Tn-seq analysis of vibrio cholerae intestinal colonization reveals a role for T6SS-mediated antibacterial activity in the host

Cell Host and Microbe

Volumn 14, Issue 6, 2013, Pages 652-663

  Fu, Yang ^a,b   Waldor, Matthew K ^a,c   Mekalanos, John J ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b NANKAI UNIVERSITY   (China)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC GMP;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL CELL; BACTERIAL COLONIZATION; BACTERIAL IMMUNITY; CELL INTERACTION; CONTROLLED STUDY; FITNESS; HOST; IN VIVO STUDY; INFECTION; INTESTINE; MUTANT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; TRANSPOSON; TYPE VI SECRETION SYSTEM; VIBRIO CHOLERAE;

ANIMALS; ANTIBIOSIS; BACTERIAL SECRETION SYSTEMS; DNA TRANSPOSABLE ELEMENTS; GENE EXPRESSION PROFILING; HOST-PATHOGEN INTERACTIONS; MUTAGENESIS, INSERTIONAL; RABBITS; SEQUENCE ANALYSIS, DNA; VIBRIO CHOLERAE;

EID: 84890266225     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2013.11.001     Document Type: Article

References (55)

1. M. Basler, and J.J. Mekalanos Type 6 secretion dynamics within and between bacterial cells Science 337 2012 815
2. M. Basler, M. Pilhofer, G.P. Henderson, G.J. Jensen, and J.J. Mekalanos Type VI secretion requires a dynamic contractile phage tail-like structure Nature 483 2012 182 186
3. S. Bhattacharya, R. Black, L. Bourgeois, J. Clemens, A. Cravioto, J.L. Deen, G. Dougan, R. Glass, R.F. Grais, and M. Greco Public health. The cholera crisis in Africa Science 324 2009 885
4. J.E. Bina, and J.J. Mekalanos Vibrio cholerae tolC is required for bile resistance and colonization Infect. Immun. 69 2001 4681 4685
5. E.S. Bradley, K. Bodi, A.M. Ismail, and A. Camilli A genome-wide approach to discovery of small RNAs involved in regulation of virulence in Vibrio cholerae PLoS Pathog. 7 2011 e1002126
6. T.M. Brooks, D. Unterweger, V. Bachmann, B. Kostiuk, and S. Pukatzki Lytic activity of the Vibrio cholerae type VI secretion toxin VgrG-3 is inhibited by the antitoxin TsaB J. Biol. Chem. 288 2013 7618 7625
7. S.M. Butler, and A. Camilli Both chemotaxis and net motility greatly influence the infectivity of Vibrio cholerae Proc. Natl. Acad. Sci. USA 101 2004 5018 5023
8. S.M. Butler, E.J. Nelson, N. Chowdhury, S.M. Faruque, S.B. Calderwood, and A. Camilli Cholera stool bacteria repress chemotaxis to increase infectivity Mol. Microbiol. 60 2006 417 426
9. D.E. Cameron, J.M. Urbach, and J.J. Mekalanos A defined transposon mutant library and its use in identifying motility genes in Vibrio cholerae Proc. Natl. Acad. Sci. USA 105 2008 8736 8741
10. M.C. Chao, J.R. Pritchard, Y.J. Zhang, E.J. Rubin, J. Livny, B.M. Davis, and M.K. Waldor High-resolution definition of the Vibrio cholerae essential gene set with hidden Markov model-based analyses of transposon-insertion sequencing data Nucleic Acids Res. 41 2013 9033 9048
11. S.L. Chiang, and J.J. Mekalanos Use of signature-tagged transposon mutagenesis to identify Vibrio cholerae genes critical for colonization Mol. Microbiol. 27 1998 797 805
12. S.L. Chiang, and J.J. Mekalanos rfb mutations in Vibrio cholerae do not affect surface production of toxin-coregulated pili but still inhibit intestinal colonization Infect. Immun. 67 1999 976 980
13. C.S. Chin, J. Sorenson, J.B. Harris, W.P. Robins, R.C. Charles, R.R. Jean-Charles, J. Bullard, D.R. Webster, A. Kasarskis, and P. Peluso The origin of the Haitian cholera outbreak strain N. Engl. J. Med. 364 2011 33 42
14. L. Craig, R.K. Taylor, M.E. Pique, B.D. Adair, A.S. Arvai, M. Singh, S.J. Lloyd, D.S. Shin, E.D. Getzoff, and M. Yeager Type IV pilin structure and assembly: X-ray and EM analyses of Vibrio cholerae toxin-coregulated pilus and Pseudomonas aeruginosa PAK pilin Mol. Cell 11 2003 1139 1150
