Skip to main content
SpringerLink
Log in

Sunscreen, antioxidant, and bactericide capacities of phlorotannins from the brown macroalga Halidrys siliquosa

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

Abstract

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.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ar Gall E, Lelchat F, Hupel M, Jegou C, Stiger-Pouvreau V (2015) Extraction and purification of phenols (phlorotannins) from brown algae. In: Stengel D, Connan S (eds) Natural products from marine algae: methods and protocols. Springer, New York, pp 131–143

    Chapter  Google Scholar 

  • Bourgougnon N, Stiger-Pouvreau V (2011) Chemodiversity and bioactivity within red and brown macroalgae along the French coasts, metropole and overseas departments and territories. In: Kim S-K (ed) Handbook of marine macroalgae. Wiley, Ltd, London, pp 58–105

    Chapter  Google Scholar 

  • Cao G, Alessio HM, Cutler RG (1993) Oxygen-radical absorbance capacity assay for antioxidants. Free Radic Biol Med 14:303–311

    Article  CAS  PubMed  Google Scholar 

  • Celis-Plá PSM, Bouzon ZL, Hall-Spencer JM et al (2016) Seasonal biochemical and photophysiological responses in the intertidal macroalga Cystoseira tamariscifolia (Ochrophyta). Mar Environ Res 115:89–97

    Article  PubMed  Google Scholar 

  • Cérantola S, Breton F, Gall EA, Deslandes E (2006) Co-occurrence and antioxidant activities of fucol and fucophlorethol classes of polymeric phenols in Fucus spiralis. Bot Mar 49:347–351

    Article  Google Scholar 

  • Cha S-H, Ko C-I, Kim D, Jeon Y-J (2012) Protective effects of phlorotannins against ultraviolet B radiation in zebrafish (Danio rerio). Vet Dermatol 23:51–e12

    Article  PubMed  Google Scholar 

  • Chua M-T, Tung Y-T, Chang S-T (2008) Antioxidant activities of ethanolic extracts from the twigs of Cinnamomum osmophloeum. Bioresour Technol 99:1918–1925

    Article  CAS  PubMed  Google Scholar 

  • Cockell CS, Knowland J (1999) Ultraviolet radiation screening compounds. Biol Rev Camb Philos Soc 74:311–345

    Article  CAS  PubMed  Google Scholar 

  • 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 62:449–452

    CAS  Google Scholar 

  • Diffey BL, Robson J (1989) A new substrate to measure sunscreen protection factors throughout the ultraviolet spectrum. J Soc Cosmet Chem 40:127–133

    CAS  Google Scholar 

  • Dudonné S, Vitrac X, Coutière P, Woillez M, Mérillon JM (2009) Comparative study of antioxidant properties and total phenolic content of 30 plant extracts of industrial interest using DPPH, ABTS, FRAP, SOD, and ORAC assays. J Agric Food Chem 57:1768–1774

    Article  PubMed  Google Scholar 

  • El-Boury S, Couteau C, Boulande L, Paparis E, Coiffard LJM (2007) Effect of the combination of organic and inorganic filters on the sun protection factor (SPF) determined by in vitro method. Int J Pharm 340:1–5

    Article  CAS  PubMed  Google Scholar 

  • Eom S-H, Kim Y-M, Kim S-K (2012) Antimicrobial effect of phlorotannins from marine brown algae. Food Chem Toxicol 50:3251–3255

    Article  CAS  PubMed  Google Scholar 

  • European Pharmacopoeia 7.0 - 2011. https://www.edqm.eu. Accessed 27 Oct 2015

  • Frankel EN, Meyer AS (2000) The problems of using one-dimensional methods to evaluate multifunctional food and biological antioxidants. J Sci Food Agric 80:1925–1941

    Article  CAS  Google Scholar 

  • Fujii Y, Tanaka R, Miyake H et al (2013) Evaluation for antioxidative properties of phlorotannins isolated from the brown alga Eisenia bicyclis, by the H-ORAC method. Food Nutr Sci 4:78–82

    Article  CAS  Google Scholar 

  • Fukumoto LR, Mazza G (2000) Assessing antioxidant and prooxidant activities of phenolic compounds. J Agric Food Chem 48:3597–3604

