Sponge-Based Ecofriendly Antifouling: Field Study on Nets, Molecular Docking with Agelasine Alkaloids



  • Walter Balansa Department of Fisheries and Maritime Technology, Politeknik Negeri Nusa Utara, Kepulauan Sangihe, North Sulawesi, 95812. Indonesia
  • Riyanti Faculty of Fisheries and Marine Science, Jenderal Soedirman University, Purwokerto 53122, Indonesia
  • Usy N. Manurung Department of Agribusiness, Universitas Terbuka, South Tanggerang, 15415. Indonesia
  • Aprelia M. Tomasoa Department of Fisheries and Maritime Technology, Politeknik Negeri Nusa Utara, Kepulauan Sangihe, North Sulawesi, 95812. Indonesia
  • Novriyandi Hanif Department of Chemistry, Faculty of Mathematics and Natural Sciences, IPB University (Bogor Agri-cultural University), Bogor 16680, Indonesia
  • Frets J. Rieuwpassa Department of Fisheries and Maritime Technology, Politeknik Negeri Nusa Utara, Kepulauan Sangihe, North Sulawesi, 95812. Indonesia
  • Till F. Schäberle Institute for Insect Biotechnology, Justus-Liebig-University of Giessen, 35392 Giessen, Germany


Agelas nakamurai, agelasines, acetylcholinesterase, Antifouling


Biofouling poses a significant threat to fisheries and maritime sectors, capable of damaging ship hulls, mariculture facilities, and marine structures. Despite the effectiveness of tributyl tin (TBT)-based antifouling in solving biofouling problems, it threatens the marine environment and human health, necessitating the exploration of ecofriendly antifouling agents. Marine sponges have evolved unique antifouling strategies that may contain potential solutions to this problem. Hence, an epoxy resin coating enriched with powder from the sponge Agelas nakamurai underwent field testing on polyethylene nets. Analysis of variance (ANOVA) demonstrated that nets pre-treated with 100, 200, and 300 mg/mL of the epoxy resin and sponge powder mix had a significant effect on biofouling growth (P < 0.05). Post-hoc Tukey’s test indicated that the 100 mg/mL treatment significantly differed from other treatments. Since the authors previously characterized and predicted the presence of agelasines A-F (1-6) and agelasidine A (7) from the same sponge using NMR/LC-MS and MS-MS annotation, the currently studied A. nakamurai contains the same molecules. Molecular docking studies identified agelasines A-F and agelasidine A as promising acetylcholinesterase (AChE) inhibitors, rivaling or surpassing the AChE specific inhibitors, such as synoxazolidinones A (8) and C (9), and the antifouling agents Seanin_211 (10) and Irgarol_1501 (11). In silico ADME-T and TEST analyses on compounds 1-11 indicated that, while agelasines A-F need further optimization, agelasidine A was the most promising compound identified as potential antifouling agent in this research. This study marks the initial step in evaluating agelasines and other marine-derived molecules as eco-friendly antifouling agents

Author Biography

Till F. Schäberle, Institute for Insect Biotechnology, Justus-Liebig-University of Giessen, 35392 Giessen, Germany

Fraunhofer Institute for Molecular Biology and Applied Ecology (IME), Branch for Bioresources, 35392 Giessen, Germany.


Gomez, BJ. Marine natural products: a promising source of environmentally friendly antifouling agents for the maritime industries. Front. Mar. Sci. 2022;9:858757. doi.org/10.3389/fmars.2022.858757.

Liu LL, Wu CH, Qian PY. Marine natural products as antifouling molecules–a mini-review (2014–2020). Biofoul. 2020;36(10):1210-1226. doi:10.1080/08927014.2020.1864343

Qi SH, Ma X. Antifouling compounds from marine invertebrates. Mar Drugs. 2017;15(9). doi:10.3390/md15090263

Qian PY, Li Z, Xu Y, Li Y, Fusetani N. Mini-review: Marine natural products and their synthetic analogs as antifouling compounds: 2009–2014. Biofoul. 2015;31(1):101-122. doi:10.1080/08927014.2014.997226

Wang KL, Xu Y, Lu L, Li Y, Han Z, Zhang J, Shao CL, Wang CY, Qian PY. Low-toxicity diindol-3-ylmethanes as potent antifouling compounds. Mar Biotechnol. 2015;17(5):624-632. doi:10.1007/s10126-015-9656-6

Wang KL, Wu ZH, Wang Y, Wang CY, Xu Y. Mini-review: Antifouling natural products from marine microorganisms and their synthetic analogs. Mar Drugs. 2017;15(9):1-21. doi:10.3390/md15090266

Prieto IM, Paola A, Pérez M, García M, Blustein G, Schejter L, Palermo JA. Antifouling diterpenoids from the sponge Dendrilla antarctica. Chem Biodivers. 2022;19(2):2003-2005.doi: doi.org/10.1002/cbdv.202100618.

