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Edited by Attila Szabo, NIH, Bethesda, MD, and approved February 12, 2019 (received for review October 21, 2018)
Significance
Biomolecular machines implement many vital activities in cells and must operate quickly and in functional directions, requiring energy dissipation. Recent experiments reveal that some evolved machines are quite energetically efficient, engendering interest in design principles that achieve such high efficiency. Recent theory predicts how to use equilibrium measurements (in the absence of driving) to design ways to drive a system to minimize energy dissipation. Here, we experimentally demonstrate the utility of this theory for designing efficient driving processes (“protocols”) by rapidly unfolding and folding single DNA hairpins. We show that such designed protocols systematically and significantly reduce energy dissipation over large variations of driving speed and DNA hairpin friction. Similar protocols may underlie the high efficiency observed in molecular machines.
Abstract
Cells must operate far from equilibrium, utilizing and dissipating energy continuously to maintain their organization and to avoid stasis and death. However, they must also avoid unnecessary waste of energy. Recent studies have revealed that molecular machines are extremely efficient thermodynamically compared with their macroscopic counterparts. However, the principles governing the efficient out-of-equilibrium operation of molecular machines remain a mystery. A theoretical framework has been recently formulated in which a generalized friction coefficient quantifies the energetic efficiency in nonequilibrium processes. Moreover, it posits that, to minimize energy dissipation, external control should drive the system along the reaction coordinate with a speed inversely proportional to the square root of that friction coefficient. Here, we demonstrate the utility of this theory for designing and understanding energetically efficient nonequilibrium processes through the unfolding and folding of single DNA hairpins.
Footnotes
↵1S.T. and S.J.L. contributed equally to this work.
↵2Present address: Scientific Application Development Group, Lumicks, Cambridge, MA 02139.
- ↵3To whom correspondence may be addressed. Email: carlosb{at}berkeley.edu or dsivak{at}sfu.ca.
Author contributions: S.T., S.J.L., S.L., C.B., and D.A.S. designed research; S.T. performed research; S.J.L. and D.A.S. analyzed data; and S.T., S.J.L., S.L., C.B., and D.A.S. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1817778116/-/DCSupplemental.
Published under the PNAS license.
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Using a system’s equilibrium behavior to reduce its energy dissipation in nonequilibrium processes
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