Spider dragline silk as torsional actuator driven by humidity

Spider dragline silk exhibits a self-powered torsion actuation driven by humidity, potentially acting as a novel torsional actuator. Self-powered actuation driven by ambient humidity is of practical interest for applications such as hygroscopic artificial muscles. We demonstrate that spider dragline silk exhibits a humidity-induced torsional deformation of more than 300°/mm. When the relative humidity reaches a threshold of about 70%, the dragline silk starts to generate a large twist deformation independent of spider species. The torsional actuation can be precisely controlled by regulating the relative humidity. The behavior of humidity-induced twist is related to the supercontraction behavior of spider dragline silk. Specifically, molecular simulations of MaSp1 and MaSp2 proteins in dragline silk reveal that the unique torsional property originates from the presence of proline in MaSp2. The large proline rings also contribute to steric exclusion and disruption of hydrogen bonding in the molecule. This property of dragline silk and its structural origin can inspire novel design of torsional actuators or artificial muscles and enable the development of designer biomaterials.

[1]  Markus J Buehler,et al.  Unraveling the Molecular Requirements for Macroscopic Silk Supercontraction. , 2017, ACS nano.

[2]  Kai Peng,et al.  Peculiar torsion dynamical response of spider dragline silk , 2017 .

[3]  Hongwei Zhu,et al.  Water-driven actuation of Ornithoctonus huwena spider silk fibers , 2017 .

[4]  Kai Peng,et al.  Direct measurement of torsional properties of single fibers , 2016 .

[5]  Kai Peng,et al.  An improved torsion pendulum based on image processing for single fibers , 2016 .

[6]  Sébastien Neukirch,et al.  In-drop capillary spooling of spider capture thread inspires hybrid fibers with mixed solid–liquid mechanical properties , 2016, Proceedings of the National Academy of Sciences.

[7]  Thierry Lefèvre,et al.  Spider silk as a blueprint for greener materials: a review , 2016 .

[8]  Markus J Buehler,et al.  Secondary Structure Transition and Critical Stress for a Model of Spider Silk Assembly. , 2016, Biomacromolecules.

[9]  Carter S. Haines,et al.  Hierarchically buckled sheath-core fibers for superelastic electronics, sensors, and muscles , 2015, Science.

[10]  Chris Holland,et al.  The Speed of Sound in Silk: Linking Material Performance to Biological Function , 2014, Advanced materials.

[11]  C. Haines,et al.  Hybrid carbon nanotube yarn artificial muscle inspired by spider dragline silk , 2014, Nature Communications.

[12]  Carter S. Haines,et al.  Artificial Muscles from Fishing Line and Sewing Thread , 2014, Science.

[13]  B. Zhang,et al.  Anomalous plasticity in the cyclic torsion of micron scale metallic wires. , 2013, Physical review letters.

[14]  Carter S. Haines,et al.  Electrically, Chemically, and Photonically Powered Torsional and Tensile Actuation of Hybrid Carbon Nanotube Yarn Muscles , 2012, Science.

[15]  Xiaopeng Huang,et al.  New Secrets of Spider Silk: Exceptionally High Thermal Conductivity and Its Abnormal Change under Stretching , 2012, Advanced materials.

[16]  Seon Jeong Kim,et al.  Torsional Carbon Nanotube Artificial Muscles , 2011, Science.

[17]  D. Porter,et al.  Two mechanisms for supercontraction in Nephila spider dragline silk. , 2011, Biomacromolecules.

[18]  David L. Kaplan,et al.  New Opportunities for an Ancient Material , 2010, Science.

[19]  Markus J. Buehler,et al.  Nanostructure and molecular mechanics of spider dragline silk protein assemblies , 2010, Journal of The Royal Society Interface.

[20]  Markus J. Buehler,et al.  Atomistic model of the spider silk nanostructure , 2010 .

[21]  Zhiping Xu,et al.  Nanoconfinement Controls Stiffness, Strength and Mechanical Toughness of Β-sheet Crystals in Silk , 2010 .

[22]  Ingi Agnarsson,et al.  Spider silk as a novel high performance biomimetic muscle driven by humidity , 2009, Journal of Experimental Biology.

[23]  Ingi Agnarsson,et al.  How super is supercontraction? Persistent versus cyclic responses to humidity in spider dragline silk , 2009, Journal of Experimental Biology.

[24]  D Thirumalai,et al.  Transmembrane structures of amyloid precursor protein dimer predicted by replica-exchange molecular dynamics simulations. , 2009, Journal of the American Chemical Society.

[25]  Janelle E. Jenkins,et al.  Determining secondary structure in spider dragline silk by carbon-carbon correlation solid-state NMR spectroscopy. , 2008, Journal of the American Chemical Society.

[26]  Thierry Lefèvre,et al.  Protein secondary structure and orientation in silk as revealed by Raman spectromicroscopy. , 2007, Biophysical journal.

[27]  Fritz Vollrath,et al.  Biopolymers: Shape memory in spider draglines , 2006, Nature.

[28]  Yi Liu,et al.  Relationships between supercontraction and mechanical properties of spider silk , 2005, Nature materials.

[29]  B. Meier,et al.  The molecular structure of spider dragline silk: Folding and orientation of the protein backbone , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  H. Hansma,et al.  Segmented nanofibers of spider dragline silk: Atomic force microscopy and single-molecule force spectroscopy , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Christopher Viney,et al.  Fibre science: Supercontraction stress in wet spider dragline , 2002, Nature.

[32]  R. Lewis,et al.  Extreme Diversity, Conservation, and Convergence of Spider Silk Fibroin Sequences , 2001, Science.

[33]  Fritz Vollrath,et al.  Liquid crystalline spinning of spider silk , 2001, Nature.

[34]  Oskar Liivak,et al.  Supercontraction and Backbone Dynamics in Spider Silk: 13C and 2H NMR Studies , 2000 .

[35]  J. Gosline,et al.  The mechanical design of spider silks: from fibroin sequence to mechanical function. , 1999, The Journal of experimental biology.

[36]  Y. Sugita,et al.  Replica-exchange molecular dynamics method for protein folding , 1999 .

[37]  Z. Shao,et al.  Analysis of spider silk in native and supercontracted states using Raman spectroscopy , 1999 .

[38]  R. Lewis,et al.  Hypotheses that correlate the sequence, structure, and mechanical properties of spider silk proteins. , 1999, International journal of biological macromolecules.

[39]  C. Riekel,et al.  Aspects of X-ray diffraction on single spider fibers. , 1999, International journal of biological macromolecules.

[40]  L W Jelinski,et al.  Molecular Orientation and Two-Component Nature of the Crystalline Fraction of Spider Dragline Silk , 1996, Science.

[41]  S. Tang,et al.  New internal structure of spider dragline silk revealed by atomic force microscopy. , 1994, Biophysical journal.

[42]  D. Noiseux Similarity laws of the internal damping of stranded cables in transverse vibrations , 1991, Proceedings of the 1991 IEEE Power Engineering Society Transmission and Distribution Conference.

[43]  R. C. Macridis A review , 1963 .

[44]  Clarence R. Robbins,et al.  Chemical and Physical Behavior of Human Hair , 2012, Springer Berlin Heidelberg.