Sánchez LI, Hernández GCJ, Muñoz, OM, Hellio C. Biomimetic approaches for the development of new antifouling solutions: Study of incorporation of macroalgae and sponge extracts for the development of new environmentally-friendly coatings. Int J Mol Sci. 2019;20(19):1-18. doi:10.3390/ijms20194863.

Chiang HY, Cheng J, Liu X, Ma C, Qian PY. Synthetic analogue of butenolide as an antifouling agent. Mar Drugs. 2021;19(9):1-12. doi:10.3390/md19090481

Liang X, Luo D, Luesch H. Advances in exploring the therapeutic potential of marine natural products. Pharmacol Res. 2019;147:104373. doi:10.1016/j.phrs.2019.104373

Fusetani N. Antifouling marine natural products. Nat Prod Rep. 2011;28(2):400-410. doi:10.1039/c0np00034e

Xu Y, He H, Schulz S, Liu X, Fusetani N, Xiong H, Xiao X, Qian PY. Potent antifouling compounds produced by marine Streptomyces. Bioresour Technol. 2010;101(4):1331-1336. doi:10.1016/j.biortech.2009.09.046

Puentes C, Carreño K, Santos-Acevedo M, Gómez-León J, García M, Pérez M, Stupak M, Blustein G. Anti-fouling paints based on extracts of marine organisms from the Colombian Caribbean. Cienc y Tecnol buques. 2014;8(15):75. doi:10.25043/19098642.105.

Henrikson AA, Pawlik JR. A new antifouling assay method: results from field experiments using extracts of four marine organisms. J Exp Mar Bio Ecol. 1995;194(2):157-165. doi:10.1016/0022-0981(95)00088-7

Satheesh S, Ba-Akdah MA, Al-Sofyani AA. Natural antifouling compound production by microbes associated with marine macroorganisms — A review. Electron J Biotechnol. 2016;21(2015):26-35. doi:10.1016/j.ejbt.2016.02.002

Pereira F, Aires-de-Sousa J. Computational methodologies in the exploration of marine natural product leads. Mar Drugs. 2018;16(7). doi:10.3390/md16070236.

Hellio C, Yebra D. Advances in marine antifouling coatings and technologies. Woodhead Publishing Limited, Cambridge. 2009. 748 p.

Agamah FE, Mazandu GK, Hassan R, Bope CD, Thomford NE, Ghansah A, Chimusa ER. Computational/in silico methods in drug target and lead prediction. Brief Bioinform. 2020;21(5):1663-1675. doi:10.1093/bib/bbz103

Lind U, Rosenblad MA, Frank LH, Falkbring S, Brive L, Laurila JM, Pohjanoksa K, Vuorenpää A, Kukkonen JP, Gunnarsson L, Scheinin M.l. Octopamine receptors from the barnacle Balanus improvisus are activated by the α2-adrenoceptor agonist medetomidine. Mol Pharmacol. 2010;78(2):237-248. doi:10.1124/mol.110.063594

Dhanjal JK, Sharma S, Grover A, Das A. Use of ligand-based pharmacophore modeling and docking approach to find novel acetylcholinesterase inhibitors for treating Alzheimer’s. Biomed Pharmacother. 2015;71:146-152. doi:10.1016/j.biopha.2015.02.010

Akıncıoğlu H, Gülçin İ. Potent Acetylcholinesterase inhibitors: potential drugs for Alzheimer’s disease. Mini Rev Med Chem. 2020;20(8):703-715.

Arabshahi HJ, Trobec T, Foulon V, Hellio C, Frangež R, Sepčić K, Cahill P, Svenson J. Using Virtual AChE Homology screening to identify small molecules with the ability to inhibit marine biofouling. Front Mar Sci. 2021;8:1-12. doi:10.3389/fmars.2021.762287

Almeida JR, Moreira J, Pereira D, Pereira S, Antunes J, Palmeira A, Vasconcelos V, Pinto M, Correia-da-Silva M, Cidade H. Potential of synthetic chalcone derivatives to prevent marine biofouling. Sci Total Environ. 2018;643:98-106. doi:10.1016/j.scitotenv.2018.06.169

Blihoghe D, Manzo E, Villela A, Cutignano A, Picariello G, Faimali M, Fontana A. Evaluation of the antifouling properties of 3-alyklpyridine compounds. Biofoul. 2011;27(1):99-109. doi:10.1080/08927014.2010.542587

