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Toxins 2018, 10(1), 29; https://doi.org/10.3390/toxins10010029

A Dipteran’s Novel Sucker Punch: Evolution of Arthropod Atypical Venom with a Neurotoxic Component in Robber Flies (Asilidae, Diptera)

1
Institute for Biology, University of Leipzig, Talstr. 33, 04103 Leipzig, Germany
2
Max Planck Institute for Evolutionary Biology, August-Thienemann-Str. 2, 24306 Plön, Germany
3
Centre for Advanced Imaging, The University of Queensland, St. Lucia, Brisbane, QLD 4072, Australia
4
Institute for Zoology, Biocenter, University of Cologne, Zuelpicher Str. 47b, 50674 Cologne, Germany
5
Medical and Biological Engineering Research Group, School of Engineering and Computer Science, University of Hull, Hull HU6 7RX, UK
6
Institute for Biomolecules Max Mousseron, UMR 5247, University of Montpellier—CNRS, Place Eugène Bataillon, 34095 Montpellier CEDEX 5, France
7
Department of Life Sciences, Natural History Museum, Cromwell Rd, London SW7 5BD, UK
*
Authors to whom correspondence should be addressed.
Received: 4 December 2017 / Revised: 19 December 2017 / Accepted: 27 December 2017 / Published: 5 January 2018
(This article belongs to the Section Animal Venoms)
Full-Text   |   PDF [9091 KB, uploaded 5 January 2018]   |  

Abstract

Predatory robber flies (Diptera, Asilidae) have been suspected to be venomous due to their ability to overpower well-defended prey. However, details of their venom composition and toxin arsenal remained unknown. Here, we provide a detailed characterization of the venom system of robber flies through the application of comparative transcriptomics, proteomics and functional morphology. Our results reveal asilid venoms to be dominated by peptides and non-enzymatic proteins, and that the majority of components in the crude venom is represented by just ten toxin families, which we have named Asilidin1–10. Contrary to what might be expected for a liquid-feeding predator, the venoms of robber flies appear to be rich in novel peptides, rather than enzymes with a putative pre-digestive role. The novelty of these peptides suggests that the robber fly venom system evolved independently from hematophagous dipterans and other pancrustaceans. Indeed, six Asilidins match no other venom proteins, while three represent known examples of peptide scaffolds convergently recruited to a toxic function. Of these, members of Asilidin1 closely resemble cysteine inhibitor knot peptides (ICK), of which neurotoxic variants occur in cone snails, assassin bugs, scorpions and spiders. Synthesis of one of these putative ICKs, U-Asilidin1-Mar1a, followed by toxicity assays against an ecologically relevant prey model revealed that one of these likely plays a role as a neurotoxin involved in the immobilization of prey. Our results are fundamental to address these insights further and to understand processes that drive venom evolution in dipterans as well as other arthropods. View Full-Text
Keywords: Asilidae; neurotoxins; cysteine inhibitor knot peptide; arthropod venom evolution; functional morphology; synchrotron micro computed tomography; Asilidin Asilidae; neurotoxins; cysteine inhibitor knot peptide; arthropod venom evolution; functional morphology; synchrotron micro computed tomography; Asilidin
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Drukewitz, S.H.; Fuhrmann, N.; Undheim, E.A.B.; Blanke, A.; Giribaldi, J.; Mary, R.; Laconde, G.; Dutertre, S.; von Reumont, B.M. A Dipteran’s Novel Sucker Punch: Evolution of Arthropod Atypical Venom with a Neurotoxic Component in Robber Flies (Asilidae, Diptera). Toxins 2018, 10, 29.

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