Post-secretion processing influences spider silk performance

Journal of the Royal Society Interface

Volumn 9, Issue 75, 2012, Pages 2479-2487

  Blamires, Sean J ^a   Wu, Chung Lin ^c   Blackledge, Todd A ^d   Tso, I Min ^a,b  

^a TUNGHAI UNIVERSITY   (Taiwan)

^b TUNGHAI UNIVERSITY   (Taiwan)

^c INDUSTRIAL TECHNOLOGY RESEARCH INSTITUTE   (Taiwan)

^d UNIVERSITY OF AKRON   (United States)

Author keywords

Biomaterial plasticity; MaSp expression model; Mechanical properties; Orb web; Spider silk; Supercontraction

Indexed keywords

AMINO ACIDS; GROUND STATE; MECHANICAL PROPERTIES; MECHANICS; PHYSIOLOGY; PROTEINS;

AMINO ACID COMPOSITIONS; COMPOSITIONAL CHANGES; MAJOR AMPULLATE; MECHANICAL PERFORMANCE; ORB WEB; PHENOTYPIC VARIATIONS; PROTEIN COMPOSITION; SHEET CRYSTALS; SILK MECHANICS; SPIDER SILKS; SPINNING SPEED; SUPERCONTRACTION;

SILK;

ALANINE; GLYCINE; PROLINE;

AMINO ACID COMPOSITION; ARGIOPE AEMULA; ARGIOPE AETHEREA; ARTICLE; BETA SHEET; CONTROLLED STUDY; CYCLOSA CONFUSA; CYCLOSA MULMEINENSIS; CYRTOPHORA MOLUCCENSIS; CYRTOPHORA UNICOLOR; FEMALE; INTERSPECIFIC RELATIONSHIP; LEUCAUGE BLANDA; LEUCAUGE TESSELATA; MAJOR AMPULLATE SILK; NEPHILA CLAVATA; NEPHILA PILIPES; NONHUMAN; PERFORMANCE; PROTEIN ANALYSIS; SILK; SPIDER;

ARANEAE; HEXAPODA;

EID: 84866242913     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2012.0277     Document Type: Article

References (52)

