Role of Bacteriophage T4 Baseplate in Regulating Assembly and Infection

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2016 Mar 2

PMID 26929357

Citations 48

Authors

Moh Lan Yap

Thomas Klose

Fumio Arisaka

Jeffrey A Speir

David Veesler

Andrei Fokine

Michael G Rossmann

Affiliations

Soon will be listed here.

Abstract

Bacteriophage T4 consists of a head for protecting its genome and a sheathed tail for inserting its genome into a host. The tail terminates with a multiprotein baseplate that changes its conformation from a "high-energy" dome-shaped to a "low-energy" star-shaped structure during infection. Although these two structures represent different minima in the total energy landscape of the baseplate assembly, as the dome-shaped structure readily changes to the star-shaped structure when the virus infects a host bacterium, the dome-shaped structure must have more energy than the star-shaped structure. Here we describe the electron microscopy structure of a 3.3-MDa in vitro-assembled star-shaped baseplate with a resolution of 3.8 Å. This structure, together with other genetic and structural data, shows why the high-energy baseplate is formed in the presence of the central hub and how the baseplate changes to the low-energy structure, via two steps during infection. Thus, the presence of the central hub is required to initiate the assembly of metastable, high-energy structures. If the high-energy structure is formed and stabilized faster than the low-energy structure, there will be insufficient components to assemble the low-energy structure.

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References

Urig M, Brown S, Tedesco P, Wood W . Attachment of tail fibers in bacteriophage T4 assembly. Identification of the baseplate protein to which tail fibers attach. J Mol Biol. 1983; 169(2):427-37. DOI: 10.1016/s0022-2836(83)80059-x. View

Yap M, Rossmann M . Structure and function of bacteriophage T4. Future Microbiol. 2014; 9(12):1319-27. PMC: 4275845. DOI: 10.2217/fmb.14.91. View

Scheres S . RELION: implementation of a Bayesian approach to cryo-EM structure determination. J Struct Biol. 2012; 180(3):519-30. PMC: 3690530. DOI: 10.1016/j.jsb.2012.09.006. View

Basler M, Pilhofer M, Henderson G, Jensen G, Mekalanos J . Type VI secretion requires a dynamic contractile phage tail-like structure. Nature. 2012; 483(7388):182-6. PMC: 3527127. DOI: 10.1038/nature10846. View

Henderson R, Sali A, Baker M, Carragher B, Devkota B, Downing K . Outcome of the first electron microscopy validation task force meeting. Structure. 2012; 20(2):205-14. PMC: 3328769. DOI: 10.1016/j.str.2011.12.014. View

Leiman P, Arisaka F, van Raaij M, Kostyuchenko V, Aksyuk A, Kanamaru S . Morphogenesis of the T4 tail and tail fibers. Virol J. 2010; 7:355. PMC: 3004832. DOI: 10.1186/1743-422X-7-355. View

Holm L, Rosenstrom P . Dali server: conservation mapping in 3D. Nucleic Acids Res. 2010; 38(Web Server issue):W545-9. PMC: 2896194. DOI: 10.1093/nar/gkq366. View

Adams P, Afonine P, Bunkoczi G, Chen V, Davis I, Echols N . PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr. 2010; 66(Pt 2):213-21. PMC: 2815670. DOI: 10.1107/S0907444909052925. View

Hood R, Singh P, Hsu F, Guvener T, Carl M, Trinidad R . A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe. 2010; 7(1):25-37. PMC: 2831478. DOI: 10.1016/j.chom.2009.12.007. View

10.

Yap M, Klose T, Plevka P, Aksyuk A, Zhang X, Arisaka F . Structure of the 3.3MDa, in vitro assembled, hubless bacteriophage T4 baseplate. J Struct Biol. 2014; 187(2):95-102. PMC: 4130566. DOI: 10.1016/j.jsb.2014.06.008. View

11.

Guo F, Jiang W . Single particle cryo-electron microscopy and 3-D reconstruction of viruses. Methods Mol Biol. 2013; 1117:401-43. PMC: 4020923. DOI: 10.1007/978-1-62703-776-1_19. View

12.

Maxwell K, Fatehi Hassanabad M, Chang T, Paul V, Pirani N, Bona D . Structural and functional studies of gpX of Escherichia coli phage P2 reveal a widespread role for LysM domains in the baseplates of contractile-tailed phages. J Bacteriol. 2013; 195(24):5461-8. PMC: 3889624. DOI: 10.1128/JB.00805-13. View

13.

Chen S, McMullan G, Faruqi A, Murshudov G, Short J, Scheres S . High-resolution noise substitution to measure overfitting and validate resolution in 3D structure determination by single particle electron cryomicroscopy. Ultramicroscopy. 2013; 135:24-35. PMC: 3834153. DOI: 10.1016/j.ultramic.2013.06.004. View

14.

Li X, Mooney P, Zheng S, Booth C, Braunfeld M, Gubbens S . Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat Methods. 2013; 10(6):584-90. PMC: 3684049. DOI: 10.1038/nmeth.2472. View

15.

Fokine A, Zhang Z, Kanamaru S, Bowman V, Aksyuk A, Arisaka F . The molecular architecture of the bacteriophage T4 neck. J Mol Biol. 2013; 425(10):1731-44. PMC: 3746776. DOI: 10.1016/j.jmb.2013.02.012. View

16.

Ge P, Scholl D, Leiman P, Yu X, Miller J, Zhou Z . Atomic structures of a bactericidal contractile nanotube in its pre- and postcontraction states. Nat Struct Mol Biol. 2015; 22(5):377-82. PMC: 4445970. DOI: 10.1038/nsmb.2995. View

17.

Hu B, Margolin W, Molineux I, Liu J . Structural remodeling of bacteriophage T4 and host membranes during infection initiation. Proc Natl Acad Sci U S A. 2015; 112(35):E4919-28. PMC: 4568249. DOI: 10.1073/pnas.1501064112. View

18.

Kikuchi Y, King J . Genetic control of bacteriophage T4 baseplate morphogenesis. II. Mutants unable to form the central part of the baseplate. J Mol Biol. 1975; 99(4):673-94. DOI: 10.1016/s0022-2836(75)80179-3. View

19.

Kostyuchenko V, Navruzbekov G, Kurochkina L, Strelkov S, Mesyanzhinov V, Rossmann M . The structure of bacteriophage T4 gene product 9: the trigger for tail contraction. Structure. 1999; 7(10):1213-22. DOI: 10.1016/s0969-2126(00)80055-6. View

20.

Ferguson P, Coombs D . Pulse-chase analysis of the in vivo assembly of the bacteriophage T4 tail. J Mol Biol. 2000; 297(1):99-117. DOI: 10.1006/jmbi.2000.3551. View