Skip to main content

Biochemical and antiviral activities of enzymatic hydrolysates from different invasive French seaweeds

Journal of Applied Phycology volume 26, pages 1029–1042 (2014)Cite this article

Abstract

Proliferations of green, brown and red algae appear in shallow sandy bays in North Brittany (France), and they represent a real economic constraint for the affected communities. In addition to the nuisance for residents and tourist activity, the communities must carry out systematic collection. The collected algae are spread on agricultural land spreading or composted, but these solutions reach their limits rapidly, bringing little added value to the collected algae. Seaweeds are potentially excellent sources of bioactive metabolites that could represent useful leads in the development of new functional ingredients in pharmaceutical and cosmetic industries. The aim of this study was to propose the use of an enzyme-assisted extraction as a tool to improve the extraction efficiency of antiviral compounds from three invasive French seaweeds. We selected the red Solieria chordalis, the green Ulva sp. and the brown Sargassum muticum as models for these experiments. In comparison with water extraction at 50 °C for the same time of treatment, enzymatic hydrolysis increased the yields. The data suggest the potential of enzymatic hydrolysis for producing active fractions in the function of the algal biomass, the behaviour of the cell wall, the selectivity and the action of the enzyme. Enzymatic hydrolysis appeared less effective for polyphenol recovery, but was a promising softer technique for recovering proteins, neutral sugars, uronic acids and sulphate groups. The solvent-free process, higher extraction rate and higher yields, coupled to time-saving and lower cost, make this method economical and sustainable. By using a cell viability assay, all hydrolysate fractions tested were shown to be non-toxic to Vero cells. After 3 days of treatment, no microscopically visible alteration of normal cell morphology was observed even at 500 μg mL−1. S. chordalis extracts have an effective antiviral activity with EC50 between 23.0 and 101.1 μg mL−1 at a multiplicity of infection of 0.001 ID50/cells; 100 % and 98 % cellular protection were obtained for 500 μg mL−1 of hydrolysate extracts carbohydrase C3 and blank, respectively. Other extracts from S. chordalis inhibited viral production less effectively.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Ahn CB, Jeon YJ, Kang DS, Shin TS, Jung BM (2004) Free radical scavenging activity of enzymatic extracts from a brown seaweed Scytosiphon lomentaria by electron spin resonance spectrometry. Food Res Int 37:253–258

    Article  CAS  Google Scholar 

  • Amano H, Noda H (1990) Proteins of protoplasts from red alga Porphyra yezoensis. Nippon Suisan Gakkaishi 56:1859–1864

    Article  CAS  Google Scholar 

  • Amano H, Noda H (1992) Proteins of protoplasts from several seaweeds. Nippon Suisan Gakkaishi 58:291–299

    Article  CAS  Google Scholar 

  • Arzel P (1987) Les Goémoniers. Le Chasse-Marée, Editions de l’estran. Douarnez, France, 305 pp

    Google Scholar 

  • Arzel P (2000) Sur la route des Algues, les goémoniers. Patrimoine maritime de Bretagne. Ed. Uhel Izel, 65 pp

  • Arzel P, Barbaroux O (2003) Les Algues, produits, saveurs et santé de la mer. Ed. Libris, 104 pp

  • Athukorala Y, Jung WK, Vasanthan T, Jeon YJ (2006) An anticoagulative polysaccharide from an enzymatic hydrolysate of Ecklonia cava. Carbohydr Polym 66:184–191

    Article  CAS  Google Scholar 

  • Athukorala Y, Lee KW, Kim SK, Jeon YJ (2007) Anticoagulant activity of marine green and brown algae collected from Jeju Island in Korea. Bioresour Technol 98:1711–1716

    Article  CAS  PubMed  Google Scholar 

  • Bergé JP, Bourgougnon N, Alban S, Pojer F, Chermann JC, Billaudel S, Robert JM, Durand P, Franz G (1999) Antiviral and anticoagulant activities of a water soluble compound extracted from the marine diatom Haslea ostrearia. Planta Med 65:604–609

    Article  PubMed  Google Scholar 

  • Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489

    Article  CAS  PubMed  Google Scholar 

  • Bondu S, Deslandes E, Fabre MS, Berthou C, Guangli Y (2010) Carrageenan from Solieria chordalis (Gigartinales): structural analysis and immunological activities of the low molecular weight fractions. Carbohydr Polymers 81:448–460

    Google Scholar 

  • Borines MG, de Leon RL, Cuello JL (2013) Bioethanol production from the macroalgae Sargassum spp. Bioresour Technol 138:22–29

    Article  CAS  PubMed  Google Scholar 

  • Bouhlal R, Riadi H, Bourgougnon N (2010) Antiviral activities of Morocco seaweeds extracts. Afr J Biotechnol 9:7968–7975

