Sunscreen, antioxidant, and bactericide capacities of phlorotannins from the brown macroalga Halidrys siliquosa
The present study focused on a brown macroalga (Halidrys siliquosa), with a particular emphasis on polyphenols and their associated biological activities. Two fractions were obtained by liquid/liquid purification from a crude hydroethanolic extract: (i) an ethyl acetate fraction and (ii) an aqueous fraction. Total phenolic contents and antioxidant activities of extract and both fractions were assessed by in vitro tests (Folin–Ciocalteu test, 2,2-diphenyl-1-picrylhydrazyl (DPPH) radical scavenging activity, reducing power assay, superoxide anion scavenging assay, and β-carotene–linoleic acid system). For the most active fraction, i.e., the ethyl acetate fraction, the oxygen radical absorbance capacity (ORAC) value, antibacterial activities, and sunscreen potential (Sun Protection Factor and UV-A-Protection Factor) were tested in vitro. A high correlation found between antioxidant activities and total phenolic content was interpreted as the involvement of polyphenolic compounds in antioxidant mechanisms. Interestingly, the ethyl acetate fraction appeared to be a broad-spectrum UV absorber and showed a strong bactericidal activity against Pseudomonas aeruginosa, Staphylococcus aureus, and Escherichia coli. In this fraction, four phenolic compounds (trifuhalols and tetrafuhalols and, for the first time, diphlorethols and triphlorethols) were identified using 1D and 2D nuclear magnetic resonance (NMR) and MS analysis. These findings are promising for the use of H. siliquosa, abundant in Brittany, as a valuable source of photoprotectant molecules for sunscreen and cosmetic applications.
KeywordsAntioxidant Bactericidal Phenolic compounds Phaeophyceae Seaweed ORAC value Sunscreen potential
This work was co-financed with the support of the European Union ERDF-Atlantic Area Programme, MARMED project no. 2011-1/164 and the project RIV-ALG (n° 13006760), financed by CBB Development, and the region Bretagne (France). Authors from LEMAR would like to thank the Labex Mer initiative, a State Grant from the French Agence Nationale de la Recherche (ANR) in the “Investissements d’avenir” Program (reference ANR-10-LABX-19-01, Labex Mer). The first author thanks Alexandre Canton for his assistance during the extraction and purification process and Helen McCombie for reviewing English.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest. All authors contributed significantly to this work and are in agreement with the content of the manuscript.
Klervi Le Lann, Valérie Stiger-Pouvreau and Laurence Coiffard conceived and designed the experiments. Klervi Le Lann, Gwladys Surget, Céline Couteau, Stéphane Cérantola, and Fanny Gaillard performed the experiments. Klervi Le Lann analyzed the data. Mayalen Zubia, Fabienne Guérard, Nathalie Poupart, and Valérie Stiger-Pouvreau contributed materials and analysis tools. Klervi Le Lann, Valérie Stiger-Pouvreau, Fabienne Guérard, Gwladys Surget, Stéphane Cérantola, Mayalen Zubia, and Laurence Coiffard wrote the paper.
- Couteau C, Pommier M, Paparis E, Coiffard LJM (2007) Study of the efficacy of 18 sun filters authorized in European Union tested in vitro. Pharm - Pharmazie 62:449–452Google Scholar
- Diffey BL, Robson J (1989) A new substrate to measure sunscreen protection factors throughout the ultraviolet spectrum. J Soc Cosmet Chem 40:127–133Google Scholar
- European Pharmacopoeia 7.0 - 2011. https://www.edqm.eu. Accessed 27 Oct 2015
- Harnita ANI, Santosa IE, Martono S, Sudarsono S, Widyarini S, Harren FJ (2013) Inhibition of lipid peroxidation induced by ultraviolet radiation by crude phlorotannis isolated from brown algae Sargassum hystrix v. buxifolium C. Agardh. Indones J Chem 13:14–20Google Scholar
- Kornprobst JM (2010) Encyclopedia of marine natural products. Wiley-Blackwell, WeinheimGoogle Scholar
- Le Lann K, Jégou C, Stiger-Pouvreau V (2008) Effect of different conditioning treatments on total phenolic content and antioxidant activities in two Sargassacean species: comparison of the frondose Sargassum muticum (Yendo) Fensholt and the cylindrical Bifurcaria bifurcata R. Ross. Phycol Res 56:238–245CrossRefGoogle Scholar
- Le Lann K, Ferret C, VanMee E, Spagnol C, Lhuillery M, Payri C, Stiger‐Pouvreau V (2012b) Total phenolic, size-fractionated phenolics and fucoxanthin content of tropical Sargassaceae (Fucales, Phaeophyceae) from the South Pacific Ocean: spatial and specific variability. Phycol Res 60:37–50CrossRefGoogle Scholar
- Liu H, Zhao L, Guo S, Xia Y, Zhou P (2011) Modification of fish skin collagen film and absorption property of tannic acid. J Food Sci Technol 51(6):1102–1109Google Scholar
- Montero L, Sánchez-Camargo AP, García-Cañas V, Tanniou A, Stiger-Pouvreau V, Russo M, Rastrelli L, Cifuentes A, Herrero M, Ibáñez E (2016) Anti-proliferative activity and chemical characterization by comprehensive two-dimensional liquid chromatography coupled to mass spectrometry of phlorotannins from the brown macroalga Sargassum muticum collected on North-Atlantic coasts. J Chromatogr A 1428:115–125CrossRefPubMedGoogle Scholar
- Parys S, Kehraus S, Krick A, Glombitza KW, Carmeli S, Klimo K, Gerhäuser C, König GM (2010) In vitro chemopreventive potential of fucophlorethols from the brown alga Fucus vesiculosus L. by anti-oxidant activity and inhibition of selected cytochrome P450 enzymes. Phytochemistry 71:221–229CrossRefPubMedGoogle Scholar
- Ragan MA, Glombitza K-W (1986) Phlorotannins, brown algal polyphenols. Prog Phycol Res 4:129–241Google Scholar
- Stiger-Pouvreau V, Jégou C, Cérantola S, Guérard F, Le Lann K (2014) Phlorotannins in Sargassaceae species from Brittany (France): Interesting molecules for ecophysiological and valorisation purposes. In: Nathalie Bourgougnon, Editor(s), Advances in Botanical Research, Academic Press. 71: 379–411Google Scholar
- Surget G, Stiger-Pouvreau V, Le Lann K, Kervarec N, Couteau C, Coiffard LJM, Gaillard F, Cahier K, Guérard F, Poupart N (2015) Structural elucidation, in vitro antioxidant and photoprotective capacities of a purified polyphenolic-enriched fraction from a saltmarsh plant. J Photochem Photobiol B 143:52–60CrossRefPubMedGoogle Scholar
- Tanniou A, Vandanjon L, Incera M, Serrano Leon E, Husa V, Le Grand J, Nicolas JL, Poupart N, Kervarec N, Engelen A, Walsh R, Guerard F, Bourgougnon N, Stiger-Pouvreau V (2014) Assessment of the spatial variability of phenolic contents and associated bioactivities in the invasive alga Sargassum muticum sampled along its European range from Norway to Portugal. J Appl Phycol 26:1215–1230Google Scholar