Nanofibrils as Building Blocks of Silk Fibers: Critical Review of the Experimental Evidence

Abstract

Silks have fascinated researchers for decades, featuring outstanding mechanical performance and vast potential as a multifunctional material. Development of synthetic fibers mimicking natural silk is a major goal but has been hindered by insufficient knowledge of the silk structure. Nanoscale fibrils have long been suggested to play a significant role in silk; in this review, we examine prior evidence of nanofibrils in spider and silkworm silks. We found the available data far from conclusive. The volumetric percentage of nanofibrils in silk fibers is totally unclear, and conflicting results have been reported regarding their physical dimensions, morphology, and spatial organization. Some works have proposed an entirely different, globular nanostructure of silk fibers. Hence, many of the structural models were developed based on incomplete evidence. Our review highlights the gaps in knowledge about the nanostructure of silk fibers and can act as a guide for future studies.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  1. 1.

    F. Vollrath and D.P. Knight, Nature 410, 541 (2001).

    Article  Google Scholar 

  2. 2.

    F.G. Omenetto and D.L. Kaplan, Science 329, 528 (2010).

    Article  Google Scholar 

  3. 3.

    J. Gosline, P. Guerette, C. Ortlepp, and K. Savage, J. Exp. Biol. 202, 3295 (1999).

    Google Scholar 

  4. 4.

    I. Agnarsson, M. Kuntner, and T.A. Blackledge, PLoS ONE 5, e11234 (2010).

    Article  Google Scholar 

  5. 5.

    H.C. Schniepp, S.R. Koebley, and F. Vollrath, Adv. Mater. 25, 7028 (2013).

    Article  Google Scholar 

  6. 6.

    S.R. Koebley, F. Vollrath, and H.C. Schniepp, Mater. Horiz. 4, 377 (2017).

    Article  Google Scholar 

  7. 7.

    M. Andersson, Q. Jia, A. Abella, X.-Y. Lee, M. Landreh, P. Purhonen, H. Hebert, M. Tenje, C.V. Robinson, Q. Meng, G.R. Plaza, J. Johansson, and A. Rising, Nat. Chem. Biol. 13, 262 (2017).

    Article  Google Scholar 

  8. 8.

    M. Heim, D. Keerl, and T. Scheibel, Angew. Chem. Int. Ed. 48, 3584 (2009).

    Article  Google Scholar 

  9. 9.

    X.-X. Xia, Z.-G. Qian, C.S. Ki, Y.H. Park, D.L. Kaplan, and S.Y. Lee, Proc. Natl. Acad. Sci. 107, 14059 (2010).

    Article  Google Scholar 

  10. 10.

    A. Heidebrecht, L. Eisoldt, J. Diehl, A. Schmidt, M. Geffers, G. Lang, and T. Scheibel, Adv. Mater. 27, 2189 (2015).

    Article  Google Scholar 

  11. 11.

    A. Koeppel and C. Holland, ACS Biomater. Sci. Eng. 3, 226 (2017).

    Article  Google Scholar 

  12. 12.

    Q. Wang and H. C. Schniepp, ACS Macro Lett. 7, 1364 (2018).

    Article  Google Scholar 

  13. 13.

    N. Du, X.Y. Liu, J. Narayanan, L. Li, M.L.M. Lim, and D. Li, Biophys. J. 91, 4528 (2006).

    Article  Google Scholar 

  14. 14.

    A. Sponner, W. Vater, S. Monajembashi, E. Unger, F. Grosse, and K. Weisshart, PLoS ONE 2, e998 (2007).

    Article  Google Scholar 

  15. 15.

    M. Kitagawa and T. Kitayama, J. Mater. Sci. 32, 2005 (1997).

    Article  Google Scholar 

  16. 16.

    C. Riekel, M. Burghammer, T.G. Dane, C. Ferrero, and M. Rosenthal, Biomacromol 18, 231 (2017).

    Article  Google Scholar 

  17. 17.

    L.P. Silva and E.L. Rech, Nat. Commun. 4, (2013).

  18. 18.

    L.D. Miller, S. Putthanarat, R.K. Eby, and W.W. Adams, Int. J. Biol. Macromol. 24, 159 (1999).

    Article  Google Scholar 

  19. 19.

