Silken toolkits: biomechanics of silk fibers spun by the orb web spider Argiope argentata (Fabricius 1775)

SUMMARY Orb-weaving spiders spin five fibrous silks from differentiated glands that contain unique sets of proteins. Despite diverse ecological functions, the mechanical properties of most of these silks are not well characterized. Here, we quantify the mechanical performance of this toolkit of silks for the silver garden spider Argiope argentata. Four silks exhibit viscoelastic behaviour typical of polymers, but differ statistically from each other by up to 250% in performance, giving each silk a distinctive suite of material properties. Major ampullate silk is 50% stronger than other fibers, but also less extensible. Aciniform silk is almost twice as tough as other silks because of high strength and extensibility. Capture spiral silk, coated with aqueous glue, is an order of magnitude stretchier than other silks. Dynamic mechanical properties are qualitatively similar, but quantitatively vary by up to 300% among silks. Storage moduli are initially nearly constant and increase after fiber yield, whereas loss tangents reach maxima of 0.1–0.2 at the yield. The remarkable mechanical diversity of Argiope argentata silks probably results in part from the different molecular structures of fibers and can be related to the specific ecological role of each silk. Our study indicates substantial potential to customize the mechanics of bioengineered silks.

[1]  C. Craig,et al.  The ecological and evolutionary interdependence between web architecture and web silk spun by orb web weaving spiders , 1987 .

[2]  Fritz Vollrath,et al.  Silk production in a spider involves acid bath treatment , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[3]  R. Lewis,et al.  Evidence from flagelliform silk cDNA for the structural basis of elasticity and modular nature of spider silks. , 1998, Journal of molecular biology.

[4]  Steven Arcidiacono,et al.  Spider Silk Fibers Spun from Soluble Recombinant Silk Produced in Mammalian Cells , 2002, Science.

[5]  D. Ginzinger,et al.  Silk Properties Determined by Gland-Specific Expression of a Spider Fibroin Gene Family , 1996, Science.

[6]  John M Gosline,et al.  Consequences of forced silking. , 2004, Biomacromolecules.

[7]  F Vollrath,et al.  Structure and function of the silk production pathway in the spider Nephila edulis. , 1999, International journal of biological macromolecules.

[8]  Todd A. Blackledge,et al.  Variation in the material properties of spider dragline silk across species , 2006 .

[9]  R. Lewis,et al.  Spider flagelliform silk: lessons in protein design, gene structure, and molecular evolution. , 2001, BioEssays : news and reviews in molecular, cellular and developmental biology.

[10]  L. Van Langenhove,et al.  MODELING OF THE STRESS-STRAIN BEHAVIOR OF EGG SAC SILK OF THE SPIDER ARANEUS DIADEMATUS , 2005 .

[11]  C. Viney,et al.  Spider (Araneus diadematus) cocoon silk: a case of non-periodic lattice crystals with a twist? , 1999, International journal of biological macromolecules.

[12]  R. Lewis,et al.  Molecular and mechanical characterization of aciniform silk: uniformity of iterated sequence modules in a novel member of the spider silk fibroin gene family. , 2004, Molecular biology and evolution.

[13]  Todd A Blackledge,et al.  Convergent evolution of behavior in an adaptive radiation of Hawaiian web-building spiders. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[14]  S. Fossey,et al.  Mechanical Properties of Major Ampulate Gland Silk Fibers Extracted fromNephila clavipesSpiders , 1993 .

[15]  R. Lewis,et al.  Structural studies of spider silk proteins in the fiber , 1997, Journal of molecular recognition : JMR.

[16]  M. Kitagawa,et al.  Mechanical properties of dragline and capture thread for the spider Nephila clavata , 1997 .

[17]  L. Van Langenhove,et al.  EGG SAC STRUCTURE OF ZYGIELLA X-NOTATA (ARACHNIDA, ARANEIDAE) , 2005 .

[18]  Mark W. Denny,et al.  Elastomeric Network Models for the Frame and Viscid Silks from the Orb Web of the SpiderAraneus diadematus , 1993 .

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

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

[21]  R. Lewis,et al.  Expression and purification of a spider silk protein: a new strategy for producing repetitive proteins. , 1996, Protein expression and purification.

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

[23]  J. Bond,et al.  Capture thread extensibility of orb-weaving spiders: testing punctuated and associative explanations , 2000 .

[24]  M. Elices,et al.  Active control of spider silk strength: comparison of drag line spun on vertical and horizontal surfaces , 2002 .

[25]  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.

[26]  Todd A Blackledge,et al.  Quasistatic and continuous dynamic characterization of the mechanical properties of silk from the cobweb of the black widow spider Latrodectus hesperus , 2005, Journal of Experimental Biology.

