Stretching self-entangled DNA molecules in elongational fields.

We present experiments of self-entangled DNA molecules stretching under a planar elongational field, and their stretching dynamics are compared to identical molecules without entanglements. Self-entangled molecules stretch in a stage-wise fashion, persisting in an "arrested" state for decades of strain prior to rapidly stretching, slowing down the stretching dynamics by an order of magnitude compared to unentangled molecules. Self-entangled molecules are shown to proceed through a transient state where one or two ends of the molecule are protruding from an entangled, knotted core. This phenomenon sharply contrasts with the wide array of transient configurations shown here and by others for stretching polymers without entanglements. The rate at which self-entangled molecules stretch through this transient state is demonstrably slower than unentangled molecules, providing the first direct experimental evidence of a topological friction. These experimental observations are shown to be qualitatively and semi-quantitatively reproduced by a dumbbell model with two fitting parameters, the values of which are reasonable in light of previous experiments of knotted DNA.

[1]  Daniel W. Trahan,et al.  Coil-stretch Transition of DNA Molecules in Slit-like Confinement. , 2010, Macromolecules.

[2]  P. Pierański,et al.  Tight open knots , 2001, physics/0103016.

[3]  C. Micheletti,et al.  Driving knots on DNA with AC/DC electric fields: topological friction and memory effects. , 2014, Soft matter.

[4]  Patrick S Doyle,et al.  Methods to electrophoretically stretch DNA: microcontractions, gels, and hybrid gel-microcontraction devices. , 2006, Lab on a chip.

[5]  C Micheletti,et al.  Topological jamming of spontaneously knotted polyelectrolyte chains driven through a nanopore. , 2012, Physical review letters.

[6]  Jie Yan,et al.  Effect of YOYO-1 on the mechanical properties of DNA. , 2014, Soft matter.

[7]  Patrick S Doyle,et al.  Permeation-driven flow in poly(dimethylsiloxane) microfluidic devices. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[8]  R. Larson,et al.  Brownian dynamics simulations of a DNA molecule in an extensional flow field , 1999 .

[9]  Anthony Balducci,et al.  Relaxation of stretched DNA in slitlike confinement. , 2007, Physical review letters.

[10]  Danielle J. Mai,et al.  Microfluidic systems for single DNA dynamics. , 2012, Soft matter.

[11]  William R. Taylor,et al.  A deeply knotted protein structure and how it might fold , 2000, Nature.

[12]  Martin Fuchs,et al.  DNA mapping using microfluidic stretching and single-molecule detection of fluorescent site-specific tags. , 2004, Genome research.

[13]  D E Smith,et al.  Single polymer dynamics in an elongational flow. , 1997, Science.

[14]  S. Chu,et al.  Effect of hydrodynamic interactions on DNA dynamics in extensional flow: Simulation and single molecule experiment , 2004 .

[15]  S. Smith,et al.  Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. , 1992, Science.

[16]  J. H. Cifre,et al.  Kinetic aspects of the coil-stretch transition of polymer chains in dilute solution under extensional flow , 2001 .

[17]  Steven Chu,et al.  Observation of Polymer Conformation Hysteresis in Extensional Flow , 2003, Science.

[18]  Gaurav Arya,et al.  Biophysics of knotting. , 2010, Annual review of biophysics.

[19]  S. Muller,et al.  Polymer-monovalent salt-induced DNA compaction studied via single-molecule microfluidic trapping. , 2012, Lab on a chip.

[20]  P. Doyle,et al.  Electrophoretic stretching of DNA molecules using microscale T junctions , 2007 .

[21]  P. Doyle,et al.  Collision of a DNA Polymer with a Small Obstacle , 2006 .

[22]  P. Doyle,et al.  Electrophoretic Stretching of DNA Molecules in Cross-Slot Nanoslit Channels , 2008 .

[23]  Harold G. Craighead,et al.  Revisiting the Conformation and Dynamics of DNA in Slitlike Confinement , 2010 .

[24]  H. Bayley,et al.  Continuous base identification for single-molecule nanopore DNA sequencing. , 2009, Nature nanotechnology.

