- Email: [email protected]
Influence of copper (II) on biomineralization of CaCO3 and preparation of micron pearl-like biomimetic CaCO3
Ceramics International 45 (2019) 14354–14359
Contents lists available at ScienceDirect
Ceramics International journal homepage: www.elsevier.com/locate/ceramint
Influence of copper (II) on biomineralization of CaCO3 and preparation of micron pearl-like biomimetic CaCO3
T
Xun Liua,b,∗, Kangxin Lia, Chaoqun Wua, Zhaoqian Lia, Bo Wua, Xiaohui Duana, Yong Zhouc, Chonghua Peia,∗∗ a
State Key Laboratory of Environment-friendly Energy Materials, Southwest University of Science and Technology, Mianyang, 621010, PR China Department of Chemical Engineering, University of Michigan, Ann Arbor, MI, 48109, USA c Department of Materials Science and Engineering, National Lab of Solid State Microstructure, ERERC, Nanjing University, Nanjing, 210093, China b
A R T I C LE I N FO
A B S T R A C T
Keywords: Biomimetic calcium carbonate Grain growth (A) Microstructure-final (B) Functional applications (E)
In all the waters where mollusks can grow, a variety of metal ions abounds. Attention has focused, however, on the effects of K+, Na+ and Mg2+ on the biomineralization of nacre, and those of other metal ions have been relatively neglected. This paper investigated the effects of representative copper (II) on the biomineralization of CaCO3 using egg white as the organic matrix. The effects of copper ion concentration, aging time and the combined actions of a high concentration of both egg white and Cu2+ on the morphology and crystal type of CaCO3 were studied, and the action mechanism was analyzed. The results show that copper (II) can induce the formation of vaterite, promote the spheroidization of mineralized particles, distort and deform the lamellar structure, and affect the surface roughness. Mechanism analysis shows that the bending and twisting of the protein molecule chain caused by the biuret reaction of Cu2+ with egg-white protein is the primary reason for the effects of copper (II) on the morphology and crystal type of CaCO3. On this basis, a micron pearl-like CaCO3 with a spherical structure consisting of uniform lamellae about 350 nm thick was obtained by exploiting the combined actions of high concentrations of egg white and Cu2+.
1. Introduction In the process of CaCO3 biomineralization, inorganic ions as well as organic matter play an important role in the formation of the morphology of the biomineral, including its final polymorph [1–4]. However, current research mainly focuses on the influence of light metal ions, such as K+, Na+ and Mg2+ [5–7]. In the water where mollusks actually live, whether fresh or salt, there are many kinds of ions, and the background levels of some ions are at very high, as illustrated in Table 1, which gives the levels of selected elements in different types of water and in the pearls that form in each [8–10]. It can be seen that, in addition to the conventional elements including K, Na, Ca and Mg, a variety of heavy metal elements, such as Sr, Hg, Pb, Cu, Fe, and so on, is also typically present, and that the levels of certain heavy metal elements (such as Sr) are quite high. Interestingly, although pearls grown in different types of water contain many different trace elements, the levels of those elements do not vary greatly, and they are much higher in the pearls than in the water where the pearls grew, showing that
these elements are enriched during the pearl's formation and suggesting that this enrichment may be related to the biomineralization process, not just a function of simple physical adsorption. In other words, the formation process for pearls may affect the levels of trace elements besides K, Na, Ca and Mg in them, and these elements may themselves have an important effect on the biomineralization process. Out of the many trace elements in water, copper (II) was selected as research object for the following reasons: i) its concentration is at an intermediate level; ii) its enrichment level in pearls is high (500-fold in freshwater pearls and 14,000-fold in seawater pearls, respectively); iii) although the background levels in fresh water and sea water differ 24fold, the levels in pearls formed in each are almost the same; iv) copper (II) is an indispensable element to the metabolism [11]. First, the effects of copper (II) concentration on the polymorph and morphology of the biomineral, regulated by egg-white protein, were investigated. Second, a micron pearl-like biomimetic calcium carbonate was prepared under the synergistic actions of a high concentration of both egg-white protein and copper (II).
∗
Corresponding author. State Key Laboratory of Environment-friendly Energy Materials, Southwest University of Science and Technology, Mianyang 621010, PR China. ∗∗ Corresponding author. E-mail addresses: [email protected] (X. Liu), [email protected] (C. Pei). https://doi.org/10.1016/j.ceramint.2019.04.150 Received 5 April 2019; Received in revised form 16 April 2019; Accepted 17 April 2019 Available online 18 April 2019 0272-8842/ © 2019 Elsevier Ltd and Techna Group S.r.l. All rights reserved.
Ceramics International 45 (2019) 14354–14359
X. Liu, et al.
Table 1 Levels of certain metallic elements in salt or fresh water and in the pearls formed in each. Element
Seawater/ppb
Freshwater/ppb
Freshwater pearl/ ppm
Seawater pearl/ ppm
Na Mg Ca K Sr Hg Pb Cu Cr Ni Mn Fe Co
10.78*106 1.28*106 412*103 399*103 7.7*103 6*10−3 1*10−3 0.12 0.33 0.18 0.01 0.04 0.02
6000 4000 15*103 2200 70 0.1
2590 39 38*104 56 394 0.01 1.01 1.5 0.08 0.9 286 5 0.42
6030 289 37*104 159 822 0.04 1.64 1.7 0.02 0.1 4 13 0.43
3 1 0.5 8 1400 0.2
Fig. 1. Molecular structure (a) and photo (b) of the products of the biuret reaction.
