Skip to main content

Advertisement

Log in

Exploring the chemodiversity of tropical microalgae for the discovery of natural antifouling compounds

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Marine microalgae and cyanobacteria have largely been studied for their biotechnological potential and proved their ability to produce a wide array of bioactive molecules. We investigated the antifouling potential of unexplored benthic tropical microalgae using anti-adhesion and toxicity bioassays against two major micro- and ma crobiofoulers, namely bacteria and barnacles. Fifty strains belonging to six phyla [Cyanobacteria, Miozoa (Dinoflagellata), Bacillariophyta, Cryptophyta, Rhodophyta and Haptophyta] were isolated from southwestern Islands of the Indian Ocean. They were chosen in order to represent as much as possible the huge biodiversity of such a rich tropical ecosystem. The associated chemodiversity was highlighted by both NMR- and LC-MS-based metabolomics. The screening of 84 algal fractions revealed that the anti-adhesion activity was concentrated in methanolic ones (i.e. 93% of all active fractions). Our results confirmed that microalgae constitute a promising source of natural antimicrofoulants as 17 out of the 30 active fractions showed high or very high capacity to inhibit the adhesion of three biofilm-forming marine bacteria. Dinoflagellate-derived fractions were the most active, both in terms of number and intensity. However, dinoflagellates were also more toxic and may not be suitable as a source of environmentally friendly antifouling compounds, in contrast to diatoms, e.g. Navicula mollis. The latter and two dinoflagellates of the genus Amphidinium also had interesting anti-settlement activities while being moderately toxic to barnacle larvae. Our approach, combining the bioprospecting of a large number of tropical microalgae for their anti-settlement potential and metabolomics analyses, constituted a first step towards the discovery of alternative ecofriendly antifoulants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Abarzua S, Jakubowski S (1995) Biotechnological investigation for the prevention of biofouling. 1. Biological and biochemical principles for the prevention of biofouling. Mar Ecol Prog Ser 123:301–312

    CAS  Google Scholar 

  • Abida H, Ruchaud S, Rios L, Humeau A, Probert I, De Vargas C, Bach S, Bowler C (2013) Bioprospecting marine plankton. Mar Drugs 11:4594–4611

    CAS  PubMed  PubMed Central  Google Scholar 

  • Adolph S, Bach S, Blondel M, Cueff A, Moreau M, Pohnert G, Poulet SA, Wichard T, Zuccaro A (2004) Cytotoxicity of diatom-derived oxylipins in organisms belonging to different phyla. J Exp Biol 207:2935–2946

    CAS  PubMed  Google Scholar 

  • Aguila-Ramirez RN, Hernandez-Guerrero CJ, Gonzalez-Acosta B, Id-Daoud G, Hewitt S, Pope J, Hellio C (2014) Antifouling activity of symbiotic bacteria from sponge Aplysina gerardogreeni. Int Biodeterior Biodegrad 90:64–70

    CAS  Google Scholar 

  • Aldred N, Clare AS (2008) The adhesive strategies of cyprids and development of barnacle-resistant marine coatings. Biofouling 24:351–363

    CAS  PubMed  Google Scholar 

  • Almeida JR, Freitas M, Cruz S, Leao PN, Vasconcelos V, Cunha I (2015) Acetylcholinesterase in biofouling species: characterization and mode of action of cyanobacteria-derived antifouling agents. Toxins 7:2739–2756

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bagwell CE, Abernathy A, Barnwell R, Milliken CE, Noble PA, Dale T, Beauchesne KR, Moeller PDR (2016) Discovery of bioactive metabolites in biofuel microalgae that offer protection against predatory bacteria. Front Microbiol 7:516

    PubMed  PubMed Central  Google Scholar 

  • Barra L, Chandrasekaran R, Corato F, Brunet C (2014) The challenge of ecophysiological biodiversity for biotechnological applications of marine microalgae. Mar Drugs 12:1641–1675

    PubMed  PubMed Central  Google Scholar 

  • Bellas J (2006) Comparative toxicity of alternative antifouling biocides on embryos and larvae of marine invertebrates. Sci Total Environ 367:573–585

