Skip to main content
SpringerLink
Log in

Iron incorporation in biosilica of the marine diatom Stephanopyxis turris: dispersed or clustered?

  • Published:
BioMetals Aims and scope Submit manuscript

Abstract

Iron incorporation into diatom biosilica was investigated for the species Stephanopyxis turris. It is known that several “foreign” elements (e.g., germanium, titanium, aluminum, zinc, iron) can be incorporated into the siliceous cell walls of diatoms in addition to silicon dioxide (SiO2). In order to examine the amount and form of iron incorporation, the iron content in the growth medium was varied during cultivation. Fe:Si ratios of isolated cell walls were measured by ICP-OES. SEM studies were performed to examine of a possible influence of excess iron during diatom growth upon cell wall formation. The chemical state of biosilica-attached iron was characterized by a combination of infrared, 29Si MAS NMR, and EPR spectroscopy. For comparison, synthetic silicagels of variable iron content were studied. Our investigations show that iron incorporation in biosilica is limited. More than 95% of biosilica-attached iron is found in the form of iron clusters/nanoparticles. In contrast, iron is preferentially dispersedly incorporated within the silica framework in synthetic silicagels leading to Si–O–Fe bond formation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aguiar H, Serra J, González P, León B (2009) Structural study of sol-gel silicate glasses by IR and Raman spectroscopies. J Non Cryst Solids 355:475–480

    Article  CAS  Google Scholar 

  • Allen AE, LaRoche J, Maheswari U et al (2008) Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc Natl Acad Sci USA 105:10438–10443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arieli D, Vaughan DEW, Strohmaier KG et al (1999) Studies of Fe(III) incorporated into AlPO4-20 by X- and W-band EPR spectroscopies. Magn Reson Chem 37:43–54

    Article  Google Scholar 

  • Armbrust EV (2009) The life of diatoms in the world’ s oceans. Nature 459:185–192

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Baumann H (1959) Polymerisation und depolymerisation der Kieselsäure unter verschiedenen Bedingungen. Kolloid-Zeitschrift 162:28–35

    Article  CAS  Google Scholar 

  • Böttger LH, Miller EP, Andresen C et al (2012) Atypical iron storage in marine brown algae: a multidisciplinary study of iron transport and storage in Ectocarpus siliculosus. J Exp Bot 63:5763–5772

    Article  PubMed  PubMed Central  Google Scholar 

  • Clapsaddle BJ, Gash AE, Satcher JH, Simpson RL (2003) Silicon oxide in an iron(III) oxide matrix: the sol-gel synthesis and characterization of Fe-Si mixed oxide nanocomposites that contain iron oxide as the major phase. J Non Cryst Solids 331:190–201

    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 

  • De La Rocha CL, Hutchins D, Brzezinski M, Zhang Y (2000) Effects of iron and zinc deficiency on elemental composition and silica production by diatoms. Mar Ecol Prog Ser 195:71–79

    Article  Google Scholar 

  • Devadas M, Kröcher O, Elsener M et al (2007) Characterization and catalytic investigation of Fe-ZSM5 for urea-SCR. Catal Today 119:137–144

    Article  CAS  Google Scholar 

  • Doelsch E, Stone WEE, Petit S, Masion A (2001) Speciation and crystal chemistry of Fe(III) chloride hydrolyzed in the presence of SiO4 Ligands. 2. Characterization of Si–Fe Aggregates by FTIR and 29Si Solid-State NMR. Langmuir 17:1399–1405

    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 frustule of the marine diatom Thalassiosira pseudonana. Limnol Ocean 45:1517–1524

    Article  CAS  Google Scholar 

  • Engelhardt G, Michel D (1987) High-resolution solid-state NMR of silicates and zeolites. Wiley VCH, Chichester

    Google Scholar 

  • Ferretti AM, Forni L, Oliva C, Ponti A (2002) EPR study of iron-doped MFI zeolite and silicalite catalysts: effect of treatments after synthesis. Res Chem Intermed 28:101–116

    Article  CAS  Google Scholar 

  • Giordano M, Kansiz M, Heraud P et al (2001) Fourier Transform Infrared Spectroscopy as a novel tool to investigate changes in intracellular macromolecular pools in the marine microalga Chaetocerus muellerii (Bacilliariophyceae). J Phycol 37:271–279

    Article  CAS  Google Scholar 

  • Godinho RM, Cabrita T, Alves C, Pinheiro T (2014) Imaging of intracellular metal partitioning in marine diatoms exposed to metal pollution: consequences to cellular toxicity and metal fate in the environment. Metallomics 6:1626–1631

    Article  CAS  PubMed  Google Scholar 

  • Goldfarb D, Bernardo M, Strohmaier KG et al (1994) Characterization of iron in zeolites by X-band and Q-band Esr, pulsed ESR, and UV-Visible spectroscopies. J Am Chem Soc 116:6344–6353

