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Licensed Unlicensed Requires Authentication Published by De Gruyter March 26, 2020

Comprehensive analysis of peptides and low molecular weight components of the giant ant Dinoponera quadriceps venom

  • Gandhi Rádis-Baptista ORCID logo EMAIL logo , Hilania V. Dodou , Álvaro R.B. Prieto-da-Silva , André J. Zaharenko , Kohei Kazuma , Ken-ichi Nihei , Hidetoshi Inagaki , Kanami Mori-Yasumoto and Katsuhiro Konno EMAIL logo
From the journal Biological Chemistry

Abstract

Ants (Hymenoptera, Apocrita, Aculeata, Formicoidea) comprise a well-succeeded group of animals. Like bees and wasps, ants are mostly venomous, having a sting system to deliver a mixture of bioactive organic compounds and peptides. The predatory giant ant Dinoponera quadriceps belongs to the subfamily Ponerinae that includes one of the largest known ant species in the world. In the present study, low molecular weight compounds and peptides were identified by online peptide mass fingerprint. These include neuroactive biogenic amines (histamine, tyramine, and dopamine), monoamine alkaloid (phenethylamine), free amino acids (e.g. glutamic acid and proline), free thymidine, and cytosine. To the best of our knowledge, most of these components are described for the first time in an ant venom. Multifunctional dinoponeratoxin peptide variants (pilosulin- and ponericin-like peptides) were characterized that possess antimicrobial, hemolytic, and histamine-releasing properties. These venom components, particularly peptides, might synergistically contribute to the overall venom activity and toxicity, for immobilizing live prey, and for defending D. quadriceps against aggressors, predators, and potential microbial infection.

Acknowledgments

The authors are thankful to the Coordination for the Improvement of Higher Education Personnel (CAPES, Toxinology Program), the Ministry of Education and Culture and the National Council of Research and Development, (CNPq), the Ministry of Science, Technology, Innovation and Communication (MCTI-C), Federal Government of Brazil, for the financial support and project endorsement.

  1. Conflict of interest statement: The authors declare no conflict of interest.

References

Abd El-Wahed, A.A., Khalifa, S.A.M., Sheikh, B.Y., Farag, M.A., Saeed, A., Larik, F.A., Koca-Caliskan, U., AlAjmi, M.F., Hassan, M., Wahabi, H.A., et al. (2019). Bee venom composition: from chemistry to biological activity. In: Studies in Natural Products Chemistry. (Amsterdam, Netherlands: Elsevier), pp. 459–484.10.1016/B978-0-444-64181-6.00013-9Search in Google Scholar

Aili, S.R., Touchard, A., Escoubas, P., Padula, M.P., Orivel, J., Dejean, A., and Nicholson, G.M. (2014). Diversity of peptide toxins from stinging ant venoms. Toxicon 92, 166–178.10.1016/j.toxicon.2014.10.021Search in Google Scholar PubMed

Aili, S.R., Touchard, A., Petitclerc, F., Dejean, A., Orivel, J., Padula, M.P., Escoubas, P., and Nicholson, G.M. (2017). Combined peptidomic and proteomic analysis of electrically stimulated and manually dissected venom from the south american bullet ant Paraponera clavata. J. Proteome Res. 16, 1339–1351.10.1021/acs.jproteome.6b00948Search in Google Scholar PubMed

Amiche, M. and Galanth, C. (2011). Dermaseptins as models for the elucidation of membrane-acting helical amphipathic antimicrobial peptides. Curr. Pharm. Biotechnol. 12, 1184–1193.10.2174/138920111796117319Search in Google Scholar PubMed

Blenau, W. and Baumann, A. (2001). Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. Arch. Insect Biochem. Physiol. 48, 13–38.10.1002/arch.1055Search in Google Scholar PubMed