2. Materials and methods 2.1. Chemicals Na2CO3, CaCl2 and CuSO4 used in this experiment were all analytically pure and purchased from Kelong Chemical Company, China. Hen eggs were purchased from the Wal-Mart supermarket in Mianyang, China. Ultra-pure water (UPT-I-5/10/20T) was used for the experiment. 2.2. Preparation The preparation method was direct precipitation, with egg-white protein as the organic substrate. The concentration of the CuSO4 solution was 0.04 mol/L, and the concentration of the CaCl2 and Na2CO3 solutions was 0.2 mol/L. The experimental process was as follows. First, a certain amount of egg white was added to 100 mL of Na2CO3 solution, and the mixture was stirred until the egg white was completely dissolved. Next, a certain volume of CuSO4 solution was added to the mixture. The solution containing CO32−, egg-white protein and Cu2+ is labeled S1. The 0.2 mol/L CaCl2 solution is labeled S2. 100 mL of S2 was then dropped into S1 at a rate of 10 mL/min. When the 100 mL of S2 had all been added, the resulting mixture was allowed to settle for one or more days in order to promote the development of mineralized particles. After this aging period, the mineralized precipitate was extracted, washed three times with ultra-pure water, and then lyophilized to obtain the target samples. For the experiment, various contents of egg white, concentrations of Cu2+ and aging times were used. 2.3. Characterization SEM and XRD were used to identify the morphology and crystal type of the samples. SEM characterization was conducted using the TM-1000 electron microscope produced by Japan Hitachi Company. The XRD test was done using an X-ray diffractometer (D/max-RB, Rigaku Co., Japan), with a Cu Ka radiation source and a step scan of 0.020 from 2.50 to 600 (λ = 0.15418 nm, voltage = 30 kV, current = 20 mA). 3. Results and discussion 3.1. Coordination and dissolution of Cu2+ The Na2CO3 solution is strongly alkaline, with the pH of the 0.2 mol/L Na2CO3 solution reaching 11.3. Cu2+ cannot persist in independent form in such a solution. Once it is added, it quickly reacts with CO32−, forming CuCO3, which is then hydrolyzed to a mixture of Cu2(OH)2CO3 and Cu(OH)2. To avoid these reactions, egg white was
added to the Na2CO3 solution before adding Cu2+. The main reason is that, in a strongly alkaline solution, Cu2+ can coordinate with four N atoms on peptide bonds (-CONH-) and two water molecules to form a purple red complex (Fig. 1). This reaction is called biuret reaction, which is often used to detect the presence of protein [12], and is independent of protein type. In fact, for fear of the precipitation of copper ion, it can be added to CaCl2 solution first, and then the mixed solution mineralizes with NaCO3 solution. After investigating the effects of seven divalent metal cations, including Mg2+, Mn2+, Cu2+, Sr2+, Cd2+, Ba2+ and Pb2+, on the formation and structure of calcium carbonate polymorphs, Brečević pointed out that whether the mineralized products are calcite or vaterite, copper ions do not enter the lattice of mineral or are adsorbed by mineral. That is to say, copper ion alone will not affect the mineralization of CaCO3 [13]. In view of the research results of Brečević and the natural enrichment of copper ions in biological CaCO3, we hold that the participation of copper ions in CaCO3 biomineralization is by interacting with organic matrix. Therefore, copper ions were added to the mixed solution of NaCO3 and egg white in the experiment, and solution S1 mentioned above was obtained. In this way, the interaction between copper ions and egg white can be enhanced by biuret reaction. 3.2. Effects of Cu2+ concentration In order to investigate the effects of the Cu2+ content on the biomineralization process, 6 different concentrations of Cu2+–0 μmol/L, 0.4 μmol/L, 0.8 μmol/L, 1.2 μmol/L, 1.6 μmol/L and 2.0 μmol/L–were added. The other reaction conditions remained as follows: the content of egg white was 1% (v/v), the volume of CaCl2 solution and Na2CO3 solution was 100 mL, and the aging time was 1 d. The morphology of the samples is shown in Fig. 2. The influences of Cu2+ concentration on the mineralization process of CaCO3 will be discussed from the following three aspects: overall morphology, surface roughness and lamellar structure. In terms of the overall morphology of mineralized particles, it can be seen that, without Cu2+, the mineralized particles mainly take on a layered cubic structure (Fig. 2a). At a low concentration of Cu2+ (0.4 μmol/L), the layered cubic structure survives with no significant change (Fig. 2b). However, as the Cu2+ level increases, particle morphology gradually changes from a cubic to a spherical lamellar structure. When the Cu2+ concentration is 0.8 μmol/L, the edges and corners of the mineralized particles start to round off obviously despite their basically cubic structure (Fig. 2c). When the concentration is 1.6 μmol/ L, the particles are mainly spherical (Fig. 2e). The second aspect is the change of surface roughness of mineralized particles. As shown in Fig. 2a, the surface of mineralized particle is smooth without Cu2+. With the addition of Cu2+, the surface becomes rough (Fig. 2b). As the Cu2+ level increases, surface roughness gradually becomes stronger and reaches the maximum at the Cu2+ concentration of 0.8 μmol/L (Fig. 2c). However, the surface of mineralized
14355
Ceramics International 45 (2019) 14354–14359
X. Liu, et al.
Fig. 3. XRD patterns of samples prepared with different concentrations of Cu2+ present: a, 0 μmol/L; b, 0.4 μmol/L; c, 0.8 μmol/L; d, 1.2 μmol/L; e, 1.6 μmol/L; f, 2.0 μmol/L.
Fig. 2. SEM images of samples prepared at different concentrations of Cu2+: a, 0 μmol/L; b, 0.4 μmol/L; c, 0.8 μmol/L; d, 1.2 μmol/L; e, 1.6 μmol/L; f, 2.0 μmol/L. Scale bar is 5 μm.
particles begins to become smooth when the concentration of copper ion continues to increase from 0.8 μmol/L (Fig. 2d, e and 2f). The last important morphological effect from the increasing levels of Cu2+ is a change in the lamellar structure. The structure induced by egg white protein alone is typically cubic and lamellar (Fig. 2a). When the concentration of Cu2+ is 0.4 μmol/L, the lamellar structure is almost intact. However, when the concentration is 0.8 μmol/L, the lamellar structure begins to distort and deform, gradually shifting to a lamellar spherical structure. As the Cu2+ level increases further, the cubic mineralized particles almost disappear, but the lamellar spherical structure survives even when the concentration increases to 1.6 μmol/L. The above analysis shows that, as the Cu2+ level rises, the following changes in the morphology of the mineralized particles occur: i) The surface roughness shows a change of rising first and then depressing; ii) They tend to become more spherical; iii) Their lamellar structure becomes more distorted and deformed; iv) The overall trend is from lamellar cube to lamellar sphere and eventually to spheres with almost no lamellar structure on their surface, as shown in Fig. 2f (their inner microstructure will be further scrutinized in the following section). The XRD patterns of samples prepared by adding different concentrations of Cu2+ are shown in Fig. 3. It can be seen that the crystal type of samples prepared without Cu2+ present is typical for calcite (PDF 47–1743#) (Curve a), and there is no visible diffraction peak for other crystal types. When the concentration of Cu2+ is 0.4 μmol/L, vaterite (PDF 33–0268#) appears alongside the calcite, but at a very low peak intensity. Its peak intensity rises steadily with the increase of Cu2+ concentration. The XRD characterization results show that Cu2+ aids the formation of vaterite and that the vaterite takes on a spherical structure. Given these results, the number of spherical particle should gradually increase as the Cu2+ level increases, as the SEM images (Fig. 2) confirm.
3.3. Effects of aging time In order to investigate the stability of the crystal types, different aging times were used, including 1 d, 3 d, 6 d and 9 d. The other reaction conditions remained as follows: the content of egg white was 1% (v/v), the volume of the CaCl2 and Na2CO3 solutions was 100 mL, and the concentration of CuSO4 was 0.8 μmol/L.
Fig. 4. SEM images of samples prepared with different aging time: 1 d (a), 3 d (b), 6 d (c) and 9 d (d). Scale bar is 30 μm.
