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Nanoscale control of silica morphology and three-dimensional structure during diatom cell wall formation

Published online by Cambridge University Press:  03 March 2011

Mark Hildebrand ,
Evelyn York ,
Jessica I. Kelz ,
Aubrey K. Davis ,
Luciano G. Frigeri ,
David P. Allison  and
Mitchel J. Doktycz
Mark Hildebrand*
Affiliation:
Scripps Institution of Oceanography, University of California—San Diego,La Jolla, California 92093-0202
Evelyn York
Affiliation:
Scripps Institution of Oceanography, University of California—San Diego,La Jolla, California 92093-0202
Jessica I. Kelz
Affiliation:
Scripps Institution of Oceanography, University of California—San Diego,La Jolla, California 92093-0202
Aubrey K. Davis
Affiliation:
Scripps Institution of Oceanography, University of California—San Diego,La Jolla, California 92093-0202
Luciano G. Frigeri
Affiliation:
Scripps Institution of Oceanography, University of California—San Diego,La Jolla, California 92093-0202
David P. Allison
Affiliation:
Biological & Nanoscale Systems Group, Life Sciences Division, Oak Ridge National Laboratory,Oak Ridge, Tennessee 37831-6123; Department of Biochemistry & Cellular & Molecular Biology, University of Tennessee, Knoxville, TN, 37996-0840; and Molecular Imaging Inc., Agilent Technologies Tempe, Arizona 85282
Mitchel J. Doktycz
Affiliation:
Biological & Nanoscale Systems Group, Life Sciences Division, Oak Ridge National Laboratory,Oak Ridge, Tennessee 37831-6123
*
a) Address all correspondence to this author. e-mail: mhildebrand@ucsd.edu
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Abstract

We present a unique approach combining biological manipulation with advanced imaging tools to examine silica cell wall synthesis in the diatom Thalassiosira pseudonana. The innate capabilities of diatoms to form complex 3D silica structures on the nano- to micro-scale exceed current synthetic approaches because they use a fundamentally different formation process. Understanding the molecular details of the process requires identifying structural intermediates and correlating their formation with genes and proteins involved. This will aid in development of approaches to controllably alter structure, facilitating the use of diatoms as a direct source of nanostructured materials. In T. pseudonana, distinct silica morphologies were observed during formation of different cell wall substructures, and three different scales of structural organization were identified. At all levels, structure formation correlated with optimal design properties for the final product. These results provide a benchmark of measurements and new insights into biosilicification processes, potentially also benefiting biomimetic approaches.

Keywords

Biological synthesis (assembly)MicrostructureMorphology
Type
Articles
Information
Journal of Materials Research , Volume 21 , Issue 10 , October 2006 , pp. 2689 - 2698
Copyright
Copyright © Materials Research Society 2006