15. O. Danilchanka, and J.J. Mekalanos Cyclic dinucleotides and the innate immune response Cell 154 2013 962 970
16. B.W. Davies, R.W. Bogard, T.S. Young, and J.J. Mekalanos Coordinated regulation of accessory genetic elements produces cyclic di-nucleotides for V. cholerae virulence Cell 149 2012 358 370
17. S.N. De, J.K. Sarkar, and B.P. Tribedi An experimental study of the action of cholera toxin J. Pathol. Bacteriol. 63 1951 707 717
18. T.G. Dong, B.T. Ho, D.R. Yoder-Himes, and J.J. Mekalanos Identification of T6SS-dependent effector and immunity proteins by Tn-seq in Vibrio cholerae Proc. Natl. Acad. Sci. USA 110 2013 2623 2628
19. L.A. Gallagher, J. Shendure, and C. Manoil Genome-scale identification of resistance functions in Pseudomonas aeruginosa using Tn-seq MBio 2 2011 e00315-e10
20. D.A. Herrington, R.H. Hall, G. Losonsky, J.J. Mekalanos, R.K. Taylor, and M.M. Levine Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans J. Exp. Med. 168 1988 1487 1492
21. B.T. Ho, T.G. Dong, and J.J. Mekalanos A view to a kill: the bacterial type 6 secretion system Cell Host Microbe 2014 10.1016/j.chom.2013.11.008 in press. Published online January 15, 2014
22. R.D. Hood, P. Singh, F. Hsu, T. Güvener, M.A. Carl, R.R. Trinidad, J.M. Silverman, B.B. Ohlson, K.G. Hicks, and R.L. Plemel A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria Cell Host Microbe 7 2010 25 37
23. B.A. Jude, and R.K. Taylor The physical basis of type 4 pilus-mediated microcolony formation by Vibrio cholerae O1 J. Struct. Biol. 175 2011 1 9
24. N. Kapitein, and A. Mogk Deadly syringes: type VI secretion system activities in pathogenicity and interbacterial competition Curr. Opin. Microbiol. 16 2013 52 58
25. L.S. Katz, A. Petkau, J. Beaulaurier, S. Tyler, E.S. Antonova, M.A. Turnsek, Y. Guo, S. Wang, E.E. Paxinos, and F. Orata Evolutionary dynamics of Vibrio cholerae O1 following a single-source introduction to Haiti MBio 4 2013 e00398 e00413
26. K.V. Korotkov, M. Sandkvist, and W.G. Hol The type II secretion system: biogenesis, molecular architecture and mechanism Nat. Rev. Microbiol. 10 2012 336 351
27. P.G. Leiman, M. Basler, U.A. Ramagopal, J.B. Bonanno, J.M. Sauder, S. Pukatzki, S.K. Burley, S.C. Almo, and J.J. Mekalanos Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin Proc. Natl. Acad. Sci. USA 106 2009 4154 4159
28. M.J. Lombardo, J. Michalski, H. Martinez-Wilson, C. Morin, T. Hilton, C.G. Osorio, J.P. Nataro, C.O. Tacket, A. Camilli, and J.B. Kaper An in vivo expression technology screen for Vibrio cholerae genes expressed in human volunteers Proc. Natl. Acad. Sci. USA 104 2007 18229 18234
29. A.T. Ma, and J.J. Mekalanos In vivo actin cross-linking induced by Vibrio cholerae type VI secretion system is associated with intestinal inflammation Proc. Natl. Acad. Sci. USA 107 2010 4365 4370
30. A.T. Ma, S. McAuley, S. Pukatzki, and J.J. Mekalanos Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells Cell Host Microbe 5 2009 234 243
31. D.L. MacIntyre, S.T. Miyata, M. Kitaoka, and S. Pukatzki The Vibrio cholerae type VI secretion system displays antimicrobial properties Proc. Natl. Acad. Sci. USA 107 2010 19520 19524
32. A. Mandlik, J. Livny, W.P. Robins, J.M. Ritchie, J.J. Mekalanos, and M.K. Waldor RNA-Seq-based monitoring of infection-linked changes in Vibrio cholerae gene expression Cell Host Microbe 10 2011 165 174
33. B. Marteyn, F.B. Scorza, P.J. Sansonetti, and C. Tang Breathing life into pathogens: the influence of oxygen on bacterial virulence and host responses in the gastrointestinal tract Cell. Microbiol. 13 2011 171 176
34. D.S. Merrell, D.L. Hava, and A. Camilli Identification of novel factors involved in colonization and acid tolerance of Vibrio cholerae Mol. Microbiol. 43 2002 1471 1491
35. S.T. Miyata, V. Bachmann, and S. Pukatzki Type VI secretion system regulation as a consequence of evolutionary pressure J. Med. Microbiol. 62 2013 663 676
