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Settlement inhibition of marine biofilm bacteria and barnacle larvae by compounds isolated from the Mediterranean brown alga Taonia atomaria

Abstract

The antifouling (AF) properties of phytochemicals isolated from the Mediterranean brown seaweed Taonia atomaria have been assayed against several colonizing organisms. Eight compounds were isolated and their chemical structures characterized by spectroscopic techniques (NMR, MS) and comparison with literature data. The phytochemical composition of the extracts of T. atomaria was found to be mainly attributable to sesquiterpenes. Accordingly, a new germacrane, germacra-4(15),5,10(14)-trien-9-ol (1), is described together with five other sesquiterpenoids (-)-gleenol (2); α-cadinol methyl ether (3), (-)-trans-calamenene (4), (1S, 5E, 7S) 1-acetoxygermacra-4(15),5,10(14)-triene (5), and 4-peroxymuurol-5-ene (6). Moreover, two lipidic compounds, a polyunsaturated fatty acid, (5Z, 8Z, 11Z, 14Z, 17Z)-eicosa-5,8,11,14,17-pentaenoic acid (7), and a glycerol derivative, sn-3-O-(geranylgeranyl)glycerol (8), were also isolated. The known compounds 3, 67 are described here for the first time from this alga. In comparison with commercial antifoulants [tributyltin oxide (TBTO), zineb, and copper pyrithione (CuPT)], compounds 1, 2, 4, 6, and 8 were evaluated for their toxicity and capacity to inhibit the settlement of five bacteria isolated from marine biofilms. Toxicity and anti-settlement activity of 1, 2, and 6 were also assessed against two barnacle species (Amphibalanus amphitrite and Balanus perforatus). Regarding bacteria, a significant anti-adhesion effect was recorded for 8 (EC50 between 25 and 50 μM) with moderate associated toxicity. Considering the settlement inhibition of barnacle cyprids, (-)-gleenol (2) exhibited a strong AF efficacy (EC50 < 5 μM) with moderate toxicity. In addition, as B. perforatus showed similar responses to the reference A. amphitrite with all compounds, this species may be proposed as an alternative model for anti-macrofouling assessment, especially in temperate areas. Overall, these results suggest that a number of the tested compounds could, alone or in combination, play a critical role in limiting the fouling at the T. atomaria surface.

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References

  1. Abatis D, Vagias C, Galanakis D, Norris JN, Moreau D, Roussakis C, Roussis V (2005) Atomarianones A and B: two cytotoxic meroditerpenes from the brown alga Taonia atomaria. Tetrahedron Lett 46:8525–8529

    CAS  Article  Google Scholar 

  2. Amico V, Oriente G, Piattelli M, Tringali C, Fattorusso E, Magno S, Mayol L (1979) Sesquiterpenes based on the cadalane skeleton from the brown alga Dilophus fasciola. Experientia 35:450–451

    CAS  Article  Google Scholar 

  3. Areche C, San-Martín A, Rovirosa J, Soto-Delgado J, Contreras R (2009) An unusual halogenated meroditerpenoid from Stypopodium flabelliforme: Studies by NMR spectroscopic and computational methods. Phytochemistry 72:1315–1320

    Article  Google Scholar 

  4. Blay G, Collado AM, García B, Pedro JR (2005) Silicon guided rearrangement of epoxydecalines to spirocyclic compounds. Synthesis of gleenol and axenol from carvone. Tetrahedron 61:10853–10860

    CAS  Article  Google Scholar 

  5. Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR (2014) Marine natural products. Nat Prod Rep 31:160–258, and previous reports in the series

    CAS  Article  PubMed  Google Scholar 

  6. Briand J-F (2009) Marine antifouling laboratory bioassays: an overview of their diversity. Biofouling 25:297–311

    CAS  Article  PubMed  Google Scholar 

  7. Brian-Jaisson F, Ortalo-Magné A, Guentas-Dombrowsky L, Armougom F, Blache Y, Molmeret M (2014) Identification of bacterial strains isolated from the Mediterranean sea exhibiting different abilities of biofilm formation. Microb Ecol 68:94–110

    Article  PubMed  Google Scholar 

  8. Camps M, Briand J-F, Guentas-Dombrowsky L, Culioli G, Bazire A, Blache Y (2011) Antifouling activity of commercial biocides vs. natural and natural-derived products assessed by marine bacteria adhesion bioassay. Mar Pollut Bull 62:1032–1040

