Composition and Antimicrobial Activity of Defensive Secretions of the Giant Millipede Anurostreptus sculptus (Diplopoda, Spirostreptida, Harpagophoridae)

Authors

  • Anuwat Tummanam Department of Biology, Faculty of Science, Mahasarakham University, Maha Sarakham 44150, THAILAND
  • Waraporn Sutthisa Department of Biology, Faculty of Science, Mahasarakham University, Maha Sarakham 44150, THAILAND
  • Widchaya Radchatawedchakoon Department of Chemistry, Faculty of Science, Mahasarakham University, Maha Sarakham 44150, THAILAND
  • Thierry Backeljau Royal Belgian Institute of Natural Sciences, Vautierstraat 29, B-1000 Brussels, BELGIUM; Evolutionary Ecology Group, University of Antwerp, Universiteitsplein 1, B-2610 Antwerp, BELGIUM
  • Piyatida Pimvichai Department of Biology, Faculty of Science, Mahasarakham University, Maha Sarakham 44150, THAILAND

Abstract

This paper reports on the chemical composition and antimicrobial activity of the defensive secretions of the giant millipede, Anurostreptus sculptus (Spirostreptida: Harpagophoridae). The chemical composition of the defensive secretions was analyzed by gas chromatography-mass spectrometry, demonstrating the presence of at least 13 identifiable compounds, including two major compounds, viz. (1) 2,3-dimethoxy-1,4-benzoquinone, and (2) 2-methyl-1,4-benzoquinone, as well as (3) 8 other quinone derivatives, and (4) 3 fatty acid esters, which may enhance the biological effects of the quinone compounds. Antimicrobial activity was tested with three gram-positive bacteria (Bacillus cereus, Staphylococcus aureus, and Staphylococcus aureus DMST20654), four gram-negative bacteria (Escherichia coli, Escherichia coli ATCC25922, Pseudomonas aeruginosa, and Salmonella ser. Typhi ATCC16122), and two yeasts (Candida albicans and Candida albicans ATCC10231), with streptomycin and fluconazole as positive controls. Disc diffusion assays showed that fresh secretions inhibited the growth of all these microorganisms. In line with this, a broth microdilution analysis indicated that fresh secretions yielded Minimum Inhibitory Concentrations (MIC) of 0.0019 to 0.2500% (v/v) and Minimum Bactericidal/Fungicidal Concentrations (MBC/MFC) of 0.0039 to 0.5000% (v/v), i.e.fresh secretions were more effective in inhibiting yeast than the antifungal medicine, fluconazole. The gram-positive bacteria and C. albicans were also inhibited by three types of extracted secretions with MIC values in the range of 0.25 to 2.00 mg/ml and MBC values of 2.00 mg/ml for gram positive-bacteria.

References

Alibi, S., Crespo, D. and Navas, J. 2021. Plant-derivatives small molecules with antibacterial activity. Antibiotics, 10: 231.

Arab, A., Zacarin, G.G., Fontanetti, C.S., Camargo-Mathias, M.I., Dos Santos, M.G. and Cabrera, A.C. 2003. Composition of the defensive secretion of the Neotropical millipede Rhinocricus padbergi Verhoeff 1938 (Diplopoda: Spirobolida: Rhinocricidae). Entomotropica, 18: 79–82.

Beheshti, A., Norouzi, P. and Ganjali, M.R. 2012. A simple and robust model for predicting the reduction potential of quinones family; electrophilicity index effect. International Journal of Electrochemical Science, 7: 4811–4821.

Billah, M.K., Kwang, D., Adofo, C., Olutaİwo, M.A. and Pesewu, G. A. 2015. Antibacterial activities of Millipede extracts against selected bacterial pathogens. Journal of Microbiology and Antimicrobial Agents, 1: 30–35.

Bodner, M., Vagalinski, B., Makarov, S.E., Antić, D.Z., Vujisić, L.V., Leis, H.J. and Raspotnig, G. 2016. “Quinone millipedes” reconsidered: evidence for a mosaic-like taxonomic distribution of phenol-based secretions across the Julidae. Journal of Chemical Ecology, 42: 249–258.

Campos-Xolalpa, N., Pérez-Ramos, J., Esquivel-Campos, A., Pérez-González, C., Sánchez-Pérez, L. and Pérez-Gutiérrez, S. 2021. Cytotoxic and Antimicrobial Activities of Quinones Isolated from Different Organism. In Soloneski, S. and Larramendy, M.L. (Eds) Cytotoxicity - New Insights into Toxic Assessment, IntechOpen, 37 pp.

