The Sponge-Associated Fungus Eurotium chevalieri MUT 2316 and its Bioactive Molecules: Potential Applications in the Field of Antifouling

  • Elena Bovio
  • Marilyne Fauchon
  • Yannick Toueix
  • Mohamed Mehiri
  • Giovanna Cristina VareseEmail author
  • Claire HellioEmail author
Original Article


The need for new environmentally friendly antifouling and the observation that many marine organisms have developed strategies to keep their surface free of epibionts has stimulated the search for marine natural compounds with antifouling activities. Sponges and in particular fungi associated with them represent one of the most appropriate sources of defence molecules and could represent a promising biomass for the supply of new antifouling compounds. The objective of this work was therefore to evaluate the antifouling potency of 7 compounds isolated from the sponge derived fungus Eurotium chevalieri MUT 2316. The assessment of their activity targeted the inhibition of the adhesion and/or growth of selected marine bacteria (5) and microalgae (5), as well as the inhibition of the mussel’s byssus thread formation (tyrosinase activity). The 7 compounds showed bioactivity, with various levels of selectivity for species. Cyclo-L-Trp-L-Ala was the most promising active compound, and led to the inhibition, at very low concentrations (0.001 μg ml−1 in 61.5% of cases), of adhesion and growth of all the microalgae, of selected bacteria, and towards the inhibition of tyrosinase. Promising results were also obtained for echinulin, neoechinulin A, dihydroauroglaucin and flavoglaucin, respectively, leading to inhibition of adhesion and/or growth of 9, 7, 8 and 8 microfouling species at various concentrations.


Antifouling Bacteria Bioprospection Marine fungi Microalgae Tyrosinase 


Funding Information

This research was supported by the Galileo project [grant number G18-701] and the Vinci project [grant number C2-22] from the Italo-French University. Biodimar team was supported by funding from Biogenouest. M. Mehiri is supported by the EMBRIC project (EU grant No 654008) and the Galileo project from the Italo-French University [grant number 34595SA]. This work was supported by the French government, managed by the French National Research Agency under the project Investissements d’Avenir UCAJEDI (# ANR-15-IDEX-01).


  1. Alzieu C (2000) Environmental impact of TBT: the French experience. Sci Total Environ 258:99–102CrossRefGoogle Scholar
  2. Amara I, Miled W, Slama RB, Ladhari N (2018) Antifouling processes and toxicity effects of antifouling paints on marine environment. A review. Environ Toxicol Pharmacol 57:115–130CrossRefGoogle Scholar
  3. Bao J, Sun YL, Zhang XY, Han Z, Gao HC, He F, Qian PY, Qi SH (2013) Antifouling and antibacterial polyketides from marine gorgonian coral-associated fungus Penicillium sp. SCSGAF 0023. J Antibiot 66:219–223CrossRefGoogle Scholar
  4. Basu S, Ghosh A, Hazra B (2005) Evaluation of the antibacterial activity of Ventilago madraspatana Gaertn., Rubia cordifolia Linn. and Lantana camara Linn.: isolation of emodin and physcion as active antibacterial agents. Phytother Res 19:888–894CrossRefGoogle Scholar
