The Structure of the Salmonella Typhimurium Type III Secretion System Needle Shows Divergence from the Flagellar System

Overview

Journal J Mol Biol

Publisher Elsevier

Specialties Microbiology
Molecular Biology

Date 2010 Jan 12

PMID 20060835

Citations 26

Authors

Vitold E Galkin

Wolfgang H Schmied

Oliver Schraidt

Thomas C Marlovits

Edward H Egelman

Affiliations

Soon will be listed here.

Abstract

The type III secretion system (T3SS) is essential for the infectivity of many pathogenic Gram-negative bacteria. The T3SS contains proteins that form a channel in the inner and outer bacterial membranes, as well as an extracellular needle that is used for transporting and injecting effector proteins into a host cell. The homology between the T3SS and the bacterial flagellar system has been firmly established, based upon both sequence similarities between respective proteins in the two systems and the structural homology of higher-order assemblies. It has previously been shown that the Shigella flexneri needle has a helical symmetry of approximately 5.6 subunits/turn, which is quite similar to that of the most intensively studied flagellar filament (from Salmonella typhimurium), which has approximately 5.5 subunits/turn. We now show that the Sa. typhimurium needle, expected by homology arguments to be more similar to the Sa. typhimurium flagellar filament than is the needle from Shigella, actually has approximately 6.3 subunits/turn. It is not currently understood how host cell contact, made at the tip of the needle, is communicated to the secretory system at the base. In contrast to the Sa. typhimurium flagellar filament, which shows a nearly crystalline order, the Sa. typhimurium needle has a highly variable symmetry, which could be used to transmit information about host cell contact.

Citing Articles

Research Progress on Small Molecular Inhibitors of the Type 3 Secretion System.

Lv C, Li Y, Wei Y, Wang J, Yu H, Gao F Molecules. 2022; 27(23).

PMID: 36500441 PMC: 9740592. DOI: 10.3390/molecules27238348.

Cryo-EM of the injectisome and type III secretion systems.

Bergeron J, Marlovits T Curr Opin Struct Biol. 2022; 75:102403.

PMID: 35724552 PMC: 10114087. DOI: 10.1016/j.sbi.2022.102403.

Helical reconstruction of and needle filaments attached to type 3 basal bodies.

Kotov V, Lunelli M, Wald J, Kolbe M, Marlovits T Biochem Biophys Rep. 2021; 27:101039.

PMID: 34258394 PMC: 8254080. DOI: 10.1016/j.bbrep.2021.101039.

Type three secretion system in Salmonella Typhimurium: the key to infection.

Dos Santos A, Ferrari R, Conte-Junior C Genes Genomics. 2020; 42(5):495-506.

PMID: 32112371 DOI: 10.1007/s13258-020-00918-8.

The Injectisome, a Complex Nanomachine for Protein Injection into Mammalian Cells.

Lara-Tejero M, Galan J EcoSal Plus. 2019; 8(2).

PMID: 30942149 PMC: 6450406. DOI: 10.1128/ecosalplus.ESP-0039-2018.

References

Yonekura K, Maki-Yonekura S, Namba K . Complete atomic model of the bacterial flagellar filament by electron cryomicroscopy. Nature. 2003; 424(6949):643-50. DOI: 10.1038/nature01830. View

Egelman E . The iterative helical real space reconstruction method: surmounting the problems posed by real polymers. J Struct Biol. 2006; 157(1):83-94. DOI: 10.1016/j.jsb.2006.05.015. View

Kenjale R, Wilson J, Zenk S, Saurya S, Picking W, Picking W . The needle component of the type III secreton of Shigella regulates the activity of the secretion apparatus. J Biol Chem. 2005; 280(52):42929-37. DOI: 10.1074/jbc.M508377200. View

Marlovits T, Kubori T, Sukhan A, Thomas D, Galan J, Unger V . Structural insights into the assembly of the type III secretion needle complex. Science. 2004; 306(5698):1040-2. PMC: 1459965. DOI: 10.1126/science.1102610. View

