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Marine Biotechnology

, Volume 16, Issue 6, pp 684–694 | Cite as

The Bromotyrosine Derivative Ianthelline Isolated from the Arctic Marine Sponge Stryphnus fortis Inhibits Marine Micro- and Macrobiofouling

  • Kine Ø. Hanssen
  • Gunnar Cervin
  • Rozenn Trepos
  • Julie Petitbois
  • Tor Haug
  • Espen Hansen
  • Jeanette H. Andersen
  • Henrik Pavia
  • Claire Hellio
  • Johan SvensonEmail author
Original Article

Abstract

The inhibition of marine biofouling by the bromotyrosine derivative ianthelline, isolated from the Arctic marine sponge Stryphnus fortis, is described. All major stages of the fouling process are investigated. The effect of ianthelline on adhesion and growth of marine bacteria and microalgae is tested to investigate its influence on the initial microfouling process comparing with the known marine antifoulant barettin as a reference. Macrofouling is studied via barnacle (Balanus improvisus) settlement assays and blue mussel (Mytilus edulis) phenoloxidase inhibition. Ianthelline is shown to inhibit both marine micro- and macrofoulers with a pronounced effect on marine bacteria (minimum inhibitory concentration (MIC) values 0.1–10 μg/mL) and barnacle larval settlement (IC50 = 3.0 μg/mL). Moderate effects are recorded on M. edulis (IC50 = 45.2 μg/mL) and microalgae, where growth is more affected than surface adhesion. The effect of ianthelline is also investigated against human pathogenic bacteria. Ianthelline displayed low micromolar MIC values against several bacterial strains, both Gram positive and Gram negative, down to 2.5 μg/mL. In summary, the effect of ianthelline on 20 different representative marine antifouling organisms and seven human pathogenic bacterial strains is presented.

Keywords

Antifouling Bromotyrosine Ianthelline Marine natural product Sponge metabolite 

Notes

Acknowledgments

Marte Albrigtsen is acknowledged for performing the terrestrial bacterial screen, and Robert Andre Johansen is acknowledged for providing the photograph of S. fortis. The authors are further grateful to Dr. Lindon Moodie (UiT) for linguistic support and to Runar Gjerp Solstad (UiT) for purifying a sample of barettin. The study was performed at MabCent which is a centre for research-based innovation at the UiT and supported by the Research Council of Norway, Grant no 174885/130. HP and GC were supported by the Centre for Marine Chemical Ecology at the University of Gothenburg.

