Skip to main content
Log in

Micro- and nano-structural characterization of six marine sponges of the class Demospongiae

  • Original Article
  • Published:
European Biophysics Journal Aims and scope Submit manuscript

Abstract

The sponges produce their skeletal elements and silicateins are the key enzymes in this process. The mechanism underlying the formation of their silica skeleton and its structural properties are of exceptional interest for applications in technology. Micro- and nano-scale structural analysis of the six marine sponges belonging to Demospongiae [Callyspongia (Cladochalia) plicifera (Lamarck, 1814), Cervicornia cuspidifera (Lamarck, 1815), Cinachyrela sp., Niphates erecta (Duchassaing and Michelotti, 1864), Xestospongia muta (Schmidt, 1870) and Amphimedon compressa (Duchassaing and Michelotti, 1864)] were carried out by Fourier transform infrared spectroscopy (FTIR), scanning electron microscopy with energy dispersive X-ray spectroscopy (SEM/EDX) and Small-Angle X-ray Scattering (SAXS) techniques. The nano-structural characterizations give some informative evidence about the manner in which silica/silicatein in spicule skeletons is produced by the sponges. The sponge species were successfully discriminated using cluster analysis (HCA) based on FTIR spectra. This study demonstrates and detection of structural differences among sponges and their spicules using combined techniques.

Graphical abstract

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Amenitsch H, Benatti U, Causa M, Croce G, Frache A, Giovine M, Marchese L, Milanesio M, Viterbo D (2001) Preliminary SAXS study of spicules from marine sponges 40. Annual Report SAXS Beamline at ELETTRA, pp 39–40

  • Bavestrello G, Benatti U, Calcinai B, Cattaneo-Vietti R, Cerrano C, Favre A, Giovine M, Lanza S, Pronzato R, Sara M (1998) Body polarity and mineral selectivity in the demosponge Chondrosia reniformis. Biol Bull 195(2):120–125

    Article  Google Scholar 

  • Bonini M, Lenz S, Giorgi R, Baglioni P (2007) Nanomagnetic sponges for the cleaning of works of art. Langmuir 23:17

    Article  CAS  Google Scholar 

  • Born R, Ehrlich H, Bazhenov V, Shapkin NP (2010) Investigation of nanoorganized biomaterials of marine origin. Arab J Chem 3:27–32

    Article  CAS  Google Scholar 

  • Boury-Esmault N, Rützler K (1997) Thesaurus of sponge morphology. Smithsonian contributions to zoology 596. Smithsonian Institute Press, Washington, DC

  • Campos M, Mothes B, Mendes ILV (2007) Antarctic sponges (Porifera, Demospongiae) of the South Shetland Islands and vicinity. Part I. Spirophorida, astrophorida, hadromerida, halichonrida and haplosclerida. Rev Bras Zool 24(3):687–708

    Article  Google Scholar 

  • Cardenas P, Menegola C, Rapp HT, Diaz MC (2009) Morphological description and DNA barcodes of shallow-water tetractinellida (porifera: Demospongiae) from Bocas del Toro, Panama, with description of a new species. Zootaxa 2276:1–39

    Google Scholar 

  • Croce G, Frache A, Milanesio M, Marchese L, Causa M, Viterbo D, Barbaglia A, Bolis V, Bavestrello G, Cerrano C, Benatti U, Pozzolini M, Giovine M, Amenitsch H (2004) Structural characterization of siliceous spicules from marine sponges. Biophys J 86:526–534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Croce G, Viterbo D, Milanesio M, Amenitsch H (2007) A Mesoporous pattern created by nature in spicules from Thetya aurantium sponge. Biophys J 92:288–292

    Article  CAS  PubMed  Google Scholar 

  • Ehrlich H, Brunner E, Simon P, Bazhenov VV, Botting JP, Tabachnik KR, Springer A, Kummer K, Vyalikh DV, Molodtsow SL, Kurek D, Kammer M, Born R, Kovalev A, Gorb SN, Koutsoukos PG, Summers A (2011) Calcite-reinforced silica–silica joints in the biocomposite skeleton of deep-sea glass sponges. Adv Funct Mater 21:3473–3481

    Article  CAS  Google Scholar 

  • Faundez RD, Valentina C (2002) Family niphatidae Van Soest, 1980, Systema porifera: a guide to the classification of sponges. New York, p 886

