From bistate molecular switches to self-directed track-walking nanomotors.

Track-walking nanomotors and larger systems integrating these motors are important for wide real-world applications of nanotechnology. However, inventing these nanomotors remains difficult, a sharp contrast to the widespread success of simpler switch-like nanodevices, even though the latter already encompasses basic elements of the former such as engine-like bistate contraction/extension or leg-like controllable binding. This conspicuous gap reflects an impeding bottleneck for the nanomotor development, namely, lack of a modularized construction by which spatially and functionally separable "engines" and "legs" are flexibly assembled into a self-directed motor. Indeed, all track-walking nanomotors reported to date combine the engine and leg functions in the same molecular part, which largely underpins the device-motor gap. Here we propose a general design principle allowing the modularized nanomotor construction from disentangled engine-like and leg-like motifs, and provide an experimental proof of concept by implementing a bipedal DNA nanomotor up to a best working regime of this versatile design principle. The motor uses a light-powered contraction-extension switch to drive a coordinated hand-over-hand directional walking on a DNA track. Systematic fluorescence experiments confirm the motor's directional motion and suggest that the motor possesses two directional biases, one for rear leg dissociation and one for forward leg binding. This study opens a viable route to develop track-walking nanomotors from numerous molecular switches and binding motifs available from nanodevice research and biology.

[1]  J. W. Ward,et al.  Sequence-Specific Peptide Synthesis by an Artificial Small-Molecule Machine , 2013, Science.

[2]  Ruojie Sha,et al.  A Bipedal DNA Brownian Motor with Coordinated Legs , 2009, Science.

[3]  A. Ajdari,et al.  Directional motion of brownian particles induced by a periodic asymmetric potential , 1994, Nature.

[4]  Paul R. Selvin,et al.  Myosin V Walks Hand-Over-Hand: Single Fluorophore Imaging with 1.5-nm Localization , 2003, Science.

[5]  Jie Yan,et al.  A contractile DNA machine. , 2008, Angewandte Chemie.

[6]  Luis Moroder,et al.  Single-Molecule Optomechanical Cycle , 2002, Science.

[7]  Iong Ying Loh,et al.  A bioinspired design principle for DNA nanomotors: mechanics-mediated symmetry breaking and experimental demonstration. , 2014, Methods.

[8]  Ruchuan Liu,et al.  Bipedal nanowalker by pure physical mechanisms. , 2012, Physical review letters.

[9]  M. Jiménez,et al.  Towards Synthetic Molecular Muscles: Contraction and Stretching of a Linear Rotaxane Dimer , 2000 .

[10]  Min Feng,et al.  Kinesin is an evolutionarily fine-tuned molecular ratchet-and-pawl device of decisively locked direction. , 2007, Biophysical journal.

[11]  Jun Wei,et al.  Autonomous synergic control of nanomotors. , 2014, ACS nano.

[12]  F. Simmel,et al.  Switching the conformation of a DNA molecule with a chemical oscillator. , 2005, Nano letters.

[13]  R. Vale,et al.  The way things move: looking under the hood of molecular motor proteins. , 2000, Science.

[14]  A. Turberfield,et al.  Coordinated chemomechanical cycles: a mechanism for autonomous molecular motion. , 2008, Physical review letters.

[15]  Younan Xia,et al.  Cover Picture: Shape‐Controlled Synthesis of Metal Nanocrystals: Simple Chemistry Meets Complex Physics? (Angew. Chem. Int. Ed. 1/2009) , 2009 .

[16]  J. Wang,et al.  Covalent bonds between protein and DNA. Formation of phosphotyrosine linkage between certain DNA topoisomerases and DNA. , 1980, The Journal of biological chemistry.

[17]  J. Reif,et al.  A unidirectional DNA walker that moves autonomously along a track. , 2004, Angewandte Chemie.

[18]  Fred Russell Kramer,et al.  Efficiencies of fluorescence resonance energy transfer and contact-mediated quenching in oligonucleotide probes. , 2002, Nucleic acids research.

[19]  Jonathan Bath,et al.  Optimizing DNA nanotechnology through coarse-grained modeling: a two-footed DNA walker. , 2013, ACS nano.

[20]  Ruizheng Hou,et al.  Role of directional fidelity in multiple aspects of extreme performance of the F(1)-ATPase motor. , 2013, Physical review. E, Statistical, nonlinear, and soft matter physics.

[21]  Heather L Tierney,et al.  Experimental demonstration of a single-molecule electric motor. , 2011, Nature nanotechnology.

[22]  F. Paolucci,et al.  Photoinduction of Fast, Reversible Translational Motion in a Hydrogen-Bonded Molecular Shuttle , 2001, Science.

[23]  J Fraser Stoddart,et al.  A molecular shuttle. , 1991, Journal of the American Chemical Society.

[24]  Wenwei Zheng,et al.  From molecular shuttles to directed procession of nanorings , 2008 .

[25]  Euan R. Kay,et al.  A Reversible Synthetic Rotary Molecular Motor , 2004, Science.

[26]  Erik Winfree,et al.  Molecular robots guided by prescriptive landscapes , 2010, Nature.

[27]  François Diederich,et al.  Geometrically precisely defined multinanometer expansion/contraction motions in a resorcin[4]arene cavitand based molecular switch. , 2005, Angewandte Chemie.