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References

REFERENCES

1.Morse, D.E.: Silicon biotechnology: Harnessing biological silica production to construct new materials. Trends Biotechnol. 17, 230 (1999).CrossRefGoogle Scholar
2.Mann, S.: Biomineralization Principles and Concepts in Bioinorganic Materials Chemistry (Oxford University Press, Oxford, UK, 2001).Google Scholar
3.Davis, S.A., Dujardin, E., Mann, S.: Biomolecular inorganic materials chemistry. Curr. Opin. Solid State Mater. Sci. 7, 273 (2003).CrossRefGoogle Scholar
4.Cha, J., Stucky, G., Morse, D., Deming, T.: Biomimetic synthesis of ordered silica structures mediated by block copolypeptides. Nature 403, 289 (2000).CrossRefGoogle ScholarPubMed
5.Naik, R.R., Whitlock, P.W., Rodriguez, F., Brott, L.L., Glawe, D.D., Clarson, S.J., Stone, M.O.: Controlled formation of biosilica structures in vitro. Chem. Comm. 2, 238 (2003).CrossRefGoogle Scholar
6.Rodriguez, F., Glawe, D.D., Naik, R.R., Hallinan, K.P., Stone, M.O.: Study of the chemical and physical influences upon in vitro peptide-mediated silica formation. Biomacromolecules 5, 261 (2004).CrossRefGoogle ScholarPubMed
7.Dickerson, M.B., Naik, R.R., Sarosi, P.M., Agarwal, G., Stone, M.O., Sandhage, K.H.: Ceramic nanoparticle assemblies with tailored shapes and tailored chemistries via biosculpting and shape-preserving inorganic conversion. J. Nanosci. Nanotechnol. 5, 63 (2005).CrossRefGoogle ScholarPubMed
8.Kisailus, D., Choi, J.H., Weaver, J.C., Yang, W.J., Morse, D.E.: Enzymatic synthesis and nanostructural control of gallium oxide at low temperature. Adv. Mater. 17, 314 (2005).CrossRefGoogle Scholar
9.Curnow, P., Bessette, P.H., Kisailus, D., Murr, M.M., Daugherty, P.S., Morse, D.E.: Enzymatic synthesis of layered titanium phosphates at low temperature and neutral pH by cell-surface display of silicatein-alpha. JACS 127, 15749 (2005).Google Scholar
10.Estroff, L.A., Hamilton, A.D.: At the interface of organic and inorganic chemistry: Bioinspired synthesis of composite materials. Chem. Mater. 13, 3227 (2001).CrossRefGoogle Scholar
11.Belton, D.J., Patwardhan, S.V., Perry, C.C.: Spermine, spermidine and their analogues generate tailored silicas. J. Mater. Chem. 15, 4629 (2005).Google Scholar
12.Belton, D., Patwardhan, S.V., Perry, C.C.: Putrescine homologues control silica morphogenesis by electrostatic interactions and the hydrophobic effect. Chem. Comm. 27, 3475 (2005).CrossRefGoogle Scholar
13.Jin, R.H., Yuan, J.J.: Simple synthesis of hierarchically structured silicas by poly(ethyleneimine) aggregates pre-organized by media modulation. Macromolec. Chem. Phys. 206, 2160 (2005).CrossRefGoogle Scholar
14.Schwenzer, B., Roth, K.M., Gomm, J.R., Murr, M., Morse, D.E.: Bio-inspired synthesis of nanostructured metal hydroxide and phosphate films using no organic reagents. J. Mater. Chem. 16, 401 (2006).Google Scholar
15.Li, C.M., Kaplan, D.L.: Biomimetic composites via molecular scale self-assembly and biomineralization. Curr. Opin. Solid State Mater. Sci. 7, 265 (2003).CrossRefGoogle Scholar
16.Kröger, N., Deutzmann, R., Sumper, M.: Polycationic peptides from diatom biosilica that direct silica nanosphere formation. Science 286, 1129 (1999).Google Scholar
17.Kröger, N., Lorenz, S., Brunner, E., Sumper, M.: Self-assembly of highly phosphorylated silaffins and their function in biosilica morphogenesis. Science 298, 584 (2002).CrossRefGoogle ScholarPubMed
18.Poulsen, N., Kröger, N.: Silica morphogenesis by alternative processing of silaffins in the diatom Thalassiosira pseudonana. J. Biol. Chem. 279, 42993 (2004).Google Scholar
19.Brott, L.L., Naik, R.R., Pikas, D.J., Kirkpatrick, S.M., Tomlin, D.W., Whitlock, P.W., Clarson, S.J., Stone, M.O.: Ultrafast holographic nanopatterning of biocatalytically formed silica. Nature 413, 291 (2001).CrossRefGoogle ScholarPubMed
20.Luckarift, H.R., Spain, J.C., Naik, R.R., Stone, M.O.: Enzyme immobilization in a biomimetic silica support. Nat. Biotechnol. 22, 211 (2004).Google Scholar
