Skip to main content

Advertisement

Log in

Fatty acid composition, TLC screening, ATR-FTIR analysis, anti-cholinesterase activity, and in vitro cytotoxicity to A549 tumor cell line of extracts of 3 macroalgae collected in Madeira

  • Seaweed For Health Conference, Galway
  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

Three macroalgae collected at Madeira Island were included in this study to determine their potential for drug, nutraceutical, food, or supplement application. Fatty acid content was higher in Zonaria tournefortii (12.32 mg g−1 dw) with 16.58% of PUFAs, eicosapentaenoic acid (C20:5ω3), and arachidonic acid (20:4ω6) having concentrations of 2.59 and 1.17%, respectively. The anti-thrombogenic and anti-atherogenicity potential was higher for Z. tournefortii due to relevant fatty acids in the biochemical composition this macroalgae. Lipid classes were assessed in the lipid extract and neutral lipids (NL) were in higher yield in Asparagopsis taxiformis (51.16%) and lower in Z. tournefortii (26.96%). The glycolipids (GL) were between 36.03 and 16.11% in Z. tournefortii and Ulva lactuca. Phospholipids (PL) fraction varied from 35.91 and 31.60% in A. taxiformis and Z. tournefortii. TLC screening identified that U. lactuca contains phytol and cholesterol in its NL, digalactosyldiacylglycerol in its GL, and cardiolipin and L-α-phosphatidylcholine in its PL. Zonaria tournefortii contains phytol and cholesterol in its NL classes, and the PL classes contain L-α-phosphatidylethanolamine and 1-(3-sn-phosphatidyl)-rac-glycerol. The macroalgae A. taxiformis revealed cholesterol in its NL fraction and the same phospholipids as Z. tournefortii in its PL fraction. ATR-FTIR analysis enabled a “fingerprint” spectra and important sulfation absorption bands were identified, revealing the functional polysaccharides within these macroalgae. Anti-cholinesterasic activity was assessed in A. taxiformis, with a low IC50 for AChE (8.92 ± 0.43 μg mL−1) and BuChE (13.96 ± 0.32 μg mL−1), demonstrating dual inhibitory activity, justifying the interest to identify the active principle which may be the scaffold of a novel drug.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Albert CM, Hennekens CH, O’Donnell CJ, Ajani UA, Carey VJ, Willett WC, Ruskin JN, Manson JE (1998) Fish consumption and risk of sudden cardiac death. J Am Med Assoc 279:23–28

    CAS  Google Scholar 

  • Alwarsamy M, Gooneratne R, Ravichandran R (2016) Effect of fucoidan from Turbinaria conoides on human lung adenocarcinoma epithelial (A549) cells. Carbohydr Polym 152:207–213

    CAS  PubMed  Google Scholar 

  • Arruda M, Viana H, Rainha N, Neng NR, Rosa JS, Nogueira JM, Barreto MC (2012) Anti-acetylcholinesterase and antioxidant activity of essential oils from Hedychium gardnerianum Sheppard ex Ker-Gawl. Molecules 17:3082–3092

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barbosa M, Valentão P, Andrade PB (2014) Bioactive compounds from macroalgae in the new millennium: implications for neurodegenerative diseases. Mar Drugs 12:4934–4972

    CAS  PubMed  PubMed Central  Google Scholar 

  • Belattmania Z, Engelen AH, Pereira H, Serrao H, Custodio EA, Varela JC, Zrid R, Reani A, Sabour B (2018) Fatty acid composition and nutraceutical perspectives of brown seaweeds from the Atlantic coast of Morocco. Int Food Res J 25:1520–1527

    CAS  Google Scholar 

  • Berteau O, Mulloy B (2003) Sulfated fucans, fresh perspectives: structures, functions, and biological properties of sulfated fucans and an overview of enzymes active toward this class of polysaccharide. Glycobiology 13:29R–40R

    CAS  PubMed  Google Scholar 

  • Burreson BJ, Moore RE, Roller PP (1976) Volatile halogen compounds in the alga Asparagopsis taxiformis (Rhodophyta). J Agric Food Chem 24:856–861

