Harnessing the metabolites from the marine sponge Melophlus sarasinorum for the discovery of eco-friendly antifoulants

Main Article Content

WALTER BALANSA
RIYANTI
MARIA A. PATRAS
KIRSTEN H. BALANSA
NOVRIYANDI HANIF
FRETS J. RIEUWPASSA
MARGARET HILL
TILL F. SCHÄBERLE

Abstract

Abstract. Balansa W, Riyanti, Patras MA, Balansa KH, Hanif N, Rieuwpassa FJ, Hill M, Schäberle TF. 2025. Harnessing the metabolites from the marine sponge Melophlus sarasinorum for the discovery of eco-friendly antifoulants. Biodiversitas 26: 1590-1606. Marine biofouling remains an unresolved issue in both the maritime industry and the marine environment, demanding the discovery of new eco-friendly antifoulants. This study aimed to evaluate the antifouling potential of the marine sponge, Melophlus sarasinorum (Thiele, 1899), through metabolomic, computational, and field studies. Seven compounds were dereplicated as sarasinosides A1-A3, D, L, M, and M2 (1-7) from extracts of M. sarasinorum from Kawaluso and Mahumu Islands. Molecular docking showed robust binding affinities for 1-7 (-8.2 to -9.6 kcal/mol), rivaling acetylcholinesterase (AChE) inhibitors, synoxazolidinones A (8) and C (9), commercial antifoulants medetomidine/selektope® (12) and econea® (13) (-9.2, -9.3, -9.5, -9.3 kcal/mol, respectively) as well as the antifouling agents, seanin_211 (10) (-8.9 kcal/mol) and irgarol_1505 (11) (-5.5, -6.5 kcal/mol, respectively). The strong binding affinities of 1-7 suggest possible new allosteric interactions with AChE. The ANOVA test revealed a significant difference in biofouling growth (p<0.05) between nets pre-treated with 1:1, 1:2, or 1:3 sponge powder/epoxy mixture compared to other treatments, as confirmed by a post-hoc Duncan test. Notably, toxicity studies with EPI SuiteTM indicated that 1-7 had more eco-friendly toxicological parameters (i.e., low Log Kow, Log Koc, Biotransformation Half-life, and water solubility) compared to AChE inhibitors and commercial antifouling agents (p<0.05). Our results demonstrate the antifouling activity of sarasinosides (1-7), providing insight into the design of novel, eco-friendly antifoulants that warrant further investigation into their mode of action and optimization.

Article Details

Section

Articles

References

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

Almeida JR, Palmeira A, Campos A, Cunha I, Freitas M, Felpeto AB, Turkina MV, Vasconcelos V, Pinto M, Correia-da-Silva M, Sousa M. 2020. Structure-antifouling activity relationship and molecular targets of bio-inspired (thio) xanthones. Biomolecules 10 (8): 1126. DOI: 10.3390/biom10081126.

Arabshahi HJ, Trobec T, Foulon V, Hellio C, Frangež R, Sep?i? K, Cahill P, Svenson J. 2021. Using virtual AChE homology screening to identify small molecules with the ability to inhibit marine biofouling. Front Mar Sci 8: 762287. DOI: 10.3389/fmars.2021.762287.

Aron AT, Gentry EC, McPhail KL et al. 2020. Reproducible molecular networking of untargeted mass spectrometry data using GNPS. Nat Protoc 15 (6): 1954-1991. DOI: 10.1038/s41596-020-0317-5.

Aronowitz AL, Ali SR, Glaun MDE, Amit M. 2022. Acetylcholine in carcinogenesis and targeting cholinergic receptors in oncology (Adv. Biology 9/2022). Adv Biol 6 (9): 2270091. DOI: 10.1002/adbi.202270091.

Austin P, Freeman SA, Gray CA, Gold MR, Vogl AW, Andersen RJ, Roberge M, Roskelley CD. 2013. The invasion inhibitor sarasinoside A1 reverses mesenchymal tumor transformation in an E-cadherin-independent manner. Mol Cancer Res 11 (5): 530-540. DOI: 10.1158/1541-7786.MCR-12-0385.

Ayesu EK. 2023. Does shipping cause environmental emissions? Evidence from African countries. Transp Res Interdiscip Persp 21: 100873. DOI: 10.1016/j.trip.2023.100873.

