A DNA packaging motor inchworms along one strand allowing it to adapt to alternative double-helical structures

Juan P. Castillo, Alexander B. Tong, Sara Tafoya, Paul J. Jardine, Carlos Bustamante

Research output: Contribution to journalArticlepeer-review

Abstract

Ring ATPases that translocate disordered polymers possess lock-washer architectures that they impose on their substrates during transport via a hand-over-hand mechanism. Here, we investigate the operation of ring motors that transport ordered, helical substrates, such as the bacteriophage ϕ29 dsDNA packaging motor. This pentameric motor alternates between an ATP loading dwell and a hydrolysis burst wherein it packages one turn of DNA in four steps. When challenged with DNA-RNA hybrids and dsRNA, the motor matches its burst to the shorter helical pitches, keeping three power strokes invariant while shortening the fourth. Intermittently, the motor loses grip on the RNA-containing substrates, indicating that it makes optimal load-bearing contacts with dsDNA. To rationalize these observations, we propose a helical inchworm translocation mechanism in which, during each cycle, the motor increasingly adopts a lock-washer structure during the ATP loading dwell and successively regains its planar form with each power stroke during the burst.

Original languageEnglish (US)
Article number3439
JournalNature communications
Volume12
Issue number1
DOIs
StatePublished - Jun 8 2021

Bibliographical note

Funding Information:
We thank all members of the Bustamante laboratory for insightful discussions, and Grace Hsu for animation work. This research was supported by the Nanomachines program (KC1203) funded by the Office of Basic Energy Sciences of the U.S. Department of Energy (DOE) contract number DE-AC02-05CH11231 (laser-tweezer force measurements) and by the National Institute of Health grants R01GM032543 (nucleic acid purification and amplification) and GM122979 (protein purification). C.B. is a Howard Hughes Medical Institute investigator. J.P.C. acknowledges support from the PEW Latin American Fellows program in the biomedical sciences.

Publisher Copyright:
© 2021, The Author(s).

PubMed: MeSH publication types

  • Journal Article
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

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