    S. Ling, D.L. Kaplan, and M.J. Buehler, Nat. Rev. Mater. 3, 18016 (2018).

    Article  Google Scholar 

  20. 20.

    M. Humenik, G. Lang, and T. Scheibel, Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 10, e1509 (2018).

    Article  Google Scholar 

  21. 21.

    T. Giesa, M. Arslan, N.M. Pugno, and M.J. Buehler, Nano Lett. 11, 5038 (2011).

    Article  Google Scholar 

  22. 22.

    C.P. Brown, C. Harnagea, H.S. Gill, A.J. Price, E. Traversa, S. Licoccia, and F. Rosei, ACS Nano 6, 1961 (2012).

    Article  Google Scholar 

  23. 23.

    N. Du, Z. Yang, X.Y. Liu, Y. Li, and H.Y. Xu, Adv. Funct. Mater. 21, 772 (2010).

    Article  Google Scholar 

  24. 24.

    R. Liu, Q. Deng, Z. Yang, D. Yang, M.-Y. Han, and X.Y. Liu, Adv. Funct. Mater. 26, 5534 (2016).

    Article  Google Scholar 

  25. 25.

    S.F. Li, A.J. McGhie, and S.L. Tang, Biophys. J. 66, 1209 (1994).

    Article  Google Scholar 

  26. 26.

    D.P. Knight and F. Vollrath, Philos. Trans. R. Soc. B Biol. Sci. 357, 155 (2002).

    Article  Google Scholar 

  27. 27.

    S.E. Naleway, M.M. Porter, J. McKittrick, and M.A. Meyers, Adv. Mater. 27, 5455 (2015).

    Article  Google Scholar 

  28. 28.

    M.D. Shoulders and R.T. Raines, Annu. Rev. Biochem. 78, 929 (2009).

    Article  Google Scholar 

  29. 29.

    A.J.S. Fox, A. Bedi, and S.A. Rodeo, Sports Health Multidiscip. Approach 1, 461 (2009).

    Article  Google Scholar 

  30. 30.

    V. Ottani, D. Martini, M. Franchi, A. Ruggeri, and M. Raspanti, Micron 33, 587 (2002).

    Article  Google Scholar 

  31. 31.

    N. Mittal, F. Ansari, V.K. Gowda, C. Brouzet, P. Chen, P.T. Larsson, S.V. Roth, F. Lundell, L.W. Agberg, N.A. Kotov, and L.D. Söderberg, ACS Nano 12, 6378 (2018).

    Article  Google Scholar 

  32. 32.

    S. Ling, W. Chen, Y. Fan, K. Zheng, K. Jin, H. Yu, M.J. Buehler, and D.L. Kaplan, Prog. Polym. Sci. 85, 1 (2018).

    Article  Google Scholar 

  33. 33.

    W. Zhang, C. Ye, K. Zheng, J. Zhong, Y. Tang, Y. Fan, M.J. Buehler, S. Ling, and D.L. Kaplan, ACS Nano 12, 6968 (2018).

    Article  Google Scholar 

  34. 34.

    M.J. Buehler, Nano Today 5, 379 (2010).

    Article  Google Scholar 

  35. 35.

    L. Eisoldt, A. Smith, and T. Scheibel, Mater. Today 14, 80 (2011).

    Article  Google Scholar 

  36. 36.

    S. Keten, Z. Xu, B. Ihle, and M.J. Buehler, Nat. Mater. 9, 359 (2010).

    Article  Google Scholar 

  37. 37.

    I. Su and M.J. Buehler, Nanotechnology 27, 302001 (2016).

    Article  Google Scholar 

  38. 38.

    I. Su and M.J. Buehler, Nat. Mater. 15, 1054 (2016).

    Article  Google Scholar 

  39. 39.

    S. Ling, C. Li, K. Jin, D.L. Kaplan, and M.J. Buehler, Adv. Mater. 28, 7783 (2016).

    Article  Google Scholar 

  40. 40.

    Q. Niu, Q. Peng, L. Lu, S. Fan, H. Shao, H. Zhang, R. Wu, B.S. Hsiao, and Y. Zhang, ACS Nano 12, 11860 (2018).

    Article  Google Scholar 

  41. 41.

    K. Augsten, P. Mühlig, and C. Herrmann, Scanning 22, 12 (2000).

    Article  Google Scholar 

  42. 42.