21.Naik, R.R., Tomczak, M.M., Luckarift, H.R., Spain, J.C., Stone, M.O.: Entrapment of enzymes and nanoparticles using biomimetically synthesized silica. Chem. Comm. 15, 1684 (2004).CrossRefGoogle Scholar
22.Mizutani, T., Nagase, H., Ogoshi, H.: Silicic acid polymerization catalyzed by amines and polyamines. Chem. Lett. Jpn. 2, 133 (1998).Google Scholar
23.Mizutani, T., Nagase, H., Fujiwara, N., Ogoshi, H.: Silicic acid polymerization catalyzed by amines and polyamines. Bull. Chem. Soc. Jpn. 71, 2017 (1998).CrossRefGoogle Scholar
24.Kröger, N., Deutzmann, R., Bergsdorf, C., Sumper, M.: Species-specific polyamines from diatoms control silica morphology. Proc. Natl. Acad. Sci. USA 97, 14133 (2000).Google Scholar
25.Sumper, M.: A phase separation model for the nanopatterning of diatom biosilica. Science 295, 2430 (2002).Google Scholar
26.Hildebrand, M.: Prospects of manipulating diatom silica nanostructure. J. Nanosci. Nanotechnol. 5, 146 (2005).Google Scholar
27.Sandhage, K.H., Allan, S.M., Dickerson, M.B., Gaddis, C.S., Shian, S., Weatherspoon, M.R., Cai, Y., Ahmad, G., Haluska, M.S., Snyder, R.L., Unocic, R.R., Zalar, F.M., Zhang, Y., Rapp, R.A., Hildebrand, M., Palenik, B.P.: Merging biological self-assembly with synthetic chemical tailoring: The potential for 3-D genetically-engineered micro/nano-devices (3-D GEMS). Int. J. Appl. Ceram. Technol. 2, 317 (2005).Google Scholar
28.Sandhage, K.H., Dickerson, M.B., Huseman, P.M., Caranna, M.A., Clifton, J.D., Bull, T.A., Heibel, T.J., Overton, W.R., Schoenwaelder, M.E.A.: Novel, bioclastic route to self-assembled, 3D, chemically tailored meso/nanostructures: Shape-preserving reactive conversion of biosilica (diatom) microshells. Adv. Mater. 14, 429 (2002).Google Scholar
29.Unocic, R.R., Zalar, F.M., Sarosi, P.M., Cai, Y., Sandhage, K.H.: Anatase assemblies from algae: Coupling biological self-assembly of 3-D nanoparticle structures with synthetic reaction chemistry. Chem. Comm. 7, 796 (2004).Google Scholar
30.Weatherspoon, M.R., Allan, S.M., Hunt, E., Cai, Y., and Sandhage, K.H.: Sol-gel synthesis on self-replicating single-cell scaffolds: Applying complex chemistries to nature’s 3-D nanostructured templates. Chem. Comm. 5, 651 (2005).CrossRefGoogle Scholar
31.Zhao, J.P., Gaddis, C.S., Cai, Y., Sandhage, K.H.: Free-standing microscale structures of nanocrystalline zirconia with biologically replicable three-dimensional shapes. J. Mater. Res. 20, 282 (2005).CrossRefGoogle Scholar
32.Drum, R.W., Pankratz, H.S.: Post mitotic fine structure of Gomphonema parvulum. J. Ultrastruc. Res. 10, 217 (1964).Google Scholar
33.Pickett-Heaps, J., Schmid, A-M.M., Edgar, L.A. The cell biology of diatom valve formation, in Progress in Phycological Research, edited by Round, F.E. and Chapman, D.J. (Biopress Ltd., Bristol, 1990), pp. 1–168.Google Scholar
34.Armbrust, E.V., Berges, J.A., Bowler, C., Green, B.R., Martinez, D., Putnam, N.H., Zhou, S.G., Allen, A.E., Apt, K.E., Bechner, M., Brzezinski, M.A., Chaal, B.K., Chiovitti, A., Davis, A.K., Demarest, M.S., Detter, J.C., Glavina, T., Goodstein, D., Hadi, M.Z., Hellsten, U., Hildebrand, M., Jenkins, B.D., Jurka, J., Kapitonov, V.V., Kroger, N., Lau, W.W.Y., Lane, T.W., Larimer, F.W., Lippmeier, J.C., Lucas, S., Medina, M., Montsant, A., Obornik, M., Parker, M.S., Palenik, B., Pazour, G.J., Richardson, P.M., Rynearson, T.A., Saito, M.A., Schwartz, D.C., Thamatrakoln, K., Valentin, K., Vardi, A., Wilkerson, F.P., Rokhsar, D.S.: The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism. Science 306, 79 (2004).Google Scholar
35.Frigeri, L.G., Radabaugh, T.R., Haynes, P.A., Hildebrand, M.: Identification of proteins from a cell wall fraction of the diatom Thalassiosira pseudonana: Insights into silica structure formation. Mol. Cell. Proteomics 5, 182 (2006).CrossRefGoogle ScholarPubMed
