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Context-dependent venom deployment and protein composition in two assassin bugs.

ABSTRACT: The Heteroptera are a diverse suborder of phytophagous, hematophagous, and zoophagous insects. The shift to zoophagy can be traced back to the transformation of salivary glands into venom glands, but the venom is used not only to kill and digest invertebrate prey but also as a defense strategy, mainly against vertebrates. In this study, we used an integrated transcriptomics and proteomics approach to compare the composition of venoms from the anterior main gland (AMG) and posterior main gland (PMG) of the reduviid bugs Platymeris biguttatus L. and Psytalla horrida Stål. In both species, the AMG and PMG secreted distinct protein mixtures with few interspecific differences. PMG venom consisted mostly of S1 proteases, redulysins, Ptu1-like peptides, and uncharacterized proteins, whereas AMG venom contained hemolysins and cystatins. There was a remarkable difference in biological activity between the AMG and PMG venoms, with only PMG venom conferring digestive, neurotoxic, hemolytic, antibacterial, and cytotoxic effects. Proteomic analysis of venom samples revealed the context-dependent use of AMG and PMG venom. Although both species secreted PMG venom alone to overwhelm their prey and facilitate digestion, the deployment of defensive venom was species-dependent. P. biguttatus almost exclusively used PMG venom for defense, whereas P. horrida secreted PMG venom in response to mild harassment but AMG venom in response to more intense harassment. This intriguing context-dependent use of defensive venom indicates that future research should focus on species-dependent differences in venom composition and defense strategies among predatory Heteroptera.

SUBMITTER: Fischer ML

PROVIDER: S-EPMC7520181 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Context-dependent venom deployment and protein composition in two assassin bugs.

Fischer Maike L ML Wielsch Natalie N Heckel David G DG Vilcinskas Andreas A Vogel Heiko H

Ecology and evolution 20200817 18

The Heteroptera are a diverse suborder of phytophagous, hematophagous, and zoophagous insects. The shift to zoophagy can be traced back to the transformation of salivary glands into venom glands, but the venom is used not only to kill and digest invertebrate prey but also as a defense strategy, mainly against vertebrates. In this study, we used an integrated transcriptomics and proteomics approach to compare the composition of venoms from the anterior main gland (AMG) and posterior main gland (P ...[more]

PMID: 33005355

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Project description:Assassin bugs are one of the most successful clades of predatory animals based on their species numbers (∼6,800 spp.) and wide distribution in terrestrial ecosystems. Various novel prey capture strategies and remarkable prey specializations contribute to their appeal as a model to study evolutionary pathways involved in predation. Here, we reconstruct the most comprehensive reduviid phylogeny (178 taxa, 18 subfamilies) to date based on molecular data (5 markers). This phylogeny tests current hypotheses on reduviid relationships emphasizing the polyphyletic Reduviinae and the blood-feeding, disease-vectoring Triatominae, and allows us, for the first time in assassin bugs, to reconstruct ancestral states of prey associations and microhabitats. Using a fossil-calibrated molecular tree, we estimated divergence times for key events in the evolutionary history of Reduviidae. Our results indicate that the polyphyletic Reduviinae fall into 11-14 separate clades. Triatominae are paraphyletic with respect to the reduviine genus Opisthacidius in the maximum likelihood analyses; this result is in contrast to prior hypotheses that found Triatominae to be monophyletic or polyphyletic and may be due to the more comprehensive taxon and character sampling in this study. The evolution of blood-feeding may thus have occurred once or twice independently among predatory assassin bugs. All prey specialists evolved from generalist ancestors, with multiple evolutionary origins of termite and ant specializations. A bark-associated life style on tree trunks is ancestral for most of the lineages of Higher Reduviidae; living on foliage has evolved at least six times independently. Reduviidae originated in the Middle Jurassic (178 Ma), but significant lineage diversification only began in the Late Cretaceous (97 Ma). The integration of molecular phylogenetics with fossil and life history data as presented in this paper provides insights into the evolutionary history of reduviids and clears the way for in-depth evolutionary hypothesis testing in one of the most speciose clades of predators.

