eNacre: AnAncientNanostructuredBiomaterial · films coating them, suggest that the formation of...

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Acta Futura 6 (2013) 37-42 DOI: 10.2420/AF06.2013.37 Acta Futura e Nacre: An Ancient Nanostructured Biomaterial C. M. P * Departamento de Cristalografía y Mineralogía, Universidad Complutense de Madrid, E-28040 Madrid, Spain Instituto de Geociencias IGEO (UCM-CSIC). C/ José Antonio Novais, 2. E-28040 Madrid, Spain A. G. C Departamento de Estratigrafía y Paleontología, Universidad de Granada, E-18071 Granada, Spain C. I. S-D J. H. E. C Instituto Andaluz de Ciencias de la Tierra, CSIC-Universidad de Granada, E-18071 Granada, Spain Abstract. Nacre is a much appreciated natural material which forms in the interior of numerous mollusc shells. Its remarkable optical and mechan- ical properties are due to a highly nanostructured combination of inorganic and organic components, which has not been reproduced by any industrial process to date. In this paper we briefly review the current knowledge on the composition, struc- ture, properties and mechanisms of formation of this iconic biomaterial. 1 Introduction Nacre, most commonly known as mother-of-pearl, is a material exclusively secreted by molluscs which ap- peared on the Earth during the Paleozoic Era. First clear evidence of fossil nacre has been found in rocks formed in the late Ordovician, i.e. about 450 million years ago [6]. However, nacre might have an even earlier origin, since well-preserved fossils from the late Cam- brian to the middle Ordovician are rare [18, 17]. e outstanding mechanical resistance of nacre suggests that this biomaterial evolved as a response to the increas- ing abilities and diversity of predators after the so-called * Corresponding author. E-mail: [email protected] Cambrian explosion, a unique event of animal diversifi- cation in the history of life. e development of claws, jaws and other novel tools of predation led to an arms race between predators and preys, which produced de- fensive adaptations such as toxicity, new escape methods (burrowing), camouflage, counter-offense, and armour. As a result of this ancient arms race, molluscs devel- oped new crush-resistant shell microstructures, among which nacre is one of the most sophisticated and effi- cient. Recent paleontological studies indicate that mol- luscs “invented” nacre several times, i.e. nacre conver- gently evolved in at least four different classes of mol- luscs [18]. e significant differences in the microstruc- ture and growth process of nacre between molluscan classes and the variation in both the genes and proteins associated with nacre in modern molluscs provide addi- tional evidence that supports the independent origin of nacre within the Mollusca. Numerous modern molluscs still produce different kinds of nacre. is natural product is a biocompos- ite, whose highly hierarchical structure and combina- tion of inorganic and organic components, results in a material with unusual mechanical and optical proper- ties [15, 13]. Until the industrial production of plastics, nacre was widely used in button-making, as construc- tion material, and for decoration purposes (e.g. special 37

Transcript of eNacre: AnAncientNanostructuredBiomaterial · films coating them, suggest that the formation of...

Page 1: eNacre: AnAncientNanostructuredBiomaterial · films coating them, suggest that the formation of the ... tension elastically up to brittle failure, in a similar way asanaragonitesinglecrystaldoes.

Acta Futura 6 (2013) 37-42DOI: 10.2420/AF06.2013.37

ActaFutura

e Nacre: An Ancient Nanostructured BiomaterialC. M. P*

Departamento de Cristalografía y Mineralogía, Universidad Complutense de Madrid, E-28040 Madrid, SpainInstituto de Geociencias IGEO (UCM-CSIC). C/ José Antonio Novais, 2. E-28040 Madrid, Spain

A. G. CDepartamento de Estratigrafía y Paleontología, Universidad de Granada, E-18071 Granada, Spain

C. I. S-D J. H. E. CInstituto Andaluz de Ciencias de la Tierra, CSIC-Universidad de Granada, E-18071 Granada, Spain

Abstract. Nacre is a much appreciated naturalmaterial which forms in the interior of numerousmollusc shells. Its remarkable optical and mechan-ical properties are due to a highly nanostructuredcombination of inorganic and organic components,which has not been reproduced by any industrialprocess to date. In this paper we briefly reviewthe current knowledge on the composition, struc-ture, properties and mechanisms of formation ofthis iconic biomaterial.

1 Introduction

Nacre, most commonly known as mother-of-pearl, isa material exclusively secreted by molluscs which ap-peared on the Earth during the Paleozoic Era. Firstclear evidence of fossil nacre has been found in rocksformed in the late Ordovician, i.e. about 450 millionyears ago [6]. However, nacremight have an even earlierorigin, since well-preserved fossils from the late Cam-brian to the middle Ordovician are rare [18, 17]. eoutstanding mechanical resistance of nacre suggests thatthis biomaterial evolved as a response to the increas-ing abilities and diversity of predators after the so-called

*Corresponding author. E-mail: [email protected]

Cambrian explosion, a unique event of animal diversifi-cation in the history of life. e development of claws,jaws and other novel tools of predation led to an armsrace between predators and preys, which produced de-fensive adaptations such as toxicity, new escape methods(burrowing), camouflage, counter-offense, and armour.As a result of this ancient arms race, molluscs devel-oped new crush-resistant shell microstructures, amongwhich nacre is one of the most sophisticated and effi-cient. Recent paleontological studies indicate that mol-luscs “invented” nacre several times, i.e. nacre conver-gently evolved in at least four different classes of mol-luscs [18]. e significant differences in the microstruc-ture and growth process of nacre between molluscanclasses and the variation in both the genes and proteinsassociated with nacre in modern molluscs provide addi-tional evidence that supports the independent origin ofnacre within the Mollusca.