References

  1. Almeida E, Diamantino TC, De Sousa O (2007) Marine paints: the particular case of antifouling paints. Prog Org Coat 59:2–20CrossRefGoogle Scholar
  2. Barnes H, Barnes M (1962) The distribution and general ecology of Balanus balanoides together with some observations on Balanus improvisus in the waters around the coasts of Denmark, southern Sweden and north-east Germany. Acta Uni Lund 58:1–41Google Scholar
  3. Bayer M, Hellio C, Marechal JP, Frank W, Lin WH, Weber H, Proksch P (2011) Antifouling bastadin congeners target mussel phenoloxidase and complex copper(ii) ions. Mar Biotechnol 13:1148–1158CrossRefPubMedGoogle Scholar
  4. Beech WB, Sunner J (2004) Biocorrosion: towards understanding interactions between biofilms and metals. Curr Opin Biotechnol 15:181–186CrossRefPubMedGoogle Scholar
  5. Beech IB, Sunner JA, Hiraoka K (2005) Microbe-surface interactions in biofouling and biocorrosion processes. Int Microbiol 8:157–168PubMedGoogle Scholar
  6. Berntsson KM, Jonsson PR, Lejhall M, Gatenholm P (2000) Analysis of behavioural rejection of micro-textured surfaces and implications for recruitment by the barnacle Balanus improvisus. J Exp Mar Biol Ecol 251:59–83CrossRefPubMedGoogle Scholar
  7. Bhadury P, Wright PC (2004) Exploitation of marine algae: biogenic compounds for potential antifouling applications. Planta 219:561–578CrossRefPubMedGoogle Scholar
  8. Bressy C, Hellio C, Marechal JP, Tanguy B, Margaillan A (2010) Bioassays and field immersion tests: a comparison of the antifouling activity of copper-free poly(methacrylic)-based coatings containing tertiary amines and ammonium salt groups. Biofouling 26:769–777CrossRefPubMedGoogle Scholar
  9. Briand JF (2009) Marine antifouling laboratory bioassays: an overview of their diversity. Biofouling 25:297–311CrossRefPubMedGoogle Scholar
  10. Chambers LD, Stokes KR, Walsh FC, Wood RJK (2006) Modern approaches to marine antifouling coatings. Surf Coat Technol 201:3642–3652CrossRefGoogle 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. Cheng S, Tian JT, Chen SG, Lei YH, Chang XT, Liu T, Yin YS (2009) Microbially influenced corrosion of stainless steel by marine bacterium Vibrio natriegens: (i) corrosion behavior. Math Sci Eng C-Biol 29:751–755CrossRefGoogle Scholar
  13. Ciminiello P, Fattorusso E, Magno S, Pansini M (1995) Chemistry of Verongida sponges. 4. Comparison of the secondary metabolite composition of several specimens of Pseudoceratina crassa. J Nat Prod 58:689–696CrossRefGoogle Scholar
  14. Dahms HU, Hellio C (2009) Laboratory bio-assays for screening marine antifouling compounds. In: Hellio C, Yebra DM (eds) Advances in marine antifouling coatings and technologies. Woodhead Publishing, New YorkGoogle Scholar
  15. De Decker S, Normand J, Saulnier D, Pernet F, Castagnet S, Boudry P (2011) Responses of diploid and triploid pacific oysters Crassostrea gigas to vibrio infection in relation to their reproductive status. J Invertebr Pathol 106:179–191CrossRefPubMedGoogle Scholar
  16. De Nys R, Steinberg PD (2002) Linking marine biology and biotechnology. Curr Opin Biotechnol 13:244–248CrossRefPubMedGoogle Scholar
  17. Dobretsov S, Dahms HU, Qian PY (2006) Inhibition of biofouling by marine microorganisms and their metabolites. Biofouling 22:43–54CrossRefPubMedGoogle Scholar
  18. Ellis DV, Pattisina LA (1990) Widespread neogastropod imposex—a biological indicator of global TBT contamination. Mar Pollut Bull 21:248–253CrossRefGoogle Scholar
  19. Fitridge I, Dempster T, Guenther J, De Nys R (2012) The impact and control of biofouling in marine aquaculture: a review. Biofouling 28:649–669CrossRefPubMedGoogle Scholar
