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A viral genome packaging ring-ATPase is a flexibly coordinated pentamer

Author

Listed:
  • Li Dai

    (The Catholic University of America)

  • Digvijay Singh

    (Johns Hopkins University School of Medicine
    University of Illinois at Urbana-Champaign
    University of California, San Diego)

  • Suoang Lu

    (University of Illinois at Urbana-Champaign)

  • Vishal I. Kottadiel

    (The Catholic University of America)

  • Reza Vafabakhsh

    (University of Illinois at Urbana-Champaign
    Northwestern University)

  • Marthandan Mahalingam

    (The Catholic University of America)

  • Yann R. Chemla

    (University of Illinois at Urbana-Champaign
    University of Illinois at Urbana-Champaign
    University of Illinois at Urbana-Champaign)

  • Taekjip Ha

    (Johns Hopkins University School of Medicine
    University of Illinois at Urbana-Champaign)

  • Venigalla B. Rao

    (The Catholic University of America)

Abstract

Multi-subunit ring-ATPases carry out a myriad of biological functions, including genome packaging in viruses. Though the basic structures and functions of these motors have been well-established, the mechanisms of ATPase firing and motor coordination are poorly understood. Here, using single-molecule fluorescence, we determine that the active bacteriophage T4 DNA packaging motor consists of five subunits of gp17. By systematically doping motors with an ATPase-defective subunit and selecting single motors containing a precise number of active or inactive subunits, we find that the packaging motor can tolerate an inactive subunit. However, motors containing one or more inactive subunits exhibit fewer DNA engagements, a higher failure rate in encapsidation, reduced packaging velocity, and increased pausing. These findings suggest a DNA packaging model in which the motor, by re-adjusting its grip on DNA, can skip an inactive subunit and resume DNA translocation, suggesting that strict coordination amongst motor subunits of packaging motors is not crucial for function.

Suggested Citation

  • Li Dai & Digvijay Singh & Suoang Lu & Vishal I. Kottadiel & Reza Vafabakhsh & Marthandan Mahalingam & Yann R. Chemla & Taekjip Ha & Venigalla B. Rao, 2021. "A viral genome packaging ring-ATPase is a flexibly coordinated pentamer," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26800-z
    DOI: 10.1038/s41467-021-26800-z
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    References listed on IDEAS

    as
    1. Mariam Ordyan & Istiaq Alam & Marthandan Mahalingam & Venigalla B. Rao & Douglas E. Smith, 2018. "Nucleotide-dependent DNA gripping and an end-clamp mechanism regulate the bacteriophage T4 viral packaging motor," Nature Communications, Nature, vol. 9(1), pages 1-9, December.
    2. Qianglin Fang & Wei-Chun Tang & Pan Tao & Marthandan Mahalingam & Andrei Fokine & Michael G. Rossmann & Venigalla B. Rao, 2020. "Structural morphing in a symmetry-mismatched viral vertex," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
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