Nanomechanics of silk: The fundamentals of a strong, tough and versatile material

Nanotechnology

Volumn 27, Issue 30, 2016, Pages

  Su, Isabelle ^a   Buehler, Markus J ^a  

^a Massachusetts Institute of Technology   (United States)

Author keywords

fracture toughness; hierarchical structure; protein folding; resilience; self assembly; Silk; spider webs

Indexed keywords

FRACTURE TOUGHNESS; PROTEIN FOLDING; SELF ASSEMBLY;

CHEMICAL DESIGNS; HIERARCHICAL STRUCTURES; MATERIAL ARCHITECTURE; MOLECULAR PROPERTIES; RESILIENCE; RESILIENT MATERIALS; SPIDER WEB; SYNTHETIC MATERIALS;

SILK;

EID: 84978289564     PISSN: 09574484     EISSN: 13616528     Source Type: Journal    
DOI: 10.1088/0957-4484/27/30/302001     Document Type: Review

References (109)

1. Vincent J F V 2001 Stealing ideas from nature Deployable Structures ed P S Pellegrino (Vienna: Springer) pp 51-8
2. Wegst U G K and Ashby M F 2004 The mechanical efficiency of natural materials Phil. Mag. 84 2167-86
3. Meyers M A, Chen P-Y, Lin A Y-M and Seki Y 2008 Biological materials: structure and mechanical properties Prog. Mater. Sci. 53 1-206
4. Gu G X, Su I, Sharma S, Voros J L, Qin Z and Buehler M J 2016 Three-dimensional-printing of bio-inspired composites J. Biomech. Eng. 138 021006
5. Ebrahimi D, Tokareva O, Rim N G, Wong J Y, Kaplan D L and Buehler M J 2015 Silk-its mysteries, how it is made, and how it is used ACS Biomater. Sci. Eng. 1 864-76
6. Tokareva O, Jacobsen M, Buehler M, Wong J and Kaplan D L 2014 Review: structure-function-property-design interplay in biopolymers: spider silk Acta Biomater. 10 1612-26
7. Lewis R V 2006 Spider silk production Bionanotechnology: Proteins to Nanodevices ed V Renugopalakrishnan and R V Lewis (Dordrecht: Springer) pp 61-78
8. Eisoldt L, Smith A and Scheibel T 2011 Decoding the secrets of spider silk Mater. Today 14 80-6
9. Vollrath F 2006 Spider silk: thousands of nano-filaments and dollops of sticky glue Curr. Biol. 16 R925-7
10. Cranford S W, Tarakanova A, Pugno N M and Buehler M J 2012 Nonlinear material behaviour of spider silk yields robust webs Nature 482 72-6
11. Hayashi C Y and Lewis R V 1998 Evidence from flagelliform silk cDNA for the structural basis of elasticity and modular nature of spider silks1 J. Mol. Biol. 275 773-84
12. Aoyanagi Y and Okumura K 2010 Simple model for the mechanics of spider webs Phys. Rev. Lett. 104 038102
13. Agnarsson I, Kuntner M and Blackledge T A 2010 Bioprospecting finds the toughest biological material: extraordinary silk from a giant riverine orb spider PLoS One 5 e11234
14. Colomban P, Herrera Ramirez J M, Paquin R, Marcellan A and Bunsell A 2006 Micro-Raman study of the fatigue and fracture behaviour of single PA66 fibres: comparison with single PET and PP fibres Eng. Fract. Mech. 73 2463-75
15. Gosline J M, Guerette P A, Ortlepp C S and Savage K N 1999 The mechanical design of spider silks: from fibroin sequence to mechanical function J. Exp. Biol. 202 3295-303
16. Colomban P and Dinh H M 2012 Origin of the variability of the mechanical properties of silk fibres: II. the nanomechanics of single silkworm and spider fibres J. Raman Spectrosc. 43 1035-41
17. Colomban P, Dinh H M, Bunsell A and Mauchamp B 2012 Origin of the variability of the mechanical properties of silk fibres: I. The relationship between disorder, hydration and stress/strain behaviour J. Raman Spectrosc. 43 425-32
18. Colomban P, Dinh H M, Riand J, Prinsloo L C and Mauchamp B 2008 Nanomechanics of single silkworm and spider fibres: a Raman and micro-mechanical in situ study of the conformation change with stress J. Raman Spectrosc. 39 1749-64
