Skip to main content
SpringerLink
Log in

Chemical defence by mono-prenyl hydroquinone in a freshwater ciliate, Spirostomum ambiguum

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

Several species of ciliates produce and accumulate low molecular weight toxic compounds in specialised membrane-bound ejectable organelles: extrusomes. These compounds can be used in predator–prey interaction for killing prey as well as for chemical defence. Here, we describe the isolation and characterisation of 2-(3-methylbut-2-enyl)benzene-1,4-diol(mono-prenyl hydroquinone), the extrusomal defensive toxin of the freshwater heterotrich ciliate Spirostomum ambiguum. The toxin was purified at homogeneity by RP-HPLC, and its structural characterisation was carried out through NMR and MS measurements. In vivo experiments involving S. ambiguum and Climacostomum virens in predator–prey interaction, and the analysis of cytotoxic activity of mono-prenyl hydroquinone on a panel of free-living freshwater ciliates, indicated that the toxin is very effective in S. ambiguum’s chemical defence.

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

Similar content being viewed by others

References

  • Abe, Y. & K. Mori, 2001. Simple synthesis of climacostol, a defense secretion by the ciliate Climacostomum virens. Bioscience, Biotechnology, and Biochemistry 65: 2110–2112.

    Article  PubMed  CAS  Google Scholar 

  • Baby, J. & S. Sujatha, 2011. Pharmacologically important natural products from marine sponges. Journal of Natural Products 4: 5–12.

    Google Scholar 

  • Bohlmann, F. & K.-M. Kleine, 1966. Über ein neues Chinon aus höheren Pflanzen. Chemische Berichte 99: 885–888.

    Article  CAS  Google Scholar 

  • Buonanno, F., 2005. Variations in the efficiency of ciliate extrusomal toxins against a common ciliate predator, the catenulid Stenostomum sphagnetorum. Italian Journal of Zoology 72: 293–295.

    Article  Google Scholar 

  • Buonanno, F., 2009. Antipredator behavior of freshwater microturbellarian Stenostomum sphagnetorum against the predatory ciliate Dileptus margaritifer. Zoological Science 26: 443–447.

    Article  PubMed  Google Scholar 

  • Buonanno, F., 2011. The changes in the predatory behavior of the microturbellarian Stenostomum sphagnetorum on two species of toxin-secreting ciliates of the genus Spirostomum. Biologia 66: 648–653.

    Article  Google Scholar 

  • Buonanno, F. & C. Ortenzi, 2010. The protozoan toxin climacostol and its derivatives: cytotoxicity studies on 10 species of free-living ciliates. Biologia 65: 675–680.

    Article  CAS  Google Scholar 

  • Buonanno, F., P. Saltalamacchia & A. Miyake, 2005. Defence function of pigmentocysts in the karyorelictid ciliate Loxodes striatus. European Journal of Protistology 41: 151–158.

    Article  Google Scholar 

  • Buonanno, F., L. Quassinti, M. Bramucci, C. Amantini, R. Lucciarini, H. Santoni & C. Iio, 2008. The protozoan toxin climacostol inhibits growth and induces apoptosis of human tumor cell lines. Chemical Biological Interactions 176: 151–164.

    Article  CAS  Google Scholar 

  • Cameron, D. W. & A. G. Riches, 1995. Synthesis of stentorin. Tetrahedron Letters 36: 2331–2334.

    Article  CAS  Google Scholar 

  • Cervia, D., M. Garcia-Gil, E. Simonetti, G. Di Giuseppe, G. Guella, P. Bagnoli & F. Dini, 2007. Molecular mechanisms of euplotin C induced apoptosis: involvement of mitochondrial dysfunction, oxidative stress and proteases. Apoptosis 12: 1349–1363.

    Article  PubMed  CAS  Google Scholar 

  • Cervia, D., G. Di Giuseppe, C. Ristori, D. Martini, G. Gambellini, P. Bagnoli & F. Dini, 2009. The secondary metabolite euplotin C induces apoptosis-like death in the marine ciliated protist Euplotes vannus. Journal of Eukaryotic Microbiology 56: 263–269.