Ceolin Mariano, D.O., de Oliveira, Ú.C., Zaharenko, A.J., Pimenta, D.C., Rádis-Baptista, G., and Prieto-da-Silva, Á.R.d.B. (2019). Bottom-up proteomic analysis of polypeptide venom components of the giant ant Dinoponera quadriceps. Toxins 11, pii: E448.10.3390/toxins11080448Search in Google Scholar PubMed PubMed Central

CLSI. (2008). Reference Method for Broth Dilution Antifungal Susceptibility Testing of Yeasts; Approved Standard – 3rd edition, CLSI document M27-A3. Clinical and Laboratory Standards Institute. CLSI, Wayne, PA, USA.Search in Google Scholar

CLSI. (2018). Methods for Diluition Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically. 11th edition, CLSI standard M07. Clinical and Laboratory Standards Institute. CLSI, Wayne, PA, USA.Search in Google Scholar

Cologna, C.T., Cardoso Jdos, S., Jourdan, E., Degueldre, M., Upert, G., Gilles, N., Uetanabaro, A.P., Costa Neto, E.M., Thonart, P., de Pauw, E., et al. (2013). Peptidomic comparison and characterization of the major components of the venom of the giant ant Dinoponera quadriceps collected in four different areas of Brazil. J. Proteomics 94, 413–422.10.1016/j.jprot.2013.10.017Search in Google Scholar PubMed

Davidson, S. and Giesler, G.J. (2010). The multiple pathways for itch and their interactions with pain. Trends Neurosci. 33, 550–558.10.1016/j.tins.2010.09.002Search in Google Scholar PubMed PubMed Central

Dhananjaya, B.L. and D’Souza, C.J.M. (2016). Purinergic mechanisms of prey acquisition by venomous organisms. In: Venom Genomics and Proteomics (Dordrecht: Springer Netherlands), pp. 381–392.10.1007/978-94-007-6416-3_1Search in Google Scholar

Dos Santos Cabrera, M.P., Rangel, M., Ruggiero Neto, J., and Konno, K. (2019). Chemical and biological characteristics of antimicrobial α-helical peptides found in solitary wasp venoms and their interactions with model membranes. Toxins 11, pii: E559.10.3390/toxins11100559Search in Google Scholar PubMed PubMed Central

Funayama, S. and Cordell, G.A. (2015). Chapter 1 – Alkaloids derived from phenylalanine and tyrosine. In: Alkaloids (Boston, USA: Academic Press), pp. 21–61.Search in Google Scholar

Griffiths, H.M., Ashton, L.A., Walker, A.E., Hasan, F., Evans, T.A., Eggleton, P., and Parr, C.L. (2018). Ants are the major agents of resource removal from tropical rainforests. J. Anim. Ecol. 87, 293–300.10.1111/1365-2656.12728Search in Google Scholar PubMed PubMed Central

Habermann, E. (1972). Bee and wasp venoms. Science 177, 314–322.10.1126/science.177.4046.314Search in Google Scholar PubMed

Hagiwara, K., Tokita, A., Miwa, A., Kawai, N., Murata, Y., Uchida, A., and Nakajima, T. (1991). Determination of biogenic amines in spider venom glands of nine typical Japanese species and chromatographic elution pattern analysis of venomous components. Med. Entomol. Zool. 42, 77–84.10.7601/mez.42.77Search in Google Scholar

Inagaki, H., Akagi, M., Imai, H.T., Taylor, R.W., and Kubo, T. (2004). Molecular cloning and biological characterization of novel antimicrobial peptides, pilosulin 3 and pilosulin 4, from a species of the Australian ant genus Myrmecia. Arch. Biochem. Biophys. 428, 170–178.10.1016/j.abb.2004.05.013Search in Google Scholar PubMed

Johnson, S.R., Copello, J.A., Evans, M.S., and Suarez, A.V. (2010). A biochemical characterization of the major peptides from the venom of the giant neotropical hunting ant Dinoponera australis. Toxicon 55, 702–710.10.1016/j.toxicon.2009.10.021Search in Google Scholar PubMed

