Persistence and variation in microstructural design during the evolution of spider silk

The extraordinary mechanical performance of spider dragline silk is explained by its highly ordered microstructure and results from the sequences of its constituent proteins. This optimized microstructural organization simultaneously achieves high tensile strength and strain at breaking by taking advantage of weak molecular interactions. However, elucidating how the original design evolved over the 400 million year history of spider silk, and identifying the basic relationships between microstructural details and performance have proven difficult tasks. Here we show that the analysis of maximum supercontracted single spider silk fibers using X ray diffraction shows a complex picture of silk evolution where some key microstructural features are conserved phylogenetically while others show substantial variation even among closely related species. This new understanding helps elucidate which microstructural features need to be copied in order to produce the next generation of biomimetic silk fibers.

[1]  D. Porter,et al.  Proline and processing of spider silks. , 2008, Biomacromolecules.

[2]  N. Ayoub,et al.  Untangling spider silk evolution with spidroin terminal domains , 2010, BMC Evolutionary Biology.

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

[4]  R. Lewis,et al.  Structure of a protein superfiber: spider dragline silk. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[5]  C. Riekel,et al.  Nanofibrillar Structure and Molecular Mobility in Spider Dragline Silk , 2005 .

[6]  C. Michal,et al.  Strain Dependent Local Phase Transitions Observed during Controlled Supercontraction Reveal Mechanisms in Spider Silk , 2004 .

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

[8]  Markus J. Buehler,et al.  Tu(r)ning weakness to strength , 2010 .

[9]  J. Warwicker Comparative studies of fibroins. II. The crystal structures of various fibroins. , 1960, Journal of molecular biology.

[10]  T. Blackledge,et al.  Evolution of supercontraction in spider silk: structure–function relationship from tarantulas to orb-weavers , 2010, Journal of Experimental Biology.

[11]  G. V. Guinea,et al.  Stretching of supercontracted fibers: a link between spinning and the variability of spider silk , 2005, Journal of Experimental Biology.

[12]  C. Hayashi,et al.  Early Events in the Evolution of Spider Silk Genes , 2012, PloS one.

[13]  F Vollrath,et al.  Variability in the mechanical properties of spider silks on three levels: interspecific, intraspecific and intraindividual. , 1999, International journal of biological macromolecules.

[14]  G. Plaza,et al.  Similarities and Differences in the Supramolecular Organization of Silkworm and Spider Silk , 2007 .

[15]  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.

[16]  F Vollrath,et al.  Strength and structure of spiders' silks. , 2000, Journal of biotechnology.

[17]  Sarah Rauscher,et al.  Proline and glycine control protein self-organization into elastomeric or amyloid fibrils. , 2006, Structure.

[18]  G. Plaza,et al.  Relationship between microstructure and mechanical properties in spider silk fibers: identification of two regimes in the microstructural changes , 2012 .

[19]  M B Hinman,et al.  Isolation of a clone encoding a second dragline silk fibroin. Nephila clavipes dragline silk is a two-protein fiber. , 1992, The Journal of biological chemistry.

[20]  R. Lewis,et al.  Analysis of major ampullate silk cDNAs from two non-orb-weaving spiders. , 2004, Biomacromolecules.

[21]  Fritz Vollrath,et al.  Structural disorder in silk proteins reveals the emergence of elastomericity. , 2008, Biomacromolecules.

[22]  Alberto Redaelli,et al.  Molecular and nanostructural mechanisms of deformation, strength and toughness of spider silk fibrils. , 2010, Nano letters.

[23]  G. Giribet,et al.  Phylogenomic Analysis of Spiders Reveals Nonmonophyly of Orb Weavers , 2014, Current Biology.

[24]  M. Burghammer,et al.  Thermal behavior of Bombyx mori silk: evolution of crystalline parameters, molecular structure, and mechanical properties. , 2007, Biomacromolecules.

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

[26]  Y. Termonia Molecular modeling of spider silk elasticity , 1994 .

[27]  Fritz Vollrath,et al.  Materials: Surprising strength of silkworm silk , 2002, Nature.

[28]  Paul A. Selden,et al.  Fossil evidence for the origin of spider spinnerets, and a proposed arachnid order , 2008, Proceedings of the National Academy of Sciences.

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

[30]  David T. Grubb,et al.  Fiber Morphology of Spider Silk: The Effects of Tensile Deformation , 1997 .

[31]  Markus J. Buehler,et al.  Nonlinear material behaviour of spider silk yields robust webs , 2012, Nature.

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

[33]  Manuel Elices,et al.  Sequential origin in the high performance properties of orb spider dragline silk , 2012, Scientific Reports.

[34]  C. Hayashi,et al.  Silk Genes Support the Single Origin of Orb Webs , 2006, Science.

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

[36]  C. Craig Spiderwebs and silk : tracing evolution from molecules to genes to phenotypes , 2003 .

[37]  W. Kenchington,et al.  Arthropod Silks: The Problem of Fibrous Proteins in Animal Tissues , 1971 .

[38]  Todd A Blackledge,et al.  Silken toolkits: biomechanics of silk fibers spun by the orb web spider Argiope argentata (Fabricius 1775) , 2006, Journal of Experimental Biology.

[39]  J. Warwicker The crystal structure of silk fibroins , 1956 .

[40]  R. W. Work,et al.  A Physico-Chemical Study of the Supercontraction of Spider Major Ampullate Silk Fibers , 1982 .

[41]  Thomas Scheibel,et al.  Spider silk: from soluble protein to extraordinary fiber. , 2009, Angewandte Chemie.

[42]  F Vollrath,et al.  Predicting the mechanical properties of spider silk as a model nanostructured polymer , 2005, The European physical journal. E, Soft matter.

[43]  J. Bond,et al.  Phylogenomics Resolves a Spider Backbone Phylogeny and Rejects a Prevailing Paradigm for Orb Web Evolution , 2014, Current Biology.

[44]  Y. Takahashi,et al.  Structure refinement and diffuse streak scattering of silk (Bombyx mori). , 1999, International journal of biological macromolecules.

[45]  Matthew A. Collin,et al.  Blueprint for a High-Performance Biomaterial: Full-Length Spider Dragline Silk Genes , 2007, PloS one.