    Article  PubMed  CAS  Google Scholar 

  • Connon, S. J. & S. Blechert, 2003. Recent developments in olefin cross-metathesis. Angewandte Chemie International Edition 42: 1900–1923.

    Article  CAS  Google Scholar 

  • Dai, R., T. Yamazaki, I. Yamazaki & P.-S. Song, 1995. Initial spectroscopic characterization of the ciliate photoreceptor stentorin. Biochimica et Biophysica Acta 1231: 58–68.

    Article  PubMed  Google Scholar 

  • De Rosa, S., A. De Giulio & C. Iodice, 1994. Biological effects of prenylated hydroquinones: structure-activity relationship studies in antimicrobial, brine shrimp, and fish lethality assays. Journal of Natural Products 57: 1711–1716.

    Article  PubMed  Google Scholar 

  • Dettner, K., 2010. Chemical defense and toxins of lower terrestrial and freshwater animals. In Mander, L. & H.-W. Lui (eds), Comprehensive Natural Products II Chemistry and Biology, Vol. 4. Elsevier, Oxford: 387–410.

    Chapter  Google Scholar 

  • Fiorini, D., S. Giuli, E. Marcantoni, L. Quassinti, M. Bramucci, C. Amantini, G. Santoni, F. Buonanno & C. Ortenzi, 2010. A straightforward diastereoselective synthesis and evaluation of climacostol, a natural product with anticancer activities. Synthesis 9: 1550–1556.

    Google Scholar 

  • Foissner, W., H. Berger & F. Kohmann, 1992. Taxonomishe und ökologische Revision der Ciliaten des Saprobiensystems – Band II: Peritrichida, Heterotrichida, Odontostomatida. In Informationsberichte des Bayer (ed.), Heterotrichida. Bayerisches Landesamt für Wasserwirtschaft, München: 1–502.

  • Giese, A. C., 1981. The photobiology of Blepharisma. In Smith, K. C. (ed.), Photochemical Photobiological Reviews. Plenum, New York: 139–180.

    Google Scholar 

  • Guella, G., R. Frassanito, I. Mancini, T. Sandron, L. Modeo, F. Verni, F. Dini & G. Petroni, 2010a. Keronopsamides, a new class of pigments from marine ciliates. European Journal of Organic Chemistry 3: 427–434.

    Article  Google Scholar 

  • Guella, G., D. Skropeta, G. Di Giuseppe & F. Dini, 2010b. Structures, biological activities and phylogenetic relationships of terpenoids from marine ciliates of the genus Euplotes. Marine Drugs 8: 2080–2116.

    Article  PubMed  CAS  Google Scholar 

  • Guilivi, C. & E. Cadenas, 1994. One- and two-electron reduction of 2-methyl-1,4-naphthoquinone bioreductive alkylating agents: kinetic studies, free-radical production, thiol oxidation and DNAstrand-break formation. Biochemical Journal 301: 21–30.

    Google Scholar 

  • Harumoto, T., A. Miyake, N. Ishikawa, R. Sugibayashi, K. Zenfuku & H. Iio, 1998. Chemical defense by means of pigmented extrusomes in the ciliate Blepharisma japonicum. European Journal of Protistology 34: 458–470.

    Article  Google Scholar 

  • Hausmann, K., 1978. Extrusive organelles in protists. International Review of Cytology 52: 197–276.

    Article  PubMed  CAS  Google Scholar 

  • Hausmann, K., 2002. Food acquisition, food ingestion and food digestion by protists. Japanese Journal of Protozoology 35: 85–95.

    Google Scholar 

  • Heide, L., 2009. Prenyl transfer to aromatic substrates: genetics and enzymology. Current Opinion in Chemical Biology 13: 171–179.

    Article  PubMed  CAS  Google Scholar 

  • Henry, R. T. & B. K. Wallace, 1996. Different mechanisms of cell killing by redox cycling and arylating quinones. Archives of Toxicology 70: 482–489.

