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Analytical studies on the incorporation of aluminium in the cell walls of the marine diatom Stephanopyxis turris

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Abstract

The eukaryotic diatoms are unicellular algae. They are well known for their filigree micro- and nanostructured cell walls which mainly consist of amorphous silica as well as various organic compounds. However, diatoms are also known to incorporate certain amounts of aluminium into their cell walls. Unexpectedly, enhanced Al concentrations in the Southern Yellow Sea were found to be correlated with a diatom spring bloom. Therefore, we have analyzed the influence of strongly enhanced Al concentrations in the culture medium upon the growth behaviour of the diatom Stephanopyxis turris (S. turris). The uptake and incorporation of Al into the cell walls was monitored. It turned out that S. turris survives aluminium concentrations up to 105.5 μM (2.85 mg/l) in the culture medium. Under the applied conditions, this corresponds to an Al/Si ratio of 1:1. These large amounts of Al had to be offered in the form of bis–tris-chelates in order to prevent uncontrolled precipitation. Under these conditions, the Al/Si ratio in the cell walls could be increased up to about 1:15 as determined by ICP-OES, the highest amount of aluminium found in diatom cell walls yet. Structural characterization of the biosilica by ATR-FTIR and solid-state 27Al NMR spectroscopy revealed that an amorphous aluminosilicate phase is formed where the aluminium exists as four- and sixfold-coordinated species.

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References

  • Azam F, Hemmingsen BB, Volcani BE (1973) Germanium incorporation into the silica of diatom cell walls. Arch Mikrobiol 92:11–20

    Article  CAS  Google Scholar 

  • Beck L, Gehlen M, Flank A-M, Van Bennekom AJ, Van Beusekom JEE (2002) The relationship between Al and Si in biogenic silica as determined by PIXE and XAS. Nucl Instr Methods Phys Res B 189:180–184

    Article  CAS  Google Scholar 

  • Beyer HK, Belenykaja IM, Hange F, Tielen M, Grobet PJ, Jocobs PA (1985) Preparation of high-silica faujasites by treatment with silicon tetrachloride. J Chem Soc 1(81):2889–2901

    Google Scholar 

  • Brunner E, Richthammer P, Ehrlich H, Paasch S, Simon P, Ueberlein S, van Pée K-H (2009a) Chitin-based organic networks: an integral part of cell wall biosilica in the diatom thalassiosira pseudonana. Angew Chem Int Edit 48(51):9724–9727

    Article  CAS  Google Scholar 

  • Brunner E, Gröger C, Lutz K, Richthammer P, Spinde K, Sumper M (2009b) Analytical studies of silica biomineralization: towards an understanding of silica processing by diatoms. Appl Microbiol Biotechnol 84(4):607–616

    Article  PubMed  CAS  Google Scholar 

  • Chester AW, Derouane EG (eds) (2009) Zeolite characterization and catalysis—a tutorial. Springer, Heidelberg

    Google Scholar 

  • Chiappino ML, Azam F, Volcani BE (1977) Effect of germanic acid on developing cell walls of diatoms. Protoplasma 93:191–204

    Article  CAS  Google Scholar 

  • Chiovitti A, Harper RE, Willis A, Bacic A, Mulvaney P, Wetherbee R (2005) Variations in the substituted 3-linked mannans closely associated with the silicified walls of diatoms. J Phycol 41:1154–1161

    Article  CAS  Google Scholar 

  • Chou L, Wollast R (1997) Biogeochemical behavior and mass balance of dissolved aluminium in the western Mediterranean Sea. Deep-Sea Res Part II 44:741–768

    Article  CAS  Google Scholar 

  • Davis AK, Hildebrand M (2008) A self-propagating system for Ge incorporation into nanostructured silica. Chem Commun 37:4495–4497

    Article  Google Scholar 

  • Dixit S, van Cappellen P, van Bennekom AJ (2001) Processes controlling solubility of biogenic silica and pore water build-up of silicic acid in marine sediments. Mar Chem 73:333–352

    Article  CAS  Google Scholar 

  • Driscoll CT, Schecher WD (1990) The chemistry of aluminum in the environment. Environ Geochem Health 12(1–2):28–49

    Article  CAS  Google Scholar 

  • Ehrlich H, Simon P, Carrillo-Cabrera W, Bazhenov VV, Botting JP, Ilan M, Ereskovsky AV, Muricy G, Worch H, Mensch A, Born R, Springer A, Kummer K, Vyalikh DV, Molodtsov SL, Kurek D, Kammer M, Paasch S, Brunner E (2010) Insights into chemistry of biological materials: newly discovered silica-aragonite-chitin biocomposites in demosponges. Chem Mater 22(4):1462–1471

