Abstract
While the geometries of diatom frustules have been investigated in detail, the processes leading to their formation—morphogenesis and biomineralization—are not well understood. The study of organic templates, which are suspected to be important for biosilicification of diatoms, have been mainly investigated on the basis of diverse demineralization techniques. In contrast to naturally occurring dissolution of diatom cell walls in natural habitats, all experiments in vitro were based on chemical reagents including HF- or alkali-based techniques with addition of some additives as presented in this chapter. Mostly, the amino acids (serine, threonine, hydrohyproline) diverse proteinaceous materials (frustulins, pleuralins, silaffins, silacidins, circulins) as well as polyamines have been proposed to regulate biosilicification in vivo in diatoms. In this chapter, we review the biochemical pathways and potential functions of these chemical compounds and their roles in the biomineralization process. In addition, we demonstrate the presence of chitin and discuss its potential as scaffolding as well as a template material in siliceous cell walls of diatoms. The current findings show that a complex network of different organic components is responsible for the biomineralization of diatoms. Since both the organic network and the precipitated silica are integrated in the material which forms the diatom frustule, the material properties must differ from that of pure silica. As the material properties are a crucial factor for the defensive performance of the frustule and thus their survival, it is likely that organic templates for silicification play a role both for the development process and for the improvement of the material properties of the finished shells.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Al-Sawalmih A (2007) Crystallographic texture of the arthropod cuticle using synchrotron wide angle X-ray diffraction. PhD Thesis, Rheinisch-westfälische Technische Hochschule Aachen
Armbrust EV et al (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86
Atkins EDT (1985) Conformation in polysaccharides and complex carbohydrates. J Biosci 8:375–387
Blackwell J (1973) Chitin. In: Walton AG, Blackwell J (eds) Biopolymers. Academic Press, New York, pp 474–489
Blackwell J, Parker KD, Rudall KM (1965) Chitin in pogonophore tubes. J Mar Biol Assoc UK 45:659–661
Blackwell J, Parker KD, Rudall KM (1967) Chitin fibres of the diatoms Thalassiosira fluviatilis and Cyclotella cryptica. J Mol Biol 28:383–385
Brunner E, Richthammer P, Ehrlich H et al (2009) Chitin-based organic networks: an integral part of cell wall biosilica in the diatom Thalassiosira pseudonana. Angew Chem Int Ed Engl 48(51):9724–9727
Cha JN, Shimizu K, Zhou Y, Christiansen S, Chmelka BF, Stucky GD, Morse DE (1999) Silicatein filaments and subunits from a marine sponge direct the polymerization of silica and silicones in vitro. Proc Natl Acad Sci U S A 96:361–365
De Yoreo JJ, Vekilov P (2003) Principles of crystal nucleation and growth. Rev Miner Geochem 54:57–93
Durkin CA, Mock T, Armbrust EV (2009) Chitin in diatoms and its association with the cell wall. Eukaryot Cell 8:1038–1050
Dweltz NE, Colvin JR, McInnes AG (1968) Studies on chitin (b-(1-4)-linked 2-acetamido-2-deoxy-D-glucan) fibers from the diatom Thalassiosira fluviatilis, Hustedt. III. The structure of chitin from X-ray diffraction and electron microscope observations. Can J Chem 46:1513–1521
Ehrlich H (2010a) Biological materials of marine origin. Invertebrates. Springer, New York, p 594