    Article  PubMed  CAS  Google Scholar 

  • Howard, B. M., K. Clarkson & R. L. Bernstein, 1979. Simple prenylated hydroquinone derivatives from the marine urochordate Aplidium californicum. Natural anticancer and antimutagenic agents. Tetrahedron Letters 46: 4449–4452.

    Article  Google Scholar 

  • Iio, H., K. Zenfuku & T. Tokoroyama, 1995. A facile synthesis of stentorin, the photoreceptor of Stentor coeruleus. Tetrahedron Letters 36: 5921–5924.

    CAS  Google Scholar 

  • Lindquist, N., M. E. Hay & W. Fenical, 1992. Defence of ascidians and their conspicuous larvae: adult vs. larval chemical defenses. Ecological Monographs 62: 547–568.

    Article  Google Scholar 

  • Masaki, M. E., S. Hiro, Y. Usuki, T. Harumoto, M. N. Terazima, F. Buonanno, A. Miyake & H. Iio, 2004. Climacostol, a defense toxin of Climacostomum virens (protozoa, ciliata), and its congeners. Tetrahedron 60: 7041–7048.

    Article  CAS  Google Scholar 

  • Miyake, A., 1981. Cell interaction by gamones in Blepharisma. In O’Day, D. H. & P. A. Horgen (eds), Sexual Interaction in Eukaryotic Microbes. Academic Press, New York: 95–129.

    Google Scholar 

  • Miyake, A., T. Harumoto, B. Slavi & V. Rivola, 1990. Defensive function of pigment granules in Blepharisma. European Journal of Protistology 25: 310–315.

    Article  Google Scholar 

  • Miyake, A., T. Harumoto & H. Iio, 2001. Defence function of pigment granules in Stentor coeruleus. European Journal of Protistology 37: 77–88.

    Article  Google Scholar 

  • Miyake, A., F. Buonanno, P. Saltalamacchia, M. E. Masaki & H. Iio, 2003. Chemical defence by means of extrusive cortical granules in the heterotrich ciliate Climacostomum virens. European Journal of Protistology 39: 25–36.

    Article  Google Scholar 

  • Muto, Y., T. Matsuoka, A. Kida, Y. Okano & Y. Kirino, 2001. Blepharismins, produced by the protozoan, Blepharisma japonicum, form ion-permeable channels in planar lipid bilayer membranes. FEBS Letters 508: 423–426.

    Article  PubMed  CAS  Google Scholar 

  • Muto, Y., Y. Tanabe, K. Kawai, Y. Okano & H. Iio, 2011. Climacostol inhibits Tetrahymena motility and mitochondrial respiration. Central European Journal of Biology 6: 99–104.

    Article  CAS  Google Scholar 

  • Pant, B., Y. Kato, T. Kumagai, T. Matsuoka & M. Sugiyama, 1997. Blepharismin produced by a protozoan Blepharisma functions as an antibiotic effective against methicillin-resistant Staphylococcus aureus. FEMS Microbiology Letters 155: 67–71.

    Article  PubMed  CAS  Google Scholar 

  • Park, M., W. Fenical & M. E. Hay, 1992. Debromoisocymobarbatol, a new chromanol feeding deterrent from the marine alga Cymopolia barbata. Phytochemistry 31: 4115–4118.

    Article  CAS  Google Scholar 

  • Pietra, F., 2002. Biodiversity and natural product diversity. In: Baldwin, J. E. & R. M. Williams (eds), Taxonomy, phylogeny, and natural products. Elsevier, Oxford: 9–11.

  • Pucciarelli, S., F. Buonanno, G. Pellegrini, P. Ballarini & C. Miceli, 2008. Biomonitoring of lake Garda: identification of ciliate species and symbiotic algae responsible for the “black-spot” bloom during the summer of 2004. Environmental Research 107: 194–200.

    Article  PubMed  CAS  Google Scholar 

  • Rosati, G. & L. Modeo, 2003. Extrusomes in ciliates: diversification, distribution, and phylogenetic implications. Journal of Eukaryotic Microbiology 50: 383–402.

