Biogenesis and structure of a type VI secretion membrane core complex

Nature

Volumn 523, Issue 7562, 2015, Pages 555-560

  Durand, Eric ^a,b,c   Nguyen, Van Son ^a,b   Zoued, Abdelrahim ^a   Logger, Laureen ^a   Péhau Arnaudet, Gérard ^c   Aschtgen, Marie Stéphanie ^a   Spinelli, Silvia ^a,b   Desmyter, Aline ^a,b   Bardiaux, Benjamin ^c   Dujeancourt, Annick ^c   Roussel, Alain ^a,b   Cambillau, Christian ^a,b   Cascales, Eric ^a   Fronzes, Rémi ^c  

^a AIX MARSEILLE UNIVERSITY   (France)

^b CNRS   (France)

^c INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; HEMOLYSIN CO REGULATED PROTEIN; UNCLASSIFIED DRUG; VALINE GLYCINE REPEAT PROTEIN G; BACTERIAL SECRETION SYSTEM; ESCHERICHIA COLI PROTEIN; LIPOPEPTIDE; MEMBRANE PROTEIN; MULTIPROTEIN COMPLEX; PROTEIN SUBUNIT; TSSJ PROTEIN, E COLI; TSSL PROTEIN, E COLI; TSSM PROTEIN, E COLI;

BACTERIUM; CRYSTAL STRUCTURE; CYTOPLASM; ELECTRON MICROSCOPY; INFECTIVITY; MEMBRANE; MICROBIAL ACTIVITY; PROTEIN; SECRETION;

ARTICLE; BACTERIAL CELL WALL; BACTERIAL INFECTION; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CHANNEL GATING; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; CYTOPLASM; ECOLOGICAL NICHE; ELECTRON MICROSCOPY; MEMBRANE STRUCTURE; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN DOMAIN; TYPE IV SECRETION SYSTEM; BACTERIAL SECRETION SYSTEM; BIOSYNTHESIS; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; ESCHERICHIA COLI; METABOLISM; PERIPLASM; POROSITY; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

BACTERIA (MICROORGANISMS);

BACTERIAL SECRETION SYSTEMS; CELL MEMBRANE; CRYSTALLOGRAPHY, X-RAY; CYTOPLASM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LIPOPEPTIDES; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PERIPLASM; POROSITY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS;

EID: 84938299015     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14667     Document Type: Article

References (75)

