Advertisement

Natural Composite Systems for Bioinspired Materials

  • Joseph A. Frezzo
  • Jin Kim MontclareEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 940)

Abstract

From a relatively limited selection of base materials, nature has steered the development of truly remarkable materials. The simplest and often overlooked organisms have demonstrated the ability to manufacture multi-faceted, molecular-level hierarchical structures that combine mechanical properties rarely seen in synthetic materials. Indeed, these natural composite systems, composed of an array of intricately arranged and functionally relevant organic and inorganic substances serve as inspiration for materials design. A better understanding of these composite systems, specifically at the interface of the hetero-assemblies, would encourage faster development of environmentally friendly “green” materials with molecular level specificities.

Keywords

Structural hierarchy Molecular-level hierarchy Biomimetic composites Interfacial materials Molecular-scale interactions Nanostructural design 

Notes

Acknowledgement

This work was supported by ARO W911NF-15-1-0304 and NSF MRSEC Program under Award Number DMR-1420073.

References

  1. 1.
    Hench LL (1998) Bioceramics. J Am Ceram Soc 81(7):1705–1728CrossRefGoogle Scholar
  2. 2.
    Chen P-Y, McKittrick J, Meyers MA (2012) Biological materials: functional adaptations and bioinspired designs. Prog Mater Sci 57(8):1492–1704CrossRefGoogle Scholar
  3. 3.
    Fratzl P (2007) Biomimetic materials research: what can we really learn from nature’s structural materials? J R Soc Interface 4(15):637–642PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Studart AR (2012) Towards high-performance bioinspired composites. Adv Mater 24(37):5024–5044PubMedCrossRefGoogle Scholar
  5. 5.
    Fratzl P, Weinkamer R (2007) Nature’s hierarchical materials. Prog Mater Sci 52(8):1263–1334CrossRefGoogle Scholar
  6. 6.
    Zhang S (2003) Building from the bottom up. Mater Today 6(5):20–27CrossRefGoogle Scholar
  7. 7.
    Weiner S, Wagner HD (1998) THE MATERIAL BONE: structure–mechanical function relations. Annu Rev Mater Sci 28(1):271–298CrossRefGoogle Scholar
  8. 8.
    Wagner DO, Aspenberg P (2011) Where did bone come from? Acta Orthop 82(4):393–398PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Sanchez C, Arribart H, Giraud Guille MM (2005) Biomimetism and bioinspiration as tools for the design of innovative materials and systems. Nat Mater 4(4):277–288PubMedCrossRefGoogle Scholar
  10. 10.
    Xia F, Jiang L (2008) Bio-inspired, smart, multiscale interfacial materials. Adv Mater 20(15):2842–2858CrossRefGoogle Scholar
  11. 11.
    Furuhashi T et al (2009) Molluscan shell evolution with review of shell calcification hypothesis. Comp Biochem Physiol B: Biochem Mol Biol 154(3):351–371CrossRefGoogle Scholar
  12. 12.
    Lia A, Steve W (2014) Biomineralization: mineral formation by organisms. Phys Scr 89(9):098003CrossRefGoogle Scholar
  13. 13.
    Marlow F, Khalil ASG, Stempniewicz M (2007) Circular mesostructures: solids with novel symmetry properties. J Mater Chem 17(21):2168–2182CrossRefGoogle Scholar
  14. 14.
    Rho J-Y, Kuhn-Spearing L, Zioupos P (1998) Mechanical properties and the hierarchical structure of bone. Med Eng Phys 20(2):92–102PubMedCrossRefGoogle Scholar
  15. 15.
    Almine JF et al (2010) Elastin-based materials. Chem Soc Rev 39(9):3371–3379PubMedCrossRefGoogle Scholar
  16. 16.