CLSI. 2012a. Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard—Eleventh Edition. CLSI document M02-A11. Wayne, PA. Clinical Laboratory Standard Institute.

CLSI. 2012b. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; Approved Standard-Ninth Edition. CLSI document M07-A9. Wayne, PA. Clinical Laboratory Standard Institute.

Dandawate, P.R., Vyas, A.C., Padhye, S.B., Singh, M.W. and Baruah, J.B. 2010. Perspectives on Medicinal Properties of Benzoquinone Compounds. Mini-Reviews in Medicinal Chemistry, 10: 436–454.

Davidson, P.M. and Branden, A.L. 1981. Antimicrobial activity of non-halogenated phenolic compounds. Journal of Food Protection, 44: 623–632.

Deml, R. and Huth, A. 2000. Benzoquinones and hydroquinones in defensive secretions of tropical millipedes. Naturwissenschaften, 87: 80–82.

Eisner, T., Alsop, D., Hicks, K. and Meinwald, J. 1978. Defensive secretions of millipedes. In Bettini, S. (Ed.), Arthropod Venoms, Handbook of Experimental Pharmacology, 48: 41–72.

Enghoff, H., Golovatch, S., Short, M., Stoev, P. and Wesener, T. 2015. Diplopoda – Taxonomic overview. In Minelli, A. (Ed.), The Myriapoda 2. Treatise on Zoology – Anatomy, Taxonomy, Biology. pp. 363–453.

Furtado, N.A.J.C., Said, S., Ito, I.Y. and Bastos, J.K. 2002. The antimicrobial activity of Aspergillus fumigatus is enhanced by a pool of bacteria. Microbiological Research, 157: 207–211.

Ilić, B., Dimkić, I., Unković, N., Ljaljević Grbić, M., Vukojević, J., Vujisić, L., Tešević, V., Stanković, S., Makarov, S. and Lučić, L. 2018. Millipedes vs. pathogens: Defensive secretions of some julids (Diplopoda: Julida) as potential antimicrobial agents. Journal of Applied Entomology, 142: 775–791.

Ilić, B., Unković, N., Ćirić, A., Glamočlija, J., Ljaljević Grbić, M., Raspotnig, G., Bodner, M., Vukojević, J. and Makarov, S. 2019a. Phenol-based millipede defence: antimicrobial activity of secretions from the Balkan endemic millipede Apfelbeckia insculpta (L. Koch, 1867) (Diplopoda: Callipodida). The Science of Nature, 106: 1–9.

Ilić, B., Unković, N., Knežević, A., Savković, Ž., Ljaljević Grbić, M., Vukojević, J., Jovanović, Z., Makarov, S. and Lučić, L. 2019b. Multifaceted activity of millipede secretions: Antioxidant, antineurodegenerative, and anti-Fusarium effects of the defensive secretions of Pachyiulus hungaricus (Karsch, 1881) and Megaphyllum unilineatum (C. L. Koch, 1838) (Diplopoda: Julida). PLoS ONE, 14(1): e0209999.

Kania, G., Kowalski, R. and Pietraś, R. 2016. Defensive secretions in millipede species of the order Julida (Diplopoda). Acta Societatis Zoologicae Bohemicae, 80: 17–20.

Morales, J.E.T. and Pedroso, M.T.C. 2019. Diplodomica I. Chemical Composition of Repugnatorial Secretions of Cuban Endemic Millipede gen. Rhinocricus sp. Multidisciplinary Digital Publishing Institute Proceedings, 41(1).

Morales, J.E.T., Siguenza, J.C., Villavicencio, C.B. and Canchingre, M. 2022. Diplodomica III. Chemical Ecology of defensive secretions from neotropical archipelago. Isolation of 3,4-dimethoxyphenol from ejected secretion of endemic Cuban millipedes (Spirobolida, Rhinocricidae, Rhinocricus). Study case Rhinocricus duvernoyi Karch 1881, La Palma population. In Proceedings of the 2nd International Electronic Conference on Diversity (IECD 2022)—New Insights into the Biodiversity of Plants, Animals and Microbes, 15–31 March 2022, MDPI: Basel, Switzerland.

Ômura, H., Kuwahara, Y. and Tanabe, T. 2002. 1-Octen-3-ol together with geosmin: new secretion compounds from a polydesmid millipede, Niponia nodulosa. Journal of Chemical Ecology, 28: 2601–2612.

Peschke, K. and Eisner, T. 1987. Defensive secretion of the tenebrionid beetle, Blaps mucronata: Physical and chemical determinants of effectiveness. Journal of Comparative Physiology, 161: 377–388.