  20. Flaten GE, Kottra G, Stensen W, Isaksen G, Karstad R, Svendsen JS, Daniel H, Svenson J (2011) In vitro characterization of human peptide transporter hPEPT1 interactions and passive permeation studies of short cationic antimicrobial peptides. J Med Chem 54:2422–2432CrossRefPubMedGoogle Scholar
  21. Fusetani N (2004) Biofouling and antifouling. Nat Prod Rep 21:94–104CrossRefPubMedGoogle Scholar
  22. Fusetani N (2011) Antifouling marine natural products. Nat Prod Rep 28:400–410CrossRefPubMedGoogle Scholar
  23. Gerwick WH, Fenner AM (2013) Drug discovery from marine microbes. Microb Ecol 65:800–806PubMedCentralCrossRefPubMedGoogle Scholar
  24. Gerwick WH, Moore BS (2012) Lessons from the past and charting the future of marine natural products drug discovery and chemical biology. Chem Biol 19:85–98PubMedCentralCrossRefPubMedGoogle Scholar
  25. Hanssen KO, Andersen JH, Stiberg T, Engh RA, Svenson J, Geneviere AM, Hansen E (2012) Antitumoral and mechanistic studies of ianthelline isolated from the arctic sponge Stryphnus fortis. Anticancer Res 32:4287–4297PubMedGoogle Scholar
  26. Hellio C, Bourgougnon N, Le Gal Y (2000) Phenoloxidase (ec 1.14.18.1) from the byssus gland of Mytilus edulis: purification, partial characterization and application for screening products with potential antifouling activities. Biofouling 16:235–244CrossRefGoogle Scholar
  27. Hellio C, Tsoukatou M, Marechal JP, Aldred N, Beaupoil C, Clare AS, Vagias C, Roussis V (2005) Inhibitory effects of Mediterranean sponge extracts and metabolites on larval settlement of the barnacle Balanus amphitrite. Mar Biotechnol 7:297–305CrossRefPubMedGoogle Scholar
  28. Hellio C, Marechal JP, Da Gama BP, Pereira RC, Clare AS (2009) Natural marine products with antifouling activities. In: Hellio C, Yebra DM (eds) Advances in marine antifouling coatings and technologies. Woodhead Publishing, New YorkCrossRefGoogle Scholar
  29. Jellali R, Campistron I, Pasetto P, Laguerre A, Gohier F, Hellio C, Pilard JF, Mouget JL (2013) Antifouling activity of novel polyisoprene-based coatings made from photocurable natural rubber derived oligomers. Prog Org Coat 76:1203–1214CrossRefGoogle Scholar
  30. Kelly SR, Jensen PR, Henkel TP, Fenical W, Pawlik JR (2003) Effects of Caribbean sponge extracts on bacterial attachment. Aquat Microb Ecol 31:175–182CrossRefGoogle Scholar
  31. Kelly SR, Garo E, Jensen PR, Fenical W, Pawlik JR (2005) Effects of Caribbean sponge secondary metabolites on bacterial surface colonization. Aquat Microb Ecol 40:191–203CrossRefGoogle Scholar
  32. Kim YJ, Uyama H (2005) Tyrosinase inhibitors from natural and synthetic sources: structure, inhibition mechanism and perspective for the future. Cell Mol Life Sci 62:1707–1723CrossRefPubMedGoogle Scholar
  33. Kotake Y (2012) Molecular mechanisms of environmental organotin toxicity in mammals. Biol Pharm Bull 35:1876–1880CrossRefPubMedGoogle Scholar
  34. Labreuche Y, Lambert C, Soudant P, Boulo V, Huvet A, Nicolas JL (2006) Cellular and molecular hemocyte responses of the pacific oyster, Crassostrea gigas, following bacterial infection with Vibrio aestuarianus strain 01/32. Microbes Infect 8:2715–2724CrossRefPubMedGoogle Scholar
  35. Lidgren G, Bohlin L (1986) Studies of Swedish marine organisms. 7. A novel biologically-active indole alkaloid from the sponge Geodia baretti. Tetrahedron Lett 27:3283–3284CrossRefGoogle Scholar
  36. Litaudon M, Guyot M (1986) Ianthelline, a new derivative of 3,5-dibromo-tyrosine isolated from the sponge Ianthella-ardis from the Bahamas. Tetrahedron Lett 27:4455–4456CrossRefGoogle Scholar
  37. Lohner K, Sevcsik E, Pabst G (2008) Liposome-based biomembrane mimetic systems: implications for lipid-peptide interactions. In: Liu AL (ed) Advances in planar lipid bilayers and liposomes. Elsevier, AmsterdamGoogle Scholar