    CAS  Article  PubMed  Google Scholar 

  9. Chakraborty K, Lipton AP, Paul Raj R, Vijayan KK (2010) Antibacterial labdane diterpenoids of Ulva fasciata Delile from southwestern coast of the Indian Peninsula. Food Chem 119:1399–1408

    CAS  Article  Google Scholar 

  10. Changyun W, Haiyan L, Changlun S, Yanan W, Liang L, Huashi G (2008) Chemical defensive substances of soft corals and gorgonians. Acta Ecol Sin 28:2320–2328

    Article  Google Scholar 

  11. Clare AS, Aldred N (2009) Surface colonisation by marine organisms and its impact on antifouling research. IN Hellio C, Yebra D (eds) Advances in Marine Antifouling Coatings and Technologies. Woodhead Publishing. Pp 46-79

  12. Clare AS, Rittschof D, Gerhart DJ, Hooper GJ, Bonaventura J (1999) Antisettlement and narcotic action of analogues of diterpene marine natural product antifoulants from octocorals. Mar Biotechnol 1:427–436

    CAS  Article  PubMed  Google Scholar 

  13. Costlow JD Jr, Bookhout CG (1958) Larval development of Balanus amphitrite var. denticulata Broch reared in the laboratory. Biol Bull 114:284–295

    Article  Google Scholar 

  14. da Gama BAP, Plouguerné E, Pereira RC (2014) The antifouling defence mechanisms of marine macroalgae. Adv Bot Res 71:413–440

    Article  Google Scholar 

  15. Dafforn KA, Lewis JA, Johnston EL (2011) Antifouling strategies: History and regulation, ecological impacts and mitigation. Mar Pollut Bull 62:453–465

    CAS  Article  PubMed  Google Scholar 

  16. De Nys R, Dworjanyn SA, Steinberg PD (1998) A new method for determining surface concentrations of marine natural products on seaweeds. Mar Ecol Prog Ser 162:79–87

    Article  Google Scholar 

  17. de Paula JC, Vallim MA, Teixeira VL (2011) What are and where are the bioactive terpenoids metabolites from Dictyotaceae (Phaeophyceae). Rev Bras Farmacogn 21:216–228

    Article  Google Scholar 

  18. De Rosa S, De Giulio A, Iodice C, Zavodink N (1994) Sesquiterpenes from the brown alga Taonia atomaria. Phytochemistry 37:1327–1330

    Article  Google Scholar 

  19. Dobretsov S, Abed RMM, Teplitski M (2013) Mini-review: Inhibition of biofouling by marine microorganisms. Biofouling 29:423–441

    CAS  Article  PubMed  Google Scholar 

  20. Dupré S, Grenz M, Jakupovic J, Bohlmann F, Niemeyer HM (1991) Eremophilane, germacrane and shikimic acid derivatives from chilean Senecio species. Phytochemistry 30:1211–1220

    Article  Google Scholar 

  21. Egan S, Harder T, Burke C, Steinberg P, Kjelleberg S, Thomas T (2013) The seaweed holobiont: understanding seaweed–bacteria interactions. FEMS Microbiol Rev 37:462–476

    CAS  Article  PubMed  Google Scholar 

  22. El Hattab M, Bouzidi N, Ortalo-Magné A, Daghbouche Y, Richou M, Chitour SE, de Reviers B, Piovetti L (2009) Eicosapentaenoic acid: Possible precursor of the phloroglucinol derivatives isolated from the brown alga Zonaria tournefortii (J.V. Lamouroux) Montagne. Biochem Syst Ecol 37:55–58

    Article  Google Scholar 

  23. Faimali M, Sepcic K, Turk T, Geraci S (2003) Non-toxic antifouling activity of polymeric 3-alkylpyridinium salts from the Mediterranean sponge Reniera sarai (Pulitzer-Finali). Biofouling 19:47–56

    CAS  Article  PubMed  Google Scholar 

  24. Fattorusso E, Magno S, Mayol L, Amico V, Oriente G, Piattelli M, Tringali C (1978) Isolation of (2S,8R)-germacra-1(11),5(12), E6-trien-2-ol acetate from the brown alga Dilophus fasciola. Tetrahedron Lett 19:4149–4152

