A viral genome packaging motor transitions between cyclic and helical symmetry to translocate dsDNA

Michael Woodson; Joshua Pajak; Bryon P. Mahler; Wei Zhao; Wei Zhang; Gaurav Arya; Mark A. White; Paul J. Jardine; Marc Morais

doi:10.1126/sciadv.abc1955

A viral genome packaging motor transitions between cyclic and helical symmetry to translocate dsDNA

Michael Woodson, Joshua Pajak, Bryon P. Mahler, Wei Zhao, Wei Zhang, Gaurav Arya, Mark A. White, Paul J. Jardine, Marc Morais

Research output: Contribution to journal › Article › peer-review

26 Scopus citations

Abstract

Molecular segregation and biopolymer manipulation require the action of molecular motors to do work by applying directional forces to macromolecules. The additional strand conserved E (ASCE) ring motors are an ancient family of molecular motors responsible for diverse biological polymer manipulation tasks. Viruses use ASCE segregation motors to package their genomes into their protein capsids and provide accessible experimental systems due to their relative simplicity. We show by cryo-EM-focused image reconstruction that ASCE ATPases in viral double-stranded DNA (dsDNA) packaging motors adopt helical symmetry complementary to their dsDNA substrates. Together with previous data, our results suggest that these motors cycle between helical and planar configurations, providing a possible mechanism for directional translocation of DNA. Similar changes in quaternary structure have been observed for proteasome and helicase motors, suggesting an ancient and common mechanism of force generation that has been adapted for specific tasks over the course of evolution.

Original language	English (US)
Article number	eabc1955
Journal	Science Advances
Volume	7
Issue number	19
DOIs	https://doi.org/10.1126/sciadv.abc1955
State	Published - May 2021
Externally published	Yes

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title = "A viral genome packaging motor transitions between cyclic and helical symmetry to translocate dsDNA",

abstract = "Molecular segregation and biopolymer manipulation require the action of molecular motors to do work by applying directional forces to macromolecules. The additional strand conserved E (ASCE) ring motors are an ancient family of molecular motors responsible for diverse biological polymer manipulation tasks. Viruses use ASCE segregation motors to package their genomes into their protein capsids and provide accessible experimental systems due to their relative simplicity. We show by cryo-EM-focused image reconstruction that ASCE ATPases in viral double-stranded DNA (dsDNA) packaging motors adopt helical symmetry complementary to their dsDNA substrates. Together with previous data, our results suggest that these motors cycle between helical and planar configurations, providing a possible mechanism for directional translocation of DNA. Similar changes in quaternary structure have been observed for proteasome and helicase motors, suggesting an ancient and common mechanism of force generation that has been adapted for specific tasks over the course of evolution.",

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AU - Pajak, Joshua

AU - Mahler, Bryon P.

AU - Zhao, Wei

AU - Zhang, Wei

AU - Arya, Gaurav

AU - White, Mark A.

AU - Jardine, Paul J.

AU - Morais, Marc

N1 - Publisher Copyright: Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

PY - 2021/5

Y1 - 2021/5

N2 - Molecular segregation and biopolymer manipulation require the action of molecular motors to do work by applying directional forces to macromolecules. The additional strand conserved E (ASCE) ring motors are an ancient family of molecular motors responsible for diverse biological polymer manipulation tasks. Viruses use ASCE segregation motors to package their genomes into their protein capsids and provide accessible experimental systems due to their relative simplicity. We show by cryo-EM-focused image reconstruction that ASCE ATPases in viral double-stranded DNA (dsDNA) packaging motors adopt helical symmetry complementary to their dsDNA substrates. Together with previous data, our results suggest that these motors cycle between helical and planar configurations, providing a possible mechanism for directional translocation of DNA. Similar changes in quaternary structure have been observed for proteasome and helicase motors, suggesting an ancient and common mechanism of force generation that has been adapted for specific tasks over the course of evolution.

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A viral genome packaging motor transitions between cyclic and helical symmetry to translocate dsDNA

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