Balansa W, Riyanti, Manurung UN, Tomasoa AM, Hanif N, Rieuwpassa FJ, Schäberle TF. 2024. Sponge-based ecofriendly antifouling: Field study on nets, molecular docking with agelasine alkaloids. Trop J Nat Prod Res 8 (1): 5913-5924. DOI: 10.26538/tjnpr/v8i1.29.

Balansa W. 2014. Discovery of novel, potent and selective glycine receptor modulators from Southern Australian sponges. [Dissertation]. Institute for Molecular Bioscience, The University of Queensland. DOI: 10.14264/uql.2016.29.

Bannister J, Sievers M, Bush F, Bloecher N. 2019. Biofouling in marine aquaculture: A review of recent research and developments. Biofouling 35 (6): 631-648. DOI: 10.1080/08927014.2019.1640214.

Bhal SK. 2007. LogP—Making Sense of the Value. Advanced Chemistry Development. Toronto, ON. Canada.

Byers JE, Blaze JA, Dodd AC, Hall HL, Gribben PE. 2023. Exotic asphyxiation: Interactions between invasive species and hypoxia. Biol Rev Camb Philos Soc 98 (1): 150-167. DOI: 10.1111/brv.12900.

Card ML, Gomez-Alvarez V, Lee W-H, Lynch DG, Orentas NS, Lee MT, Wong EM, Boethling RS. 2017. History of EPI SuiteTM and future perspectives on chemical property estimation in US toxic substances control act new chemical risk assessments. Environ Sci Process Impacts 19 (3): 203-212. DOI: 10.1039/c7em00064b.

Carroll AR, Copp BR, Davis RA, Keyzers RA, Prinsep MR. 2022. Marine natural products. Nat Prod Rep 39 (6): 1122-1171. DOI: 10.1039/D1NP00076D.

Chen J, Bai W, Jian R, Lin Y, Zheng X, Wei F, Lin Q, Lin F, Xu Y. 2024a. Molecular structure design of polybenzoxazines with low surface energy and low modulus for marine antifouling application. Prog Org Coat 187: 108165. DOI: 10.1016/j.porgcoat.2023.108165.

Chen J, Jian R, Yang K, Bai W, Huang C, Lin Y, Zheng B, Wei F, Lin Q, Xu Y. 2021. Urushiol-based benzoxazine copper polymer with low surface energy, strong substrate adhesion and antibacterial for marine antifouling application. J Clean Prod 318: 128527. DOI: 10.1016/j.jclepro.2021.128527.

Chen J, Zhao J, Lin F, Zheng X, Jian R, Lin Y, Wei F, Lin Q, Bai W, Xu Y. 2023. Polymerized tung oil toughened urushiol-based benzoxazine copper polymer coatings with excellent antifouling performances. Prog Org Coat 177: 107411. DOI: 10.1016/j.porgcoat.2023.107411.

Chen J, Zheng X, Jian R, Bai W, Zheng G, Xie Z, Lin Q, Lin F, Xu Y. 2024b. In situ reduction of silver nanoparticles/urushiol-based polybenzoxazine composite coatings with enhanced antimicrobial and antifouling performances. Polymers 16 (8): 1167. DOI: 10.3390/polym16081167.

Chen L, Lam JCW. 2017. SeaNine 211 as antifouling biocide: A coastal pollutant of emerging concern. J Environ Sci 61: 68-79. DOI: 10.1016/j.jes.2017.03.040.

Costanzo LG, Marletta G, Alongi G. 2021. Non-indigenous macroalgal species in coralligenous habitats of the marine protected area Isole Ciclopi (Sicily, Italy). Ital Bot 11: 31-44. DOI: 10.3897/italianbotanist.11.60474.

Cui YT, Teo SLM, Leong W, Chai CLL. 2014. Searching for "environmentally-benign" antifouling biocides. Intl J Mol Sci 15 (6): 9255-9284. DOI: 10.3390/ijms15069255.

Cuthbert RN, Pattison Z, Taylor NG et al. 2021. Global economic costs of aquatic invasive alien species. Sci Total Environ 775: 145238. DOI: 10.1016/j.scitotenv.2021.145238.

Dai HF, Edrada RA, Ebel R, Nimtz M, Wray V, Proksch P. 2005. Norlanostane triterpenoidal saponins from the marine Sponge Melophlus sarassinorum. J Nat Prod 68: 1231-1237. DOI: 10.1021/np050152d.