[27]  Adam P. Summers,et al.  Gumfooted lines in black widow cobwebs and the mechanical properties of spider capture silk. , 2005, Zoology.

[28]  F. Vollrath,et al.  Secondary structures and conformational changes in flagelliform, cylindrical, major, and minor ampullate silk proteins. Temperature and concentration effects. , 2004, Biomacromolecules.

[29]  J. Bond,et al.  Changes in the mechanical properties of capture threads and the evolution of modern orb-weaving spiders , 2001 .

[30]  Fritz Vollrath,et al.  Structural engineering of an orb-spider's web , 1995, Nature.

[31]  M. Elices,et al.  Tensile properties of Argiope trifasciata drag line silk obtained from the spider's web , 2001 .

[32]  R. Foelix,et al.  The biology of spiders. , 1987 .

[33]  C. Viney,et al.  Non-periodic lattice crystals in the hierarchical microstructure of spider (major ampullate) silk. , 1997, Biopolymers.

[34]  David L Kaplan,et al.  Genetic engineering of fibrous proteins: spider dragline silk and collagen. , 2002, Advanced drug delivery reviews.

[35]  H. Hansma,et al.  Molecular nanosprings in spider capture-silk threads , 2003, Nature materials.

[36]  T. Scheibel,et al.  Novel Assembly Properties of Recombinant Spider Dragline Silk Proteins , 2004, Current Biology.

[37]  Steven L. Miller,et al.  Molecular Orientation and Two-Component Nature of the Crystalline Fraction of Spider Dragline Silk , 2007 .

[38]  F Vollrath,et al.  Biology of spider silk. , 1999, International journal of biological macromolecules.

[39]  David L. Kaplan,et al.  Silk: biology, structure, properties, and genetics , 1994 .

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

[41]  C. Hieber The role of spider cocoons in controlling desiccation , 1992, Oecologia.

[42]  C. Hieber Spider cocoons and their suspension systems as barriers to generalist and specialist predators , 1992, Oecologia.

[43]  Fritz Vollrath,et al.  Molecular deformation in spider dragline silk subjected to stress , 2000 .

[44]  Robert W. Work,et al.  Dimensions, Birefringences, and Force-Elongation Behavior of Major and Minor Ampullate Silk Fibers from Orb-Web-Spinning Spiders—The Effects of Wetting on these Properties , 1977 .

[45]  Mark W. Denny,et al.  THE PHYSICAL PROPERTIES OF SPIDER'S SILK AND THEIR ROLE IN THE DESIGN OF ORB-WEBS , 1976 .

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

[47]  R. Lewis,et al.  Molecular architecture and evolution of a modular spider silk protein gene. , 2000, Science.

[48]  C. Hayashi,et al.  Modular evolution of egg case silk genes across orb-weaving spider superfamilies. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[49]  Robert W. Work,et al.  The Force-Elongation Behavior of Web Fibers and Silks Forcibly Obtained from Orb-Web-Spinning Spiders , 1976 .

[50]  S. G. Srinivasan,et al.  Characterizing the cross-sectional geometry of thin, non-cylindrical, twisted fibres (spider silk) , 1995, Journal of Materials Science.

[51]  Todd A. Blackledge,et al.  Are three-dimensional spider webs defensive adaptations? , 2002 .

[52]  D. Kaplan,et al.  Purification and characterization of recombinant spider silk expressed in Escherichia coli , 1998, Applied Microbiology and Biotechnology.

[53]  R. Lewis,et al.  Molecular characterization and evolutionary study of spider tubuliform (eggcase) silk protein. , 2005, Biochemistry.

[54]  F. Vollrath,et al.  Thread biomechanics in the two orb-weaving spiders Araneus diadematus(Araneae, Araneidae)and Uloborus walckenaerius(Araneae, Uloboridae) , 1995 .

[55]  F Vollrath,et al.  The effect of spinning conditions on the mechanics of a spider's dragline silk , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[56]  Fritz Vollrath,et al.  Modulation of the mechanical properties of spider silk by coating with water , 1989, Nature.

[57]  M. E. Demont,et al.  Spider silk as rubber , 1984, Nature.

[58]  J. Czernuszka,et al.  Multiaxial anisotropy of spider (Araneus diadematus) cocoon silk fibres , 2001 .

[59]  R. Cardullo,et al.  Polarized Light Microscopy, Variability in Spider Silk Diameters, and the Mechanical Characterization of Spider Silk , 2005 .

[60]  D. Kirschner,et al.  Designing recombinant spider silk proteins to control assembly. , 1999, International journal of biological macromolecules.