1. Bull, J. J. 1987 Evolution of phenotypic variance. Evolution 41, 303-315. (doi:10.2307/2409140)
2. Behera, N. & Nanjundiah, V. 2004 Phenotypic plasticity can potentiate rapid evolutionary change. J. Theor. Biol. 226, 177-184. (doi:10.1016/j.jtbi. 2003.08.011)
3. Rice, S. H. 2004 Evolutionary theory: mathematical and conceptual foundations. Sunderland, MA: Sinauer Press.
4. Ghalambor, C. K., McKay, J. K., Carroll, S. P. & Reznik, D. N. 2007 Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21, 394-407. (doi:10.1111/j.1365-2435.2007.01283.x)
5. Harvell, C. D. 1990 The ecology and evolution of inducible defenses. Q. Rev. Biol. 65, 323-340. (doi:10.1086/416841)
6. Nussey, D. H., Wilson, A. J. & Brommer, J. E. 2007 The evolutionary ecology of individual phenotypic plasticity in wild populations. J. Evol. Biol. 20, 831-844. (doi:10.1111/j.1420-9101.2007.01300.x)
7. Scoville, A. G. & Pfender, M. E. 2010 Phenotypic plasticity facilitates recurrent rapid adaptation to introduced predators. Proc. Natl Acad. Sci. USA 107, 4260-4263. (doi:10.1073/pnas.0912748107)
8. Gosline, J. M., Lillie, M., Guerette, P., Ortlepp, C. & Savage, K. 2002 Elastic proteins: biological role and mechanical properties. Phil. Trans. R. Soc. Lond. B 357, 121-132. (doi:10.1098/rstb.2001.1022)
9. Fudge, D. S., Winegard, T., Ewoldt, R. H., Beriault, D., Szewciw, L. & McKinley, G. H. 2009 From ultra-soft slime to hard α-keratins: the many lives of intermediate filaments. Integr. Comp. Biol. 49, 32-39. (doi:10.1093/icb/icp007)
10. Waite, J. H.& Broomell, C. C. 2012 Changing environments and structure-property relationships in marine biomaterials. J. Exp. Biol. 215, 873-883. (doi:10.1242/jeb.058925)
11. Vollrath, F., Porter, D. & Holland, C. 2011 There are many more lessons still to be learned from spider silk. Soft Mater. 7, 9595-9600. (doi:10.1039/c1sm05812f)
12. Blamires, S. J. & Tso, I. M. 2012 Ecophysiological influences on spider silk properties and the potential for producing adaptable, degradation resistant biomaterials. In Silks: properties, production and uses (ed. P. Aramwit), pp. 139-154. New York, NY: Nova Science.
13. Swanson, B. O., Blackledge, T. A., Summers, A. P. & Hayashi, C. Y. 2006 Spider dragline silk: correlated and mosaic evolution in high-performance biological materials. Evolution 60, 2539-2551.
14. Giesa, T., Arslan, M., Pugno, N. M. & Buehler, M. J. 2011 Nanoconfinement of spider silk fibers begets superior strength, extensibility and toughness. Nano Lett. 11, 5038-5046. (doi:10.1021/nl203108t)
15. Xu, M. & Lewis, R. V. 1990 Structure of a protein superfiber: spider dragline silk. Proc. Natl Acad. Sci. USA 87, 7120-7124. (doi:10.1073/pnas.87.18. 7120)
16. Hinman, M. B. & Lewis, R. V. 1992 Isolation of a clone encoding a second dragline silk fibroin: Nephila clavipes dragline silk is a two-protein fiber. J. Biol. Chem. 267, 19 320-19 324.
17. Savage, K. N. & Gosline, J. M. 2008 The effect of proline on the network structure of major ampullate silks as inferred from their mechanical and optical properties. J. Exp. Biol. 211, 1937-1947. (doi:10.1242/jeb.014217)
18. Liu, Y., Sponner, A., Porter, D. & Vollrath, F. 2008 Proline and processing of spider silks. Biomacromolecules 9, 116-121. (doi:10.1021/ bm700877g)
19. Guinea, G. V., Cerdeira, M., Plaza, G. R., Elices, M. & Perez-Rigueiro, J. 2010 Recovery in viscid line fibers. Biomacromolecules 11, 1174-1179. (doi:10.1021/bm901285c)
20. Ayoub, N. A., Garb, J. E., Tinghitella, R. M., Collin, M. A. & Hayashi, C. Y. 2007 Blueprint for a high-performance biomaterial: full-length spider dragline silk genes. PLoS ONE 2, e514. (doi:10.1371/journal.pone.0000514)
21. Blamires, S. J., Wu, C. L. & Tso, I. M. 2012 Variation in protein expression induces variation in spider silk expression. PLoS ONE 7, e31626. (doi:10.1371/journal.pone.0031626)
22. Bittencourt, D. et al. 2007 Spidroins from the Brazilian spider Nephilengys cruentata (Araneae: Nephilidae). Comp. Biochem. Physiol. B 147, 597-606. (doi:10.1016/j.cbpb.2007.03.013)
23. Creager, M. S., Jenkins, J. E., Thagard-Yeaman, L. A., Brooks, A. E., Jones, J. A., Lewis, R. V., Holland, G. P. & Yarger, J. L. 2010 Solid-state NMR comparison of various spider's dragline silk fiber. Biomacromolecules 11, 2039-2043. (doi:10.1021/bm100399x)
24. Madsen, B., Shao, Z. & Vollrath, F. 1999 Variability in the mechanical properties of spider silks on three levels: interspecific, intraspecific and intraindividual. Inter. J. Biol. Macromol. 24, 301-306. (doi:10.1016/S0141-8130(98)00094-4)
25. Garrido, M. A., Elices, M., Viney, C. & Perez-Riguero, J. 2002 Active control of spider silk strength: comparison of draglines spun on vertical and horizontal surfaces. Polymer 43, 1537-1540. (doi:10.1016/S0032-3861(01)00713-3)
26. Boutry, C., Rezac, M. & Blackledge, T. A. 2011 Plasticity in major ampullate silk production in relation to spider phylogeny and ecology. PLoS ONE 6, e22467. (doi:10.1371/journal.pone.0022467)
27. Vollrath, F. & Knight, D. P. 2001 Liquid crystalline spinning of spider silk. Nature 410, 541-548. (doi:10.1038/35069000)