SEM images of the samples prepared using different aging times appear in Fig. 4. It can be seen that particle size gradually tends to be more uniform as aging time increases, but in contrast, the proportion of spherical particles tends to decrease. When aging time is 1 d, more than 50% of the particles are spherical. The white arrows in Fig. 4b and c point to spherical particles. It can be seen that the proportion of spherical particles decreases significantly. When aging time reaches 9 d, there are no spherical particles in the sample. This trend can be explained by the Ostwald-Freundlich equation [14].
log
S2 2σM ⎛ 1 1 = − ⎞ S1 ρRT ⎝ r2 r1 ⎠ ⎜
⎟
In the equation, S is solubility, σ is surface tension, ρ is solid density, r is particle size and M is molecular weight. It can be seen from the formula that the smaller the particle size, the greater the solubility. Therefore, when the dissolution of large particles reaches saturation, the dissolution of small particles is still unsaturated. This will cause small particles to dissolve and large particles to grow until the solubility of all particles eventually reaches the same value, that is, until particle size approaches uniformity. The SEM images show that the fine mineralized particles have disappeared completely when the aging time reaches 6 d. Therefore, maximum uniformity of particle size is achieved after 6 d of aging. The XRD patterns of samples prepared with different aging times appear in Fig. 5. It can be seen that vaterite appears in samples with a
14356
Ceramics International 45 (2019) 14354–14359
X. Liu, et al.
Fig. 5. XRD patterns of samples prepared with different aging times: 1 d (a), 3 d (b), 6 d (c) and 9 d (d).
short aging time (curves a, b and c), but its peak intensity gradually diminishes as aging time increases, and it disappears completely at 9 d. This finding is consistent with the SEM results. The change of crystal type indicates that, although the addition of copper ions promotes the formation of spheroidal vaterite, the vaterite is still metastable as compared to calcite. As long as conditions (such as the liquid environment) permit, vaterite will gradually transform into calcite, and the shape of mineralized particles will change from spherical to cubic.
Fig. 6. SEM images of samples prepared at different concentrations of Cu2+: a, 0.4 μmol/L; b, 1.2 μmol/L; c, 2.4 μmol/L (1#); d, 2.8 μmol/L (2#); e, 3.2 μmol/ L (3#), and the profile of a single spherical particle in image e (f). Scale bar is 10 μm.
3.4. Combined effects of high concentrations of both egg white and Cu2+ The experimental results in Section 3.2 show that, as the copper ion level increases, the shape of mineralized particles tends to become spheroidal, and their lamellar structure tends to become distorted. What is the end-point of this trend? This is a very interesting question. If the egg-white concentration remains unchanged, further precipitation will occur if the copper ion level increases. In order to avoid this problem, one must increase the egg white and copper ion concentrations in tandem. Therefore, the combined effects of high concentrations of both egg white and copper ions were studied, as spelled out in this section. Table 2 shows the contents of egg white and the corresponding concentrations of CuSO4 in S1 solution. The other reaction conditions remained as follows: the volume of the CaCl2 and Na2CO3 solutions was 100 mL, and the aging time was 1 d. The SEM images in Fig. 6 show that the proportion of spherical particles increases with the concentration of egg white and copper ions. For comparison, two SEM images with low magnification of samples prepared at the Cu2+ concentration of 0.4 μmol/L and 1.2 μmol/L are also put together (Fig. 6a and b). As can be seen from the figure, more than 90% of the particles in sample 1# show spherical shape (Fig. 6c), while the proportion of sample 2# increases to more than 95% (Fig. 6d). The white arrows in Fig. 6d point to cubic particles. When the content of egg white is 5% (v/v) and the concentration of copper ion reaches 3.2 μmol/L (3#), the mineralized particles are all spherical (Fig. 6e). To better illustrate the influence of Cu2+ concentration on Table 2 Composition and assigned number of the samples showing the combined effects of high concentrations of both egg white and Cu2+. Number
Content of egg white/% (v/v)
Concentration of Cu2+/μmol/L
1# 2# 3#
3 4 5
2.4 2.8 3.2
Fig. 7. Content of spherical particle in the samples prepared at different concentrations of Cu2+. When the Cu2+ concentration is not more than 2.0 μmol/L, the egg-white content is 1% (v/v). Instead, the egg-white content is consistent with Table 2.
CaCO3 sphericity, the spherical particles in the SEM images of samples prepared at different concentrations of Cu2+ were counted and analyzed, and a relationship curve was obtained as shown in Fig. 7. As can be seen from the curve, on the whole, the increasing copper ion level helps the mineralized particles become more spherical, which is consistent with the conclusion of Section 3.2. However, when the Cu2+ concentration is lower or higher, the increase rate is lower. XRD patterns of the samples (Fig. 8) show that as more egg white and copper ions are added, the peak intensity of vaterite continues to increase, meaning that the proportion of vaterite in the mineralized samples is increasing. This is consistent with the results of the SEM analysis. Fig. 8 also shows that there is still a large amount of calcite in the samples. The main reason for this may be that the vaterite is an
14357
Ceramics International 45 (2019) 14354–14359
X. Liu, et al.
Fig. 8. XRD patterns of samples 1#, 2# and 3#.
unstable phase that is easily and relatively quickly converted to calcite, as Section 3.3 discussed. This transformation may be limited to fine particles and a short time-frame, so in general particle morphology remains spherical. In order to ascertain the internal structure of the spherical particles, we microetched one from sample 3#, and characterized its internal morphology using SEM, as shown in Fig. 6f. It can be seen that the interior of the particle still has a lamellar structure, but the lamellae are concentric. Their thickness is uniform at about 350 nm. Because this spherical mineralized particle and pearls are very similar in shape and structure, we call the particle micron pearl-like biomimetic CaCO3. The similarity includes the following features: i) sphericity; ii) lamellar inner structure; iii) thickness of the lamellae (the typical thickness of a nacre lamella is between 200 nm and 500 nm) [15]. However, one can also note that the spherical particles prepared in the experiment are quite different from natural pearls in two ways: i) CaCO3 exists as aragonite in pearls, not as the mixture of vaterite and calcite found in our sample, and ii) the sizes of the spherical particles and of pearls differ by about 3 orders of magnitude. 3.5. Mechanism of Cu2+ influence on CaCO3 biomineralization process Fig. 9 illustrates this mechanism. When egg white is added to CaCl2 solution, Ca2+ first coordinates with functional groups like -OH or -C=O on the egg-white protein (Fig. 9a) [16,17]. Without Cu2+, this coordination would not affect the dispersion of protein molecules. Indeed, due to homo-repulsion, the complexes would be as far away from each other as possible in order to achieve an overall balance [18]. Next, CO32− reacts with Ca2+, and CaCO3 is deposited around the egg white protein chain (Fig. 9b), which is the so-called linear crystal in classical
crystallography. Due to their large surface energy, linear crystals attract each other to form planar crystals. As a result of alternation between coordination of Ca2+ with protein molecules and reaction of Ca2+ with CO32−, a lamellar cubic structure is produced. If the solution contains Cu2+, it coordinates with peptide bonds on egg white protein due to the above-mentioned biuret reaction. It is noteworthy that the coordination of Cu2+ and the coordination of Ca2+ with the protein molecules are essentially independent of each other, because their ligands are different. The two peptide bonds required for the coordination of Cu2+ may come from the same protein molecule or from two different protein molecules. If two peptide bonds originate from the same protein molecule, it will cause the bending of the protein chain. If coordination occurs between two protein chains, it will cause entanglement between molecules. In fact, bending and entanglement can both happen on the same protein chain (Fig. 9f). The higher the copper ion content, the more intense the bending and entanglement of the protein chains, a process that eventually leads to the aggregation of protein chains into spheres (Fig. 9g). At this point, growth assumes a spherical pattern (Fig. 9h), with new calcium carbonate being deposited under the action of egg-white protein. Continuous cycling eventually leads to the formation of spherical lamellar calcium carbonate (Fig. 9j). The crystal type also changes from calcite to vaterite. 4. Conclusion To conclude, due to synergistic effects from egg white, copper (II) can have an important effect on the biomineralization of CaCO3. With regard to the morphology of mineralized particles, Cu2+ can promote the spheroidization of mineralized particles, distort and deform the lamellar structure, and affect the surface roughness. With regard to the crystal type of the mineralized particles, Cu2+ is beneficial to the formation of vaterite. The more copper ions, the more vaterite. However, because vaterite is metastable, aging causes spheroids to transform into cubes, and the crystal type into calcite. A micron pearl-like CaCO3 can be obtained by the combined actions of high concentrations of both egg white and Cu2+, with uniform lamellae about 350 nm thick. Mechanism analysis shows that the biuret reaction of Cu2+ with eggwhite protein will result in bending and twisting of or between protein chains, which is the main reason for the effects of copper ions on the morphology and crystal type of calcium carbonate. The results of this study may help to further enrich understanding of the biomineralization mechanism in nacre and provide theoretical guidance for the preparation of nacre-like materials. Acknowledgements This work is supported by the National Natural Science Foundation of China (11572270), the Scientific Research Fund of Sichuan
Fig. 9. Diagrammatic sketch of the effect of copper ions on CaCO3 mineralization. 14358