    Article  CAS  PubMed  Google Scholar 

  • Glombitza K-W, Sattler E (1973) Trifuhalol, ein neuer triphenyldiäther aus Halidrys siliquosa (1). Tet Lett 14:4277–4280

    Article  Google Scholar 

  • Glombitza K-W, Rosener H-U, Müller D (1975) Bifuhalol und diphlorethol aus Cystoseira tamariscifolia. Phytochemistry 14:1115–1116

    Article  CAS  Google Scholar 

  • Guinea M, Franco V, Araujo-Bazán L, Rodríguez-Martín I, González S (2012) In vivo UVB-photoprotective activity of extracts from commercial marine macroalgae. Food Chem Toxicol 50:1109–1117

    Article  CAS  PubMed  Google Scholar 

  • 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 13:14–20

    CAS  Google Scholar 

  • Heffernan N, Brunton NP, FitzGerald RJ, Smyth TJ (2015) Profiling of the molecular weight and structural isomer abundance of macroalgae-derived phlorotannins. Mar Drugs 13:509–528

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang D, Ou B, Prior RL (2005) The chemistry behind antioxidant capacity assays. J Agric Food Chem 53:1841–1856

    Article  CAS  PubMed  Google Scholar 

  • Huang W-Y, Majumder K, Wu J (2010) Oxygen radical absorbance capacity of peptides from egg white protein ovotransferrin and their interaction with phytochemicals. Food Chem 123:635–641

    Article  CAS  Google Scholar 

  • Huovinen P, Gómez I (2015) UV sensitivity of vegetative and reproductive tissues of two antarctic brown algae is related to differential allocation of phenolic substances. Photochem Photobiol 91:1382–1388

    Article  CAS  PubMed  Google Scholar 

  • Ichihashi M, Ueda M, Budiyanto A, Bito T, Oka M, Fukunaga M, Horikawa T (2003) UV-induced skin damage. Toxicology 189:21–39

    Article  CAS  PubMed  Google Scholar 

  • Ishimoto H, Tai A, Yoshimura M, Amakura Y, Yoshida T, Hatano T, Ito H (2012) Antioxidative properties of functional polyphenols and their metabolites assessed by an ORAC assay. Biosci Biotech Biochem 76:395–399

    Article  CAS  Google Scholar 

  • Jarzycka A, Lewińska A, Gancarz R, Wilk KA (2013) Assessment of extracts of Helichrysum arenarium, Crataegus monogyna, Sambucus nigra in photoprotective UVA and UVB; photostability in cosmetic emulsions. J Photochem Photobiol B 128:50–57

    Article  CAS  PubMed  Google Scholar 

  • Jégou C, Kervarec N, Cérantola S, Bihannic I, Stiger-Pouvreau V (2015) NMR use to quantify phlorotannins. The case of Cystoseira tamariscifolia, a phloroglucinol-producing brown macroalga in Brittany (France). Talanta 135:1–6

    Article  PubMed  Google Scholar 

  • Kang Y-M, Eom S-H, Kim Y-M (2013) Protective effect of phlorotannins from Eisenia bicyclis against lipopolysaccharide-stimulated inflammation in HepG2 cells. Environ Toxicol Pharmacol 35:395–401

    Article  CAS  PubMed  Google Scholar 

  • Kaur C, Kapoor HC (2002) Anti-oxidant activity and total phenolic content of some Asian vegetables. Int J Food Sci Technol 37:153–161

    Article  CAS  Google Scholar 

  • Keusgen M, Glombitza K-W (1995) Phlorethols, fuhalols and their derivatives from the brown alga Sargassum spinuligerum. Phytochemistry 38:975–985

    Article  CAS  Google Scholar 

  • Kim AR, Shin TS, Lee MS, Park JY, Park KE, Yoon NY, Kim JS, Choi JS, Jang BC, Byun DS, Park NK, Kim HR (2009) Isolation and identification of phlorotannins from Ecklonia stolonifera with antioxidant and anti-inflammatory properties. J Agric Food Chem 57:3483–3489

    Article  CAS  PubMed  Google Scholar 

  • Koleva II, Van Beek TA, Linssen JPH, Groot AD, Evstatieva LN (2002) Screening of plant extracts for antioxidant activity: a comparative study on three testing methods. Phytochem Anal 13:8–17