    CAS  Google Scholar 

  • Cardoso C, Ripol A, Afonso C, Freire M, Varela J, Quental-Ferreira H, Pousão-Ferreira P, Bandarra N (2017) Fatty acid profiles of the main lipid classes of green seaweeds from fish pond aquaculture. Food Sci Nutr 5:1186–1194

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cohen Z, Vonshak A, Richmond A (1988) Effect of environmental conditions on fatty acid composition of the red alga Porphyridium cruentum: correlation to growth rate. J Phycol:328–332

  • Colovic MB, Krstic DZ, Lazarevic-Pasti TD, Bondzic AM, Vasic VM (2013) Acetylcholinesterase inhibitors: pharmacology and toxicology. Curr Neuropharmacol 11:315–335

    CAS  PubMed  PubMed Central  Google Scholar 

  • Custódio L, Silvestre L, Rocha MI, Rodrigues MJ, Vizetto-Duarte C, Pereira H, Barreira L, Varela J (2016) Methanol extracts from Cystoseira tamariscifolia and Cystoseira nodicaulis are able to inhibit cholinesterases and protect a human dopaminergic cell line from hydrogen peroxide-induced cytotoxicity. Pharm Biol 54:1687–1696

    PubMed  Google Scholar 

  • Dawczynski C, Schubert R, Jahreis G (2007) Amino acids, fatty acids, and dietary fibre in edible seaweed products. Food Chem 103:891–899

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Derenne A, Vandersleyen O, Goormaghtigh E (2014) Lipid quantification method using FTIR spectroscopy applied on cancer cell extracts. Biochim Biophys Acta - Mol Cell Biol Lipids 1841:1200–1209

    CAS  Google Scholar 

  • Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    CAS  PubMed  Google Scholar 

  • Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • Giacobini E (2003) Cholinesterases : new roles in brain function and in Alzheimer’s disease. Neurochem Res 28:515–522

    CAS  PubMed  Google Scholar 

  • Gómez-Ordóñez E, Rupérez P (2011) FTIR-ATR spectroscopy as a tool for polysaccharide identification in edible brown and red seaweeds. Food Hydrocoll 25:1514–1520

    Google Scholar 

  • Gressler V, Yokoya NS, Fujii MT, Colepicolo P, Filho JM, Torres RP, Pinto E (2010) Lipid, fatty acid, protein, amino acid and ash contents in four Brazilian red algae species. Food Chem 120:585–590

    CAS  Google Scholar 

  • Gutiérrez-Rodríguez AG, Juárez-Portilla C, Olivares-Bañuelos T, Zepeda RC (2018) Anticancer activity of seaweeds. Drug Discov Today 23:434–447

    PubMed  Google Scholar 

  • Hoffman DR, Boettcher JA, Diersen-Schade DA (2009) Toward optimizing vision and cognition in term infants by dietary docosahexaenoic and arachidonic acid supplementation: a review of randomized controlled trials. Prostaglandins Leukot Essent Fatty Acids 81:151–158

    CAS  PubMed  Google Scholar 

  • Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597

    CAS  Google Scholar 

  • Howes MR, Perry NSL, Houghton PJ (2003) Plants with traditional uses and activities, relevant to the management of Alzheimer’s disease and other cognitive disorders. 18:1–18

  • Kang Y, Wang ZJ, Xie D, Sun X, Yang W, Zhao X, Xu N (2017) Characterization and potential antitumor activity of polysaccharide from Gracilariopsis lemaneiformis. Mar Drugs 15. https://doi.org/10.3390/md15040100

  • Kendel M, Wielgosz-Collin G, Bertrand S, Roussakis C, Bourgougnon N, Bedoux G (2015) Lipid composition, fatty acids and sterols in the seaweeds Ulva armoricana and Solieria chordalis from Brittany (France): an analysis from nutritional, chemotaxonomic, and antiproliferative activity perspectives. Mar Drugs 13:5606–5628

    PubMed  PubMed Central  Google Scholar 

  • Khotimchenko SV, Vaskovsky VE, Titlyanova TV (2002) Fatty acids of marine algae from the Pacific coast of North California. Bot Mar 45:17–22