  5. Bayer M, Hellio C, Maréchal JP, Frank W, Lin W, Weber H, Proksch P (2011) Antifouling bastadin congeners target mussel phenoloxidase and complex copper (II) ions. Mar Biotechnol 13:1148–1158CrossRefGoogle Scholar
  6. Bergman J (2013) Synthesis and studies of two marine indole alkaloids, barettin and caulersin. Phytochem Rev 12:487–494CrossRefGoogle Scholar
  7. Bode HB, Bethe B, Höfs R, Zeeck A (2002) Big effects from small changes: possible ways to explore nature’s chemical diversity. Chem Bio Chem 3:619–627CrossRefGoogle Scholar
  8. Bovio E (2019) Marine fungi from sponges: biodiversity, chemodiversity and biotechnological applications. Ph.D. dissertation. Mycotheca Universitatis Taurinensis, University of Turin (Turin), Italy - Institut de Chimie de Nice (ICN), UMR 7272 CNRS, Université Côte d’Azur (Nice), FranceGoogle Scholar
  9. Bovio E, Garzoli L, Poli A, Prigione V, Firsova D, McCormack GP, Varese GC (2018) The culturable mycobiota associated with three Atlantic sponges, including two new species: Thelebolus balaustiformis and T. spongiae. Fungal Syst Evol 1:141–167CrossRefGoogle Scholar
  10. Bovio E, Garzoli L, Poli A, Luganini A, Villa P, Musumeci R, McCormack GP, Cocuzza CE, Gribaudo G, Mehiri M, Varese GC (2019) Marine Fungi from the sponge Grantia compressa: biodiversity, Chemodiversity, and biotechnological potential. Mar Drugs 17:220–242CrossRefGoogle Scholar
  11. Chambers LD, Hellio C, Stokes KR, Dennington SP, Goodes LR, Wood RJK, Walsh FC (2011) Investigation of Chondrus crispus as a potential source of new antifouling agents. Int Biodeterior Biodegrad 65:939–946CrossRefGoogle Scholar
  12. Champ MA (2000) A review of organotin regulatory strategies, pending actions, related costs and benefits. Sci Total Environ 258:21–71CrossRefGoogle Scholar
  13. Chen L, Qian PY (2017) Review on molecular mechanisms of antifouling compounds: an update since 2012. Mar Drugs 15:264–284CrossRefGoogle Scholar
  14. Chen M, Wang KL, Wang CY (2018) Antifouling indole alkaloids of a marine-derived fungus Eurotium sp. Chem Nat Compd 54:207–209CrossRefGoogle Scholar
  15. Cho JY, Kang JY, Hong YK, Baek HH, Shin HW, Kim MS (2012) Isolation and structural determination of the antifouling diketopiperazines from marine-derived Streptomyces praecox 291-11. Biosci Biotechnol Biochem 76:1116–1121CrossRefGoogle Scholar
  16. Cronin ER, Cheshire AC, Clarke SM, Melville AJ (1999) An investigation into the composition, biomass and oxygen budget of the fouling community on a tuna aquaculture farm. Biofouling 13:279–299CrossRefGoogle Scholar
  17. Debbab A, Aly AH, Proksch P (2012) Endophytes and associated marine derived fungi—ecological and chemical perspectives. Fungal Divers 57:45–83CrossRefGoogle Scholar
  18. Duckworth HW, Coleman JE (1970) Physicochemical and kinetic properties of mushroom tyrosinase. J Biol Chem 245:1613–1625Google Scholar
  19. Eckman JE, Thistle D, Burnett WC, Paterson GLJ, Robertson CY, Lambshead PJD (2001) Performance of cages as large animal-exclusion devices in the deep sea. J Mar Res 59:79–95CrossRefGoogle Scholar
  20. Ganihigama DU, Sureram S, Sangher S, Hongmanee P, Aree T, Mahidol C, Ruchirawat S, Kittakoop P (2015) Antimycobacterial activity of natural products and synthetic agents: pyrrolodiquinolines and vermelhotin as anti-tubercular leads against clinical multidrug resistant isolates of Mycobacterium tuberculosis. Eur J Med Chem 89:1–12CrossRefGoogle Scholar
