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Atomistic basis of force generation, translocation, and coordination in a viral genome packaging motor.

Publication ,  Journal Article
Pajak, J; Dill, E; Reyes-Aldrete, E; White, MA; Kelch, BA; Jardine, PJ; Arya, G; Morais, MC
Published in: Nucleic acids research
June 2021

Double-stranded DNA viruses package their genomes into pre-assembled capsids using virally-encoded ASCE ATPase ring motors. We present the first atomic-resolution crystal structure of a multimeric ring form of a viral dsDNA packaging motor, the ATPase of the asccφ28 phage, and characterize its atomic-level dynamics via long timescale molecular dynamics simulations. Based on these results, and previous single-molecule data and cryo-EM reconstruction of the homologous φ29 motor, we propose an overall packaging model that is driven by helical-to-planar transitions of the ring motor. These transitions are coordinated by inter-subunit interactions that regulate catalytic and force-generating events. Stepwise ATP binding to individual subunits increase their affinity for the helical DNA phosphate backbone, resulting in distortion away from the planar ring towards a helical configuration, inducing mechanical strain. Subsequent sequential hydrolysis events alleviate the accumulated mechanical strain, allowing a stepwise return of the motor to the planar conformation, translocating DNA in the process. This type of helical-to-planar mechanism could serve as a general framework for ring ATPases.

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Published In

Nucleic acids research

DOI

EISSN

1362-4962

ISSN

0305-1048

Publication Date

June 2021

Volume

49

Issue

11

Start / End Page

6474 / 6488

Related Subject Headings

  • Viral Proteins
  • Viral Genome Packaging
  • Protein Subunits
  • Protein Structure, Tertiary
  • Protein Structure, Quaternary
  • Phosphates
  • Molecular Dynamics Simulation
  • Developmental Biology
  • Crystallography, X-Ray
  • Catalytic Domain
 

Citation

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Pajak, J., Dill, E., Reyes-Aldrete, E., White, M. A., Kelch, B. A., Jardine, P. J., … Morais, M. C. (2021). Atomistic basis of force generation, translocation, and coordination in a viral genome packaging motor. Nucleic Acids Research, 49(11), 6474–6488. https://doi.org/10.1093/nar/gkab372
Pajak, Joshua, Erik Dill, Emilio Reyes-Aldrete, Mark A. White, Brian A. Kelch, Paul J. Jardine, Gaurav Arya, and Marc C. Morais. “Atomistic basis of force generation, translocation, and coordination in a viral genome packaging motor.Nucleic Acids Research 49, no. 11 (June 2021): 6474–88. https://doi.org/10.1093/nar/gkab372.
Pajak J, Dill E, Reyes-Aldrete E, White MA, Kelch BA, Jardine PJ, et al. Atomistic basis of force generation, translocation, and coordination in a viral genome packaging motor. Nucleic acids research. 2021 Jun;49(11):6474–88.
Pajak, Joshua, et al. “Atomistic basis of force generation, translocation, and coordination in a viral genome packaging motor.Nucleic Acids Research, vol. 49, no. 11, June 2021, pp. 6474–88. Epmc, doi:10.1093/nar/gkab372.
Pajak J, Dill E, Reyes-Aldrete E, White MA, Kelch BA, Jardine PJ, Arya G, Morais MC. Atomistic basis of force generation, translocation, and coordination in a viral genome packaging motor. Nucleic acids research. 2021 Jun;49(11):6474–6488.
Journal cover image

Published In

Nucleic acids research

DOI

EISSN

1362-4962

ISSN

0305-1048

Publication Date

June 2021

Volume

49

Issue

11

Start / End Page

6474 / 6488

Related Subject Headings

  • Viral Proteins
  • Viral Genome Packaging
  • Protein Subunits
  • Protein Structure, Tertiary
  • Protein Structure, Quaternary
  • Phosphates
  • Molecular Dynamics Simulation
  • Developmental Biology
  • Crystallography, X-Ray
  • Catalytic Domain