    CAS  Google Scholar 

  • Kiso Y (2011) Pharmacology in health foods: effects of arachidonic acid and docosahexaenoic acid on the age-related decline in brain and cardiovascular system function. J Pharmacol Sci 115:471–475

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lee H, Kang C, Jung E, Kim JS, Kim E (2011) Antimetastatic activity of polyphenol-rich extract of Ecklonia cava through the inhibition of the Akt pathway in A549 human lung cancer cells. Food Chem 127:1229–1236

    CAS  PubMed  Google Scholar 

  • Lemke SL, Maki KC, Hughes G, Taylor ML, Krul ES, Goldstein DA, Su H, Rains TM, Mukherjea R (2013) Consumption of stearidonic acid-rich oil in foods increases red blood cell eicosapentaenoic acid. J Acad Nutr Diet 113:1044–1056

    PubMed  Google Scholar 

  • Lepage G, Roy CC (1986) Direct transesterification of all classes of lipids in a one-step reaction. Notes Methodol 27:114–120

    CAS  Google Scholar 

  • Li X, Norman HC, Kinley RD, Laurence M, Wilmot M, Bender H, de Nys R, Tomkins N (2016) Asparagopsis taxiformis decreases enteric methane production from sheep. Anim Prod Sci 58:681–688

    Google Scholar 

  • Mai K, Mercer JP, Donlon J (1994) Comparative studies on the nutrition of two species of abalone, Haliotis tuberculata L and Haliotis discus hannai Ino. Aquaculture 128:115–130

    CAS  Google Scholar 

  • Marudhupandi T, Ajith Kumar TT, Lakshmanasenthil S, Suja G, Vinothkumar T (2015) In vitro anticancer activity of fucoidan from Turbinaria conoides against A549 cell lines. Int J Biol Macromol 72:919–923

    CAS  PubMed  Google Scholar 

  • Mattson MP (2004) Pathways towards and away from Alzheimer’s disease. Nature 430:631–639

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mellouk Z, Benammar I, Krouf D, Goudjil M, Okbi M, Malaisse W (2017) Antioxidant properties of the red alga Asparagopsis taxiformis collected on the North West Algerian coast. Exp Ther Med 13:3281–3290

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mišurcová L, Ambrožová J, Samek D (2011) Seaweed lipids as nutraceuticals. In: Kim S-K, Taylor S (eds) Advances in food and nutrition research marine medicinal foods: implications and applications, macro and microalgae. Elsevier, London, pp 339–355

    Google Scholar 

  • Miyashita K, Mikami N, Hosokawa M (2013) Chemical and nutritional characteristics of brown seaweed lipids: a review. J Funct Foods 5:1507–1517

    CAS  Google Scholar 

  • Nelson MM, Phleger CF, Nichols PD (2002) Seasonal lipid composition in macroalgae of the northeastern Pacific Ocean. Bot Mar 45:58–65

    CAS  Google Scholar 

  • Pádua D, Rocha E, Gargiulo D, Ramos AA (2015) Bioactive compounds from brown seaweeds: Phloroglucinol, fucoxanthin and fucoidan as promising therapeutic agents against breast cancer. Phytochem Lett 14:91–98

    Google Scholar 

  • Paiva L, Lima E, Patarra RF, Neto AI, Baptista J (2014) Edible Azorean macroalgae as source of rich nutrients with impact on human health. Food Chem 164:128–135

    CAS  PubMed  Google Scholar 

  • Polat S, Ozogul Y (2013) Seasonal proximate and fatty acid variations of some seaweeds from the northeastern Mediterranean coast. Oceanologia 55:375–391

    Google Scholar 

  • Ragonese C, Tedone L, Beccaria M, Torre G, Cichello F, Cacciola F, Dugo P, Mondello L (2014) Characterisation of lipid fraction of marine macroalgae by means of chromatography techniques coupled to mass spectrometry. Food Chem 145:932–940

