A viral packaging motor varies its DNA rotation and step size to preserve subunit coordination as the capsid fills

Shixin Liu, Gheorghe Chistol, Craig L. Hetherington, Sara Tafoya, K. Aathavan, Joerg Schnitzbauer, Shelley Grimes, Paul J. Jardine, Carlos Bustamante

Research output: Contribution to journalArticlepeer-review

78 Scopus citations

Abstract

Multimeric, ring-shaped molecular motors rely on the coordinated action of their subunits to perform crucial biological functions. During these tasks, motors often change their operation in response to regulatory signals. Here, we investigate a viral packaging machine as it fills the capsid with DNA and encounters increasing internal pressure. We find that the motor rotates the DNA during packaging and that the rotation per base pair increases with filling. This change accompanies a reduction in the motor's step size. We propose that these adjustments preserve motor coordination by allowing one subunit to make periodic, specific, and regulatory contacts with the DNA. At high filling, we also observe the downregulation of the ATP-binding rate and the emergence of long-lived pauses, suggesting a throttling-down mechanism employed by the motor near the completion of packaging. This study illustrates how a biological motor adjusts its operation in response to changing conditions, while remaining highly coordinated.

Original languageEnglish (US)
Pages (from-to)702-713
Number of pages12
JournalCell
Volume157
Issue number3
DOIs
StatePublished - Apr 24 2014

Bibliographical note

Funding Information:
We thank T. Lionberger, N. Liu, J. Moffitt, and M. Sen for critical readings of the manuscript; Z. Bryant, A. Lee, C. Lee, J. Moffitt, M. Nöllmann, and D. Reid for help with preliminary experiments and analysis; J. Kittleson for plasmids; and L. Comolli, A. Edelstein, Y. Mejia, M. Morais, and S. Smith for discussions. This work is supported in part by the U.S. National Institutes of Health under grants R01-GM071552 (to C.B.) and R01-GM059604 (to S.G.), the U.S. Department of Energy under contract number DE-AC02-05CH11231 (to C.B.), and the Howard Hughes Medical Institute (to C.B.). S.L. acknowledges support from the NIH Pathway to Independence Award K99-GM107365.

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