    F. Vollrath, T. Holtet, H.C. Thogersen, and S. Frische, Proc. R. Soc. B Biol. Sci. 263, 147 (1996).

    Article  Google Scholar 

  43. 43.

    P. Poza, J. Pérez-Rigueiro, M. Elices, and J. Llorca, Eng. Fract. Mech. 69, 1035 (2002).

    Article  Google Scholar 

  44. 44.

    S. Putthanarat, N. Stribeck, S.A. Fossey, R.K. Eby, and W.W. Adams, Polymer 41, 7735 (2000).

    Article  Google Scholar 

  45. 45.

    M. Boulet-Audet, C. Holland, T. Gheysens, and F. Vollrath, Biomacromolecules 17, 3198 (2016).

    Article  Google Scholar 

  46. 46.

    J. Pérez-Rigueiro, M. Elices, G.R. Plaza, and G.V. Guinea, Macromolecules 40, 5360 (2007).

    Article  Google Scholar 

  47. 47.

    O. Hakimi, D.P. Knight, M.M. Knight, M.F. Grahn, and P. Vadgama, Biomacromolecules 7, 2901 (2006).

    Article  Google Scholar 

  48. 48.

    Y. Shen, M.A. Johnson, and D.C. Martin, Macromolecules 31, 8857 (1998).

    Article  Google Scholar 

  49. 49.

    D.C. Joy and J.B. Pawley, Ultramicroscopy 47, 80 (1992).

    Article  Google Scholar 

  50. 50.

    D.B. Williams and C.B. Carter, Transmission Electron Microscopy (New York: Springer, 1996), pp. 3–17.

    Google Scholar 

  51. 51.

    Q. Wan, K.J. Abrams, R.C. Masters, A.C.S. Talari, I.U. Rehman, F. Claeyssens, C. Holland, and C. Rodenburg, Adv. Mater. 29, 1703510 (2017).

    Article  Google Scholar 

  52. 52.

    S.A.C. Gould, K.T. Tran, J.C. Spagna, A.M.F. Moore, and J.B. Shulman, Int. J. Biol. Macromol. 24, 151 (1999).

    Article  Google Scholar 

  53. 53.

    I. Greving, M. Cai, F. Vollrath, and H.C. Schniepp, Biomacromolecules 13, 676 (2012).

    Article  Google Scholar 

  54. 54.

    B.R. Neugirg, S.R. Koebley, H.C. Schniepp, and A. Fery, Nanoscale 8, 8414 (2016).

    Article  Google Scholar 

  55. 55.

    J. Pérez-Rigueiro, M. Elices, G.R. Plaza, J. Rueda, and G.V. Guinea, J. Polym. Sci. Part B Polym. Phys. 45, 786 (2007).

    Article  Google Scholar 

  56. 56.

    Z. Yang, D.T. Grubb, and L.W. Jelinski, Macromolecules 30, 8254 (1997).

    Article  Google Scholar 

  57. 57.

    D. Sapede, T. Seydel, V.T. Forsyth, M.M. Koza, R. Schweins, F. Vollrath, and C. Riekel, Macromolecules 38, 8447 (2005).

    Article  Google Scholar 

  58. 58.

    P.L. Babb, N.F. Lahens, S.M. Correa-Garhwal, D.N. Nicholson, E.J. Kim, J.B. Hogenesch, M. Kuntner, L. Higgins, C.Y. Hayashi, I. Agnarsson, and B.F. Voight, Nat. Genet. 49, 895 (2017).

    Article  Google Scholar 

  59. 59.

    E.R. Hoebeke, W. Huffmaster, and B.J. Freeman, PeerJ 3, e763 (2015).

    Article  Google Scholar 

  60. 60.

    D.P. Knight and F. Vollrath, Philos. Trans. R. Soc. B Biol. Sci. 357, 219 (2002).

    Article  Google Scholar 

  61. 61.

    A. Sponner, B. Schlott, F. Vollrath, E. Unger, F. Grosse, and K. Weisshart, Biochemistry 44, 4727 (2005).

    Article  Google Scholar 

  62. 62.