    Giraud-Guille M-M, Belamie E, Mosser G (2004) Organic and mineral networks in carapaces, bones and biomimetic materials. C R Palevol 3(6–7):503–513CrossRefGoogle Scholar
  17. 17.
    Roer R, Dillaman R (1984) The structure and calcification of the crustacean cuticle. Am Zool 24(4):893–909CrossRefGoogle Scholar
  18. 18.
    Wilt FH (2005) Developmental biology meets materials science: morphogenesis of biomineralized structures. Dev Biol 280(1):15–25PubMedCrossRefGoogle Scholar
  19. 19.
    Lopez MI et al (2011) Growth of nacre in abalone: seasonal and feeding effects. Mater Sci Eng C 31(2):238–245CrossRefGoogle Scholar
  20. 20.
    Chen PY et al (2008) Structure and mechanical properties of selected biological materials. J Mech Behav Biomed Mater 1(3):208–226PubMedCrossRefGoogle Scholar
  21. 21.
    Meyers MA et al (2011) Biological materials: a materials science approach. J Mech Behav Biomed Mater 4(5):626–657PubMedCrossRefGoogle Scholar
  22. 22.
    Welinder BS (1975) The crustacean cuticle—III. Composition of the individual layers in cancer pagurus cuticle. Comp Biochem Physiol A Physiol 52(4):659–663CrossRefGoogle Scholar
  23. 23.
    Giraud-Guille MM (1984) Fine structure of the chitin-protein system in the crab cuticle. Tissue Cell 16(1):75–92PubMedCrossRefGoogle Scholar
  24. 24.
    Sachs C, Fabritius H, Raabe D (2008) Influence of microstructure on deformation anisotropy of mineralized cuticle from the lobster Homarus americanus. J Struct Biol 161(2):120–132PubMedCrossRefGoogle Scholar
  25. 25.
    Raabe D et al (2007) Preferred crystallographic texture of α-chitin as a microscopic and macroscopic design principle of the exoskeleton of the lobster Homarus americanus. Acta Biomater 3(6):882–895PubMedCrossRefGoogle Scholar
  26. 26.
    Suzuki M, Nagasawa H (2013) Mollusk shell structures and their formation mechanism1. Can J Zool 91(6):349–366CrossRefGoogle Scholar
  27. 27.
    Sun J, Bhushan B (2012) Hierarchical structure and mechanical properties of nacre: a review. RSC Adv 2(20):7617–7632CrossRefGoogle Scholar
  28. 28.
    Gotliv B-A, Addadi L, Weiner S (2003) Mollusk shell acidic proteins: in search of individual functions. ChemBioChem 4(6):522–529PubMedCrossRefGoogle Scholar
  29. 29.
    Mann S (1988) Molecular recognition in biomineralization. Nature 332(6160):119–124CrossRefGoogle Scholar
  30. 30.
    Cartwright JHE, Checa AG (2007) The dynamics of nacre self-assembly. J R Soc Interface 4(14):491–504PubMedCrossRefGoogle Scholar
  31. 31.
    Lin A, Meyers MA (2005) Growth and structure in abalone shell. Mater Sci Eng A 390(1–2):27–41CrossRefGoogle Scholar
  32. 32.
    Takeuchi T et al (2008) In vitro regulation of CaCO3 crystal polymorphism by the highly acidic molluscan shell protein Aspein. FEBS Lett 582(5):591–596PubMedCrossRefGoogle Scholar
  33. 33.
    Kim IW et al (2005) Molecular “Tuning” of crystal growth by nacre-associated polypeptides. Cryst Growth Des 6(1):5–10CrossRefGoogle Scholar
  34. 34.
    Amos FF, Evans JS (2009) AP7, a partially disordered pseudo C-RING protein, is capable of forming stabilized aragonite in vitro. Biochemistry 48(6):1332–1339PubMedCrossRefGoogle Scholar
  35. 35.
    Kono M, Hayashi N, Samata T (2000) Molecular mechanism of the nacreous layer formation in Pinctada maxima. Biochem Biophys Res Commun 269(1):213–218PubMedCrossRefGoogle Scholar
  36. 36.
    Keene EC, Evans JS, Estroff LA (2010) Silk fibroin hydrogels coupled with the n16N − β-chitin complex: an in vitro organic matrix for controlling calcium carbonate mineralization. Cryst Growth Des 10(12):5169–5175CrossRefGoogle Scholar