  21. Gao J, Radwan MM, León F, Wang X, Jacob MR, Tekwani BL, Khan SI, Lupien S, Hill RA, Dugan FM, Cutler HG, Cutler SJ (2012) Antimicrobial and antiprotozoal activities of secondary metabolites from the fungus Eurotium repens. Med Chem Res 21:3080–3086CrossRefGoogle Scholar
  22. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239CrossRefGoogle Scholar
  23. Hanssen KØ, Cervin G, Trepos R, Petitbois J, Haug T, Hansen E, Andersen JH, Pavia H, Hellio C, Svenson J (2014) The bromotyrosine derivative ianthelline isolated from the arctic marine sponge Stryphnus fortis inhibits marine micro-and macrobiofouling. Mar Biotechnol 16:684–694CrossRefGoogle Scholar
  24. Hedner E, Sjögren M, Hodzic S, Andersson R, Göransson U, Jonsson PR, Bohlin L (2008) Antifouling activity of a dibrominated cyclopeptide from the marine sponge Geodia barretti. J Nat Prod 71:330–333CrossRefGoogle Scholar
  25. Hellio C, De La Broise D, Dufosse L, Le Gal Y, Bourgougnon N (2001) Inhibition of marine bacteria by extracts of macroalgae: potential use for environmentally friendly antifouling paints. Mar Environ Res 52:231–247CrossRefGoogle Scholar
  26. Hellio C, Trepos R, Aguila-Ramírez RN, Hernández-Guerrero CJ (2015) In: Stengel DB, Connan S (eds) Natural products from marine algae. New York, Humana PressGoogle Scholar
  27. Kang JY, Bangoura I, Cho JY, Joo J, Choi YS, Hwang DS, Hong YK (2016) Antifouling effects of the periostracum on algal spore settlement in the mussel Mytilus edulis. Fish Aquat Sci 19:7–13CrossRefGoogle Scholar
  28. Kelley EW, Norman SG, Scheerer JR (2017) Synthesis of monoalkylidene diketopiperazines and application to the synthesis of barettin. Org Biomol Chem 15:8634–8640CrossRefGoogle Scholar
  29. Le Norcy T, Niemann H, Proksch P, Tait K, Linossier I, Réhel K, Hellio C, Faÿ F (2017) Sponge-inspired dibromohemibastadin prevents and disrupts bacterial biofilms without toxicity. Mar Drugs 15:222–241CrossRefGoogle Scholar
  30. Li X, Dobretsov S, Xu Y, Xiao X, Hung OS, Qian PY (2006) Antifouling diketopiperazines produced by a deep-sea bacterium, Streptomyces fungicidicus. Biofouling 22:187–194CrossRefGoogle Scholar
  31. Li D, Xu Y, Shao CL, Yang RY, Zheng CJ, Chen YY, Fu XM, Qian PJ, She GS, de Voogd NJ, Wang CY (2012) Antibacterial bisabolane-type sesquiterpenoids from the sponge-derived fungus Aspergillus sp. Mar Drugs 10:234–241CrossRefGoogle Scholar
  32. Li YX, Wu HX, Xu Y, Shao CL, Wang CY, Qian PY (2013) Antifouling activity of secondary metabolites isolated from Chinese marine organisms. Mar Biotechnol 15:552–558CrossRefGoogle Scholar
  33. Li Y, Liu L, Liu J, Yang F, Ren N (2014) PPy/AQS (9, 10-anthraquinone-2-sulfonic acid) and PPy/ARS (alizarin Red’s) modified stainless steel mesh as cathode membrane in an integrated MBR/MFC system. Desalination 349:94–101CrossRefGoogle Scholar
  34. Liang TM, Fang YW, Zheng JY, Shao CL (2018) Secondary metabolites isolated from the gorgonian-derived fungus Aspergillus ruber and their antiviral activity. Chem Nat Compd 54:559–561CrossRefGoogle Scholar
  35. Maréchal JP, Hellio C (2009) Challenges for the development of new non-toxic antifouling solutions. Int J Mol Sci 10:4623–4637CrossRefGoogle Scholar