Ehrlich H (2010b) Chitin and collagen as universal and alternative templates in biomineralization. Int Geol Rev 52:661–699
Ehrlich H, Worch H (2007a) Collagen, a huge matrix in glass-sponge flexible spicules of meter-long Hyalonema sieboldi. In: Bäuerlein E (ed) Handbook of biomineralization vol. 1. The biology of biominerals structure formation, chapter 2. Wiley VCH, Weinheim, pp 23–41
Ehrlich H, Worch H (2007b) Sponges as natural composites: from biomimetic potential to development of new biomaterials. In: Custodio MR, Lobo-Hajdu G, Hajdu E, Muricy G (eds) Porifera research- biodiversity, innovation & sustainability. Museu Nacional, Rio de Janeiro, pp 303–312
Ehrlich H, Ereskovsky AV, Vyalikh DV, Molodtsov SL, Mertig M, Göbel C, Simon P, Hanke T, Heinemann S, Krylova DD, Pompe W, Worch H (2007a) Collagen in natural fibres of deep-sea glass sponge. In: Arias JL, Fernandez MS (eds) Biomineralization: from paleontology to materials science. Editorial Universitaria, Santiago de Chile, pp 439–448
Ehrlich H, Krautter M, Hanke T et al (2007b) First evidence of the presence of chitin in skeletons of marine sponges. Part II. Glass sponges (Hexactinellida: Porifera). J Exp Zool B Mol Dev Evol 308B:473–483
Ehrlich H, Heinemann S, Heinemann C, Bazhenov VV, Shapkin NP, Simon P, Tabachnick KD, Worch H, Hanke T (2008a) Nanostructural organisation of naturally occurring composites: Part I. Silica-collagen-based biocomposites. J Nanomat (available online doi:10.1155/2008/623838)
Ehrlich H, Janussen D, Simon P, Heinemann S, Bazhenov VV, Shapkin NP, Mertig M, Erler C, Born R, Worch H, Hanke T (2008b) Nanostructural organisation of naturally occuring composites: part II. Silica-chitin-based biocomposites. J Nanomat (available online doi:10.1155/2008/670235)
Ehrlich H, Koutsoukos PG, Demadis KD, Pokrovsky OS (2008c) Principles of demineralization: modern strategies for the isolation of organic frameworks. Part I. Common definitions and history. Micron 39:1062–1091
Ehrlich H, Deutzmann R, Capellini E, Koon H, Solazzo C, Yang Y, Ashford D, Thomas- Oates J, Lubeck M, Baessmann C, Langrock T, Hoffmann R, Wörheide G, Reitner J, Simon P, Ereskovsky AV, Mertig M, Vyalikh DV, Molodtsov SL, Worch H, Brunner E, Smetacek V, Collins M (2010a) Mineralization of the meter-long biosilica structures of glass sponges is template on hydroxylated collagen. Nat Chem 2:1084–1088
Ehrlich H, Demadis K, Pokrovsky O, Koutsoukos P (2010b) Modern views on desilicification: biosilica and abiotic silica dissolution in natural and artificial environments. Chem Rev 110:4656–4689
Exposito J-Y, Cluzel C, Garrone R, Lethias C (2002) Evolution of collagens. Anat Rec 268:302–316
Gaill F, Persson J, Sugiyama P, Vuong R, Chanzy H (1992) The chitin system in the tubes of deep sea hydrothermal vent worms. J Struct Biol 109:116–128
Gifford DJ, Bohrer RN, Boyd CM (1981) Spines on diatoms: do copepods care? Limnol Oceanogr 26(6):1057–1061
Gooday GW, Woodman J, Casson EA, Browne CA (1985) Effect of nikkomycin on chitin spine formation in the diatom Thalassiosira fluviatilis, and observations on its peptide uptake. FEMS Microbiol Lett 28:335–340
Goodrich JD, Winter WT (2007) Alpha-chitin nanocrystals prepared from shrimp shells and their specific surface area measurement. Biomacromolecules 8:252–257
Gordon R, Parkinson J (2005) Potential roles for diatomists in nanotechnology. J Nanosci Nanotechnol 5:35–40
Hamm CE, Smetacek V (2007) Armor: why, when and how? In: Falkowski P, Knoll A (eds) Evolution of primary producers in the sea. Elsevier, San Diego, pp 311–332