19. Heim M, Keerl D and Scheibel T 2009 Spider silk: from soluble protein to extraordinary fiber Angew. Chem., Int. Ed. Engl. 48 3584-96
20. Vollrath F and Knight D P 2001 Liquid crystalline spinning of spider silk Nature 410 541-8
21. Zhang J, Kaur J, Rajkhowa R, Li J L, Liu X Y and Wang X G 2013 Mechanical properties and structure of silkworm cocoons: a comparative study of Bombyx mori, Antheraea assamensis, Antheraea pernyi and Antheraea mylitta silkworm cocoons Mater. Sci. Eng. C 33 3206-13
22. Zhang J, Kaur J, Rajkhowa R, Li J L, Liu X Y and Wang X G 2013 Wild silkworm cocoon as a natural tough biological composite structure Proc. 8th Int. Conf. Structural Integrity Fracture 2013 pp 1-4
23. Porter D and Vollrath F 2007 Nanoscale toughness of spider silk Nano Today 2 6
24. Tarakanova A and Buehler M 2012 A materiomics approach to spider silk: protein molecules to webs JOM J. Miner. Met. Mater. Soc. TMS 64 214-25
25. Buehler M J 2010 Tu(r)ning weakness to strength Nano Today 5 379-83
26. Papadopoulos P, Sölter J and Kremer F 2008 Hierarchies in the structural organization of spider silk - a quantitative model Colloid Polym. Sci. 287 231-6
27. Guinea G V, Elices M, Pérez-Rigueiro J and Plaza G R 2005 Stretching of supercontracted fibers: a link between spinning and the variability of spider silk J. Exp. Biol. 208 25-30
28. Blackledge T A, Boutry C, Wong S-C, Baji A, Dhinojwala A, Sahni V and Agnarsson I 2009 How super is supercontraction? Persistent versus cyclic responses to humidity in spider dragline silk J. Exp. Biol. 212 1981-9
29. Widhe M, Johansson J, Hedhammar M and Rising A 2012 Current progress and limitations of spider silk for biomedical applications Biopolymers 97 468-78
30. Gellynck K, Verdonk P, Forsyth R, Almqvist K F, Nimmen E V, Gheysens T, Mertens J, Langenhove L V, Kiekens P and Verbruggen G 2008 Biocompatibility and biodegradability of spider egg sac silk J. Mater. Sci., Mater. Med. 19 2963-70
31. Allmeling C, Jokuszies A, Reimers K, Kall S and Vogt P M 2006 Use of spider silk fibres as an innovative material in a biocompatible artificial nerve conduit J. Cell. Mol. Med. 10 770-7
32. Parker S T, Domachuk P, Amsden J, Bressner J, Lewis J A, Kaplan D L and Omenetto F G 2009 Biocompatible silk printed optical waveguides Adv. Mater. 21 2411-5
33. Hu Y, Zhang Q, You R, Wang L and Li M 2012 The relationship between secondary structure and biodegradation behavior of silk fibroin scaffolds Adv. Mater. Sci. Eng. 2012 e185905
34. Holland C, Terry A E, Porter D and Vollrath F 2006 Comparing the rheology of native spider and silkworm spinning dope Nat. Mater. 5 870-4
35. Seidel A, Liivak O, Calve S, Adaska J, Ji G, Yang Z, Grubb D, Zax D B and Jelinski L W 2000 Regenerated spider silk: processing, properties, and structure Macromolecules 33 775-80
36. Shao Z, Vollrath F, Yang Y and Thøgersen H C 2003 Structure and behavior of regenerated spider silk Macromolecules 36 1157-61
37. Wojcieszak M, Percot A, Noinville S, Gouadec G, Mauchamp B and Colomban P 2014 Origin of the variability of the mechanical properties of silk fibers: IV. Order/crystallinity along silkworm and spider fibers J. Raman Spectrosc. 45 895-902
38. Pérez-Rigueiro J, Viney C, Llorca J and Elices M 1998 Silkworm silk as an engineering material J. Appl. Polym. Sci. 70 2439-47
39. Koh L-D et al 2015 Structures, mechanical properties and applications of silk fibroin materials Prog. Polym. Sci. 46 86-110