    CAS  PubMed  Google Scholar 

  • Berry JP, Gantar M, Perez MH, Berry G, Noriega FG (2008) Cyanobacterial toxins as allelochemicals with potential applications as algaecides, herbicides and insecticides. Mar Drugs 6:117–146

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bhadury P, Wright PC (2004) Exploitation of marine algae: biogenic compounds for potential antifouling applications. Planta 219:561–578

    CAS  PubMed  Google Scholar 

  • Briand JF (2009) Marine antifouling laboratory bioassays: an overview of their diversity. Biofouling 25:297–311

    CAS  PubMed  Google Scholar 

  • Brian-Jaisson F, Ortalo-Magne 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

    PubMed  Google Scholar 

  • Burgess JG, Boyd KG, Armstrong E, Jiang Z, Yan L, Berggren M, May U, Pisacane T, Granmo Å, Adams DR (2003) The development of a marine natural product-based antifouling paint. Biofouling 19(sup1):197–205

    CAS  PubMed  Google Scholar 

  • Burja AM, Banaigs B, Abou-Mansour E, Burgess JG, Wright PC (2001) Marine cyanobacteria – a prolific source of natural products. Tetrahedron 57:9347–9377

    CAS  Google Scholar 

  • Camps M, Briand JF, 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  PubMed  Google Scholar 

  • Choi H, Mascuch Samantha J, Villa Francisco A, Byrum T, Teasdale Margaret E, Smith Jennifer E, Preskitt Linda B, Rowley David C, Gerwick L, Gerwick William H (2012) Honaucins A−C, potent inhibitors of inflammation and bacterial quorum sensing: synthetic derivatives and structure-activity relationships. Chem Biol 19:589–598

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Dang HY, Lovell CR (2016) Microbial surface colonization and biofilm development in marine environments. Microbiol Mol Biol Res 80:91–138

    CAS  Google Scholar 

  • Desbois AP, Lebl T, Yan L, Smith VJ (2008) Isolation and structural characterisation of two antibacterial free fatty acids from the marine diatom, Phaeodactylum tricornutum. Appl Microbiol Biotechnol 81:755–764

    CAS  PubMed  Google Scholar 

  • Desbois AP, Mearns-Spragg A, Smith VJ (2009) A fatty acid from the diatom Phaeodactylum tricornutum is antibacterial against diverse bacteria including multi-resistant Staphylococcus aureus (MRSA). Mar Biotechnol 11:45–52

    CAS  PubMed  Google Scholar 

  • Dobretsov S, Dahms HU, Qian PY (2006) Inhibition of biofouling by marine microorganisms and their metabolites. Biofouling 22:43–54

    CAS  PubMed  Google Scholar 

  • Doi Y, Ishibashi M, Nakamichi H, Kosaka T, Ishikawa T, Kobayashi J (1997) Luteophanol A, a new polyhydroxyl compound from symbiotic marine dinoflagellate Amphidinium sp. J Org Chem 62:3820–3823

    CAS  Google Scholar 

  • Falaise C, François C, Travers M-A, Morga B, Haure J, Tremblay R, Turcotte F, Pasetto P, Gastineau R, Hardivillier Y, Leignel V, Mouget J-L (2016) Antimicrobial compounds from eukaryotic microalgae against human pathogens and diseases in aquaculture. Mar Drugs 14:159

    PubMed Central  Google Scholar 

  • Favre L, Ortalo-Magné A, Greff S, Pérez T, Thomas OP, Martin J-C, Culioli G (2017) Discrimination of four marine biofilm-forming bacteria by LC–MS metabolomics and influence of culture parameters. J Proteome Res 16:1962–1975

    CAS  PubMed  Google Scholar 

  • Fernández-Alba AR, Hernando MD, Piedra L, Chisti Y (2002) Toxicity evaluation of single and mixed antifouling biocides measured with acute toxicity bioassays. Anal Chim Acta 456:303–312

    Google Scholar 

  • Fiehn O (2002) Metabolomics – the link between genotypes and phenotypes. Plant Mol Biol 48:155–171

