Abstract
The internal nanostructure of the diatoms Cyclotella meneghiniana, Seminavis robusta and Achnanthes subsessilis was investigated using small angle neutron scattering (SANS) to examine thin biosilica samples, consisting of isotropic (powder) from their isolated cell walls. The interpretation of SANS data was assisted by several other measurements. The N2 adsorption, interpreted within the Branuer–Emmet–Teller isotherm, yielded the specific surface area of the material. Fourier transform infrared (FTIR) and Raman spectroscopy indicates that the isolated material is amorphous silica with small amounts of organic cell wall materials acting as a filling material between the silica particles. A two-phase (air and amorphous silica) model was used to interpret small angle neutron scattering data. After correction for instrumental resolution, the measurements on two SANS instruments covered an extended range of scattering vectors 0.0011 nm−1 < q < 5.6 nm−1, giving an almost continuous SANS curve over a range of scattering vectors, q, on an absolute scale of intensity for each sample. Each of the samples gave a characteristic scattering curve where log (intensity) versus log (q) has a −4 dependence, with other features superimposed. In the high-q regime, departure from this behaviour was observed at a length-scales equivalent to the proposed unitary silica particle. The limiting Porod scattering law was used to determine the specific area per unit of volume of each sample illuminated by the neutron beam. The Porod behaviour, and divergence from this behaviour, is discussed in terms of various structural features and the proposed mechanisms for the bio-assembly of unitary silica particles in frustules.
Similar content being viewed by others
References
Brunauer S, Copeland LE, Kantro DL (1967) The Langmuir and BET theories. In: Flood EA (ed) The solid–gas interface, vol 1. M. Dekker, New York, pp 77–104
Cannell D, Aubert C (1986) Aggregation of colloidal silica. In: Stanley HE, Ostrowsky N (eds) On growth and form: fractal and non-fractal patterns in physics. M. Nijhoff, The Hague, pp 145–162
Drum RW, Pankratz HS (1964) Post mitotic fine structure of Gomphonema parvulum. J Ultrastruct Res 10(3–4):217–223. doi:10.1016/s0022-5320(64)80006-x
Fröhlich F (1989) Deep-sea biogenic silica: new structural and analytical data from infrared analysis—geological implications. Terra Nova 1(3):267–273. doi:10.1111/j.1365-3121.1989.tb00368.x
Gendron-Badou A, Coradin T, Maquet J, Fröhlich F, Livage J (2003) Spectroscopic characterization of biogenic silica. J Non Cryst Solids 316(2–3):331–337. doi:10.1016/s0022-3093(02)01634-4
Giordano M, Kansiz M, Heraud P, Beardall J, Wood B, McNaughton D (2001) Fourier transform infrared spectroscopy as a novel tool to investigate changes in intracellular macromolecular pools in the marine microalga chaetoceros muellerii (Bacillariophyceae). J Phycol 37(2):271–279. doi:10.1046/j.1529-8817.2001.037002271.x
Gordon R, Drum RW (1994) The chemical basis of diatom morphogenesis. In: Richard G (ed) International review of cytology, vol 150. Academic Press, pp 243–372. doi:10.1016/s0074-7696(08)61544-2
Gordon R, Sterrenburg FAS, Sandhage KH (2005) A special issue on diatom nanotechnology. J Nanosci Nanotechnol 5(1):1–4. doi:10.1166/jnn.2005.017
Higgins MJ, Sader JE, Mulvaney P, Wetherbee R (2003) Probing the surface of living diatoms with atomic force microscopy: the nanostructure and nanomechanical properties of the mucilage layer. J Phycol 39(4):722–734. doi:10.1046/j.1529-8817.2003.02163.x
Hill TL (1960) An introduction to statistical thermodynamics. Dover Publications, New York
Iler RK (1979) The chemistry of silica: solubility, polymerization, colloid and surface properties, and biochemistry. Wiley, New York
Israelachvili JN (2010) Intermolecular and surface forces. Academic Press, New York
Kammer M, Hedrich R, Ehrlich H, Popp J, Brunner E, Krafft C (2010) Spatially resolved determination of the structure and composition of diatom cell walls by Raman and FTIR imaging. Anal Bioanal Chem 398(1):509–517. doi:10.1007/s00216-010-3924-0
Keiderling U (2002) The new ‘BerSANS-PC’ software for reduction and treatment of small angle neutron scattering data. Appl Phys A Mater Sci Process 74:s1455–s1457. doi:10.1007/s003390201561
Keiderling U, Wiedenmann A (1995) New SANS instrument at the BER II reactor in Berlin, Germany. Phys B Condens Matter 213–214:895–897. doi:10.1016/0921-4526(95)00316-2
Kröger N, Lorenz S, Brunner E, Sumper M (2002) Self-assembly of highly phosphorylated silaffins and their function in biosilica morphogenesis. Science 298(5593):584–586
Lindner P (2004) Scattering experiments: experimental aspects, initial data reduction and absolute calibration. In: Lindner P, Zemb T (eds) Neutrons, X-rays, and light: scattering methods applied to soft condensed matter. Elsevier, Amsterdam, pp 23–48
Pedersen JS, Posselt D, Mortensen K (1990) Analytical treatment of the resolution function for small-angle scattering. J Appl Crystallogr 23(4):321–333. doi:10.1107/s0021889890003946