Hamm CE, Merkel R, Springer O, Jurkojc P, Maier C, Prechtel K, Smetacek V (2003) Architecture and material properties of diatom shells provide efficient mechanical protection. Nature 421:841–843
Hattori S, Adachi E, Ebihara T, Shirai T, Someki I, Irie S (1999) Alkali-treated collagen retained the triple helical conformation and ligand activity for the cell adhesion. J Biochem 125:676–684
Hecky RE, Mopper K, Kilham P, Degens ET (1973) The amino acid and sugar composition of diatom cell-walls. Mar Biol 19:323–331
Herth W (1978) A special chitin-fibril-synthesizing apparatus in the centric diatom Cyclotella. Naturwissenschaften 65:260–261
Herth W (1979) The site of β-chitin fibril formation in centric diatoms. II. The chitin-forming cytoplasmic structures. J Ultrastruct Res 68:16–27
Herth W (1980) Calcofluor white and congo red inhibit chitin microfibril assembly of Poterioochromonas: evidence for a gap between polymerization and microfibril formation. J Cell Biol 87:442–450
Herth W, Barthlott W (1979) The site of β-chitin fibril formation in centric diatoms. I. Pores and fibril formation. J Ultrastruct Res 68:6–15
Herth W, Zugenmaier P (1977) Ultrastructure of the chitin fibrils of the centric diatom Cyclotella cryptica. J Ultrastruct Res 61:230–239
Herth W, Kuppel A, Schnepf E (1977) Chitinous fibrils in the lorica of the flagellate chrysophyte Poteriochromonas stipitata (syn. Ochromonas malhamensis). J Cell Biol 72:311–321
Herth W, Mulisch M, Zugenmaier P (1986) Comparison of chitin fibril structure and assembly in three unicellular organisms. In: Muzzarelli R, Jeuniaux C, Gooday GW (eds) Chitin in nature and technology. Plenum Publishing Corporation, New York, pp 107–120
Kamada T, Takemaru T, Prosser JI, Gooday GW (1991) Right and left helicity of chitin microfibrils in stipe cells in Coprinus cinereus. Protoplasma 165:64–70
Kamatani A (1971) Physical and chemical characteristics of biogenous silica. Mar Biol 8:89–95
Kröger N, Paulsen N (2008) Diatoms—from cell wall biogenesis to nanotechnology. Annu Rev Genet 42:83–107
Kröger N, Sandhage KH (2010) From diatom biomolecules to bioinspired syntheses of silica- and titania-based materials. MRS Bull 35:122–126
Kröger N, Sumper M (1998) Diatom cell wall proteins and the cell biology of silica biomineralization. Protist 149:213–219
Kröger N, Sumper M (2004) The molecular basis of diatom biosilica formation. In: Baeueurlein E (ed) Biomineralization, 2nd edn. Wiley-VCH, Weinheim, pp 137–158
Kröger N, Bergsdorf C, Sumper M (1994) A new calcium binding glycoprotein family constitutes a major diatom cell wall component. EMBO J 13:4676–4683
Kröger N, Bergsdorf C, Sumper M (1996) Frustulins: domain conservation in a protein family associated with diatom cell walls. Eur J Biochem 239:259–264
Kröger N, Lehmann G, Rachel R, Sumper M (1997) Characterization of a 200-kDa diatom protein that is specifically associated with a silica-based substructure of the cell wall. Eur J Biochem. 250:99–105
Kröger N, Deutzmann R, Sumper M (1999) Polycationic peptides from diatombiosilica that direct silica nanosphere formation. Science 286:1129–1132
Kröger N, Deutzmann R, Bergsdorf C, Sumper M (2000) Species-specific polyamines from diatoms control silica morphology. Proc Natl Acad Sci U S A 97:14133–38
Kröger N, Lorenz S, Brunner E, Sumper M (2002) Self-assembly of highly phosphorylated silaffins and their function in biosilica morphogenesis. Science 298:584–586
Lewin JC (1955) The capsule of the diatom Navicula pelliculosa. J Gen Microbiol 13:162–169
