Biomimetic synthesis of oriented aragonite crystals and nacre-like composite material by controlling the fluid type

Powder Technology 302 (2016) 455–461

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Biomimetic synthesis of oriented aragonite crystals and nacre-like composite material by controlling the fluid type Jianxin Chen a,b,⁎, Yinqiang Huang a, Min Su a,⁎⁎, Kun Cheng b, Yingying Zhao a a b

School of Marine Science and Engineering, Hebei University of Technology, Tianjin 300130, China School of Chemical Engineering, Hebei University of Technology, Tianjin 300130, China

a r t i c l e

i n f o

Article history: Received 12 February 2015 Received in revised form 12 May 2016 Accepted 27 May 2016 Available online 29 May 2016 Keywords: Biomineralization Nacre Aragonite Layer-by-layer Composite material

a b s t r a c t Shape-controlled biomineralization and self-assembly of highly ordered aragonite architectures were achieved under laminar flow on a fresh natural nacre substrate at 35 °C. In this paper, a film of tightly packed needles of c-axis oriented aragonite was obtained under the circumstance of laminar-flow. The mass transfer rate and growth time of crystals play important roles in the formation of aragonite crystals with different forms and sizes. In order to fabricate an artificial nacreous structure, polyacrylic acid (PAA) was used as an organic film in coating the aragonite layer. Then, the aragonite layer and PAA film were alternately assembled. The structures and morphologies of the products were characterized by X-ray diffractometry, scanning electron microscopy and FTIR spectroscopy. The results indicate that the layer-by-layer aragonite structure has potential applications in biomimetic synthesis materials. © 2016 Elsevier B.V. All rights reserved.

1. Introduction Biominerals in natural organisms exhibit delicate architectures and excellent mechanical properties due to the complex hierarchical structure regulated by the combination of bioorganic and inorganic matter [1–3]. As one of the most striking biomaterials, the nacre has drawn great attention for the fabrication of biomimetic nanocomposite because of their superior hierarchical organization and high toughness [4]. It also provides an inspiration in material science and nanotechnology [5]. Nacre consists of a brick-and-mortar like structure, in which hard aragonite tablets are glued together with soft bioorganic materials to form tiles [6]. The bioorganic matrix is usually composed of an assembly of β-chitin frameworks, silk-fibroin-like proteins and acidic macromolecules [7,8]. Moreover, many specific proteins can be binded to organized β-chitin and then form layered sheets to inhibit further growth of nacre [9]. Through nanopores in the bioorganic matrix layered sheets, the continued orientation of aragonite crystal layer can be obtained by building a mineral bridge [1,10,11]. Soluble acidic proteins play an important role in directing the growth and self-assembly of hierarchical superstructures [12]. Recently, organic matrix components extracted from natural biomaterials were used

⁎ Correspondence to: J. Chen School of Marine Science and Engineering, Hebei University of Technology, Tianjin 300130, China. ⁎⁎ Corresponding author. E-mail addresses: [email protected] (J. Chen), [email protected] (M. Su).

http://dx.doi.org/10.1016/j.powtec.2016.05.060 0032-5910/© 2016 Elsevier B.V. All rights reserved.

to analyze the biomineralization mechanism and regulate the crystallization of calcium carbonate [13–15]. Moreover, some proteins also play a pivotal role in the formation of biominerals in vivo [16]. For example, two hybrid CaCO3-protein materials that have highly ordered superstructures can be obtained from a process utilizing trypsin and bovine hemoglobin directed assembly of calcium carbonate nanoparticles using gas-diffused method [17]. There are reports about the fabrication of biomineralslike CaCO3 structure via Langmuir monolayer [18,19], catalytic method [20], self-assembled method [21], double-hydrophilic block copolymers [22] and polymers [23,24]. These results indicate that organic matrix plays an important role in spatial and chemical control of the crystal nucleation and growth. Additionally, poly aspartic acid [25] and polyacrylic acid [26,27] can induce formation of thin calcium carbonate film on substrates such as cellulose, chitosan, and porphyrin. Gong reported that three-dimensional chitosan self-assembled nanostructures as templates, controlling the growing process of calcium carbonate [28]. Inorganic substrates have also been used as templates to induce formation and assembly of calcium carbonate [29,30]. A process was recently reported for fabrication of a nacre-like aragonite/PAA multilayer film with nacre substrate in CaCl2 solution in a closed system containing NH4HCO3 [9]. In their study, a, b axes of nanostacks are oriented perfectly. To get c-axis oriented aragonite, we speculated that homogeneous-film fabrication aragonite can be obtained by mixing CaCl2 with Na2CO3 in an aqueous solution. However, c-axis oriented aragonite was not directly fabricated because the crystal growth direction was influenced by flow pattern of the solution. Laminar fluid with directional flow was designed to promote the

