{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,18]],"date-time":"2026-08-18T05:12:26Z","timestamp":1787029946045,"version":"build-2736575974"},"reference-count":54,"publisher":"MDPI AG","issue":"6","license":[{"start":{"date-parts":[[2024,6,14]],"date-time":"2024-06-14T00:00:00Z","timestamp":1718323200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Studienstiftung des deutschen Volkes"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Toxins"],"abstract":"<jats:p>The larvae of some lampyrid beetles are highly specialized predators of snails. They have been observed to climb on the shells of their prey and use this exposed position to bite and inject secretions potentially originating from the midgut. Besides serving the purpose of extra-oral digestion (EOD), injected compounds also seem to have a paralyzing effect. Up to now, the toxins causing this paralyzing activity have not been identified. In the current study, we provide a first compositional analysis of the midgut secretion from lampyrid larvae, with a focus on identifying putative neurotoxins causing the observed paralyzing effect. For this purpose, we utilized a combined proteo-transcriptomic approach to characterize the compounds present in the midgut secretion of larval stages of Lampyris noctiluca. In terms of the absolute numbers of identified compounds, the midgut secretion is dominated by hydrolyzing enzymes comprising peptidases, carboxylesterases, and glycosidases. However, when considering expression levels, a few rather short cysteine-rich peptides exceed all other compounds. Some of these compounds show moderate similarity to putative neurotoxins identified in the venom of other arthropods and could be responsible for paralyzing effects. In addition to these potential toxins, we provide a list of peptides typical of the midgut secretion of L. noctiluca, supplemented by the corresponding precursor sequences.<\/jats:p>","DOI":"10.3390\/toxins16060272","type":"journal-article","created":{"date-parts":[[2024,6,14]],"date-time":"2024-06-14T10:42:34Z","timestamp":1718361754000},"page":"272","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":7,"title":["How to Overcome a Snail? Identification of Putative Neurotoxins of Snail-Feeding Firefly Larvae (Coleoptera: Lampyridae, Lampyris noctiluca)"],"prefix":"10.3390","volume":"16","author":[{"given":"Jonas","family":"Kr\u00e4mer","sequence":"first","affiliation":[{"name":"Institute of Zoology, University of Cologne, Zuelpicher Strasse 47b, 50674 Cologne, Germany"},{"name":"Institute for Insect Biotechnology, Justus-Liebig-University of Giessen, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9464-7985","authenticated-orcid":false,"given":"Patrick","family":"H\u00f6lker","sequence":"additional","affiliation":[{"name":"Institute of Zoology, University of Cologne, Zuelpicher Strasse 47b, 50674 Cologne, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0202-6672","authenticated-orcid":false,"given":"Reinhard","family":"Predel","sequence":"additional","affiliation":[{"name":"Institute of Zoology, University of Cologne, Zuelpicher Strasse 47b, 50674 Cologne, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,6,14]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"39","DOI":"10.2307\/1536232","article-title":"Notes on the Biology of Some Common Lampyridae","volume":"38","author":"Hess","year":"1920","journal-title":"Biol. Bull."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"e12121","DOI":"10.7717\/peerj.12121","article-title":"A Comprehensive Review and Call for Studies on Firefly Larvae","volume":"9","author":"Riley","year":"2021","journal-title":"PeerJ"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"e8080","DOI":"10.7717\/peerj.8080","article-title":"Prey-Tracking Behavior and Prey Preferences in a Tree-Climbing Firefly","volume":"7","author":"Sato","year":"2019","journal-title":"PeerJ"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1649\/907.1","article-title":"Biological Characteristics of the Terrestrial Firefly Pyrocoelia pectoralis (Cleoptera: Lampyridae)","volume":"61","author":"Wang","year":"2007","journal-title":"Coleopt. Bull."