  38. Marechal JP, Hellio C (2009) Challenges for the development of new non-toxic antifouling solutions. Int J Mol Sci 10:4623–4637PubMedCentralCrossRefPubMedGoogle Scholar
  39. Marechal JP, Hellio C (2011) Antifouling activity against barnacle cypris larvae: do target species matter (Amphibalanus amphitrite versus Semibalanus balanoides)? Int Biodeterior Biodegrad 65:92–101CrossRefGoogle Scholar
  40. Melander C, Moeller PDR, Ballard TE, Richards JJ, Huigens RW, Cavanagh J (2009) Evaluation of dihydrooroidin as an antifouling additive in marine paint. Int Biodeterior Biodegrad 63:529–532CrossRefGoogle Scholar
  41. Melo MN, Ferre R, Castanho M (2009) Opinion antimicrobial peptides: linking partition, activity and high membrane-bound concentrations. Nat Rev Microbiol 7:245–250CrossRefPubMedGoogle Scholar
  42. Molino PJ, Wetherbee R (2008) The biology of biofouling diatoms and their role in the development of microbial slimes. Biofouling 24:365–379CrossRefPubMedGoogle Scholar
  43. Muller WEG, Wang XH, Proksch P, Perry CC, Osinga R, Garderes J, Schroder HC (2013) Principles of biofouling protection in marine sponges: a model for the design of novel biomimetic and bio-inspired coatings in the marine environment? Mar Biotechnol 15:375–398CrossRefPubMedGoogle Scholar
  44. Nakanishi T (2008) Endocrine disruption induced by organotin compounds; organotins function as a powerful agonist for nuclear receptors rather than an aromatase inhibitor. J Toxicol Sci 33:269–276CrossRefPubMedGoogle Scholar
  45. Okoro HK, Fatoki OS, Adekola FA, Ximba BJ, Snyman RG (2011) Sources, environmental levels and toxicity of organotin in marine environment-a review. Asian J Chem 23:473–482Google Scholar
  46. Ortlepp S, Sjogren M, Dahlstrom M, Weber H, Ebel R, Edrada R, Thoms C, Schupp P, Bohlin L, Proksch P (2007) Antifouling activity of bromotyrosine-derived sponge metabolites and synthetic analogues. Mar Biotechnol 9:776–785CrossRefPubMedGoogle Scholar
  47. Qian PY, Lau SCK, Dahms HU, Dobretsov S, Harder T (2007) Marine biofilms as mediators of colonization by marine macroorganisms: implications for antifouling and aquaculture. Mar Biotechnol 9:399–410CrossRefPubMedGoogle Scholar
  48. Qian PY, Xu Y, Fusetani N (2010) Natural products as antifouling compounds: recent progress and future perspectives. Biofouling 26:223–234CrossRefPubMedGoogle Scholar
  49. Richards JJ, Ballard TE, Huigens RW, Melander C (2008) Synthesis and screening of an oroidin library against Pseudomonas aeruginosa biofilms. Chembiochem 9:1267–1279CrossRefPubMedGoogle Scholar
  50. Richards JJ, Reyes S, Stowe SD, Tucker AT, Ballard TE, Mathies LD, Cavanagh J, Melander C (2009) Amide isosteres of oroidin: assessment of antibiofilm activity and C. elegans toxicity. J Med Chem 52:4582–4585PubMedCentralCrossRefPubMedGoogle Scholar
  51. Santos Acevedo M, Puentes C, Carreno K, Gomez Leon J, Stupak M, Garcia M, Perez M, Blustein G (2013) Antifouling paints based on marine natural products from Colombian Caribbean. Int Biodeterior Biodegrad 83:97–104CrossRefGoogle Scholar
  52. Shai Y (1999) Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides. BBA-Biomembr 1462:55–70CrossRefGoogle Scholar
  53. Shearman JW, Myers RM, Beale TM, Brenton JD, Ley SV (2010) Total syntheses of the bromotyrosine-derived natural products ianthelline, 5-bromoverongamine and jbir-44. Tetrahedron Lett 51:4812–4814CrossRefGoogle Scholar
  54. Sipkema D, Franssen MCR, Osinga R, Tramper J, Wijffels RH (2005) Marine sponges as pharmacy. Mar Biotechnol 7:142–162CrossRefPubMedGoogle Scholar
