Dataset Information

Venomics of the Central-European Myrmicine Ants Myrmica rubra and Myrmica ruginodis

ABSTRACT: Animal venoms are a rich source of novel biomolecules with tremendous potential in medicine and agriculture. Ants represent one of the most species-rich lineages of venomous animals. However, only a fraction of their biodiversity has been studied so far. Here, we investigated the venom compositions from Myrmica rubra and Myrmica ruginodis, two members of the Myrmicinae subfamily of ants. We applied a proteo-transcriptomics based venomics workflow. Our analysis revealed that venoms of both species are composed of several protein classes, such as venom serine protease, cysteine-rich secretory proteins, antigen 5 and pathogenesis-related 1 proteins (CAP), Kunitz-type serine protease inhibitors or venom acid phosphatase. Several protein classes identified are known venom allergens, and for the first time we detected phospholipase A1 in the venom of M. ruginodis. We also identified two novel toxins of the epidermal growth factor (EGF) family in its venom proteome and an array of additional EGF-like toxins in venom gland transcriptomes of both species. They display similarity to known toxins from the related myrmecine Manica rubida and the Australian red bulldog ant Myrmecia gullosa of the Myrmeciinae subfamily and may serve as nociceptive weapons in defensive scenarios. Our work suggests that the venoms of M. rubra and M. ruginodis contain many high molecular proteins and enzymes with putatively cell damaging functions. Nevertheless, the presence of EGF-like toxins underpins that myrmicine ants also recruited smaller peptide components into their venom arsenal. Although little is known about the bioactivity and function of these EGF-like toxins, their presence in Myrmecinae and Myrmeciinae suggests that they play an important role for the venom systems of Formicoidea. Our work adds to the emerging picture of ant venoms as a source for novel biomolecules. This underlines the importance to incorporate such taxa in future venom bioprospecting programs.

INSTRUMENT(S): Orbitrap Eclipse

ORGANISM(S): Myrmica Ruginodis Myrmica Rubra

TISSUE(S): Venom Gland

SUBMITTER: Günter Lochnit

LAB HEAD: Lochnit, Guenter

PROVIDER: PXD033537 | Pride | 2022-06-09

REPOSITORIES: Pride

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Venomics of the Central European Myrmicine Ants Myrmica rubra and Myrmica ruginodis.

Hurka Sabine S Brinkrolf Karina K Özbek Rabia R Förster Frank F Billion André A Heep John J Timm Thomas T Lochnit Günter G Vilcinskas Andreas A Lüddecke Tim T

Toxins 20220521 5

Animal venoms are a rich source of novel biomolecules with potential applications in medicine and agriculture. Ants are one of the most species-rich lineages of venomous animals. However, only a fraction of their biodiversity has been studied so far. Here, we investigated the venom components of two myrmicine (subfamily Myrmicinae) ants: Myrmica rubra and Myrmica ruginodis. We applied a venomics workflow based on proteotranscriptomics and found that the venoms of both species are c ...[more]

PMID: 35622604

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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.

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:We found that assassin bugs from the earliest-diverging subfamily of higher Reduviidae (Peiratinae), as well as a subfamily closely related to Triatominae (Stenopodainae) have venom that is highly similar in composition to that produced by previously examined reduviids from Harpactorinae and Reduviinae. This finding suggests that venom composition has been largely stable due to purifying selection among the higher Reduviidae, which is consistent with the ancient origin of venom in the ancestors of Heteroptera 250–300 million years ago (Sunagar and Moran 2015; Walker et al. 2018a). This near homogeneity of venom composition is perhaps surprising considering that reduviid predators have evolved numerous instances of prey specialization and specialized hunting strategies that might be expected to co-evolve with venom. Possibly, further studies focussing on species with more specialized hunting strategies, or different kinds of venom bioactivities, will uncover more nuanced venom adaptations. Alternatively, it is possible that the protease-rich venoms of predatory reduviids are simply well-suited to myriad different hunting strategies. These data are consistent with other examples where venoms are surprisingly similar despite great differences in biology, for example between solitary and eusocial bees. A more detailed picture of venom evolution in Reduviidae would examine venom produced by the early-diverging Phymatine complex as well as venoms of non-reduviid cimicomorphs, prey specialists such as the arachnophagous Emesinae and the myrmecophagous Holoptilinae, and some of the many groups that employ hunting specializations, such as the use of plant resins to catch prey (Hwang and Weirauch 2012). Within Triatominae, examination of saliva produced by additional species from multiple lineages (especially those that switched to blood-feeding independently, if the subfamily is shown to be polyphyletic) and including generalists and specialists on different host taxa and species associated especially with nests and burrows will be informative. The venoms of predatory reduviids such as Zelurus spp. and Opisthacidius spp. that are most closely related to Triatominae, and share some behaviours such as habitation of bird nests by Opisthacidius spp. may also provide more information about the evolution of triatomine saliva.

			Action	DRS
	20210219TVLC0013-_1_.msf	Msf
	20210219TVLC0013-_1_.mzML	Mzml
	20210219TVLC0013-_1_.mzid.gz	Mzid
	20210219TVLC0013.raw	Raw
	20210219TVLC0014.msf	Msf

Dataset Information

Venomics of the Central-European Myrmicine Ants Myrmica rubra and Myrmica ruginodis

Dataset's files

Publications

Venomics of the Central European Myrmicine Ants <i>Myrmica rubra</i> and <i>Myrmica ruginodis</i>.

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