Bending friction: a new mechanism of dissipation within DNA explains its slow looping dynamics.

Abstract

DNA bending and looping is crucial for gene expression, packaging, and chromatin organisation, as well as the design of artificial nanomaterials and devices. But what determines how quickly DNA bends? While DNAs static flexibility is well-characterised by its persistence length, we lack an understanding of how quickly DNA responds to mechanical forces: remarkably current semiflexible polymer theory based on solvent dissipation underestimates spontaneous looping times by ~1000-fold. By analysing fluctuations of DNA several kilobases long and developing new theory for bending dissipation in semiflexible polymers, we show DNA bending dynamics cannot be explained by solvent friction alone and requires significant contributions from intramolecular friction. The theory defines a new material constant of DNA -- the bending friction, which we determine to be{zeta} B = 241 {+/-} 17 g nm3/ms. Strikingly, our measurement does not depend on the buffer ionic conditions. We predict bending friction will dominate DNA dynamics between {approx} 50 nm and 420 nm and significantly longer under external force. We show that mean first passage time calculations are greatly simplified when bending friction dominates and so using this constant, with no fitting parameters, we accurately predict the slow experimental spontaneous looping times. Our discovery of significant bending dissipation is unexpected as DNA has no obvious large (> kBT) internal energy barriers. The salt-independence of this dissipation also rules out long range electrostatic interactions as its origins. Instead our findings point to a complex local energy landscape for bending and a potential previously unappreciated role of water binding DNA constraining its local mobility. Our findings radically change our understanding of DNA dynamics and reveal DNA as a viscoelastic semiflexible polymer with dramatically slower dynamics compared to an ideal elastic rod. This work establishes bending friction as a fundamental material property that must underpin any model of DNA dynamics in biology, physics, and nanotechnology.