{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T02:48:50Z","timestamp":1790650130360,"version":"4.1.0"},"reference-count":94,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2022,5,21]],"date-time":"2022-05-21T00:00:00Z","timestamp":1653091200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"BMBF","award":["FKZ 031A533"],"award-info":[{"award-number":["FKZ 031A533"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Toxins"],"abstract":"<jats:p>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.<\/jats:p>","DOI":"10.3390\/toxins14050358","type":"journal-article","created":{"date-parts":[[2022,5,21]],"date-time":"2022-05-21T09:18:08Z","timestamp":1653124688000},"page":"358","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":26,"title":["Venomics of the Central European Myrmicine Ants Myrmica rubra and Myrmica ruginodis"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-2083-5198","authenticated-orcid":false,"given":"Sabine","family":"Hurka","sequence":"first","affiliation":[{"name":"Institute for Insect Biotechnology, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany"},{"name":"LOEWE Centre for Translational Biodiversity Genomics (LOEWE-TBG), Senckenberganlage 25, 60325 Frankfurt, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0253-0024","authenticated-orcid":false,"given":"Karina","family":"Brinkrolf","sequence":"additional","affiliation":[{"name":"Bioinformatics and Systems Biology, Justus Liebig University Giessen, Heinrich-Buff-Ring 58, 35392 Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6756-384X","authenticated-orcid":false,"given":"Rabia","family":"\u00d6zbek","sequence":"additional","affiliation":[{"name":"Department of Bioresources, Fraunhofer Institute for Molecular Biology and Applied Ecology, Ohlebergsweg 12, 35392 Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4166-5423","authenticated-orcid":false,"given":"Frank","family":"F\u00f6rster","sequence":"additional","affiliation":[{"name":"Bioinformatics and Systems Biology, Justus Liebig University Giessen, Heinrich-Buff-Ring 58, 35392 Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5073-3347","authenticated-orcid":false,"given":"Andr\u00e9","family":"Billion","sequence":"additional","affiliation":[{"name":"Department of Bioresources, Fraunhofer Institute for Molecular Biology and Applied Ecology, Ohlebergsweg 12, 35392 Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4412-4748","authenticated-orcid":false,"given":"John","family":"Heep","sequence":"additional","affiliation":[{"name":"Institute for Insect Biotechnology, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8569-7537","authenticated-orcid":false,"given":"Thomas","family":"Timm","sequence":"additional","affiliation":[{"name":"Institute of Biochemistry, Justus Liebig University Giessen, Friedrichstra\u00dfe 24, 35392 Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0377-395X","authenticated-orcid":false,"given":"G\u00fcnter","family":"Lochnit","sequence":"additional","affiliation":[{"name":"Institute of Biochemistry, Justus Liebig University Giessen, Friedrichstra\u00dfe 24, 35392 Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8276-4968","authenticated-orcid":false,"given":"Andreas","family":"Vilcinskas","sequence":"additional","affiliation":[{"name":"Institute for Insect Biotechnology, Justus Liebig University Giessen, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany"},{"name":"LOEWE Centre for Translational Biodiversity Genomics (LOEWE-TBG), Senckenberganlage 25, 60325 Frankfurt, Germany"},{"name":"Department of Bioresources, Fraunhofer Institute for Molecular Biology and Applied Ecology, Ohlebergsweg 12, 35392 Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7234-8685","authenticated-orcid":false,"given":"Tim","family":"L\u00fcddecke","sequence":"additional","affiliation":[{"name":"LOEWE Centre for Translational Biodiversity Genomics (LOEWE-TBG), Senckenberganlage 25, 60325 Frankfurt, Germany"},{"name":"Department of Bioresources, Fraunhofer Institute for Molecular Biology and Applied Ecology, Ohlebergsweg 12, 35392 Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,5,21]]},"reference":[{"key":"ref_1","unstructured":"(2022, March 02). California Academy of Science AntWeb. Version 8.69.2. Available online: https:\/\/www.antweb.org\/."