1. West, S. A., Griffin, A. S. & Gardner, A. Evolutionary explanations for cooperation. Curr. Biol. 17, 661-672 (2007).
2. Blango, M. G. & Mulvey, M. A. Bacterial landlines: contact-dependent signaling in bacterial populations. Curr. Opin. Microbiol. 12, 177-181 (2009).
3. Russell, A. B., Peterson, S. B. & Mougous, J. D. Type VI secretion system effectors: poisons with a purpose. Nature Rev. Microbiol. 12, 137-148 (2014).
4. Silverman, J.M., Brunet, Y. R., Cascales, E. &Mougous, J. D. Structure and regulation of the type VI secretion system. Annu. Rev. Microbiol. 66, 453-472 (2012).
5. Pukatzki, S., Ma, A. T., Revel, A. T., Sturtevant,D., & Mekalanos, J. J. Type VI secretion systemtranslocates a phage tail spike-like protein into target cells where it crosslinks actin. Proc. Natl Acad. Sci. USA 104, 15508-15513 (2007).
6. Russell, A. B. et al. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475, 343-347 (2011).
7. Russell, A. B. et al. Diverse type VI secretion phospholipases are functionally plastic antibacterial effectors. Nature 496, 508-512 (2013).
8. Ma, L. S., Hachani, A., Lin, J. S., Filloux, A. & Lai, E. M. Agrobacterium tumefaciens deploys a superfamily of type VI secretion DNase effectors as weapons for interbacterial competition in planta. Cell Host Microbe 16, 94-104 (2014).
9. Durand, E., Cambillau,C., Cascales, E., Journet, L., &Vgr,G. Tae, Tle,andbeyond: the versatile arsenal of Type VI secretion effectors. Trends Microbiol. 22, 498-507 (2014).
10. Borgeaud, S., Metzger, L. C., Scrignari, T. & Blokesch, M. Bacterial evolution. The type VI secretion systemof Vibrio cholerae fosters horizontal gene transfer. Science 347, 63-67 (2015).
11. Cascales, E. The type VI secretion toolkit. EMBO Rep. 9, 735-741 (2008).
12. Bönemann, G., Pietrosiuk, A., Diemand, A., Zentgraf, H. & Mogk, A. Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J. 28, 315-325 (2009).
13. 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).
14. Kudryashev, M. et al. Structure of the type VI secretion system contractile sheath. Cell 160, 952-962 (2015).
15. Coulthurst, S. J. The type VI secretion system-A widespread and versatile cell targeting system. Res. Microbiol. 164, 640-654 (2013).
16. Ho, B. T.,Dong, T. G., &Mekalanos, J. J. A view to a kill: the bacterial type VI secretion system. Cell Host Microbe 15, 9-21 (2014).
17. Zoued, A. et al. Architecture and assembly of the type VI secretion system. Biochim. Biophys. Acta 1843, 1664-1673 (2014).
18. Bönemann, G., Pietrosiuk, A. & Mogk, A. Tubules and donuts: a type VI secretion story. Mol. Microbiol. 76, 815-821 (2010).
19. 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).
20. Shneider, M. M. et al. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature 500, 350-353 (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. Aschtgen, M. S., Gavioli, M., Dessen, A., Lloubés, 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).
23. Aschtgen, M. S., Bernard, C. S., de Bentzmann, S., Lloubés, R. & Cascales, E. SciN is an outermembrane lipoprotein required for typeVI secretion in enteroaggregative Escherichia coli. J. Bacteriol. 190, 7523-7531 (2008).
24. Ma, L. S., Lin, J. S. & Lai, E. M. An IcmF family protein, ImpLM, is an integral inner membrane protein interacting with ImpKL, and its walker a motif is required for type VI secretion system-mediated Hcp secretion in Agrobacteriumtumefaciens. J. Bacteriol. 191, 4316-4329 (2009).
25. 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).
26. Ma, L. S., Narberhaus, F. & Lai, E. M. IcmF family protein TssM exhibits ATPase activity and energizes type VI secretion. J. Biol. Chem. 287, 15610-15621 (2012).
27. Aschtgen, M. S., Zoued, A., Lloubés, R., Journet, L. & Cascales, E. The C-tail anchored TssL subunit, an essential protein of the enteroaggregative Escherichia coli Sci-1 type VI secretion system, is inserted by YidC. MicrobiologyOpen 1, 71-82 (2012).
28. Durand, E. et al. Structural characterization and oligomerization of the TssL protein, a component shared bybacterial typeVI andtype IVb secretion systems. J. Biol. Chem. 287, 14157-14168 (2012).
29. Chang, J. H. & Kim, Y. G. Crystal structure of the bacterial type VI secretion system component TssL from Vibrio cholerae. J. Microbiol. 53, 32-37 (2015).
30. Kucukelbir, A., Sigworth, F. J. & Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nature Methods 11, 63-65 (2014).
31. Nguyen, V. S. et al. Production, crystallization and X-ray diffraction analysis of a complex between a fragment of the TssM T6SS protein and a camelid antibody. Acta Crystallogr F. 71, 266-271 (2015).
32. Nguyen, V. S. et al. Inhibition of type VI secretion by an anti-TssMllama nanobody. PLoS ONE 10, e0122187 (2015).
33. Diepold, A. et al. Deciphering the assembly of the Yersinia type III secretion injectisome. EMBO J. 29, 1928-1940 (2010).
34. Judd, P. K., Kumar, R. B. & Das, A. Spatial location and requirements for the assembly of the Agrobacteriumtumefaciens type IV secretion apparatus. Proc. Natl Acad. Sci. USA 102, 11498-11503 (2005).