Ceramics International 45 (2019) 14354–14359
X. Liu, et al.
Provincial Education Department (18ZA0493), the Innovation Team of the Sichuan Education Department (15TD0014) and the Scientific Research Fund of the Southwest University of Science and Technology (18LZX556 and 17ZX9104).
[10]
[11]
References [1] S. Mann, Biomineralization and biomimetic materials chemistry, J. Mater. Chem. 5 (1995) 935–946 https://doi.org/10.1039/jm9950500935. [2] J.W. Ko, E.J. Son, C.B. Park, Nature-inspired synthesis of nanostructured electrocatalysts through mineralization of calcium carbonate, ChemSusChem 10 (2017) 2585–2591 https://doi.org/10.1002/cssc.201700616. [3] M. Sancho-Tomás, S. Fermani, M. Reggi, J.M. García-Ruiz, J. Gómez-Morales, G. Falini, Polypeptide effect on Mg2+ hydration inferred from CaCO3 formation: a biomineralization study by counter-diffusion, CrystEngComm 18 (2016) 3265–3272 https://doi.org/10.1039/c6ce00184j. [4] X. Liu, Y. Zhou, C. Pei, Mimic biomineralization matrix using bacterial cellulose hydrogel and egg white to prepare various morphologies of CaCO3, CrystEngComm 20 (2018) 4536–4540 https://doi.org/10.1039/c8ce00988k. [5] M. Cusack, A. Freer, Biomineralization: elemental and organic influence in carbonate systems, Chem. Rev. 108 (2008) 4433–4454 https://doi.org/10.1021/ cr078270o. [6] P. Dalbeck, J. England, M. Cusack, M.R. Lee, A.E. Fallick, Crystallography and chemistry of the calcium carbonate polymorph switch in M. edulis shells, Eur. J. Mineral. 18 (2006) 601–609 https://doi.org/10.1127/0935-1221/2006/00180601. [7] G. Falini, S. Fermani, G. Tosi, E. Dinelli, Calcium carbonate morphology and structure in the presence of seawater ions and humic acids, Cryst. Growth Des. 9 (2009) 2065–2072 https://doi.org/10.1021/cg8002959. [8] K. Wang, Trace Elements in Life Science, China Measurement Press, Beijing, 1996. [9] C. Wang, J. He, T. Xie, A preliminary comparison on the composition of several
[12]
[13]
[14]
[15]
[16]
[17]
[18]
14359
nacres living in different seawaters and freshwaters in China, Acta Mineral. Sin. 32 (2012) 310–315. Z. Qiao, X. Liu, X. Duan, Y. Zhou, C. Pei, Y. Ma, Biomimetic interfacial assembly of CaCO3 microspheres using egg-white foam and their interaction with Sr2+, Ceram. Int. 43 (2017) 12870–12875 https://doi.org/10.1016/j.ceramint.2017.06.179. S.R. Smith, K.Z. Bencze, K.A. Russ, K. Wasiukanis, M. Benore-Parsons, T.L. Stemmler, Investigation of the copper binding site and the role of histidine as a ligand in riboflavin binding protein, Inorg. Chem. 47 (2008) 6867–6872 https:// doi.org/10.1021/ic800431b. X. Liu, W. Hu, S. Yang, Z. Li, C. Pei, Y. Zhou, G. Yin, Severe corrosion of copper in a highly alkaline egg white solution due to a biuret corrosion reaction, Corros. Sci. 94 (2015) 270–274 https://doi.org/10.1016/j.corsci.2015.02.011. L. Brečević, V. Nöthig-Laslo, D. Kralj, S. Popović, Effect of divalent cations on the formation and structure of calcium carbonate polymorphs, J. Chem. Soc., Faraday Trans. 92 (1996) 1017–1022 https://doi.org/10.1039/ft9969201017. F. Liu, L. Zargarzadeh, H.J. Chung, J.A.W. Elliott, Thermodynamic investigation of the effect of interface curvature on the solid-liquid equilibrium and eutectic point of binary mixtures, J. Phys. Chem. B 121 (2017) 9452–9462 https://doi.org/10.1021/ acs.jpcb.7b07271. J.L. Arias, M.S. Fernandez, Biomimetic processes through the study of mineralized shells, Mater. Char. 50 (2003) 189–195 https://doi.org/10.1016/S1044-5803(03) 00088-3. R. Lizatović, M. Assent, A. Barendregt, J. Dahlin, A. Bille, K. Satzinger, D. Tupina, A.J.R. Heck, S. Wennmalm, I. André, A protein-based encapsulation system with calcium-controlled cargo loading and detachment, Angew. Chem. Int. Ed. 57 (2018) 11334–11338 https://doi.org/10.1002/anie.201806466. Y. Chen, B.S. Bal, J.P. Gorski, Calcium and collagen binding properties of osteopontin, bone sialoprotein, and bone acidic glycoprotein-75 from bone, J. Biol. Chem. 26 (1992) 24871–24878. W. Hu, F. Dong, J. Zhang, M. Liu, H. He, Y. Wu, D. Yang, H. Deng, Differently ordered TiO2 nanoarrays regulated by solvent polarity, and their photocatalytic performances, Appl. Surf. Sci. 442 (2018) 298–307 https://doi.org/10.1016/j. apsusc.2018.02.147.