Project description:Assassin bugs (Hemiptera: Heteroptera: Reduviidae) are venomous insects that prey on invertebrates. Assassin bug venom has features in common with venoms from other animals, such as paralysing and lethal activity when injected, and a molecular composition that includes disulfide-rich peptide neurotoxins. Uniquely, this venom also has strong liquefying activity that has been hypothesised to facilitate feeding through the narrow channel of the proboscis—a structure inherited from sap- and phloem-feeding phytophagous hemipterans and adapted during the evolution of Heteroptera into a fang and feeding structure. However, further understanding of the function of assassin bug venom is impeded by the lack of proteomic studies detailing its molecular composition. In addition, the lack of knowledge regarding venoms of predaceous reduviids limits our understanding of how the venoms of the blood-feeding kissing bugs (Reduviidae: Triatominae) evolved to facilitate hematophagy. By using a combined transcriptomic/proteomic approach we show that the venom proteome of the harpactorine assassin bug Pristhesancus plagipennis includes a complex suite of >100 proteins comprising disulfide-rich peptides, CUB-domain proteins, cystatins, putative cytolytic toxins, triabin-like protein, odorant binding protein, serine proteases, catabolic enzymes, putative nutrient-binding proteins, plus eight families of proteins without homology to characterised proteins. Serine proteases, CUB domain proteins and other novel proteins in the 10–16 kDa mass range, as well as putative cytolytic toxins, were the most abundant venom components. Thus, in addition to putative neurotoxins, assassin bug venom includes a high proportion of enzymatic and cytolytic venom components well suited to tissue liquefaction. While some protein families such as lipocalin/triabins occur in the venoms of both predaceous and blood-feeding reduviids, the composition of venoms in these two groups differs markedly. These results provide insights into the venom evolution in the insect suborder Heteroptera.

Project description:Assassin bugs (Hemiptera: Heteroptera: Reduviidae) are venomous insects, most of which prey on invertebrates. Assassin bug venom has features in common with venoms from other animals, such as paralyzing and lethal activity when injected, and a molecular composition that includes disulfide-rich peptide neurotoxins. Uniquely, this venom also has strong liquefying activity that has been hypothesized to facilitate feeding through the narrow channel of the proboscis-a structure inherited from sap- and phloem-feeding phytophagous hemipterans and adapted during the evolution of Heteroptera into a fang and feeding structure. However, further understanding of the function of assassin bug venom is impeded by the lack of proteomic studies detailing its molecular composition.By using a combined transcriptomic/proteomic approach, we show that the venom proteome of the harpactorine assassin bug Pristhesancus plagipennis includes a complex suite of >100 proteins comprising disulfide-rich peptides, CUB domain proteins, cystatins, putative cytolytic toxins, triabin-like protein, odorant-binding protein, S1 proteases, catabolic enzymes, putative nutrient-binding proteins, plus eight families of proteins without homology to characterized proteins. S1 proteases, CUB domain proteins, putative cytolytic toxins, and other novel proteins in the 10-16-kDa mass range, were the most abundant venom components. Thus, in addition to putative neurotoxins, assassin bug venom includes a high proportion of enzymatic and cytolytic venom components likely to be well suited to tissue liquefaction. Our results also provide insight into the trophic switch to blood-feeding by the kissing bugs (Reduviidae: Triatominae). Although some protein families such as triabins occur in the venoms of both predaceous and blood-feeding reduviids, the composition of venoms produced by these two groups is revealed to differ markedly. These results provide insights into the venom evolution in the insect suborder Heteroptera.

Dataset Information

Context-dependent venom deployment and protein composition in two assassin bugs.

Publications

Context-dependent venom deployment and protein composition in two assassin bugs.

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