  • Friday S, Poppell E, Hill M (2013) Cliona tumula sp. nov., a conspicuous zooxanthellate clionaid from the lower Florida Keys (USA) (Hadromerida: Clionaidae). Zootaxa 3750:375–382

    Article  PubMed  Google Scholar 

  • Gal A, Weiner S, Addadi L (2015) A perspective on underlying crystal growth mechanisms in biomineralization: solution mediated growth versus nanosphere particle accretion. Cryst Eng Commun 17:2606–2615

    Article  CAS  Google Scholar 

  • Haris P, Severcan F (1999) FTIR spectroscopic characterization of protein structure in aqueous and non-aqueous media. J Mol Catal B Enzym 7:207–221

    Article  CAS  Google Scholar 

  • Harvey THP (2010) Carbonaceous preservation of Cambrian hexactinellid sponge spicules. Biol Lett 6:834–837

    Article  PubMed  PubMed Central  Google Scholar 

  • Hooper JNA, van Soest RWM (2002) Systema porifera: a guide to the classification of sponges. Kluwer Academic/Plenum Publishers, New York

    Book  Google Scholar 

  • Hu GP, Yuan J, Sun L, She ZG, Wu JH, Lan XJ, Zhu X, Lin YC, Chen SP (2011) Statistical research on marine natural products based on data obtained between 1985 and 2008. Mar Drugs 9(4):514–525

    Article  PubMed  PubMed Central  Google Scholar 

  • Jensen M, Keding R, Höche T, Yue Y (2009) Biologically formed mesoporous amorphous silica. J Am Chem Soc 131(7):2717–2721

    Article  CAS  PubMed  Google Scholar 

  • Jensen M, Keding R, Yue Y (2011) Microscopic features of biologically formed amorphous silica. In: Lilyana P (ed), On Biomimetics, InTech, Chapter 20, Croatia, pp 439–452

  • Jones WC (1987) Seasonal variations in the skeleton and spicule dimensions of Haliclona elegans (Bowerbank) sensu Topsent (1887) from two sites in north Wales. In: Jones WC (ed) European contributions to the taxonomy of sponges. Litho Press, Middleton, pp 109–129

    Google Scholar 

  • Legentil SL, Erwin PM, Henkel TP, Loh TL, Pawlik JR (2010) Phenotypic plasticity in the Caribbean sponge Callyspongia vaginalis (Porifera: Haplosclerida). Sci Mar 74(3):445–453

    Article  Google Scholar 

  • Mehbub MF, Lei J, Franco C, Zhang W (2014) Marine sponge derived natural products between 2001 and 2010: trends and opportunities for discovery of bioactives. Mar Drugs 12(8):4539–4577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morrow C, Cardenas P (2015) Proposal for a revised classification of the Demospongiae (Porifera). Front Zool 12(7):1–27

    Google Scholar 

  • Morse DE (1999) Silicon biotechnology: harnessing biological silica production to construct new materials. Tibtech 17:230–232

    Article  CAS  Google Scholar 

  • Müller WEG, Krasko A, Pennec GL, Schröder HC (2003) Biochemistry and cell biology of silica formation in sponges. Microsc Res Tech 62:368–377

    Article  CAS  PubMed  Google Scholar 

  • Müller WEG, Schloßmacher U, Wang X, Boreiko A, Brandt D, Wolf SE, Tremel W, Schröder HC (2008) Poly(silicate)-metabolizing silicatein in siliceous spicules and silicasomes of demosponges comprises dual enzymatic activities (silica polymerase and silica esterase). FEBS J 275:362–370

    Article  CAS  PubMed  Google Scholar 

  • Müller WEG, Wang X, Cui FZ, Jochum KP, Tremel W, Bill J, Schröder HC, Natalio F, Schloßmacher U, Wiens M (2009) Sponge spicules as blueprints for the biofabrication of inorganic–organic composites and biomaterials. Appl Microbiol Biotechnol 83:397–413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Otzen D (2012) The role of potein in biosilification, sientifica. Review article

  • Prencipe M, Pascale F, Zicovich-Wilson CM, Saunders VR, Orlando R, Dovesi R (2004) The vibrational spectrum of calcite (CaCO3): an ab initio quantum-mechanical calculation. Phys Chem Miners 31:559–564

