Dataset Information

Venom proteome of the limacodid caterpillar Doratifera vulnerans

ABSTRACT: Caterpillars of moths in the family Limacodidae produce pain-inducing defensive venoms that have evolved independently to previously characterised lepidopteran venoms, but their composition and mechanism of action are unknown. Here, we examine the limacodid venom system using the species Doratifera vulnerans as a model. Large secretory cells at the base of each spine produce a complex venom (151 proteinaceous toxins in 59 families) that consists predominantly of peptides <10 kDa. Three abundant families of venom peptides (vulnericins) are analogues of adipokinetic hormone/corazonin-like neurohormone that activate the endogenous receptor with picomolar efficacy (Family 1); cationic peptides related to cecropin that disrupt lipid bilayers, induce pain, and kill bacteria and helminths (Family 2); and disulfide-rich knottins (Family 3). Our data reveal convergent molecular evolution between limacodids, hymenopterans, and arachnids, and highlight the potential of Limacodidae for peptide biodiscovery.

INSTRUMENT(S): TripleTOF 5600, TripleTOF 6600

ORGANISM(S): Doratifera Vulnerans

TISSUE(S): Venom

SUBMITTER: Andrew Walker

LAB HEAD: Glenn F. King

PROVIDER: PXD022400 | Pride | 2021-04-12

REPOSITORIES: Pride

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Project description:Spider venoms are a unique source of bioactive peptides displaying remarkable structural stability and potent neuroactivity. Phoneutria nigriventer, often referred to as Brazilian wandering spider, banana spider or “armed” spider, is endemic from South America and amongst the most dangerous venomous spiders in the world. Envenomation accidents with P. nigriventer often occur in Brazil with approximately 4,000 cases per year and which symptoms include priapism, hypertension, blurred vision, sweating, and vomiting, amongst others. Besides its clinical relevance, P. nigriventer venom comprises promising peptide drug leads providing therapeutic effects in a range of disease models. In this study, we further explored the neuroactivity and molecular diversity of the venom from P. nigriventer using fractionation-guided high-throughput cellular assays coupled to proteomics analysis and multi-pharmacology activity to broaden the knowledge and therapeutic potential of this venom, as well as a proof-of-concept for an investigative pipeline to study spider-venom derived neuroactive peptides. We applied ion channel assays in a neuroblastoma cell line to investigate modulation of voltage-gated sodium and calcium channels, and nicotinic acetylcholine α7 receptor. We then investigated the venom components using mass spectrometry to identify peptide masses and sequences associated to the observed neuromodulations. Our findings showed this venom is highly complex compared to other neurotoxin-rich venoms and comprises potent modulators of voltage-gated sodium and calcium channels which were classified into 4 families of neuroactive peptides based on their activities and structures. In addition to the reported P. nigriventer neuroactive peptides, we identified at least 27 novel cysteine-rich venom peptides in which neuroactivities are still to be elucidated in voltage-gated ion channels and other potential targets. Our findings provide a new basis for studying non-explored bioactivities of known and novel neuroactive components in P. nigriventer venom, and further supports the successful application of our discovery pipeline for identifying ion channel-targeting venom peptides with potential to become drug leads with diverse exploratory and therapeutic applications.

Project description:Background: Eusociality is widely considered to evolve through kin selection, where the reproductive success of an individual’s close relative is favored at the expense of its own. High genetic relatedness is thus considered a prerequisite for eusociality. While ants are textbook examples of eusocial animals, not all ants form colonies of closely related individuals. One such example is the ectatommine ant Rhytidoponera metallica, which predominantly forms predominantly queen-less colonies that have such a low intra-colony relatedness that they have been proposed to represent a transient, unstable form of eusociality. However, R. metallica is among the most abundant and widespread ants on the Australian continent. This apparent contrast provides an example of how inclusive fitness may not by itself explain the maintenance of eusociality and raises the question of what other selective advantages maintain their eusocial lifestyle. Results: We provide a comprehensive portrait of the venom of R. metallica and show that the colony-wide venom consists of a, for an ant, exceptionally high diversity of functionally distinct toxins. These toxins have evolved under strong positive selection, which is normally expected to reduce genetic variance. Yet, R. metallica exhibits remarkable intra-colony variation, with workers sharing only a relatively small proportion of toxins in their venoms. We also find that this variation is not due to the presence of chemical castes, but that it has a genetic foundation that is at least in part explained by toxin allelic diversity. Conclusions: Taken together, our results suggest that the toxin diversity contained in R. metallica colonies may be maintained by a form of group selection, which selects for colonies that can exploit more resources and defend against a wider range of predators. We propose that increased intra-colony genetic variance resulting from low kinship may itself provide a selective advantage in the form of an expanded pharmacological venom repertoire. These findings provide an example of how group selection on adaptive phenotypes may contribute to maintaining eusociality where a prerequisite for kin selection is diminished.

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Venom proteome of the limacodid caterpillar Doratifera vulnerans

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