40. Vepari C and Kaplan D L 2007 Silk as a biomaterial Prog. Polym. Sci. 32 991-1007
41. Foo C W P and Kaplan D L 2002 Genetic engineering of fibrous proteins: spider dragline silk and collagen Adv. Drug Deliv. Rev. 54 1131-43
42. Xu M and Lewis R V 1990 Structure of a protein superfiber: spider dragline silk Proc. Natl Acad. Sci. 87 7120-4
43. Ittah S, Cohen S, Garty S, Cohn D and Gat U 2006 An essential role for the C-terminal domain of a dragline spider silk protein in directing fiber formation Biomacromolecules 7 1790-5
44. Hu X, Vasanthavada K, Kohler K, McNary S, Moore A M F and Vierra C A 2006 Molecular mechanisms of spider silk Cell. Mol. Life Sci. CMLS 63 1986-99
45. Lefèvre T, Rousseau M-E and Pézolet M 2007 Protein secondary structure and orientation in silk as revealed by Raman spectromicroscopy Biophys. J. 92 2885-95
46. Hayashi C Y, Shipley N H and Lewis R V 1999 Hypotheses that correlate the sequence, structure, and mechanical properties of spider silk proteins Int. J. Biol. Macromol. 24 271-5
47. Knight D P, Knight M M and Vollrath F 2000 Beta transition and stress-induced phase separation in the spinning of spider dragline silk Int. J. Biol. Macromol. 27 205-10
48. Knight D P and Vollrath F 2001 Changes in element composition along the spinning duct in a Nephila spider Naturwissenschaften 88 179-82
49. Brooks A E, Steinkraus H B, Nelson S R and Lewis R V 2005 An investigation of the divergence of major ampullate silk fibers from Nephila clavipes and Argiope aurantia Biomacromolecules 6 3095-9
50. Rising A, Widhe M, Johansson J and Hedhammar M 2010 Spider silk proteins: recent advances in recombinant production, structure-function relationships and biomedical applications Cell. Mol. Life Sci. 68 169-84
51. Sponner A, Unger E, Grosse F and Weisshart K 2005 Differential polymerization of the two main protein components of dragline silk during fibre spinning Nat. Mater. 4 772-5
52. Keten S and Buehler M J 2010 Atomistic model of the spider silk nanostructure Appl. Phys. Lett. 96 153701
53. Rising A, Nimmervoll H, Grip S, Fernandez-Arias A, Storckenfeldt E, Knight D P, Vollrath F and Engström W 2005 Spider silk proteins - mechanical property and gene sequence Zoological Sci. 22 273-81
54. Hijirida D H, Do K G, Michal C, Wong S, Zax D and Jelinsk L W 1996 13C NMR of Nephila clavipes major ampullate silk gland Biophys. J. 71 3442-7
55. Knight D P and Vollrath F 1999 Liquid crystals and flow elongation in a spider's silk production line Proc. R. Soc. Lond. B Biol. Sci. 266 519-23
56. Vollrath F, Knight D P and Hu X W 1998 Silk production in a spider involves acid bath treatment Proc. R. Soc. Lond. B Biol. Sci. 265 817-20
57. Römer L and Scheibel T 2008 The elaborate structure of spider silk Prion 2 154-61
58. Rammensee S, Slotta U, Scheibel T and Bausch A R 2008 Assembly mechanism of recombinant spider silk proteins Proc. Natl Acad. Sci. 105 6590-5
59. Hardy J G, Römer L M and Scheibel T R 2008 Polymeric materials based on silk proteins Polymer 49 4309-27
60. Percot A, Colomban P, Paris C, Dinh H M, Wojcieszak M and Mauchamp B 2014 Water dependent structural changes of silk from Bombyx mori gland to fibre as evidenced by Raman and IR spectroscopies Vib. Spectrosc. 73 79-89
61. Gauthier M, Leclerc J, Lefèvre T, Gagné S M and Auger M 2014 Effect of pH on the structure of the recombinant C-terminal domain of Nephila clavipes dragline silk protein Biomacromolecules 15 4447-54