    Article  CAS  Google Scholar 

  • Ellwood MJ, Hunter KA (1999) Determination of the Zn/Si ratio in diatom opal: a method for the separation, cleaning and dissolution of diatoms. Mar Chem 66:149–160

    Article  CAS  Google Scholar 

  • Ellwood MJ, Hunter KA (2000) The incorporation of zinc and iron into the frustules of the marine diatom Thalassiosira pseudonana. Limnol Oceanogr 45(7):1517–1524

    Article  CAS  Google Scholar 

  • Falasco E, Bona F, Ginepro M, Hlúbikova D, Hoffmann L, Ector L (2009) Morphological abnormalities of diatom silica wall in relation to heavy metal contamination and artificial growth conditions. Water SA 35:595–606

    Article  CAS  Google Scholar 

  • Fung BM, Khitrin AK, Ermolaev K (2000) An improved broadband decoupling sequence for liquid crystals and solids. Magn Reson 142(1):97–101

    Article  CAS  Google Scholar 

  • Gal A, Hirsch A, Siegel S, Li C, Aichmayer B, Politi Y, Fratzl P, Weiner S, Addadi L (2012) Plant cystoliths: a complex functional biocomposite of four distinct silica and amorphous calcium carbonate phases. Chem Eur J 33:10262–10270

    Article  Google Scholar 

  • Gehlen M, Beck L, Calas G, Flank A-M, van Bennekom AJ, van Beusekom JEE (2002) Unraveling the atomic structure of biogenic silica: evidence of the structural association of Al and Si in diatom frustules. Geochim Cosmochim Acta 66(9):1601–1609

    Article  CAS  Google Scholar 

  • Harrison PJ, Waters RE, Taylor FJR (1980) A broad spectrum artificial sea water medium for coastal and open ocean phytoplankton. J Phycol 16:28–35

    Google Scholar 

  • Heredia A, Figueira E, Rodrigues CT, Rodríguez-Galván A, Basiuk VA, Vrieling EG, Almeida SFP (2012) Cd2+ affects the growth, hierarchical structure and peptide composition of the biosilica of the freshwater diatom Nitzschia palea (Kützing) W Smith. Phycol Res 60:229–240

    Article  CAS  Google Scholar 

  • Hydes DJ, de Lange GJ, de Baar HJW (1988) Dissolved aluminium in the Mediterranean. Geochim Cosmochim Acta 52:2107–2114

    Article  CAS  Google Scholar 

  • Iler RK (1979) The chemistry of silica. Wiley, New York

    Google Scholar 

  • Jaccard T, Ariztegui D, Wilkinson KJ (2009) Incorporation of zinc into the frustules of the freshwater diatom Stephanodiscus hantzschii. Chem Geol 265:381–386

    Article  CAS  Google Scholar 

  • Jeffryes C, Gutu T, Jiao J, Rorrer L (2008a) Two-stage photobioreactor process for the metabolic insertion of nanostructured germanium into the silica microstructure of the diatom Pinnularia sp. Biomimetic Supramol Syst 28(1):107–118

    Article  CAS  Google Scholar 

  • Jeffryes C, Gutu T, Jiao J, Rorrer L (2008b) metabolic insertion of nanostructered TiO2 into the patterned biosilica of the diatom pinnularia sp. by a two-stage bioreactor cultivation process. ACS Nano 2(10):2103–2112

    Article  PubMed  CAS  Google Scholar 

  • Kröger N, Poulsen N (2008) Diatoms—from cell wall biogenesis to nanotechnology. Annu Rev Genet 42:83–107

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Kubelková L, Seidl V, Borbély G, Beyer HK (1988) Correlations between wavenumbers of skeletal vibrations, unit-cell size and molar fraction of aluminium of Y zeolites. J Chem SOC Faraday Trans 1 84(5):1447–1454

    Google Scholar 

  • MacKenzie KJD, Smith ME (2008) Multinuclear solid-state NMR of inorganic materials. Pergamon, Oxford

    Google Scholar 

  • Marchetti A, Cassar N (2009) Diatom elemental and morphological changes in response to iron limitation: a brief review with potential paleoceanographic applications. Geobiology 7:419–431

