Diverse and conserved nano‐ and mesoscale structures of diatom silica revealed by atomic force microscopy

An outstanding example of biological pattern formation at the single cell level is the diversity of biomineral structures in the silica cell walls of the unicellular eukaryotic algae known as diatoms. We present a survey of cell wall silica structures of 16 diatom species, which included all major cell wall components (valves, girdle bands and setae), imaged across the nano‐, meso‐ and microscales using atomic force microscopy. Because of atomic force microscopy's superior ability to image surface topology, this approach enabled visualization of the organization of possible underlying organic molecules involved in mineral structure formation. Diatom nanoscale silica structure varied greatly comparing the same feature in different species and different features within a single species, and frequently on different faces of the same object. These data indicate that there is not a strict relation between nanoscale silica morphology and the type of structure that contains it. On the mesoscale, there was a preponderance of linear structures regardless of the object imaged, suggesting that assembly or organization of linear organic molecules or subcellular assemblies that confine a linear space play an essential and conserved role in structure formation on that scale. Microscale structure imparted an overall influence over nano‐ and mesoscale structure, indicating that shaping of the silica deposition vesicle plays a key role in structure formation. These results provide insights into the design and assembly principles involved in diatom silica structure formation, facilitating an understanding of the native system and potentially aiding in development of biomimetic approaches.

[1]  F. Azam,et al.  Effect of germanic acid on developing cell walls of diatoms , 1977, Protoplasma.

[2]  Christopher S. Gaddis,et al.  Merging Biological Self-Assembly with Synthetic Chemical Tailoring: The Potential for 3-D Genetically Engineered Micro/Nano-Devices (3-D GEMS) , 2005 .

[3]  D. H. Robinson,et al.  How do diatoms make silicon biominerals , 1987 .

[4]  B. Volcani,et al.  Studies on the biochemistry and fine structure of silicia shell formation in diatoms VII. Sequential cell wall development in the pennateNavicula pelliculosa , 1977, Protoplasma.

[5]  N. Kröger,et al.  Species-specific polyamines from diatoms control silica morphology. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[6]  Richard Gordon,et al.  The chemical basis of diatom morphogenesis , 1994 .

[7]  D. M. Porterfield,et al.  Calcification and measurements of net proton and oxygen flux reveal subcellular domains in Acetabularia acetabulum , 2000, Planta.

[8]  R. Naik,et al.  Study of the chemical and physical influences upon in vitro peptide-mediated silica formation. , 2004, Biomacromolecules.

[9]  P. Mulvaney,et al.  THE STRUCTURE AND NANOMECHANICAL PROPERTIES OF THE ADHESIVE MUCILAGE THAT MEDIATES DIATOM‐SUBSTRATUM ADHESION AND MOTILITY 1 , 2003 .

[10]  M. Hildebrand,et al.  SYNCHRONIZED GROWTH OF THALASSIOSIRA PSEUDONANA (BACILLARIOPHYCEAE) PROVIDES NOVEL INSIGHTS INTO CELL‐WALL SYNTHESIS PROCESSES IN RELATION TO THE CELL CYCLE 1 , 2007 .

[11]  David G. Mann,et al.  Diatoms: Biology and Morphology of the Genera , 1990 .

[12]  M. Sumper,et al.  A Phase Separation Model for the Nanopatterning of Diatom Biosilica , 2002, Science.

[13]  Ruijin Huang,et al.  Segmentation of the vertebrate body , 1997, Anatomy and Embryology.

[14]  M. Sumper,et al.  Silacidins: highly acidic phosphopeptides from diatom shells assist in silica precipitation in vitro. , 2008, Angewandte Chemie.

[15]  J. Leftley,et al.  The first record of Nitzschia alba from UK coastal waters with notes on its growth potential , 2000, Journal of the Marine Biological Association of the United Kingdom.

[16]  W. Darley,et al.  Studies on the biochemistry and fine structure of silica shell formation in diatoms , 2004, Planta.

[17]  N. Kröger,et al.  Polycationic peptides from diatom biosilica that direct silica nanosphere formation. , 1999, Science.

[18]  H. Plattner,et al.  My favorite cell--Paramecium. , 2002, BioEssays : news and reviews in molecular, cellular and developmental biology.

[19]  Nicole Poulsen,et al.  Silica Morphogenesis by Alternative Processing of Silaffins in the Diatom Thalassiosira pseudonana* , 2004, Journal of Biological Chemistry.