    CAS  PubMed  Google Scholar 

  • Findlay JA, Patil AD (1984) Antibacterial constituents of the diatom Navicula delognei. J Nat Prod 47:815–818

    CAS  PubMed  Google Scholar 

  • Fu E, Friedman L, Siegelman HW (1979) Mass-spectral identification and purification of phycoerythrobilin and phycocyanobilin. Biochem J 179:1–6

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fuentes-Grünewald C, Bayliss C, Fonlut F, Chapuli E (2016) Long-term dinoflagellate culture performance in a commercial photobioreactor: Amphidinium carterae case. Bioresour Technol 218:533–540

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Gademann K (2007) Cyanobacterial natural products for the inhibition of biofilm formation and biofouling. CHIMIA 61:373–377

    CAS  Google Scholar 

  • Gastineau R, Hardivillier Y, Leignel V, Tekaya N, Morançais M, Fleurence J, Davidovich N, Jacquette B, Gaudin P, Hellio C, Bourgougnon N, Mouget J-L (2012a) Greening effect on oysters and biological activities of the blue pigments produced by the diatom Haslea karadagensis (Naviculaceae). Aquaculture 368:61–67

    Google Scholar 

  • Gastineau R, Pouvreau J-B, Hellio C, Morançais M, Fleurence J, Gaudin P, Bourgougnon N, Mouget J-L (2012b) Biological activities of purified marennine, the blue pigment responsible for the greening of oysters. J Agric Food Chem 60:3599–3605

    CAS  PubMed  Google Scholar 

  • Gordon BR, Leggat W (2010) Symbiodinium-invertebrate symbioses and the role of metabolomics. Mar Drugs 8:2546–2568

    CAS  PubMed  PubMed Central  Google Scholar 

  • Guedes AC, Barbosa CR, Amaro HM, Pereira CI, Xavier Malcata F (2011) Microalgal and cyanobacterial cell extracts for use as natural antibacterial additives against food pathogens. Int J Food Sci Technol 46:862–870

    CAS  Google Scholar 

  • Guillard RL (1975) Culture of phytoplankton for feeding marine invertebrates. In: Smith W, Chanley M (eds) Culture of marine invertebrate animals. Springer, New York, pp 29–60

  • Guiry MD, Guiry GM (2017) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org/. Accessed 21 Jul 2017

  • Hadfield MG (2011) Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites. Annu Rev Mar Sci 3:453–470

    Google Scholar 

  • Hay ME, Fenical W (1996) Chemical ecology and marine biodiversity: insights and products from the sea. Oceanography 9:10–20

    Google Scholar 

  • Holmström C, James S, Neilan BA, White DC, Kjelleber S (1998) Pseudoalteromonas tunicata sp. nov., a bacterium that produces antifouling agents. Int J Syst Evol Microbiol 48:1205–1212

    Google Scholar 

  • Hou Y, Braun DR, Michel CR, Klassen JL, Adnani N, Wyche TP, Bugni TS (2012) Microbial strain prioritization using metabolomics tools for the discovery of natural products. Anal Chem 84:4277–4283

    CAS  PubMed  PubMed Central  Google Scholar 

  • Houdai T, Matsuoka S, Matsumori N, Murata M (2004) Membrane-permeabilizing activities of amphidinol 3, polyene-polyhydroxy antifungal from a marine dinoflagellate. Biochim Biophys Acta Biomembr 1667:91–100

    CAS  Google Scholar 

  • Hu Y, Chen J, Hu G, Yu J, Zhu X, Lin Y, Chen S, Yuan J (2015) Statistical research on the bioactivity of new marine natural products discovered during the 28 years from 1985 to 2012. Mar Drugs 13:202–221

    PubMed  PubMed Central  Google Scholar 

  • Ingebrigtsen RA, Hansen E, Andersen JH, Eilertsen HC (2016) Light and temperature effects on bioactivity in diatoms. J Appl Phycol 28:939–950

