Intersubunit coordination in a homomeric ring ATPase

Jeffrey R. Moffitt, Yann R. Chemla, K. Aathavan, Shelley Grimes, Paul J. Jardine, Dwight L. Anderson, Carlos Bustamante

Research output: Contribution to journalArticlepeer-review

199 Scopus citations

Abstract

Homomeric ring ATPases perform many vital and varied tasks in the cell, ranging from chromosome segregation to protein degradation. Here we report the direct observation of the intersubunit coordination and step size of such a ring ATPase, the double-stranded-DNA packaging motor in the bacteriophage φ29. Using high-resolution optical tweezers, we find that packaging occurs in increments of 10 base pairs (bp). Statistical analysis of the preceding dwell times reveals that multiple ATPs bind during each dwell, and application of high force reveals that these 10-bp increments are composed of four 2.5-bp steps. These results indicate that the hydrolysis cycles of the individual subunits are highly coordinated by means of a mechanism novel for ring ATPases. Furthermore, a step size that is a non-integer number of base pairs demands new models for motor-DNA interactions.

Original languageEnglish (US)
Pages (from-to)446-450
Number of pages5
JournalNature
Volume457
Issue number7228
DOIs
StatePublished - Jan 22 2009

Bibliographical note

Funding Information:
Acknowledgements We thank C. L. Hetherington, M. Nollmann and G. Chistol for a critical reading of the manuscript; C. L. Hetherington, A. Politzer, M. Strycharska, M. Kopaczynska and J. Yu for critical discussions; and J. Choy, S. Grill and S. Smith for advice regarding instrumentation. J.R.M. acknowledges the National Science Foundation’s Graduate Research Fellowship and Y.R.C. the Burroughs Welcome Fund’s Career Awards at the Scientific Interface for funding. This research was supported in part by NIH grants GM-071552, DE-003606 and GM-059604. The content of this paper is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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