Venom evolution in glycerid polychaetes (Annelida, Glyceridae) with special emphasis on alpha-glycerotoxin
Final Report Abstract
Venoms and venom systems evolved many times independently across the animal tree of life. Whereas the venom of snakes and spiders have been investigated in detail, annelids were neglected so far. Glycerids are a group of worldwide distributed venomous annelids, which are easily recognizable by an eversible pharynx that possesses four cross-arranged jaws for venom injection. A 320 kDa protein toxin isolated from the venom of Glycera tridactyla and named α-glycerotoxin (gltx). Potential medical usefulness has been suggested by other authors due to its specific, dose-dependent and reversible mode of action. In this project, we were able to present the first molecular characterization of the neurotoxin gltx. Genomic structure, as well as domain organization has been described, however, only 80% of the large neurotoxin showed any similarities with known domains. Analysing the expression of this neurotoxin, it could be shown that the organization of the venom system of glycerid annelids is different than previously described. We found strong expression in so far neglected lobe-like structures connected to the so-called venom glands, as evidenced by in situ hybridization, immunochemistry, tissue-specific RNAseq, and real-time PCR. In contrast, the gland-like structures known as venom glands only show a very low level of gltx expression. Based on our data we propose a new view on the organization of the glycerid venom system. Moreover, the composition of the venom gland transcriptome has been described and compared for three different glycerid species. The putative toxins we recovered are comprised by five functionally distinguishable toxin classes: pore-forming and membrane-disrupting toxins, neurotoxins, protease inhibitors, other enzymes, and CAP domain toxins. Our results have been partly summarized in the widely read National Geographic “Phenomena” blog of the science journalist Ed Yong.
Publications
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(2014) 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 31, 48-58
von Reumont, B., Blanke, A., Richter, S., Alvarez, F., Bleidorn, C., Jenner, R.A.
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(2014): A polychaete’s powerful punch: venom gland transcriptomics of Glycera reveals a complex cocktail of toxin homologs. Genome Biology and Evolution 6, 2406-2423
von Reumont, B., Campbell, L., Richter, S., Hering, L., Sykes, D., Jenner, R.A., Bleidorn, C.
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(2015) The utility of genome skimming for phylogenomic analyses as demonstrated for glycerid relationships (Annelida, Glyceridae). Genome Biology and Evolution 7, 3443-3462
Richter, S., Schwarz, F., Hering, L., Böggemann, M., Bleidorn, C.
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(2017) Comparative analyses of glycerotoxin expression unveil a novel structural organization of the bloodworm venom system. BMC Evolutionary Biology 17, Art.-No. 64
Richter, S., Helm, C., Meunier, F.A., Hering, L., Campbell, L.I., Drukewitz, S.H., Undheim, E.A.B., Jenner, R.A., Schiavo, G., Bleidorn, C.