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formation of c-axis oriented aragonite, and the alternate drop-coating of PAA on the aragonite film resulted in layered composite structure. This process provides a new method to prepare nacre-like composite material by controlling the flow pattern of the fluid. 2. Experimental 2.1. Materials Calcium chloride dihydrate (CaCl2·2H2O, purity N 99%), anhydrous sodium carbonate (Na2CO3, purity N99%) and magnesium chloride hexahydrate (MgCl2·6H2O, purity N98%) were purchased from Tianjin recovery technology development company and used without further purification. NaOH and HCl used in this work were of analytical grade. Polyacrylic acid (PAA) with Mw of ca. 2.0 × 103 Da was purchased from Acros Chemical Company. Nacre was obtained from Beihai, Guangxi province of China. Distilled water was used in all experiments. 2.2. Methods In a typical procedure, MgCl2 was dissolved into 5 mM CaCl2 aqueous solution with the Mg2 +/Ca2 + molar ratio of 4:1. Then the pH of the solution was adjusted to 8 by using NaOH or HCl solution. A vertical section plate of nacre (5 × 5 mm2) was prepared and fixed on the microscope slides as a substrate. The microscope slides were put into the reaction tube. Standard laboratory apparatus was established to allow a rapid mixing of the constituting solutions (CaCl2 and Na2CO3). Fig. 1 shows the principal setup of the crystallization apparatus. The two solutions were heated to 35 °C with circulating water in crystallizer, before entering the reaction tube, two solutions were rapidly mixed in specific flow rate using peristaltic pumps. The volume flow rates of both solutions (calcium-containing and carbonate-containing) were controlled to be identical. The reacting solution passed through the reaction tube for CaCO3 precipitation which was kept in 35 °C water bath. Then the superfluous mixing solution was removed by another peristaltic pump. In this process, the flow rate of the feed solution and output solution was 1.354 × 10− 3 m/s. The microscope slides were taken out at the end of the reaction (after 23 min), rinsed with deionized water and dried in vacuum. A layer of 0.1 mM PAA in ethanol was coated by dropping on the aragonite (CaCO3) layer and then dried. The microscope slides were put back into the reaction tube for crystal precipitation again. The above crystal precipitation and PAA coating process was repeated for several times to fabricate multilayered artificial nacre material.

2.3. Characterization The morphologies of CaCO3 depositions were characterized using a Nova NanoSEM 430 scanning electron microscope (SEM) equipped with an energy-dispersive spectroscope (EDS). SEM was also used to observe the overgrowth of calcium carbonate crystals on the fresh surface of nacre after different treatment. X-ray powder diffraction (XRD) patterns were recorded using a Bruker D8 Advanced XRD diffractometer with Cu Ka in the 2θ range of 20–70°. Solid–liquid interfacial tension measurement was conducted with DSA30 research contact angle measuring instrument. The main components of shell nacreous layer were analyzed using a Bruker (TENSOR 27, Germany) FTIR spectrometer. 3. Results and discussion Fig. 2a shows the morphological characteristic of calcium carbonate induced by fresh nacre treated with 0.1 M HCl. Generally, HCl solution can conduct a strong decomposition on the calcium carbonate. After the nacre surface was treated by HCl solution, the nacre surface was covered with the residue of chemical decomposition and a few pyramid-shaped calcium carbonate crystals grew on some steps of the nacre surface, which might be due to some remnants of proteins at those steps. Fig. 2b shows that alkaline treatment of the substrate was covered with a nonuniform deposition of calcium carbonate. As is known, NaOH solution was one of the important solutions for protein and lipid removal, then it was used for surface modification in this work. Fig. 2c shows the morphology of calcium carbonate supported on untreated substrate and tightly packed needles of calcium carbonate crystals grew on the surface. These needles were perfectly perpendicular to the nacre surface and grew in the c-axis oriented direction. This behavior could be indicated that organic layer in nacre was important for fabrication of homogeneous aragonite film. The XRD pattern of nacre powder and standard data of aragonite (JCPDS 41-1475) are presented in Fig. 3a and b respectively. From Fig. 3b it is evident that the dominate phase is aragonite in nacre powder. The peak at (104) plane is for calcite. The molar percentage composition of aragonite and calcite were calculated using Kontoyannis equation [31], Eqs. (1) and (2), and was found to be 95.11 mol.% and 4.89 mol.% respectively. The Kontoyannis equation is expressed as below:

