Abstract
Alginate fractions from the pelagic Sargassum fluitans (Børgesen) Børgesen and kelp, Ecklonia maxima (Osbeck) Papenfuss sourced from the coastal waters of Ghana and South Africa respectively, were extracted by a simple sequential protocol different from the conventional methods. A total of six different phycocolloids were obtained, with two extracted under ambient conditions (fractions 1A) and the remaining four under hot conditions (fractions 2A and 3A) using ethanol and CaCl2, respectively, for precipitation. These extracts were assessed for variations in their physicochemical properties, tyrosinase inhibition, antioxidation and anticoagulation activities. Molecular weights of the extracts were ~ 58–1506 kDa with their yields ranging between 4.8 to 11.1%. A sequential reduction (up to tenfold) was observed in their total phenolic compounds, proteins and sulphate contents. 1H-NMR analysis of their uronic acid block structure revealed M/G ratios less than 1 for all extracts with dominant FGG and FGGG units depicting guluronic acid rich alginate fractions. Extracts from S. fluitans, notably, showed distinct antioxidation activity comparable to the well-known antioxidants like ascorbic acid. For tyrosinase inhibition, the highest was from S. fluitans fraction 1A (~ 37.1 ± 4.38%). The variations in properties of extracts reported herein, elucidates the possibility of obtaining series of relatively desirable alginate fractions from E. maxima and Ghanaian sourced S. fluitans via this modified extraction process.
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References
Abka-Khajouei R, Tounsi L, Shahabi N, Patel AK, Abdelkafi S. Michaud P (2022) Structures, properties and applications of alginates. Mar Drugs 20:364
Addico GND, deGraft-Johnson KAA (2016) Preliminary investigation into the chemical composition of the invasive brown seaweed Sargassum along the West Coast of Ghana. Afr J Biotechnol 15:2184–2191
Ahmad Z, Pandey R, Sharma S, Khuller GK (2006) Pharmacokinetic and pharmacodynamic behaviour of antitubercular drugs encapsulated in alginate nanoparticles at two doses. Int J Antimicrob 27:409–416
Bertagnolli C, Espindola APDM, Kleinübing SJ, Tasic L, Da Silva MGC (2014) Sargassum filipendula alginate from Brazil: seasonal influence and characteristics. Carbohydr Polym 111:619–623
Boateng JS, Matthews KH, Stevens HN, Eccleston GM (2008) Wound healing dressings and drug delivery systems: a review. J Pharm Sci 97:2892–2923
Bordoloi A, Goosen NJ (2020) A greener alternative using subcritical water extraction to valorize the brown macroalgae Ecklonia maxima for bioactive compounds. J Appl Phycol 32:2307–2319
Bouhadir KH, Lee KY, Alsberg E, Damm KL, Anderson KW, Mooney DJ (2001) Degradation of partially oxidized alginate and its potential application for tissue engineering. Biotechnol 17:945–950
Brand-Williams W, Cuvelier ME, Berset CLWT (1995) Use of a free radical method to evaluate antioxidant activity. LWT-Food Sci Technol 28:25–30
Chan YY, Kim KH, Cheah SH (2011) Inhibitory effects of Sargassum polycystum on tyrosinase activity and melanin formation in B16F10 murine melanoma cells. J Ethnopharmacol 137:1183–1188
Chee SY, Wong PK, Wong CL (2011) Extraction and characterisation of alginate from brown seaweeds (Fucales, Phaeophyceae) collected from Port Dickson, Peninsular Malaysia. J Appl Phycol 23:191–196
Chen Q, Kou L, Wang F, Wang Y (2019) Size-dependent whitening activity of enzyme-degraded fucoidan from Laminaria japonica. Carbohydr Polym 225:115211
Ching SH, Bansal N, Bhandar B (2017) Alginate gel particles–A review of production techniques and physical properties. Crit Rev Food Sci Nutr 57:1133–1152