    CAS  PubMed  Google Scholar 

  • Kobayashi J, Kubota T (2007) Bioactive macrolides and polyketides from marine dinoflagellates of the genus Amphidinium. J Nat Prod 70:451–460

    CAS  PubMed  Google Scholar 

  • Kong XY, Han XR, Gao M, Su RG, Wang K, Li XZ, Lu W (2016) Antialgal and antilarval activities of bioactive compounds extracted from the marine dinoflagellate Amphidinium carterae. J Ocean Univ China 15:1014–1020

    CAS  Google Scholar 

  • Kotai J (1972) Instructions for preparation of modified nutrient solution Z8 for algae. Norwegian Institute for Water Research, Oslo

  • Kubota T, Iwai T, Sakai K, Gonoi T, Kobayashi J (2014) Amphidinins C-F, Amphidinolide Q analogues from marine dinoflagellate Amphidinium sp. Org Lett 16:5624–5627

    CAS  PubMed  Google Scholar 

  • Landoulsi J, Cooksey KE, Dupres V (2011) Review – interactions between diatoms and stainless steel: focus on biofouling and biocorrosion. Biofouling 27:1105–1124

    CAS  Google Scholar 

  • Leao PN, Engene N, Antunes A, Gerwick WH, Vasconcelos V (2012) The chemical ecology of cyanobacteria. Nat Prod Rep 29:372–391

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee KWK, Periasamy S, Mukherjee M, Xie C, Kjelleberg S, Rice SA (2014) Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J 8:894–907

    CAS  PubMed  Google Scholar 

  • Lejars M, Margaillan A, Bressy C (2012) Fouling release coatings: a nontoxic alternative to biocidal antifouling coatings. Chem Rev 112:4347–4390

    CAS  PubMed  Google Scholar 

  • Lenoir S, Ten-Hage L, Turquet J, Quod J-P, Bernard C, Hennion M-C (2004) First evidence of palytoxin analogues from an Ostreopsis mascarensis (Dinophycea) benthic bloom in southwestern Indian Ocean. J Phycol 40:1042–1051

    CAS  Google Scholar 

  • Lopes VR, Fernández N, Martins RF, Vasconcelos V (2010) Primary screening of the bioactivity of brackishwater cyanobacteria: toxicity of crude extracts to Artemia salina larvae and Paracentrotus lividus embryos. Mar Drugs 8:471–482

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martins R, Fernandez N, Beiras R, Vasconcelos V (2007) Toxicity assessment of crude and partially purified extracts of marine Synechocystis and Synechococcus cyanobacterial strains in marine invertebrates. Toxicon 50:791–799

    CAS  PubMed  Google Scholar 

  • Mazur-Marzec H, Blaszczyk A, Felczykowska A, Hohlfeld N, Kobos J, Torunska-Sitarz A, Devi P, Montalvao S, D'Souza L, Tammela P, Mikosik A, Bloch S, Nejman-Falenczyk B, Wegrzyn G (2015) Baltic cyanobacteria – a source of biologically active compounds. Eur J Phycol 50:343–360

    CAS  Google Scholar 

  • Montalvao S, Demirel Z, Devi P, Lombardi V, Hongisto V, Perala M, Hattara J, Imamoglu E, Tilvi SS, Turan G, Dalay MC, Tammela P (2016) Large-scale bioprospecting of cyanobacteria, micro- and macroalgae from the Aegean Sea. New Biotechnol 33:399–406

    CAS  Google Scholar 

  • Mudimu O, Rybalka N, Bauersachs T, Born J, Friedl T, Schulz R (2014) Biotechnological screening of microalgal and cyanobacterial strains for biogas production and antibacterial and antifungal effects. Metabolites 4:373–393

    PubMed  PubMed Central  Google Scholar 

  • Najdenski HM, Gigova LG, Iliev II, Pilarski PS, Lukavský J, Tsvetkova IV, Ninova MS, Kussovski VK (2013) Antibacterial and antifungal activities of selected microalgae and cyanobacteria. Int J Food Sci Technol 48:1533–1540

