Mechanism of force generation of a viral DNA packaging motor

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

Research output: Contribution to journalArticlepeer-review

235 Scopus citations

Abstract

A large family of multimeric ATPases are involved in such diverse tasks as cell division, chromosome segregation, DNA recombination, strand separation, conjugation, and viral genome packaging. One such system is the Bacillus subtilis phage φ29 DNA packaging motor, which generates large forces to compact its genome into a small protein capsid. Here we use optical tweezers to study, at the single-molecule level, the mechanism of force generation in this motor. We determine the kinetic parameters of the packaging motor and their dependence on external load to show that DNA translocation does not occur during ATP binding but is likely triggered by phosphate release. We also show that the motor subunits act in a coordinated, successive fashion with high processivity. Finally, we propose a minimal mechanochemical cycle of this DNA-translocating ATPase that rationalizes all of our findings.

Original languageEnglish (US)
Pages (from-to)683-692
Number of pages10
JournalCell
Volume122
Issue number5
DOIs
StatePublished - Sep 9 2005

Bibliographical note

Funding Information:
We thank S.B. Smith, D.E. Smith, S.J. Tans, N.R. Forde, Z.D. Bryant, S. Dumont, J. Gore, J. Erzberger, J. Berger, O. Igoshin, J.-C. Liao, G. Oster, and L. Aravind for helpful discussion. This research was supported in part by grants from NIH GM-071552 (C.B.), NIH DE-03606 (D.L.A.), NIH GM-059604 (S.G.), DOE DE-AC03-76DF00098 (C.B.), and the Packard Foundation 1999-8325 (C.B.). Y.R.C. is supported by a National Research Service Award fellowship from NIH GM-65786 and a Career Award at the Scientific Interface from the Burroughs Wellcome Fund. K.A. is supported by the Program in Mathematics and Molecular Biology through a Burroughs Wellcome Fund fellowship.

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