Priming and polymerization of a bacterial contractile tail structure

Nature

Volumn 531, Issue 7592, 2016, Pages 59-63

  Zoued, Abdelrahim ^a   Durand, Eric ^a,b,c,d   Brunet, Yannick R ^a,g   Spinelli, Silvia ^b,c   Douzi, Badreddine ^a,b,c   Guzzo, Mathilde ^e   Flaugnatti, Nicolas ^a   Legrand, Pierre ^f   Journet, Laure ^a   Fronzes, Rémi ^d   Mignot, Tâm ^e   Cambillau, Christian ^b,c   Cascales, Eric ^a  

^a CNRS and Aix Marseille University   (France)

^b CNRS   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d INSTITUT PASTEUR   (France)

^e AIX MARSEILLE UNIVERSITÉ   (France)

^f SYNCHROTRON SOLEIL   (France)

^g HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CONTRACTILE PROTEIN; CORE PROTEIN; ESCHERICHIA COLI PROTEIN; TSSA PROTEIN, E COLI; TYPE VI SECRETION SYSTEM;

BACTERIUM; CELLS AND CELL COMPONENTS; MEMBRANE; POLYMERIZATION; PROTEIN; SECRETION; TOXIN;

ARTICLE; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; ELECTRON MICROSCOPY; ENTEROAGGREGATIVE ESCHERICHIA COLI; FLUORESCENCE LIFETIME IMAGING MICROSCOPY; FLUORESCENCE MICROSCOPY; MEMBRANE; MICROSCOPY; MITOCHONDRIAL BIOGENESIS; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN STRUCTURE; TAIL; TYPE VI SECRETION SYSTEM; X RAY CRYSTALLOGRAPHY; CHEMICAL STRUCTURE; CHEMISTRY; ESCHERICHIA COLI; METABOLISM; PROTEIN TERTIARY STRUCTURE; ULTRASTRUCTURE;

ASTEROIDEA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MICROSCOPY, ELECTRON; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; POLYMERIZATION; PROTEIN STRUCTURE, TERTIARY; TYPE VI SECRETION SYSTEMS;

EID: 84960192253     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature17182     Document Type: Article

References (56)

