Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta

Cell Host and Microbe

Volumn 16, Issue 1, 2014, Pages 94-104

  Ma, Lay Sun ^a,b   Hachani, Abderrahman ^b   Lin, Jer Sheng ^a   Filloux, Alain ^b   Lai, Erh Min ^a  

^a INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE; NUCLEASE; TOXIN; TYPE VI DNASE EFFECTOR; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; VIRULENCE FACTOR; BACTERIAL TOXIN;

AGROBACTERIUM TUMEFACIENS; ARTICLE; ASSAY; BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIAL STRAIN; CARCINOGENESIS; CONTROLLED STUDY; ECOLOGICAL NICHE; ENZYME ACTIVITY; ENZYME INHIBITION; ESCHERICHIA COLI; GENE CLUSTER; IN VITRO STUDY; INTRASPECIFIC COMPETITION; PLANT CELL; PLANT IMMUNITY; PLANTA COINFECTION ASSAY; PRIORITY JOURNAL; PROTEIN MOTIF; PSEUDOMONAS AERUGINOSA; TYPE VI SECRETION SYSTEM; ANTIBIOSIS; BACTERIAL SECRETION SYSTEM; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SECRETION (PROCESS); TOBACCO; ANTIBACTERIAL ACTIVITY; BACTERIAL CELL; BIOFILM; DNA DEGRADATION; NONHUMAN; OPERON; PLANT PATHOGEN INTERACTION; PLANT TUMOR; PROTEOBACTERIA; TYPE IV SECRETION SYSTEM;

AGROBACTERIUM TUMEFACIENS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; PROKARYOTA; PROTEOBACTERIA; PSEUDOMONAS AERUGINOSA;

AGROBACTERIUM TUMEFACIENS; ANTI-BACTERIAL AGENTS; ANTIBIOSIS; BACTERIAL SECRETION SYSTEMS; DEOXYRIBONUCLEASES; ESCHERICHIA COLI; PSEUDOMONAS AERUGINOSA; TOBACCO; VIRULENCE FACTORS;

EID: 84904198712     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2014.06.002     Document Type: Article

References (55)