Kazuma, K., Masuko, K., Konno, K., and Inagaki, H. (2017). Combined venom gland transcriptomic and venom peptidomic analysis of the predatory ant Odontomachus monticola. Toxins 9, pii: E323.10.3390/toxins9100323Search in Google Scholar PubMed PubMed Central

Konno, K., Kazuma, K., and Nihei, K.-I. (2016). Peptide toxins in solitary wasp venoms. Toxins 8, pii: E114.10.3390/toxins8040114Search in Google Scholar PubMed PubMed Central

Lee, S.H., Baek, J.H., and Yoon, K.A. (2016). Differential properties of venom peptides and proteins in solitary vs. social hunting wasps. Toxins 8, 32–32.10.3390/toxins8020032Search in Google Scholar PubMed PubMed Central

Lenhart, P.A., Dash, S.T., and Mackay, W.P. (2013). A revision of the giant Amazonian ants of the genus Dinoponera (Hymenoptera, Formicidae). J. Hymenopt. Res. 31, 119–164.10.3897/jhr.31.4335Search in Google Scholar

Lima, D.B., Mello, C.P., Bandeira, I.C.J., Pessoa Bezerra de Menezes, R.R.P., Sampaio, T.L., Falcao, C.B., Morlighem, J.R.L., Radis-Baptista, G., and Martins, A.M.C. (2018). The dinoponeratoxin peptides from the giant ant Dinoponera quadriceps display in vitro antitrypanosomal activity. Biol. Chem. 399, 187–196.10.1515/hsz-2017-0198Search in Google Scholar PubMed

Miliano, C., Serpelloni, G., Rimondo, C., Mereu, M., Marti, M., and De Luca, M.A. (2016). Neuropharmacology of New Psychoactive Substances (NPS): focus on the rewarding and reinforcing properties of cannabimimetics and amphetamine-like stimulants. Front. Neurosci. 10, 153–153.10.3389/fnins.2016.00153Search in Google Scholar

Owen, M.D. (1971). Insect venoms: identification of dopamine and noradrenaline in wasp and bee stings. Experientia 27, 544–545.10.1007/BF02147590Search in Google Scholar

Owen, M.D. and Bridges, A.R. (1982). Catecholamines in honey bee (Apis mellifera L.) and various vespid (Hymenoptera) venoms. Toxicon 20, 1075–1084.10.1016/0041-0101(82)90110-6Search in Google Scholar

Sabia Junior, E.F., Menezes, L.F.S., de Araujo, I.F.S., and Schwartz, E.F. (2019). Natural occurrence in venomous arthropods of antimicrobial peptides active against protozoan parasites. Toxins 11, pii: E563.10.3390/toxins11100563Search in Google Scholar PubMed PubMed Central

Shanholtzer, C.J., Peterson, L.R., Mohn, M.L., Moody, J.A., and Gerding, D.N. (1984). MBCs for Staphylococcus aureus as determined by macrodilution and microdilution techniques. Antimicrob. Agents Chemother. 26, 214–219.10.1128/AAC.26.2.214Search in Google Scholar PubMed PubMed Central

Shigeri, Y., Yasuda, A., Hagihara, Y., Nishi, K., Watanabe, K., Imura, T., Inagaki, H., Haramoto, Y., Ito, Y., and Asashima, M. (2015). Identification of novel peptides from amphibian (Xenopus tropicalis) skin by direct tissue MALDI-MS analysis. FEBS J. 282, 102–113.10.1111/febs.13107Search in Google Scholar PubMed

Sousa, P.L., Quinet, Y., Ponte, E.L., do Vale, J.F., Torres, A.F.C., Pereira, M.G., and Assreuy, A.M.S. (2012). Venom’s antinociceptive property in the primitive ant Dinoponera quadriceps. J. Ethnopharmacol. 144, 213–216.10.1016/j.jep.2012.08.033Search in Google Scholar PubMed

