A Dipteran’s Novel Sucker Punch: Evolution of Arthropod Atypical Venom with a Neurotoxic Component in Robber Flies (Asilidae, Diptera)
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...
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2018-01-01
|
| Series: | Toxins |
| Subjects: | |
| Online Access: | http://www.mdpi.com/2072-6651/10/1/29 |
| _version_ | 1828371340903579648 |
|---|---|
| author | Stephan Holger Drukewitz Nico Fuhrmann Eivind A. B. Undheim Alexander Blanke Julien Giribaldi Rosanna Mary Guillaume Laconde Sébastien Dutertre Björn Marcus von Reumont |
| author_facet | Stephan Holger Drukewitz Nico Fuhrmann Eivind A. B. Undheim Alexander Blanke Julien Giribaldi Rosanna Mary Guillaume Laconde Sébastien Dutertre Björn Marcus von Reumont |
| author_sort | Stephan Holger Drukewitz |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-14T06:48:36Z |
| format | Article |
| id | doaj.art-846b91b9dcf244bd87fffe2e95cd4b51 |
| institution | Directory Open Access Journal |
| issn | 2072-6651 |
| language | English |
| last_indexed | 2024-04-14T06:48:36Z |
| publishDate | 2018-01-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Toxins |
| spelling | doaj.art-846b91b9dcf244bd87fffe2e95cd4b512022-12-22T02:07:05ZengMDPI AGToxins2072-66512018-01-011012910.3390/toxins10010029toxins10010029A Dipteran’s Novel Sucker Punch: Evolution of Arthropod Atypical Venom with a Neurotoxic Component in Robber Flies (Asilidae, Diptera)Stephan Holger Drukewitz0Nico Fuhrmann1Eivind A. B. Undheim2Alexander Blanke3Julien Giribaldi4Rosanna Mary5Guillaume Laconde6Sébastien Dutertre7Björn Marcus von Reumont8Institute for Biology, University of Leipzig, Talstr. 33, 04103 Leipzig, GermanyMax Planck Institute for Evolutionary Biology, August-Thienemann-Str. 2, 24306 Plön, GermanyCentre for Advanced Imaging, The University of Queensland, St. Lucia, Brisbane, QLD 4072, AustraliaInstitute for Zoology, Biocenter, University of Cologne, Zuelpicher Str. 47b, 50674 Cologne, GermanyInstitute for Biomolecules Max Mousseron, UMR 5247, University of Montpellier—CNRS, Place Eugène Bataillon, 34095 Montpellier CEDEX 5, FranceInstitute for Biomolecules Max Mousseron, UMR 5247, University of Montpellier—CNRS, Place Eugène Bataillon, 34095 Montpellier CEDEX 5, FranceInstitute for Biomolecules Max Mousseron, UMR 5247, University of Montpellier—CNRS, Place Eugène Bataillon, 34095 Montpellier CEDEX 5, FranceInstitute for Biomolecules Max Mousseron, UMR 5247, University of Montpellier—CNRS, Place Eugène Bataillon, 34095 Montpellier CEDEX 5, FranceInstitute for Biology, University of Leipzig, Talstr. 33, 04103 Leipzig, GermanyPredatory 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.http://www.mdpi.com/2072-6651/10/1/29Asilidaeneurotoxinscysteine inhibitor knot peptidearthropod venom evolutionfunctional morphologysynchrotron micro computed tomographyAsilidin |
| spellingShingle | Stephan Holger Drukewitz Nico Fuhrmann Eivind A. B. Undheim Alexander Blanke Julien Giribaldi Rosanna Mary Guillaume Laconde Sébastien Dutertre Björn Marcus von Reumont A Dipteran’s Novel Sucker Punch: Evolution of Arthropod Atypical Venom with a Neurotoxic Component in Robber Flies (Asilidae, Diptera) Toxins Asilidae neurotoxins cysteine inhibitor knot peptide arthropod venom evolution functional morphology synchrotron micro computed tomography Asilidin |
| title | A Dipteran’s Novel Sucker Punch: Evolution of Arthropod Atypical Venom with a Neurotoxic Component in Robber Flies (Asilidae, Diptera) |
| title_full | A Dipteran’s Novel Sucker Punch: Evolution of Arthropod Atypical Venom with a Neurotoxic Component in Robber Flies (Asilidae, Diptera) |
| title_fullStr | A Dipteran’s Novel Sucker Punch: Evolution of Arthropod Atypical Venom with a Neurotoxic Component in Robber Flies (Asilidae, Diptera) |
| title_full_unstemmed | A Dipteran’s Novel Sucker Punch: Evolution of Arthropod Atypical Venom with a Neurotoxic Component in Robber Flies (Asilidae, Diptera) |
| title_short | A Dipteran’s Novel Sucker Punch: Evolution of Arthropod Atypical Venom with a Neurotoxic Component in Robber Flies (Asilidae, Diptera) |
| title_sort | dipteran s novel sucker punch evolution of arthropod atypical venom with a neurotoxic component in robber flies asilidae diptera |
| topic | Asilidae neurotoxins cysteine inhibitor knot peptide arthropod venom evolution functional morphology synchrotron micro computed tomography Asilidin |
| url | http://www.mdpi.com/2072-6651/10/1/29 |
| work_keys_str_mv | AT stephanholgerdrukewitz adipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT nicofuhrmann adipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT eivindabundheim adipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT alexanderblanke adipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT juliengiribaldi adipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT rosannamary adipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT guillaumelaconde adipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT sebastiendutertre adipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT bjornmarcusvonreumont adipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT stephanholgerdrukewitz dipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT nicofuhrmann dipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT eivindabundheim dipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT alexanderblanke dipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT juliengiribaldi dipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT rosannamary dipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT guillaumelaconde dipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT sebastiendutertre dipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera AT bjornmarcusvonreumont dipteransnovelsuckerpunchevolutionofarthropodatypicalvenomwithaneurotoxiccomponentinrobberfliesasilidaediptera |