1. C.J. Alteri, S.D. Himpsl, S.R. Pickens, J.R. Lindner, J.S. Zora, J.E. Miller, P.D. Arno, S.W. Straight, and H.L. Mobley Multicellular bacteria deploy the type VI secretion system to preemptively strike neighboring cells PLoS Pathog. 9 2013 e1003608
2. C.E. Alvarez-Martinez, and P.J. Christie Biological diversity of prokaryotic type IV secretion systems Microbiol. Mol. Biol. Rev. 73 2009 775 808
3. D. An, T. Danhorn, C. Fuqua, and M.R. Parsek Quorum sensing and motility mediate interactions between Pseudomonas aeruginosa and Agrobacterium tumefaciens in biofilm cocultures Proc. Natl. Acad. Sci. USA 103 2006 3828 3833
4. A. Anand, Z. Vaghchhipawala, C.M. Ryu, L. Kang, K. Wang, O. del-Pozo, G.B. Martin, and K.S. Mysore Identification and characterization of plant genes involved in Agrobacterium-mediated plant transformation by virus-induced gene silencing Mol. Plant Microbe Interact. 20 2007 41 52
5. M. Basler, and J.J. Mekalanos Type 6 secretion dynamics within and between bacterial cells Science 337 2012 815
6. 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
7. M. Basler, B.T. Ho, and J.J. Mekalanos Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions Cell 152 2013 884 894
8. J. Benz, and A. Meinhart Antibacterial effector/immunity systems: it's just the tip of the iceberg Curr. Opin. Microbiol. 17 2014 1 10
9. G. Bönemann, A. Pietrosiuk, and A. Mogk Tubules and donuts: a type VI secretion story Mol. Microbiol. 76 2010 815 821
10. V. Braun, and S.I. Patzer Intercellular communication by related bacterial protein toxins: colicins, contact-dependent inhibitors, and proteins exported by the type VI secretion system FEMS Microbiol. Lett. 345 2013 13 21
11. 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
12. Y.R. Brunet, J. Hénin, H. Celia, and E. Cascales Type VI secretion and bacteriophage tail tubes share a common assembly pathway EMBO Rep. 15 2014 315 321
13. E. Cascales The type VI secretion toolkit EMBO Rep. 9 2008 735 741
14. 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
15. G. English, K. Trunk, V.A. Rao, V. Srikannathasan, W.N. Hunter, and S.J. Coulthurst New secreted toxins and immunity proteins encoded within the Type VI secretion system gene cluster of Serratia marcescens Mol. Microbiol. 86 2012 921 936
16. A. Filloux Microbiology: a weapon for bacterial warfare Nature 500 2013 284 285
17. A. Filloux, A. Hachani, and S. Bleves The bacterial type VI secretion machine: yet another player for protein transport across membranes Microbiology 154 2008 1570 1583
18. Y. Fu, M.K. Waldor, and J.J. Mekalanos Tn-Seq analysis of vibrio cholerae intestinal colonization reveals a role for T6SS-mediated antibacterial activity in the host Cell Host Microbe 14 2013 652 663
19. S.B. Gelvin Plant proteins involved in Agrobacterium-mediated genetic transformation Annu. Rev. Phytopathol. 48 2010 45 68
20. A. Hachani, N.S. Lossi, A. Hamilton, C. Jones, S. Bleves, D. Albesa-Jové, and A. Filloux Type VI secretion system in Pseudomonas aeruginosa: secretion and multimerization of VgrG proteins J. Biol. Chem. 286 2011 12317 12327
21. A. Hachani, N.S. Lossi, and A. Filloux A visual assay to monitor T6SS-mediated bacterial competition J. Vis. Exp. 73 2013 e50103
22. A. Hachani, L.P. Allsopp, Y. Oduko, and A. Filloux The VgrG proteins are "A la carte" delivery systems for bacterial type VI effectors J. Biol. Chem. 2014 10.1074/jbc.M114.563429
23. M.E. Hibbing, and C. Fuqua Inhibition and dispersal of Agrobacterium tumefaciens biofilms by a small diffusible Pseudomonas aeruginosa exoproduct(s) Arch. Microbiol. 194 2012 391 403
24. B.T. Ho, M. Basler, and J.J. Mekalanos Type 6 secretion system-mediated immunity to type 4 secretion system-mediated gene transfer Science 342 2013 250 253
25. B.T. Ho, T.G. Dong, and J.J. Mekalanos A view to a kill: the bacterial type VI secretion system Cell Host Microbe 15 2014 9 21
26. 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 et al. A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria Cell Host Microbe 7 2010 25 37
27. J.Y. Hu, Y. Fan, Y.H. Lin, H.B. Zhang, S.L. Ong, N. Dong, J.L. Xu, W.J. Ng, and L.H. Zhang Microbial diversity and prevalence of virulent pathogens in biofilms developed in a water reclamation system Res. Microbiol. 154 2003 623 629
28. C.I. Kado, and M.G. Heskett Selective media for isolation of Agrobacterium, Carynebacterium, Erwinia, Pseudomonas, and Xanthomonas Phytopathology 60 1970 969 976
29. N. Kapitein, G. Bönemann, A. Pietrosiuk, F. Seyffer, I. Hausser, J.K. Locker, and A. Mogk ClpV recycles VipA/VipB tubules and prevents non-productive tubule formation to ensure efficient type VI protein secretion Mol. Microbiol. 87 2013 1013 1028
30. S. Koskiniemi, J.G. Lamoureux, K.C. Nikolakakis, C. t'Kint de Roodenbeke, M.D. Kaplan, D.A. Low, and C.S. Hayes Rhs proteins from diverse bacteria mediate intercellular competition Proc. Natl. Acad. Sci. USA 110 2013 7032 7037