Contents lists available at ScienceDirect
Ceramics International journal homepage: www.elsevier.com/locate/ceramint
Influence of copper (II) on biomineralization of CaCO3 and preparation of micron pearl-like biomimetic CaCO3
T
Xun Liua,b,∗, Kangxin Lia, Chaoqun Wua, Zhaoqian Lia, Bo Wua, Xiaohui Duana, Yong Zhouc, Chonghua Peia,∗∗ a
State Key Laboratory of Environment-friendly Energy Materials, Southwest University of Science and Technology, Mianyang, 621010, PR China Department of Chemical Engineering, University of Michigan, Ann Arbor, MI, 48109, USA c Department of Materials Science and Engineering, National Lab of Solid State Microstructure, ERERC, Nanjing University, Nanjing, 210093, China b
A R T I C LE I N FO
A B S T R A C T
Keywords: Biomimetic calcium carbonate Grain growth (A) Microstructure-final (B) Functional applications (E)
In all the waters where mollusks can grow, a variety of metal ions abounds. Attention has focused, however, on the effects of K+, Na+ and Mg2+ on the biomineralization of nacre, and those of other metal ions have been relatively neglected. This paper investigated the effects of representative copper (II) on the biomineralization of CaCO3 using egg white as the organic matrix. The effects of copper ion concentration, aging time and the combined actions of a high concentration of both egg white and Cu2+ on the morphology and crystal type of CaCO3 were studied, and the action mechanism was analyzed. The results show that copper (II) can induce the formation of vaterite, promote the spheroidization of mineralized particles, distort and deform the lamellar structure, and affect the surface roughness. Mechanism analysis shows that the bending and twisting of the protein molecule chain caused by the biuret reaction of Cu2+ with egg-white protein is the primary reason for the effects of copper (II) on the morphology and crystal type of CaCO3. On this basis, a micron pearl-like CaCO3 with a spherical structure consisting of uniform lamellae about 350 nm thick was obtained by exploiting the combined actions of high concentrations of egg white and Cu2+.
1. Introduction In the process of CaCO3 biomineralization, inorganic ions as well as organic matter play an important role in the formation of the morphology of the biomineral, including its final polymorph [1–4]. However, current research mainly focuses on the influence of light metal ions, such as K+, Na+ and Mg2+ [5–7]. In the water where mollusks actually live, whether fresh or salt, there are many kinds of ions, and the background levels of some ions are at very high, as illustrated in Table 1, which gives the levels of selected elements in different types of water and in the pearls that form in each [8–10]. It can be seen that, in addition to the conventional elements including K, Na, Ca and Mg, a variety of heavy metal elements, such as Sr, Hg, Pb, Cu, Fe, and so on, is also typically present, and that the levels of certain heavy metal elements (such as Sr) are quite high. Interestingly, although pearls grown in different types of water contain many different trace elements, the levels of those elements do not vary greatly, and they are much higher in the pearls than in the water where the pearls grew, showing that
these elements are enriched during the pearl's formation and suggesting that this enrichment may be related to the biomineralization process, not just a function of simple physical adsorption. In other words, the formation process for pearls may affect the levels of trace elements besides K, Na, Ca and Mg in them, and these elements may themselves have an important effect on the biomineralization process. Out of the many trace elements in water, copper (II) was selected as research object for the following reasons: i) its concentration is at an intermediate level; ii) its enrichment level in pearls is high (500-fold in freshwater pearls and 14,000-fold in seawater pearls, respectively); iii) although the background levels in fresh water and sea water differ 24fold, the levels in pearls formed in each are almost the same; iv) copper (II) is an indispensable element to the metabolism [11]. First, the effects of copper (II) concentration on the polymorph and morphology of the biomineral, regulated by egg-white protein, were investigated. Second, a micron pearl-like biomimetic calcium carbonate was prepared under the synergistic actions of a high concentration of both egg-white protein and copper (II).
∗
Corresponding author. State Key Laboratory of Environment-friendly Energy Materials, Southwest University of Science and Technology, Mianyang 621010, PR China. ∗∗ Corresponding author. E-mail addresses: [email protected] (X. Liu), [email protected] (C. Pei). https://doi.org/10.1016/j.ceramint.2019.04.150 Received 5 April 2019; Received in revised form 16 April 2019; Accepted 17 April 2019 Available online 18 April 2019 0272-8842/ © 2019 Elsevier Ltd and Techna Group S.r.l. All rights reserved.
Ceramics International 45 (2019) 14354–14359
X. Liu, et al.
Table 1 Levels of certain metallic elements in salt or fresh water and in the pearls formed in each. Element
Seawater/ppb
Freshwater/ppb
Freshwater pearl/ ppm
Seawater pearl/ ppm
Na Mg Ca K Sr Hg Pb Cu Cr Ni Mn Fe Co
10.78*106 1.28*106 412*103 399*103 7.7*103 6*10−3 1*10−3 0.12 0.33 0.18 0.01 0.04 0.02
6000 4000 15*103 2200 70 0.1
2590 39 38*104 56 394 0.01 1.01 1.5 0.08 0.9 286 5 0.42
6030 289 37*104 159 822 0.04 1.64 1.7 0.02 0.1 4 13 0.43
3 1 0.5 8 1400 0.2
Fig. 1. Molecular structure (a) and photo (b) of the products of the biuret reaction.