Pimvichai, P., Enghoff, H. and Panha, S. 2010. The Rhynchoproctinae, a south-east Asiatic subfamily of giant millipedes: cladistic analysis, classification, four new genera and a deviating new species from north-west Thailand (Diplopoda: Spirostreptida: Harpagophoridae). Invertebrate Systematics, 24: 51–80.

Pimvichai, P., Enghoff, H. and Panha, S. 2014. Molecular phylogeny of the Thyropygus allevatus group of giant millipedes and some closely related groups. Molecular Phylogenetics and Evolution, 71: 170–183.

Pimvichai, P., Enghoff, H. and Panha, S. 2016. A revision of the Thyropygus allevatus group. Part 5: the T. allevatus subgroup (Diplopoda: Spirostreptida: Harpagophoridae). European Journal of Taxonomy, 199: 1–37.

Rodriguez, J., Jones, T.H., Sierwald, P., Marek, P.E., Shear, W.A., Brewer, M.S., Kocot, K.M. and Bond, J.E. 2018. Step-wise evolution of complex chemical defenses in millipedes: a phylogenomic approach. Scientific Reports, 8: 3209.

Shahidi, F. and Yeo, J. 2018. Bioactivities of phenolics by focusing on suppression of chronic diseases: A review. International Journal of Molecular Sciences, 19: 1573.

Shear, W.A. 2015. The chemical defenses of millipedes (Diplopoda): biochemistry, physiology and ecology. Biochemical Systematics and Ecology, 61: 78–117.

Shimizu, N., Kuwahara, Y., Yakumaru, R. and Tanabe, T. 2012. n-Hexyl laurate and fourteen related fatty acid esters: new secretory compounds from the julid millipede, Anaulaciulus sp. Journal of Chemical Ecology, 38: 23–28.

Stanković, S., Dimkić, I., Vujisić, L., Pavković-Lučić, S., Jovanović, Z., Stević, T., T, Sofrenić, I., Mitić, B. and Tomić, V. 2016. Chemical defence in a millipede: Evaluation and characterization of antimicrobial activity of the defensive secretion from Pachyiulus hungaricus (Karsch, 1881) (Diplopoda, Julida, Julidae). PLoS One, 11(12).

Tomsone, L., Kruma, Z. and Galoburda, R. 2012. Comparison of different solvents and extraction methods for isolation of phenolic compounds from horseradish roots (Armoracia rusticana). International Scholarly and Scientific Research & Innovation, 6: 236–241.

Valderrama, X., Robinson, J.G., Attygalle, A.B. and Eisner, T. 2000. Seasonal anointment with millipedes in a wild primate: a chemical defense against insects? Journal of Chemical Ecology, 26: 2781–2790.

Vujisić, L.V., Makarov, S.E., Ćurčić, B.P.M., Ilić, B.S., Tešević, V.V., Godevac, D.M., Vučković, I.M., Ćurčić, S.B. and Mitić, B.M. 2011. Composition of the defensive secretion in three species of European millipedes. Journal of Chemical Ecology, 37: 1358–1364.

Vujisić, L.V., Antić, D.Ž., Vučković, I.M., Sekulić, T.L., Tomić, V.T., Mandić, B.M., Tešević, V.V., Ćurčić, B.P.M., Vajs, V.E. and Makarov, S.E. 2014. Chemical defense in millipedes (Myriapoda, Diplopoda): do representatives of the family Blaniulidae belong to the ‘quinone’ clade? Chemistry and Biodiversity, 11: 483–490.

Weldon, P.J., Aldrich, J.R., Klun, J.A., Oliver, J.E. and Debboun, M. 2003. Benzoquinones from millipedes deter mosquitoes and elicit self-anointing in capuchin monkeys (Cebus spp.). Naturwissenschaften, 90: 301–304.

Downloads

Published

2023-03-21

How to Cite

[1]
Tummanam, A. , Sutthisa, W. , Radchatawedchakoon, W. , Backeljau, T. and Pimvichai, P. 2023. Composition and Antimicrobial Activity of Defensive Secretions of the Giant Millipede Anurostreptus sculptus (Diplopoda, Spirostreptida, Harpagophoridae). Tropical Natural History. 23, 1 (Mar. 2023), 42–51.

Issue

Vol. 23 (2023): Tropical Natural History

Section

Original Articles

Categories

License

Chulalongkorn University. All rights reserved. No part of this publication may be reproduced, translated, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without prior written permission of the publisher