    Article  Google Scholar 

  25. Fusetani N (2004) Biofouling and antifouling. Nat Prod Rep 21:94–104

    CAS  Article  PubMed  Google Scholar 

  26. Fusetani N (2011) Antifouling marine natural products. Nat Prod Rep 28:400–410

    CAS  Article  PubMed  Google Scholar 

  27. Gonzalez AG, Darias J, Martin JD (1971) Taondiol, a new component from Taonia atomaria. Tetrahedron Lett 12:2729–2732

    Article  Google Scholar 

  28. Gonzalez AG, Darias J, Martin JD, Pascual C (1973) Marine natural products of the atlantic zone.V.The structure and chemistry of taondiol and related compounds. Tetrahedron 29:1605–1609

    CAS  Article  Google Scholar 

  29. Gonzalez AG, Darias J, Martin JD, Norte M (1974) Atomaric acid, a new component from Taonia atomaria. Tetrahedron Lett 15:3951–3954

    Article  Google Scholar 

  30. Grasland B, Mitalane J, Briandet R, Quémener E, Meylheuc T, Linossier I, Vallée-Réhel K, Haras D (2003) Bacterial biofilm in seawater: cell surface properties of early-attached marine bacteria. Biofouling 19:307–313

    CAS  Article  PubMed  Google Scholar 

  31. Guiry MD, Guiry GM (2014) AlgaeBase. World-wide electronic publication. National University of Ireland, Galway

  32. Hanssen K, Cervin G, Trepos R, Petitbois J, Haug T, Hansen E, Andersen J, 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 16:684–694

    CAS  Article  PubMed  Google Scholar 

  33. Harder T, Campbell A, Egan S, Steinberg P (2012) Chemical mediation of ternary interactions between marine holobionts and their environment as exemplified by the red alga Delisea pulchra. J Chem Ecol 38:442–450

    CAS  Article  PubMed  Google Scholar 

  34. Hiraga Y, Taino K, Kurokawa M, Takagi R, Ohkata K (1997) (−)-Loliolide and other germination inhibitory active constituents in Equisetum arvense. Nat Prod Lett 10:181–186

    CAS  Article  Google Scholar 

  35. Hirota H, Tomono Y, Fusetani N (1996) Terpenoids with antifouling activity against barnacle larvae from the marine sponge Acanthella cavernosa. Tetrahedron 52:2359–2368

    CAS  Article  Google Scholar 

  36. Konstantinou IK, Albanis TA (2004) Worldwide occurrence and effects of antifouling paint booster biocides in the aquatic environment: a review. Environ Internat 30:235–248

    CAS  Article  Google Scholar 

  37. Lachnit T, Wahl M, Harder T (2010) Isolated thallus-associated compounds from the macroalga Fucus vesiculosus mediate bacterial surface colonization in the field similar to that on the natural alga. Biofouling 26:247–255

    CAS  Article  PubMed  Google Scholar 

  38. Lachnit T, Fischer M, Künzel S, Baines JF, Harder T (2013) Compounds associated with algal surfaces mediate epiphytic colonization of the marine macroalga Fucus vesiculosus. FEMS Microbiol Ecol 84:411–420

    CAS  Article  PubMed  Google Scholar 

  39. Lankadurai B, Wolfe D, Whitfield Åslund M, Simpson A, Simpson M (2013) 1H NMR-based metabolomic analysis of polar and non-polar earthworm metabolites after sub-lethal exposure to phenanthrene. Metabolomics 9:44–56

    CAS  Article  Google Scholar 

  40. Leroy C, Delbarre-Ladrat C, Ghillebaert F, Rochet MJ, Compère C, Combes D (2007) A marine bacterial adhesion microplate test using the DAPI fluorescent dye: a new method to screen antifouling agents. Lett Appl Microbiol 44:372–378

    CAS  Article  PubMed  Google Scholar 

  41. Manzo S, Schiavo S, Aleksi P, Tabaku A (2014) Application of a toxicity test battery integrated index for a first screening of the ecotoxicological threat posed by ports and harbors in the southern Adriatic Sea (Italy). Environ Monit Assess 186:7127–7139

    CAS  Article  PubMed  Google Scholar 

  42. Maréchal J-P, Hellio C (2011) Antifouling activity against barnacle cypris larvae: Do target species matter (Amphibalanus amphitrite versus Semibalanus balanoides)? Int Biodeter Biodegr 65:92–101