},{"key":"ref_5","first-page":"399","article-title":"Beitr\u00e4ge zur Biologie der Einheimischen Lampyriden Lampyris noctiluca Geoffr. und Phausis splendidula Lec. und Experimentelle Analyse ihres Beutefang- und Sexualsverhaltens","volume":"88","author":"Schwalb","year":"1961","journal-title":"Zool. Jahrb. Abt. Syst. Geogr. Biol. Tiere"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Krenn, H.W. (2019). Insect Mouthparts: Form, Function, Development and Performance, Springer International Publishing. Zoological Monographs.","DOI":"10.1007\/978-3-030-29654-4"},{"key":"ref_7","first-page":"292","article-title":"Beitrag zur Kenntnis des Baues und der Lebensweise der Larve von Lampyris noctiluca","volume":"112","author":"Vogel","year":"1915","journal-title":"Z. Wiss. Zool."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1146\/annurev.en.27.010182.002011","article-title":"Biochemistry of Insect Venoms","volume":"27","author":"Schmidt","year":"1982","journal-title":"Annu. Rev. Entomol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"3488","DOI":"10.3390\/toxins6123488","article-title":"Quo Vadis Venomics? A Roadmap to Neglected Venomous Invertebrates","volume":"6","author":"Campbell","year":"2014","journal-title":"Toxins"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1016\/j.toxicon.2018.09.004","article-title":"Entomo-Venomics: The Evolution, Biology and Biochemistry of Insect Venoms","volume":"154","author":"Walker","year":"2018","journal-title":"Toxicon"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"giac048","DOI":"10.1093\/gigascience\/giac048","article-title":"Modern Venomics\u2014Current Insights, Novel Methods, and Future Perspectives in Biological and Applied Animal Venom Research","volume":"11","author":"Anderluh","year":"2022","journal-title":"GigaScience"},{"key":"ref_12","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_13","doi-asserted-by":"crossref","unstructured":"Drukewitz, S., Fuhrmann, N., Undheim, E., Blanke, A., Giribaldi, J., Mary, R., Laconde, G., Dutertre, S., and von Reumont, B. (2018). A Dipteran\u2019s Novel Sucker Punch: Evolution of Arthropod Atypical Venom with a Neurotoxic Component in Robber Flies (Asilidae, Diptera). Toxins, 10.","DOI":"10.3390\/toxins10010029"},{"key":"ref_14","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_15","doi-asserted-by":"crossref","first-page":"2748","DOI":"10.1093\/molbev\/msz181","article-title":"Parallel Evolution of Complex Centipede Venoms Revealed by Comparative Proteotranscriptomic Analyses","volume":"36","author":"Jenner","year":"2019","journal-title":"Mol. Biol. Evol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"92","DOI":"10.1016\/j.toxicon.2021.08.012","article-title":"A Pseudoscorpion\u2019s Promising Pinch: The Venom of Chelifer cancroides Contains a Rich Source of Novel Compounds","volume":"201","author":"Peigneur","year":"2021","journal-title":"Toxicon"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"von Reumont, B., Undheim, E., Jauss, R.-T., and Jenner, R. (2017). Venomics of Remipede Crustaceans Reveals Novel Peptide Diversity and Illuminates the Venom\u2019s Biological Role. Toxins, 9.","DOI":"10.3390\/toxins9080234"},{"key":"ref_18","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_19","doi-asserted-by":"crossref","unstructured":"Herzig, V., Cristofori-Armstrong, B., Israel, M.R., Nixon, S.A., Vetter, I., and King, G.F. (2020). Animal Toxins\u2014Nature\u2019s Evolutionary-Refined Toolkit for Basic Research and Drug Discovery. Biochem. Pharmacol., 181.","DOI":"10.1016\/j.bcp.2020.114096"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1132","DOI":"10.3389\/fphar.2020.01132","article-title":"From Animal Poisons and Venoms to Medicines: Achievements, Challenges and Perspectives in Drug Discovery","volume":"11","author":"Bordon","year":"2020","journal-title":"Front. Pharmacol."},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Chow, C.Y., Absalom, N., Biggs, K., King, G.F., and Ma, L. (2020). Venom-Derived Modulators of Epilepsy-Related Ion Channels. Biochem. Pharmacol., 181.","DOI":"10.1016\/j.bcp.2020.114043"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"17534","DOI":"10.1073\/pnas.1306285110","article-title":"Discovery of a Selective Na V 1.7 Inhibitor from Centipede Venom with Analgesic Efficacy Exceeding Morphine in Rodent Pain Models","volume":"110","author":"Yang","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Tarcha, E.J., Olsen, C.M., Probst, P., Peckham, D., Mu\u00f1oz-El\u00edas, E.J., Kruger, J.G., and Iadonato, S.P. (2017). Safety and Pharmacodynamics of Dalazatide, a Kv1.3 Channel Inhibitor, in the Treatment of Plaque Psoriasis: A Randomized Phase 1b Trial. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0180762"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"3750","DOI":"10.1073\/pnas.1614728114","article-title":"Potent Neuroprotection after Stroke Afforded by a Double-Knot Spider-Venom Peptide That Inhibits Acid-Sensing Ion Channel 1a","volume":"114","author":"Chassagnon","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"464","DOI":"10.1016\/j.toxicon.2010.12.016","article-title":"The Development of Byetta (Exenatide) from the Venom of the Gila Monster as an Anti-Diabetic Agent","volume":"59","author":"Furman","year":"2012","journal-title":"Toxicon"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1002\/prot.20390","article-title":"A Novel Strategy for the Identification of Toxinlike Structures in Spider Venom","volume":"59","author":"Kozlov","year":"2005","journal-title":"Proteins Struct. Funct. Bioinform."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1146\/annurev.en.40.010195.000505","article-title":"Extra-Oral Digestion in Predaceous Terrestrial Arthropoda","volume":"40","author":"Cohen","year":"1995","journal-title":"Annu. Rev. Entomol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1016\/j.cois.2020.07.006","article-title":"Extraoral Digestion: Outsourcing the Role of the Hemipteran Midgut","volume":"41","author":"Bonning","year":"2020","journal-title":"Curr. Opin. Insect Sci."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Fuzita, F.J., Pinkse, M.W.H., Patane, J.S.L., Verhaert, P.D.E.M., and Lopes, A.R. (2016). High Throughput Techniques to Reveal the Molecular Physiology and Evolution of Digestion in Spiders. BMC Genom., 17.","DOI":"10.1186\/s12864-016-3048-9"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1111\/brv.12062","article-title":"Poisons, Toxungens, and Venoms: Redefining and Classifying Toxic Biological Secretions and the Organisms That Employ Them: Redefining Toxic Secretions and Organisms","volume":"89","author":"Nelsen","year":"2014","journal-title":"Biol. Rev."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1016\/j.toxicon.2015.07.005","article-title":"Snake Venoms: A Brief Treatise on Etymology, Origins of Terminology, and Definitions","volume":"103","author":"Weinstein","year":"2015","journal-title":"Toxicon"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"5141","DOI":"10.1096\/fj.12-218479","article-title":"A Natural Point Mutation Changes Both Target Selectivity and Mechanism of Action of Sea Anemone Toxins","volume":"26","author":"Peigneur","year":"2012","journal-title":"FASEB J."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"546","DOI":"10.1093\/molbev\/msu038","article-title":"Experimental Conversion of a Defensin into a Neurotoxin: Implications for Origin of Toxic Function","volume":"31","author":"Zhu","year":"2014","journal-title":"Mol. Biol. Evol."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Langenegger, N., Nentwig, W., and Kuhn-Nentwig, L. (2019). Spider Venom: Components, Modes of Action, and Novel Strategies in Transcriptomic and Proteomic Analyses. Toxins, 11.","DOI":"10.3390\/toxins11100611"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"11399","DOI":"10.1073\/pnas.1914536117","article-title":"Structural Venomics Reveals Evolution of a Complex Venom by Duplication and Diversification of an Ancient Peptide-Encoding Gene","volume":"117","author":"Pineda","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1002\/neu.480220108","article-title":"Odorant-binding-protein Subfamilies Associate with Distinct Classes of Olfactory Receptor Neurons in Insects","volume":"22","author":"Vogt","year":"1991","journal-title":"J. Neurobiol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1002\/arch.21206","article-title":"Venom of the Parasitoid Wasp Pteromalus puparum Contains an Odorant Binding Protein","volume":"88","author":"Wang","year":"2015","journal-title":"Arch. Insect Biochem. Physiol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"411","DOI":"10.1111\/1744-7917.12955","article-title":"Comparative Analyses of the Venom Components in the Salivary Gland Transcriptomes and Saliva Proteomes of Some Heteropteran Insects","volume":"29","author":"Yoon","year":"2022","journal-title":"Insect Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1111\/imb.12388","article-title":"Major Venom Proteins of the Fire Ant Solenopsis invicta: Insights into Possible Pheromone-binding Function from Mass Spectrometric Analysis","volume":"27","author":"Das","year":"2018","journal-title":"Insect Mol. Biol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Rihani, K., Ferveur, J.