Volume 13 Number 4 28 January 2015 Pages 957–1266 Organic & Biomolecular Chemistry www.rsc.org/obc ISSN 1477-0520 REVIEW ARTICLE Atsushi Arakaki, Takashi Kato et al. Biomineralization-inspired synthesis of functional organic/inorganic hybrid materials: organic molecular control of self-organization of hybrids Organic & Biomolecular Chemistry View Article Online REVIEW View Journal | View Issue Biomineralization-inspired synthesis of functional organic/inorganic hybrid materials: organic Cite this: Org. Biomol. Chem., 2015, 13, 974 molecular control of self-organization of hybrids Atsushi Arakaki,*a Katsuhiko Shimizu,b Mayumi Oda,a Takeshi Sakamoto,c Tatsuya Nishimurac and Takashi Kato*c Organisms produce various organic/inorganic hybrid materials, which are called biominerals. They form through the self-organization of organic molecules and inorganic elements under ambient conditions. Biominerals often have highly organized and hierarchical structures from nanometer to macroscopic length scales, resulting in their remarkable physical and chemical properties that cannot be obtained by simple accumulation of their organic and inorganic constituents. These observations motivate us to create novel functional materials exhibiting properties superior to conventional materials—both synthetic and natural. Herein, we introduce recent progress in understanding biomineralization processes at the Creative Commons Attribution-NonCommercial 3.0 Unported Licence. molecular level and the development of organic/inorganic hybrid materials by these processes. We Received 22nd August 2014, specifically outline fundamental molecular studies on silica, iron oxide, and calcium carbonate biominera- Accepted 14th October 2014 lization and describe material synthesis based on these mechanisms. These approaches allow us to DOI: 10.1039/c4ob01796j design a variety of advanced hybrid materials with desired morphologies, sizes, compositions, and struc- www.rsc.org/obc tures through environmentally friendly synthetic routes using functions of organic molecules. the earth.9 The optical and mechanical properties of biomin- This article is licensed under a Introduction erals are derived from their complex structures consisting of Biominerals are organic/inorganic hybrid materials that organic and inorganic constituents.7,10,11 Most biominerals are are essential components of living organisms and support formed using abundant elements in earth’s crust. Moreover, Open Access Article. Published on 14 October 2014. Downloaded 10/2/2021 4:17:43 PM. important functions. Typical examples are hydroxyapatite they are synthesized under mild conditions at a near-neutral 1 (Ca10(PO4)6(OH)2) in bones and teeth of mammals, calcium pH and ambient temperature. Owing to these interesting fea- 2 carbonate (CaCO3) in molluscan shells, amorphous silica tures, the formation processes of biominerals have attracted 3 4 (SiO2) in diatoms and marine sponges, and magnetite much attention with the aim of understanding the mecha- 5 (Fe3O4) in chiton teeth. These biominerals have elaborate nisms and applying them to material synthesis in industry. hierarchical structures giving them conspicuously high mech- Over the last three decades, a number of proteins that anical hardness and flexibility, which are not provided by con- control biomineralization processes, including promotion of ventional synthetic materials.6,7 Single calcite crystals found in crystal formation,3,4,12 matrix-assisted orientation of crys- the skeletal construction of brittle stars are a component of tals,13,14 growth inhibition by face-selective surface adsorp- specialized photosensory organs, possibly functioning as a tion,15,16 and control of the crystal phase,16,17 have been compound eye.8 Magnetite nanocrystals in some organisms isolated and analyzed (Table 1). Although it has been believed such as birds and bacteria function as biological geomagnetic that proteins play important roles in biomineralization pro- sensors that help them find and survive in their habitats on cesses, most studies are still limited to fundamental analyses of proteins, such as amino acid sequence comparisons and biochemical characterization. The functions of proteins at the aDivision of Biotechnology and Life Science, Institute of Engineering, molecular level have remained largely unknown so far. A sig- Tokyo University of Agriculture and Technology, 2-24-16, Naka-cho, Koganei, nificant breakthrough in material synthesis using a biominera- Tokyo 184-8588, Japan. E-mail: [email protected] lization protein was achieved by a study involving sponges.18 b Organization for Regional Industrial Academic Cooperation, Tottori University, The protein—known as silicatein—was isolated from silica spi- 4-101, Minami, Koyama-cho, Tottori 