  36. Martins SE, Fillmann G, Lillicrap A, Thomas KV (2018) Ecotoxicity of organic and organo-metallic antifouling co-biocides and implications for environmental hazard and risk assessments in aquatic ecosystems. Biofouling 34:34–52CrossRefGoogle Scholar
  37. Meng LH, Du FY, Li XM, Pedpradab P, Xu GM, Wang BG (2015) Rubrumazines A–C, indolediketopiperazines of the isoechinulin class from Eurotium rubrum MA-150, a fungus obtained from marine mangrove-derived rhizospheric soil. J Nat Prod 78:909–913CrossRefGoogle Scholar
  38. Pereira F, Madureira AM, Sancha S, Mulhovo S, Luo X, Duarte A, Ferreira MJU (2016) Cleistochlamys kirkii chemical constituents: antibacterial activity and synergistic effects against resistant Staphylococcus aureus strains. J Ethnopharmacol 178:180–187CrossRefGoogle Scholar
  39. Phillippi AL, O’Connor NJ, Lewis AF, Kim YK (2001) Surface flocking as a possible anti-biofoulant. Aquaculture 195:225–238CrossRefGoogle Scholar
  40. Pita L, Rix L, Slaby BM, Franke A, Hentschel U (2018) The sponge holobiont in a changing ocean: from microbes to ecosystems. Microbiome 6:46–60CrossRefGoogle Scholar
  41. Qian PY, Chen L, Xu Y (2013) Mini-review: molecular mechanisms of antifouling compounds. Biofouling 29:381–400CrossRefGoogle Scholar
  42. Rodríguez-Marconi S, De la Iglesia R, Díez B, Fonseca CA, Hajdu E, Trefault N (2015) Characterization of bacterial, archaeal and eukaryote symbionts from Antarctic sponges reveals a high diversity at a three-domain level and a particular signature for this ecosystem. PLoS One 10:e0138837–e0138856CrossRefGoogle Scholar
  43. Satheesh S, Ba-akdah MA, Al-Sofyani AA (2016) Natural antifouling compound production by microbes associated with marine macroorganisms: a review. Electron J Biotechnol 19:26–35CrossRefGoogle Scholar
  44. Sun XP, Xu Y, Cao F, Xu RF, Zhang XL, Wang CY (2014) Isoechinulin-type alkaloids from a soft coral-derived fungus Nigrospora oryzae. Chem Nat Compd 50:1153–1155Google Scholar
  45. Suryanarayanan TS (2012) In fungal endosymbionts of seaweeds. In: Se-Kwon K (ed) Biology of marine fungi. Springer, Berlin/HeidelbergGoogle Scholar
  46. Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347CrossRefGoogle Scholar
  47. Thabard M, Gros O, Hellio C, Maréchal JP (2011) Sargassum polyceratium (Phaeophyceae, Fucaceae) surface molecule activity towards fouling organisms and embryonic development of benthic species. Bot Mar 54:147–157CrossRefGoogle Scholar
  48. Tian SZ, Pu X, Luo G, Zhao LX, Xu LH, Li WJ, Luo Y (2013) Isolation and characterization of new p-terphenyls with antifungal, antibacterial, and antioxidant activities from halophilic actinomycete Nocardiopsis gilva YIM 90087. J Agric Food Chem 61:3006–3012CrossRefGoogle Scholar
  49. Travers MA, Tourbiez D, Parizadeh L, Haffner P, Kozic-Djellouli A, Aboubaker M, Koken M, Dégremont L, Lupo C (2017) Several strains, one disease: experimental investigation of Vibrio aestuarianus infection parameters in the Pacific oyster, Crassostrea gigas. Vet Res 48:32–40CrossRefGoogle Scholar
  50. Trepos R, Cervin G, Hellio C, Pavia H, Stensen W, Stensvåg K, Svendsen JS, Huag T, Svenson J (2014) Antifouling compounds from the sub-arctic ascidian Synoicum pulmonaria: Synoxazolidinones A and C, pulmonarins A and B, and synthetic analogues. J Nat Prod 77:2105–2113CrossRefGoogle Scholar
