Journal of Applied Phycology

, Volume 27, Issue 4, pp 1599–1605 | Cite as

Phenolic profiles, antioxidant capacity, and acetylcholinesterase inhibitory activity of eight South African seaweeds

  • Kannan R. R. Rengasamy
  • Stephen O. Amoo
  • Adeyemi O. Aremu
  • Wendy A. Stirk
  • Jiří Gruz
  • Michaela Šubrtová
  • Karel Doležal
  • Johannes Van Staden


In the search for new, safe, and natural sources as antioxidant and acetylcholinesterase (AChE) inhibitors, eight seaweeds were collected from the intertidal region in KwaZulu-Natal, South Africa and screened. Their total phenolic, flavonoid, and condensed tannin contents were determined, and the specific phenolic acids were identified. The highest total phenolics, flavonoids, and condensed tannin were recorded in Rhodomelopsis africana (7.89 mg gallic acid equivalents g−1), Halimeda cuneata (3.64 mg catechin equivalents g−1), and Codium duthieae (0.60 mg cyanide chloride equivalents g−1), respectively. Based on UHPLC-MS/MS, different concentrations of protocatechuic acid, p-hydroxybenzoic acid, and m-hydroxybenzoic acid were quantified in the seaweeds. The highest radical scavenging ability and oxygen radical absorbance capacity (ORAC) were observed in red Gelidium foliaceum (52.2 %) and green C. duthieae (44 μmol TE g−1), respectively. In terms of AChE inhibition, the green H. cuneata exhibited greatest bioactivity (IC50 = 70 μg mL−1). Overall, the findings suggest that these seaweeds could be potential candidates as new sources of natural antioxidant and AChE inhibitors.


Alzheimer’s disease AChE inhibitors Phenolics Macroalgae UHPLC-MS/MS 



RRRK, SOA, and AOA thank the National Research Foundation, Claude Leon Foundation, and the University of KwaZulu-Natal for support in the form of postdoctoral fellowships. We also acknowledge the support of the Ministry of Education, Youth and Sports, Czech Republic (Grant L01204 from the National Program of Sustainability Land Agricultural Research), and IGA of Palacký University (Grant PrF 2013 012).