  37. 37.
    Asakura T et al (2006) Conformational study of silklike peptides modified by the addition of the calcium-binding sequence from the shell nacreous matrix protein MSI60 using 13C CP/MAS NMR spectroscopy. Biomacromolecules 7(6):1996–2002PubMedCrossRefGoogle Scholar
  38. 38.
    Kato T et al (1998) Effects of macromolecules on the crystallization of CaCO3 the formation of organic/inorganic composites. Supramol Sci 5(3–4):411–415CrossRefGoogle Scholar
  39. 39.
    Amos FF, Ponce CB, Evans JS (2011) Formation of framework nacre polypeptide supramolecular assemblies that nucleate polymorphs. Biomacromolecules 12(5):1883–1890PubMedCrossRefGoogle Scholar
  40. 40.
    Smith BL et al (1999) Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature 399(6738):761–763CrossRefGoogle Scholar
  41. 41.
    Wang R, Gupta HS (2011) Deformation and fracture mechanisms of bone and nacre. Annu Rev Mater Res 41(1):41–73CrossRefGoogle Scholar
  42. 42.
    Wegst UGK, Ashby MF (2004) The mechanical efficiency of natural materials. Philos Mag 84(21):2167–2186CrossRefGoogle Scholar
  43. 43.
    Espinosa HD et al (2009) Merger of structure and material in nacre and bone – perspectives on de novo biomimetic materials. Prog Mater Sci 54(8):1059–1100CrossRefGoogle Scholar
  44. 44.
    Lin AY-M, Meyers MA (2009) Interfacial shear strength in abalone nacre. J Mech Behav Biomed Mater 2(6):607–612PubMedCrossRefGoogle Scholar
  45. 45.
    Lopez MI, Meza Martinez PE, Meyers MA (2014) Organic interlamellar layers, mesolayers and mineral nanobridges: contribution to strength in abalone (haliotis rufescence) nacre. Acta Biomater 10(5):2056–2064PubMedCrossRefGoogle Scholar
  46. 46.
    Song F, Soh AK, Bai YL (2003) Structural and mechanical properties of the organic matrix layers of nacre. Biomaterials 24(20):3623–3631PubMedCrossRefGoogle Scholar
  47. 47.
    Huang Z, Li X (2013) Origin of flaw-tolerance in nacre. Sci Rep 3:1693PubMedPubMedCentralGoogle Scholar
  48. 48.
    Yao N et al (2009) Organic–inorganic interfaces and spiral growth in nacre. J R Soc Interface 6(33):367–376PubMedCrossRefGoogle Scholar
  49. 49.
    Iqbal P, Preece JA, Mendes PM (2012) Nanotechnology: the “Top-Down” and “Bottom-Up” approaches, in supramolecular chemistry. Wiley, ChichesterGoogle Scholar
  50. 50.
    Meyers MA et al (2008) Mechanical strength of abalone nacre: role of the soft organic layer. J Mech Behav Biomed Mater 1(1):76–85PubMedCrossRefGoogle Scholar
  51. 51.
    Marin F, Luquet G (2004) Molluscan shell proteins. C R Palevol 3(6–7):469–492CrossRefGoogle Scholar
  52. 52.
    Cheng Y et al (2014) On the strength of β-sheet crystallites of Bombyx mori silk fibroin. J R Soc Interface 11(96):20140305PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Lefèvre T, Rousseau M-E, Pézolet M (2007) Protein secondary structure and orientation in silk as revealed by Raman spectromicroscopy. Biophys J 92(8):2885–2895PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Blank S et al (2003) The nacre protein perlucin nucleates growth of calcium carbonate crystals. J Microsc 212(Pt 3):280–291PubMedCrossRefGoogle Scholar
  55. 55.
    Montagnani C et al (2011) Pmarg-Pearlin is a matrix protein involved in nacre framework formation in the pearl oyster pinctada margaritifera. ChemBioChem 12(13):2033–2043PubMedCrossRefGoogle Scholar
  56. 56.
