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On the trail of the first venomous crustacean: venom gland transcriptome profiling of Remipedia (Crustacea)

Subject Area Evolution, Anthropology
Term from 2012 to 2014
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 220551938
 
Final Report Year 2015

Final Report Abstract

Venomous animals live in almost all aquatic and terrestrial habitats, however, only a narrow range of those venomous species and venoms is studied so far. More extensive and broader studies of neglected or suspected venomous taxa are needed to complete our understanding and knowledge of highly convergent evolution of venoms and the biology of venomous taxa. Next generation sequencing technologies opened recently new possibilities but also new aspects to describe and identify putative new toxins of so far neglected species by sampling snapshots of expressed genes in tissue samples. Anecdotal reports assumed that representatives of the most recently described, enigmatic crustacean class, the Remipedia could be venomous, an assumption that was also based on their very centipede-like habitus. Despite these early assumptions no further, more detailed studies were conducted. Main questions addressed in this project were: 1.) Are remipedes the first venomous crustacean? 2.) Which toxins are expressed? 3.) How differs the remiped venom composition from that of other arthropods and non-arthropods? 4.) Does the putative venom delivery system show any specific adaptations? It was shown that remipeds obviously utilized venom to prey in the dark underwater cave systems they live in. This description of the first venomous crustacean is sensational and fascinating because so far crustaceans were the only major arthropod taxon for which no venomous species were known. Their venom composition is rather unique for arthropods. The toxin cocktail resembles rather the venom of rattlesnakes than any other arthropod. It shows proteinase and chitinase as major components, but also a specific neurotoxin, of which variants were so far only described for spiders. The venom delivery system described in detail by the 3D computer tomography shows a complex muscle arrangement. After the venom injection prey is probably paralyzed by the neurotoxin, while the proteinase cocktail liquefies its body. The liquids are than probably slurped in by remipeds. Several methodological aspects using next generation sequencing technology were shown in this project for the first time in that extent. In particular, the importance to include transcriptome samples of non-venomous taxa and non-venom gland tissue additionally to venomous taxa and venom gland samples for subsequent analyses. The fact that remipeds have a neurotoxin like component that is highly similar to spiders opens many possibilities for practical use, but also to address fundamental questions for our understanding of generally highly convergent evolving venoms. This was one reason why describing the first venomous crustacean drew a lot of attention in public and scientific press and news platforms, such as Nature Comments, BBC News, National Geographic and more. Natural History Museum (2014): http://www.nhm.ac.uk/discover/risking-life-and-limb-for-venom.html Nature comments (2013): http://www.nature.com/news/first-venomous-crustacean-discovered-1.13985 BBC News (2013): http://www.bbc.co.uk/news/science-environment-24625424 National Geographic (2013): http://phenomena.nationalgeographic.com/2013/10/22/of-70000-crustacean-species-heres-thefirst-venomous-one/

Publications

  • A Polychaete's Powerful Punch: Venom Gland Transcriptomics of Glycera Reveals a Complex Cocktail of Toxin Homologs. Genome Biology and Evolution 2014, 6, 2406–2423
    Reumont, von, B. M.; Campbell, L. I.; Richter, S.; Hering, L.; Sykes, D.; Hetmank, J.; Jenner, R. A.; Bleidorn, C.
    (See online at https://doi.org/10.1093/gbe/evu190)
  • Quo vadis venomics? A roadmap to neglected venomous invertebrates. Invited Review. Toxins 2014, 6: 3488- 3551
    Reumont, von, B. M. ; Campbell, L. I.; Jenner, R. A.
    (See online at https://doi.org/10.3390/toxins6123488)
  • The First Venomous Crustacean Revealed by Transcriptomics and Functional Morphology: Remipede Venom Glands Express a Unique Toxin Cocktail Dominated by Enzymes and a Neurotoxin. Molecular Biology and Evolution 2014, 31, 48–58
    Reumont, von, B. M.; Blanke, A.; Richter, S.; Alvarez, F.; Bleidorn, C.; Jenner, R. A.
    (See online at https://doi.org/10.1093/molbev/mst199)
  • Venomics of Remipede Crustaceans Reveals Novel Peptide Diversity and Illuminates the Venom’s Biological Role. Toxins 2017, 9(8), 234. Umfang 25 S.
    Reumont, von, B. M.; Jenner, R. A; Undheim, E., Jauss, R. T.
    (See online at https://doi.org/10.3390/toxins9080234)
 
 

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