36. J.D. Mougous, M.E. Cuff, S. Raunser, A. Shen, M. Zhou, C.A. Gifford, A.L. Goodman, G. Joachimiak, C.L. Ordoñez, and S. Lory A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus Science 312 2006 1526 1530
37. A. Mutreja, D.W. Kim, N.R. Thomson, T.R. Connor, J.H. Lee, S. Kariuki, N.J. Croucher, S.Y. Choi, S.R. Harris, and M. Lebens Evidence for several waves of global transmission in the seventh cholera pandemic Nature 477 2011 462 465
38. E.T. Nelson, J.D. Clements, and R.A. Finkelstein Vibrio cholerae adherence and colonization in experimental cholera: electron microscopic studies Infect. Immun. 14 1976 527 547
39. J. Nesper, C.M. Lauriano, K.E. Klose, D. Kapfhammer, A. Kraiss, and J. Reidl Characterization of Vibrio cholerae O1 El tor galU and galE mutants: influence on lipopolysaccharide structure, colonization, and biofilm formation Infect. Immun. 69 2001 435 445
40. L.G. Pell, V. Kanelis, L.W. Donaldson, P.L. Howell, and A.R. Davidson 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 2009 4160 4165
41. K.M. Peterson, and J.J. Mekalanos Characterization of the Vibrio cholerae ToxR regulon: identification of novel genes involved in intestinal colonization Infect. Immun. 56 1988 2822 2829
42. D. Provenzano, D.A. Schuhmacher, J.L. Barker, and K.E. Klose The virulence regulatory protein ToxR mediates enhanced bile resistance in Vibrio cholerae and other pathogenic Vibrio species Infect. Immun. 68 2000 1491 1497
43. S. Pukatzki, A.T. Ma, D. Sturtevant, B. Krastins, D. Sarracino, W.C. Nelson, J.F. Heidelberg, and J.J. Mekalanos Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system Proc. Natl. Acad. Sci. USA 103 2006 1528 1533
44. S. Pukatzki, A.T. Ma, A.T. Revel, D. Sturtevant, and J.J. Mekalanos 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 2007 15508 15513
45. J.M. Ritchie, and M.K. Waldor Vibrio cholerae interactions with the gastrointestinal tract: lessons from animal studies Curr. Top. Microbiol. Immunol. 337 2009 37 59
46. J.M. Ritchie, H. Rui, R.T. Bronson, and M.K. Waldor Back to the future: studying cholera pathogenesis using infant rabbits MBio 1 2010 e00047-e10
47. A.B. Russell, R.D. Hood, N.K. Bui, M. LeRoux, W. Vollmer, and J.D. Mougous Type VI secretion delivers bacteriolytic effectors to target cells Nature 475 2011 343 347
48. M.M. Shneider, S.A. Buth, B.T. Ho, M. Basler, J.J. Mekalanos, and P.G. Leiman PAAR-repeat proteins sharpen and diversify the type VI secretion system spike Nature 500 2013 350 353
49. A.E. Sikora, S.R. Lybarger, and M. Sandkvist Compromised outer membrane integrity in Vibrio cholerae Type II secretion mutants J. Bacteriol. 189 2007 8484 8495
50. R.K. Taylor, V.L. Miller, D.B. Furlong, and J.J. Mekalanos Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin Proc. Natl. Acad. Sci. USA 84 1987 2833 2837
51. K.D. Tew, and D.M. Townsend Glutathione-s-transferases as determinants of cell survival and death Antioxid. Redox Signal. 17 2012 1728 1737
52. T. van Opijnen, and A. Camilli Transposon insertion sequencing: a new tool for systems-level analysis of microorganisms Nat. Rev. Microbiol. 11 2013 435 442
53. S.M. Wong, M. Bernui, H. Shen, and B.J. Akerley Genome-wide fitness profiling reveals adaptations required by Haemophilus in coinfection with influenza A virus in the murine lung Proc. Natl. Acad. Sci. USA 110 2013 15413 15418
54. Y.J. Zhang, T.R. Ioerger, C. Huttenhower, J.E. Long, C.M. Sassetti, J.C. Sacchettini, and E.J. Rubin Global assessment of genomic regions required for growth in Mycobacterium tuberculosis PLoS Pathog. 8 2012 e1002946
55. J. Zheng, O.S. Shin, D.E. Cameron, and J.J. Mekalanos Quorum sensing and a global regulator TsrA control expression of type VI secretion and virulence in Vibrio cholerae Proc. Natl. Acad. Sci. USA 107 2010 21128 21133