Yu X, Yan Y, Gu JD. Attachment of the biofouling bryozoan Bugula neritina larvae affected by inorganic and organic chemical cues. Int Biodeterior Biodegrad. 2007;60(2):81-89. doi:10.1016/j.ibiod.2006.12.003

Mansueto V, Cangialosi MV, Arukwe A. Acetylcholinesterase activity in juvenile Ciona intestinalis (Ascidiacea, Urochordata) after exposure to tributyltin. Caryolog. 2012;65(1):18-26. doi:10.1080/00087114.2012.678082

Sjögren M, Dahlström M, Hedner E, Jonsson PR, Vik A, Gundersen LL, Bohlin L. Antifouling activity of the sponge metabolite agelasine D and synthesised analogs on Balanus improvisus. Biofoul. 2008;24(4):251-258. doi:10.1080/08927010802072753

Tadesse, M., Svenson, J., Sepčić, K., Trembleau, L., Engqvist, M., Andersen, J.H., Jaspars, M., Stensvåg, K. and Haug, T. Isolation and synthesis of pulmonarins A and B, acetylcholinesterase inhibitors from the colonial ascidian Synoicum pulmonaria. J Nat Prod. 2014;77(2):364-369. doi:10.1021/np401002s

Chu MJ, Li M, Ma H, Li PL, Li GQ. Secondary metabolites from marine sponges of the genus Agelas: A comprehensive update insight on structural diversity and bioactivity. RSC Adv. 2022;12(13):7789-7820. doi:10.1039/d1ra08765g

Balansa W, Wodi SIM, Rieuwpassa FJ, Ijong FG. Agelasines B, D and antimicrobial extract of a marine sponge Agelas sp. From Tahuna Bay, Sangihe Islands, Indonesia. Biodiv. 2020;21(2):699-706. doi:10.13057/biodiv/d210236

Riyanti, Marner M, Hartwig C, Patras MA, Wodi SI, Rieuwpassa FJ, Ijong FG, Balansa W, Schäberle TF. Sustainable low-volume analysis of environmental samples by semi-automated prioritization of extracts for natural product research (SeaPEPR). Mar Drugs. 2020;18(649):1-15.

Liu Y, Grimm M, Dai W tao, Hou M chun, Xiao ZX, Cao Y. CB-Dock: a web server for cavity detection-guided protein–ligand blind docking. Acta Pharmacol Sin. 2020;41(1):138-144. doi:10.1038/s41401-019-0228-6

Pires DEV, Blundell TL, Ascher DB. pkCSM: Predicting small-molecule pharmacokinetic and toxicity properties using graph-based signatures. J Med Chem. 2015;58(9):4066-4072. doi:10.1021/acs.jmedchem.5b00104

Daina A, Michielin O, Zoete V. SwissADME: A free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Sci Rep. 2017;7(March):1-13. doi:10.1038/srep42717

Hattori T, Adachi K, Shizuri Y. New agelasine compound from the marine sponge Agelas mauritiana as an antifouling substance against macroalgae. J Nat Prod. 1997;60(4):411-413. doi:10.1021/np960745b

Hertiani T, Edrada-Ebel R, Ortlepp S, van Soest RW, de Voogd NJ, Wray V, Hentschel U, Kozytska S, Müller WE, Proksch P. From anti-fouling to biofilm inhibition: New cytotoxic secondary metabolites from two Indonesian Agelas sponges. Bioorganic Med Chem. 2010;18(3):1297-1311. doi:10.1016/j.bmc.2009.12.028

Hodson SL, Lewis TE, Burke CM. Biofouling of fish-cage netting: Efficacy and problems of in situ cleaning. Aquaculture. 1997;152(1-4):77-90. doi:10.1016/S0044-8486(97)00007-0

Hudson S, Lewis TE, Burke CM. In situ quantification of fish-cage fouling by underwater photography and image analysis. Biofoul. 1995;9(2):145-151. doi:10.1080/08927019509378298

Kartal GE, Sarıışık AM. Providing antifouling properties to fishing nets with encapsulated econea. J Ind Text. 2022;5:7569S-7586S. doi:10.1177/1528083720920568

Yoda I, Koseki H, Tomita M, Shida T, Horiuchi H, Sakoda H, Osaki, M. Effect of surface roughness of biomaterials on Staphylococcus epidermidis adhesion. BMC Microbiol. 2014;14(1):1-7. doi:10.1186/s12866-014-0234-2

Bollen CML, Papaioanno W, Van Eldere J, Schepers E, Quirynen M, Van Steenberghe D. The influence of abutment surface roughness on plaque accumulation and peri-implant mucositis. Clin Oral Implants Res. 1996;7(3):201-211. doi:10.1034/j.1600-0501.1996.070302.x

