Scrignari T, Blokesch M, (2015) Bacterial evolution. The type VI secretion system of Vibrio cholerae fosters horizontal gene transfer. Science 347: 63-67
5. Brooks TM, Unterweger D, Bachmann V, Kostiuk B, Pukatzki S, (2013) Lytic activity of the Vibrio cholerae type VI secretion toxin VgrG-3 is inhibited by the antitoxin TsaB. J Biol Chem 288: 7618-7625
6. Crooks GE, Hon G, Chandonia JM, Brenner SE, (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190
7. Daleke MH, van der Woude AD, Parret AH, Ummels R, de Groot AM, Watson D, Piersma SR, Jimenez CR, Luirink J, Bitter W, Houben EN, (2012) Specific chaperones for the type VII protein secretion pathway. J Biol Chem 287: 31939-31947
8. Diniz JA, Coulthurst SJ, (2015) Intra-species competition in Serratia marcescens is mediated by type VI secretion Rhs effectors and a conserved effector-associated accessory protein. J Bacteriol 197: 2350-2360
9. Dong TG, Ho BT, Yoder-Himes DR, Mekalanos JJ, (2013) Identification of T6SS-dependent effector and immunity proteins by Tn-seq in Vibrio cholerae. Proc Natl Acad Sci USA 110: 2623-2628
10. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797
11. Fu Y, Waldor MK, Mekalanos JJ, (2013) Tn-Seq analysis of Vibrio cholerae intestinal colonization reveals a role for T6SS-mediated antibacterial activity in the host. Cell Host Microbe 14: 652-663
12. Geer LY, Domrachev M, Lipman DJ, Bryant SH, (2002) CDART: protein homology by domain architecture. Genome Res 12: 1619-1623
13. Guzman LM, Belin D, Carson MJ, Beckwith J, (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177: 4121-4130
14. Harris JB, LaRocque RC, Qadri F, Ryan ET, Calderwood SB, (2012) Cholera. Lancet 379: 2466-2476
15. Ho BT, Dong TG, Mekalanos JJ, (2014) A view to a kill: the bacterial type VI secretion system. Cell Host Microbe 15: 9-21
16. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A, (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647-1649
17. Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ, (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10: 845-858
18. Leiman PG, Basler M, Ramagopal UA, Bonanno JB, Sauder JM, Pukatzki S, Burley SK, Almo SC, Mekalanos JJ, (2009) Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci USA 106: 4154-4159
19. 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: 234-243
20. Ma LS, Hachani A, Lin JS, Filloux A, Lai EM, (2014) Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell Host Microbe 16: 94-104
21. 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: 19520-19524
22. Marchler-Bauer A, Zheng C, Chitsaz F, Derbyshire MK, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Lu S, Marchler GH, Song JS, Thanki N, Yamashita RA, Zhang D, Bryant SH, (2013) CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res 41: D348-D352
23. Metcalf WW, Jiang W, Daniels LL, Kim SK, Haldimann A, Wanner BL, (1996) Conditionally replicative and conjugative plasmids carrying lacZ alpha for cloning, mutagenesis, and allele replacement in bacteria. Plasmid 35: 1-13
24. 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: 2941-2949
25. Miyata ST, Unterweger D, Rudko SP, Pukatzki S, (2013) Dual expression profile of type VI secretion system immunity genes protects pandemic Vibrio cholerae. PLoS Pathog 9: e1003752
26. Page AL, Parsot C, (2002) Chaperones of the type III secretion pathway: jacks of all trades. Mol Microbiol 46: 1-11
27. Pearson WR, (2013) An introduction to sequence similarity ("homology") searching. Curr Protoc Bioinformatics 42: 3. 1
28. Pukatzki S, Ma AT, Sturtevant D, Krastins B, Sarracino D, Nelson WC, Heidelberg JF, Mekalanos JJ, (2006) Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci USA 103: 1528-1533
29. 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: 15508-15513
30. Russell AB, LeRoux M, Hathazi K, Agnello DM, Ishikawa T, Wiggins PA, Wai SN, Mougous JD, (2013) Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 496: 508-512
31. Russell AB, Peterson SB, Mougous JD, (2014) Type VI secretion system effectors: poisons with a purpose. Nat Rev Microbiol 12: 137-148
32. Salomon D, Kinch LN, Trudgian DC, Guo X, Klimko JA, Grishin NV, Mirzaei H, Orth K, (2014) Marker for type VI secretion system effectors. Proc Natl Acad Sci USA 111: 9271-9276
33. Sheahan KL, Cordero CL, Satchell KJ, (2004) Identification of a domain within the multifunctional Vibrio cholerae RTX toxin that covalently cross-links actin. Proc Natl Acad Sci USA 101: 9798-9803
34. Shneider MM, Buth SA, Ho BT, Basler M, Mekalanos JJ, Leiman PG, (2013) PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500: 350-353
35. Silverman JM, Agnello DM, Zheng H, Andrews BT, Li M, Catalano CE, Gonen T, Mougous JD, (2013) Haemolysin coregulated protein is an exported receptor and chaperone of type VI secretion substrates. Mol Cell 51: 584-593
36. Stamatakis A, (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313
37. Unterweger D, Kitaoka M, Miyata ST, Bachmann V, Brooks TM, Moloney J, Sosa O, Silva D, Duran-Gonzalez J, Provenzano D, Pukatzki S, (2012) Constitutive type VI secretion system expression gives Vibrio cholerae intra- and interspecific competitive advantages. PLoS ONE 7: e48320
38. Unterweger D, Miyata ST, Bachmann V, Brooks TM, Mullins T, Kostiuk B, Provenzano D, Pukatzki S, (2014) The Vibrio cholerae type VI secretion system employs diverse effector modules for intraspecific competition. Nat Commun 5: 3549
39. Whitney JC, Beck CM, Goo YA, Russell AB, Harding BN, De Leon JA, Cunningham DA, Tran BQ, Low DA, Goodlett DR, Hayes CS, Mougous JD, (2014) Genetically distinct pathways guide effector export through the type VI secretion system. Mol Microbiol 92: 529-542
40. Zhang J, Zhang H, Gao Z, Hu H, Dong C, Dong YH, (2014) Structural basis for recognition of the type VI spike protein VgrG3 by a cognate immunity protein. FEBS Lett 588: 1891-1898
41. Zoued A, Brunet YR, Durand E, Aschtgen MS, Logger L, Douzi B, Journet L, Cambillau C, Cascales E, (2014) Architecture and assembly of the Type VI secretion system. Biochim Biophys Acta 1843: 1664-1673