    Article  Google Scholar 

  43. Maximilien R, de Nys R, Holmström C, Gram L, Givskov M, Crass K, Kjelleberg S, Steinberg PD (1998) Chemical mediation of bacterial surface colonisation by secondary metabolites from the red alga Delisea pulchra. Aquat Microb Ecol 15:233–246

    Article  Google Scholar 

  44. Mokrini R, Mesaoud MB, Daoudi M, Hellio C, Maréchal J-P, El Hattab M, Ortalo-Magné A, Piovetti L, Culioli G (2008) Meroditerpenoids and derivatives from the brown alga Cystoseira baccata and their antifouling properties. J Nat Prod 71:1806–1811

    CAS  Article  PubMed  Google Scholar 

  45. Nagashima F, Asakawa Y (2001) Sesqui- and diterpenoids from two Japanese and three European liverworts. Phytochemistry 56:347–352

    CAS  Article  PubMed  Google Scholar 

  46. Nagashima F, Toyota M, Asakawa Y (1990) Terpenoids from some Japanese liverworts. Phytochemistry 29:2169–2174

    CAS  Article  Google Scholar 

  47. Nakashima K, Imoto M, Sono M, Tori M, Nagashima F, Asakawa Y (2002) Total synthesis of (-)-(7S,10R)-calamenene and (-)-(7S,10R)-2-hydroxycalamenene by use of a ring-closing metathesis reaction. A comparison of the cis- and trans-isomers. Molecules 7:517–527

    CAS  Article  Google Scholar 

  48. Nakazaki A, Era T, Kobayashi S (2007) Total synthesis of (±)-gleenol and (±)-axenol via a functionalized spiro[4.5]decane. Chem Pharm Bull 55:1606–1609

    CAS  Article  PubMed  Google Scholar 

  49. Nogata Y, Yoshimura E, Shinshima K, Kitano Y, Sakaguchi I (2003) Antifouling substances against larvae of the barnacle Balanus amphitrite from the marine sponge, Acanthella cavernosa. Biofouling 19:193–196

    CAS  Article  PubMed  Google Scholar 

  50. Norms E, Crisp DJ (1953) The distribution and planktonic stages of the cirripede Balanus perforatus Bruguière. Proc Zool Soc Lond 123:393–409

    Article  Google Scholar 

  51. Nylund GM, Gribben PE, De Nys R, Steinberg PD, Pavia H (2007) Surface chemistry versus whole-cell extracts: antifouling tests with seaweed metabolites. Mar Ecol Prog Ser 329:73–84

    Article  Google Scholar 

  52. Nylund GM, Persson F, Lindegarth M, Cervin G, Hermansson M, Pavia H (2010) The red alga Bonnemaisonia asparagoides regulates epiphytic bacterial abundance and community composition by chemical defence. FEMS Microbiol Ecol 71:84–93

    CAS  Article  PubMed  Google Scholar 

  53. Nylund GM, Weinberger F, Rempt M, Pohnert G (2011) Metabolomic assessment of induced and activated chemical defence in the invasive red alga Gracilaria vermiculophylla. PLoS One 6, e29359

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. Okino T, Yoshimura E, Hirota H, Fusetani N (1996) New antifouling kalihipyrans from the marine sponge Acanthella cavernosa. J Nat Prod 59:1081–1083

    CAS  Article  Google Scholar 

  55. Okunade AL, Wiemer DF (1985) (-)-Loliolide, an ant-repellent compound from Xanthoxyllum setulosum. J Nat Prod 48:472–473

    CAS  Article  Google Scholar 

  56. Othmani A, Bouzidi N, Viano Y, Alliche Z, Seridi H, Blache Y, El Hattab M, Briand J-F, Culioli G (2014) Anti-microfouling properties of compounds isolated from several Mediterranean Dictyota spp. J Appl Phycol 26:1573–1584

    CAS  Google Scholar 

  57. Percot A, Yalçin A, Aysel V, Erdugan H, Dural B, Güven KC (2009) Loliolide in marine algae. Nat Prod Res 23:460–465

    CAS  Article  PubMed  Google Scholar 

  58. Persson F, Svensson R, Nylund GM, Fredriksson NJ, Pavia H, Hermansson M (2011) Ecological role of a seaweed secondary metabolite for a colonizing bacterial community. Biofouling 27:579–588