    Google Scholar 

  • Bouhlal R, Haslin C, Chermann JC, Colliec-Jouault S, Sinquin C, Simon G, Cerantola S, Riadi H, Bourgougnon N (2011) Antiviral activities of sulfated polysaccharides isolated from Sphaerococcus coronopifolius (Rhodophytha, Gigartinales) and Boergeseniella thuyoides (Rhodophyta, Ceramiales). Mar Drugs 7:1187–1209

    Article  Google Scholar 

  • Bourgougnon N (2003) Anti-HIV compounds from red seaweeds. In: Fingerman M, Nagabhushanam R (eds) Biomaterials and bioprocessing, vol 9, Recent advances in marine biotechnology. Science, Enfield, pp 16–206

    Google Scholar 

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

    Chapter  Google Scholar 

  • Bourgougnon N, Lahaye M, Chermann JC, Kornprobst JM (1993) Composition and antiviral activities of sulfated polysaccharide from Schizymenia dubyi (Rhodophyta, Gigartinales). Bioorg Med Chem Lett 3:1141–1146

    Article  CAS  Google Scholar 

  • Cardozo KHM, Guaratini T, Barros MP (2007) Metabolites from algae with economical impact Comp. Biochem Physiol C 146:60–78

    Article  Google Scholar 

  • Castro R, Piazzon MC, Zarra I, Leiro J, Noya M, Lamas J (2006) Stimulation of turbot phagocytes by Ulva rigida C. Agardh polysaccharides. Aquaculture 254:9–20

    Article  CAS  Google Scholar 

  • Cian RE, Martínez-Augustin O, Drago SR (2012) Bioactive properties of peptides obtained by enzymatic hydrolysis from protein byproducts of Porphyra columbina. Food Res Internat 49:364–372

    Article  CAS  Google Scholar 

  • Crooke WM, Simpson WE (1971) Determination of ammonium in Kjeldahl digests of crops by an automated procedure. J Agric Food Chem 27:1256–1262

    Google Scholar 

  • Damonte EB, Matulewicz MC, Cerezo AS (2004) Sulfated seaweed polysaccharides as antiviral agents. Curr Med Chem 11:2399–2419

    Article  CAS  PubMed  Google Scholar 

  • Demais H, Brendle J, Jaber M, Laza Anca L (2006a) Exfoliating an intercalated clay, useful in e.g. animal/human feeds, plastification, surface coatings and in nanocomposite, comprises preparing intercalated clay from clay and intercalating compound and lyophilizing in presence of water. French Patent FR2882997

  • Demais H, Brendle J, Le Deit H, Laza Anca L, Lurton L, Brault D (2006b) Interspersed clay. PCT Patent Application WO2006030075

  • Dizerbo AH, Herpé E (2007) Liste et répartition des algues marines des côtes françaises de la Manche et de l'Atlantique Iles Normandes incluses Éditions Anaximandre Landernau, 315 pp

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    Article  CAS  Google Scholar 

  • Dumay J, Clément N, Morançais M, Fleurence J (2013) Optimization of hydrolysis conditions of Palmaria palmata to enhance R-phycoerythrin extraction. Bioresour Technol 131:21–27

    Article  CAS  PubMed  Google Scholar 

  • El Gamal AA (2010) Biological importance of marine algae. Saudi Pharm J 18:1–25

    Article  PubMed Central  PubMed  Google Scholar 

  • Fleurence J (1999) Seaweed proteins: biochemical, nutritional aspects and potential uses. Trends Food Sci Technol 10:25–28

    Article  CAS  Google Scholar 

  • Fleurence J, Massiani L, Guyader O, Mabeau S (1995a) Use of enzymatic cell wall degradation for improvement of protein extraction from Chondrus crispus, Gracilaria verrucosa and Palmaria palmata. J Appl Phycol 7:393–395

    Article  CAS  Google Scholar 

  • Fleurence J, Le Cœur C, Mabeau S, Maurice M, Landrein A (1995b) Comparison of different extractive procedures for proteins from the edible seaweeds Ulva rigida and Ulva rotundata. J Appl Phycol 7:577–582

    Article  CAS  Google Scholar 

  • Fleurence J, Morançais M, Dumay J, Decottignies P, Turpin V, Munier M, Garcia-Bueno N, Jaouen P (2012) What are the prospects for using seaweed in human nutrition and for marine animals raised through aquaculture? Trends Food Sci Technol 27:57–61

    Article  CAS  Google Scholar 

  • Hansen HR, Hector BL, Feldmann J (2003) A qualitative and quantitative evaluation of the seaweed diet of North Ronaldsay sheep. Anim Feed Sci Technol 105:21–28