  1. Bolton JJ, Stegenga H (2002) Seaweed species diversity in South Africa. S Afr J Mar Sci 24:9–18CrossRefGoogle Scholar
  2. De Clerck O, Bolton JJ, Anderson RJ, Coppejans E (2005) Guide to the seaweeds of KwaZulu-Natal. Meise, National Botanic Garden of Belgium, 33, pp. 294Google Scholar
  3. De Souza ET, De Lira DP, Queiroz AC, Da Silva JC, De Aquino AB, Campessato Mella EA, Lorenzo VP, Miranda GEC, De Araujo-Junior JX, De Oliveira Chaves MC, Barbosa-Filho JM, De Athavde-Filho PF, De Oliveira Santos BV, Alexandre-Moreira MS (2009) The antinociceptive and anti-inflammatory activities of caulerpin, a bisindole alkaloid isolated from seaweeds of the genus Caulerpa. Mar Drugs 7:689–704PubMedCentralPubMedCrossRefGoogle Scholar
  4. Dellai A, Laajili S, Morvan VL, Robert J, Bouraoui A (2013) Antiproliferative activity and phenolics of the Mediterranean seaweed Laurencia obusta. Ind Crop Prod 47:252–255CrossRefGoogle Scholar
  5. Díaz E, Güldenzoph C, Molis M, McQuaid C, Wahl M (2006) Variability in grazer-mediated defensive responses of green and red macroalgae on the south coast of South Africa. Mar Biol 149:1301–1311CrossRefGoogle Scholar
  6. Dixon RA, Xie D-Y, Sharma SB (2005) Proanthocyanidins—a final frontier in flavonoid research? New Phytol 165:9–28PubMedCrossRefGoogle Scholar
  7. Elgorashi EE, Stafford GI, Van Staden J (2004) Acetylcholinesterase enzyme inhibitory effects of Amaryllidaceae alkaloids. Planta Med 70:260–262PubMedCrossRefGoogle Scholar
  8. Ellman GL, Coutney D, Andies V, Featherstone RM (1961) A new and rapid colourimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95PubMedCrossRefGoogle Scholar
  9. Emiliani G, Fondi M, Fani R, Gribaldo S (2009) A horizontal gene transfer at the origin of phenylpropanoid metabolism: a key adaptation of plants to land. Biol Direct 4:1–12CrossRefGoogle Scholar
  10. Fawole OA, Amoo SO, Ndhlala AR, Light ME, Finnie JF, Van Staden J (2010) Anti-inflammatory, acetylcholinesterase, antioxidant and phytochemical properties of medicinal plants used for pain-related ailments in South Africa. J Ethnopharmacol 127:235–241PubMedCrossRefGoogle Scholar
  11. Ganesan K, Suresh Kumar K, Subba Rao PV (2011) Comparative assessment of antioxidant activity in three edible species of green seaweed, Enteromorpha from Okha, Northwest coast of India. Innov Food Sci Emerg Technol 12:73–78CrossRefGoogle Scholar
  12. Gruz J, Novák O, Strnad M (2008) Rapid analysis of phenolic acids in beverages by UPLC–MS/MS. Food Chem 111:789–794CrossRefGoogle Scholar
  13. Guinea M, Franco V, AraujoBazan L, Rodriguez-Martin I, Gonzalez S (2012) In vivo UVB-photoprotective activity of extracts from commercial marine macroalgae. Food Chem Toxicol 50:1109–1117PubMedCrossRefGoogle Scholar
  14. Gülçin İ (2012) Antioxidant activity of food constituents: an overview. Arch Toxicol 86:345–391PubMedCrossRefGoogle Scholar
  15. Güven KC, Percot A, Sezik E (2010) Alkaloids in marine algae. Mar Drugs 8:269–284PubMedCentralPubMedCrossRefGoogle Scholar
  16. Halpin CM, Reilly C, Walsh JJ (2010) Nature’s anti-Alzheimer’s drugs: isolation and structure elucidation of galantamine from Leucojum aestivum. J Chem Edu 87:1242–1243CrossRefGoogle Scholar
  17. Hodges JR (2006) Alzheimer’s centennial legacy: origins, landmarks and the current status of knowledge concerning cognitive aspects. Brain 129:2811–2822PubMedCrossRefGoogle Scholar
  18. Huang D, Ou B, Prior RL (2005) The chemistry behind antioxidant capacity assays. J Agric Food Chem 53:1841–1856PubMedCrossRefGoogle Scholar
  19. Hudson JB, Kim JH, Lee MK, De Wreede RE, Hong YK (1999) Antiviral compounds in extracts of Korean seaweeds: evidence for multiple activities. J Appl Phycol 10:427–434CrossRefGoogle Scholar
  20. Kannan RRR, Aderogba M, Amoo SO, Stirk WA, Van Staden J (2013a) Potential antiradical and alpha glucosidase inhibitors from Ecklonia maxima. Food Chem 141:1412–1415CrossRefGoogle Scholar
  21. Kannan RRR, Aderogba MA, Ndhlala AR, Stirk WA, Van Staden J (2013b) Acetylcholinesterase inhibitory activity of phlorotannins isolated from the brown alga, Ecklonia maxima (Osbeck) Papenfuss. Food Res Int 54:1250–1254CrossRefGoogle Scholar
  22. Karioti A, Hadjipavlou-Litina D, Mensah MLK, Fleischer TC, Skaltsa H (2004) Composition and antioxidant activity of the essential oil of Xylopia aethiopica (Dun) A. Rich. (Annonaceae) leaves, stem bark, root bark and fresh and dried fruits, growing in Ghana. J Agric Food Chem 52:8094–8098PubMedCrossRefGoogle Scholar