2. Materials and methods 2.1. Chemicals Na2CO3, CaCl2 and CuSO4 used in this experiment were all analytically pure and purchased from Kelong Chemical Company, China. Hen eggs were purchased from the Wal-Mart supermarket in Mianyang, China. Ultra-pure water (UPT-I-5/10/20T) was used for the experiment. 2.2. Preparation The preparation method was direct precipitation, with egg-white protein as the organic substrate. The concentration of the CuSO4 solution was 0.04 mol/L, and the concentration of the CaCl2 and Na2CO3 solutions was 0.2 mol/L. The experimental process was as follows. First, a certain amount of egg white was added to 100 mL of Na2CO3 solution, and the mixture was stirred until the egg white was completely dissolved. Next, a certain volume of CuSO4 solution was added to the mixture. The solution containing CO32−, egg-white protein and Cu2+ is labeled S1. The 0.2 mol/L CaCl2 solution is labeled S2. 100 mL of S2 was then dropped into S1 at a rate of 10 mL/min. When the 100 mL of S2 had all been added, the resulting mixture was allowed to settle for one or more days in order to promote the development of mineralized particles. After this aging period, the mineralized precipitate was extracted, washed three times with ultra-pure water, and then lyophilized to obtain the target samples. For the experiment, various contents of egg white, concentrations of Cu2+ and aging times were used. 2.3. Characterization SEM and XRD were used to identify the morphology and crystal type of the samples. SEM characterization was conducted using the TM-1000 electron microscope produced by Japan Hitachi Company. The XRD test was done using an X-ray diffractometer (D/max-RB, Rigaku Co., Japan), with a Cu Ka radiation source and a step scan of 0.020 from 2.50 to 600 (λ = 0.15418 nm, voltage = 30 kV, current = 20 mA). 3. Results and discussion 3.1. Coordination and dissolution of Cu2+ The Na2CO3 solution is strongly alkaline, with the pH of the 0.2 mol/L Na2CO3 solution reaching 11.3. Cu2+ cannot persist in independent form in such a solution. Once it is added, it quickly reacts with CO32−, forming CuCO3, which is then hydrolyzed to a mixture of Cu2(OH)2CO3 and Cu(OH)2. To avoid these reactions, egg white was
added to the Na2CO3 solution before adding Cu2+. The main reason is that, in a strongly alkaline solution, Cu2+ can coordinate with four N atoms on peptide bonds (-CONH-) and two water molecules to form a purple red complex (Fig. 1). This reaction is called biuret reaction, which is often used to detect the presence of protein [12], and is independent of protein type. In fact, for fear of the precipitation of copper ion, it can be added to CaCl2 solution first, and then the mixed solution mineralizes with NaCO3 solution. After investigating the effects of seven divalent metal cations, including Mg2+, Mn2+, Cu2+, Sr2+, Cd2+, Ba2+ and Pb2+, on the formation and structure of calcium carbonate polymorphs, Brečević pointed out that whether the mineralized products are calcite or vaterite, copper ions do not enter the lattice of mineral or are adsorbed by mineral. That is to say, copper ion alone will not affect the mineralization of CaCO3 [13]. In view of the research results of Brečević and the natural enrichment of copper ions in biological CaCO3, we hold that the participation of copper ions in CaCO3 biomineralization is by interacting with organic matrix. Therefore, copper ions were added to the mixed solution of NaCO3 and egg white in the experiment, and solution S1 mentioned above was obtained. In this way, the interaction between copper ions and egg white can be enhanced by biuret reaction. 3.2. Effects of Cu2+ concentration In order to investigate the effects of the Cu2+ content on the biomineralization process, 6 different concentrations of Cu2+–0 μmol/L, 0.4 μmol/L, 0.8 μmol/L, 1.2 μmol/L, 1.6 μmol/L and 2.0 μmol/L–were added. The other reaction conditions remained as follows: the content of egg white was 1% (v/v), the volume of CaCl2 solution and Na2CO3 solution was 100 mL, and the aging time was 1 d. The morphology of the samples is shown in Fig. 2. The influences of Cu2+ concentration on the mineralization process of CaCO3 will be discussed from the following three aspects: overall morphology, surface roughness and lamellar structure. In terms of the overall morphology of mineralized particles, it can be seen that, without Cu2+, the mineralized particles mainly take on a layered cubic structure (Fig. 2a). At a low concentration of Cu2+ (0.4 μmol/L), the layered cubic structure survives with no significant change (Fig. 2b). However, as the Cu2+ level increases, particle morphology gradually changes from a cubic to a spherical lamellar structure. When the Cu2+ concentration is 0.8 μmol/L, the edges and corners of the mineralized particles start to round off obviously despite their basically cubic structure (Fig. 2c). When the concentration is 1.6 μmol/ L, the particles are mainly spherical (Fig. 2e). The second aspect is the change of surface roughness of mineralized particles. As shown in Fig. 2a, the surface of mineralized particle is smooth without Cu2+. With the addition of Cu2+, the surface becomes rough (Fig. 2b). As the Cu2+ level increases, surface roughness gradually becomes stronger and reaches the maximum at the Cu2+ concentration of 0.8 μmol/L (Fig. 2c). However, the surface of mineralized
14355
Ceramics International 45 (2019) 14354–14359
X. Liu, et al.
Fig. 3. XRD patterns of samples prepared with different concentrations of Cu2+ present: a, 0 μmol/L; b, 0.4 μmol/L; c, 0.8 μmol/L; d, 1.2 μmol/L; e, 1.6 μmol/L; f, 2.0 μmol/L.
Fig. 2. SEM images of samples prepared at different concentrations of Cu2+: a, 0 μmol/L; b, 0.4 μmol/L; c, 0.8 μmol/L; d, 1.2 μmol/L; e, 1.6 μmol/L; f, 2.0 μmol/L. Scale bar is 5 μm.
particles begins to become smooth when the concentration of copper ion continues to increase from 0.8 μmol/L (Fig. 2d, e and 2f). The last important morphological effect from the increasing levels of Cu2+ is a change in the lamellar structure. The structure induced by egg white protein alone is typically cubic and lamellar (Fig. 2a). When the concentration of Cu2+ is 0.4 μmol/L, the lamellar structure is almost intact. However, when the concentration is 0.8 μmol/L, the lamellar structure begins to distort and deform, gradually shifting to a lamellar spherical structure. As the Cu2+ level increases further, the cubic mineralized particles almost disappear, but the lamellar spherical structure survives even when the concentration increases to 1.6 μmol/L. The above analysis shows that, as the Cu2+ level rises, the following changes in the morphology of the mineralized particles occur: i) The surface roughness shows a change of rising first and then depressing; ii) They tend to become more spherical; iii) Their lamellar structure becomes more distorted and deformed; iv) The overall trend is from lamellar cube to lamellar sphere and eventually to spheres with almost no lamellar structure on their surface, as shown in Fig. 2f (their inner microstructure will be further scrutinized in the following section). The XRD patterns of samples prepared by adding different concentrations of Cu2+ are shown in Fig. 3. It can be seen that the crystal type of samples prepared without Cu2+ present is typical for calcite (PDF 47–1743#) (Curve a), and there is no visible diffraction peak for other crystal types. When the concentration of Cu2+ is 0.4 μmol/L, vaterite (PDF 33–0268#) appears alongside the calcite, but at a very low peak intensity. Its peak intensity rises steadily with the increase of Cu2+ concentration. The XRD characterization results show that Cu2+ aids the formation of vaterite and that the vaterite takes on a spherical structure. Given these results, the number of spherical particle should gradually increase as the Cu2+ level increases, as the SEM images (Fig. 2) confirm.
3.3. Effects of aging time In order to investigate the stability of the crystal types, different aging times were used, including 1 d, 3 d, 6 d and 9 d. The other reaction conditions remained as follows: the content of egg white was 1% (v/v), the volume of the CaCl2 and Na2CO3 solutions was 100 mL, and the concentration of CuSO4 was 0.8 μmol/L.
Fig. 4. SEM images of samples prepared with different aging time: 1 d (a), 3 d (b), 6 d (c) and 9 d (d). Scale bar is 30 μm.