    Amos FF et al (2011) A C-RING-like domain participates in protein self-assembly and mineral nucleation. Biochemistry 50(41):8880–8887PubMedCrossRefGoogle Scholar
  57. 57.
    Dodenhof T et al (2014) Splice variants of perlucin from haliotis laevigata modulate the crystallization of CaCO3. PLoS ONE 9(5):e97126PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Weiss IM et al (2000) Purification and characterization of perlucin and perlustrin, two new proteins from the shell of the mollusc haliotis laevigata. Biochem Biophys Res Commun 267(1):17–21PubMedCrossRefGoogle Scholar
  59. 59.
    Evans JS (2012) Aragonite-associated biomineralization proteins are disordered and contain interactive motifs. Bioinformatics 28(24):3182–3185PubMedCrossRefGoogle Scholar
  60. 60.
    Wustman BA et al (2003) Structure-function studies of the lustrin a polyelectrolyte domains, RKSY and D4. Connect Tissue Res 44(1):10–15PubMedCrossRefGoogle Scholar
  61. 61.
    Li C, Kaplan DL (2003) Biomimetic composites via molecular scale self-assembly and biomineralization. Curr Opinion Solid State Mater Sci 7(4–5):265–271CrossRefGoogle Scholar
  62. 62.
    Raabe D, Sachs C, Romano P (2005) The crustacean exoskeleton as an example of a structurally and mechanically graded biological nanocomposite material. Acta Mater 53(15):4281–4292CrossRefGoogle Scholar
  63. 63.
    Luquet G, Marin F (2004) Biomineralisations in crustaceans: storage strategies. C R Palevol 3(6–7):515–534CrossRefGoogle Scholar
  64. 64.
    Wheatly MG, Zanotto FP, Hubbard MG (2002) Calcium homeostasis in crustaceans: subcellular Ca dynamics. Comp Biochem Physiol B: Biochem Mol Biol 132(1):163–178CrossRefGoogle Scholar
  65. 65.
    Al-Sawalmih A et al (2008) Microtexture and chitin/calcite orientation relationship in the mineralized exoskeleton of the American lobster. Adv Funct Mater 18(20):3307–3314CrossRefGoogle Scholar
  66. 66.
    Raabe D et al (2005) Discovery of a honeycomb structure in the twisted plywood patterns of fibrous biological nanocomposite tissue. J Cryst Growth 283(1–2):1–7CrossRefGoogle Scholar
  67. 67.
    Kunkel JG, Nagel W, Jercinovic MJ (2012) Mineral fine structure of the American lobster cuticle. J Shellfish Res 31(2):515–526CrossRefGoogle Scholar
  68. 68.
    Cheng L, Wang L, Karlsson AM (2008) Image analyses of two crustacean exoskeletons and implications of the exoskeletal microstructure on the mechanical behavior. J Mater Res 23(11):2854–2872CrossRefGoogle Scholar
  69. 69.
    Hild S, Marti O, Ziegler A (2008) Spatial distribution of calcite and amorphous calcium carbonate in the cuticle of the terrestrial crustaceans Porcellio scaber and Armadillidium vulgare. J Struct Biol 163(1):100–108PubMedCrossRefGoogle Scholar
  70. 70.
    Raabe D et al (2006) Microstructure and crystallographic texture of the chitin–protein network in the biological composite material of the exoskeleton of the lobster Homarus americanus. Mater Sci Eng A 421(1–2):143–153CrossRefGoogle Scholar
  71. 71.
    Weaver JC et al (2012) The stomatopod dactyl club: a formidable damage-tolerant biological hammer. Science 336(6086):1275–1280PubMedCrossRefGoogle Scholar
  72. 72.
    Grunenfelder LK et al (2014) Bio-inspired impact-resistant composites. Acta Biomater 10(9):3997–4008PubMedCrossRefGoogle Scholar
  73. 73.
    Grunenfelder LK, Herrera S, Kisailus D (2014) Crustacean-derived biomimetic components and nanostructured composites. Small 10(16):3207–3232PubMedCrossRefGoogle Scholar
  74. 74.