  23. Kumar M, Kumari P, Trivedi N, Shukla MK, Gupta V, Reddy CRK, Jha B (2011) Minerals, PUFAs and antioxidant properties of some tropical seaweeds from Sourashtra coast of India. J Appl Phycol 23:797–810Google Scholar
  24. Makkar HPS (2000) Quantification of tannins in tree foliage: a laboratory manual for the FAO/IAEA co-ordinated research project on “use of nuclear and related techniques to develop simple tannin assays for predicting and improving the safety and efficiency of feeding ruminants on tanniniferous tree foliage”. Joint FAO/IAEA Division of Nuclear Techniques in Food and Agriculture, Vienna, AustriaGoogle Scholar
  25. Matkowski A (2008) Plant in vitro culture for the production of antioxidants—a review. Biotechnol Adv 26:548–560PubMedCrossRefGoogle Scholar
  26. Mayer A, Hamann MT (2002) Marine pharmacology in 1999: compounds with antibacterial, anticoagulant, antifungal, anthelmintic, anti-inflammatory, antiplatelet, antiprotozoal and antiviral activities affecting the cardiovascular, endocrine, immune and nervous systems, and other miscellaneous mechanisms of action. Comp Biochem Physiol C: Toxicol Pharmacol 132:315–339CrossRefGoogle Scholar
  27. McHugh D (2003) A guide to the seaweed industry. FAO Fisheries Technical Paper No 441Google Scholar
  28. Moosmann B, Behl C (2002) Antioxidants as treatment for neurodegenerative disorders. Expert Opin Investig Drugs 11:1407–1435PubMedCrossRefGoogle Scholar
  29. Nair JJ, Aremu AO, Van Staden J (2011) Isolation of narciprimine from Cyrtanthus contactus (Amaryllidaceae) and evaluation of its acetylcholinesterase inhibitory activity. J Ethnopharmacol 137:1102–1106PubMedCrossRefGoogle Scholar
  30. Ndhlala AR, Aremu AO, Moyo M, Amoo SO, Van Staden J (2012) Acetylcholinesterase inhibitors from plant sources: friends or foes? In: White CJ, Tait JE (eds) Cholinesterase: production, uses and health effects. Nova, New York, pp 67–98Google Scholar
  31. Nuissier G, Rezzonico R, Grignon-Dubois M (2010) Chicoric acid from Syringodium filiforme. Food Chem 120:783–788CrossRefGoogle Scholar
  32. Ou B, Hampsch-Woodill M, Prior RL (2001) Development and validation of an improved oxygen radical absorbance capacity assay using fluorescein as the fluorescent probe. J Agric Food Chem 49:4619–4626PubMedCrossRefGoogle Scholar
  33. Pangestuti R, Kim SK (2011) Neuroprotective effects of marine algae. Mar Drugs 9:803–818PubMedCentralPubMedCrossRefGoogle Scholar
  34. Sabeena Farvin KH, Jacobsen C (2013) Phenolic compounds and antioxidant activities of selected species of seaweeds from Danish coast. Food Chem 138:1670–1681PubMedCrossRefGoogle Scholar
  35. Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158Google Scholar
  36. Sramek JJ, Frackiewicz EJ, Cutler NR (2000) Review of the acetylcholinesterase inhibitor galanthamine. Expert Opin Investig Drugs 9:2393–2402PubMedCrossRefGoogle Scholar
  37. Stirk WA, Reinecke DL, Van Staden J (2007) Seasonal variation in antifungal, antibacterial and acetylcholineesterase activity in seven South African seaweeds. J Appl Phycol 19:271–276Google Scholar
  38. Su JY, Xu XH, Zeng LM, Wang MY, Lu N, Lu Y, Zhang QT (1998) Sym-triazine derivative from Halimeda xishaensis. Phytochemistry 48:583–584CrossRefGoogle Scholar
  39. Wildermuth MC (2006) Variations on a theme: synthesis and modification of plant benzoic acids. Curr Opin Plant Biol 9:288–296PubMedCrossRefGoogle Scholar
  40. Yan X, Nagata T, Fan X (1998) Antioxidative activities in some common seaweeds. Plant Foods Hum Nutr 52:253–262PubMedCrossRefGoogle Scholar
  41. Yoshie Y, Wang W, Hsieh YP, Suzuki T (2002) Compositional difference of phenolic compounds between two seaweeds, Halimeda spp. J Tokyo Univ Fish 88:21–24Google Scholar
  42. Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Kannan R. R. Rengasamy
    • 1
  • Stephen O. Amoo
    • 1
  • Adeyemi O. Aremu
    • 1
  • Wendy A. Stirk
    • 1
  • Jiří Gruz
    • 2
  • Michaela Šubrtová
    • 2
  • Karel Doležal
    • 2
  • Johannes Van Staden
    • 1
  1. 1.Research Centre for Plant Growth and Development, School of Life SciencesUniversity of KwaZulu-Natal PietermaritzburgScottsvilleSouth Africa
  2. 2.Laboratory of Growth Regulators & Department of Chemical Biology and Genetics, Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of SciencePalacký University & Institute of Experimental Botany AS CROlomoucCzech Republic

Personalised recommendations