    Article  CAS  Google Scholar 

  • Rützler K (1978) Sponges in coral reefs. In: Stoddart DR, Johannes RE (eds), Coral reefs: research methods. Paris, France: UNESCO, pp 209–313

  • Rützler K (2002) Family clionaidae d’orbigny, 1851, systema porifera: a guide to the classification of sponges. New York, pp 174–175

  • Sandford F (2003) Physical and chemical analysis of the siliceous skeletons in six sponges of two groups (Demospongiae and hexactinellida). Microsc Res Tech 62:336–355

    Article  CAS  PubMed  Google Scholar 

  • Sarikaya M, Fong H, Sunderland N, Flinn BD, Mayer G, Mescher A, Gaino E (2001) Biomimetic model of a spongespicular optical fiber-mechanical properties and structure. J Mater Res 16:1420–1428

    Article  CAS  Google Scholar 

  • Schröder HC, Wang X, Tremel W, Ushijima H, Müller WEG (2008) Biofabrication of biosilica-glass by living organisms. Nat Prod Rep 25:455–474

    Article  CAS  PubMed  Google Scholar 

  • Shimizu K, Cha J, Stucky GD, Morse DE (1998) Silicatein α: cathepsin L-like protein in sponge biosilica. Genetics 95:6234–6238

    CAS  Google Scholar 

  • Simpson TL (1984) The cell biology of sponges. Springer, New York

    Book  Google Scholar 

  • Sundar VC, Yablon AD, Grazul JL, Ilan M, Aizenberg J (2003) Fibre-optical features of a glass sponge. Nature 424(6951):899–900

    Article  CAS  PubMed  Google Scholar 

  • Swann GEA, Patwardhan SV (2011) Application of Fourier Transform Infrared Spectroscopy (FTIR) for assessing biogenic silica sample purity in geochemical analyses and palaeoenvironmental research. Clim Past 7:65–74

    Article  Google Scholar 

  • Uriz MJ (2006) Mineral skeletogenesis in sponges. Can J Zool 84:322–356

    Article  CAS  Google Scholar 

  • Uriz MJ, Turon X, Becerrov MA, Agell G (2003) Siliceous spicules and skeleton frameworks in sponges: origin, diversity, ultrastructural patterns, and biological functions. Microsc Res Tech 62:279–299

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Wiens M, Schröder HC, Hu S, Mugnaioli E, Kolb U, Tremel W, Pisignano D, Müller WEG (2010) Morphology of sponge spicules: silicatein a structural protein for bio-silica formation. Adv Eng Mater 12(9):B422–B437

    Article  CAS  Google Scholar 

  • Weaver JC, Pietrasanta LI, Hedin N, Chmelka BF, Hansma PK, Morse DE (2003) Nanostructural features of demosponge biosilica. J Struct Biol 144:271–281

    Article  CAS  PubMed  Google Scholar 

  • Wiedenmayer F (1977) Shallow-water sponges of the western Bahamas, Springer Basel AG, pp 115–117

  • Wijffels RH (2008) Potential of sponges and microalgae for marine biotechnology. Trends Biotechnol 26:26–31

    Article  CAS  PubMed  Google Scholar 

  • Woesz A, Weaver JC, Kazanci M, Dauphin Y, Aizenberg J, Morse DE, Fratzl P (2006) Micromechanical properties of biological silica in skeletons of deep-sea sponges. J Mater Res 21(8):2068–2078

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Elif Hilal Şen would like to thank the Scientific and Technological Research Council of Turkey (TUBITAK) because of her postdoctoral research fellowships.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Elif Hilal Şen or Sevgi Haman Bayari.

Ethics declarations

Conflict of interest

The authors confirm that there are no known conflicts of interest associated with this publication. Funding sources had no involvement in study design; collection, analysis, and interpretation of data; writing of the report; and in the decision to submit the article for publication.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Şen, E.H., Ide, S., Bayari, S.H. et al. Micro- and nano-structural characterization of six marine sponges of the class Demospongiae. Eur Biophys J 45, 831–842 (2016). https://doi.org/10.1007/s00249-016-1127-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00249-016-1127-0

Keywords

Navigation