    Article  CAS  Google Scholar 

  • Groussman RD, Parker MS, Armbrust EV (2015) Diversity and evolutionary history of iron metabolism genes in diatoms. PLoS ONE 10:e0129081

    Article  PubMed  PubMed Central  Google Scholar 

  • Harrison PJ, Waters RE, Taylor FJR (1980) A broad spectrum artificial seawater medium for coastal and open phytoplankton. Phycology 16:28–35

    Article  Google Scholar 

  • Hronský V, Rákoš M, Belák J et al (1978) EPR study of Mn2+ ions adsorption on silica gel. Czech J Phys B 28:1277–1286

    Article  Google Scholar 

  • Ingall ED, Diaz JM, Longo AF et al (2013) Role of biogenic silica in the removal of iron from the Antarctic seas. Nat Commun 4:1981–1984

    Article  PubMed  Google Scholar 

  • Innocenzi P (2003) Infrared spectroscopy of sol-gel derived silica-based films: A spectra-microstructure overview. J Non Cryst Solids 316:309–319

    Article  CAS  Google Scholar 

  • Jeffryes CS (2009) Biological insertion of nanostructured germanium and titanium oxide into diatom biosilica. Dissertation, Oregon State University

  • Jeffryes C, Gutu T, Jiao J, Rorrer GL (2008a) Metabolic insertion of nanostructured TiO2 into the patterned biosilica of the diatom Pinnularia sp. by a two-stage bioreactor cultivation process. ACS Nano 2:2103–2112

    Article  CAS  PubMed  Google Scholar 

  • Jeffryes C, Gutu T, Jiao J, Rorrer GL (2008b) Two-stage photobioreactor process for the metabolic insertion of nanostructured germanium into the silica microstructure of the diatom Pinnularia sp. Mater Sci Eng C 28:107–118

    Article  CAS  Google Scholar 

  • Jia Y, Han W, Xiong G, Yang W (2007) Diatomite as high performance and environmental friendly catalysts for phenol hydroxylation with H2O2. Sci Technol Adv Mater 8:106–109

    Article  CAS  Google Scholar 

  • Jitianu A, Crisan M, Meghea A et al (2002) Influence of the silica based matrix on the formation of iron oxide nanoparticles in the Fe2O3–SiO2 system, obtained by sol–gel method. J Mater Chem 12:1401–1407

    Article  CAS  Google Scholar 

  • Kröger N, Bergsdorf C (1994) A new calcium binding glycoprotein family constitutes a major diatom cell wall component. EMBO J 13:4676–4683

    PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Kubiak T, Krzyminiewski R, Dobosz B (2013) EPR study of paramagnetic centers in human blood. Curr Top Biophys 36:7–13

    Google Scholar 

  • Lang Y, del Monte F, Rodriguez BJ et al (2013) Integration of TiO2 into the diatom Thalassiosira weissflogii during frustule synthesis. Sci Rep 3:3205

    PubMed  PubMed Central  Google Scholar 

  • Leynaert A, Bucciarelli E, Claquin P (2004) Effect of iron deficiency on diatom cell size and silicic acid uptake kinetics. Limnol Ocean 49:1134–1143

    Article  CAS  Google Scholar 

  • Li B, Xu J, Liu J et al (2012) Preparation of mesoporous ferrisilicate with high content of framework iron by pH-modification method and its catalytic performance. J Colloid Interface Sci 366:114–119

    Article  CAS  PubMed  Google Scholar 

  • López T, Méndez J, Zamudio T, Villa M (1992) Spectroscopic study of sol-gel silica doped with iron ions. Mater Chem Phys 30:161–167

    Article  Google Scholar 

  • Machill S, Köhler L, Ueberlein S et al (2013) Analytical studies on the incorporation of aluminium in the cell walls of the marine diatom Stephanopyxis turris. Biometals 26:141–150

    Article  CAS  PubMed  Google Scholar 

  • Marchetti A, Parker MS, Moccia LP et al (2009) Ferritin is used for iron storage in bloom-forming marine pennate diatoms. Nature 457:467–470

    Article  CAS  PubMed  Google Scholar 

  • Mock T, Samanta MP, Iverson V et al (2008) Whole-genome expression profiling of the marine diatom Thalassiosira pseudonana identifies genes involved in silicon bioprocesses. PNAS 105:1579–1584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morrissey J, Bowler C (2012) Iron utilization in marine cyanobacteria and eukaryotic algae. Front Microbiol 3:1–13

    Article  Google Scholar 

  • Morrissey J, Sutak R, Paz-Yepes J et al (2015) A novel protein, ubiquitous in marine phytoplankton, concentrates iron at the cell surface and facilitates uptake. Curr Biol 25:364–371

