- Email: [email protected]
Nanoscale toughness of spider silk
OPINION
Nanoscale toughness of spider silk Silk has been used as a textile for thousands of years and yet it is only recently that we are beginning to fully understand its structure. David Porter and Fritz Vollrath* | The University of Oxford, UK | *[email protected]
Silk is a remarkable biological product. A commercial champion for over 6000 years, the silk of the Bombyx moth larva is well known for its textile qualities, which still ensure an annual market on a par with top quality synthetic fibers. Spider silks have no commercial market yet, but their study has led to revolutionary new insights into silk properties because, unlike insect silks, they have evolved to perform best under tension and so are uniform in material qualities along the length of the fiber. Moreover, spider silks can be drawn from the animal ‘on demand’ and under highly controlled conditions. Hence, much of what we know about the molecular structure-function relations in the biological elastomer ‘silk’ derives from recent studies of spider silks1,2. A key factor of this remarkable material is the scaling of its semicrystalline morphology3,4. Silk typically consists of two proteins, one very large and one much smaller. They combine to form a nanoscale morphology of domains composed, at the simplest level, of ordered (crystalline) and disordered (amorphous) polymers. The ordered domains can be attributed to oriented beta-sheet crystals with strong amide-amide hydrogen bonding, while the disordered domains assume a wide range of structures with varying degrees of hydrogen bonding5,6. Throughout this heterogeneous complex, the dimensions of the various domains are kept well within nanoscale dimensions, thus allowing for a highly efficient (i.e. rapid and comprehensive) transfer of energy throughout the material7. This prevents local stress concentrations that would lead to premature failure. Perhaps counterintuitively, silk has a relatively low stiffness (5-15 GPa) for a high strength fiber, and its high degree of orientation is actually fragmented into nanoscale ‘beads’ of molecular hairpin folds. Quantitatively, spider silk with a maximum strength of ~1.4 GPa is estimated to require domains of the order 2-4 nm in size,
6
JUNE 2007 | VOLUME 2 | NUMBER 3
comparable in ‘grain dimensions’ to the units that convey strength in super-hard metals and ceramics8. Silk, unlike other important biological materials, is the result of continuous extrusion and not the cellular growth processes that produce collagen, chitin, or keratin9. Because polymer extrusion is an industrial reality, while industrial growth of controlled structures is as yet a dream, silk is the prime contender to provide the template needed to design and mass produce a functional imitationbiomaterial1. The structural simplicity but functional complexity of the nanoscale interactions gives silk its desirable and highly tunable properties. These rely on the processing procedure, whereby the protein molecules fold into a complex containing both intramolecular self-organization, as well as intermolecular selfassembly10,11. The guidance for these two processes lies in the genetic control of the exact positioning of the amino acids that make up the side chains of silk-polymer macromolecules. Whether the block copolymer molecules of the individual silk proteins form true liquid crystals (LCs)1 or semicrystalline complexes (that behave like an LC) is still open to debate11. However, a precursor morphology appears to be generated in the synthesis of the primary structure of the protein. This viscous precursor is converted to a nanostructured fiber as minute changes in pH, in combination with mechanical forces of the extrusion rheology, destabilize the aqueous spinning dope. In this denaturing sol-gel process, the solvent water is spontaneously ejected from the fiber as it is drawn1,11. Silk is an ideal natural material to provide a model for a wide range of other biological elastomers, most of which must perform in the hydrated state. Silk can function in a wide range of states
of hydration; from the dry structural threads of a web to its wet capture strands. Understanding the interaction of biological elastomers with water is a key requirement if we are to produce synthetic biomimetic analogues. Biological functionality, after all, tends to rely on wet engineering. For example, bone is another wet, natural hybrid nanocomposite. Here 2 nm hydroxyapatite sheets are embedded in 5 nm layers of hydrated tropocollagen tuned to operate in a state of optimal energy dissipation around its glass transition point12. In nanoscale functionality, bone resembles silk, with domain order/disorder distributed between the mineral and the tropocollagen. Bone may be a more flexible scaffold for mechanical energy distribution over a wide range of scales, but silk is better for direct energy transfer and manipulation at the nanoscale. Combining the two materials might lead to very interesting nanocomposites. REFERENCES 1. Vollrath, F., and Knight, D. P., Nature (2001) 410, 541 2. Vollrath, F., and Porter, D., Softmatter (2006) 2, 377 3. Vollrath, F., and Porter, D., J. Phys. A (2005) 82, 205 4. Porter, D., et al., Eur. Phys. J. E (2005) 16, 199 5. Van Beek, J. D., et al., Proc. Natl. Acad. Sci., USA (2002) 99, 10266 6. Riekel, C., and Vollrath, F., Int. J. Biol. Macromol. (2001) 29, 203 7. Porter, D., Group Interaction Modelling of Polymer Properties. Marcel Dekker, New York, (1995) 8. Barnett, S., and Madan, S., Phys. World, Jan 1998, 45 9. Vincent, J. F. V., Biomechanics – Materials. Oxford University Press, Oxford, (1992) 10. Liu, Y., et al., Nat. Mater. (2005) 4, 901 11. Holland, C., et al., Nat. Mater. (2006) 5, 870 12. Porter, D., Mater. Sci. Eng. A. (2004) 365, 38