    CAS  Article  PubMed  Google Scholar 

  59. Piazza V, Roussis V, Garaventa F, Greco G, Smyrniotopoulos V, Vagias C, Faimali M (2011) Terpenes from the red alga Sphaerococcus coronopifolius inhibit the settlement of barnacles. Mar Biotechnol 13:764–772

    CAS  Article  PubMed  Google Scholar 

  60. Piazza V, Dragić I, Sepčić K, Faimali M, Garaventa F, Turk T, Berne S (2014) Antifouling activity of synthetic alkylpyridinium polymers using the barnacle model. Mar Drugs 12:1959–1976

    Article  PubMed  PubMed Central  Google Scholar 

  61. Puglisi MP, Sneed JM, Sharp KH, Ritson-Williams R, Paul VJ (2014) Marine chemical ecology in benthic environments. Nat Prod Rep 31:1510–1553

    CAS  Article  PubMed  Google Scholar 

  62. Qian P-Y, Xu Y, Fusetani N (2010) Natural products as antifouling compounds: recent progress and future perspectives. Biofouling 26:223–234

    CAS  Article  PubMed  Google Scholar 

  63. Qian P-Y, Chen L, Xu Y (2013) Mini-review: molecular mechanisms of antifouling compounds. Biofouling 29:381–400

    CAS  Article  PubMed  Google Scholar 

  64. Qiu J-W, Thiyagarajan V, Cheung S, Qian P-Y (2005) Toxic effects of copper on larval development of the barnacle Balanus amphitrite. Mar Pollut Bull 51:688–693

    CAS  Article  PubMed  Google Scholar 

  65. Qiu J-W, Hung OS, Qian P-Y (2008) An improved barnacle attachment inhibition assay. Biofouling 24:259–266

    CAS  Article  PubMed  Google Scholar 

  66. Rittschof D, Clare AS, Gerhart DJ, Mary SA, Bonaventura J (1992) Barnacle in vitro assays for biologically active substances: toxicity and settlement inhibition assays using mass cultured Balanus amphitrite amphitrite Darwin. Biofouling 6:115–122

    CAS  Article  Google Scholar 

  67. Rohde S, Wahl M (2008) Antifeeding defense in baltic macroalgae: induction by direct grazing versus waterborne cues. J Phycol 44:85–90

    Article  PubMed  Google Scholar 

  68. Romano JA, Rittschof D, McClellan-Green PD, Holm ER (2010) Variation in toxicity of copper pyrithione among populations and families of the barnacle, Balanus amphitrite. Biofouling 26:341–347

    Article  PubMed  Google Scholar 

  69. Saha M, Wahl M (2013) Seasonal variation in the antifouling defence of the temperate brown alga Fucus vesiculosus. Biofouling 29:661–668

    CAS  Article  PubMed  Google Scholar 

  70. Saha M, Rempt M, Grosser K, Pohnert G, Weinberger F (2011) Surface-associated fucoxanthin mediates settlement of bacterial epiphytes on the rockweed Fucus vesiculosus. Biofouling 27:423–433

    CAS  Article  PubMed  Google Scholar 

  71. Saha M, Rempt M, Gebser B, Grueneberg J, Pohnert G, Weinberger F (2012) Dimethylsulphopropionate (DMSP) and proline from the surface of the brown alga Fucus vesiculosus inhibit bacterial attachment. Biofouling 28:593–604

    CAS  Article  PubMed  Google Scholar 

  72. Saha M, Rempt M, Stratil SB, Wahl M, Pohnert G, Weinberger F (2014) Defence chemistry modulation by light and temperature shifts and the resulting effects on associated epibacteria of Fucus vesiculosus. PLoS One 9, e105333

    Article  PubMed  PubMed Central  Google Scholar 

  73. Salta M, Wharton JA, Stoodley P, Dennington SP, Goodes LR, Werwinski S, Mart U, Wood RJK, Stokes KR (2010) Designing biomimetic antifouling surfaces. Phil Trans Roy Soc A 368:4729–4754

    CAS  Article  Google Scholar 

  74. Scardino AJ, de Nys R (2010) Mini review: Biomimetic models and bioinspired surfaces for fouling control. Biofouling 27:73–86