Egelman E . A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy. 2000; 85(4):225-34. DOI: 10.1016/s0304-3991(00)00062-0. View

Blocker A, Komoriya K, Aizawa S . Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc Natl Acad Sci U S A. 2003; 100(6):3027-30. PMC: 152238. DOI: 10.1073/pnas.0535335100. View

Cordes F, Daniell S, Kenjale R, Saurya S, Picking W, Picking W . Helical packing of needles from functionally altered Shigella type III secretion systems. J Mol Biol. 2005; 354(2):206-11. DOI: 10.1016/j.jmb.2005.09.062. View

Yamashita I, Hasegawa K, Suzuki H, Vonderviszt F, Namba K . Structure and switching of bacterial flagellar filaments studied by X-ray fiber diffraction. Nat Struct Biol. 1998; 5(2):125-32. DOI: 10.1038/nsb0298-125. View

Deane J, Roversi P, Cordes F, Johnson S, Kenjale R, Daniell S . Molecular model of a type III secretion system needle: Implications for host-cell sensing. Proc Natl Acad Sci U S A. 2006; 103(33):12529-33. PMC: 1567912. DOI: 10.1073/pnas.0602689103. View

10.

Galkin V, Yu X, Bielnicki J, Heuser J, Ewing C, Guerry P . Divergence of quaternary structures among bacterial flagellar filaments. Science. 2008; 320(5874):382-5. DOI: 10.1126/science.1155307. View

11.

Wang Y, Ouellette A, Egan C, Rathinavelan T, Im W, De Guzman R . Differences in the electrostatic surfaces of the type III secretion needle proteins PrgI, BsaL, and MxiH. J Mol Biol. 2007; 371(5):1304-14. PMC: 1976599. DOI: 10.1016/j.jmb.2007.06.034. View

12.

Galan J . Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol. 2001; 17:53-86. DOI: 10.1146/annurev.cellbio.17.1.53. View

13.

Darboe N, Kenjale R, Picking W, Picking W, Middaugh C . Physical characterization of MxiH and PrgI, the needle component of the type III secretion apparatus from Shigella and Salmonella. Protein Sci. 2006; 15(3):543-52. PMC: 2249775. DOI: 10.1110/ps.051733506. View

14.

Kubori T, Sukhan A, Aizawa S, Galan J . Molecular characterization and assembly of the needle complex of the Salmonella typhimurium type III protein secretion system. Proc Natl Acad Sci U S A. 2000; 97(18):10225-30. PMC: 27824. DOI: 10.1073/pnas.170128997. View

15.

Desvaux M, Hebraud M, Henderson I, Pallen M . Type III secretion: what's in a name?. Trends Microbiol. 2006; 14(4):157-60. DOI: 10.1016/j.tim.2006.02.009. View

16.

Galkin V, Orlova A, Cherepanova O, Lebart M, Egelman E . High-resolution cryo-EM structure of the F-actin-fimbrin/plastin ABD2 complex. Proc Natl Acad Sci U S A. 2008; 105(5):1494-8. PMC: 2234172. DOI: 10.1073/pnas.0708667105. View

17.

Wall J, Hainfeld J . Mass mapping with the scanning transmission electron microscope. Annu Rev Biophys Biophys Chem. 1986; 15:355-76. DOI: 10.1146/annurev.bb.15.060186.002035. View

18.

Fujii T, Kato T, Namba K . Specific arrangement of alpha-helical coiled coils in the core domain of the bacterial flagellar hook for the universal joint function. Structure. 2009; 17(11):1485-93. DOI: 10.1016/j.str.2009.08.017. View

19.

Cordes F, Komoriya K, Larquet E, Yang S, Egelman E, Blocker A . Helical structure of the needle of the type III secretion system of Shigella flexneri. J Biol Chem. 2003; 278(19):17103-7. DOI: 10.1074/jbc.M300091200. View