35. Hardie, K. R., Lory, S. & Pugsley, A. P. Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO J. 15, 978-988 (1996).
36. Drake, S. L., Sandstedt, S. A. & Koomey, M. PilP, a pilus biogenesis lipoprotein in Neisseria gonorrhoeae, affects expression of PilQ as a high-molecular-mass multimer. Mol. Microbiol. 23, 657-668 (1997).
37. Burghout, P. et al. Role of the pilot protein YscW in the biogenesis of the YscC secretin in Yersinia enterocolitica. J. Bacteriol. 186, 5366-5375 (2004).
38. Crago, A. M. & Koronakis, V. Salmonella InvG forms a ring-like multimer that requires the InvH lipoprotein for outer membrane localization. Mol. Microbiol. 30, 47-56 (1998).
39. Daefler, S. & Russel, M. The Salmonella typhimurium InvH protein is an outer membrane lipoprotein required for the proper localization of InvG. Mol. Microbiol. 28, 1367-1380 (1998).
40. Brunet, Y. R., Bernard, C. S., Gavioli, M., Lloubés, 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).
41. Datsenko, K. A. & Wanner, B. L. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCRproducts. Proc.Natl Acad. Sci.USA97, 6640-6645 (2000).
42. 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).
43. van den Ent, F. & Löwe, J. RF cloning: a restriction-freemethod for inserting target genes into plasmids. J. Biochem. Biophys. Methods 67, 67-74 (2006).
44. Gueguen, E. & Cascales, E. Promoter swapping unveils the role of the Citrobacter rodentium CTS1 type VI secretion system in interbacterial competition. Appl. Environ. Microbiol. 79, 32-38 (2013).
45. Zaslaver, A. et al. A comprehensive library of fluorescent transcriptional reporters for Escherichia coli. Nature Methods 3, 623-628 (2006).
46. 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).
47. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
48. Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
49. Scheres, S. H. Semi-Automated selection of cryo-EM particles in RELION-1.3. J. Struct. Biol. 189, 114-122 (2015).
50. 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).
51. Kucukelbir, A., Sigworth, F. J. & Tagare, H. D. Quantifying the local resolution of cryo-EM density maps. Nature Methods 11, 63-65 (2014).
52. Pettersen, E. F. et al. UCSF Chimera-A visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612 (2004).
53. 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).
54. 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).
55. Guinier, A. La diffraction des rayons X aux trés petits angles; application á l'étude de phénoménes ultramicroscopiques. Ann. Phys. (Paris) 12, 161-237 (1939).
56. Svergun, D. I. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503 (1992).
57. 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).
58. Volkov, V. V. & Svergun, D. I. Uniqueness of ab initio shape determination in smallangle scattering. J. Appl. Crystallogr. 36, 860-864 (2003).
59. Kozin, M. B. & Svergun, D. I. Automated matching of high-And low-resolution structural models. J. Appl. Crystallogr. 34, 33-41 (2001).
60. Kabsch, W. XDS. Acta Crystallogr. D 66, 125-132 (2010).
61. Vagin, A. & Teplyakov, A. Molecular replacement with MOLREP. Acta Crystallogr. D 66, 22-25 (2010).
62. Blanc, E. et al. Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D 60, 2210-2221 (2004).
63. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486-501 (2010).
64. Winn, M. D., Murshudov, G. N. & Papiz, M. Z. Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol. 374, 300-321 (2003).
65. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010).
66. Krissinel, E., &Henrick, K. Inference ofmacromolecular assemblies fromcrystalline state. J. Mol. Biol. 372, 774-797 (2007).
67. The PyMOL Molecular Graphics System. v.1.5.0.4 (Schrödinger, LLC, 2014).
68. Chapman, M. S., Trzynka, A. & Chapman, B. K. Atomic modeling of cryo-electron microscopy reconstructions-joint refinement ofmodel and imaging parameters. J. Struct. Biol. 182, 10-21 (2013).
69. Sali, A. & Blundell, T. L. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234, 779-815 (1993).
70. Brunger,A. T.Version1.2 of theCrystallography andNMRsystem.Nature Protocols 2, 2728-2733 (2007).
71. Bogdanov, M., Zhang, W., Xie, J. & Dowhan, W. Transmembrane protein topology mapping by the substituted cysteine accessibility method (SCAMTM): application to lipid-specific membrane protein topogenesis. Methods 36, 148-171 (2005).
72. Goemaere, E. L., Devert, A., Lloubés, R. & Cascales, E. Movements of the TolR C-terminal domain depend on TolQR ionizable key residues and regulate activity of the Tol complex. J. Biol. Chem. 282, 17749-17757 (2007).
73. Du, D. et al. Structure of the AcrAB-TolC multidrug efflux pump. Nature 509, 512-515 (2014).
74. Hodgkinson, J. L. et al. Three-dimensional reconstruction of the Shigella T3SS transmembrane regions reveals 12-fold symmetry and novel features throughout. Nature Struct. Mol. Biol. 16, 477-485 (2009).
75. Low, H. H. et al. Structure of a type IV secretion system. Nature 508, 550-553 (2014).