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1146\/annurev-ecolsys-120213-091824","article-title":"The Phylogeny and Evolution of Ants","volume":"45","author":"Ward","year":"2014","journal-title":"Annu. Rev. Ecol. Evol. Syst."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"H\u00f6lldobler, B., and Wilson, E.O. (1990). The Ants, Harvard University Press.","DOI":"10.1007\/978-3-662-10306-7"},{"key":"ref_4","unstructured":"Piek, T. (1986). Chemistry, Pharmacology, and Chemical Ecology of Ant Venoms. Venoms of the Hymenoptera: Biochemical, Pharmacological and Behavioural Aspects, Academic Press."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1016\/j.tree.2012.10.020","article-title":"Complex Cocktails: The Evolutionary Novelty of Venoms","volume":"28","author":"Casewell","year":"2013","journal-title":"Trends Ecol. Evol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1146\/annurev.genom.9.081307.164356","article-title":"The Toxicogenomic Multiverse: Convergent Recruitment of Proteins Into Animal Venoms","volume":"10","author":"Fry","year":"2009","journal-title":"Annu. Rev. Genom. Hum. Genet."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Schendel, V., Rash, L.D., Jenner, R.A., and Undheim, E.A.B. (2019). The Diversity of Venom: The Importance of Behavior and Venom System Morphology in Understanding Its Ecology and Evolution. Toxins, 11.","DOI":"10.3390\/toxins11110666"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1071\/ZO9680133","article-title":"A Morphological and Functional Study of the Venom Apparatus in Representatives of Some Major Groups of Hymenoptera","volume":"16","author":"Robertson","year":"1968","journal-title":"Aust. J. Zool."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1146\/annurev-ento-072821-063525","article-title":"On the Biological Diversity of Ant Alkaloids","volume":"67","author":"Fox","year":"2022","journal-title":"Annu. Rev. Entomol."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Touchard, A., Aili, S., Fox, E., Escoubas, P., Orivel, J., Nicholson, G., and Dejean, A. (2016). The Biochemical Toxin Arsenal from Ant Venoms. Toxins, 8.","DOI":"10.3390\/toxins8010030"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"166","DOI":"10.1016\/j.toxicon.2014.10.021","article-title":"Diversity of Peptide Toxins from Stinging Ant Venoms","volume":"92","author":"Aili","year":"2014","journal-title":"Toxicon"},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Barass\u00e9, V., Touchard, A., T\u00e9n\u00e9, N., Tindo, M., Kenne, M., Klopp, C., Dejean, A., Bonnaf\u00e9, E., and Treilhou, M. (2019). The Peptide Venom Composition of the Fierce Stinging Ant Tetraponera aethiops (Formicidae: Pseudomyrmecinae). Toxins, 11.","DOI":"10.3390\/toxins11120732"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"3503","DOI":"10.1021\/acs.jproteome.8b00452","article-title":"Deciphering the Molecular Diversity of an Ant Venom Peptidome through a Venomics Approach","volume":"17","author":"Touchard","year":"2018","journal-title":"J. Proteome Res."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1800","DOI":"10.1021\/acs.jproteome.0c00048","article-title":"Venom Peptide Repertoire of the European Myrmicine Ant Manica rubida: Identification of Insecticidal Toxins","volume":"19","author":"Touchard","year":"2020","journal-title":"J. Proteome Res."