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

Sabine Hurka; Karina Brinkrolf; Rabia Özbek; Frank Förster; André Billion; John Heep; Thomas Timm; Günter Lochnit; Andreas Vilcinskas; Tim Lüddecke

doi:10.3390/toxins14050358

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

Toxins (Basel). 2022 May 21;14(5):358. doi: 10.3390/toxins14050358.

Authors

Sabine Hurka^{1

2}, Karina Brinkrolf³, Rabia Özbek⁴, Frank Förster³, André Billion⁴, John Heep¹, Thomas Timm⁵, Günter Lochnit⁵, Andreas Vilcinskas^{1

2

4}, Tim Lüddecke^{2

4}

Affiliations

¹ Institute for Insect Biotechnology, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany.
² LOEWE Centre for Translational Biodiversity Genomics (LOEWE-TBG), Senckenberganlage 25, 60325 Frankfurt, Germany.
³ Bioinformatics and Systems Biology, Justus Liebig University Giessen, Heinrich-Buff-Ring 58, 35392 Giessen, Germany.
⁴ Department of Bioresources, Fraunhofer Institute for Molecular Biology and Applied Ecology, Ohlebergsweg 12, 35392 Giessen, Germany.
⁵ Institute of Biochemistry, Justus Liebig University Giessen, Friedrichstraße 24, 35392 Giessen, Germany.

Abstract

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 composed of several protein classes, including venom serine proteases, cysteine-rich secretory protein, antigen 5 and pathogenesis-related 1 (CAP) superfamily proteins, Kunitz-type serine protease inhibitors and venom acid phosphatases. Several of these protein classes are known venom allergens, and for the first time we detected phospholipase A1 in the venom of M. ruginodis. We also identified two novel epidermal growth factor (EGF) family toxins in the M. ruginodis venom proteome and an array of additional EGF-like toxins in the venom gland transcriptomes of both species. These are similar to known toxins from the related myrmicine ant, Manica rubida, and the myrmecine (subfamily Myrmeciinae) Australian red bulldog ant Myrmecia gullosa, and are possibly deployed as weapons in defensive scenarios or to subdue prey. Our work suggests that M.rubra and M. ruginodis venoms contain many enzymes and other high-molecular-weight proteins that cause cell damage. Nevertheless, the presence of EGF-like toxins suggests that myrmicine ants have also recruited smaller peptide components into their venom arsenal. Although little is known about the bioactivity and function of EGF-like toxins, their presence in myrmicine and myrmecine ants suggests they play a key role in the venom systems of the superfamily Formicoidea. Our work adds to the emerging picture of ant venoms as a source of novel bioactive molecules and highlights the need to incorporate such taxa in future venom bioprospecting programs.

Keywords: EGF-like toxins; allergens; biodiscovery; insect venom; phospholipase A1; proteotranscriptomics.

MeSH terms

Animals
Ant Venoms*
Ants*
Australia
Biodiversity
Epidermal Growth Factor

Substances

Ant Venoms
Epidermal Growth Factor

Grants and funding

The work is a result of the Animal Venomics project embedded into the Centre for Translational Biodiversity Genomics (LOEWE–TBG) and was granted to A.V. under the program “LOEWE–Landes-Offensive zur Entwicklung Wissenschaftlich-Ökonomischer Exzellenz” of the Hessian Ministry of Higher Education, Research and the Arts. We acknowledge access to resources financially supported by the BMBF grant FKZ 031A533 within the de.NBI network. The authors also acknowledge funding supporting the LOEWE Centre for Insect Biotechnology and Bioresources.