    Article  Google Scholar 

  • Harden EA, Hartline C, Falshaw R, Carnachan SM, Kern ER, Prichard MN (2009) Virucidal activity of polysaccharide extracts from four algal species against herpes simplex virus. Antivir Res 83:282–289

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Harnedy PA, FitzGerald RJ (2013) Extraction of protein from the macroalga Palmaria palmata. Food Sci Technol 51:375–382

    CAS  Google Scholar 

  • Heo SJ, Park EJ, Lee KW, Jeon YJ (2005) Anti oxidant activities of enzymatic extracts from brown seaweeds. Bioresour Technol 96:1613–1623

    Article  CAS  PubMed  Google Scholar 

  • Ioannou E, Roussis V (2009) Natural products from seaweeds. Springer, Berlin, pp 51–81

    Google Scholar 

  • Jaques LB, Ballieux RE, Dietrich CP, Kavanagh LW (1968) A microelectrophoresis method for heparin. Can J Physiol Pharmacol 46:351–360

    Article  CAS  PubMed  Google Scholar 

  • Khanzada AK, Kazi WSTG, Kabir S, Soofia S (2007) Antifungal activity, elemental analysis and determination of total protein of seaweed, Solieria robusta (Greville) Kylin from the coast of Karachi. Pak J Bot 39:931–937

    Google Scholar 

  • Lahaye M (1991) Marine algae as sources of fibres: determination of soluble and insoluble dietary fibre contents in some “sea vegetables”. J Sci Food Agric 54:587–594

    Article  CAS  Google Scholar 

  • Lahaye M, Robic A (2007) Structure and functional properties of ulvans, a polysaccharide from green seaweeds. Biomacromolecules 8:1765–1774

    Article  CAS  PubMed  Google Scholar 

  • Lahaye M, Vigouroux J (1992) Liquefaction of dulse (Palmaria palmata (L.) Kuntze) by a commercial enzyme preparation and purified endo-β-1,4-d-xylanase. J Appl Phycol 4:329–337

    Article  CAS  Google Scholar 

  • Langlois M, Allard JP, Nugier F, Aymard M (1986) A rapid and automated colorimetric assay for evaluating in the sensitivity of Herpes simplex strains to antiviral drugs. J Biol Stand 14:201–211

    Article  CAS  PubMed  Google Scholar 

  • Mayer AMS, Rodríguez AD, Berlinck RGS, Hamann MT (2007) Marine pharmacology in 2003–4: marine compounds with anthelmintic antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial, antiplatelet, antiprotozoal, antituberculosis, and antiviral activities; affecting the cardiovascular, immune and nervous systems, and other miscellaneous mechanisms of action. Comp Biochem Physiol C 145:553–581

    Google Scholar 

  • McLaren C, Ellis MN, Hunter GA (1983) A colorimetric assay or the measurement of the sensitivity of Herpes simplex viruses to antiviral agents. Antivir Res 3:223–234

    Article  CAS  PubMed  Google Scholar 

  • Mohamed S, Hashim SN, Rahman HA (2012) Seaweeds: a sustainable functional food for complementary and alternative therapy. Trends Food Sci Technol 23:83–96

    Article  CAS  Google Scholar 

  • Murakami K, Yamaguchi Y, Noda K, Fujii T, Shinohara N, Ushirokawa T, Sugawa-Katayama Y, Katayama M (2011) Seasonal variation in the chemical composition of a marine brown alga, Sargassum horneri (Turner) C. Agardh. J Food Compos Anal 24:231–236

    Article  CAS  Google Scholar 

  • Peña-Rodríguez A, Mawhinney TP, Ricque-Marie D, Cruz-Suárez LE (2011) Chemical composition of cultivated seaweed Ulva clathrata (Roth) C. Agardh. Food Chem 129:491–498

    Article  Google Scholar 

  • Plouguerné E, Le Lann K, Connan S, Jechoux G, Deslandes E, Stiger-Pouvreau V (2006) Spatial and seasonal variations in density, maturity, length and phenolic content of the invasive brown macroalga Sargassum muticum along the coast of Western Brittany (France). Aquat Bot 85:337–344

    Article  Google Scholar 

  • Ray B, Lahaye M (1995) Cell-wall polysaccharide from the marine green alga Ulva “rigida” (Ulvales, Chlorophyta)—extraction and chemical composition. Carbohydr Res 274:251–261

    Article  CAS  Google Scholar 

  • Robic A, Sassi JF, Lahaye M (2008) Impact of stabilization treatments of the green seaweed Ulva rotundata (Chlorophyta) on the extraction yield, the physico-chemical and rheological properties of ulvan. Carbohydr Polym 74:344–352