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Aili, S.R., Touchard, A., Hayward, R., Robinson, S.D., Pineda, S.S., Lalag\u00fce, H., Vetter, I., Undheim, E.A.B., Kini, R.M., and Escoubas, P. (2020). An Integrated Proteomic and Transcriptomic Analysis Reveals the Venom Complexity of the Bullet Ant Paraponera clavata. Toxins, 12.","DOI":"10.3390\/toxins12050324"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1016\/j.toxicon.2014.05.022","article-title":"Venom Toxicity and Composition in Three Pseudomyrmex Ant Species Having Different Nesting Modes","volume":"88","author":"Touchard","year":"2014","journal-title":"Toxicon"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1339","DOI":"10.1021\/acs.jproteome.6b00948","article-title":"Combined Peptidomic and Proteomic Analysis of Electrically Stimulated and Manually Dissected Venom from the South American Bullet Ant Paraponera clavata","volume":"16","author":"Aili","year":"2017","journal-title":"J. Proteome Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1002\/rcm.7116","article-title":"The Complexity and Structural Diversity of Ant Venom Peptidomes Is Revealed by Mass Spectrometry Profiling","volume":"29","author":"Touchard","year":"2015","journal-title":"Rapid. Commun. Mass Spectrom."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"100005","DOI":"10.1016\/j.toxcx.2018.100005","article-title":"Can We Resolve the Taxonomic Bias in Spider Venom Research?","volume":"1","author":"Herzig","year":"2019","journal-title":"Toxicon X"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"L\u00fcddecke, T., Vilcinskas, A., and Lemke, S. (2019). Phylogeny-Guided Selection of Priority Groups for Venom Bioprospecting: Harvesting Toxin Sequences in Tarantulas as a Case Study. Toxins, 11.","DOI":"10.3390\/toxins11090488"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"163","DOI":"10.3389\/fevo.2019.00163","article-title":"The Significance of Comparative Genomics in Modern Evolutionary Venomics","volume":"7","author":"Drukewitz","year":"2019","journal-title":"Front. Ecol. Evol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"eaau4640","DOI":"10.1126\/sciadv.aau4640","article-title":"A Comprehensive Portrait of the Venom of the Giant Red Bull Ant, Myrmecia gulosa, Reveals a Hyperdiverse Hymenopteran Toxin Gene Family","volume":"4","author":"Robinson","year":"2018","journal-title":"Sci. Adv."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Ceolin Mariano, D.O., de Oliveira, \u00da.C., Zaharenko, A.J., Pimenta, D.C., R\u00e1dis-Baptista, G., and Prieto-da-Silva, \u00c1.R.d.B. (2019). Bottom-Up Proteomic Analysis of Polypeptide Venom Components of the Giant Ant Dinoponera quadriceps. Toxins, 11.","DOI":"10.3390\/toxins11080448"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e21424","DOI":"10.1002\/arch.21424","article-title":"Proteomic Analysis of the Venom of the Predatory Ant Pachycondyla striata (Hymenoptera: Formicidae)","volume":"96","author":"Santos","year":"2017","journal-title":"Arch. Insect Biochem. Physiol."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Heep, J., Klaus, A., Kessel, T., Seip, M., Vilcinskas, A., and Skaljac, M. (2019). Proteomic Analysis of the Venom from the Ruby Ant Myrmica rubra and the Isolation of a Novel Insecticidal Decapeptide. Insects, 10.","DOI":"10.3390\/insects10020042"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"1222","DOI":"10.1111\/cea.13224","article-title":"Towards Complete Identification of Allergens in Jack Jumper (Myrmecia pilosula) Ant Venom and Their Clinical Relevance: An Immunoproteomic Approach","volume":"48","author":"Wanandy","year":"2018","journal-title":"Clin. Exp. Allergy"},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Pessoa, W.F.B., Silva, L.C.C., De Oliveira Dias, L., Delabie, J.H.C., Costa, H., and Romano, C.C. (2016). Analysis of Protein Composition and Bioactivity of Neoponera villosa Venom (Hymenoptera: Formicidae). Int. J. Mol. Sci., 17.","DOI":"10.3390\/ijms17040513"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"Holding, M.L., Margres, M.J., Mason, A.J., Parkinson, C.L., and Rokyta, D.R. (2018). Evaluating the Performance of De Novo Assembly Methods for Venom-Gland Transcriptomics. Toxins, 10.","DOI":"10.3390\/toxins10060249"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"von Reumont, B.M. (2018). Studying Smaller and Neglected Organisms in Modern Evolutionary Venomics Implementing RNASeq (Transcriptomics)\u2014A Critical Guide. Toxins, 10.","DOI":"10.3390\/toxins10070292"},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Smith, J.J., and Undheim, E.A.B. (2018). True Lies: Using Proteomics to Assess the Accuracy of Transcriptome-Based Venomics in Centipedes Uncovers False Positives and Reveals