Abstract
The purification of the chloroform extract from the brown invasive macroalga Sargassum muticum, through a series of chromatographic separations, yielded 12 fractions that were tested against strains of bacteria, microalgae, and fungi involved in marine biofilm formation. The chemical composition of four (a, c, g, and k) out of the six fractions that exhibited anti-microfouling activity was investigated. Fraction a contained saturated and unsaturated linear hydrocarbons (C12–C27). Arachidonic acid was identified as the major metabolite in fraction c whereas fraction g contained mainly palmitic, linolenic, and palmitoleic acids. Fraction k was submitted to further purification yielding the fraction kAcaF1e that was composed of galactoglycerolipids, active against the growth of two of the four bacterial strains (Shewanella putrefaciens and Polaribacter irgensii) and all tested fungi. These promising results, in particular the isolation and the activity of galactoglycerolipids, attest the potential of the huge biomass of S. muticum as a source of new environmentally friendly antifouling compounds.
Similar content being viewed by others
References
Abarzua S, Jakubowski S (1995) Biotechnological investigation for the prevention of biofouling. I. Biological and biochemical principles for the prevention of biofouling. Mar Ecol Prog Ser 123:301–312
Abarzua S, Jakubowski S, Eckert S, Fuchs P (1999) Biotechnological investigation for the prevention of marine biofouling II. Blue-green algae as potential producers of biogenic agents for the growth inhibition of microfouling organisms. Bot Mar 42:459–465
Alzieu C, Sanjuan J, Deltreil JP, Borel M (1986) Tin contamination in Arcachon Bay—effects on oyster shell anomalies. Mar Pollut Bull 17:494–8
Alzieu C, Sanjuan J, Michel P, Borel M, Dreno JP (1989) Monitoring and assessment of butyltins in Atlantic coastal waters. Mar Pollut Bull 20:22–6
Antizar-Ladislao B (2008) Environmental levels, toxicity and human exposure to tributyltin (TBT)-contaminated marine environment. A review. Environ Int 34:292–308
Barbosa JP, Fleury BG, Da Gama BAP, Teixeira VL, Pereira RC (2007) Natural products as antifoulants in the Brazilian brown alga Dictyota pfaffii (Phaeophyta, Dictyotales). Biochem Syst Ecol 35:549–553
Beech IB (1999) La corrosion microbienne. Biofutur 186:36–41
Beech IB, Sunner J (2004) Biocorrosion: towards understanding interactions between biofilms and metals. Curr Opin Biotechnol 15:181–186
Bhosale SH, Nagle VL, Jagtap TG (2002) Antifouling potential of some marine organisms from India against species of Bacillus and Pseudomonas. Mar Biotechnol 4:111–118
Blaber SJM (1970) The occurrence of a penis-like outgrowth behind the right tentacle in spent females of Nucella lapillus. Proc Malacol Soc Lond 39:231–233
Braithwaite RA, McEvoy LA (2005) Marine biofouling on fish farms and its remediation. Adv Mar Biol 47:215–252
Briand JF (2009) Marine antifouling laboratory bioassays: an overview of their diversity. Biofouling 25:297–311
Cassano V, De-Paula JC, Fujii MT, Da Gama BAP, Teixeira VL (2008) Sesquiterpenes from the introduced red seaweed Laurencia caduciramulosa (Rhodomelaceae, Ceramiales). Biochem Syst Ecol 36:223–226
CD Commission Directive 2002/62/EC of 9 July 2002. O J Eur Commun 2002. L183:58–9
Champ MA (2000) A review of organotin regulatory strategies, pending actions, related costs and benefits. Sci Total Environ 258:21–71
Champ MA (2003) Economic and environmental impacts on ports and harbors from the convention to ban harmful marine anti-fouling systems. Mar Pollut Bull 46:935–40
Columbo D, Franchini L, Toma L, Ronchetti F, Tanaka R, Takayasu J, Nishino H, Tokuda H (2006) Cyclic and branched acyl chain galactoglycerolipids and their effect on anti-tumor-promoting activity. Eur J Med Chem 41:1456–1463
Culioli G, Ortalo-Magné A, Valls R, Hellio C, Clare AS, Piovetti L (2008) Antifouling activity of meroditerpenoids from the marine brown alga Halidrys siliquosa. J Nat Prod 71:1121–1126
Da Gama BA, Pereira RC, Carvalho AGV, Coutinho R, Yoneshigue Valentin Y (2002) The effects of seaweed secondary metabolites on biofouling. Biofouling 18:13–20
De Mora SJ, Stewart C, Phillips D (1995) Sources and rate of degradation of tri(n-butyl) tin in marine sediments near Auckland, New Zealand. Mar Pollut Bull 30:50–7