    Article  CAS  PubMed  Google Scholar 

  • Kornprobst JM (2010) Encyclopedia of marine natural products. Wiley-Blackwell, Weinheim

  • Lautenschlager S, Wulf HC, Pittelkow MR (2007) Photoprotection. Lancet 370:528–537

    Article  CAS  PubMed  Google 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 56:238–245

    Article  Google Scholar 

  • Le Lann K, Connan S, Stiger-Pouvreau V (2012a) Phenology, TPC and size-fractioning phenolics variability in temperate Sargassaceae (Phaeophyceae, Fucales) from Western Brittany: native vs. introduced species. Mar Environ Res 80:1–11

    Article  PubMed  Google 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 60:37–50

    Article  Google Scholar 

  • Li Y-X, Wijesekara I, Li Y, Kim S-K (2011) Phlorotannins as bioactive agents from brown algae. Process Biochem 46:2219–2224

    Article  CAS  Google 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):1102–1109

  • Lohézic-Le Dévéhat F, Legouin B, Couteau C, Boustie J, Coiffard L (2013) Lichenic extracts and metabolites as UV filters. J Photochem Photobiol B 120:17–28

    Article  PubMed  Google Scholar 

  • McInnes AG, Ragan MA, Smith DG, Walter JA (1984) High-molecular-weight phloroglucinol-based tannins from brown algae: structural variants. Hydrobiologia 116-117:597–602

    Article  CAS  Google 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 1428:115–125

    Article  CAS  PubMed  Google Scholar 

  • Nagayama K, Iwamura Y, Shibata T, Hirayama I, Nakamura T (2002) Bactericidal activity of phlorotannins from the brown alga Ecklonia kurome. J Antimicrob Chemother 50:889–893

    Article  CAS  PubMed  Google Scholar 

  • Parys S, Kehraus S, Pete R, Küpper FC, Glombitza KW, König GM (2009) Seasonal variation of polyphenolics in Ascophyllum nodosum (Phaeophyceae). Eur J Phycol 44:331–338

    Article  CAS  Google 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 71:221–229

    Article  CAS  PubMed  Google Scholar 

  • Pavia H, Brock E (2000) Extrinsic factors influencing phlorotannin production in the brown alga Ascophyllum nodosum. Mar Ecol Process Ser 193:285–294

    Article  CAS  Google Scholar 

  • Ragan MA, Glombitza K-W (1986) Phlorotannins, brown algal polyphenols. Prog Phycol Res 4:129–241

    CAS  Google Scholar 

  • Rancan F, Rosan S, Boehm K, Fernández E, Hidalgo ME, Quihot W, Rubio C, Boehm F, Piazena H, Oltmanns U (2002) Protection against UVB irradiation by natural filters extracted from lichens. J Photochem Photobiol B 68:133–139

    Article  CAS  PubMed  Google Scholar 

  • Saewan N, Jimtaisong A (2015) Natural products as photoprotection. J Cosmet Dermatol 14:47–63

    Article  PubMed  Google Scholar 

  • Sambandan DR, Ratner D (2011) Sunscreens: an overview and update. J Am Acad Dermatol 64:748–758

    Article  CAS  PubMed  Google Scholar 

  • Sattler E, Glombitza K-W, Wehrli FW, Eckhardt G (1977) Antibiotica aus algen—XVI : Polyhydroxyphenyläther aus der Phaeophycee Halidrys siliquosa. Tetrahedron 33:1239–1244

    Article  CAS  Google Scholar 

  • Schoenwaelder MEA (2002) The occurrence and cellular significance of physodes in brown algae. Phycologia 41:125–139

    Article  Google Scholar 

  • Shibata T, Nagayama K, Sugiura S, Makino S, Ueda M, Tamaru Y (2015) Analysis on composition and antioxidative properties of phlorotannins isolated from Japanese Eisenia and Ecklonia species. Am J Plant Sci 06:2510–2521

    Article  CAS  Google Scholar 

  • Singh IP, Bharate SB (2006) Phloroglucinol compounds of natural origin. Nat Prod Rep 23:558–591

