June 2013, Volume 15, Issue 3, pp 329-339,
Open Access This content is freely available online to anyone, anywhere at any time.
Date: 15 Nov 2012
Analysis of Soluble Protein Contents from the Nematocysts of a Model Sea Anemone Sheds Light on Venom Evolution
The nematocyst is one of the most complex intracellular structures found in nature and is the defining feature of the phylum Cnidaria (sea anemones, corals, jellyfish, and hydroids). This miniature stinging organelle contains and delivers venom into prey and foe yet little is known about its toxic components. In the present study, we identified by tandem mass spectrometry 20 proteins released upon discharge from the nematocyst of the model sea anemone Nematostella vectensis. The availability of genomic and transcriptomic data for this species enabled accurate identification and phylogenetic study of these components. Fourteen of these proteins could not be identified in other animals suggesting that they might be the products of taxonomically restricted genes, a finding which fits well their origin from a taxon-specific organelle. Further, we studied by in situ hybridization the localization of two of the transcripts encoding the putative nematocyst venom proteins: a metallopeptidase related to the Tolloid family and a cysteine-rich protein. Both transcripts were detected in nematocytes, which are the cells containing nematocysts, and the metallopeptidase was found also in pharyngeal gland cells. Our findings reveal for the first time the possible venom components of a sea anemone nematocyst and suggest their evolutionary origins.
Béress L, Béress R, Wunderer G (1975) Isolation and characterisation of three polypeptides with neurotoxic activity from Anemonia sulcata. FEBS Lett 50:311–314PubMed
da Silveira RB, Wille AC, Chaim OM, Appel MH, Silva DT, Franco CR, Toma L, Mangili OC, Gremski W, Dietrich CP et al (2007) Identification, cloning, expression and functional characterization of an astacin-like metalloprotease toxin from Loxosceles intermedia (brown spider) venom. Biochem J 406:355–363PubMedCrossRef
Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinforma 5:113CrossRef
Fry BG, Roelants K, Norman JA (2009b) Tentacles of venom: toxic protein convergence in the Kingdom Animalia. J Mol Evo 68:311–321CrossRef
Genikhovich, G, Technau U (2009) In situ hybridization of starlet sea anemone (Nematostella vectensis) embryos, larvae, and polyps. Cold Spring Harb Protoc 2009, pdb.prot5282.
Hessinger DA, Lenhoff HM, Kahan LB (1973) Hemolytic, phospholipase a and nerve-affecting activities of sea anemone nematocyst venom. Nat New Biol 241:125–127PubMed
Hwang JS, Takaku Y, Momose T, Adamczyk P, Ozbek S, Ikeo K, Khalturin K, Hemmrich G, Bosch TC, Holstein TW et al (2010) Nematogalectin, a nematocyst protein with GlyXY and galectin domains, demonstrates nematocyte-specific alternative splicing in Hydra. Proc Natl Acad Sci USA 107:18539–18544PubMedCrossRef
Kass-Simon G, Scappaticci AA (2002) The behavioral and developmental physiology of nematocysts. Can J Zool 80:1772–1794CrossRef
Krishnan A, Nair PN, Jones D (1994) Isolation, cloning, and characterization of new chitinase stored in active form in chitin-lined venom reservoir. J Biol Chem 269:20971–20976PubMed
Marchler-Bauerm A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR et al (2011) CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39:D225–229CrossRef
Mohrlen F, Maniura M, Plickert G, Frohme M, Frank U (2006) Evolution of astacin-like metalloproteases in animals and their function in development. Evo Dev 8:223–231CrossRef
Rodriguez AA, Cassoli JS, Sa F, Dong ZQ, de Freitas JC, Pimenta AM, de Lima ME, Konno K, Lee SM, Garateix A et al (2011) Peptide fingerprinting of the neurotoxic fractions isolated from the secretions of sea anemones Stichodactyla helianthus and Bunodosoma granulifera. New members of the APETx-like family identified by a 454 pyrosequencing approach. Peptides 34:26–28PubMedCrossRef
Trevisan-Silva D, Gremski LH, Chaim OM, da Silveira RB, Meissner GO, Mangili OC, Barbaro KC, Gremski W, Veiga SS, Senff-Ribeiro A (2010) Astacin-like metalloproteases are a gene family of toxins present in the venom of different species of the brown spider (genus Loxosceles). Biochimie 92:21–32PubMedCrossRef
Weber J (1990) Poly(γ-glutamic acid)s are the major constituents of nematocysts in Hydra (Hydrozoa, Cnidaria). J Biol Chem 265:9664–9669PubMed
- Analysis of Soluble Protein Contents from the Nematocysts of a Model Sea Anemone Sheds Light on Venom Evolution
- Open Access
- Available under Open Access This content is freely available online to anyone, anywhere at any time.
Volume 15, Issue 3 , pp 329-339
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- 1. Department of Molecular Evolution and Development, Centre for Organismal Systems Biology, Faculty of Life Sciences, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria
- 2. Maagan Michael; D.N., Menashe, 37805, Israel
- 3. Golda Meir St. 54, Haifa, 34982, Israel
- 4. Hamigdal St. 14, Caesarea, 30889, Israel