-F., and Briand, L. (2021). The 40-Year Mystery of Insect Odorant-Binding Proteins. Biomolecules, 11.","DOI":"10.3390\/biom11040509"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0305-0491(94)90141-4","article-title":"Insect Digestive Enzymes: Properties, Compartmentalization and Function","volume":"109","author":"Terra","year":"1994","journal-title":"Comp. Biochem. Physiol. Part B Comp. Biochem."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"505","DOI":"10.1007\/s00441-019-03076-w","article-title":"The Amazing Complexity of Insect Midgut Cells: Types, Peculiarities, and Functions","volume":"377","author":"Caccia","year":"2019","journal-title":"Cell Tissue Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"100931","DOI":"10.1016\/j.asd.2020.100931","article-title":"Evolutionary Trends of Digestion and Absorption in the Major Insect Orders","volume":"56","author":"Terra","year":"2020","journal-title":"Arthropod Struct. Dev."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"191","DOI":"10.3389\/fphys.2020.00191","article-title":"Peptide Hormones in the Insect Midgut","volume":"11","author":"Wu","year":"2020","journal-title":"Front. Physiol."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Kr\u00e4mer, J., Pommerening, R., and Predel, R. (2022). Equipped for Sexual Stings? Male-Specific Venom Peptides in Euscorpius italicus. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms231911020"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"2114","DOI":"10.1093\/bioinformatics\/btu170","article-title":"Trimmomatic: A Flexible Trimmer for Illumina Sequence Data","volume":"30","author":"Bolger","year":"2014","journal-title":"Bioinformatics"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"644","DOI":"10.1038\/nbt.1883","article-title":"Full-Length Transcriptome Assembly from RNA-Seq Data without a Reference Genome","volume":"29","author":"Grabherr","year":"2011","journal-title":"Nat. Biotechnol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"3210","DOI":"10.1093\/bioinformatics\/btv351","article-title":"BUSCO: Assessing Genome Assembly and Annotation Completeness with Single-Copy Orthologs","volume":"31","author":"Waterhouse","year":"2015","journal-title":"Bioinformatics"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1038\/s41587-021-01156-3","article-title":"SignalP 6.0 Predicts All Five Types of Signal Peptides Using Protein Language Models","volume":"40","author":"Teufel","year":"2022","journal-title":"Nat. Biotechnol."},{"key":"ref_50","unstructured":"(2021). The UniProt Consortium UniProt: The Universal Protein Knowledgebase in 2021. Nucleic Acids Res., 49, D480\u2013D489."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1038\/s41592-022-01488-1","article-title":"ColabFold: Making Protein Folding Accessible to All","volume":"19","author":"Mirdita","year":"2022","journal-title":"Nat. Methods"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1038\/s41586-021-03819-2","article-title":"Highly Accurate Protein Structure Prediction with AlphaFold","volume":"596","author":"Jumper","year":"2021","journal-title":"Nature"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"D20","DOI":"10.1093\/nar\/gkab1112","article-title":"Database Resources of the National Center for Biotechnology Information","volume":"50","author":"Sayers","year":"2022","journal-title":"Nucleic Acids Res."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"D543","DOI":"10.1093\/nar\/gkab1038","article-title":"The PRIDE Database Resources in 2022: A Hub for Mass Spectrometry-Based Proteomics Evidences","volume":"50","author":"Bai","year":"2022","journal-title":"Nucleic Acids Res."}],"container-title":["Toxins"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6651\/16\/6\/272\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:59:06Z","timestamp":1760108346000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6651\/16\/6\/272"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,6,14]]},"references-count":54,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2024,6]]}},"alternative-id":["toxins16060272"],"URL":"https:\/\/doi.org\/10.3390\/toxins16060272","relation":{},"ISSN":["2072-6651"],"issn-type":[{"value":"2072-6651","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,6,14]]}}}