    Article  CAS  Google Scholar 

  • Smith AH, Imlay JA, Mackie RI (2003) Increasing the oxidative stress response allows Escherichia coli to overcome inhibitory effects of condensed tannins. Appl Environ Microbiol 69:3406–3411

    Article  CAS  PubMed  PubMed Central  Google 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: 379–411

  • 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 143:52–60

    Article  CAS  PubMed  Google Scholar 

  • Swanson AK, Druehl LD (2002) Induction, exudation and the UV protective role of kelp phlorotannins. Aquat Bot 73:241–253

    Article  CAS  Google 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 26:1215–1230

    CAS  Google Scholar 

  • Thomas P, Swaminathan A, Lucas RM (2012) Climate change and health with an emphasis on interactions with ultraviolet radiation: a review. Glob Change Biol 18:2392–2405

    Article  Google Scholar 

  • Turkmen N, Velioglu YS, Sari F, Polat G (2007) Effect of extraction conditions on measured total polyphenol contents and antioxidant and antibacterial activities of black tea. Molecules 12:484–496

    Article  CAS  PubMed  Google Scholar 

  • Wang T, Jónsdóttir R, Olafsdóttir G (2009) Total phenolic compounds, radical scavenging and metal chelation of extracts from Icelandic seaweeds. Food Chem 116:240–248

    Article  CAS  Google Scholar 

  • Wang T, Jónsdóttir R, Liu H, Gu L, Kristinsson HG, Raghavan S, Ólafsdóttir G (2012) Antioxidant capacities of phlorotannins extracted from the brown algae Fucus vesiculosus. J Agric Food Chem 60:5874–5883

    Article  CAS  PubMed  Google Scholar 

  • Zhu QY, Hackman RM, Ensunsa JL, Holt RR, Keen CL (2002) Antioxidative activities of oolong tea. J Agric Food Chem 50:6929–6934

    Article  CAS  PubMed  Google Scholar 

  • Zubia M, Fabre MS, Kerjean V, Le Lann K, Stiger-Pouvreau V, Fauchon M, Deslandes E (2009) Antioxidant and antitumoural activities of some Phaeophyta from Brittany coasts. Food Chem 116:693–701

    Article  CAS  Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. European Institute of Marine Studies (IUEM), LEMAR UMR 6539 UBO CNRS Ifremer IRD, Université de Bretagne Occidentale (UBO), Technopôle Brest-Iroise, 29280, Plouzané, France

    Klervi Le Lann, Gwladys Surget, Fabienne Guérard, Nathalie Poupart & Valérie Stiger-Pouvreau

  2. Faculty of Pharmacy, Université de Nantes, Nantes Atlantique Universités, LPiC, MMS, EA2160, 9 rue Bias, BP 53508, 44 000, Nantes, France

    Céline Couteau & Laurence Coiffard

  3. RMN - RPE - MS, Université de Bretagne Occidentale (UBO), 6 avenue, Victor-Le-Gorgeu-CS93837, 29238, Brest Cedex 3, France

    Stéphane Cérantola

  4. Plateforme de spectrométrie de masse MétaboMER, CNRS, FR2424, Station Biologique, Place Georges Teissier, BP 74, 29682, Roscoff Cedex, France

    Fanny Gaillard

  5. Laboratoires Science et Mer, Venelle du Carros, CS 70002, 29480, Le Relecq-Kerhuon, France

    Maud Larnicol

  6. EIO UMR 244, Université de la Polynésie française, LabEx CORAIL, B.P. 6570, 98702, Faa’a, Tahiti, Polynésie française

    Mayalen Zubia

Authors
  1. Klervi Le Lann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gwladys Surget
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Céline Couteau
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Laurence Coiffard
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stéphane Cérantola
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fanny Gaillard
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Maud Larnicol
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mayalen Zubia
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Fabienne Guérard
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Nathalie Poupart
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Valérie Stiger-Pouvreau
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Klervi Le Lann.

Ethics declarations

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.

Authors’ contributions

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.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Le Lann, K., Surget, G., Couteau, C. et al. Sunscreen, antioxidant, and bactericide capacities of phlorotannins from the brown macroalga Halidrys siliquosa . J Appl Phycol 28, 3547–3559 (2016). https://doi.org/10.1007/s10811-016-0853-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-016-0853-0

Keywords

Search

Navigation