    Article  CAS  PubMed  Google Scholar 

  • Nozaki C, Lugmair CG, Bell AT et al (2002) Synthesis, characterization, and catalytic performance of single-site Iron (III) centers on the surface of SBA-15 silica. Society 124:13194–13203

  • Nüster J, Vogt S, Twining BS (2012) Localization of iron within centric diatoms of the genus Thalassiosira. J Phycol 48:626–634

    Article  Google Scholar 

  • Piazzesi G, Nicosia D, Devadas M et al (2007) Investigation of HNCO adsorption and hydrolysis on Fe-ZSM5. Catal Lett 115:33–39

    Article  CAS  Google Scholar 

  • Qin T, Gutu T, Jiao J et al (2008) Biological fabrication of photoluminescent nanocomb structures by metabolic incorporation of germanium into the biosilica of the diatom Nitzschia frustulum. ACS Nano 2:1296–1304

    Article  CAS  PubMed  Google Scholar 

  • Raisewell R, Canfield DE (2012) The iron biogeochemical cycle past and present. Geochem Perspect 1(1):1–2

    Article  Google Scholar 

  • Raven JA (2013) Iron acquisition and allocation in stramenopile algae. J Exp Bot 64:2119–2127

    Article  CAS  PubMed  Google Scholar 

  • Round FE, Crawford RM, Mann DG (1990) The diatoms. Biology & morphology of the genera. Cambridge University Press, Cambridge

    Google Scholar 

  • Scheffel A, Poulsen N, Shian S, Kröger N (2011) Nanopatterned protein microrings from a diatom that direct silica morphogenesis. Proc Natl Acad Sci USA 108:3175–3180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schenkeveld WDC and Temminghoff EJM (2011) The effectiveness of FeEDDHA chelates in mending and preventing iron chlorosis in soil-grown soybean plants, soybean physiology and biochemistry. In: Hany El-Shemy (ed.). ISBN: 978-953-307-534-1, InTech

  • Scher M, Baker R (1982) Effect of Pseudomonas putida and synthetic iron chelator on induction of soil suppressiveness to Fusarium Wilt pathogens. Phytopathology 72:1567–1573

    Article  CAS  Google Scholar 

  • Schwertmann U (1976) The influence of [Fe(II)], [Si], and pH on the formation of lepidocrocite and ferrihydrate during oxidation of aqueous FeCl2 solution. Clay Miner 11:189–200

    Article  CAS  Google Scholar 

  • Sims P, Mann DG, Medlin LK (2006) Evolution of the diatoms: insights from fossil, biological and molecular data. Phycologia 45:361–402

    Article  Google Scholar 

  • Spinde K, Pachis K, Antonakaki I et al (2011) Influence of polyamines and related macromolecules on silicic acid polycondensation: relevance to “soluble silicon pools”? Chem Mater 23:4676–4687

    Article  CAS  Google Scholar 

  • Sutak R, Botebol H, Blaiseau PL et al (2012) A comparative study of iron uptake mechanisms in marine microalgae: iron binding at the cell surface is a critical step. Plant Physiol 160:2271–2284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vrieling EG, Gieskes WWC, Beelen TPM (1999) Silicon deposition in diatoms: control by the pH inside the silicon deposition vesicle. J Phycol 35:548–559

    Article  CAS  Google Scholar 

  • Zhang J, Goldfarb D (2000) Manganese incorporation into the mesoporous material MCM-41 under acidic conditions as studied by high field pulsed EPR and ENDOR spectroscopies. J Am Chem Soc 122:7034–7041

    Article  CAS  Google Scholar 

  • Zscherpel D, Brunner E, Koch M (1995) The influence of oxygen on the 1H MAS NMR spectra of H-ZSM-5 zeolites. Zeitschrift für Physikalische Chemie 190:123–127

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Renate Schulze for ICP-OES measurements and Susanne Goldberg for SEM micrographs. Financial support from Deutsche Forschungsgemeinschaft (BR 1278/22-1) is gratefully acknowledged.

Author information

Authors and Affiliations

  1. School of Mathematics and Science, TU Dresden, 01062, Dresden, Germany

    Janine Kaden, Stephan I. Brückner, Susanne Machill & Eike Brunner

  2. Leibniz Institute of Photonic Technologies (IPHT) Jena, 07745, Jena, Germany

    Christoph Krafft

  3. Faculty of Physics and Earth Sciences, University Leipzig, 04103, Leipzig, Germany

    Andreas Pöppl

Authors
  1. Janine Kaden
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephan I. Brückner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Susanne Machill
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christoph Krafft
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andreas Pöppl
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eike Brunner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eike Brunner.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 4559 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kaden, J., Brückner, S.I., Machill, S. et al. Iron incorporation in biosilica of the marine diatom Stephanopyxis turris: dispersed or clustered?. Biometals 30, 71–82 (2017). https://doi.org/10.1007/s10534-016-9987-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-016-9987-4

Keywords

Search

Navigation