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

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Abstract

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.

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References

  • Bolton JJ, Stegenga H (2002) Seaweed species diversity in South Africa. S Afr J Mar Sci 24:9–18

    Article  Google Scholar 

  • 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. 294

  • 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 7:689–704

    Article  PubMed Central  PubMed  Google Scholar 

  • Dellai A, Laajili S, Morvan VL, Robert J, Bouraoui A (2013) Antiproliferative activity and phenolics of the Mediterranean seaweed Laurencia obusta. Ind Crop Prod 47:252–255

    Article  CAS  Google Scholar 

  • 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 149:1301–1311

    Article  Google Scholar 

  • Dixon RA, Xie D-Y, Sharma SB (2005) Proanthocyanidins—a final frontier in flavonoid research? New Phytol 165:9–28

    Article  CAS  PubMed  Google Scholar 

  • Elgorashi EE, Stafford GI, Van Staden J (2004) Acetylcholinesterase enzyme inhibitory effects of Amaryllidaceae alkaloids. Planta Med 70:260–262

    Article  CAS  PubMed  Google Scholar 

  • Ellman GL, Coutney D, Andies V, Featherstone RM (1961) A new and rapid colourimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  CAS  PubMed  Google Scholar 

  • 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 4:1–12

    Article  Google Scholar 

  • 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 127:235–241

    Article  CAS  PubMed  Google Scholar 

  • 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 12:73–78

    Article  CAS  Google Scholar 

  • Gruz J, Novák O, Strnad M (2008) Rapid analysis of phenolic acids in beverages by UPLC–MS/MS. Food Chem 111:789–794

    Article  CAS  Google Scholar 

  • 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 50:1109–1117

    Article  CAS  PubMed  Google Scholar 

  • Gülçin İ (2012) Antioxidant activity of food constituents: an overview. Arch Toxicol 86:345–391

    Article  PubMed  Google Scholar 

  • Güven KC, Percot A, Sezik E (2010) Alkaloids in marine algae. Mar Drugs 8:269–284

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 87:1242–1243

    Article  CAS  Google Scholar 

  • Hodges JR (2006) Alzheimer’s centennial legacy: origins, landmarks and the current status of knowledge concerning cognitive aspects. Brain 129:2811–2822

    Article  PubMed  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 

  • 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 10:427–434

    Article  Google Scholar 

  • Kannan RRR, Aderogba M, Amoo SO, Stirk WA, Van Staden J (2013a) Potential antiradical and alpha glucosidase inhibitors from Ecklonia maxima. Food Chem 141:1412–1415

    Article  Google Scholar 

  • 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 54:1250–1254

    Article  CAS  Google Scholar 

  • 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 52:8094–8098

    Article  CAS  PubMed  Google Scholar 

  • 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 23:797–810

  • 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, Austria

  • Matkowski A (2008) Plant in vitro culture for the production of antioxidants—a review. Biotechnol Adv 26:548–560

    Article  CAS  PubMed  Google Scholar 

  • 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 132:315–339

    Article  Google Scholar 

  • McHugh D (2003) A guide to the seaweed industry. FAO Fisheries Technical Paper No 441

  • Moosmann B, Behl C (2002) Antioxidants as treatment for neurodegenerative disorders. Expert Opin Investig Drugs 11:1407–1435

    Article  CAS  PubMed  Google Scholar 

  • Nair JJ, Aremu AO, Van Staden J (2011) Isolation of narciprimine from Cyrtanthus contactus (Amaryllidaceae) and evaluation of its acetylcholinesterase inhibitory activity. J Ethnopharmacol 137:1102–1106

    Article  CAS  PubMed  Google Scholar 

  • 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 67–98

    Google Scholar 

  • Nuissier G, Rezzonico R, Grignon-Dubois M (2010) Chicoric acid from Syringodium filiforme. Food Chem 120:783–788

    Article  CAS  Google Scholar 

  • 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 49:4619–4626

    Article  CAS  PubMed  Google Scholar 

  • Pangestuti R, Kim SK (2011) Neuroprotective effects of marine algae. Mar Drugs 9:803–818

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sabeena Farvin KH, Jacobsen C (2013) Phenolic compounds and antioxidant activities of selected species of seaweeds from Danish coast. Food Chem 138:1670–1681

    Article  CAS  PubMed  Google Scholar 

  • Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158

    CAS  Google Scholar 

  • Sramek JJ, Frackiewicz EJ, Cutler NR (2000) Review of the acetylcholinesterase inhibitor galanthamine. Expert Opin Investig Drugs 9:2393–2402

    Article  CAS  PubMed  Google Scholar 

  • Stirk WA, Reinecke DL, Van Staden J (2007) Seasonal variation in antifungal, antibacterial and acetylcholineesterase activity in seven South African seaweeds. J Appl Phycol 19:271–276

  • Su JY, Xu XH, Zeng LM, Wang MY, Lu N, Lu Y, Zhang QT (1998) Sym-triazine derivative from Halimeda xishaensis. Phytochemistry 48:583–584

    Article  CAS  Google Scholar 

  • Wildermuth MC (2006) Variations on a theme: synthesis and modification of plant benzoic acids. Curr Opin Plant Biol 9:288–296

    Article  CAS  PubMed  Google Scholar 

  • Yan X, Nagata T, Fan X (1998) Antioxidative activities in some common seaweeds. Plant Foods Hum Nutr 52:253–262

    Article  CAS  PubMed  Google Scholar 

  • Yoshie Y, Wang W, Hsieh YP, Suzuki T (2002) Compositional difference of phenolic compounds between two seaweeds, Halimeda spp. J Tokyo Univ Fish 88:21–24

    Google Scholar 

  • Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559

    Article  CAS  Google Scholar 

Download references

Acknowledgments

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).

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Authors and Affiliations

  1. Research Centre for Plant Growth and Development, School of Life Sciences, University of KwaZulu-Natal Pietermaritzburg, Private Bag X01, Scottsville, 3209, South Africa

    Kannan R. R. Rengasamy, Stephen O. Amoo, Adeyemi O. Aremu, Wendy A. Stirk & Johannes Van Staden

  2. Laboratory of Growth Regulators & Department of Chemical Biology and Genetics, Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of Science, Palacký University & Institute of Experimental Botany AS CR, Šlechtitelů 11, 783 71, Olomouc, Czech Republic

    Jiří Gruz, Michaela Šubrtová & Karel Doležal

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  1. Kannan R. R. Rengasamy
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  2. Stephen O. Amoo
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  3. Adeyemi O. Aremu
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  4. Wendy A. Stirk
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  5. Jiří Gruz
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  7. Karel Doležal
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  8. Johannes Van Staden
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Correspondence to Johannes Van Staden.

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Rengasamy, K.R.R., Amoo, S.O., Aremu, A.O. et al. Phenolic profiles, antioxidant capacity, and acetylcholinesterase inhibitory activity of eight South African seaweeds. J Appl Phycol 27, 1599–1605 (2015). https://doi.org/10.1007/s10811-014-0438-8

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  • DOI: https://doi.org/10.1007/s10811-014-0438-8

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