Startling Intraspecific Variation in Scolopendra subspinipes. Toxins, 10.","DOI":"10.3390\/toxins10030096"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"e2112630119","DOI":"10.1073\/pnas.2112630119","article-title":"A Peptide Toxin in Ant Venom Mimics Vertebrate EGF-like Hormones to Cause Long-Lasting Hypersensitivity in Mammals","volume":"119","author":"Eagles","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"510","DOI":"10.1002\/iub.186","article-title":"Serine Proteases","volume":"61","year":"2009","journal-title":"IUBMB Life"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Choo, Y.M., Lee, K.S., Yoon, H.J., Kim, B.Y., Sohn, M.R., Roh, J.Y., Je, Y.H., Kim, N.J., Kim, I., and Woo, S.D. (2010). Dual Function of a Bee Venom Serine Protease: Prophenoloxidase-Activating Factor in Arthropods and Fibrin(Ogen)Olytic Enzyme in Mammals. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0010393"},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Choo, Y.M., Lee, K.S., Yoon, H.J., Qiu, Y., Wan, H., Sohn, M.R., Sohn, H.D., and Jin, B.R. (2012). Antifibrinolytic Role of a Bee Venom Serine Protease Inhibitor That Acts as a Plasmin Inhibitor. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0032269"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1016\/j.ibmb.2004.03.003","article-title":"Towards a Comprehensive View of the Primary Structure of Venom Proteins from the Parasitoid Wasp Pimpla hypochondriaca","volume":"34","author":"Parkinson","year":"2004","journal-title":"Insect Biochem. Mol. Biol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.toxicon.2012.11.004","article-title":"Molecular Cloning and Antifibrinolytic Activity of a Serine Protease Inhibitor from Bumblebee (Bombus terrestris) Venom","volume":"63","author":"Qiu","year":"2013","journal-title":"Toxicon"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1210\/er.2008-0032","article-title":"The CAP Superfamily: Cysteine-Rich Secretory Proteins, Antigen 5, and Pathogenesis-Related 1 Proteins\u2014Roles in Reproduction, Cancer, and Immune Defense","volume":"29","author":"Gibbs","year":"2008","journal-title":"Endocr. Rev."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"58:1","DOI":"10.1007\/s11882-020-00954-0","article-title":"Antigen 5 Allergens of Hymenoptera Venoms and Their Role in Diagnosis and Therapy of Venom Allergy","volume":"20","author":"Blank","year":"2020","journal-title":"Curr. Allergy Asthma Rep."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1016\/S0091-6749(97)70173-8","article-title":"Reactions to Less Common Species of Fire Ants","volume":"100","author":"Hoffman","year":"1997","journal-title":"J. Allergy Clin. Immunol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"988","DOI":"10.1016\/0091-6749(90)90042-3","article-title":"Allergens in Hymenoptera Venom. XXII. Comparison of Venoms from Two Species of Imported Fire Ants, Solenopsis invicta and richteri","volume":"85","author":"Hoffman","year":"1990","journal-title":"J. Allergy Clin. Immunol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1385\/CRIAI:30:2:109","article-title":"Hymenoptera Venom Allergens","volume":"30","author":"Hoffman","year":"2006","journal-title":"Clin. Rev. Allergy Immunol."},{"key":"ref_42","unstructured":"Jentsch, J. (1969, January September). A Procedure for Purification of Myrmica Venom: The Isolation of the Compulsive Component. Proceedings of the VI Congress of the IUSSI, Bern, Switzerland."},{"key":"ref_43","unstructured":"Piek, T. (2013). Venoms of the Hymenoptera: Biochemical, Pharmacological and Behavioural Aspects, Elsevier."},{"key":"ref_44","unstructured":"Mebs, D. (1992). Gifttiere: Ein Handbuch f\u00fcr Biologen, Toxikologen, \u00c4rzte, Apotheker, Wissenschaftliche Verlagsgesellschaft."