Dobretsov S, Rittschof D. 2023. "Omics" Techniques used in marine biofouling studies. Intl J Mol Sci 24 (13): 10518. DOI: 10.3390/ijms241310518.

ECHA [Environment and Climate Change Canada]. 2017. Guidance on information requirements and chemical safety assessment. Environment and Climate Change, Canada.

ECHA [Environment and Climate Change Canada]. 2021. Toxic substances list: schedule 1 (Tech.). Retrieved from https://www.canada.ca/en/ environment-climate-change/services/canadian-environmental-protection-act-registry/substances-list/toxic/schedule-1.html.

Farkas A, Degiuli N, Marti? I, Vujanovi? M. 2021. Greenhouse gas emissions reduction potential by using antifouling coatings in a maritime transport industry. J Clean Prod 295: 126428. DOI: 10.1016/j.jclepro.2021.126428.

Ferreira Montenegro P, Pham GN, Abdoul-Latif FM, Taffin-de-Givenchy E, Mehiri M. 2024. Marine bromotyrosine derivatives in spotlight: Bringing discoveries and biological significance. Mar Drugs 22 (3): 132. DOI: 10.3390/md22030132.

Gaudêncio SP, Pereira F. 2022. Predicting antifouling activity and acetylcholinesterase inhibition of marine-derived compounds using a computer-aided drug design approach. Mar Drugs 20 (2): 129. DOI: 10.3390/md20020129.

Georgiades E, Kluza D, Bates T, Lubarsky K, Brunton J, Growcott A, Smith T, McDonald S, Gould B, Parker N, Bell A. 2020. Regulating vessel biofouling to support New Zealand's marine biosecurity system-a blue print for evidence-based decision making. Front Mar Sci 7: 390. DOI: 10.3389/fmars.2020.00390.

Georgiades E, Scianni C, Davidson I, Tamburri MN, First MR, Ruiz G, Ellard K, Deveney M, Kluza D. 2021. The role of vessel biofouling in the translocation of marine pathogens: Management considerations and challenges. Front Mar Sci 8: 660125. DOI: 10.3389/fmars.2021.660125.

Gomez-Banderas J. 2022. Marine natural products: A promising source of environmentally friendly antifouling agents for the maritime industries. Front Mar Sci 9: 858757. DOI: 10.3389/fmars.2022.858757.

Hadži? N, Gatin I, Uroi? T, Ložar V. 2022. Biofouling dynamic and its impact on ship powering and dry-docking. Ocean Eng 245: 110522. DOI: 10.1016/j.oceaneng.2022.110522.

Hodson SL, Lewis TE, Burkea CM. 1997. Biofouling of fish-cage netting: Efficacy and problems of in situ cleaning. Aquaculture 152 (1-4): 77-90. DOI: 10.1016/s0044-8486(97)00007-0.

Hooper JNA, Van Soest RWM. 2002. Systema Porifera: A Guide to The Supraspecific Classification of The Phylum Sponges. Kluwer Academic/Plenum Publishers, New York.

Ivanchina NV, Kalinin VI. 2023. Triterpene and steroid glycosides from marine sponges (Porifera, Demospongiae): Structures, taxonomical distribution, biological activities. Molecules 28 (6): 2503. DOI: 10.3390/molecules28062503.

James GA, Boegli L, Hancock J, Bowersock L, Parker A, Kinney BM. 2019. Bacterial adhesion and biofilm formation on textured breast implant shell materials. Aesthetic Plast Surg 43 (2): 490-497. DOI: 10.1007/s00266-018-1234-7.

Johnson G, Moore SW. 2006. The peripheral anionic site of acetylcholinesterase: Structure, functions and potential role in rational drug design. Curr Pharm Des 12 (2): 217-225. DOI: 10.2174/138161206775193127.

Kalinin VI, Ivanchina NV, Krasokhin VB, Makarieva TN, Stonik VA. 2012. Glycosides from marine sponges (porifera, Demospongiae): Structures, taxonomical distribution, biological activities and biological roles. Mar Drugs 10 (8): 1671-1710. DOI: 10.3390/md10081671.

Kartal GE, Sar????k AM. 2022. Providing antifouling properties to fishing nets with encapsulated Econea. J Indust Text 51: 7569S-7586S. DOI: 10.1177/1528083720920568.