    Article  CAS  Google Scholar 

  • Samarakoon K, Jeon YJ (2012) Bio-functionalities of proteins derived from marine algae—a review. Food Res Int 48:948–960

    Article  CAS  Google Scholar 

  • Sassi AB, Harzallah-Skhiri F, Bourgougnon N, Aouni M (2008) Antiviral activity of some Tunisian medicinal plants against Herpes simplex virus type 1. Nat Prod Res 22:53–65

    Article  PubMed  Google Scholar 

  • Siriwardhana N, Kim KN, Lee KW, Kim SH, Ha JH, Song CB (2008) Optimisation of hydrophilic antioxidant extraction from Hizikia fusiformis by integrating treatments of enzymes, heat and pH control. Int J Food Sci Technol 43:587–596

    Article  CAS  Google Scholar 

  • Smith PK, Krohn RI, Hermanson GT, Mallia AK, Gartner FH, Provenzano MD, Fujimoto EK, Goeke NM, Olson BJ, Klenk DC (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85

    Article  CAS  PubMed  Google Scholar 

  • Stengel DB, Connan S, Popper ZA (2011) Algal chemodiversity and bioactivity: sources of natural variability and implications for commercial application. Biotech Adv 29:483–501

    Google Scholar 

  • Stern JL, Hagerman AE, Steinberg PD, Mason PK (1996) Phlorotannin–protein interactions. J Chem Ecol 22:1877–1899

    Article  CAS  PubMed  Google Scholar 

  • Tavennec M (2009) La gestion d’une problématique algale dans un secteur hautement touristique, la presqu’île de Rhuys. Masters Thesis, Université de Nantes, 107 pp

  • Turkmen N, Sari F, Velioglu YS (2005) The effect of cooking methods on total phenolics and antioxidant activity of selected green vegetables. Food Chem 93:713–718

    Article  CAS  Google Scholar 

  • Vo TS, Ngo DH, Ta QV, Kim SK (2011) Marine organisms as a therapeutic source against herpes simplex virus infection. Eur J Pharm Sci 44:11–20

    Article  CAS  PubMed  Google Scholar 

  • Wang T, Jónsdóttir R, Kristinsson HG, Hreggvidsson GO, Jónsson JÓ, Thorkelsson G, Ólafsdóttir G (2010) Enzyme-enhanced extraction of antioxidant ingredients from red algae Palmaria palmata. Food Sci Technol 43:1387–1393

    CAS  Google Scholar 

  • Wang X, Liu X, Wang G (2011) Two stage hydrolysis of invasive algal feedstock for ethanol fermentation. J Integr Plant Biol 53:246–253

    Article  CAS  PubMed  Google Scholar 

  • Wijesinghe WAJP, Jeon Y-J (2012) Enzyme-assistant extraction (EAE) of bioactive components: a useful approach for recovery of industrially important metabolites from seaweeds: a review. Fitoterapia 83:6–12

    Article  CAS  PubMed  Google Scholar 

  • Yaich H, Garna H, Besbes S, Paquot M, Blecker C, Attia H (2011) Chemical composition and functional properties of Ulva lactuca seaweed collected in Tunisia. Food Chem 128:895–901

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire de Biotechnologie et Chimie Marines, EA3884, UBS, IUEM, 56000, Vannes, France

    K. Hardouin, A-S. Burlot, A. Umami, G. Bedoux & N. Bourgougnon

  2. Fakultas Perikanan dan Ilmu Kelautan, Kampus Tembalang, Universitas Diponegoro, Semarang, Indonesia

    A. Umami & I. Widowati

  3. LEMAR (UMR 6539 CNRS UBO Ifremer IRD), Institut Universitaire Européen de la Mer (IUEM), Université de Bretagne Occidentale (UBO), Technopôle Brest-Iroise, 29280, Plouzané, France

    A. Tanniou & V. Stiger-Pouvreau

Authors
  1. K. Hardouin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A-S. Burlot
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Umami
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Tanniou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. V. Stiger-Pouvreau
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. I. Widowati
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. G. Bedoux
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. N. Bourgougnon
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. Bourgougnon.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Hardouin, K., Burlot, AS., Umami, A. et al. Biochemical and antiviral activities of enzymatic hydrolysates from different invasive French seaweeds. J Appl Phycol 26, 1029–1042 (2014). https://doi.org/10.1007/s10811-013-0201-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-013-0201-6

Keywords

  • Sargassum muticum
  • Solieria chordalis
  • Ulva sp
  • Hydrolysates
  • Protease
  • Carbohydrase
  • Antiherpetic activity