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Nucleotide-dependent DNA gripping and an end-clamp mechanism regulate the bacteriophage T4 viral packaging motor

Author

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  • Mariam Ordyan

    (University of California, San Diego)

  • Istiaq Alam

    (The Catholic University of America)

  • Marthandan Mahalingam

    (The Catholic University of America)

  • Venigalla B. Rao

    (The Catholic University of America)

  • Douglas E. Smith

    (University of California, San Diego)

Abstract

ATP-powered viral packaging motors are among the most powerful biomotors known. Motor subunits arranged in a ring repeatedly grip and translocate the DNA to package viral genomes into capsids. Here, we use single DNA manipulation and rapid solution exchange to quantify how nucleotide binding regulates interactions between the bacteriophage T4 motor and DNA substrate. With no nucleotides, there is virtually no gripping and rapid slipping occurs with only minimal friction resisting. In contrast, binding of an ATP analog engages nearly continuous gripping. Occasional slips occur due to dissociation of the analog from a gripping motor subunit, or force-induced rupture of grip, but multiple other analog-bound subunits exert high friction that limits slipping. ADP induces comparably infrequent gripping and variable friction. Independent of nucleotides, slipping arrests when the end of the DNA is about to exit the capsid. This end-clamp mechanism increases the efficiency of packaging by making it essentially irreversible.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-07834-2
    DOI: 10.1038/s41467-018-07834-2
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    Cited by:

    1. 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.

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