Kobayashi M, Okamoto Y, Kitagawa I. 1991. Marine natural products. XXVIII. The structures of sarasinosides A1, A2, A3, B1, B2, B3, C1, C2, and C3, nine new norlanostane-triterpenoidal oligoglycosides from the Palauan marine sponge Asteropus sarasinosum. Chem Pharm Bull 39 (11): 2867-2877.

Kobayashi Y. 2021. Analysis of The Environmental Parameters for Risk Assessment of Pesticides by Machine Learning Approach. [Dissertation]. University of Tsukuba, Japan.

Lee D-H, Eom H-J, Kim M, Jung J-H, Rhee J-S. 2017. Non-target effects of antifouling agents on mortality, hatching success, and acetylcholinesterase activity in the brine shrimp Artemia salina. Toxicol Environ Health Sci 9: 237-243. DOI: 10.1007/s13530-017-0326-0.

Liu H, Yang W, Zhao W, Zhang J, Cai M, Pei X, Zhou F. 2020. Natural product inspired environmentally friendly strategy based on dopamine chemistry toward sustainable marine antifouling. ACS Omega 5 (34): 21524-21530. DOI: 10.1021/acsomega.0c02114.

Luque FJ, Muñoz-Torrero D. 2024. Acetylcholinesterase: A versatile template to coin potent modulators of multiple therapeutic targets. Acc Chem Res 57 (4): 450-467. DOI: 10.1021/acs.accounts.3c00617.

Mackay D, Fraser A. 2000. Bioaccumulation of persistent organic chemicals: Mechanisms and models. Environ Pollut 110 (3): 375-391. DOI: 10.1016/S0269-7491(00)00162-7.

Marcelo F, Dias C, Martins A, Madeira PJ, Jorge T, Florêncio MH, Cañada FJ, Cabrita EJ, Jiménez?Barbero J, Rauter AP. 2013. Molecular recognition of rosmarinic acid from Salvia sclareoides extracts by acetylcholinesterase: A new binding site detected by NMR spectroscopy. Chemistry 19 (21): 6641-6649. DOI: 10.1002/chem.201203966.

Marucci G, Buccioni M, Ben DD, Lambertucci C, Volpini R, Amenta F. 2021. Efficacy of acetylcholinesterase inhibitors in Alzheimer's disease. Neuropharmacology 190: 108352. DOI: 10.1016/j.neuropharm.2020.108352.

Maslin M, Gaertner-Mazouni N, Debitus C, Joy N, Ho R. 2021. Marine sponge aquaculture towards drug development: An ongoing history of technical, ecological, chemical considerations and challenges. Aquac Rep 21: 100813. DOI: 10.1016/j.aqrep.2021.100813.

Mehbub MF, Yang Q, Cheng Y, Franco CMM, Zhang W. 2024. Marine sponge-derived natural products: Trends and opportunities for the decade of 2011-2020. Front Mar Sci 11: 1462825. DOI: 10.3389/fmars.2024.1462825.

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

Nong X-H, Wang Y-F, Zhang X-Y, Zhou M-P, Xu X-Y, Qi S-H. 2014. Territrem and butyrolactone derivatives from a marine-derived fungus Aspergillus terreus. Mar Drugs 12 (12): 6113-6124. DOI: 10.3390/md12126113.

O’Brien S, Lacret R, Reddy MM, Jennings LK, Sánchez P, Reyes F, Mungkaje A, Calabro K, Thomas OP. 2023. Additional sarasinosides from the marine sponge Melophlus sarasinorum collected from the Bismarck Sea. J Nat Prod 86 (12): 2730-2738. DOI: 10.1021/acs.jnatprod.3c01045.

Okamura H, Aoyama I, Liu D, Maguire RJ, Pacepavicius GJ, Lau YL. 2000. Fate and ecotoxicity of the new antifouling compound irgarol 1051 in the aquatic environment. Water Res 34 (14): 3523-3530. DOI: 10.1016/s0043-1354(00)00095-6.

Olick D. 2023. Shipping industry could lose S10 billiong a year battling climate change by 2050. CNBC. https://www.cnbc.com/2023/10/30/ climate-change-to-cost-shipping-industry-10-billion-a-year-by-2050.html.