    CAS  Google Scholar 

  • Neves RAF, Fernandes T, Santos LN, Nascimento SM (2017) Toxicity of benthic dinoflagellates on grazing, behavior and survival of the brine shrimp Artemia salina. PLoS One 12(4):e0175168

    PubMed  PubMed Central  Google Scholar 

  • Nieva-Echevarría B, Goicoechea E, Manzanos MJ, Guillén MD (2014) A method based on 1H NMR spectral data useful to evaluate the hydrolysis level in complex lipid mixtures. Food Res Int 66:379–387

    Google Scholar 

  • Noaman NH, Fattah A, Khaleafa M, Zaky SH (2004) Factors affecting antimicrobial activity of Synechococcus leopoliensis. Microbiol Res 159:395–402

    CAS  PubMed  Google Scholar 

  • Othmani A, Bouzidi N, Viano Y, Alliche Z, Seridi H, Blache Y, 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 

  • Othmani A, Briand J-F, Ayé M, Molmeret M, Culioli G (2016a) Surface metabolites of the brown alga Taonia atomaria have the ability to regulate epibiosis. Biofouling 32:801–813

    CAS  PubMed  Google Scholar 

  • Othmani A, Bunet R, Bonnefont J-L, Briand J-F, Culioli G (2016b) 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

    CAS  Google Scholar 

  • Paul VJ, Thacker RW, Banks K, Golubic S (2005) Benthic cyanobacterial bloom impacts the reefs of South Florida (Broward County, USA). Coral Reefs 24:693–697

    Google Scholar 

  • Pérez M, Falqué E, Domínguez H (2016) Antimicrobial action of compounds from marine seaweed. Mar Drugs 14:52

    PubMed Central  Google Scholar 

  • Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65:635–648

    CAS  PubMed  Google Scholar 

  • 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 9:399–410

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Qian PY, Li ZR, Xu Y, Li YX, Fusetani N (2015) Mini-review: marine natural products and their synthetic analogs as antifouling compounds: 2009-2014. Biofouling 31:101–122

    CAS  PubMed  Google Scholar 

  • Raniello R, Iannicelli MM, Nappo M, Avila C, Zupo V (2007) Production of Cocconeis neothumensis (Bacillariophyceae) biomass in batch cultures and bioreactors for biotechnological applications: light and nutrient requirements. J Appl Phycol 19:383–391

    CAS  Google Scholar 

  • 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  Google Scholar 

  • Saeed AF, Awan SA, Ling SM, Wang RZ, Wang S (2017) Domoic acid: attributes, exposure risks, innovative detection techniques and therapeutics. Algal Res 24:97–110

    Google Scholar 

  • Salta M, Wharton JA, Blache Y, Stokes KR, Briand J-F (2013) Marine biofilms on artificial surfaces: structure and dynamics. Environ Microbiol 15:2879–2893

    PubMed  Google Scholar 

  • Sanchez-Saavedra MD, Licea-Navarro A, Bernaldez-Sarabia J (2010) Evaluation of the antibacterial activity of different species of phytoplankton. Rev Biol Mar Oceanogr 45:531–536

    Google Scholar 

  • Scardino AJ, de Nys R (2011) Mini review: biomimetic models and bioinspired surfaces for fouling control. Biofouling 27:73–86

    CAS  PubMed  Google Scholar 

  • Schultz MP, Bendick JA, Holm ER, Hertel WM (2011) Economic impact of biofouling on a naval surface ship. Biofouling 27:87–98

    CAS  PubMed  Google Scholar 

  • Singh S, Verma SK (2012) Application of direct analysis in real time mass spectrometry (DART-MS) for identification of an epiphytic cyanobacterium, Nostoc sp. Anal Lett 45:2562–2568

    CAS  Google Scholar 

  • Smida DB, Lundholm N, Kooistra WHCF, Sahraoui I, Ruggiero MV, Kotaki Y, Ellegaard M, Lambert C, Mabrouk HH, Hlaili AS (2014) Morphology and molecular phylogeny of Nitzschia bizertensis sp. nov.—a new domoic acid-producer. Harmful Algae 32:49–63