XA ¼

3:157  IA 221 IC

104

þ 3:157  IA 221

Fig. 1. Schematic diagram of the proposed continuous flow in vitro crystallization process setup.

ð1Þ

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457

Fig. 2. SEM images of crystals grown on fresh nacre surface treated with different method. (a) 0.1 M HCl, (b) 0.1 M NaOH, (c) distilled water.

X C ¼ 1−X A

ð2Þ

where XA, XC are the molar percentage composition of aragonite and and I104 are peak heights of characteristic calcite, respectively; I221 A C adsorptions for aragonite (2θ = 45.8) and calcite (2θ = 29.4). Fig. 4 is the FTIR spectra of shell nacreous layer and CaCO3 deposition on a nacre surface. Two peaks at around 708 and 862 cm−1 are presented in Fig. 4a, indicating that the crystalline phase is aragonite in shell nacreous layer. In Fig. 4b, the appearance of the 700, 713 and 856 cm−1 peaks in the FTIR spectra suggests that aragonite is precipitated on the nacre surface. In Fig. 4, the peak intensities of CaCO3 deposition on a nacre surface substrate are similar to the natural shell nacre, the EDS spectra is used to identify the deposition on the substrate surface. Fig. 5 shows SEM micrographs, EDS spectra of nacre substrate and an aragonite film deposited on a fresh nacre substrate at the flow rate of 1.354 × 10−3 m/s. It can be clearly observed that needles of aragonite covering the nacre substrate entirely. The morphology of the film is similar to the Fig. 2c. The EDS spectrum of nacre substrate showed the presence of C (Kα), O (Kα) and Ca (Kα, Kβ), while the deposited aragonite film showed the presence of C (Kα), O (Kα), Ca (Kα, Kβ) and Mg (Kα). The Mg signal is evident on the deposited aragonite, but it does not present in the EDS spectrum of nacre substrate. Because the process of biomineralization might involve the selective identification and uptake of elements and ionic molecules from the local environment, they were incorporated into the structure under strict biological mediation and control [32]. The growth of the aragonite component of the composite occurred by the successive nucleation of aragonite crystals and their arrest by

Fig. 3. XRD pattern of nacre powder. (a) The standard data of aragonite (JCPDS 41-1475), (b) XRD graph of nacre powder.

means of a protein-mediated mechanism [6]. This would agree that attached soluble acidic proteins on the matrix surface act as crystallization inhibitors in solution and nucleates when bound to chitin. Accordingly, magnesium was an important modifier of CaCO3 morphology and growth in natural waters [33]. Many studies indicated that highdensity Mg2+ was found in bioenvironment and it took an important part in the biomineralization of calcium carbonate. When the Mg2 + ion was at high concentration, it induced the synthesis of aragonite [34]. As regards the effects of adding organic additives along with Mg2 +, it promoted the formation of aragonite crystals [35]. In this paper, it is favor to the formation of aragonite at the molar rate of Mg:Ca = 4 combined with organic matrix on the nacre. Fig. 6 shows SEM micrographs of deposited calcium carbonate on the fresh substrate by different flow type such as static and vortex. In static flow type the solutions were kept in stationary state after the two reactants were mixed and in vortex flow type the solution were mixed using magnetic stirring at a rate of 1.78 r/s (Fig. 6d) and 5.17 r/s (Fig. 6e). The film's degree of orientation was much smaller during static and vortex flow type (Fig. 6d and e) than at the flow rate of 1.354 × 10− 3 m/s and 4.514 × 10−3 m/s. In Fig. 6b and c, the nanostacks grew perpendicular to the substrate, they agree with the c-axis degree of orientation and it may be attributed due to the role of τ in the radial direction. But the size of the aragonite crystals in Fig. 6c is clearly larger and more intensive than that in Fig. 6b. This fact suggested that when the crystallization was carried out at a flow rate of 4.514 × 10−3 m/s, the reaction time was shorter than at a flow rate of 1.354 × 10−3 m/s. With the increase of the reaction time, the size of aragonite crystals was larger. In Fig. 6a–e, a mount of pyramid-shaped aragonite crystals