    Article  PubMed  CAS  Google Scholar 

  • Martinez JR, Ruiz F, Vorobiev YV, Perez-Robles F, Gonzalez-Hernandez J (1998) Infrared spectroscopy analysis of the local atomic structure in silica prepared by sol-gel. J Chem Phys 109:7511–7514

    Article  CAS  Google Scholar 

  • Measures CI, Brown ET (1996) Estimating dust input to the Atlantic Ocean using surface water aluminium concentrations. In: Guerzoni S, Chester R (eds) The impact of desert dust across the Mediterranean. Kluwer, Dordrecht

    Google Scholar 

  • Measures CI, Edmond JM (1990) Aluminium in the South Atlantic: steady state distribution of a short residence time element. J Geophys Res 95:5331–5340

    Article  CAS  Google Scholar 

  • Mugnaioli E, Natalio F, Schloßmacher U, Wang X, Müller WEG, Kolb U (2009) Crystalline nanorods as possible templates for the synthesis of amorphous biosilica during spicule formation. ChemBioChem 10:683–689

    Article  PubMed  CAS  Google Scholar 

  • Qin T, Gutu T, Jiao J, Chang C-H, Rorrer GL (2008) Biological fabrication of photoluminescent nanocomb structures by metabolic incorporation of germanium into the biosilica of the diatom Nitzschia frustulum. ACS Nano 2(6):1296–1304

    Article  PubMed  CAS  Google Scholar 

  • Ren J-L, Zhang G-L, Zhang J, Shi J-H, Liu S-M, Li F-M, Jin J, Liu C-G (2011) Distribution of dissolved aluminium in the Southern Yellow Sea: influences of a dust storm and the spring bloom. Mar Chem 125:69–81

    Article  CAS  Google Scholar 

  • Rorrer GL, Chang C-H, Liu S-H, Jeffryes C, Jiao J, Hedberg JA (2005) Biosynthesis of silicon-germanium oxide nanocomposites by the marine diatom Nitzschia frustulum. J Nanosci Nanotechnol 5(1):41–49

    Article  PubMed  CAS  Google Scholar 

  • Round FE, Crawford RM, Mann DG (1990) The diatoms. Cambridge University Press, Cambridge

    Google Scholar 

  • Sumper M, Brunner E (2006) Learning from Diatoms: nature’s tools for the production of nanostructured silica. Adv Funct Mater 16:17–26

    Article  CAS  Google Scholar 

  • Sumper M, Brunner E (2008) Silica biomineralisation in diatoms: the model organism Thalassiosira pseudonana. ChemBioChem 9:1187–1194

    Article  PubMed  CAS  Google Scholar 

  • van Bennekom AJ, Buma AGJ, Nolting RF (1991) Dissolved aluminium in the Weddell-Scotia confluence and effect of Al on the dissolution kinetics of biogenic silica. Mar Chem 35:423–434

    Article  Google Scholar 

  • van Beusekom JEE, Weber A (1995) Der einfluß von aluminium auf das wachstum und die entwicklung von kieselalgen in der nordsee. Deutsche hydrographische Z Suppl 5:213–220

    Google Scholar 

  • 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 Engl 47:1729–1732

    Article  PubMed  CAS  Google Scholar 

  • Wesolowski DJ, Palmer DA, Begun GM (1990) Complexation of aluminate anion by bis–tris in aqueous media at 25–50°C. J Solut Chem 19:159–173

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Financial support from the Deutsche Forschungsgemeinschaft (Br 1278/12 and Br 1278/17-1) and the Fonds der Chemischen Industrie is gratefully acknowledged.

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Authors and Affiliations

  1. Bioanalytical Chemistry, Dresden University of Technology, 01062, Dresden, Germany

    Susanne Machill, Lydia Köhler, Susanne Ueberlein, René Hedrich, Marco Kunaschk, Silvia Paasch, Renate Schulze & Eike Brunner

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  1. Susanne Machill
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  2. Lydia Köhler
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  3. Susanne Ueberlein
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  4. René Hedrich
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  8. Eike Brunner
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Correspondence to Eike Brunner.

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Susanne Machill, Lydia Köhler and Susanne Ueberlein contributed equally to this study.

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Machill, S., Köhler, L., Ueberlein, S. et al. Analytical studies on the incorporation of aluminium in the cell walls of the marine diatom Stephanopyxis turris . Biometals 26, 141–150 (2013). https://doi.org/10.1007/s10534-012-9601-3

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  • DOI: https://doi.org/10.1007/s10534-012-9601-3

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