SEM images of the samples prepared using different aging times appear in Fig. 4. It can be seen that particle size gradually tends to be more uniform as aging time increases, but in contrast, the proportion of spherical particles tends to decrease. When aging time is 1 d, more than 50% of the particles are spherical. The white arrows in Fig. 4b and c point to spherical particles. It can be seen that the proportion of spherical particles decreases significantly. When aging time reaches 9 d, there are no spherical particles in the sample. This trend can be explained by the Ostwald-Freundlich equation [14].
log
S2 2σM ⎛ 1 1 = − ⎞ S1 ρRT ⎝ r2 r1 ⎠ ⎜
⎟
In the equation, S is solubility, σ is surface tension, ρ is solid density, r is particle size and M is molecular weight. It can be seen from the formula that the smaller the particle size, the greater the solubility. Therefore, when the dissolution of large particles reaches saturation, the dissolution of small particles is still unsaturated. This will cause small particles to dissolve and large particles to grow until the solubility of all particles eventually reaches the same value, that is, until particle size approaches uniformity. The SEM images show that the fine mineralized particles have disappeared completely when the aging time reaches 6 d. Therefore, maximum uniformity of particle size is achieved after 6 d of aging. The XRD patterns of samples prepared with different aging times appear in Fig. 5. It can be seen that vaterite appears in samples with a
14356
Ceramics International 45 (2019) 14354–14359
X. Liu, et al.
Fig. 5. XRD patterns of samples prepared with different aging times: 1 d (a), 3 d (b), 6 d (c) and 9 d (d).
short aging time (curves a, b and c), but its peak intensity gradually diminishes as aging time increases, and it disappears completely at 9 d. This finding is consistent with the SEM results. The change of crystal type indicates that, although the addition of copper ions promotes the formation of spheroidal vaterite, the vaterite is still metastable as compared to calcite. As long as conditions (such as the liquid environment) permit, vaterite will gradually transform into calcite, and the shape of mineralized particles will change from spherical to cubic.
Fig. 6. SEM images of samples prepared at different concentrations of Cu2+: a, 0.4 μmol/L; b, 1.2 μmol/L; c, 2.4 μmol/L (1#); d, 2.8 μmol/L (2#); e, 3.2 μmol/ L (3#), and the profile of a single spherical particle in image e (f). Scale bar is 10 μm.
3.4. Combined effects of high concentrations of both egg white and Cu2+ The experimental results in Section 3.2 show that, as the copper ion level increases, the shape of mineralized particles tends to become spheroidal, and their lamellar structure tends to become distorted. What is the end-point of this trend? This is a very interesting question. If the egg-white concentration remains unchanged, further precipitation will occur if the copper ion level increases. In order to avoid this problem, one must increase the egg white and copper ion concentrations in tandem. Therefore, the combined effects of high concentrations of both egg white and copper ions were studied, as spelled out in this section. Table 2 shows the contents of egg white and the corresponding concentrations of CuSO4 in S1 solution. The other reaction conditions remained as follows: the volume of the CaCl2 and Na2CO3 solutions was 100 mL, and the aging time was 1 d. The SEM images in Fig. 6 show that the proportion of spherical particles increases with the concentration of egg white and copper ions. For comparison, two SEM images with low magnification of samples prepared at the Cu2+ concentration of 0.4 μmol/L and 1.2 μmol/L are also put together (Fig. 6a and b). As can be seen from the figure, more than 90% of the particles in sample 1# show spherical shape (Fig. 6c), while the proportion of sample 2# increases to more than 95% (Fig. 6d). The white arrows in Fig. 6d point to cubic particles. When the content of egg white is 5% (v/v) and the concentration of copper ion reaches 3.2 μmol/L (3#), the mineralized particles are all spherical (Fig. 6e). To better illustrate the influence of Cu2+ concentration on Table 2 Composition and assigned number of the samples showing the combined effects of high concentrations of both egg white and Cu2+. Number
Content of egg white/% (v/v)
Concentration of Cu2+/μmol/L
1# 2# 3#
3 4 5
2.4 2.8 3.2
Fig. 7. Content of spherical particle in the samples prepared at different concentrations of Cu2+. When the Cu2+ concentration is not more than 2.0 μmol/L, the egg-white content is 1% (v/v). Instead, the egg-white content is consistent with Table 2.
CaCO3 sphericity, the spherical particles in the SEM images of samples prepared at different concentrations of Cu2+ were counted and analyzed, and a relationship curve was obtained as shown in Fig. 7. As can be seen from the curve, on the whole, the increasing copper ion level helps the mineralized particles become more spherical, which is consistent with the conclusion of Section 3.2. However, when the Cu2+ concentration is lower or higher, the increase rate is lower. XRD patterns of the samples (Fig. 8) show that as more egg white and copper ions are added, the peak intensity of vaterite continues to increase, meaning that the proportion of vaterite in the mineralized samples is increasing. This is consistent with the results of the SEM analysis. Fig. 8 also shows that there is still a large amount of calcite in the samples. The main reason for this may be that the vaterite is an
14357
Ceramics International 45 (2019) 14354–14359
X. Liu, et al.
Fig. 8. XRD patterns of samples 1#, 2# and 3#.
unstable phase that is easily and relatively quickly converted to calcite, as Section 3.3 discussed. This transformation may be limited to fine particles and a short time-frame, so in general particle morphology remains spherical. In order to ascertain the internal structure of the spherical particles, we microetched one from sample 3#, and characterized its internal morphology using SEM, as shown in Fig. 6f. It can be seen that the interior of the particle still has a lamellar structure, but the lamellae are concentric. Their thickness is uniform at about 350 nm. Because this spherical mineralized particle and pearls are very similar in shape and structure, we call the particle micron pearl-like biomimetic CaCO3. The similarity includes the following features: i) sphericity; ii) lamellar inner structure; iii) thickness of the lamellae (the typical thickness of a nacre lamella is between 200 nm and 500 nm) [15]. However, one can also note that the spherical particles prepared in the experiment are quite different from natural pearls in two ways: i) CaCO3 exists as aragonite in pearls, not as the mixture of vaterite and calcite found in our sample, and ii) the sizes of the spherical particles and of pearls differ by about 3 orders of magnitude. 3.5. Mechanism of Cu2+ influence on CaCO3 biomineralization process Fig. 9 illustrates this mechanism. When egg white is added to CaCl2 solution, Ca2+ first coordinates with functional groups like -OH or -C=O on the egg-white protein (Fig. 9a) [16,17]. Without Cu2+, this coordination would not affect the dispersion of protein molecules. Indeed, due to homo-repulsion, the complexes would be as far away from each other as possible in order to achieve an overall balance [18]. Next, CO32− reacts with Ca2+, and CaCO3 is deposited around the egg white protein chain (Fig. 9b), which is the so-called linear crystal in classical
crystallography. Due to their large surface energy, linear crystals attract each other to form planar crystals. As a result of alternation between coordination of Ca2+ with protein molecules and reaction of Ca2+ with CO32−, a lamellar cubic structure is produced. If the solution contains Cu2+, it coordinates with peptide bonds on egg white protein due to the above-mentioned biuret reaction. It is noteworthy that the coordination of Cu2+ and the coordination of Ca2+ with the protein molecules are essentially independent of each other, because their ligands are different. The two peptide bonds required for the coordination of Cu2+ may come from the same protein molecule or from two different protein molecules. If two peptide bonds originate from the same protein molecule, it will cause the bending of the protein chain. If coordination occurs between two protein chains, it will cause entanglement between molecules. In fact, bending and entanglement can both happen on the same protein chain (Fig. 9f). The higher the copper ion content, the more intense the bending and entanglement of the protein chains, a process that eventually leads to the aggregation of protein chains into spheres (Fig. 9g). At this point, growth assumes a spherical pattern (Fig. 9h), with new calcium carbonate being deposited under the action of egg-white protein. Continuous cycling eventually leads to the formation of spherical lamellar calcium carbonate (Fig. 9j). The crystal type also changes from calcite to vaterite. 4. Conclusion To conclude, due to synergistic effects from egg white, copper (II) can have an important effect on the biomineralization of CaCO3. With regard to the morphology of mineralized particles, Cu2+ can promote the spheroidization of mineralized particles, distort and deform the lamellar structure, and affect the surface roughness. With regard to the crystal type of the mineralized particles, Cu2+ is beneficial to the formation of vaterite. The more copper ions, the more vaterite. However, because vaterite is metastable, aging causes spheroids to transform into cubes, and the crystal type into calcite. A micron pearl-like CaCO3 can be obtained by the combined actions of high concentrations of both egg white and Cu2+, with uniform lamellae about 350 nm thick. Mechanism analysis shows that the biuret reaction of Cu2+ with eggwhite protein will result in bending and twisting of or between protein chains, which is the main reason for the effects of copper ions on the morphology and crystal type of calcium carbonate. The results of this study may help to further enrich understanding of the biomineralization mechanism in nacre and provide theoretical guidance for the preparation of nacre-like materials. Acknowledgements This work is supported by the National Natural Science Foundation of China (11572270), the Scientific Research Fund of Sichuan
Fig. 9. Diagrammatic sketch of the effect of copper ions on CaCO3 mineralization. 14358