Ozupek NM, Cavas L. 2017. Triterpene glycosides associated antifouling activity from Holothuria tubulosa and H. polii. Reg Stud Mar Sci 13: 32-41. DOI: 10.1016/j.rsma.2017.04.003.

Pérez-Aguilar B, Marquardt JU, Muñoz-Delgado E, López-Durán RM, Gutiérrez-Ruiz MC, Gomez-Quiroz LE, Gómez-Olivares JL. 2023. Changes in the Acetylcholinesterase enzymatic activity in tumor development and progression. Cancers 15 (18): 4629. DOI: 10.3390/cancers15184629.

Pinteus S, Lemos MFL, Alves C, Silva J, Pedrosa R. 2021. The marine invasive seaweeds Asparagopsis armata and Sargassum muticum as targets for greener antifouling solutions. Sci Total Environ 750: 141372. DOI: 10.1016/j.scitotenv.2020.141372.

Puentes C, Carreño K, Santos-Acevedo M, Gómez-León J, García M, Pérez M, Stupak M, Blustein G. 2014. Antifouling paints based on extracts of marine organisms from the Colombian Caribbean. Cienc Tecnol Buq 8 (15): 75-90. DOI: 10.25043/19098642.105.

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

Qiu Q, Gu Y, Ren Y, Ding H, Hu C, Wu D, Mou J, Wu Z, Dai D. 2024. Research progress on eco-friendly natural antifouling agents and their antifouling mechanisms. Chem Eng J 495: 153638. DOI: 10.1016/j.cej.2024.153638.

Quémener M, Kikionis S, Fauchon M, Toueix Y, Aulanier F, Makris AM, Roussis V, Ioannou E, Hellio C. 2021. Antifouling activity of halogenated compounds derived from the red alga Sphaerococcus coronopifolius: Potential for the development of environmentally friendly solutions. Mar Drugs 20 (1): 32. DOI: 10.3390/md20010032.

Rieuwpassa FJ, Tomasoa AM, Palawe JFP, Rieuwpassa F, Mege RA, Balansa W. 2023. A new and practical method for measuring sponge. Jurnal Ilmiah Platax 11: 322-332. DOI: 10.35800/jip.v10i2.47882.

Riyanti, Balansa W, Liu Y et al. 2020b. Selection of sponge-associated bacteria with high potential for the production of antibacterial compounds. Sci Rep 10: 19614. DOI: 10.1038/s41598-020-76256-2.

Riyanti, Marner M, Hartwig C, Patras MA, Wodi SIM, Rieuwpassa FJ, Ijong FG, Balansa W, Schäberle TF. 2020a. Sustainable low-volume analysis of environmental samples by semi-automated prioritization of extracts for natural product research (SeaPEPR). Mar Drugs 18 (12): 649. DOI: 10.3390/md18120649.

Roca C, Requena C, Sebastián-Pérez V, Malhotra S, Radoux C, Pérez C, Martinez A, Páez JA, Blundell TL, Campillo NE. 2018. Identification of new allosteric sites and modulators of AChE through computational and experimental tools. J Enzyme Inhib Med Chem 33 (1): 1034-1047. DOI: 10.1080/14756366.2018.1476502.

Roney M, Mohd Aluwi MFF. 2024. The importance of in-silico studies in drug discovery. Intell Pharm 2 (4): 578-579. DOI: 10.1016/j.ipha.2024.01.010.

Ross JG, Graham BJ, Pitt KA. 2024. Predator-free New Zealand 2050: Techniques for improving ground-based control and monitoring of the Brushtail Possum. Proc Vertebr Pest Conf 31: 1-5.

Selim MS, Shenashen MA, El-Safty SA, Higazy SA, Selim MM, Isago H, Elmarakbi A. 2017. Recent progress in marine foul-release polymeric nanocomposite coatings. Prog Mater Sci 87: 1-32. DOI: 10.1016/j.pmatsci.2017.02.001.

Song S, Muscat-Fenech CDM, Demirel YK. 2021. Economic and environmental impacts of antifouling coatings used on the fishing boats in Turkey. In: 2nd International Conference on Ship and Marine Technology. https://www.gmoshipmar.org/GMOSHIPMAR2021/.

Stowe SD, Richards JJ, Tucker AT, Thompson R, Melander C, Cavanagh J. 2011. Anti-biofilm compounds derived from marine sponges. Mar Drugs 9 (10): 2010-2035. DOI: 10.3390/md9102010.