[28]  A. Najafi,et al.  Simple swimmer at low Reynolds number: three linked spheres. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[29]  Ruizheng Hou,et al.  Directional fidelity of nanoscale motors and particles is limited by the 2nd law of thermodynamics--via a universal equality. , 2013, The Journal of chemical physics.

[30]  Linke,et al.  Experimental tunneling ratchets , 1999, Science.

[31]  J. F. Stoddart,et al.  A chemically and electrochemically switchable molecular shuttle , 1994, Nature.

[32]  A. Turberfield,et al.  Mechanism for a directional, processive, and reversible DNA motor. , 2009, Small.

[33]  Francesco Zerbetto,et al.  Synthetic molecular motors and mechanical machines. , 2007, Angewandte Chemie.

[34]  Günter Mayer,et al.  Cover Picture: Light‐Induced Formation of G‐Quadruplex DNA Secondary Structures (ChemBioChem 11/2005) , 2005 .

[35]  Zhisong Wang,et al.  General mechanism for inchworm nanoscale track walkers: analytical theory and realistic simulation. , 2007, The Journal of chemical physics.

[36]  David A Leigh,et al.  An allosterically regulated molecular shuttle. , 2006, Angewandte Chemie.

[37]  Matthias Rief,et al.  Myosin-V is a mechanical ratchet. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[38]  A. Turberfield,et al.  A free-running DNA motor powered by a nicking enzyme. , 2005, Angewandte Chemie.

[39]  N. Seeman,et al.  A Proximity-Based Programmable DNA Nanoscale Assembly Line , 2010, Nature.

[40]  H. Gaub,et al.  Single-Molecule Cut-and-Paste Surface Assembly , 2008, Science.

[41]  Samara L. Reck-Peterson,et al.  Force-Induced Bidirectional Stepping of Cytoplasmic Dynein , 2007, Cell.

[42]  P. Yin,et al.  A DNAzyme that walks processively and autonomously along a one-dimensional track. , 2005, Angewandte Chemie.

[43]  David G Grier,et al.  Observation of flux reversal in a symmetric optical thermal ratchet. , 2005, Physical review letters.

[44]  N. Seeman,et al.  A precisely controlled DNA biped walking device , 2004 .

[45]  Jie Yan,et al.  Dynamics and Regulation of RecA Polymerization and De-Polymerization on Double-Stranded DNA , 2013, PloS one.

[46]  David R. Liu,et al.  Autonomous Multistep Organic Synthesis in a Single Isothermal Solution Mediated by a DNA Walker , 2010, Nature nanotechnology.

[47]  Artem Efremov,et al.  Maximum directionality and systematic classification of molecular motors. , 2011, Physical chemistry chemical physics : PCCP.

[48]  Artem Efremov,et al.  Universal optimal working cycles of molecular motors. , 2011, Physical chemistry chemical physics : PCCP.

[49]  J Klafter,et al.  Atomic scale engines: cars and wheels. , 2000, Physical review letters.

[50]  Zhisong Wang,et al.  Bioinspired laser-operated molecular locomotive. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[51]  Kevin W Plaxco,et al.  Thermodynamic basis for the optimization of binding-induced biomolecular switches and structure-switching biosensors , 2009, Proceedings of the National Academy of Sciences.

[52]  R. Cross,et al.  Molecular Motors: Dynein's Gearbox , 2004, Current Biology.

[53]  Zhisong Wang,et al.  Synergic mechanism and fabrication target for bipedal nanomotors , 2007, Proceedings of the National Academy of Sciences.

[54]  Xingguo Liang,et al.  A supra-photoswitch involving sandwiched DNA base pairs and azobenzenes for light-driven nanostructures and nanodevices. , 2009, Small.

[55]  Weihong Tan,et al.  An autonomous and controllable light-driven DNA walking device. , 2012, Angewandte Chemie.

[56]  K. Hamad-Schifferli,et al.  Remote electronic control of DNA hybridization through inductive coupling to an attached metal nanocrystal antenna , 2002, Nature.

[57]  Kaplan,et al.  Optical thermal ratchet. , 1995, Physical review letters.

[58]  Jie Yan,et al.  A divalent switch drives H-NS/DNA-binding conformations between stiffening and bridging modes. , 2010, Genes & development.

[59]  N. Pierce,et al.  A synthetic DNA walker for molecular transport. , 2004, Journal of the American Chemical Society.

[60]  N. Nakashima,et al.  A Light-Driven Molecular Shuttle Based on a Rotaxane , 1997 .

[61]  Chih-Ming Ho,et al.  Linear artificial molecular muscles. , 2005, Journal of the American Chemical Society.

[62]  Kevin W Plaxco,et al.  Fluorescence detection of single-nucleotide polymorphisms with a single, self-complementary, triple-stem DNA probe. , 2009, Angewandte Chemie.

[63]  David A Leigh,et al.  A synthetic small molecule that can walk down a track. , 2010, Nature chemistry.

[64]  Jean-Louis Mergny,et al.  DNA duplex–quadruplex exchange as the basis for a nanomolecular machine , 2003, Proceedings of the National Academy of Sciences of the United States of America.