    CAS  Google Scholar 

  • Smith CA, Want EJ, O'Maille G, Abagyan R, Siuzdak G (2006) XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem 78:779–787

    CAS  PubMed  Google Scholar 

  • Stanier RY, Kunisawa R, Mandel M, Cohen-Bazire G (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bact Rev 35:171–205

  • Suriyanti SNP, Usup G (2015) First report of the toxigenic Nitzschia navis-varingica (Bacillariophyceae) isolated from Tebrau Straits, Johor, Malaysia. Toxicon 108:257–263

    CAS  PubMed  Google Scholar 

  • Taylor MS, Stahl-Timmins W, Redshaw CH, Osborne NJ (2014) Toxic alkaloids in Lyngbya majuscula and related tropical marine cyanobacteria. Harmful Algae 31:1–8

    CAS  PubMed  Google Scholar 

  • Ten-Hage LC, Robillot C, Turquet J, Le Gall F, Le Caer J-P, Bultel V, Guyot M, Molgó J (2002) Effects of toxic extracts and purified borbotoxins from Prorocentrum borbonicum (Dinophyceae) on vertebrate neuromuscular junctions. Toxicon 40:137–148

    CAS  PubMed  Google Scholar 

  • Van Wagoner RM, Satake M, Wright JLC (2014) Polyketide biosynthesis in dinoftagellates: what makes it different? Nat Prod Rep 31:1101–1137

    PubMed  Google Scholar 

  • Viles HA, Spencer T, Teleki K, Cox C (2000) Observations on 16 years of microfloral recolonization data from limestone surfaces, Aldabra Atoll, Indian Ocean: implications for biological weathering. Earth Surf Process Landf 25:1355–1370

    Google Scholar 

  • Volk R-B, Furkert FH (2006) Antialgal, antibacterial and antifungal activity of two metabolites produced and excreted by cyanobacteria during growth. Microbiol Res 161:180–186

    CAS  PubMed  Google Scholar 

  • Washida K, Koyama T, Yamada K, Kita M, Uemura D (2006) Karatungiols A and B, two novel antimicrobial polyol compounds, from the symbiotic marine dinoflagellate Amphidinium sp. Tetrahedron Lett 47:2521–2525

    CAS  Google Scholar 

  • Wichard T, Poulet AS, Halsband-Lenk C, Albaina A, Harris R, Liu D, Pohnert G (2005) Survey of the chemical defence potential of diatoms: screening of fifty species for α,β,γ,δ-unsaturated aldehydes. J Chem Ecol 31:949–958

    CAS  PubMed  Google Scholar 

  • Xu L, Weathers PJ, Xiong X-R, Liu C-Z (2009) Microalgal bioreactors: challenges and opportunities. Eng Life Sci 9:178–189

    CAS  Google Scholar 

  • 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 50:75–104

    CAS  Google Scholar 

  • Zea Obando C, Linossier I, Kervarec N, Zubia M, Turquet J, Faÿ F, Rehel K (2016) Rapid identification of osmolytes in tropical microalgae and cyanobacteria by 1H HR-MAS NMR spectroscopy. Talanta 153:372–380

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would particularly like to thank Dr. Nicolas Chomérat (Ifremer, France), Maurice Loir and Dr. Mitsunori Iwataki (University of Tokyo, Japan), for their help in Amphidinium, Prorocentrum and Navicula species identification. They also would like to thank Qiong-Yao Xue, Emmanuelle Espuche and Lucie Bruno for the technical assistance (extraction of microalgae and some bioassays).

Funding

This study was funded by the French National Research Agency (project BioPainTrop, ANR-12-CDII-0008).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Gérald Culioli or Jean-François Briand.

Electronic supplementary material

ESM 1

(DOCX 1937 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Réveillon, D., Tunin-Ley, A., Grondin, I. et al. Exploring the chemodiversity of tropical microalgae for the discovery of natural antifouling compounds. J Appl Phycol 31, 319–333 (2019). https://doi.org/10.1007/s10811-018-1594-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-018-1594-z

Keywords

Navigation