680-8550, Japan cules that form the skeletal structures of marine sponges.4 Sur- cDepartment of Chemistry and Biotechnology, School of Engineering, The University of Tokyo, Hongo, Bunkyo-ku, Tokyo 113-8656, Japan. prisingly, this protein shows a direct catalytic function of silica E-mail: [email protected] biomineralization and it allows us to synthesize new materials 974 | Org. Biomol. Chem.,2015,13,974–989 This journal is © The Royal Society of Chemistry 2015 View Article Online Organic & Biomolecular Chemistry Review with a non-natural composition and a wide spectrum of pro- Table 1 Examples of proteins directly involved in calcium carbonate, perties.19,20 After the identification of silicatein, many proteins silica, and iron oxide biomineralization were isolated from various biominerals in diverse organisms, Protein Biomineral Function References which encouraged researchers to use them for material syn- thesis.3,14,17 Silaffins isolated from diatoms can induce and Calcium carbonate regulate silica precipitation.3 A small iron-binding protein, Perlucin The nacreous Calcite precipitation 12 layer of the shell Mms6, isolated from magnetotactic bacteria regulates the MSI31, 60 The nacreous Framework of the 13 surface structure of magnetite nanoparticles.17 A calcium- layer of the shell prismatic layer binding protein, Pif, regulates the nacre formation in the pearl Pif The nacreous Aragonite crystal 14 14 layer of the shell formation oyster Pinctada fucata. These proteins, isolated from different Ansocalcin Goose egg shell Template for calcite 15 biominerals, opened the door for bio-inspired synthesis of matrix nucleation functional organic/inorganic hybrid materials with controlled CAP-1 The exoskeleton Crystal growth 16 of crayfish regulation micro- to nanoscale properties. On the basis of these funda- mental molecular studies, the functional regions of organic Silica Silicatein Sponge spicules Silica polymerization 4 molecules have been adopted for biomimetic nanofabrication ffi – Sila n Diatom shells Silica precipitation 3 processes and the development of bio-inspired materials.21 25 In this review, we introduce the recent advances in the fun- Iron oxide damental molecular analyses of biomineralization in several Mms6 Bacterial Crystal size and shape 17 magnetites control of magnetites biological systems. Here, we focus on the studies on silica, iron oxide, and calcium carbonate (Fig. 1). We also emphasize the application of the proteins associated with biomineraliza- plants, which produce structures composed of amorphous 26 tion toward the controlled synthesis of organic/inorganic func- hydrated silica. Biological siliceous structures (biosilica) are synthesized by biological processes and possess exquisite Creative Commons Attribution-NonCommercial 3.0 Unported Licence. tional materials. species-specific morphology with sizes ranging from the nano- meter to, occasionally, the meter scale.26 Organic molecules, whose expression is under the control of genetic information, Silica biomineralization and determine the uniqueness of biosilica. Scientists have taken application advantage of recent advances in molecular biology and analyti- cal technology to explore the organic molecules involved in – Learning the essence of silica biomineralization in sponges biosilicification.3,4,27 29 Understanding its mechanism will Silicon (Si) is the second most abundant element in the lead to the development of new routes to synthesize functional This article is licensed under a earth’s crust, existing naturally as silicon dioxide or silicates. materials under environmentally benign conditions. This common element is incorporated into a wide range of Biosilica occurs in sponges in the form of structures called living organisms, including diatoms, sponges, and higher spicules that are needle shaped, with dimensions ranging Open Access Article. Published on 14 October 2014. Downloaded 10/2/2021 4:17:43 PM. Atsushi Arakaki received his PhD Katsuhiko Shimizu received his from the Tokyo University of PhD in Biological Science at Agriculture and Technology in Tokyo Metropolitan University in 2003 under the supervision of 1992. He conducted his post- Prof. Tadashi Matsunaga. After doctoral research at several insti- his postdoctoral research at tutions, including the Fusetani Waseda University, Japan, he Biofouling Project, Exploratory joined the Tokyo University of Research for Advanced Technol- Agriculture and Technology and ogy (ERATO), Research Develop- became an associate professor in ment Corporation of Japan 2011. His current research (JRDC), and the University of focuses on understanding the California Santa Barbara under Atsushi Arakaki mechanism controlling the mag- Katsuhiko Shimizu the guidance of Prof. Daniel