Venom profile of the European carpenter bee Xylocopa violacea: Evolutionary and applied considerations on its toxin components

Reumont, Björn M. von; Dutertre, Sébastien; Koludarov, Ivan

doi:10.1016/j.toxcx.2022.100117

Cited by 9 publications

(11 citation statements)

References 50 publications

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“…To resolve this comprehensively would require the individual analysis of multiple specimens. However we note that studies of the congeneric X. appendiculata 13 and X. violacea 14 which used multiple individuals, present what appear to be near identical venom compositions to what we report here for X. aruana. This suggests that intra-specific variation in venom composition in X. aruana is unlikely to alter the major conclusions of our study.…”

Section: Discussionsupporting

confidence: 82%

“…The major components of the venom of the Japanese carpenter bee Xylocopa appendiculata are two 17-residue cysteine-free and amphipathic peptides, called xylopin (Xac-1) and xylopinin (Xac-2), and a venom phospholipase-A 2 12,13 . Finally, a recent study of the venom of Xylocopa violacea revealed that it is largely composed of melittin/xylopin-like peptides, apamin-like peptides and phospholipase-A 2 14 . Venom composition and venom toxin bioactivity, like other phenotypic traits, are frequently adapted to the specific ecological niches occupied by the organisms that produce them.…”

Section: Openmentioning

confidence: 99%

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Venom composition and pain-causing toxins of the Australian great carpenter bee Xylocopa aruana

Shi

Szanto

et al. 2022

Sci Rep

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Most species of bee are capable of delivering a defensive sting which is often painful. A solitary lifestyle is the ancestral state of bees and most extant species are solitary, but information on bee venoms comes predominantly from studies on eusocial species. In this study we investigated the venom composition of the Australian great carpenter bee, Xylocopa aruana Ritsema, 1876. We show that the venom is relatively simple, composed mainly of one small amphipathic peptide (XYTX1-Xa1a), with lesser amounts of an apamin homologue (XYTX2-Xa2a) and a venom phospholipase-A2 (PLA2). XYTX1-Xa1a is homologous to, and shares a similar mode-of-action to melittin and the bombilitins, the major components of the venoms of the eusocial Apis mellifera (Western honeybee) and Bombus spp. (bumblebee), respectively. XYTX1-Xa1a and melittin directly activate mammalian sensory neurons and cause spontaneous pain behaviours in vivo, effects which are potentiated in the presence of venom PLA2. The apamin-like peptide XYTX2-Xa2a was a relatively weak blocker of small conductance calcium-activated potassium (KCa) channels and, like A. mellifera apamin and mast cell-degranulating peptide, did not contribute to pain behaviours in mice. While the composition and mode-of-action of the venom of X. aruana are similar to that of A. mellifera, the greater potency, on mammalian sensory neurons, of the major pain-causing component in A. mellifera venom may represent an adaptation to the distinct defensive pressures on eusocial Apidae.

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Section: Discussionsupporting

confidence: 82%

Section: Openmentioning

confidence: 99%

Venom composition and pain-causing toxins of the Australian great carpenter bee Xylocopa aruana

Shi

Szanto

et al. 2022

Sci Rep

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“…The venom compositions and species-specific differences (especially for H. scabiosa ) will be discussed in-depth elsewhere (see von Reumont etal. 2022 for X. violacea 21 ). In general, the new profiles corroborate our selection of prevalent bee venom proteins (Figure 2).…”

Section: Resultsmentioning

confidence: 99%

“…Unsurprisingly, given their economic significance, honeybee and bumblebee venoms have received the lion"s share of toxinological attention, and are among the bestcharacterized venoms in the animal kingdom 16,17 . The venoms of the remaining species of the hymenopteran radiation, however, including the majority of bees, remain largely unexplored despite recent proteo-transcriptomic studies on several ant and wasp species [18][19][20][21] . Where studies of lesserknown Hymenoptera have been conducted, they typically deal with single crude fractions or even individual components either due to technical limitations at the time or because of applied research focus 16,22,23 .…”

mentioning

confidence: 99%

A common venomous ancestor? Prevalent bee venom genes evolved before the aculeate stinger while few major toxins are bee-specific