De Nys R, Steinberg PD (2002) Linking marine biology and biotechnology. Curr Opin Biotechnol 13:244–248
Deal MS, Hay ME, Wilson D, Fenical W (2003) Galactolipids rather than phlorotannins as herbivore deterrents in the brown seaweed Fucus vesiculosus. Oecologia 136:107–114
Desbois AP, Mearns-Spragg A, Smith VJ (2009) A fatty acid from the diatom Phaeodactylum tricornutum as antibacterial against diverse bacteria including multi-resistant Staphylococcus aureus (MRSA). Mar Biotechnol 11:45–52
Di Landa G, Ansanelli G, Ciccoli R, Cremisini C (2006) Occurrence of antifouling paint booster biocides in selected harbors and marinas inside the Gulf of Napoli: a preliminary survey. Mar Pollut Bull 52:1541–1546
Dowson PH, Bubb JM, Lester JN (1993) Temporal distribution of organotins in the aquatic environment: five years after the 1987 UK retail ban on TBT based antifouling paints. Mar Pollut Bull 26:487–94
Etahiri S, Bultel-Poncé V, Caux C, Guyot M (2001) New bromoditerpenes from the red alga Sphaerococcus coronopifolius. J Nat Prod 64:1024–1027
Fletcher RL (1975) Heteroantagonism observed in mixed algal cultures. Nature 253:534–535
Freile-Pelegrin Y, Morales JL (2004) Antibacterial activity in marine algae from Yucatan coast, Mexico. Bot Mar 47:140–146
Fusetani N (2004) Biofouling and antifouling. Nat Prod Rep 21:94–104
Ganti VS, Kim KH, Bhattarai HD and Shin HW (2006) Isolation and characterisation of some antifouling agents from the brown alga Sargassum confusum. J Asian Nat Prod Res 8:309–315
Glombitza KW, Klapperich K (1985) Antibiotics from algae. XXXIV. Cleavage of the high-molecular-weight methylated phlorotannin fraction from the brown alga Pelvetia canaliculata. Bot Mar 28:139–144
Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can J Microbiol 8:229–239
Hellio C, Bremer G, Pons A, Le Gal Y, Bourgougnon N (2000) Inhibition of the development of microorganisms (bacteria and fungi) by extracts of marine algae from Brittany (France). Appl Microbiol Biotechnol 54:543–549
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 52:231–247
Hellio C, Berge JP, Beaupoil C, Le Gal Y, Bougougnon N (2002) Screening of marine algal extracts for anti-settlement activities against microalgae and macroalgae. Biofouling 18:205–215
Hellio C, Maréchal JP, Véron B, Bremer G, Clare AS, Le Gal Y (2004) Seasonal variation of antifouling activities of marine algae from the Brittany coast (France). Mar Biotech 6:67–82
Hellio C, Maréchal JP, Da Gama BAP, Pereira R, Clare AS (2009) Natural marine products with antifouling activities In: Advances in marine antifouling coatings and technologies. Woodshead, Cambridge, pp 572–622
IMO. International Marine Organisation (2001). International convention on the control of harmful antifouling systems on ships. Available from: http://www.imo.org/Conventions/mainframe.asp?topic_id=529
Jennings JG, Steinberg PD (1997) Phlorotannins vs. others factors affecting epiphyte abundance on the kelp Ecklonia radiata. Oecologia 109:461–473
Karlsson J, Eklund B (2004) New biocide-free anti-fouling paints are toxic. Mar Pollut Bull 49:456–464
Katsuoka M, Ogura C, Etoh H, Sakata K (1990) Galactosyl and sulfo-quinovosyl-diacylglycerols isolated from the brown algae, Undaria pinnatifida and Costaria costata as repellents of blue mussel, Mytilus edulis. Agric Biol Chem 54:3043–3044
Konstantinou IK, Albanis TA (2004) Worldwide occurrence and effects of antifouling paint booster biocides in the aquatic environment: a review. Environ Int 30:235–48
Koutsaftis A, Aoyama I (2007) Toxicity of four antifouling biocides and their mixtures on the brine shrimp Artemia salina. Sci Total Environ 387:166–174
Kubanek J, Jensen PR, Keifer PA, Sullards MC, Collins DO, Fenical W (2003) Seaweed resistance to microbial attack: a targeted chemical defense against marine fungi. Proc Natl Acad Sci USA 100:6916–6921
Langlois G (1975) Effect of algal exudates on substratum selection by the motile marine telotroch Vorticella marina. J Protozool 221:115–123
Maréchal JP, Culioli G, Hellio C, Thomas-Guyon H, Callow ME, Clare AS, Ortalo-Magne A (2004) Seasonal variation in antifouling activity of crude extracts of the brown alga Bifurcaria bifurcata (Cystoseiraceae) against cyprids of Balanus amphitrite and the marine bacteria Cobetia marina and Pseudoalteromonas haloplanktis. J Exp Mar Biol Ecol 313:47–62