Abdalla MM, Ali IA, Khan K, Mattheos N, Murbay S, Matinlinna JP, Neelakantan P. The Influence of surface roughening and polishing on microbial biofilm development on different ceramic materials. J Prosthodont. 2021;30(5):447-453. doi:10.1111/jopr.13260

Nogueira RD, Silva CB, Lepri CP, Palma-Dibb RG, Geraldo-Martins VR. Evaluation of surface roughness and bacterial adhesion on tooth enamel irradiated with high intensity lasers. Braz Dent J. 2017;28(1):24-29. doi:10.1590/0103-6440201701190

Yu B, Chen X, Li J, Qu Y, Su L, Peng Y, Huang J, Yan J, Yu Y, Gu Q, Zhu Z. Stromal fibroblasts in the microenvironment of gastric carcinomas promote tumor metastasis via upregulating TAGLN expression. BMC Cell Biol. 2013;14(1):1. doi:10.1186/1471-2121-14-17

Xing R, Lyngstadaas SP, Ellingsen JE, Taxt-Lamolle S, Haugen HJ. The influence of surface nanoroughness, texture and chemistry of TiZr implant abutment on oral biofilm accumulation. Clin Oral Implants Res. 2015;26(6):649-656. doi:10.1111/clr.12354

Yao WL, Lin JC, Salamanca E, Pan YH, Tsai PY, Leu SJ, Yang KC, Huang HM, Huang HY, Chang WJ. Er, Cr. Laser Performance Improves Biological. Mater. 2020;13(1):1-14.

Gaudêncio SP, Pereira F. Predicting antifouling activity and acetylcholinesterase inhibition of marine-derived compounds using a computer-aided drug design approach. Mar Drugs. 2022;20(2). doi:10.3390/md20020129

Hayes AW, Loomis TA. Loomis's essentials of toxicology. (4th ed.). New York: Academic Press; 1996, 282 p.

Chu MJ, Li M, Ma H, Li PL, Li GQ. Secondary metabolites from marine sponges of the genus Agelas: a comprehensive update insight on structural diversity and bioactivity. RSC adv. 2022;12(13):7789-820

Do JW, Haque MN, Lim HJ, Min BH, Lee DH, Kang JH, Kim M, Jung JH, Rhee JS. Constant exposure to environmental concentrations of the antifouling biocide Sea-Nine retards growth and reduces acetylcholinesterase activity in a marine mysid. Aquat Toxicol. 2018;205:165-173. doi:10.1016/j.aquatox.2018.10.019

Lee DH, Eom HJ, Kim M, Jung JH, Rhee JS. Non-target effects of antifouling agents on mortality, hatching success, and acetylcholinesterase activity in the brine shrimp Artemia salina. Toxicol Environ Health Sci. 2017;9(3):237-243. doi:10.1007/s13530-017-0326-0

Polanski J, Bogocz J, Tkocz A. The analysis of the market success of FDA approvals by probing top 100 bestselling drugs. J Comput Aided Mol Des. 2016;30(5):381-389. doi:10.1007/s10822-016-9912-5

Wang S, Dong G, Sheng C. Structural simplification: an efficient strategy in lead optimization. Acta Pharm Sin B. 2019;9(5):880-901. doi:10.1016/j.apsb.2019.05.004

Pereira F. Have marine natural product drug discovery efforts been productive and how can we improve their efficiency? Exp. Op. Drug Dis. 2019;14(8):717-22.

Indraningrat AAG, Smidt H, Sipkema D. Bioprospecting sponge-associated microbes for antimicrobial compounds. Mar Drugs. 2016;14(5):1-66. doi:10.3390/md14050087

Qiu H, Feng K, Gapeeva A, Meurisch K, Kaps S, Li X, Yu L, Mishra YK, Adelung R, Baum M. Functional polymer materials for modern marine biofouling control. Prog Polym Sci. 2022;127. doi:10.1016/j.progpolymsci.2022.101516

Zheng S, Bawazir M, Dhall A, Kim HE, He L, Heo J, Hwang G. Implication of surface properties, bacterial motility, and hydrodynamic conditions on bacterial surface sensing and their initial adhesion. Front Bioeng Biotechnol. 2021;9:1-22. doi:10.3389/fbioe.2021.643722



How to Cite

Balansa, W., Riyanti, Manurung, U. N., Tomasoa, A. M., Hanif, N., Rieuwpassa, F. J., & Schäberle, T. F. (2024). Sponge-Based Ecofriendly Antifouling: Field Study on Nets, Molecular Docking with Agelasine Alkaloids: http://www.doi.org/10.26538/tjnpr/v8i1.29. Tropical Journal of Natural Product Research (TJNPR), 8(1), 5913–5924. Retrieved from https://tjnpr.org/index.php/home/article/view/3414