31. E.M. Lai, and C.I. Kado Processed VirB2 is the major subunit of the promiscuous pilus of Agrobacterium tumefaciens J. Bacteriol. 180 1998 2711 2717
32. 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
33. M. LeRoux, J.A. De Leon, N.J. Kuwada, A.B. Russell, D. Pinto-Santini, R.D. Hood, D.M. Agnello, S.M. Robertson, P.A. Wiggins, and J.D. Mougous Quantitative single-cell characterization of bacterial interactions reveals type VI secretion is a double-edged sword Proc. Natl. Acad. Sci. USA 109 2012 19804 19809
34. J.S. Lin, L.S. Ma, and E.M. Lai Systematic dissection of the agrobacterium type VI secretion system reveals machinery and secreted components for subcomplex formation PLoS ONE 8 2013 e67647
35. J.S. Lin, H.H. Wu, P.H. Hsu, L.S. Ma, Y.Y. Pang, M.D. Tsai, and E.M. Lai Fha interaction with phosphothreonine of TssL activates type VI secretion in Agrobacterium tumefaciens PLoS Pathog. 10 2014 e1003991
36. A.C. Liu, H.W. Shih, T. Hsu, and E.M. Lai A citrate-inducible gene, encoding a putative tricarboxylate transporter, is downregulated by the organic solvent DMSO in Agrobacterium tumefaciens J. Appl. Microbiol. 105 2008 1372 1383
37. N.S. Lossi, E. Manoli, A. Förster, R. Dajani, T. Pape, P. Freemont, and A. Filloux The HsiB1C1 (TssB-TssC) complex of the Pseudomonas aeruginosa type VI secretion system forms a bacteriophage tail sheathlike structure J. Biol. Chem. 288 2013 7536 7548
38. L, and its walker a motif is required for type VI secretion system-mediated Hcp secretion in Agrobacterium tumefaciens J. Bacteriol. 191 2009 4316 4329
39. L.S. Ma, F. Narberhaus, and E.M. Lai IcmF family protein TssM exhibits ATPase activity and energizes type VI secretion J. Biol. Chem. 287 2012 15610 15621
40. 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
41. L.G. Rahme, E.J. Stevens, S.F. Wolfort, J. Shao, R.G. Tompkins, and F.M. Ausubel Common virulence factors for bacterial pathogenicity in plants and animals Science 268 1995 1899 1902
42. 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
43. A.B. Russell, P. Singh, M. Brittnacher, N.K. Bui, R.D. Hood, M.A. Carl, D.M. Agnello, S. Schwarz, D.R. Goodlett, W. Vollmer, and J.D. Mougous A widespread bacterial type VI secretion effector superfamily identified using a heuristic approach Cell Host Microbe 11 2012 538 549
44. A.B. Russell, M. LeRoux, K. Hathazi, D.M. Agnello, T. Ishikawa, P.A. Wiggins, S.N. Wai, and J.D. Mougous Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors Nature 496 2013 508 512
45. A.B. Russell, S.B. Peterson, and J.D. Mougous Type VI secretion system effectors: poisons with a purpose Nat. Rev. Microbiol. 12 2014 137 148
46. C. Schmeisser, C. Stöckigt, C. Raasch, J. Wingender, K.N. Timmis, D.F. Wenderoth, H.C. Flemming, H. Liesegang, R.A. Schmitz, K.E. Jaeger, and W.R. Streit Metagenome survey of biofilms in drinking-water networks Appl. Environ. Microbiol. 69 2003 7298 7309
47. G. Shalom, J.G. Shaw, and M.S. Thomas In vivo expression technology identifies a type VI secretion system locus in Burkholderia pseudomallei that is induced upon invasion of macrophages Microbiology 153 2007 2689 2699
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. J. Troxler, P. Azelvandre, M. Zala, G. Defago, and D. Haas Conjugative transfer of chromosomal genes between fluorescent Pseudomonads in the rhizosphere of wheat Appl. Environ. Microbiol. 63 1997 213 219
50. L.M. Wenren, N.L. Sullivan, L. Cardarelli, A.N. Septer, and K.A. Gibbs Two independent pathways for self-recognition in Proteus mirabilis are linked by type VI-dependent export MBio. 4 2013 e00374-13
51. J.C. Whitney, S. Chou, A.B. Russell, J. Biboy, T.E. Gardiner, M.A. Ferrin, M. Brittnacher, W. Vollmer, and J.D. Mougous Identification, structure, and function of a novel type VI secretion peptidoglycan glycoside hydrolase effector-immunity pair J. Biol. Chem. 288 2013 26616 26624
52. J.C. Whitney, C.M. Beck, Y.A. Goo, A.B. Russell, B.N. Harding, J.A. De Leon, D.A. Cunningham, B.Q. Tran, D.A. Low, and D.R. Goodlett et al. Genetically distinct pathways guide effector export through the type VI secretion system Mol. Microbiol. 92 2014 529 542
53. H.Y. Wu, P.C. Chung, H.W. Shih, S.R. Wen, and E.M. Lai Secretome analysis uncovers an Hcp-family protein secreted via a type VI secretion system in Agrobacterium tumefaciens J. Bacteriol. 190 2008 2841 2850
54. C.F. Wu, J.S. Lin, G.C. Shaw, and E.M. Lai Acid-induced type VI secretion system is regulated by ExoR-ChvG/ChvI signaling cascade in Agrobacterium tumefaciens PLoS Pathog. 8 2012 e1002938
55. D. Zhang, R.F. de Souza, V. Anantharaman, L.M. Iyer, and L. Aravind Polymorphic toxin systems: Comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics Biol. Direct 7 2012 18