    Hillerton JE (1984) Cuticle: mechanical properties. In: Bereiter-Hahn J, Matoltsy AG, Richards KS (eds) Biology of the integument. Springer, Berlin/Heidelberg, pp 626–637CrossRefGoogle Scholar
  75. 75.
    Andersen SO (1999) Exoskeletal proteins from the crab, cancer pagurus. Comp Biochem Physiol A Mol Integr Physiol 123(2):203–211PubMedCrossRefGoogle Scholar
  76. 76.
    Andersen SO (1998) Characterization of proteins from arthrodial membranes of the lobster, Homarus americanus. Comp Biochem Physiol A Mol Integr Physiol 121(4):375–383PubMedCrossRefGoogle Scholar
  77. 77.
    Shechter A et al (2008) A gastrolith protein serving a dual role in the formation of an amorphous mineral containing extracellular matrix. Proc Natl Acad Sci 105(20):7129–7134PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Shafer TH, McCartney MA, Faircloth LM (2006) Identifying exoskeleton proteins in the blue crab from an expressed sequence tag (EST) library. Integr Comp Biol 46(6):978–990PubMedCrossRefGoogle Scholar
  79. 79.
    Rebers JE, Willis JH (2001) A conserved domain in arthropod cuticular proteins binds chitin. Insect Biochem Mol Biol 31(11):1083–1093PubMedCrossRefGoogle Scholar
  80. 80.
    Inoue H et al (2004) A novel calcium-binding peptide from the cuticle of the crayfish, Procambarus clarkii. Biochem Biophys Res Commun 318(3):649–654PubMedCrossRefGoogle Scholar
  81. 81.
    Inoue H, Ohira T, Nagasawa H (2007) Significance of the N- and C-terminal regions of CAP-1, a cuticle calcification-associated peptide from the exoskeleton of the crayfish, for calcification. Peptides 28(3):566–573PubMedCrossRefGoogle Scholar
  82. 82.
    Wynn A, Shafer TH (2005) Four differentially expressed cDNAs in Callinectes sapidus containing the Rebers–Riddiford consensus sequence. Comp Biochem Physiol B: Biochem Mol Biol 141(3):294–306CrossRefGoogle Scholar
  83. 83.
    Mayer G (2005) Rigid biological systems as models for synthetic composites. Science 310(5751):1144–1147PubMedCrossRefGoogle Scholar
  84. 84.
    Munch E et al (2008) Tough, bio-inspired hybrid materials. Science 322(5907):1516–1520PubMedCrossRefGoogle Scholar
  85. 85.
    Sommerdijk NAJM, With G (2008) Biomimetic CaCO3 mineralization using designer molecules and interfaces. Chem Rev 108(11):4499–4550PubMedCrossRefGoogle Scholar
  86. 86.
    Sudo S et al (1997) Structures of mollusc shell framework proteins. Nature 387(6633):563–564PubMedCrossRefGoogle Scholar
  87. 87.
    Znidarsic WJ, Chen IW, Shastri VP (2012) Influence of surface charge and protein intermediary layer on the formation of biomimetic calcium phosphate on silica nanoparticles. J Mater Chem 22(37):19562–19569CrossRefGoogle Scholar
  88. 88.
    Wang T, Porter D, Shao Z (2012) The intrinsic ability of silk fibroin to direct the formation of diverse aragonite aggregates. Adv Funct Mater 22(2):435–441CrossRefGoogle Scholar
  89. 89.
    Munro NH, Green DW, McGrath KM (2013) In situ continuous growth formation of synthetic biominerals. Chem Commun 49(33):3407–3409CrossRefGoogle Scholar
  90. 90.
    Ma Y, Feng Q, Bourrat X (2013) A novel growth process of calcium carbonate crystals in silk fibroin hydrogel system. Mater Sci Eng C 33(4):2413–2420CrossRefGoogle Scholar
  91. 91.
    Falini G et al (1996) Control of aragonite or calcite polymorphism by mollusk shell macromolecules. Science 271(5245):67–69CrossRefGoogle Scholar
  92. 92.
    Huang X et al (2014) Biomineralization regulation by nano-sized features in silk fibroin proteins: synthesis of water-dispersible nano-hydroxyapatite. J Biomed Mater Res B Appl Biomater 102(8):1720–1729PubMedCrossRefGoogle Scholar