    Article  Google Scholar 

  75. Sera Y, Adachi K, Nishida F, Shizuri Y (1999) A new sesquiterpene as an antifouling substance from a Palauan marine sponge, Dysidea herbacea. J Nat Prod 62:395–396

    CAS  Article  PubMed  Google Scholar 

  76. Shaker KH, Müller M, Ghani MA, Dahse H-M, Seifert K (2010) Terpenes from the soft corals Litophyton arboreum and Sarcophyton ehrenbergi. Chem Biodivers 7:2007–2015

    CAS  Article  PubMed  Google Scholar 

  77. Sneed JM, Pohnert G (2011) The green alga Dicytosphaeria ocellata and its organic extracts alter natural bacterial biofilm communities. Biofouling 27:347–356

    CAS  Article  PubMed  Google Scholar 

  78. Sudatti DB, Rodrigues SV, Coutinho R, da Gama BAP, Salgado LT, Filho GMA, Pereira RC (2008) Transport and defensive role of elatol at the surface of the red seaweed Laurencia obtusa (Ceramiales, Rhodophyta). J Phycol 44:584–591

    Article  PubMed  Google Scholar 

  79. Taylor HF, Burden RS (1970) Identification of plant growth inhibitors produced by photolysis of violaxanthin. Phytochemistry 9:2217–2223

    CAS  Article  Google Scholar 

  80. Thomas KV, Brooks S (2010) The environmental fate and effects of antifouling paint biocides. Biofouling 26:73–88

    CAS  Article  PubMed  Google Scholar 

  81. Tringali C, Piattelli M, Spatafora C (1995) Sesquiterpenes and geranylgeranylglycerol from the brown algae Taonia lacheana and Taonia atomaria f. ciliata : Their chemotaxonomic significance. Phytochemistry 40:827–831

    CAS  Article  Google Scholar 

  82. Tziveleka L-A, Abatis D, Paulus K, Bauer R, Vagias C, Roussis V (2005) Marine polyprenylated hydroquinones, quinones, and chromenols with inhibitory effects on leukotriene formation. Chem Biodivers 2:901–909

    CAS  Article  PubMed  Google Scholar 

  83. Vairappan CS, Suzuki M, Ishii T, Okino T, Abe T, Masuda M (2008) Antibacterial activity of halogenated sesquiterpenes from Malaysian Laurencia spp. Phytochemistry 69:2490–2494

    CAS  Article  PubMed  Google Scholar 

  84. Vairappan C, Anangdan S, Tan K, Matsunaga S (2010) Role of secondary metabolites as defense chemicals against ice-ice disease bacteria in biofouler at carrageenophyte farms. J Appl Phycol 22:305–311

    CAS  Article  Google Scholar 

  85. Viano Y, Bonhomme D, Camps M, Briand J-F, Ortalo-Magné A, Blache Y, Piovetti L, Culioli G (2009) Diterpenoids from the mediterranean brown alga Dictyota sp. evaluated as antifouling substances against a marine bacterial biofilm. J Nat Prod 72:1299–1304

    CAS  Article  PubMed  Google Scholar 

  86. Xu Y, He H, Schultz S, Liu X, Fusetani N, Xiong H, Xiao X, Qian P-Y (2010) Potent antifouling compounds produced by marine Streptomyces. Bioresource Technol 101:1331–1336

    CAS  Article  Google Scholar 

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Acknowledgments

This work was financially supported by the Ministry of Higher Education and Scientific Research of Tunisia (A.O. PhD grant). Special thanks are given to Pr. O. De Clerck (Ghent University) for taxonomic identification of the algal material, and to C. Compère (IFREMER, Brest, France) and D. Haras (LBCM, Université de Bretagne Sud, France) for the supply of the D41 and 4M6 strains, respectively. The authors also would like to thank P. Aublanc, D. Kirchhofer, and T. Miard (Institut Océanographique Paul Ricard, France) for technical assistance.

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Othmani, A., Bunet, R., Bonnefont, JL. et al. Settlement inhibition of marine biofilm bacteria and barnacle larvae by compounds isolated from the Mediterranean brown alga Taonia atomaria . J Appl Phycol 28, 1975–1986 (2016). https://doi.org/10.1007/s10811-015-0668-4

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Keywords

  • Antifouling
  • Algal metabolite
  • Biofilm-forming bacteria
  • Anti-adhesion
  • Toxicity
  • Barnacles