Fig. 4. FTIR spectra of shell nacreous layer and CaCO3 deposition on a nacre surface. (a) The shell nacre, (b) CaCO3 deposition on a nacre surface.

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Fig. 5. EDS spectra of nacre substrate and CaCO3 film on the nacre.

grew in the direction of freedom. These spinous aragonite crystals in stationary state (Fig. 6a) were thinner than the particles obtained in vortex flow type (Fig. 6d). Meanwhile, a few irregular crystals deposited on the pyramid-shaped calcium carbonate in Fig. 6d. In Fig. 6e, the aragonite crystals are flower-shape, which are aggregates of the pyramids aragonite. In the static and vortex flow type, the CaCl2 and Na2CO3 solution was mixed directly by a quick stirring to keep reaction liquid homogeneous mixing. Compared with laminar liquid with directional flow, the growth time of crystals was longer and the supersaturation degree of reaction liquid was larger in the static and vortex flow type. Flowrates and stirring rate had impact on mass transfer rate. Therefore, the facts indicated that mass transfer rate and growth time of crystals played important role in directing the forms and sizes of aragonite crystals. Meanwhile, flow type and flow velocity of fluid flow were influential to the crystallization of calcium carbonate, the following analysis would clarify the difference. Method of hanging-drop was used to measure the solid–liquid interfacial tension in this paper. The classical Yong equation is frequently written as follows:

Solid-liquid interfacial tension (F) is calculated as follows: F ¼ 2γsl l

The actual measured relationship between contact angle and interfacial is shown in Fig. 7. The measured contact angle (θ) is 51.5° which is less than 90°, indicating that this process is a wet process in which solid-vapor interface is completely replaced by solid-liquid. The measured γsl is 46.4 mN/m and solid-liquid interfacial tension (F) is 4.6 × 10− 4 N. Therefore, crystals can be attached to the surface of nacre which induces the crystallization of calcium carbonate. In this work, the physical parameters of the fluid is as follows: d ¼ 2:8  10−2 m; ρ ¼ 1006:56 kg=m ; μ ¼ 0:908  10−3 pa  s 3

Fluid flow mode is determined as follows: Re ¼

s

s1

1

γ ¼ γ þγ cos θ s

sl

ð3Þ l

Where γ , γ and γ are the solid-vapor, solid-liquid and liquidvapor surface tensions, respectively, θ is the contact angle.

ð4Þ

duρ μ

ð5Þ

By substituting the fluid velocities of u1 = 1.354 × 10−3 m/s (Fig. 6b) and u2 = 4.514 × 10−3 m/s (Fig. 6c), Re in Eq. (5) are calculated to be 42 and 140 respectively, reveals that they belong to the laminar flow.

Fig. 6. SEM images of CaCO3 grown on nacre surface for different solution flow type. (a) Static, (b) 1.354 × 10−3 m/s, (c) 4.514 × 10−3 m/s, (d) 1.78 r/s, (e) 5.17 r/s.

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Fig. 7. Image of a sessile drop as produced by a laser printer from the computer-digitized image.

In this study, the flow is assumed to be incompressible, steady state and laminar for three-dimensional. The governing equations for fluid flow are the continuity equation and the motion differential equations. Continuity equation: ∂ux ∂uy ∂uz þ þ ¼0 ∂x ∂y ∂z

ð6Þ

Motion differential equations:

ux

∂ux ∂ux ∂ux ∂ux 1 ∂p μ þ þ uy þ uz þ ¼ X− ρ ∂x ρ ∂x ∂y ∂z ∂θ

2

2

2

∂ ux ∂ ux ∂ ux þ þ 2 ∂x2 ∂y2 ∂z

2

2

2

∂ uy ∂ uy ∂ uy þ þ 2 ∂x2 ∂y2 ∂z

!