  93. 93.
    Seto J et al (2014) Nacre protein sequence compartmentalizes mineral polymorphs in solution. Cryst Growth Des 14(4):1501–1505CrossRefGoogle Scholar
  94. 94.
    Inoue H et al (2003) Cloning and expression of a cDNA encoding a matrix peptide associated with calcification in the exoskeleton of the crayfish. Comp Biochem Physiol B: Biochem Mol Biol 136(4):755–765CrossRefGoogle Scholar
  95. 95.
    Sugawara A et al (2006) Self-organization of oriented calcium carbonate/polymer composites: effects of a matrix peptide isolated from the exoskeleton of a crayfish. Angew Chem Int Ed 45(18):2876–2879CrossRefGoogle Scholar
  96. 96.
    Weber E et al (2014) Incorporation of a recombinant biomineralization fusion protein into the crystalline lattice of calcite. Chem Mater 26(17):4925–4932CrossRefGoogle Scholar
  97. 97.
    Haghpanah JS et al (2009) Artificial protein block copolymers blocks comprising two distinct self-assembling domains. Chembiochem 10(17):2733–2735PubMedCrossRefGoogle Scholar
  98. 98.
    Haghpanah JS et al (2013) Bionanocomposites: differential effects of cellulose nanocrystals on protein diblock copolymers. Biomacromolecules 14(12):4360–4367PubMedCrossRefGoogle Scholar
  99. 99.
    Laaksonen P et al (2011) Genetic engineering of biomimetic nanocomposites: diblock proteins, graphene, and nanofibrillated cellulose. Angew Chem Int Ed 50(37):8688–8691CrossRefGoogle Scholar
  100. 100.
    Laaksonen P, Szilvay GR, Linder MB (2012) Genetic engineering in biomimetic composites. Trends Biotechnol 30(4):191–197PubMedCrossRefGoogle Scholar
  101. 101.
    Partlow BP et al (2014) Highly tunable elastomeric silk biomaterials. Adv Funct Mater 24:4615–4624PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Bonderer LJ, Studart AR, Gauckler LJ (2008) Bioinspired design and assembly of platelet reinforced polymer films. Science 319(5866):1069–1073PubMedCrossRefGoogle Scholar
  103. 103.
    Lu Y, Weng L, Zhang L (2004) Morphology and properties of soy protein isolate thermoplastics reinforced with chitin whiskers. Biomacromolecules 5(3):1046–1051PubMedCrossRefGoogle Scholar
  104. 104.
    Hu X et al (2012) Protein-based composite materials. Mater Today 15(5):208–215CrossRefGoogle Scholar
  105. 105.
    Lapidot S et al (2012) Clues for biomimetics from natural composite materials. Nanomedicine 7(9):1409–1423PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Dai M et al (2011) Artificial protein block polymer libraries bearing two SADs: effects of elastin domain repeats. Biomacromolecules 12(12):4240–4246PubMedCrossRefGoogle Scholar
  107. 107.
    Haghpanah JS et al (2010) Supramolecular assembly and small molecule recognition by genetically engineered protein block polymers composed of two SADs. Mol Biosyst 6(9):1662–1667PubMedCrossRefGoogle Scholar
  108. 108.
    Varjonen S et al (2011) Self-assembly of cellulose nanofibrils by genetically engineered fusion proteins. Soft Matter 7(6):2402–2411CrossRefGoogle Scholar
  109. 109.
    Nikolov S et al (2010) Revealing the design principles of high-performance biological composites using Ab initio and multiscale simulations: the example of lobster cuticle. Adv Mater 22(4):519–526PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Chemical and Biomolecular EngineeringNew York University Tandon School of EngineeringBrooklynUSA
  2. 2.Department of ChemistryNew York UniversityNew YorkUSA

Personalised recommendations