  55. Sjogren M, Dahlstrom M, Goransson U, Jonsson PR, Bohlin L (2004a) Recruitment in the field of Balanus improvisus and Mytilus edulis in response to the antifouling cyclopeptides barettin and 8,9-dihydrobarettin from the marine sponge Geodia barretti. Biofouling 20:291–297CrossRefPubMedGoogle Scholar
  56. Sjogren M, Goransson U, Johnson AL, Dahlstrom M, Andersson R, Bergman J, Jonsson PR, Bohlin L (2004b) Antifouling activity of brominated cyclopeptides from the marine sponge Geodia barretti. J Nat Prod 67:368–372CrossRefPubMedGoogle Scholar
  57. Solter S, Dieckmann R, Blumenberg M, Francke W (2002) Barettin, revisited? Tetrahedron Lett 43:3385–3386CrossRefGoogle Scholar
  58. Sonak S, Bhosle NB (1995) A simple method to assess bacterial attachment to surfaces. Biofouling 9:31–38CrossRefGoogle Scholar
  59. Stowe SD, Richards JJ, Tucker AT, Thompson R, Melander C, Cavanagh J (2011) Anti-biofilm compounds derived from marine sponges. Mar Drugs 9:2010–2035PubMedCentralCrossRefPubMedGoogle Scholar
  60. Svenson J (2013) MabCent: Arctic marine bioprospecting in Norway. Phytochem Rev 12:567–578PubMedCentralCrossRefPubMedGoogle Scholar
  61. Tadesse M, Gulliksen B, Strom MB, Styrvold OB, Haug T (2008) Screening for antibacterial and antifungal activities in marine benthic invertebrates from northern Norway. J Invertebr Pathol 99:286–293CrossRefPubMedGoogle Scholar
  62. Tadesse M, Strom MB, Svenson J, Jaspars M, Milne BF, Torfoss V, Andersen JH, Hansen E, Stensvag K, Haug T (2010) Synoxazolidinones a and b: novel bioactive alkaloids from the ascidian Synoicum pulmonaria. Org Lett 12:4752–4755CrossRefPubMedGoogle Scholar
  63. Takada N, Watanabe R, Suenaga K, Yamada K, Ueda K, Kita M, Uemura D (2001) Zamamistatin, a significant antibacterial bromotyrosine derivative, from the Okinawan sponge Pseudoceratina purpurea. Tetrahedron Lett 42:5265–5267CrossRefGoogle Scholar
  64. Thabard M, Gros O, Hellio C, Marechal JP (2011) Sargassum polyceratium (phaeophyceae, fucaceae) surface molecule activity towards fouling organisms and embryonic development of benthic species. Bot Mar 54:147–157CrossRefGoogle Scholar
  65. Tsukamoto S, Kato H, Hirota H, Fusetani N (1996a) Ceratinamides a and b: new antifouling dibromotyrosine derivatives from the marine sponge Pseudoceratina purpurea. Tetrahedron 52:8181–8186CrossRefGoogle Scholar
  66. Tsukamoto S, Kato H, Hirota H, Fusetani N (1996b) Mauritiamine, a new antifouling oroidin dimer from the marine sponge Agelas mauritiana. J Nat Prod 59:501–503CrossRefGoogle Scholar
  67. Yamada A, Kitamura H, Yamaguchi K, Fukuzawa S, Kamijima C, Yazawa K, Kuramoto M, Wang GYS, Fujitani Y, Uemura D (1997) Development of chemical substances regulating biofilm formation. B Chem Soc Jpn 70:3061–3069CrossRefGoogle Scholar
  68. 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

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Kine Ø. Hanssen
    • 1
  • Gunnar Cervin
    • 2
  • Rozenn Trepos
    • 3
  • Julie Petitbois
    • 3
  • Tor Haug
    • 4
  • Espen Hansen
    • 5
  • Jeanette H. Andersen
    • 5
  • Henrik Pavia
    • 2
  • Claire Hellio
    • 6
  • Johan Svenson
    • 7
    Email author
  1. 1.Centre for Research-based Innovation on Marine Bioactivities and Drug Discovery (MabCent)UiT The Arctic University of NorwayTromsøNorway
  2. 2.Department of Biological and Environmental Sciences-TjärnöUniversity of GothenburgStrömstadSweden
  3. 3.School of Biological SciencesUniversity of PortsmouthPortsmouthUK
  4. 4.Norwegian College of Fishery ScienceUiT The Arctic University of NorwayTromsøNorway
  5. 5.Marbio, UiT The Arctic University of NorwayTromsøNorway
  6. 6.Université de Bretagne Occidentale, LEMAR UMR 6539, IUEM - Technopole Brest-IroisePlouzanéFrance
  7. 7.Department of ChemistryUiT The Arctic University of NorwayTromsøNorway

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