Venomics survey of six myrmicine ants provides insights into the molecular and structural diversity of their peptide toxins

Barassé, Valentine; Téné, Nathan; Klopp, Christophe; Paquet, Françoise; Tysklind, Niklas; Troispoux, Valérie; Lalagüe, Hadrien; Orivel, Jérôme; Lefranc, Benjamin; Leprince, Jérôme; Kenné, Martin; Tindo, Maurice; Treilhou, Michel; Touchard, Axel; Bonnafé, Elsa

doi:10.1016/j.ibmb.2022.103876

Cited by 7 publications

(4 citation statements)

References 58 publications

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“…Among the species that use their venom exclusively for predation, A. emarginatus and D. armigerum are associated with a complete shift in venom bioactivities that correlate with a switch to a neurotoxic venom composition. The venom of D. armigerum showed a unique profile, as previously reported (18), and our analysis confirmed that this venom consists of a single family of peptides (dimeric MYRTX, family 61) that display some amino acid sequence similarity with the neurotoxic U 11 venom peptide from Tetramorium bicarinatum (34) ( SI Appendix , Figure S20 ). Given the lack of cytotoxicity but strong paralytic activity on blowflies and inhibition of cell membrane potential, these data suggest that D. armigerum has an insect neurotoxic venom.…”

Section: Resultssupporting

confidence: 87%

“…feigning death) (16), escape behavior (17), or rely on morphological attributes such as spines as a deterrent rather than using their sting against vertebrate predators (7). Among different lineages of stinging ants, venoms can exhibit very different peptide toxin profiles (18, 19), presumably in response to distinct ecological pressures. To date, no studies have integrated ecological traits, biochemical composition, and bioactivity in a phylogenetic framework to explore the factors that lead to distinct venom compositions in ants and, more broadly, very few in other venomous lineages (20).…”

Section: Introductionmentioning

confidence: 99%

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Adaptive trade-offs between vertebrate defense and insect predation drive ant venom evolution

Touchard,

Robinson,

Lalagüe

et al. 2024

Preprint

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Stinging ants have diversified into various ecological niches, and several evolutionary drivers may have contributed to shape the composition of their venom. To comprehend the drivers underlying venom variation in ants, we selected 15 Neotropical species and recorded a range of traits, including ecology, morphology, and venom bioactivity. Principal component analysis of both morphological and venom bioactivity traits revealed that stinging ants display two functional strategies. Additionally, phylogenetic comparative analysis indicated that venom function (predatory, defensive, or both) and mandible morphology significantly correlate with venom bioactivity and amount, while pain-inducing activity trades off with insect paralysis. Further analysis of the venom biochemistry of the 15 species revealed switches between cytotoxic and neurotoxic venom compositions in some species. This study highlights the fact that ant venoms are not homogenous, and for some species, there are major shifts in venom composition associated with the diversification of venom ecological functions.SignificanceVenoms are under severe evolutionary pressures, exerted either on the innovation of toxins or the reduction of the metabolic cost of production (1). To reduce the metabolic costs associated with venom secretion, some venomous animals can regulate venom expenditure by metering the amount of venom injected and by switching between offensive and defensive compositions (2–2). Many ants use venom for subduing a wide range of arthropod prey, as well as for defensive purposes against invertebrates and vertebrates, but are unable to adapt venom composition to stimuli (5, 6). Consequently, the expression of venom genes directly affects the ability of ants to interact with the biotic environment, and the venom composition may be fine-tuned to the ecology of each species. A previous study showed that defensive traits in ants exhibit an evolutionary trade-off in which the presence of a sting is negatively correlated with several other defensive traits, further supporting that trade-offs in defensive traits significantly constrain trait evolution and influence species diversification in ants (7). However, the sting is not used for the same purpose depending on the ant species. Our study supports an evolutionary trade-off between the ability of venom to deter vertebrates and to paralyze insects which are correlated with different life history strategies among Formicidae.

