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Structure of the bacteriophage φ29 DNA packaging motor

Nature volume 408, pages 745–750 (2000)Cite this article

Abstract

Motors generating mechanical force, powered by the hydrolysis of ATP, translocate double-stranded DNA into preformed capsids (proheads) of bacterial viruses1,2 and certain animal viruses3. Here we describe the motor that packages the double-stranded DNA of the Bacillus subtilis bacteriophage φ29 into a precursor capsid. We determined the structure of the head–tail connector—the central component of the φ29 DNA packaging motor—to 3.2 Å resolution by means of X-ray crystallography. We then fitted the connector into the electron densities of the prohead and of the partially packaged prohead as determined using cryo-electron microscopy and image reconstruction analysis. Our results suggest that the prohead plus dodecameric connector, prohead RNA, viral ATPase and DNA comprise a rotary motor with the head–prohead RNA–ATPase complex acting as a stator, the DNA acting as a spindle, and the connector as a ball-race. The helical nature of the DNA converts the rotary action of the connector into translation of the DNA.

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Figure 1: Cryo-EM reconstructions.
Figure 2: Connector structure ribbon diagrams.
Figure 3: Cryo-EM density fitted with atomic structures.
Figure 4: The DNA packaging mechanism.

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Acknowledgements

We thank J. Carrascosa for comments and discussions of this paper. We also thank the staff of CHESS, APS BioCARS and APS Structural Biology Center for assistance in data collection. This work was supported by the NSF (M.G.R.), the NIH (D.L.A. and T.S.B.), and an NSF Shared Instrumentation grant (T.S.B. and M.G.R).

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Author notes

  1. Paul J. Jardine

    Present address: Department of Biology, University of New Brunswick, Fredericton, E3B 6E1, New Brunswick, Canada

  2. Yizhi Tao

    Present address: Department of Molecular and Cellular Biology, Harvard University, 7 Divinity Avenue, Cambridge, Massachusetts, 02138, USA

  3. Alan A. Simpson, Yizhi Tao, Mohammed O. Badasso, Shelley Grimes and Dwight L. Anderson: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Biological Sciences, Purdue University, West Lafayette, 47907-1392, Indiana, USA

    Alan A. Simpson, Yizhi Tao, Petr G. Leiman, Yongning He, Norman H. Olson, Marc C. Morais, Timothy S. Baker & Michael G. Rossmann

  2. Departments of Microbiology and Oral Science, 18-246 Moos Tower, University of Minnesota, Minneapolis, 55455, Minnesota, USA

    Mohammed O. Badasso, Shelley Grimes & Dwight L. Anderson

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Correspondence to Michael G. Rossmann.

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Simpson, A., Tao, Y., Leiman, P. et al. Structure of the bacteriophage φ29 DNA packaging motor. Nature 408, 745–750 (2000). https://doi.org/10.1038/35047129

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