28. Dicko, C., Kennedy, J. M., Knight, D. P. & Vollrath, F. 2004 Transition to a β-sheet-rich structure in spidroin in vitro: the effects of pH and cations. Biochemistry 43, 14 080-14 087.
29. Peng, X, Shao, Z., Chen, X., Knight, D. P., Wu, P. & Vollrath, F. 2005 Further investigation of the potassium-induced conformation transition of Nephila spidroin film with two-dimensional infrared correlation spectroscopy. Biomacromolecules 6, 302-308. (doi:10.1021/bm049598j)
30. Casem, M. L., Tran, K. T. & Moore, A. M. F. 2002 Ultrastructure of the major ampullate gland of the black widow spider, Latrodectus hesperus. Tissue Cell 34, 427-436. (doi:10.1016/S0040816602000836)
31. Lefevre, T., Boudreault, S., Cloutier, C. & Pezolet, M. 2011 Diversity of molecular transformations involved in the formation of spider silks. J. Mol. Biol. 405, 238-253. (doi:10.1016/j.jmb.2010.10.052)
32. Liao, C. P., Chi, K. J. & Tso, I. M. 2009 The effects of wind on trap structural and material properties of a sit-and-wait predator. Behav. Ecol. 20, 1194-1203. (doi:10.1093/beheco/arp119)
33. Work, R. W. 1985 Viscoelastic behaviour and wet supercontraction of major ampullate silk fibres of certain web-building spiders (Araneae). J. Exp. Biol. 118, 379-404.
34. Liu, Y., Shao, Z. & Vollrath, F. 2005 Relationships between supercontraction and mechanical properties of spider silk. Nat. Mater. 4, 901-905. (doi:10.1038/nmat1534)
35. Agnarsson, I., Boutry, C., Wong, S. C., Baji, A., Dhinojwala, A., Sensenig, A. & Blackledge, T. A. 2009 Supercontraction forces in spider dragline silk depend on hydration rate. Zoology 112, 325-331. (doi:10.1016/j.zool.2008.11.003)
36. Boutry, C. & Blackledge, T. A. 2010 Evolution of supercontraction in spider silk: structure-function relationship from tarantulas to orb-weavers. J. Exp. Biol. 213, 3505-3514. (doi:10.1242/jeb.046110)
37. Fu, C., Porter, D. & Shao, Z. 2009 Moisture effects on Antheraea pernyi silk's mechanical property. Macromolecules 42, 7877-7880. (doi:10.1021/ma901321k)
38. Elices, M., Guinea, G. V., Plaza, G. R., Karatzas, C., Riekel, C., Agullo-Rueda, F., Daza, R. & Perez-Riguero, J. 2011 Bioinspired fibers follow the track of natural spider silk. Macromolecules 44, 1166-1176. (doi:10.1021/ma102291m)
39. Elices, M., Plaza, G. R., Pérez-Rigueiro, J. & Guinea, G. V. 2011 The hidden link between supercontraction and mechanical behavior of spider silks. J. Mech. Behav. Biomed. Mater. 4, 658-669. (doi:10.1016/j.jmbbm.2010.09. 008)
40. Brooks, A. E., Nelson, S. R., Jones, J. A., Koenig, C., Hinman, M., Stricker, S. & Lewis, R. V. 2008 Distinct contributions of model MaSp1 and MaSp2 like peptides to the mechanical properties of synthetic major ampullate silk fibers as revealed in silico. Nanotechnol. Sci. Appl. 1, 9-16.
41. Felsenstein, J. 1985 Phylogenies and the comparative method. Am. Nat. 125, 1-15. (doi:10.1086/284325)
42. Blamires, S. J., Wu, C. L., Blackledge, T. A. & Tso, I.-M. In press. Environmentally-induced post-spin property changes in spider silks: influences of web type, spidroin composition and ecology. Biol. J. Linn. Soc. (doi:10.1111/j.1095-8312.2012.01884.x)
43. Blackledge, T. A., Scharff, N., Coddington, J. A., Szuts, T., Wenzel, J. W., Hayashi, C. Y. & Agnarsson, I. 2009 Reconstructing web evolution and spider diversification in the molecular era. Proc. Natl Acad. Sci. USA 106, 5229-5234. (doi:10.1073/pnas.0901377106)
44. Sensenig, A., Agnarsson, I. & Blackledge, T. A. 2010 Behavioural and biomaterial coevolution in spider orb webs. J. Evol. Biol. 23, 1839-1856. (doi:10.1111/j.1420-9101.2010.02048.x)
45. Sensenig, A., Agnarsson, I. & Blackledge, T. A. 2011 Adult spiders use tougher silk: ontogenetic changes in web architecture and silk biomechanics in the orb-weaver spider. J. Zool. 285, 28-38.
46. Herberstein, M. E. & Tso, I. M. 2000 Evaluation of formulae to estimate the capture area and mesh height of orb webs (Araneoidea, Araneae). J. Arachnol. 28, 180-184. (doi:10.1636/0161-8202(2000)028[0180:EOFTET]2.0.CO;2)
47. Tso, I. M. & Severinghaus, L. L. 2000 Argyrodes fissifrons inhabiting webs of Cyrtophora hosts: prey size distribution and population characteristics. Zool. Stud. 39, 236-242.
48. Blackledge, T. A. & Hayashi, C. Y. 2006 Unraveling the mechanical properties of composite silk threads spun by cribellate orb-weaving spiders. J. Exp. Biol. 209, 3131-3140. (doi:10.1242/jeb.02327)
49. Guinea, G. V., Perez-Rigueiro, J., Plaza, G. R. & Elices, M. 2006 Volume constancy during stretching of spider silk. Biomacromolecules 7, 2173-2177. (doi:10.1021/bm060138v)
50. Blamires, S. J., Chao, I. C. & Tso, I. M. 2010 Prey type, vibrations and handling interactively influence spider silk expression. J. Exp. Biol. 213, 3906-3910. (doi:10.1242/jeb.046730)
51. Savage, K. N. & Gosline, J. M. 2008 The role of proline in the elastic mechanism of hydrated spider silks. J. Exp. Biol. 211, 1948-1957. (doi:10.1242/jeb.014225)
52. Elices, M., Plaza, G. R., Arnedo, M. A., Perez-Riguero, J., Torres, F. G. & Guinea, G. V. 2009 Mechanical behavior of silk during the evolution of orb-web spinning spiders. Biomacromolecules 10, 1904-1910. (doi:10.1021/ bm900312c)