Ceramics International 45 (2019) 14354–14359
X. Liu, et al.
Provincial Education Department (18ZA0493), the Innovation Team of the Sichuan Education Department (15TD0014) and the Scientific Research Fund of the Southwest University of Science and Technology (18LZX556 and 17ZX9104).
[10]
[11]
References [1] S. Mann, Biomineralization and biomimetic materials chemistry, J. Mater. Chem. 5 (1995) 935–946 https://doi.org/10.1039/jm9950500935. [2] J.W. Ko, E.J. Son, C.B. Park, Nature-inspired synthesis of nanostructured electrocatalysts through mineralization of calcium carbonate, ChemSusChem 10 (2017) 2585–2591 https://doi.org/10.1002/cssc.201700616. [3] M. Sancho-Tomás, S. Fermani, M. Reggi, J.M. García-Ruiz, J. Gómez-Morales, G. Falini, Polypeptide effect on Mg2+ hydration inferred from CaCO3 formation: a biomineralization study by counter-diffusion, CrystEngComm 18 (2016) 3265–3272 https://doi.org/10.1039/c6ce00184j. [4] X. Liu, Y. Zhou, C. Pei, Mimic biomineralization matrix using bacterial cellulose hydrogel and egg white to prepare various morphologies of CaCO3, CrystEngComm 20 (2018) 4536–4540 https://doi.org/10.1039/c8ce00988k. [5] M. Cusack, A. Freer, Biomineralization: elemental and organic influence in carbonate systems, Chem. Rev. 108 (2008) 4433–4454 https://doi.org/10.1021/ cr078270o. [6] P. Dalbeck, J. England, M. Cusack, M.R. Lee, A.E. Fallick, Crystallography and chemistry of the calcium carbonate polymorph switch in M. edulis shells, Eur. J. Mineral. 18 (2006) 601–609 https://doi.org/10.1127/0935-1221/2006/00180601. [7] G. Falini, S. Fermani, G. Tosi, E. Dinelli, Calcium carbonate morphology and structure in the presence of seawater ions and humic acids, Cryst. Growth Des. 9 (2009) 2065–2072 https://doi.org/10.1021/cg8002959. [8] K. Wang, Trace Elements in Life Science, China Measurement Press, Beijing, 1996. [9] C. Wang, J. He, T. Xie, A preliminary comparison on the composition of several
[12]
[13]
[14]
[15]
[16]
[17]
[18]
14359
nacres living in different seawaters and freshwaters in China, Acta Mineral. Sin. 32 (2012) 310–315. Z. Qiao, X. Liu, X. Duan, Y. Zhou, C. Pei, Y. Ma, Biomimetic interfacial assembly of CaCO3 microspheres using egg-white foam and their interaction with Sr2+, Ceram. Int. 43 (2017) 12870–12875 https://doi.org/10.1016/j.ceramint.2017.06.179. S.R. Smith, K.Z. Bencze, K.A. Russ, K. Wasiukanis, M. Benore-Parsons, T.L. Stemmler, Investigation of the copper binding site and the role of histidine as a ligand in riboflavin binding protein, Inorg. Chem. 47 (2008) 6867–6872 https:// doi.org/10.1021/ic800431b. X. Liu, W. Hu, S. Yang, Z. Li, C. Pei, Y. Zhou, G. Yin, Severe corrosion of copper in a highly alkaline egg white solution due to a biuret corrosion reaction, Corros. Sci. 94 (2015) 270–274 https://doi.org/10.1016/j.corsci.2015.02.011. L. Brečević, V. Nöthig-Laslo, D. Kralj, S. Popović, Effect of divalent cations on the formation and structure of calcium carbonate polymorphs, J. Chem. Soc., Faraday Trans. 92 (1996) 1017–1022 https://doi.org/10.1039/ft9969201017. F. Liu, L. Zargarzadeh, H.J. Chung, J.A.W. Elliott, Thermodynamic investigation of the effect of interface curvature on the solid-liquid equilibrium and eutectic point of binary mixtures, J. Phys. Chem. B 121 (2017) 9452–9462 https://doi.org/10.1021/ acs.jpcb.7b07271. J.L. Arias, M.S. Fernandez, Biomimetic processes through the study of mineralized shells, Mater. Char. 50 (2003) 189–195 https://doi.org/10.1016/S1044-5803(03) 00088-3. R. Lizatović, M. Assent, A. Barendregt, J. Dahlin, A. Bille, K. Satzinger, D. Tupina, A.J.R. Heck, S. Wennmalm, I. André, A protein-based encapsulation system with calcium-controlled cargo loading and detachment, Angew. Chem. Int. Ed. 57 (2018) 11334–11338 https://doi.org/10.1002/anie.201806466. Y. Chen, B.S. Bal, J.P. Gorski, Calcium and collagen binding properties of osteopontin, bone sialoprotein, and bone acidic glycoprotein-75 from bone, J. Biol. Chem. 26 (1992) 24871–24878. W. Hu, F. Dong, J. Zhang, M. Liu, H. He, Y. Wu, D. Yang, H. Deng, Differently ordered TiO2 nanoarrays regulated by solvent polarity, and their photocatalytic performances, Appl. Surf. Sci. 442 (2018) 298–307 https://doi.org/10.1016/j. apsusc.2018.02.147.