62. Gronau G, Qin Z and Buehler M J 2013 Effect of sodium chloride on the structure and stability of spider silk's N-terminal protein domain Biomater. Sci. 1 276-84
63. Lin S et al 2015 Predictive modelling-based design and experiments for synthesis and spinning of bioinspired silk fibres Nat. Commun. 6 6892-92
64. Giesa T, Perry C C and Buehler M J 2015 Secondary structure transition and critical stress for a model of spider silk assembly Biomacromolecules 17 427-36
65. Cranford S W and Buehler M J 2012 Biomateriomics (Dordrecht: Springer) vol 165
66. Bratzel G and Buehler M J 2012 Molecular mechanics of silk nanostructures under varied mechanical loading Biopolymers 97 408-17
67. van Beek J D, Hess S, Vollrath F and Meier B H 2002 The molecular structure of spider dragline silk: folding and orientation of the protein backbone Proc. Natl Acad. Sci. 99 10266-71
68. Keten S and Buehler M J 2010 Nanostructure and molecular mechanics of spider dragline silk protein assemblies J. R. Soc. Interface 7 1709-21
69. Keten S, Xu Z, Ihle B and Buehler M J 2010 Nanoconfinement controls stiffness, strength and mechanical toughness of β-sheet crystals in silk Nat. Mater. 9 359-67
70. Alam P 2014 Protein unfolding versus β-sheet separation in spider silk nanocrystals Adv. Nat. Sci.: Nanosci. Nanotechnol. 5 015015
71. Qin Z and Buehler M J 2012 Cooperativity governs the size and structure of biological interfaces J. Biomech. 45 2778-83
72. Qin Z and Buehler M J 2010 Cooperative deformation of hydrogen bonds in beta-strands and beta-sheet nanocrystals Phys. Rev. E 82 061906
73. Keten S and Buehler M J 2008 Geometric confinement governs the rupture strength of H-bond assemblies at a critical length scale Nano Lett. 8 743-8
74. Qin Z, Dimas L, Adler D, Bratzel G and Buehler M J 2014 Biological materials by design J. Phys.: Condens. Matter 26 073101
75. Nova A, Keten S, Pugno N M, Redaelli A and Buehler M J 2010 Molecular and nanostructural mechanisms of deformation, strength and toughness of spider silk fibrils Nano Lett. 10 2626-34
76. Du N, Yang Z, Liu X Y, Li Y and Xu H Y 2011 Structural origin of the strain-hardening of spider silk Adv. Funct. Mater. 21 772-8
77. Qin Z and Buehler M J 2013 Spider silk: webs measure up Nat. Mater. 12 185-7
78. Blackledge T A, Scharff N, Coddington J A, Szüts T, Wenzel J W, Hayashi C Y and Agnarsson I 2009 Reconstructing web evolution and spider diversification in the molecular era Proc. Natl Acad. Sci. 106 5229-34
79. Qin Z, Compton B G, Lewis J A and Buehler M J 2015 Structural optimization of 3D-printed synthetic spider webs for high strength Nat. Commun. 6 7038
80. Venner S and Casas J 2005 Spider webs designed for rare but life-saving catches Proc. R. Soc. Lond. B Biol. Sci. 272 1587-92
81. Koski K J, Akhenblit P, McKiernan K and Yarger J L 2013 Non-invasive determination of the complete elastic moduli of spider silks Nat. Mater. 12 262-7
82. Chen F, Porter D and Vollrath F 2010 Silkworm cocoons inspire models for random fiber and particulate composites Phys. Rev. E 82 041911
83. Chen F, Porter D and Vollrath F 2012 Morphology and structure of silkworm cocoons Mater. Sci. Eng. C 32 772-8
84. Chen F, Porter D and Vollrath F 2012 Structure and physical properties of silkworm cocoons J. R. Soc. Interface 9 2299-308
85. Chen F, Porter D and Vollrath F 2012 Silk cocoon (Bombyx mori): multi-layer structure and mechanical properties Acta Biomater. 8 2620-7
86. Chen F, Hesselberg T, Porter D and Vollrath F 2013 The impact behaviour of silk cocoons J. Exp. Biol. 216 2648-57