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1","DOI":"10.32473\/edis-in746-2007","article-title":"European Fire Ant, Red Ant (Suggested Common Names), Myrmica rubra Linnaeus (Insecta: Hymenoptera: Formicidae: Myrmicinae): EENY-410\/IN746, 8\/2007","volume":"2007","author":"Arevalo","year":"2007","journal-title":"EDIS"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1016\/S0041-0101(02)00281-7","article-title":"An Epidermal Growth Factor-like Toxin and Two Sodium Channel Toxins from the Sea Anemone Stichodactyla gigantea","volume":"41","author":"Shiomi","year":"2003","journal-title":"Toxicon"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"539","DOI":"10.1016\/j.toxicon.2012.05.020","article-title":"Development of a Rational Nomenclature for Naming Peptide and Protein Toxins from Sea Anemones","volume":"60","author":"Oliveira","year":"2012","journal-title":"Toxicon"},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"L\u00fcddecke, T., von Reumont, B.M., F\u00f6rster, F., Billion, A., Timm, T., Lochnit, G., Vilcinskas, A., and Lemke, S. (2020). An Economic Dilemma between Molecular Weapon Systems May Explain an Arachno-Atypical Venom in Wasp Spiders (Argiope bruennichi). Biomolecules, 10.","DOI":"10.1101\/2020.06.04.133660"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1111\/brv.12793","article-title":"The Biology and Evolution of Spider Venoms","volume":"97","author":"Herzig","year":"2022","journal-title":"Biol. Rev."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1283","DOI":"10.1016\/j.str.2015.05.003","article-title":"Weaponization of a Hormone: Convergent Recruitment of Hyperglycemic Hormone into the Venom of Arthropod Predators","volume":"23","author":"Undheim","year":"2015","journal-title":"Structure"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1074\/mcp.RA118.000908","article-title":"Parasitoid Jewel Wasp Mounts Multipronged Neurochemical Attack to Hijack a Host Brain","volume":"18","author":"Arvidson","year":"2019","journal-title":"Mol. Cell Proteom."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.ygcen.2015.07.012","article-title":"Hormone-like Peptides in the Venoms of Marine Cone Snails","volume":"244","author":"Robinson","year":"2017","journal-title":"Gen. Comp. Endocrinol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"2593","DOI":"10.1517\/14656566.8.15.2593","article-title":"Exenatide","volume":"8","author":"Barnett","year":"2007","journal-title":"Expert Opin. Pharmacother."},{"key":"ref_54","first-page":"749","article-title":"Weitere Beitr\u00e4ge zur Kenntnis der chemischen Zusammensetzung des Giftes von Ameisen aus der Gattung Formica","volume":"16","author":"Osman","year":"1961","journal-title":"Z. Nat. B"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1126\/science.abb9303","article-title":"Convergent Evolution of Pain-Inducing Defensive Venom Components in Spitting Cobras","volume":"371","author":"Kazandjian","year":"2021","journal-title":"Science"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2255","DOI":"10.1097\/j.pain.0000000000001326","article-title":"Lionfish Venom Elicits Pain Predominantly through the Activation of Nonpeptidergic Nociceptors","volume":"159","author":"Lesperance","year":"2018","journal-title":"PAIN"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"e2023815118","DOI":"10.1073\/pnas.2023815118","article-title":"Production, Composition, and Mode of Action of the Painful Defensive Venom Produced by a Limacodid Caterpillar, Doratifera vulnerans","volume":"118","author":"Walker","year":"2021","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"114693","DOI":"10.1016\/j.bcp.2021.114693","article-title":"Multipurpose Peptides: The Venoms of Amazonian Stinging Ants Contain Anthelmintic Ponericins with Diverse Predatory and Defensive Activities","volume":"192","author":"Nixon","year":"2021","journal-title":"Biochem. Pharmacol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"9932","DOI":"10.1002\/ece3.6652","article-title":"Context-Dependent Venom Deployment and Protein Composition in Two Assassin Bugs","volume":"10","author":"Fischer","year":"2020","journal-title":"Ecol. Evol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1038\/s41467-018-03091-5","article-title":"The Assassin Bug Pristhesancus plagipennis Produces Two Distinct Venoms in Separate Gland Lumens","volume":"9","author":"Walker","year":"2018","journal-title":"Nat. Commun."