ð8Þ

ux

∂uz ∂uz ∂uz ∂uz 1 ∂p μ þ þ uy þ uz þ ¼ Z− ρ ∂z ρ ∂x ∂y ∂z ∂θ

uy ¼ uz ¼ 0; y ¼ h;

∂ ∂ ¼ 0; ¼ 0; y ¼ −g ∂θ ∂z

ux ¼ 0;

y ¼ 0;

dux ¼ 0; dy

ux ¼ u0

ð10Þ ð11Þ

Substituting the above initial values Eq. (10) for Eqs. (6)–(9): !

ð7Þ ∂uy ∂uy ∂uy ∂uy 1 ∂p μ þ ux þ uy þ uz þ ¼ Y− ρ ∂y ρ ∂x ∂y ∂z ∂θ

required in order to avoid trapping the procedure in non-trivial solution:

2

2

2

∂ uz ∂ uz ∂ uz þ þ 2 ∂x2 ∂y2 ∂z

!

ð9Þ Where d, ρ, μ, u, p, θ and Re are the diameter of the reaction tube, the density, the viscosity, the velocity, the pressure, the time and the Reynolds number, respectively. For this experiment, rectangular coordinate system is established and x-axis is the axial direction. An appropriate initial condition is

∂ux ¼0 ∂x 2 ∂ ux ∂p ¼ μ ∂x ∂y2 ∂p ∂p ¼ ¼0 ∂y ∂z

ð12Þ

By substituting the initial values Eq. (11) for Eq. (12), u(y) can be expressed by Eq. (13):   2  y ux ¼ u0 1‐ h

ð13Þ

dux 2 yu0 ¼‐ 2 dy h

ð14Þ

Fig. 8. Schematic of CaCO3/PAA multilayered formation by reputation CaCO3 growth in raw material liquid at the flow rate of 1.354 × 10−3 m/s and drop coating of 0.1 mM PAA/ethanol.

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Fig. 9. SEM images of samples. (a) First layer of the aragonite deposition on nacre, (b) aragonite layer covered with a PAA layer, (c) cross section of the multilayer film on the substrate.

Tangential force per unit area is the shear stress τ. For most of the fluid, τ obeys the following Newton's law of viscosity: τ ¼ ‐μ

dux dy

ð15Þ

can see from Fig. 9c that the single-layer thickness of the prepared multilayered aragonite is about 1 μm. As we can see from Fig. 9a, the diameter of needles of aragonite crystals is about 0.11 μm. The cross section has several openings and the morphology differs from the first aragonite layer deposited on the substrate because the nanostacks grew in inorganic solution with PAA.

From Eq. (14) and Eq. (15), we can obtain Eq. (16): τ¼

4. Conclusions

2μyu0

ð16Þ

2

h

−3

m/s, u2 = Finally, we can obtain that when u1 = 1.354 × 10 4.514 × 10−3 m/s, τ1 ≠ τ2. These nacre substrates which were subjected to different shear stress in the radial direction were present in Fig. 6b and c. With shear stress, it prompted orientated growth of aragonite crystals. In Fig. 6d and e, propeller agitator mixing state was used to discuss the effect of flow type and flow velocity of fluid flow on the growth of aragonite crystals. The rotate speed is 1.78 r/s and 5.17 r/s respectively. Determine fluid flow mode is as follows: 2

ReM ¼

ρnd μ

ð17Þ

By substituting the known rotate speeds of 1.78 r/s and 5.17 r/s, ReM in Eq. (17) are calculated to be 1.02 × 104 and 2.97 × 104 respectively, revealing that they belong to the turbulent flow. In this process, sample was subject to centrifugal force which can be written as follows: F¼m