  51. Trepos R, Cervin G, Pile C, Pavia H, Hellio C, Svenson J (2015) Evaluation of cationic micropeptides derived from the innate immune system as inhibitors of marine biofouling. Biofouling 31:393–403CrossRefGoogle Scholar
  52. Tsukamoto S, Kato H, Hirota H, Fusetani N (1997) Antifouling terpenes and steroids against barnacle larvae from marine sponges. Biofouling 11:283–291CrossRefGoogle Scholar
  53. Wang CY, Wang KL, Qian PY, Xu Y, Chen M, Zheng JJ, Liu M, Shao CL, Wang CY (2016) Antifouling phenyl ethers and other compounds from the invertebrates and their symbiotic fungi collected from the South China Sea. AMB Express 6:102–112CrossRefGoogle Scholar
  54. Wang KL, Wu ZH, Wang Y, Wang CY, Xu Y (2017) Mini-review: antifouling natural products from marine microorganisms and their synthetic analogs. Mar Drugs 15:266–287CrossRefGoogle Scholar
  55. Xu L, Zhang GQ, Yuan GE, Liu HY, Liu JD, Yang FL (2015) Anti-fouling performance and mechanism of anthraquinone/polypyrrole composite modified membrane cathode in a novel MFC–aerobic MBR coupled system. RSC Adv 5:22533–22543CrossRefGoogle Scholar
  56. Yang LH, Miao L, Lee OO, Li X, Xiong H, Pang KL, Vrijmoed L, Qian PY (2007) Effect of culture conditions on antifouling compound production of a sponge-associated fungus. Appl Microbiol Biotechnol 74:1221–1231CrossRefGoogle Scholar
  57. Yang B, Huang J, Lin XP, Zhang Y, Tao H, Liu YH (2016) A new Diketopiperazine from the marine sponge Callyspongia species. Rec Nat Prod 10:117–121Google Scholar
  58. Yebra DM, Kiil S, Dam-johansen K (2004) Antifouling technology—past, present and future steps towards efficient and environmentally friendly antifouling coatings. Prog Org Coat 50:75–104CrossRefGoogle Scholar
  59. Zhao D, Cao F, Guo XJ, Zhang YR, Kang Z, Zhu HJ (2018) Antibacterial indole alkaloids and anthraquinones from a sewage-derived fungus Eurotium sp. Chem Nat Compd 54:399–401CrossRefGoogle Scholar
  60. Zhou Y, Debbab A, Wray V, Lin W, Schulz B, Trepos R, Pile C, Hellio C, Proksch P, Aly AH (2014) Marine bacterial inhibitors from the sponge-derived fungus Aspergillus sp. Tetrahedron Lett 55:2789–2792CrossRefGoogle Scholar
  61. Zin WWM, Buttachon S, Dethoup T, Pereira JA, Gales L, Inacio A, Costa PM, Lee M, Sekeroglu N, Silva AMS, Pinto MM, Kijjoa A (2017) Antibacterial and antibiofilm activities of the metabolites isolated from the culture of the mangrove-derived endophytic fungus Eurotium chevalieri KUFA 06. Phytochemistry 141:86–97CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Elena Bovio
    • 1
    • 2
  • Marilyne Fauchon
    • 3
  • Yannick Toueix
    • 3
  • Mohamed Mehiri
    • 2
  • Giovanna Cristina Varese
    • 1
    Email author
  • Claire Hellio
    • 3
    Email author
  1. 1.Mycotheca Universitatis Taurinensis, Department of Life Sciences and Systems BiologyUniversity of TurinTurinItaly
  2. 2.CNRS, Nice Institute of Chemistry, UMR 7272, Marine Natural Products TeamUniversity Nice Côte d’AzurNiceFrance
  3. 3.University Brest, CNRS, IRD, Ifremer, LEMARInstitut Universitaire Européen de la MerPlouzanéFrance

Personalised recommendations