Lewin JC (1961) The dissolution of silica from diatom cell walls. Geochim Cosmochim Acta 21:182–189
Liebisch W (1929) Experimentelle und kritische Untersuchungen uber die Pektinmembran der Diatomeen unter besonderer Berucksichtigung der Auxosporenbildung und der Kratikularzustande. Z Bot 22:1–97
Lotmar W, Picken LER (1950) A new crystallographic modification of chitin and its distribution. Experientia 6:58–59
Mangin LA (1908) Observations sur les diatomees. Ann Sci Nut Bot Biol Veg 8:177–219
Mann S (2001) Biomineralization principles and concepts in bioinorganic materials chemistry. University Press, Oxford, p 198
Marshall KE, Robinson EW, Hengel SM, Paša-Tolić L, Roesijadi G (2012) FRET imaging of diatoms expressing a biosilica-localized ribose sensor. PLoS One 7(3):e33771
Martin R, Hild S, Walther P et al (2007) Granular chitin in the epidermis of nudibranch molluscs. Biol Bull 213:307–315
Matsunaga S, Sakai R, Jimbo M, Kamiya H (2007) Long chain polyamines (LCPAs) from marine sponge: possible implication in spicule formation. Chem Biochem 8:1729–1735
McLachlan J, McInnes AG, Falk M (1965) Studies on the chitan (chitin: poly-N acetylglucosamine) fibers of the diatom Thalassiosira fluviatilis Hustedt. I. Production and isolation of chitan fibers. Can J Bot 43:707–713
Müller WEG, Rothenberger M, Boreiko A, Tremel W, Reiber A, Schröder HC (2005) Formation of siliceous spicules in the marine demosponge Suberitues domuncula. Cell Tissue Res 321(2):285–297
Nakajima T, Volcani BE (1969) 3,4-dihydroxyproline, a new amino acid from diatom cell walls. Science 164:1400–1401
Patwardhan SV (2011) Biomimetic and bioinspired silica: recent developments and applications. Chem Commun 47:7567–7582
Patwardhan S, Patwardhan G, Perry CC (2007) Interactions of biomolecules with inorganic materials: principles, applications and future prospects. J Mater Chem 17:2875–2884
Reimann BEF, Lewin JC, Volcani BE (1965) Studies on the biochemistry and fine structure of silica shell formation in diatoms. I. The structure of the cell wall of Cylindrotheca fusiformis Reimann and Lewin. J Cell Biol 24:39–55
Reimann BEF, Lewin JC, Volcani BE (1966) Studies on the biochemistry and fine structure of silica shell formation in diatoms. II. The structure of the cell wall of Navicula pelliculosa (Breb.) Hilse. J Phycol 2:74–84
Revol J-F, Chanzy H (1986) High-resolution electron microscopy of β-chitin microfibrils. Biopolymers 25:1599–1601
Rinaudo M (2006) Chitin and chitosan: properties and applications. Prog Polym Sci 31:603–632
Round FE, Crawford RM, Mann DG (1990) The diatoms: biology and morphology of the genera. Cambridge University Press, Cambridge, pp 747
Rudall KM (1955) The distribution of collagen and chitin. In: Brown R, Danielli JF (eds) Fibrous proteins and their biological significance. Symposia of society of experimental biology, No. IX, University Press, Cambridge, pp 49–71
Rudall KM (1969) Chitin and its association with other molecules. J Polym Sci 28:83–102
Rudall KM, Kenchington W (1973) The chitin system. Biol Rev 49:597–636
Sadava D, Volcani BE (1977) Studies on the biochemistry and fine structure of silica shell formation in diatoms formation of hydroxyproline and dihydroxyproline in Nitzschia angularis. Planta 135:7–11
Scheffel A, Poulsen N, Shian S, Kröger N (2011) Nanopatterned protein microrings from a diatom that direct silica morphogenesis. Proc Natl Acad Sci U S A 108:3175–3180
Schumacher MA, Mizuno K, Bachinger HP (2006) The crystal structure of a collagen-like polypeptide with 3(S)-hydroxyproline residues in the Xaa position forms a standard 7/2 collagen triple helix. J Biol Chem 281:27566–27574