ν2 ¼ mrω2 r

ð18Þ

Finally, we can obtain that ω1 = 1.78 r/s, ω2 = 5.17 r/s, F1 = 1.06 × 10−4 N and F2 = 8.94 × 10−4 N. So, the crystals were moving with the stirring, the direction was not certain and the aragonite grew in the direction of freedom. Fig. 8 shows a schematic image of aragonite/PAA multilayered formation on a nacre substrate. The substrate was fresh nacre pretreated with deionized water, which retained the original component and structure. The method can enable observation of an arrangement of nanostacks that tightly packed needles of aragonite crystals and form a multilayer structure. Aragonite film was deposited in CaCl2 and Na2CO3 mixture solution at the flow rate of 1.354 × 10−3 m/s, washed with distilled water, then dried. Finally a drop of 0.1 mM PAA/ethanol solution was dropped on the aragonite film. Fig. 9 shows SEM micrographs of the multilayered aragonite formation process. Fig. 9a shows the first layer of aragonite tightly deposited on the nacre substrate. Fig. 9b shows an aragonite layer covered with a porous PAA layer. Fig. 9c shows a cross section of the multilayer aragonite films on the nacre substrate. Generally, PAA was used as a soluble accelerator for calcium carbonate crystallization because it could induce crystallization on numerous organic templates [9]. Thus, PAA was used as an interlamellar substrate for the multilayered aragonite film. We

Tightly packed needles of aragonite homogeneous-film were fabricated on a fresh nacre substrate. The optimal condition for the growth of highly c-axis oriented aragonite is 1.354 × 10− 3 m/s under the circumstance of laminar-flow. The results indicate that mass transfer rate and growth time of crystals play important roles in directing the forms and sizes of aragonite crystals. Artificial nacre-like composite material was fabricated by the reaction of CaCl2 and Na2CO3 mixed solution with the addition of magnesium ions and drop-coating of 0.1 mM PAA/ ethanol which provided an interlamellar substrate for the multilayer film. The single-layer thickness of the nacre-like composite material is about 1 μm. The oriented of deposited aragonite can be controlled by the flow type and flow velocity. The process of obtaining highly c-axis oriented aragonite may provide a new method to control the growing of aragonite. Acknowledgments Thanks for the supports by the National Natural Science Fund of China (21276063, 21306037, 21406050 and 21476059), the Natural Science Fund of Hebei Province (E2014202266), the Hebei Science and Technology Support Program (16273101D), Agency of Science and Technology and Agency of Human and Resource of Hebei Province (15273105, C2015003039). References [1] X.L. Zhang, Z.H. Fan, Q. Lu, Y.L. Huang, D.L. Kaplan, H.S. Zhu, Hierarchical biomineralization of calcium carbonate regulated by silk microspheres, Acta Biomater. 9 (2013) 6974–6980. [2] K. Gries, R. Kröger, C. Kübel, M. Fritz, A. Rosenauer, Investigations of voids in the aragonite platelets of nacre, Acta Biomater. 5 (2009) 3038–3044. [3] K. Lee, W. Wagermaier, A. Masic, K.P. Kommareddy, M. Bennet, I. Manjubala, et al., Self-assembly of amorphous calcium carbonate microlens arrays, Nat. Commun. 3 (2012) 725. [4] M. Ni, B.D. Ratner, Nacre surface transformation to hydroxyapatite in a phosphate buffer solution, Biomaterials 24 (2003) 4323–4331. [5] L. Qiao, Q. Feng, S. Lu, In vitro growth of nacre-like tablet forming: from amorphous calcium carbonate, nanostacks to hexagonal tablets, Cryst. Growth Des. 8 (2008) 1509–1514. [6] J. Sun, B. Bhushan, Hierarchical structure and mechanical properties of nacre: a review, RSC Adv. 2 (2012) 7617–7632. [7] M. Suzuki, K. Saruwatari, T. Kogure, Y. Yamamoto, T. Nishimura, T. Kato, et al., An acidic matrix protein, Pif, is a key macromolecule for nacre formation, Science 325 (2009) 1388–1390. [8] M.I. Lopez, P.E. Meza Martinez, M.A. Meyers, Organic interlamellar layers, mesolayers and mineral nanobridges: contribution to strength in abalone (Haliotis rufescence) nacre, Acta Biomater. 10 (2014) 2056–2064. [9] A. Hayashi, T. Nakamura, T. Watanabe, Fabrication of a nacre-like aragonite/PAA multilayer film on a nacre substrate, Cryst. Growth Des. 10 (2010) 5085–5091.

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