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Section: Resultssupporting

confidence: 87%

Section: Introductionmentioning

confidence: 99%

Adaptive trade-offs between vertebrate defense and insect predation drive ant venom evolution

Touchard,

Robinson,

Lalagüe

et al. 2024

Preprint

Self Cite

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“…In order to fully characterize the venoms of aculeates, a comparative study of venomgland transcriptomes and proteomes is necessary. In recent years, the number of studies that included these data for hymenopterans has increased, but in the face of the enormous diversity of the order, it is clear that the research community has only started to scratch the surface of what there is to be discovered [ 62 , 78 , 91 , 92 , 93 , 94 , 95 , 96 , 97 , 98 , 99 , 100 , 101 , 102 , 103 , 104 ]. One interesting aspect of our own contribution to this enormous task is that the transcripts we identified from the venom gland of A. mellifera were found to have nearly identical sequences to other A. mellifera venom proteins which are available in the Uniprot database ( Figure 2 ) and those identified by Koludarov et al [ 78 ].…”

Section: Discussionmentioning

confidence: 99%

Functional and Proteomic Insights into Aculeata Venoms

Dashevsky

Baumann

Undheim

et al. 2023

Toxins

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Aculeate hymenopterans use their venom for a variety of different purposes. The venom of solitary aculeates paralyze and preserve prey without killing it, whereas social aculeates utilize their venom in defence of their colony. These distinct applications of venom suggest that its components and their functions are also likely to differ. This study investigates a range of solitary and social species across Aculeata. We combined electrophoretic, mass spectrometric, and transcriptomic techniques to characterize the compositions of venoms from an incredibly diverse taxon. In addition, in vitro assays shed light on their biological activities. Although there were many common components identified in the venoms of species with different social behavior, there were also significant variations in the presence and activity of enzymes such as phospholipase A2s and serine proteases and the cytotoxicity of the venoms. Social aculeate venom showed higher presence of peptides that cause damage and pain in victims. The venom-gland transcriptome from the European honeybee (Apis mellifera) contained highly conserved toxins which match those identified by previous investigations. In contrast, venoms from less-studied taxa returned limited results from our proteomic databases, suggesting that they contain unique toxins.

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“…Until recently, alkaloids in the venom of ants have been relatively well-studied [ 9 ], while other venomous chemical compounds and proteinaceous venoms remain largely unveiled. Proteinaceous venom components have only been deciphered in a limited number of ants from several subfamilies including Ectatomminae, Myrmeciinae, Myrmicinae, Ponerinae, Paraponerinae, and Pseudomyrmecinae, mostly focused on emblematic species [ 10 , 11 , 12 , 13 , 14 , 15 , 16 , 17 ]. The characterization of venom components from more ant species belonging to diverse subfamilies will contribute to a better understanding of the evolution of ant venoms and facilitate their applications.…”

Section: Introductionmentioning

confidence: 99%

Proteinaceous Venom Expression of the Yellow Meadow Ant, Lasius flavus (Hymenoptera: Formicidae)

Wang

Xiao

et al. 2023

Toxins

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Ants are one of the important groups of venomous animals with about 14,000 described species. Studies so far focused on the discovery of venom proteins are only available for limited stinging ants, and the proteinaceous compositions of the stingless ants are completely unknown. Here, we used the transcriptomic approach to identify venom components from the yellow meadow ant, Lasius flavus, a stingless ant. The transcriptomic analysis yielded an extraordinary simplicity of the venom expression profile, with 17 venom proteins, such as phospholipase B, odorant binding protein, and apolipoprotein D. Ten of them were discovered as novel toxins for future functional investigations. Quantitative real time PCR analysis revealed that genes encoding the identified venom proteins display exclusively or highly expression profiles in venom glands, validating them as venom compositions. Our findings contribute to the understanding of the evolutional diversity of toxins between stinging and stingless ants.

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Venomics survey of six myrmicine ants provides insights into the molecular and structural diversity of their peptide toxins

Cited by 7 publications

References 58 publications

Adaptive trade-offs between vertebrate defense and insect predation drive ant venom evolution

Adaptive trade-offs between vertebrate defense and insect predation drive ant venom evolution

Functional and Proteomic Insights into Aculeata Venoms

Proteinaceous Venom Expression of the Yellow Meadow Ant, Lasius flavus (Hymenoptera: Formicidae)

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