[25]  Chih-Chen Hsieh,et al.  An experimental study of DNA rotational relaxation time in nanoslits , 2007 .

[26]  P. Doyle,et al.  Electrophoretic collision of a DNA molecule with an insulating post. , 2004, Physical review letters.

[27]  V. Steinberg,et al.  Critical slowing down in polymer dynamics near the coil-stretch transition in elongation flow. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[28]  C. Chou,et al.  Entropy-driven single molecule tug-of-war of DNA at micro-nanofluidic interfaces. , 2012, Nano letters.

[29]  C. Abrams,et al.  Swelling dynamics of collapsed polymers , 2004 .

[30]  Dmitrii E Makarov,et al.  Translocation of a knotted polypeptide through a pore. , 2008, The Journal of chemical physics.

[31]  Eric S. G. Shaqfeh,et al.  The dynamics of single-molecule DNA in flow , 2005 .

[32]  P. de Gennes,et al.  POLYMER PHYSICS: Molecular Individualism , 1997 .

[33]  Enzo Orlandini,et al.  Knotting and metric scaling properties of DNA confined in nano-channels: a Monte Carlo study , 2012 .

[34]  M. Vázquez,et al.  Knotting probability of DNA molecules confined in restricted volumes: DNA knotting in phage capsids , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Toyoichi Tanaka,et al.  Metastable globules in good solvents: Topologically stabilized state of polymers , 1995 .

[36]  Javier Arsuaga,et al.  DNA knots reveal a chiral organization of DNA in phage capsids. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Liang Dai,et al.  Effect of Nanoslit Confinement on the Knotting Probability of Circular DNA. , 2012, ACS macro letters.

[38]  Douglas E. Smith,et al.  Response of flexible polymers to a sudden elongational flow , 1998, Science.

[39]  Patrick S. Doyle,et al.  Compression and self-entanglement of single DNA molecules under uniform electric field , 2011, Proceedings of the National Academy of Sciences.

[40]  K. Dorfman,et al.  DNA electrophoresis in a sparse ordered post array. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[41]  C. Abrams,et al.  Arrested swelling of highly entangled polymer globules. , 2003, Physical review letters.

[42]  Amanda B. Marciel,et al.  New directions in single polymer dynamics , 2013 .

[43]  Rebecca Dylla-Spears,et al.  Single-molecule sequence detection via microfluidic planar extensional flow at a stagnation point. , 2010, Lab on a chip.

[44]  P. Doyle,et al.  Design and numerical simulation of a DNA electrophoretic stretching device. , 2007, Lab on a chip.

[45]  Jongyoon Han,et al.  Double-Stranded DNA Diffusion in Slitlike Nanochannels , 2006 .

[46]  M. Graham Fluid Dynamics of Dissolved Polymer Molecules in Confined Geometries , 2011 .

[47]  A. Alexander-Katz,et al.  Globule−Stretch Transitions of Collapsed Polymers in Elongational Flow Fields , 2010 .

[48]  Yael Michaeli,et al.  Channeling DNA for optical mapping , 2012, Nature Biotechnology.

[49]  Davide Marenduzzo,et al.  Topological friction strongly affects viral DNA ejection , 2013, Proceedings of the National Academy of Sciences.

[50]  Erwin Frey,et al.  Statics and dynamics of single DNA molecules confined in nanochannels. , 2005, Physical review letters.

[51]  P. Doyle,et al.  Conformational Preconditioning by Electrophoresis of DNA through a Finite Obstacle Array , 2008 .

[52]  K. Dorfman DNA electrophoresis in microfabricated devices , 2010 .

[53]  Davide Marenduzzo,et al.  Polymers with spatial or topological constraints: Theoretical and computational results , 2011, 1103.4222.

[54]  A. Alexander-Katz,et al.  Dynamics of collapsed polymers under the simultaneous influence of elongational and shear flows. , 2011, The Journal of chemical physics.

[55]  Stephen R Quake,et al.  Behavior of complex knots in single DNA molecules. , 2003, Physical review letters.

[56]  C. Micheletti,et al.  Numerical Study of Linear and Circular Model DNA Chains Confined in a Slit: Metric and Topological Properties , 2012, 1204.1983.