1. Leiman, P. G. & Shneider, M. M. Contractile tail machines of bacteriophages. Adv. Exp. Med. Biol. 726, 93-114 (2012).
2. Ge, P. et al. Atomic structures of a bactericidal contractile nanotube in its pre- and postcontraction states. Nature Struct. Mol. Biol. 22, 377-382 (2015).
3. Bönemann, G., Pietrosiuk, A. & Mogk, A. Tubules and donuts: a type VI secretion story. Mol. Microbiol. 76, 815-821 (2010).
4. Yang, G., Dowling, A. J., Gerike, U. ffrench-Constant, R. H. & Waterfield, N. R. Photorhabdus virulence cassettes confer injectable insecticidal activity against the wax moth. J. Bacteriol. 188, 2254-2261 (2006).
5. Shikuma, N. J. et al. Marine tubeworm metamorphosis induced by arrays of bacterial phage tail-like structures. Science 343, 529-533 (2014).
6. Heymann, J. B. et al. Three-dimensional structure of the toxin-delivery particle antifeeding prophage of Serratia entomophila. J. Biol. Chem. 288, 25276-25284 (2013).
7. Kube, S. & Wendler, P. Structural comparison of contractile nanomachines. AIMS Biophysics. 2, 88-115 (2015).
8. Leiman, P. G. et al. Morphogenesis of the T4 tail and tail fibers. Virol. J. 7, 355 (2010).
9. Ferguson, P. L. & Coombs, D. H. Pulse-chase analysis of the in vivo assembly of the bacteriophage T4 tail. J. Mol. Biol. 297, 99-117 (2000).
10. Rybakova, D. et al. Role of antifeeding prophage (Afp) protein Afp16 in terminating the length of the Afp tailocin and stabilizing its sheath. Mol. Microbiol. 89, 702-714 (2013).
11. Aschtgen, M. S., Gavioli, M., Dessen, A., Lloubès, R. & Cascales, E. The SciZ protein anchors the enteroaggregative Escherichia coli Type VI secretion system to the cell wall. Mol. Microbiol. 75, 886-899 (2010).
12. Felisberto-Rodrigues, C. et al. 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 (2011).
13. Durand, E. et al. Biogenesis and structure of the Type VI secretion membrane core complex. Nature 523, 555-560 (2015).
14. Zoued, A. et al. Architecture and assembly of the Type VI secretion system. Biochim. Biophys. Acta 1843, 1664-1673 (2014).
15. Brunet, Y. R., Hénin, J., Celia, H. & Cascales, E. Type VI secretion and bacteriophage tail tubes share a common assembly pathway. EMBO Rep. 15, 315-321 (2014).
16. 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).
17. 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).
18. English, G., Byron, O., Cianfanelli, F. R., Prescott, A. R. & Coulthurst, S. J. Biochemical analysis of TssK, a core component of the bacterial Type VI secretion system, reveals distinct oligomeric states of TssK and identifies a TssK-TssFG subcomplex. Biochem. J. 461, 291-304 (2014).
19. Brunet, Y. R., Zoued, A., Boyer, F., Douzi, B. & Cascales, E. The Type VI secretion TssEFGK-VgrG phage-like baseplate is recruited to the TssJLM membrane complex via multiple contacts and serves as assembly platform for tail tube/sheath polymerization. PLoS Genet. 11, e1005545 (2015).
20. Basler, M., Ho, B. T. & Mekalanos, J. J. Tit-for-tat: type VI secretion system counterattack during bacterial cell-cell interactions. Cell 152, 884-894 (2013).
21. Brunet, Y. R., Espinosa, L., Harchouni, S., Mignot, T. & Cascales, E. Imaging type VI secretion-mediated bacterial killing. Cell Rep. 3, 36-41 (2013).
22. Kube, S. et al. Structure of the VipA/B type VI secretion complex suggests a contraction-state-specific recycling mechanism. Cell Rep. 8, 20-30 (2014).
23. Kudryashev, M. et al. Structure of the type VI secretion system contractile sheath. Cell 160, 952-962 (2015).
24. Kapitein, N. et al. ClpV recycles VipA/VipB tubules and prevents nonproductive tubule formation to ensure efficient type VI protein secretion. Mol. Microbiol. 87, 1013-1028 (2013).
25. Zoued, A. et al. 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 (2013).
26. King, J. Assembly of the tail of bacteriophage T4. J. Mol. Biol. 32, 231-262 (1968).
27. Vegge, C. S. et al. Structural characterization and assembly of the distal tail structure of the temperate lactococcal bacteriophage TP901-1. J. Bacteriol. 187, 4187-4197 (2005).
28. Pell, L. G. et al. The X-ray crystal structure of the phage λ tail terminator protein reveals the biologically relevant hexameric ring structure and demonstrates a conserved mechanism of tail termination among diverse long-tailed phages. J. Mol. Biol. 389, 938-951 (2009).
29. Fokine, A. et al. The molecular architecture of the bacteriophage T4 neck. J. Mol. Biol. 425, 1731-1744 (2013).
30. Yonekura, K. et al. The bacterial flagellar cap as the rotary promoter of flagellin self-assembly. Science 290, 2148-2152 (2000).
31. Brunet, Y. R., Bernard, C. S., Gavioli, M., Lloubès, 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).
32. Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl Acad. Sci. USA 97, 6640-6645 (2000).
33. Chaveroche, M. K., Ghigo, J. M. & d'Enfert, C. A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res. 28, E97 (2000).
34. van den Ent, F. & Löwe, J. RF cloning: a restriction-free method for inserting target genes into plasmids. J. Biochem. Biophys. Methods 67, 67-74 (2006).
35. Karimova, G., Pidoux, J., Ullmann, A. & Ladant, D. A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc. Natl Acad. Sci. USA 95, 5752-5756 (1998).
36. Battesti, A. & Bouveret, E. The bacterial two-hybrid system based on adenylate cyclase reconstitution in Escherichia coli. Methods 58, 325-334 (2012).
37. Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nature Methods 9, 676-682 (2012).
38. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
39. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
40. Scheres, S. H. Semi-automated selection of cryo-EM particles in RELION-1.3. J. Struct. Biol. 189, 114-122 (2015).
41. Chen, S. et al. High-resolution noise substitution to measure overfitting and validate resolution in 3D structure determination by single particle electron cryomicroscopy. Ultramicroscopy 135, 24-35 (2013).
42. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, M. H. & Svergun, D. I. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282 (2003).
43. Konarev, P. V., Petoukhov, M. V., Volkov, V. V. & Svergun, D. I. ATSAS 2.1, a program package for small-angle scattering data analysis. J. Appl. Crystallogr. 39, 277-286 (2006).
44. Guinier, A. La diffraction des rayons X aux très petits angles; application à l'étude de phénomènes ultramicroscopiques. Ann. Phys. (Paris) 12, 161-237 (1939).
45. Svergun, D. I. Determination of the regularization parameter in indirecttransform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503 (1992).
46. Franke, D. & Svergun, D. I. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J. Appl. Crystallogr. 42, 342-346 (2009).
47. Volkov, V. V. & Svergun, D. I. Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 36, 860-864 (2003).
48. Kozin, M. B. & Svergun, D. I. Automated matching of high- and low-resolution structural models. J. Appl. Crystallogr. 34, 33-41 (2001).
49. Kabsch, W. XDS. Acta Crystallogr. D 66, 125-132 (2010).
50. Schneider, T. R. & Sheldrick, G. M. Substructure solution with SHELXD. Acta Crystallogr. D 58, 1772-1779 (2002).
51. Blanc, E. et al. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D 60, 2210-2221 (2004).
52. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004).
53. DeLano, W.L. The PyMOL Molecular Graphics System, Version 1.8 Schrödinger, LLC.
54. Pettersen, E. F. et al. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
55. Gerc, A. J. et al. Visualization of the Serratia Type VI secretion system reveals unprovoked attacks and dynamic assembly. Cell Rep. 12, 2131-2142 (2015).
56. Douzi, B. et al. Crystal structure and self-interaction of the type VI secretion tail-tube protein from enteroaggregative Escherichia coli. PLoS ONE 9, e86918 (2014).