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.

Hexapod Assassins’ Potion: Venom Composition and Bioactivity from the Eurasian Assassin Bug Rhynocoris iracundus

“…However, as it was observed with R. personatus and for other assassin bug species [25,57], R. iracundus venom also caused potent, quick and generalized paralysis in the entire insect body. This is in accordance with previous suggestions [25,27,57] that paralysis is not the result of localized cell membrane disruption, but it is due to molecular components of the venom targeting nerve cells. The neurotoxic effects on prey could be attributed, probably among other factors, to the presence of Ptu1 [26].…”

“…In 1961, the paralysis observed in assassin bug prey was attributed to the disruption of cell membranes [23]. However, as it was observed with R. personatus and for other assassin bug species [25,57], R. iracundus venom also caused potent, quick and generalized paralysis in the entire insect body. This is in accordance with previous suggestions [25,27,57] that paralysis is not the result of localized cell membrane disruption, but it is due to molecular components of the venom targeting nerve cells.…”

Crouching Tiger, Hidden Protein: Searching for Insecticidal Toxins in Venom of the Red Tiger Assassin Bug (Havinthus rufovarius)

“…Since it has previously been reported that electrostimulation and harassment of assassin bugs can yield different venoms from different gland lumens [ 4 , 12 , 13 ], we investigated if this was also true for H. rufovarius ( Figure 1 ). Although venom could be obtained by either stimulus, venom obtained by electrostimulation and harassment of H. rufovarius yielded similar mass profiles using matrix-assisted laser desorption/ionisation time-of-flight mass spectrometry (MALDI-TOF-MS) using a 5800 MALDI-TOF instrument (SCIEX, Framingham, MA, USA) ( Figure 2 ).…”

“…This may be due to the complexity of the nerve-muscle systems involved in regulating venom injection [ 4 ] or species-specific differences among assassin bugs [ 12 , 13 , 14 ]. The spectra obtained revealed venom components with monoisotopic masses of 3735.7, 3826, 3509.5, and 2880.6 Da that may represent venom peptides.…”

“…In P. plagipennis venom, CUB domain protein 1 is one of five solitary CUB domain proteins, and among the most abundant protein in the venom [ 10 ]. Contigs encoding similar solitary CUB domain proteins have also been reported in a cDNA library enriched for proteins selectively expressed in the venom gland of a related cimicomorphan heteropteran, the minute pirate bug Orius laevigatus [ 13 ], suggesting they may be present in a broad phylogenetic range of heteropteran venoms. While the phylogeny of Australian assassin bugs is poorly characterised, P. plagipennis and H. rufovarius both belong to the tribe Harpactorini in the subfamily Harpactorinae.…”