87. Frische S, Maunsbach A B and Vollrath F 1998 Elongate cavities and skin-core structure in Nephilia spider silk observed by electron microscopy J. Microsc. 189 64-70
88. Poza P, Pérez-Rigueiro J, Elices M and LLorca J 2002 Fractographic analysis of silkworm and spider silk Eng. Fract. Mech. 69 1035-48
89. Thiel B L and Viney C 1997 Spider major ampullate silk (drag line): smart composite processing based on imperfect crystals J. Microsc. 185 179-87
90. Giesa T, Arslan M, Pugno N M and Buehler M J 2011 Nanoconfinement of spider silk fibrils begets superior strength, extensibility, and toughness Nano Lett. 11 5038-46
91. Alam M S, Wahab M A and Jenkins C H 2007 Mechanics in naturally compliant structures Mech. Mater. 39 145-60
92. Cranford S W, Pugno N M and Buehler M J 2014 Silk and web synergy: the merging of material and structural performance Biotechnology of Silk ed T Asakura and T Miller (Dordrecht: Springer) pp 219-68
93. Giesa T, Pugno N M and Buehler M J 2012 Natural stiffening increases flaw tolerance of biological fibers Phys. Rev. E 86 041902
94. Giesa T, Pugno N M, Wong J Y, Kaplan D L and Buehler M J 2014 What's inside the box? - Length-scales that govern fracture processes of polymer fibers Adv. Mater. 26 412-7
95. Porter D, Guan J and Vollrath F 2013 Spider silk: super material or thin fibre? Adv. Mater. 25 1275-9
96. Bažant Z P 2004 Scaling theory for quasibrittle structural failure Proc. Natl Acad. Sci. USA 101 13400-7
97. Buehler M J, Yao H, Gao H and Ji B 2006 Cracking and adhesion at small scales: atomistic and continuum studies of flaw tolerant nanostructures Model. Simul. Mater. Sci. Eng. 14 799
98. Schänzel L, Dal H and Miehe C 2013 On micromechanically-based approaches to failure in polymers PAMM 13 557-60
99. Griffith A A 1921 The phenomena of rupture and flow in solids Phil. Trans. R. Soc. Lond. Ser. Contain. Pap. Math. Phys. Character 221 163-98
100. Anderson T L 2005 Fracture Mechanics: Fundamentals and Applications 3rd edn (Boca Raton, FL: CRC Press)
101. Du N, Liu X Y, Narayanan J, Li L, Lim M L M and Li D 2006 Design of superior spider silk: from nanostructure to mechanical properties Biophys. J. 91 4528-35
102. An B, Hinman M B, Holland G P, Yarger J L and Lewis R V 2011 Inducing β-sheets formation in synthetic spider silk fibers by aqueous post-spin stretching Biomacromolecules 12 2375-81
103. Xia X-X, Qian Z-G, Ki C S, Park Y H, Kaplan D L and Lee S Y 2010 Native-sized recombinant spider silk protein produced in metabolically engineered Escherichia coli results in a strong fiber Proc. Natl Acad. Sci. 107 14059-63
104. Vollrath F, Porter D and Holland C 2011 There are many more lessons still to be learned from spider silks Soft Matter 7 9595
105. Fraser M J, Lewis R, Jarvis D, Thompson K, Hull J, Mao Y-G, Teule F, Sohn B and Kim Y 2015 Transgenic silkworms capable of producing chimeric spider silk polypeptides and fibers US Patent Specification 20150322122 A1
106. Wen H, Lan X, Zhang Y, Zhao T, Wang Y, Kajiura Z and Nakagaki M 2009 Transgenic silkworms (Bombyx mori) produce recombinant spider dragline silk in cocoons Mol. Biol. Rep. 37 1815-21
107. Hardy J G and Scheibel T R 2010 Composite materials based on silk proteins Prog. Polym. Sci. 35 1093-115
108. Doblhofer E, Heidebrecht A and Scheibel T 2015 To spin or not to spin: spider silk fibers and more Appl. Microbiol. Biotechnol. 99 9361-80
109. Lepore E, Bonaccorso F, Bruna M, Bosia F, Taioli S, Garberoglio G, Ferrari A C and Pugno N M 2015 Silk reinforced with graphene or carbon nanotubes spun by spiders arXiv:150406751