Koludarov

Velasque

Lochnit

et al. 2022

Preprint

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Venoms have convergently evolved in all major animal lineages and are ideal candidates to unravel the genomic processes underlying convergent trait evolution. However, few animal groups have been studied in detail, and large-scale comparative genomic analyses to address toxin gene evolution are rare. The hyper-diverse hymenopterans are the most speciose group of venomous animals, but the origin of their toxin genes has been largely overlooked. We combined proteo-transcriptomics with comparative genomics compiling an up-to-date list of core bee venom proteins to investigate the origin of 11 venom genes in 30 hymenopteran genomes including two newly sequenced genomes of stingless bees. We found a more distinct pattern in which toxin genes originated predominantly by single gene co-option, a prevalent mechanism in parasitoid wasps. These are always accompanied by parallel expansion events in other bee and hymenopteran sister gene groups. The short toxic peptides melittin and apamin appear to be unique to bees, a result supported by a novel machine learning approach. Based on the syntenic pattern we propose here Anthophilin1 as a bee-unique gene family that includes apamin and MCDP. It appears that bees co-adapted their venom genes which predominantly already existed before the aculeate ovipositor evolved to a stinger which exclusively injects venom. Our results provide insight into the large-scale evolution of bee venom compounds, and we present here the first study revealing general processes of venom evolution at a comparative genomic level for this mega-diverse Hymenoptera.

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“…Only a small subset of species has been studied, and few analyses have been conducted focusing on solitary bee species to identify and test anti-microbial peptides. Recently, the venoms of the solitary bees Xylocopa violacea and Halictus scabiosae (and complementary Apis mellifera) were proteo-transcriptomically analyzed in combination with comparative genomics to unravel the evolution of prevalent bee venom genes [7,19]. Interestingly, most of the small peptides identified in the solitary bees such as halictin (Hal), codesane (Cod), xylopin (Xac), melectin (Mel), and osmin (Osm) were identified as variants of melittin, which is a toxin family unique to bees sensu lato [7].…”

Section: Introductionmentioning

confidence: 99%

The Pharmacological Potential of Novel Melittin Variants from the Honeybee and Solitary Bees against Inflammation and Cancer

Erkoc

Reumont

Lüddecke

et al. 2022

Toxins

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The venom of honeybees is composed of numerous peptides and proteins and has been used for decades as an anti-inflammatory and anti-cancer agent in traditional medicine. However, the bioactivity of specific biomolecular components has been evaluated for the predominant constituent, melittin. So far, only a few melittin-like peptides from solitary bee species have been investigated, and the molecular mechanisms of bee venoms as therapeutic agents remain largely unknown. Here, the preclinical pharmacological activities of known and proteo-transcriptomically discovered new melittin variants from the honeybee and more ancestral variants from phylogenetically older solitary bees were explored in the context of cancer and inflammation. We studied the effects of melittin peptides on cytotoxicity, second messenger release, and inflammatory markers using primary human cells, non-cancer, and cancerous cell lines. Melittin and some of its variants showed cytotoxic effects, induced Ca2+ signaling and inhibited cAMP production, and prevented LPS-induced NO synthesis but did not affect the IP3 signaling and pro-inflammatory activation of endothelial cells. Compared to the originally-described melittin, some phylogenetically more ancestral variants from solitary bees offer potential therapeutic modalities in modulating the in vitro inflammatory processes, and hindering cancer cell viability/proliferation, including aggressive breast cancers, and are worth further investigation.

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Venom profile of the European carpenter bee Xylocopa violacea: Evolutionary and applied considerations on its toxin components

Cited by 9 publications

References 50 publications

Venom composition and pain-causing toxins of the Australian great carpenter bee Xylocopa aruana

Venom composition and pain-causing toxins of the Australian great carpenter bee Xylocopa aruana

A common venomous ancestor? Prevalent bee venom genes evolved before the aculeate stinger while few major toxins are bee-specific

The Pharmacological Potential of Novel Melittin Variants from the Honeybee and Solitary Bees against Inflammation and Cancer

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