Metzger JO, Bornsheuer U (2006) Lipids as renewable resources: current state of chemical and biotechnological conversion and diversification. Appl Microbiol Biotechnol 71:13–22
McLachlan J, Craigie JS (1964) Algal inhibition by yellow ultraviolet absorbing substances from Fucus vesiculosus. Can J Bot 42:287–292
Mokrini R, Ben Mesaoud M, Daoudi M, Hellio C, Marechal JP, El Hattab M, Ortalo-Magne 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
Paul VJ (1992) Chemical defences of benthic marine invertebrates. In: Paul VJ (ed) Ecological roles of marine natural products. Comstock, Ithaca, pp 164–188
Pereira RC, Da Gama BAP (2008) Macroalgal chemical defenses and their roles in structuring tropical marine communities. In: Amsler AM (ed) Algal chemical ecology. Springer, Heidelberg, pp 25–56
Plouguerné, E. (2006). Etude écologique et chimique de deux algues récemment introduites sur les côtes bretonnes, Grateloupia turuturu Yamada et Sargassum muticum (Yendo) Fensholt : nouvelles ressources biologiques de composés à activité antifouling. PhD dissertation. Université de Bretagne Occidentale, Brest
Plouguerné E, Kikuchi H, Oshima Y, Deslandes E, Stiger-Pouvreau V (2006a) Isolation of Cholest-5-en-3-ol formate from the red alga Grateloupia turuturu Yamada and its chemotaxonomic significance. Biochem Syst Ecol 34:714–717
Plouguerné E, Le Lann K, Connan S, Jechoux G, Deslandes E, Stiger-Pouvreau V (2006b) Spatial and seasonal variation in density, reproductive status, length and phenolic content of the invasive brown macroalga Sargassum muticum (Yendo) Fensholt along the coast of Western Brittany (France). Aquat Bot 85:337–344
Plouguerné E, Hellio C, Deslandes E, Véron B, Stiger-Pouvreau V (2008) Anti-microfouling activities of extracts of two invasive algae: Grateloupia turuturu and Sargassum muticum. Bot Mar 51:202–208
Rosell, K.G. and Srivastava, L.M. (1987). Fatty acids as antimicrobial substances in brown algae. In: Ragan A. and Bird C.J. (eds.). Twelfth International Seaweed Symposium. Developments in hydrobiology 41 (reprinted from Hydrobiologia 151/152). Junk, Dordrecht , pp. 471–475
Sanchez I, Fernandez C, Arrontes J (2005) Long-term changes in the structure of intertidal assemblages after invasion by Sargassum muticum (Phaeophyta). J Phycol 41:942–949
Schmitt TM, Hay ME, Lindquist N (1995) Constraints on chemically mediated coevolution: multiple functions for seaweed secondary metabolites. Ecology 76:107–123
Sieburth JM, Conover JT (1965) Sargassum tannin, an anti-biotic which retards fouling. Nature 208:52–53
Smith BS (1981) Tributyltin compounds induce male characteristics on female mudsnails Nassarius obsoletus = Ilyanassa obsoleta. J Appl Toxicol 1:141–144
Steinberg PD, De Nys R (2002) Chemical mediation of colonization of seaweed surfaces. J Phycol 38:621–629
Tsoukatou M, Hellio C, Vagias C, Harvala C, Roussis V (2002) Chemical defense and antifouling activity of three Mediterranean sponges of the genus Ircinia. Z Naturforsch 57:161–171
Tsoukatou M, Maréchal JP, Hellio C, Novaković I, Tufegdzic S, Sladić D, Gašić MJ, Clare AS, Vagias C, Roussis V (2007) Evaluation of the activity of the sponge metabolites avarol and avarone and their synthetic derivatives against fouling micro- and macroorganisms. Molecules 12:1022–1034
Yebra DM, Kiil S, Dam-Johansen K (2004) Antifouling technology: past, present and future steps towards efficient and environmentally friendly antifouling coatings. Progr Org Coating 50:75–104 Brest, France
Acknowledgments
This research was part of the first author’s Ph.D. project carried out in the Laboratory of Ecophysiology and Biotechnology of Halophytes and Marine algae (LEBHAM, France) under the supervision of the last author, with the financial support of the Brest Metropole Oceane (BMO) and the region Bretagne (PRIR SUBVEMAR). Financial support from the University of Athens, in the form of a “Kapodistrias” grant, is gratefully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Plouguerné, E., Ioannou, E., Georgantea, P. et al. Anti-microfouling Activity of Lipidic Metabolites from the Invasive Brown Alga Sargassum muticum (Yendo) Fensholt. Mar Biotechnol 12, 52–61 (2010). https://doi.org/10.1007/s10126-009-9199-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-009-9199-9