Numerous modern molluscs still produce differentkinds of nacre. is natural product is a biocompos-ite, whose highly hierarchical structure and combina-tion of inorganic and organic components, results in amaterial with unusual mechanical and optical proper-ties [15, 13]. Until the industrial production of plastics,nacre was widely used in button-making, as construc-tion material, and for decoration purposes (e.g. special

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F . AFM images taken in tapping mode while displaying the amplitude signal. (a) Aragonitic tablets that form the nacre ofthe mollusc Pteria hirundo. Note that the coalescence of tablets at the upper right results in a homogeneous mineralised layer. (Size ofthe image: 14.8×14.8 µm2). (b) Detail of the surface of an aragonitic tablet (red square marked in (a)) showing the agglomerate ofnanounits that form it. (Size of the image: 773×773 nm2).

tiles and glossy coatings of walls, doors and ceilings).When nacre is deposited in concentric layers around aforeign body in the interior of a mollusc, a pearl is pro-duced. Pearls are appreciated objects in jewellery, whosecommercial value depends on their size, perfection androundness.

In the last few decades, nacre has attracted much at-tention in material science. Scientists and engineershave realized that nacre is a model material for a newgeneration of composite ceramics [1]. However, the de-velopment of nacre-bioinspired ceramics requires a pro-found knowledge of the relationships between compo-sition, structure and properties of this ancient naturalmaterial.

2 e composition and structure of nacre

Nacre is composed of ≈ 95% of aragonite (orthorhom-bic CaCO3) and ≈ 5% of a mixture of proteins andthe polysaccharide chitin [10, 3]. In nacre, aragoniteis in the form of polygonal tablets with a size rangingfrom 5 to 15 µm and a thickness of about 0.5 µm. Al-though the shape of the polygonal tablets varies fromone species to another, in all the cases their surfaces arerough and formed by numerous mineral subunits of afew nanometres in diameter each (Fig. 1). In molluscshells, aragonite tablets are arranged forming brickwall-

like microstructures in which the organic matter (i.e.proteins and chitin) is the “mortar”. e arrangement ofaragonite tablets varies with the mollusc species and twomain patterns can be recognised. While nacre secretedby gastropods is made of columns of tablets, in bivalves,layers of tablets are offset in successive step-like layers(Fig. 2).

3 Formation of nacre

e mechanism of nacre formation is not completelyunderstood yet. Nacre is an extracellular material whichforms between the external layer of the shell and the softliving body of the organism, i.e., between a thick layerof calcite or aragonite crystals with a prismatic habit andthe so-called mantle. ere, one can find the extrapallialcavity, a micro-sized liquid-filled space where the self-assembly of aragonite tablets and organic matter occurs(Fig. 3). Recent authors have proposed a multi-step hi-erarchic mechanism of nacre formation [3, 4, 5]. Such acomplex mechanism begins with the secretion of chitinmolecules from the cells of the organism into the ex-trapallial cavity. ese molecules polymerise formingrods of several microns in length which self-organiseinto a liquid crystal structure. Subsequently the chitinliquid crystal layer is coated by proteins resulting in theformation of an interlamellar membrane. is mem-

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e Nacre: An Ancient Nanostructured Biomaterial

F. Examples of the two nacre microstructures found inmolluscs. (a) Columnar arrangement of aragonite tablets in the gasteropodGlibula umbilicalis (transmission electron microscopy image). (b) Sheet arrangement of aragonite tablets in the bivalve Neotrigoniamargaritacea after the coalescence of tablets (amplitude atomic force microscopy image).

brane is immersed in the extrapallial fluid which is su-persaturated with respect to calcium carbonate. enthe growth of aragonite tablets occurs and the spacebetween interlamellar membranes is progressively min-eralised. However, the process leading to the growthand coalescence of aragonite tablets is not well known.Although numerous X-ray diffraction and transmissionelectron microscopy studies have confirmed the arago-nitic nature of the tablets, the formation of amorphouscalcium carbonate as a precursor phase of aragonite isstill under investigation [19]. e high roughness of thearagonite tablets together with the observation of thinfilms coating them, suggest that the formation of thetablets takes place by accretion of aragonite nanounitscovered by organic membranes. However, thin filmsmight also appear as the result of the “exsolution” oforganic molecules during the conversion of amorphouscalcium carbonate into aragonite. e fact that the arag-onite of nacre frequently incorporates fibrous proteinsthat previously were found in the interlamelar liquidseems to support both mechanism of tablet formation.