36.Doktycz, M.J., Sullivan, C.J., Hoyt, P.R., Pelletier, D.A., Wu, S., Allison, D.P.: AFM imaging of bacteria in liquid media immobilized on gelatin coated mica surfaces. Ultramicroscopy 97, 209 (2003).Google Scholar
37.Ross, R., Cox, E.J., Karayeva, N.I., Mann, D.G., Paddock, T.B.B., Simonson, R., Sims, P.A.: An amended terminology for the siliceous components of the diatom cell. Nova Hedwiga 64, 513 (1979).Google Scholar
38.Hildebrand, M., Frigeri, L.G., Davis, A.K.: Synchronized growth of Thalassiosira pseudonana (Bacillariophyceae) provides novel insights into cell wall synthesis processes in relation to the cell cycle. (unpublished).Google Scholar
39.Herth, W.: A special chitin-fibril-synthesizing apparatus in the centric diatom Cyclotella. Naturwissen 65, 260 (1979).Google Scholar
40.Herth, W.: The site of β-chitin fibril formation in centric diatoms. II. The chitin forming cytoplasmic structures. J. Ultrastruc. Res. 68, 16 (1979).Google Scholar
41.Walsby, A.E., Xypolyta, A.: The form resistance of chitan fibres attached to cells of Thalassiosira fluviatilis Hustedt. Br. Phycol. J. 12, 215 (1977).Google Scholar
42.Hamm, C.E., Merkel, R., Springer, O., Jurkojc, P., Maier, C., Prechtel, K., Smetacek, V.: Architecture and material properties of diatom shells provide effective mechanical protection. Nature 421, 841 (2003).CrossRefGoogle ScholarPubMed
43.Reimann, B.E.F., Lewin, J.C., Volcani, B.E.: 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 (1966).Google Scholar
44.Crawford, R.M., Schmid, A.M. Ultrastructure of silica deposition in diatoms, in Biomineralization in Lower Plants and Animals, edited by Leadbeater, B.S. and Riding, R. (The Systematics Society, London, UK, 1986), p. 291.Google Scholar
45.Crawford, S.A., Higgins, M.J., Mulvaney, P., Wetherbee, R.: Nanostructure of the diatom frustule as revealed by atomic force and scanning electron microscopy. J. Phycol. 37, 543 (2001).CrossRefGoogle Scholar
46.Hildebrand, M., Wetherbee, R. Components and control of silicification in diatoms, in Progress in Molecular and Subcellular Biology, Silicon Biomineralization, edited by Muller, W.E.G. (Springer-Verlag, Heidelberg, Germany, 2003), p. 11.Google Scholar
47.Noll, F., Sumper, M., Hampp, N.: Nanostructure of diatom silica surfaces and of biomimetic analogues. Nano Lett. 2, 91 (2002).CrossRefGoogle Scholar
48.Schmid, A-M., Schulz, D.: Wall morphogenesis in diatoms: Deposition of silica by cytoplasmic vesicles. Protoplasma 100, 267 (1979).CrossRefGoogle Scholar
49.Schmid, A-M.M., Volcani, B.E.: Wall morphogenesis in Coscinodiscus wailesii. I. Valve morphology and development of its architecture. J. Phycol. 19, 387 (1983).Google Scholar
50.Schnepf, E., Deichgräber, G., Drebes, G.: Morphogenetic processes in Attheya decora. Pl. Syst. Evol. 135, 265 (1980).CrossRefGoogle Scholar
51.Li, C-W., Volcani, B.E.: Studies on the biochemistry and fine structure of silica shell formation in diatoms. VIII. Morphogenesis of the cell wall in a centric diatom, Ditylum brightwellii. Protoplasma 124, 10 (1985).CrossRefGoogle Scholar
52.van Meene, A.M.L. de, Pickett-Heaps, J.D.: Valve morphogenesis in the centric diatom Proboscia alata Sundstrom. J. Phycol. 38, 351 (2002).Google Scholar
53.Zaslavskaia, L.A., Lippmeier, J.C., Kroth, P.G., Grossman, A.R., Apt, K.E.: Transformation of the diatom Phaeodactylum tricornutum with a variety of selectable marker and reporter genes. J. Phycol. 36, 379 (2000).CrossRefGoogle Scholar
54.Schmid, A-M.M.: Valve morphogenesis in diatoms: A pattern-related filamentous system in pennates and the effect of APM, colchicine, and osmotic pressure. Nova Hedwiga. 33, 811 (1980).Google Scholar
55.Poulsen, N., Sumper, M., Kröger, N.: Biosilica formation in diatoms: Characterization of native silaffin-2 and its role in silica morphogenesis. Proc. Natl. Acad. Sci. USA 100, 12075 (2003).Google Scholar
56.Zimmerberg, J., Kozlov, M.M. How proteins produce cellular membrane curvature. Nature Rev. Mol. Cell. Biol. AOP Nov. 2005; DOI:10.1038/nrm1784, 1 (2005).Google Scholar