Steinberg, D.A. and Lehrer, R.I. (1997). Designer assays for antimicrobial peptides. Disputing the “one-size-fits-all” theory. Methods Mol. Biol. 78, 169–186.10.1385/0-89603-408-9:169Search in Google Scholar

Szabados, L. and Savoure, A. (2010). Proline: a multifunctional amino acid. Trends Plant Sci. 15, 89–97.10.1016/j.tplants.2009.11.009Search in Google Scholar PubMed

Takahashi, M., Fuchino, H., Satake, M., Agatsuma, Y., and Sekita, S. (2004). In vitro screening of leishmanicidal activity in myanmar timber extracts. Biol. Pharm. Bull. 27, 921–925.10.1248/bpb.27.921Search in Google Scholar PubMed

Tani, N., Kazuma, K., Ohtsuka, Y., Shigeri, Y., Masuko, K., Konno, K., and Inagaki, H. (2019). Mass spectrometry analysis and biological characterization of the predatory ant Odontomachus monticola venom and venom sac components. Toxins 11, pii: E50.10.3390/toxins11010050Search in Google Scholar PubMed PubMed Central

Taylor, P.C., Schoenknecht, F.D., Sherris, J.C., and Linner, E.C. (1983). Determination of minimum bactericidal concentrations of oxacillin for Staphylococcus aureus: influence and significance of technical factors. Antimicrob. Agents Chemother. 23, 142–150.10.1128/AAC.23.1.142Search in Google Scholar PubMed PubMed Central

Torres, A.F., Huang, C., Chong, C.M., Leung, S.W., Prieto-da-Silva, A.R., Havt, A., Quinet, Y.P., Martins, A.M., Lee, S.M., and Radis-Baptista, G. (2014). Transcriptome analysis in venom gland of the predatory giant ant Dinoponera quadriceps: insights into the polypeptide toxin arsenal of hymenopterans. PLoS One 9, e87556.10.1371/journal.pone.0087556Search in Google Scholar PubMed PubMed Central

Touchard, A., Koh, J.M., Aili, S.R., Dejean, A., Nicholson, G.M., Orivel, J., and Escoubas, P. (2015). The complexity and structural diversity of ant venom peptidomes is revealed by mass spectrometry profiling. Rapid Commun. Mass Spectrom. 29, 385–396.10.1002/rcm.7116Search in Google Scholar PubMed

Touchard, A., Aili, S.R., Fox, E.G., Escoubas, P., Orivel, J., Nicholson, G.M., and Dejean, A. (2016). The biochemical toxin arsenal from ant venoms. Toxins 8, pii: E30.10.3390/toxins8010030Search in Google Scholar PubMed PubMed Central

Wang, X. and Wang, G. (2016). Insights into antimicrobial peptides from spiders and scorpions. Protein Peptide Lett. 23, 707–721.10.2174/0929866523666160511151320Search in Google Scholar PubMed PubMed Central

Ward, P.S. (2006). Ants. Curr. Biol. 16, R152–155.10.1016/j.cub.2006.02.054Search in Google Scholar PubMed

Zaprasis, A., Brill, J., Thüring, M., Wünsche, G., Heun, M., Barzantny, H., Hoffmann, T., and Bremer, E. (2013). Osmoprotection of Bacillus subtilis through import and proteolysis of proline-containing peptides. Appl. Environ. Microbiol. 79, 576–587.10.1128/AEM.01934-12Search in Google Scholar PubMed PubMed Central

Zhao, H. and Kinnunen, P.K.J. (2003). Modulation of the activity of secretory phospholipase A2 by antimicrobial peptides. Antimicrob. Agents Chemother. 47, 965–971.10.1128/AAC.47.3.965-971.2003Search in Google Scholar PubMed PubMed Central


Supplementary Material

The online version of this article offers supplementary material (https://doi.org/10.1515/hsz-2019-0397).


Received: 2019-10-19
Accepted: 2020-02-19
Published Online: 2020-03-26
Published in Print: 2020-07-28

©2020 Walter de Gruyter GmbH, Berlin/Boston

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