Neurotoxin localization to ectodermal gland cells uncovers an alternative mechanism of venom delivery in sea anemones
- PMID:22048953
- PMCID: PMC3282367
- DOI: 10.1098/rspb.2011.1731
Neurotoxin localization to ectodermal gland cells uncovers an alternative mechanism of venom delivery in sea anemones
Abstract
Jellyfish, hydras, corals and sea anemones (phylum Cnidaria) are known for their venomous stinging cells, nematocytes, used for prey and defence. Here we show, however, that the potent Type I neurotoxin of the sea anemone Nematostella vectensis, Nv1, is confined to ectodermal gland cells rather than nematocytes. We demonstrate massive Nv1 secretion upon encounter with a crustacean prey. Concomitant discharge of nematocysts probably pierces the prey, expediting toxin penetration. Toxin efficiency in sea water is further demonstrated by the rapid paralysis of fish or crustacean larvae upon application of recombinant Nv1 into their medium. Analysis of other anemone species reveals that in Anthopleura elegantissima, Type I neurotoxins also appear in gland cells, whereas in the common species Anemonia viridis, Type I toxins are localized to both nematocytes and ectodermal gland cells. The nematocyte-based and gland cell-based envenomation mechanisms may reflect substantial differences in the ecology and feeding habits of sea anemone species. Overall, the immunolocalization of neurotoxins to gland cells changes the common view in the literature that sea anemone neurotoxins are produced and delivered only by stinging nematocytes, and raises the possibility that this toxin-secretion mechanism is an ancestral evolutionary state of the venom delivery machinery in sea anemones.
Figures




Similar articles
- The Birth and Death of Toxins with Distinct Functions: A Case Study in the Sea Anemone Nematostella.Sachkova MY, Singer SA, Macrander J, Reitzel AM, Peigneur S, Tytgat J, Moran Y.Sachkova MY, et al.Mol Biol Evol. 2019 Sep 1;36(9):2001-2012. doi: 10.1093/molbev/msz132.Mol Biol Evol. 2019.PMID:31134275
- Intron retention as a posttranscriptional regulatory mechanism of neurotoxin expression at early life stages of the starlet anemone Nematostella vectensis.Moran Y, Weinberger H, Reitzel AM, Sullivan JC, Kahn R, Gordon D, Finnerty JR, Gurevitz M.Moran Y, et al.J Mol Biol. 2008 Jul 11;380(3):437-43. doi: 10.1016/j.jmb.2008.05.011. Epub 2008 May 11.J Mol Biol. 2008.PMID:18538344
- Evolution of an ancient venom: recognition of a novel family of cnidarian toxins and the common evolutionary origin of sodium and potassium neurotoxins in sea anemone.Jouiaei M, Sunagar K, Federman Gross A, Scheib H, Alewood PF, Moran Y, Fry BG.Jouiaei M, et al.Mol Biol Evol. 2015 Jun;32(6):1598-610. doi: 10.1093/molbev/msv050. Epub 2015 Mar 9.Mol Biol Evol. 2015.PMID:25757852
- The Anemonia viridis Venom: Coupling Biochemical Purification and RNA-Seq for Translational Research.Nicosia A, Mikov A, Cammarata M, Colombo P, Andreev Y, Kozlov S, Cuttitta A.Nicosia A, et al.Mar Drugs. 2018 Oct 25;16(11):407. doi: 10.3390/md16110407.Mar Drugs. 2018.PMID:30366463Free PMC article.Review.
- Never, Ever Make an Enemy… Out of an Anemone: Transcriptomic Comparison of Clownfish Hosting Sea Anemone Venoms.Delgado A, Benedict C, Macrander J, Daly M.Delgado A, et al.Mar Drugs. 2022 Nov 23;20(12):730. doi: 10.3390/md20120730.Mar Drugs. 2022.PMID:36547877Free PMC article.Review.
Cited by
- Tissue-Specific Venom Composition and Differential Gene Expression in Sea Anemones.Macrander J, Broe M, Daly M.Macrander J, et al.Genome Biol Evol. 2016 Aug 25;8(8):2358-75. doi: 10.1093/gbe/evw155.Genome Biol Evol. 2016.PMID:27389690Free PMC article.
- Transcriptomic and Proteomic Analysis of the Tentacles and Mucus ofAnthopleura dowii Verrill, 1869.Ramírez-Carreto S, Vera-Estrella R, Portillo-Bobadilla T, Licea-Navarro A, Bernaldez-Sarabia J, Rudiño-Piñera E, Verleyen JJ, Rodríguez E, Rodríguez-Almazán C.Ramírez-Carreto S, et al.Mar Drugs. 2019 Jul 25;17(8):436. doi: 10.3390/md17080436.Mar Drugs. 2019.PMID:31349621Free PMC article.
- Tentacle Transcriptomes of the Speckled Anemone (Actiniaria: Actiniidae: Oulactis sp.): Venom-Related Components and Their Domain Structure.Mitchell ML, Tonkin-Hill GQ, Morales RAV, Purcell AW, Papenfuss AT, Norton RS.Mitchell ML, et al.Mar Biotechnol (NY). 2020 Apr;22(2):207-219. doi: 10.1007/s10126-020-09945-8. Epub 2020 Jan 24.Mar Biotechnol (NY). 2020.PMID:31981004
- Cellular adaptations leading to coral fragment attachment on artificial substrates in Acropora millepora (Am-CAM).Lewis BM, Suggett DS, Prentis PJ, Nothdurft LD.Lewis BM, et al.Sci Rep. 2022 Nov 1;12(1):18431. doi: 10.1038/s41598-022-23134-8.Sci Rep. 2022.PMID:36319668Free PMC article.
- Proteotransciptomics of the Most Popular Host Sea AnemoneEntacmaea quadricolor Reveals Not All Toxin Genes Expressed by Tentacles Are Recruited into Its Venom Arsenal.Hoepner CM, Stewart ZK, Qiao R, Fobert EK, Prentis PJ, Colella A, Chataway T, Burke da Silva K, Abbott CA.Hoepner CM, et al.Toxins (Basel). 2024 Feb 5;16(2):85. doi: 10.3390/toxins16020085.Toxins (Basel). 2024.PMID:38393163Free PMC article.
References
- Ruppert E. E., Barnes R. D. 1994. The cnidarians. In Invertebrate zoology, pp. 103–154, 6th edn. Philadelphia, PA: Saunders College Publishing
- Tibballs J. 2006. Australian venomous jellyfish, envenomation syndromes, toxins and therapy. Toxicon 48, 830–85910.1016/j.toxicon.2006.07.020 (doi:10.1016/j.toxicon.2006.07.020) - DOI - DOI - PubMed
- Kass-Simon G., Scappaticci A. A., Jr 2002. The behavioral and developmental physiology of nematocysts. Can. J. Zool. 80, 1772–179410.1139/z02-135 (doi:10.1139/z02-135) - DOI - DOI
- Özbek S., Balasubramanian P. G., Holstein T. W. 2009. Cnidocyst structure and the biomechanics of discharge. Toxicon 54, 1038–104510.1016/j.toxicon.2009.03.006 (doi:10.1016/j.toxicon.2009.03.006) - DOI - DOI - PubMed
- Nüchter T., Benoit M., Engel U., Ozbek S., Holstein T. W. 2006. Nanosecond-scale kinetics of nemtocyst discharge. Curr. Biol. 16, R316–R31810.1016/j.cub.2006.03.089 (doi:10.1016/j.cub.2006.03.089) - DOI - DOI - PubMed
Publication types
MeSH terms
Substances
Grants and funding
LinkOut - more resources
Full Text Sources