    CAS  PubMed  Google Scholar 

  • Robic A, Bertrand D, Sassi JF, Lerat Y, Lahaye M (2009) Determination of the chemical composition of ulvan, a cell wall polysaccharide from Ulva spp. (Ulvales, Chlorophyta) by FT-IR and chemometrics. J Appl Phycol 21:451–456

    CAS  Google Scholar 

  • Sánchez-Machado DI, López-Cervantes J, López-Hernández J, Paseiro-Losada P (2004) Fatty acids, total lipid, protein and ash contents of processed edible seaweeds. Food Chem 85:439–444

    Google Scholar 

  • Santos SA, Vilela C, Freire CS, Abreu MH, Rocha SM, Silvestre AJ (2015) Chlorophyta and rhodophyta macroalgae: a source of health promoting phytochemicals. Food Chem 183:122–128

    CAS  PubMed  Google Scholar 

  • Schmid M, Kraft LGK, van der Loos LM, Kraft GT, Virtue P, Nichols PD, Hurd CL (2018) Southern Australian seaweeds: a promising resource for omega-3 fatty acids. Food Chem 265:70–77

    CAS  PubMed  Google Scholar 

  • Senthilkumar K, Manivasagan P, Venkatesan J, Kim SK (2013) Brown seaweed fucoidan: biological activity and apoptosis, growth signaling mechanism in cancer. Int J Biol Macromol 60:366–374

    CAS  PubMed  Google Scholar 

  • Simopoulos AP (2002) The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed Pharmacother 56:365–379

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Ulbricht TLV, Southgate DAT (1991) Coronary heart disease: seven dietary factors. Lancet 338:985–992

    CAS  PubMed  Google Scholar 

  • Verma P, Kumar M, Mishra G, Sahoo D (2017) Multivariate analysis of fatty acid and biochemical constitutes of seaweeds to characterize their potential as bioresource for biofuel and fine chemicals. Bioresour Technol 226:132–144

    CAS  PubMed  Google Scholar 

  • Vizetto-Duarte C, Pereira H, De Sousa CB, Rauter AP, Albericio F, Custodio L, Barreira L, Varela J (2015) Fatty acid profile of different species of algae of the Cystoseira genus: a nutraceutical perspective. Nat Prod Res 29:1264–1270

    CAS  PubMed  Google Scholar 

  • Wahbeh MI (1997) Amino acid and fatty acid profiles of four species of macroalgae from Aqaba and their suitability for use in fish diets. Aquaculture 159:101–109

    CAS  Google Scholar 

Download references

Acknowledgments

The authors present their acknowledgment to DRCT (Azores Regional Government) for co-financing, the Portuguese National Funds, through FCT-Fundação para a Ciência e a Tecnologia, and as applicable co-financed by the FEDER within the PT2020 Partnership Agreement by funding the cE3c centre (UID/BIA/00329/2013), (UID/BIA/00329/2019) and to DRCT for funding Azorean Biodiversity Group (ABG).

Funding

This work was financially supported by DemoBlueAlgae “Desenvolvimento de metodologias e optimização dos processos de cultivo e processamento de macroalgas para a indústria e economia azul” PROCiência 2020 (M1420-01-0247-FEDER000002); MACBIOBLUE “Proyecto demostrativo y de transferencia tecnológica para ayudar a las empresas a desarrollar nuevos produtos y procesos en el ambito de la Biotecnología Azul de la Macaronesia” (MAC/1.1b/ 086), program Interreg MAC 2014–2020; ARDITI - Regional Agency for the Development of Research Technology and Innovation (M14-20-09-5369-FSE-000001-Doctorate in Business; Blue Iodine II “Boost Blue economy through market uptake an innovative seaweed bioextract for iodine fortification II”, grant agreement no. 733552, H2020-SMEInst-2016-2017.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. Nunes.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nunes, N., Rosa, G.P., Ferraz, S. et al. Fatty acid composition, TLC screening, ATR-FTIR analysis, anti-cholinesterase activity, and in vitro cytotoxicity to A549 tumor cell line of extracts of 3 macroalgae collected in Madeira. J Appl Phycol 32, 759–771 (2020). https://doi.org/10.1007/s10811-019-01884-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-019-01884-9

Keywords

Navigation