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"3521","DOI":"10.1038\/ncomms4521","article-title":"Evolution of Separate Predation- and Defence-Evoked Venoms in Carnivorous Cone Snails","volume":"5","author":"Dutertre","year":"2014","journal-title":"Nat. Commun."},{"key":"ref_62","unstructured":"Seifert, B. (2007). Die Ameisen Mittel- und Nordeuropas, lutra Verlags- und Vertriebsgesellschaft."},{"key":"ref_63","unstructured":"Andrews, S. (2022, February 08). Babraham Bioinformatics\u2014FastQC A Quality Control Tool for High Throughput Sequence Data. Available online: https:\/\/www.bioinformatics.babraham.ac.uk\/projects\/fastqc\/."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"10","DOI":"10.14806\/ej.17.1.200","article-title":"Cutadapt Removes Adapter Sequences from High-Throughput Sequencing Reads","volume":"17","author":"Martin","year":"2011","journal-title":"EMBnet J."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1494","DOI":"10.1038\/nprot.2013.084","article-title":"De novo Transcript Sequence Reconstruction from RNA-Seq Using the Trinity Platform for Reference Generation and Analysis","volume":"8","author":"Haas","year":"2013","journal-title":"Nat. Protoc."},{"key":"ref_66","unstructured":"Haas, B.J. (2021, February 08). HPC GridRunner. Available online: https:\/\/github.com\/HpcGridRunner\/HpcGridRunner."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"giz100","DOI":"10.1093\/gigascience\/giz100","article-title":"rnaSPAdes: A de novo Transcriptome Assembler and Its Application to RNA-Seq Data","volume":"8","author":"Bushmanova","year":"2019","journal-title":"GigaScience"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"48","DOI":"10.1186\/s13742-015-0089-y","article-title":"Rcorrector: Efficient and Accurate Error Correction for Illumina RNA-Seq Reads","volume":"4","author":"Song","year":"2015","journal-title":"GigaScience"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"3150","DOI":"10.1093\/bioinformatics\/bts565","article-title":"CD-HIT: Accelerated for Clustering the next-Generation Sequencing Data","volume":"28","author":"Fu","year":"2012","journal-title":"Bioinformatics"},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Kollmar, M. (2019). BUSCO: Assessing Genome Assembly and Annotation Completeness. Gene Prediction: Methods and Protocols, Springer. Methods in Molecular Biology.","DOI":"10.1007\/978-1-4939-9173-0"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"907","DOI":"10.1038\/s41587-019-0201-4","article-title":"Graph-Based Genome Alignment and Genotyping with HISAT2 and HISAT-Genotype","volume":"37","author":"Kim","year":"2019","journal-title":"Nat. Biotechnol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1186\/s13059-019-1910-1","article-title":"Transcriptome Assembly from Long-Read RNA-Seq Alignments with StringTie2","volume":"20","author":"Kovaka","year":"2019","journal-title":"Genome Biol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","article-title":"The Sequence Alignment\/Map Format and SAMtools","volume":"25","author":"Li","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1016\/S0022-2836(05)80360-2","article-title":"Basic Local Alignment Search Tool","volume":"215","author":"Altschul","year":"1990","journal-title":"J. Mol. Biol."},{"key":"ref_75","doi-asserted-by":"crossref","unstructured":"(2019). The UniProt Consortium UniProt: A Worldwide Hub of Protein Knowledge. Nucleic Acids Res., 47, D506\u2013D515.","DOI":"10.1093\/nar\/gky1049"},{"key":"ref_76","unstructured":"de Castro, E., and Jungo, F. (2021, January 11). VenomZone. Available online: https:\/\/venomzone.expasy.org\/."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/j.toxicon.2004.10.018","article-title":"Tox-Prot, the Toxin Protein Annotation Program of the Swiss-Prot Protein Knowledgebase","volume":"45","author":"Jungo","year":"2005","journal-title":"Toxicon"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"10915","DOI":"10.1073\/pnas.89.22.10915","article-title":"Amino Acid Substitution Matrices from Protein Blocks","volume":"89","author":"Henikoff","year":"1992","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"1422","DOI":"10.1093\/bioinformatics\/btp163","article-title":"Biopython: Freely Available Python Tools for Computational Molecular Biology and Bioinformatics","volume":"25","author":"Cock","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"2.7.1","DOI":"10.1002\/0471250953.bi0207s21","article-title":"The InterPro Database and Tools for Protein Domain Analysis","volume":"21","author":"Mulder","year":"2008","journal-title":"Curr. Protoc. Bioinform."