Sheppard V, Scheffel A, Poulsen N, Kröger N (2012) Live diatom silica immobilization of multimeric and redox-active enzymes. Appl Environ Microbiol 78:211–218
Spinde K, Kammer M, Freyer K et al (2011) Biomimetic silicification of fibrous chitin from diatoms. Chem Mater 23:2973–2978
Subburaman K, Pernodet N, Kwak SY et al (2006) Templated biomineralization on self-assembled protein fibers. Proc Natl Acad Sci U S A 103:14672–14677
Sugiyama J, Boisset C, Hashimoto M, Watanabe T (1999) Molecular directionality of β-chitin biosynthesis. J Mol Biol 286:247–255
Sumper M (2002) A phase separation model for the nanopatterning of diatom biosilica. Science 295:2430–2433
Sumper M, Brunner E (2006) Learning from diatoms: nature’s tools for the production of nanostructured silica. Adv Funct Mat 16:17–26
Tesson B, Hildebrand M (2010) Extensive and intimate association of the cytoskeleton with forming silica in diatoms: control over patterning on the meso- and micro-scale. PLoS One 5(12):e14300
Tilburey GE, Patwardhan SV, Huang J et al (2007) Are hydroxyl-containing biomolecules important in biosilicification? A model study. J Phys Chem B 111:4630–4638
van de Poll WH, Vrieling EG, Gieskes WWC (1999) Location and expression of frustulins in the pennate diatoms Cylindrotheca fusiformis, Navicula pelliculosa, and Navicula salinarum (Bacillariophyceae). J Phycol 35:1044–1053
Vincent JVC (2002) Arthropod cuticle: a natural composite shell system. Composites A 33(10):1311–1321
Vournakis J, Pariser ER, Finkielsztein S, Helton M (1997a) Poly-N-acetyl glucosamine. US patent # 5,623,064. Issued April 22, 1997
Vournakis J, Pariser ER, Finkielsztein S, Helton M (1997b) Method of isolating Poly-N-acetyl glucosamine from microalgal culture. US Patent # 5,622,834. Issued April 22, 1997
Walsby AE, Xypolyta A (1977) The form resistance of chitan fibers attached to the cells of Thalassiosira fluviatilis Hustedt. Br Phycol J 12:215–223
Weaver JC, Morse DE (2003) Molecular biology of demosponge axial filaments and their roles in biosilicification. Microsc Res Tech 62:356–367
Wenzl S, Hett R, Richthammer P, Sumper M (2008) Silacidins: highly acidic phosphopeptides from diatom shells assist in silica precipitation in vitro. Angew Chem 47:1729–1732
Wieneke R, Bernecker A, Riedel R, Sumper M, Steinem C et al (2011) Silica precipitation with synthetic silaffin peptides. Org Biomol Chem 9:5482–5486
Yang W, Lopez PJ, Rosengarten G (2011) Diatoms: self assembled silica nanostructures, and templates for bio/chemical sensors and biomimetic membranes. Analyst 136:42–53
Acknowledgements
H.E. is very grateful to the German Research Foundation (DFG, Project EH 394/1) for financial support as well as to Vasily V. Bazhenov and Alexey Rusakov for their technical assistance. We cordially thank Alex Kraberg and Karen Wiltshire for specimens of T. rotula and Diana Krawczyk for images of T. rotula. Kevin McCartney is acknowledged for the revision of the English language of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2015 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Ehrlich, H., Witkowski, A. (2015). Biomineralization in Diatoms: The Organic Templates. In: Hamm, C. (eds) Evolution of Lightweight Structures. Biologically-Inspired Systems, vol 6. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-9398-8_3
Download citation
DOI: https://doi.org/10.1007/978-94-017-9398-8_3
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-017-9397-1
Online ISBN: 978-94-017-9398-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)