    Article  PubMed  Google Scholar 

  • Scheepers, B. A., R. Klein & M. T. Davies-Coleman, 2006. Synthesis of triprenylated toluquinone and toluhydroquinone metabolites from a marine-derived Penicillium fungus. Tetrahedron Letters 47: 8243–8246.

    Article  CAS  Google Scholar 

  • Sera, Y., Y. Usuki & H. Iio, 2006. Synthetic studies on spirostomin, a defense toxin of Spirostomum teres. Nippon Kagakkai Koen Yokoshu 86: 1382.

    Google Scholar 

  • Sladić, D. & M. J. Gašić, 2006. Reactivity and biological activity of the marine sesquiterpene hydroquinone avarol and related compounds from sponges of the order Dictyoceratida. Molecules 11: 1–33.

    Article  PubMed  Google Scholar 

  • Sugibayashi, R. & T. Harumoto, 2000. Defensive function of trichocysts in Paramecium tetraurelia against heterotrich ciliate Climacostomum virens. European Journal of Protistology 36: 415–422.

    Article  Google Scholar 

  • Terazima, M. N. & T. Harumoto, 2004. Defense function of pigment granules in the ciliate Blepharisma japonicum against two predatory protists, Amoeba proteus (Rhizopodea) and Climacostomum virens (Ciliata). Zoological Science 21: 823–828.

    Article  PubMed  Google Scholar 

  • Terencio, M. C., M. L. Ferrándiz, I. Posadas, E. Roig, S. De Rosa, A. De Giulio, M. Payá & M. J. Alcaraz, 1998. Suppression of leukotriene B4 and tumour necrosis factor alpha release in acute inflammatory responses by novel prenylated hydroquinone derivatives. Naunyn-Schmiedeberg’s Archives of Pharmacology 357: 565–572.

    Article  PubMed  CAS  Google Scholar 

  • Tillmann, U., 2004. Interactions between planktonic microalgae and protozoan grazers. Journal of Eukaryotic Microbiology 51: 156–168.

    Article  PubMed  Google Scholar 

  • Yang, H.-C., J. Yu, K.-B. Oh, D.-S. Shin, W.-J. Cho, J. Shin & S. Kim, 2007. Synthesis and evaluation of hydroquinone derivatives as inhibitors of isocitrate lyase. Archives of Pharmacal Researches 30: 955–961.

    Article  CAS  Google Scholar 

  • Yoshioka, K., S. Tominaga, U. Yoshiyuki, U. Yoshinosuke & H. Iio, 2008. Starter units of the biosynthesis of blepharismins: self-defence pigments of Blepharisma japonicum. Tetrahedron 64: 4103–4107.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Financial support was provided by the CARIMA Foundation (Fondazione Cassa di Risparmio della Provincia di Macerata) and Regione Marche. The authors are very grateful to Dr. Gill Philip for the linguistic revision of the text.

Author information

Authors and Affiliations

  1. Department of Education Science, University of Macerata, 62100, Macerata, Italy

    Federico Buonanno & Claudio Ortenzi

  2. Bioorganic Chemistry Laboratory, Department of Physics, University of Trento, 38050, Povo, Trento, Italy

    Graziano Guella & Cristian Strim

  3. Institute of Biophysics, CNR, 38050, Povo, Trento, Italy

    Graziano Guella

Authors
  1. Federico Buonanno
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Graziano Guella
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Cristian Strim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Claudio Ortenzi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claudio Ortenzi.

Additional information

Handling editor: Stefano Amalfitano

Rights and permissions

Reprints and permissions

About this article

Cite this article

Buonanno, F., Guella, G., Strim, C. et al. Chemical defence by mono-prenyl hydroquinone in a freshwater ciliate, Spirostomum ambiguum . Hydrobiologia 684, 97–107 (2012). https://doi.org/10.1007/s10750-011-0972-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-011-0972-1

Keywords

Search

Navigation