4 e properties of nacre

4.1 Mechanical properties

Nacre shows outstanding mechanical properties, whichare superior to those of most common construction ma-

terials. As can be seen in Fig. 4, both types of nacre,columnar and sheet nacre, are much more resistant totensile and compression stress than bricks, cement andconcrete. In addition, nacre is significantly stiffer thanthese materials (i.e. it has a higher Young’s modu-lus). Interestingly, nacre has a higher mechanical resis-tance than pure aragonite. It has been found that whilethe fracture toughness of nacre ranges from 3.3 to 9.0MPam1/2, the fracture toughness of inorganic aragonitecrystals is approximately 1 MPam1/2 [9, 14, 20, 8, 16].e high toughness of nacre is comparable to advancedengineering materials and ceramic metal composites(cermets). is is remarkable considering that the 95%of nacre is made of the brittle mineral aragonite [1].

e mechanical properties of nacre also change withthe degree of hydration. us, dry nacre behaves undertension elastically up to brittle failure, in a similar wayas an aragonite single crystal does. In contrast, hydratednacre, has an almost ductile response to tension. Such aresponse of nacre begins at tensile stresses of about 60-

F . Schematic drawing of the structure of a mollusc shell.

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F . Comparison between main mechanical properties ofnacre and construction materials. Data for nacre are averagedfrom those in [7]. Data for construction materials are typical val-ues found in the literature and internet sources.

70 MPa, the deformation of the material at the brittlefailure being of almost 1% [1]. is strain at the failureis low compared to many engineering materials but it isten times higher than the strain at failure of aragonite.e ductile behaviour of wet nacre can be explained interms of a collective sliding of aragonite tables at themicroscale [16].

4.2 Optical properties

Undoubtedly, the most remarkable optical property ofnacre is its iridescent shine. is shine is due to thefact that the thickness of the aragonite tablets is withinthe range of wavelengths of visible light (i.e. from 400nm to 700 nm, approximately). As a consequence, lightrays interfere constructively and destructively within thearagonite platelets depending on their incident angle.is angle-dependent interference generates differentpale colours whose intensity varies with the position ofthe observer. e resulting effect is called structural col-oration, since it is not related to any pigment but to ananostructured reflective and refractive surface.

When nacre is arranged more or less concentrically,as is the case with pearls, propagation of light becomesmore complex and diffraction, birefringence and scat-tering phenomena modify the iridescent shine [13].ese phenomena, combined with the presence of or-ganic and inorganic impurities, play a major role in de-termining the variety and quality of the natural and cul-tivated pearls used in jewellery.

5 Synthetic analogues of nacre

e production of materials with similar properties tothose of nacre is not an easy task. Even though complexfabrication methods have been used to obtain compos-ites with the stiffness and toughness of nacre, none ofthem entirely reproduce all the mechanical properties ofthe natural material [1]. In all the cases, these syntheticcomposites are made of hard particles glued togetherwith a much softer and ductile component. e key toachieving all the characteristic mechanical properties ofnacre is the control of: (i) the size, thickness and orien-tation of the hard particles, (ii) the interfacial propertiesbetween hard and ductile components, and (iii) the for-mation of a self-assembled hierarchical microstructure.To this end, various fabrication techniques, which in-clude layer-by-layer deposition, colloidal assembly andsintering, have been explored.

By using a layer-by-layer assembly technique, a“nacre-like” nanocomposite has been recently preparedfrom vinyl alcohol and Na+− montmorillonite claynanosheets [12]. e obtained material shows a lam-inar microstructure which is strong and flexible. Inter-estingly, the surfaces of this laminated nanocompositeare highly transparent, resembling those of nacre.

Colloidal assembly also resulted in an interesting wayof fabricating materials inspired by nacre. Based onthis technique, an alumina/chitosan polymer was syn-thesised to have a low ceramic content but with a struc-ture and mechanical properties similar to nacre [2]. Inthis case, the aspect ratio of the alumina embedded inthe chitosan matrix was essential to ensure an adequatetablet sliding when fracture occurs.

To date, the synthetic material closest to naturalnacre is a composite made of alumina and polymethylmethacrylate (PMMA) [11]. To produce such a ma-terial a complex protocol is required. Firstly, micro-scopic particles with a specific size have to be producedfrom alumina powder and using ice platelets as a tem-plate. Only then a sintering process and the infiltra-tion of PMMA are conducted. e result is a highlydeformable composite with a remarkable toughness butstill not as fracture resistant as that of nacre.

6 Conclusion

Although nacre has been intensively investigated dur-ing the last few decades, the origin of its valuable fea-tures, as well as the mechanisms of its formation, stillremain incompletely understood. Further investigations

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are needed to elucidate the complex relationships be-tween microstructure, composition and mechanical andoptical properties of nacre. In addition, the sequenceof processes which lead to a hierarchical self-assemblyof organic and inorganic components still requires morematerial characterisations, experimental work and mod-elling. e acquisition of this knowledge is fundamentalfor mimicking all the properties of nacre. Only then, themicrostructures and construction principles of nacre willbe successfully transferred from nature to technology.

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