Nanoscale toughness of spider silk Silk has been used as a textile for thousands of years and yet it is only recently that we are beginning to fully understand its structure. David Porter and Fritz Vollrath* | The University of Oxford, UK | *[email protected]
Silk is a remarkable biological product. A commercial champion for over 6000 years, the silk of the Bombyx moth larva is well known for its textile qualities, which still ensure an annual market on a par with top quality synthetic fibers. Spider silks have no commercial market yet, but their study has led to revolutionary new insights into silk properties because, unlike insect silks, they have evolved to perform best under tension and so are uniform in material qualities along the length of the fiber. Moreover, spider silks can be drawn from the animal ‘on demand’ and under highly controlled conditions. Hence, much of what we know about the molecular structure-function relations in the biological elastomer ‘silk’ derives from recent studies of spider silks1,2. A key factor of this remarkable material is the scaling of its semicrystalline morphology3,4. Silk typically consists of two proteins, one very large and one much smaller. They combine to form a nanoscale morphology of domains composed, at the simplest level, of ordered (crystalline) and disordered (amorphous) polymers. The ordered domains can be attributed to oriented beta-sheet crystals with strong amide-amide hydrogen bonding, while the disordered domains assume a wide range of structures with varying degrees of hydrogen bonding5,6. Throughout this heterogeneous complex, the dimensions of the various domains are kept well within nanoscale dimensions, thus allowing for a highly efficient (i.e. rapid and comprehensive) transfer of energy throughout the material7. This prevents local stress concentrations that would lead to premature failure. Perhaps counterintuitively, silk has a relatively low stiffness (5-15 GPa) for a high strength fiber, and its high degree of orientation is actually fragmented into nanoscale ‘beads’ of molecular hairpin folds. Quantitatively, spider silk with a maximum strength of ~1.4 GPa is estimated to require domains of the order 2-4 nm in size,
6
JUNE 2007 | VOLUME 2 | NUMBER 3
comparable in ‘grain dimensions’ to the units that convey strength in super-hard metals and ceramics8. Silk, unlike other important biological materials, is the result of continuous extrusion and not the cellular growth processes that produce collagen, chitin, or keratin9. Because polymer extrusion is an industrial reality, while industrial growth of controlled structures is as yet a dream, silk is the prime contender to provide the template needed to design and mass produce a functional imitationbiomaterial1. The structural simplicity but functional complexity of the nanoscale interactions gives silk its desirable and highly tunable properties. These rely on the processing procedure, whereby the protein molecules fold into a complex containing both intramolecular self-organization, as well as intermolecular selfassembly10,11. The guidance for these two processes lies in the genetic control of the exact positioning of the amino acids that make up the side chains of silk-polymer macromolecules. Whether the block copolymer molecules of the individual silk proteins form true liquid crystals (LCs)1 or semicrystalline complexes (that behave like an LC) is still open to debate11. However, a precursor morphology appears to be generated in the synthesis of the primary structure of the protein. This viscous precursor is converted to a nanostructured fiber as minute changes in pH, in combination with mechanical forces of the extrusion rheology, destabilize the aqueous spinning dope. In this denaturing sol-gel process, the solvent water is spontaneously ejected from the fiber as it is drawn1,11. Silk is an ideal natural material to provide a model for a wide range of other biological elastomers, most of which must perform in the hydrated state. Silk can function in a wide range of states
of hydration; from the dry structural threads of a web to its wet capture strands. Understanding the interaction of biological elastomers with water is a key requirement if we are to produce synthetic biomimetic analogues. Biological functionality, after all, tends to rely on wet engineering. For example, bone is another wet, natural hybrid nanocomposite. Here 2 nm hydroxyapatite sheets are embedded in 5 nm layers of hydrated tropocollagen tuned to operate in a state of optimal energy dissipation around its glass transition point12. In nanoscale functionality, bone resembles silk, with domain order/disorder distributed between the mineral and the tropocollagen. Bone may be a more flexible scaffold for mechanical energy distribution over a wide range of scales, but silk is better for direct energy transfer and manipulation at the nanoscale. Combining the two materials might lead to very interesting nanocomposites. REFERENCES 1. Vollrath, F., and Knight, D. P., Nature (2001) 410, 541 2. Vollrath, F., and Porter, D., Softmatter (2006) 2, 377 3. Vollrath, F., and Porter, D., J. Phys. A (2005) 82, 205 4. Porter, D., et al., Eur. Phys. J. E (2005) 16, 199 5. Van Beek, J. D., et al., Proc. Natl. Acad. Sci., USA (2002) 99, 10266 6. Riekel, C., and Vollrath, F., Int. J. Biol. Macromol. (2001) 29, 203 7. Porter, D., Group Interaction Modelling of Polymer Properties. Marcel Dekker, New York, (1995) 8. Barnett, S., and Madan, S., Phys. World, Jan 1998, 45 9. Vincent, J. F. V., Biomechanics – Materials. Oxford University Press, Oxford, (1992) 10. Liu, Y., et al., Nat. Mater. (2005) 4, 901 11. Holland, C., et al., Nat. Mater. (2006) 5, 870 12. Porter, D., Mater. Sci. Eng. A. (2004) 365, 38