    L.R. Parent, D. Onofrei, D. Xu, D. Stengel, J.D. Roehling, J.B. Addison, C. Forman, S.A. Amin, B.R. Cherry, J.L. Yarger, N.C. Gianneschi, and G.P. Holland, Proc. Natl. Acad. Sci. 115, 11507 (2018).

    Article  Google Scholar 

  63. 63.

    R.W. Work, Text. Res. J. 47, 650 (1977).

    Article  Google Scholar 

  64. 64.

    G.P. Holland, J.E. Jenkins, M.S. Creager, R.V. Lewis, and J.L. Yarger, Biomacromolecules 9, 651 (2008).

    Article  Google Scholar 

  65. 65.

    P. Papadopoulos, R. Ene, I. Weidner, and F. Kremer, Macromol. Rapid Commun. 30, 851 (2009).

    Article  Google Scholar 

  66. 66.

    C.Y. Hayashi and R.V. Lewis, BioEssays 23, 750 (2001).

    Article  Google Scholar 

  67. 67.

    C.Y. Hayashi, Mol. Biol. Evol. 21, 1950 (2004).

    Article  Google Scholar 

  68. 68.

    E. Gnesa, Y. Hsia, J.L. Yarger, W. Weber, J. Lin-Cereghino, G. Lin-Cereghino, S. Tang, K. Agari, and C. Vierra, Biomacromolecules 13, 304 (2012).

    Article  Google Scholar 

  69. 69.

    A. Rising, G. Hjälm, W. Engström, and J. Johansson, Biomacromolecules 7, 3120 (2006).

    Article  Google Scholar 

  70. 70.

    G.V. Guinea, M. Elices, G.R. Plaza, G.B. Perea, R. Daza, C. Riekel, F. Agulló-Rueda, C. Hayashi, Y. Zhao, and J. Pérez-Rigueiro, Biomacromolecules 13, 2087 (2012).

    Article  Google Scholar 

  71. 71.

    W. Eberhard and F. Pereira, J. Arachnol. 21, 161 (1993).

    Google Scholar 

  72. 72.

    G. Xu, L. Gong, Z. Yang, and X.Y. Liu, Soft Matter 10, 2116 (2014).

    Article  Google Scholar 

  73. 73.

    L.-S. Dai, C. Qian, L. Wang, G.-Q. Wei, Q.-N. Liu, Y. Sun, C.-F. Zhang, J. Li, D.-R. Liu, B.-J. Zhu, and C.-L. Liu, J. Asia-Pac. Entomology 18, 701 (2015).

    Article  Google Scholar 

  74. 74.

    A. Bram, C.I. Brändén, C. Craig, I. Snigireva, and C. Riekel, J. Appl. Crystallogr. 30, 390 (1997).

    Article  Google Scholar 

  75. 75.

    C. Riekel, M. Rössle, D. Sapede, and F. Vollrath, Naturwissenschaften 91, 30 (2004).

    Article  Google Scholar 

  76. 76.

    C. Riekel and F. Vollrath, Int. J. Biol. Macromol. 29, 203 (2001).

    Article  Google Scholar 

  77. 77.

    C. Riekel, B. Madsen, D. Knight, and F. Vollrath, Biomacromolecules 1, 622 (2000).

    Article  Google Scholar 

  78. 78.

    C. Riekel, C. Bränden, C. Craig, C. Ferrero, F. Heidelbach, and M. Müller, Int. J. Biol. Macromol. 24, 179 (1999).

    Article  Google Scholar 

  79. 79.

    D.T. Grubb and L.W. Jelinski, Macromolecules 30, 2860 (1997).

    Article  Google Scholar 

  80. 80.

    E. Oroudjev, J. Soares, S. Arcidiacono, J.B. Thompson, S.A. Fossey, and H.G. Hansma, Proc. Natl. Acad. Sci. 99, 6460 (2002).

    Article  Google Scholar 

  81. 81.

    A. Tarakanova and M.J. Buehler, JOM 64, 214 (2012).

    Article  Google Scholar 

Download references

Acknowledgements

This material is based upon work supported by the National Science Foundation under Grant No. DMR-1352542.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Hannes C. Schniepp.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Wang, Q., Schniepp, H.C. Nanofibrils as Building Blocks of Silk Fibers: Critical Review of the Experimental Evidence. JOM 71, 1248–1263 (2019). https://doi.org/10.1007/s11837-019-03340-y

Download citation