Perry CC (1989) Chemical studies of biogenic silica. In: Mann S, Webb J, Williams RJP (eds) Biomineralization: chemical and biochemical perspectives. VCH, New York
Pickett-Heaps J, Schmid A-M, Edgar L (1990) The cell biology of diatom valve formation. In: Round FE, Chapman DJ (eds) Progress in phycological research, vol 7. Elsevier Biomedical Press, North Holland, pp 1–168
Porod G (1951) Die Röntgenkleinwinkelstreuung von dichtgepackten kolloiden Systemen. Colloid Polym Sci 124(2):83–114. doi:10.1007/bf01512792
Porod G (1952) Die Röntgenkleinwinkelstreuung von dichtgepackten kolloiden Systemen. II. Teil. Colloid Polym Sci 125(2):108–122. doi:10.1007/bf01526289
Round FE, Crawford RM, Mann DG (1990) The diatoms: biology & morphology of the genera. Cambridge University Press, Cambridge
Sabbe K, Chepurnov VA, Vyverman W, Mann DG (2004) Apomixis in Achnanthes (Bacillariophyceae); development of a model system for diatom reproductive biology. Eur J Phycol 39(3):327–341. doi:10.1080/0967026042000236445
Šaroun J (2000) Evaluation of double-crystal SANS data influenced by multiple scattering. J Appl Crystallogr 33(3–1):824–828. doi:10.1107/s0021889899013370
Scheffel A, Poulsen N, Shian S, Kroger N (2011) Nanopatterned protein microrings from a diatom that direct silica morphogenesis. Proc Natl Acad Sci USA 108(8):3175–3180. doi:10.1073/pnas.1012842108
Schmidt PW, Hight R Jr (1960) Slit height corrections in small angle X-ray scattering. Acta Crystallogr A 13(6):480–483. doi:10.1107/S0365110X60001138
Sears VF (1992) Neutron scattering lengths and cross sections. Neutron News 3(3):26–37. doi:10.1080/10448639208218770
Sinha SK, Sirota EB, Garoff S, Stanley HB (1988) X-ray and neutron scattering from rough surfaces. Phys Rev B 38(4):2297–2311
Spalla O (2004) General theorems in small-angle scattering. In: Lindner P, Zemb T (eds) Neutrons, X-rays, and light: scattering methods applied to soft condensed matter. Elsevier, Amsterdam, pp 49–71
Spooner S, Hastings JB (1976) Small angle neutron scattering from glassy SiO2. J Non Cryst Solids 22(2):443–445. doi:10.1016/0022-3093(76)90072-7
Strobl M, Treimer W, Hilger A (2006) Scattering-related contrast signals in neutron computerized tomography and the new V12 instrument at HMI Berlin. Phys B Condens Matter 385–386(2):1209–1212. doi:10.1016/j.physb.2006.05.423
Strobl M, Treimer W, Ritzoulis C, Wagh AG, Abbas S, Manke I (2007) The new V12 ultra-small-angle neutron scattering and tomography instrument at the Hahn-Meitner Institute. J Appl Crystallogr 40(s1):s463–s465. doi:10.1107/S0021889806050813
Sumper M (2002) A phase separation model for the nanopatterning of diatom biosilica. Science 295(5564):2430–2433
Teixeira J (1988) Small-angle scattering by fractal systems. J Appl Crystallogr 21:781–785. doi:10.1107/s0021889888000263
Tesson B, Hildebrand M (2010) Dynamics of silica cell wall morphogenesis in the diatom Cyclotella cryptica: substructure formation and the role of microfilaments. J Struct Biol 169(1):62–74. doi:10.1016/j.jsb.2009.08.013
Tesson B, Masse S, Laurent G, Maquet J, Livage J, Martin-Jézéquel V, Coradin T (2008) Contribution of multi-nuclear solid state NMR to the characterization of the Thalassiosira pseudonana diatom cell wall. Anal Bioanal Chem 390(7):1889–1898. doi:10.1007/s00216-008-1908-0
Vrieling EG, Beelen TPM, Van Santen RA, Gieskes WWC (2000) Nanoscale uniformity of pore architecture in diatomaceous silica: a combined small and wide angle X-ray scattering study. J Phycol 36(1):146–159. doi:10.1046/j.1529-8817.2000.99120.x
Vrieling EG, Beelen TPM, Sun Q, Hazelaar S, van Santen RA, Gieskes WWC (2004) Ultrasmall, small, and wide angle X-ray scattering analysis of diatom biosilica: interspecific differences in fractal properties. J Mater Chem 14(13):1970–1975
Wenzl S, Hett R, Richthammer P, Sumper M (2008) Silacidins: highly acidic phosphopeptides from diatom shells assist in silica precipitation in vitro. Angew Chem Int Ed 47(9):1729–1732. doi:10.1002/anie.200704994
Witten TA Jr, Sander LM (1981) Diffusion-limited aggregation, a kinetic critical phenomenon. Phys Rev Lett 47(19):1400–1403
Witten TA, Sander LM (1983) Diffusion-limited aggregation. Phys Rev B 27(9):5686–5697
Acknowledgments
The authors would like to acknowledge the following for their assistance: Dr. Robert Knott for comments on the manuscript; the Australian Governments Access to Major Research Facilities Program; and the Berlin Neutron Scattering Center at the Hahn-Meitner Institute. Establishment, maintenance and development of the culture collection have become possible thanks to integrated support provided by the BCCM program C3/00/14 and the BOF-project GOA 12050398 (Ghent University, Belgium).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Garvey, C.J., Strobl, M., Percot, A. et al. Small angle neutron scattering on an absolute intensity scale and the internal surface of diatom frustules from three species of differing morphologies. Eur Biophys J 42, 395–404 (2013). https://doi.org/10.1007/s00249-013-0889-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00249-013-0889-x