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1093\/molbev\/mst010","article-title":"MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability","volume":"30","author":"Katoh","year":"2013","journal-title":"Mol. Biol. Evol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1189","DOI":"10.1093\/bioinformatics\/btp033","article-title":"Jalview Version 2\u2014A Multiple Sequence Alignment Editor and Analysis Workbench","volume":"25","author":"Waterhouse","year":"2009","journal-title":"Bioinformatics"},{"key":"ref_83","doi-asserted-by":"crossref","unstructured":"Price, M.N., Dehal, P.S., and Arkin, A.P. (2010). FastTree 2\u2014Approximately Maximum-Likelihood Trees for Large Alignments. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0009490"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"W293","DOI":"10.1093\/nar\/gkab301","article-title":"Interactive Tree Of Life (iTOL) v5: An Online Tool for Phylogenetic Tree Display and Annotation","volume":"49","author":"Letunic","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref_85","doi-asserted-by":"crossref","unstructured":"Teufel, F., Almagro Armenteros, J.J., Johansen, A.R., G\u00edslason, M.H., Pihl, S.I., Tsirigos, K.D., Winther, O., Brunak, S., von Heijne, G., and Nielsen, H. (2022). SignalP 6.0 Predicts All Five Types of Signal Peptides Using Protein Language Models. Nat. Biotechnol., 1\u20133.","DOI":"10.1038\/s41587-021-01156-3"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"D412","DOI":"10.1093\/nar\/gkaa913","article-title":"Pfam: The Protein Families Database in 2021","volume":"49","author":"Mistry","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"e2584:1","DOI":"10.7717\/peerj.2584","article-title":"VSEARCH: A Versatile Open Source Tool for Metagenomics","volume":"4","author":"Rognes","year":"2016","journal-title":"PeerJ"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"355","DOI":"10.1111\/j.1471-8286.2007.01678.x","article-title":"BOLD: The Barcode of Life Data System","volume":"7","author":"Ratnasingham","year":"2007","journal-title":"Mol. Ecol. Notes"},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"von Reumont, B.M., L\u00fcddecke, T., Timm, T., Lochnit, G., Vilcinskas, A., von D\u00f6hren, J., and Nilsson, M.A. (2020). Proteo-Transcriptomic Analysis Identifies Potential Novel Toxins Secreted by the Predatory, Prey-Piercing Ribbon Worm Amphiporus lactifloreus. Mar. Drugs, 18.","DOI":"10.3390\/md18080407"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"3551","DOI":"10.1002\/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2","article-title":"Probability-Based Protein Identification by Searching Sequence Databases Using Mass Spectrometry Data","volume":"20","author":"Perkins","year":"1999","journal-title":"Electrophoresis"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1016\/j.toxicon.2008.05.020","article-title":"A Rational Nomenclature for Naming Peptide Toxins from Spiders and Other Venomous Animals","volume":"52","author":"King","year":"2008","journal-title":"Toxicon"},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1093\/molbev\/msx281","article-title":"UFBoot2: Improving the Ultrafast Bootstrap Approximation","volume":"35","author":"Hoang","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1093\/molbev\/msu300","article-title":"IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies","volume":"32","author":"Nguyen","year":"2015","journal-title":"Mol. Biol. Evol."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1038\/nmeth.4285","article-title":"ModelFinder: Fast Model Selection for Accurate Phylogenetic Estimates","volume":"14","author":"Kalyaanamoorthy","year":"2017","journal-title":"Nat. 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