Sumner LW, Amberg A, Barrett D et al. 2007. Proposed minimum reporting standards for chemical analysis: Chemical Analysis Working Group (CAWG) Metabolomics Standards Initiative (MSI). Metabolomics 3 (3): 211-221. DOI: 10.1007/s11306-007-0082-2.

Sussman JL, Harel M, Frolow F, Oefner C, Goldman A, Toker L, Silman I. 1991. Atomic structure of acetylcholinesterase from Torpedo californica: A prototypic acetylcholine-binding protein. Science 253 (5022): 872-879. DOI: 10.1126/science.1678899.

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

Tintillier F, Moriou C, Petek S, Fauchon M, Hellio C, Saulnier D, Ekins M, Hooper JNA, Al-Mourabit A, Debitus C. 2020. Quorum sensing inhibitory and antifouling activities of new Bromotyrosine metabolites from the Polynesian sponge Pseudoceratina n. sp. Mar Drugs 18 (5): 272. DOI: 10.3390/md18050272.

Van Gestel CA, Otermann K, Canton JH. 1985. Relation between water solubility, cctanol/water partition coefficients, and bioconcentration of organic chemicals in fish: A review. Regul Toxicol Pharmacol 5 (4): 422-431. DOI: 10.1016/0273-2300(85)90007-8.

Vilas-Boas C, Neves AR, Carvalhal F et al. 2021. Multidimensional characterization of a new antifouling xanthone: Structure-activity relationship, environmental compatibility, and immobilization in marine coatings. Ecotoxicol Environ Saf 228: 112970. DOI: 10.1016/j.ecoenv.2021.112970.

Vilas-Boas C, Silva ER, Resende D, Pereira B, Sousa G, Pinto M, Almeida JR, Correia-da-Silva M, Sousa M. 2023. 3,4-Dioxygenated xanthones as antifouling additives for marine coatings: In silico studies, seawater solubility, degradability, leaching, and antifouling performance. Environ Sci Pollut Res Intl 30 (26): 68987-68997. DOI: 10.1007/s11356-023-26899-1.

Wassmann T, Kreis S, Behr M, Buergers R. 2017. The influence of surface texture and wettability on initial bacterial adhesion on titanium and zirconium oxide dental implants. Intl J Implant Dent 3 (1): 32. DOI: 10.1186/s40729-017-0093-3.

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

Yao W-L, Lin JCY, Salamanca E, Pan Y-H, Tsai P-Y, Leu S-J, Yang K-C, Huang H-M, Huang H-Y, Chang W-J. 2020. YSGG laser performance improves biological response on titanium surfaces. Materials 13 (3): 756. DOI: 10.3390/ma13030756.

Yousef ANAA. 2023. Examining the effects of biofouling on ships and how it contributes to the introduction of non-native species in newly discovered coastal areas in biofouling on ship hulls and its ecological ramification. SSRN Electronic J 2024: 1-26. DOI: 10.2139/ssrn.4666557.

Yu P, Wang C, Zhou J, Jiang L, Xue J, Li W. 2016. Influence of surface properties on adhesion forces and attachment of Streptococcus mutans to zirconia in vitro. Biomed Res Intl 2016: 8901253. DOI: 10.1155/2016/8901253.

Zang X, Ni Y, Wang Q, Cheng Y, Huang J, Cao X, Carmalt CJ, Lai Y, Kim DH, Liu Y, Lin Z. 2024. Non-toxic evolution: Advances in multifunctional antifouling coatings. Mater Today 75: 210-243. DOI: 10.1016/j.mattod.2024.03.018.

Zhang J, Liang Y, Wang K-L, Liao X-J, Deng Z, Xu S-H. 2014. Antifouling steroids from the South China Sea gorgonian coral Subergorgia suberosa. Steroids 79: 1-6. DOI: 10.1016/j.steroids.2013.10.007.

Zheng S, Bawazir M, Dhall A, Kim H-E, He L, Heo J, Hwang G. 2021. Implication of surface properties, bacterial motility, and hydrodynamic conditions on bacterial surface sensing and their initial adhesion. Front Bioeng Biotechnol 9: 634722. DOI: 10.3389/fbioe.2021.643722.

Most read articles by the same author(s)