[20]  P K Hansma,et al.  Micromechanical and structural properties of a pennate diatom investigated by atomic force microscopy , 2001, Journal of microscopy.

[21]  B. Volcani,et al.  Studies on the biochemistry and fine structure of silica shell formation in diatoms , 2004, Archiv für Mikrobiologie.

[22]  K. Pyke Tansley Review No. 75 Arabidopsis- its use in the genetic and molecular analysis of plant morphogenesis. , 1994, The New phytologist.

[23]  T. Schultz,et al.  Diatom gliding is the result of an actin-myosin motility system. , 1999, Cell motility and the cytoskeleton.

[24]  Nicolas H Voelcker,et al.  AFM nanoindentations of diatom biosilica surfaces. , 2007, Langmuir : the ACS journal of surfaces and colloids.

[25]  Eileen J. Cox,et al.  VARIATION IN PATTERNS OF VALVE MORPHOGENESIS BETWEEN REPRESENTATIVES OF SIX BIRAPHID DIATOM GENERA (BACILLARIOPHYCEAE) , 1999 .

[26]  Paul Mulvaney,et al.  NANOSTRUCTURE OF THE DIATOM FRUSTULE AS REVEALED BY ATOMIC FORCE AND SCANNING ELECTRON MICROSCOPY , 2001 .

[27]  N. Hampp,et al.  Nanostructure of Diatom Silica Surfaces and of Biomimetic Analogues , 2002 .

[28]  G. Fryxell CHAIN‐FORMING DIATOMS: THREE SPECIES OF CHAETOCERACEAE 1, 2 , 1978 .

[29]  M. Hildebrand,et al.  Application of AFM in understanding biomineral formation in diatoms , 2008, Pflügers Archiv - European Journal of Physiology.

[30]  M. Marsh,et al.  Regulation of CaCO3 formation in coccolithophores , 2003 .

[31]  W. Darley,et al.  Role of silicon in diatom metabolism. A silicon requirement for deoxyribonucleic acid synthesis in the diatom Cylindrotheca fusiformis Reimann and Lewin. , 1969, Experimental cell research.

[32]  M J Doktycz,et al.  AFM imaging of bacteria in liquid media immobilized on gelatin coated mica surfaces. , 2003, Ultramicroscopy.

[33]  A. Mcinnes,et al.  GROWTH RATES AND ULTRASTRUCTURE OF SILICEOUS SETAE OF CHAETOCEROS GRACILIS (BACILLARIOPHYCEAE) 1 2 , 1986 .

[34]  G. Stucky,et al.  Silicatein alpha: cathepsin L-like protein in sponge biosilica. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[35]  A. Schmid,et al.  Wall morphogenesis in diatoms: Deposition of silica by cytoplasmic vesicles , 1979, Protoplasma.

[36]  J. Pickett-Heaps,et al.  VALVE MORPHOGENESIS IN THE CENTRIC DIATOM PROBOSCIA ALATA SUNDSTROM1 , 2002 .

[37]  S. Lorenz,et al.  Self-Assembly of Highly Phosphorylated Silaffins and Their Function in Biosilica Morphogenesis , 2002, Science.

[38]  G. Stucky,et al.  Silicatein α: Cathepsin L-like protein in sponge biosilica , 1998 .

[39]  Jessica I. Kelz,et al.  Nanoscale control of silica morphology and three-dimensional structure during diatom cell wall formation , 2006 .

[40]  David G. Mann,et al.  The species concept in diatoms , 1999 .

[41]  B. Volcani,et al.  STUDIES ON THE BIOCHEMISTRY AND FINE STRUCTURE OF SILICA SHELL FORMATION IN DIATOMS. II. THE STRUCTURE OF THE CELL WALL OF NAVICULA PELLICULOSA (BRÉB.) HILSE , 1966, Journal of phycology.

[42]  Daniel J Müller,et al.  Imaging and manipulation of biological structures with the AFM. , 2002, Micron.

[43]  M. Hildebrand,et al.  Molecular Processes of Biosilicification in Diatoms , 2010 .

[44]  H. Pankratz,et al.  POST MITOTIC FINE STRUCTURE OF GOMPHONEMA PARVULUM. , 1964, Journal of ultrastructure research.

[45]  B. Volcani,et al.  WALL MORPHOGENESIS IN COSCINODISCUS WAILESII GRAN AND ANGST. I. VALVE MORPHOLOGY AND DEVELOPMENT OF ITS ARCHITECTURE 1 , 1983 .