Cox S, Abu-Ghannam N, Gupta S (2010) An assessment of the antioxidant and antimicrobial activity of six species of edible Irish seaweeds. Int Food Res J 17:205–220
Daemi H, Barikani M (2012) Synthesis and characterization of calcium alginate nanoparticles, sodium homopolymannuronate salt and its calcium nanoparticles. Sci Iran 19:2023–2028
Darko CNS, Agyei-Tuffour B, Faloye DF, Goosen NJ, Nyankson E, Dodoo-Arhin D (2022) Biomethane production from residual algae biomass (Ecklonia maxima): Effects of inoculum acclimatization on yield. Waste Biomass Valoriz 13:497–509
Davis TA, Ramirez M, Mucci A, Larsen B (2004) Extraction, isolation and cadmium binding of alginate from Sargassum spp. J Appl Phycol 16:275–284
Davis TA, Llanes F, Volesky B, Diaz-Pulido G, McCook L, Mucci A (2003) 1 H-NMR study of Na alginates extracted from Sargassum spp. in relation to metal biosorption. Appl Biochem 110:75–90
Davis D, Simister R, Campbell S, Marston M, Bose S, McQueen-Mason SJ, Gomez LD, Gallimore WA Tonon T (2021) Biomass composition of the golden tide pelagic seaweeds Sargassum fluitans and S. natans (morphotypes I and VIII) to inform valorisation pathways. Sci Total Environ 762:143134
Dobrinčić A, Balbino S, Zorić Z, Pedisić S, Bursać Kovačević D, Elez Garofulić I, Dragović-Uzelac V (2020) Advanced technologies for the extraction of marine brown algal polysaccharides. Mar Drugs 18:168
Dodgson KS, Price RG (1962) A note on the determination of the ester sulphate content of sulphated polysaccharides. Biochem J 84:106–110
Farvin KS, Jacobsen C (2013) Phenolic compounds and antioxidant activities of selected species of seaweeds from Danish coast. Food Chem 138:1670–1681
Fawzy MA, Gomaa M, Hifney AF, Abdel-Gawad KM (2017) Optimization of alginate alkaline extraction technology from Sargassum latifolium and its potential antioxidant and emulsifying properties. Carbohydr Polym 157:1903–1912
Fernando IPS, Lee W, Ahn G (2022) Marine algal flavonoids and phlorotannins; an intriguing frontier of biofunctional secondary metabolites. Crit Rev Biotechnol 42:23–45
Filisetti Cozzi TMCC, Carpita NC (1991) Measurement of uronic acids without interference from neutral sugars. Anal Biochem 197:157–162
García-Vaquero M, Rajauria G, O’Doherty JV, Sweeney T (2017) Polysaccharides from macroalgae: Recent advances, innovative technologies and challenges in extraction and purification. Food Res Int 99:1011–1020
Georg Jensen M, Pedersen C, Kristensen M, Frost G, Astrup A (2013) Efficacy of alginate supplementation in relation to appetite regulation and metabolic risk factors: Evidence from animal and human studies. Obes Rev 14:129–144
Gomez CG, Pérez Lambrecht MV, Lozano JE, Rinaudo M, Villar MA (2009) Influence of the extraction–purification conditions on final properties of alginates obtained from brown algae (Macrocystis pyrifera). Int J Biol Macromol 44:365–371
Gorin PAJ, Spencer JFT (1966) Exocellular alginic acid from Azotobacter vinelandii. Can J Chem 44:993–998
Grasdalen H, Larsen B, Smidsrød O (1979) A p.m.r. study of the composition and sequence of uronate residues in alginates. Carbohydr Res 68:23–31
Haque KF, Chy SY, Akter S, Wahab MA, Nath KK (2009) Collection, identification and biochemical analyses of different seaweeds from Saint Martin’s island. Bangladesh J Ag Res 34:59–65
Haug A, Larsen B, Smidsrød O (1967) Studies on the sequence of uronic acid residues in alginic acid. Acta Chem Scand 21:691–704
Haug A, Smidsrød O, Larsen B (1963) Degradation of alginates at different pH values. Acta Chem Scand 17:1466
Hecht H, Srebnik S (2016) Structural characterization of sodium alginate and calcium alginate. Biomacromol 17:2160–2167
Hentati F, Ursu AV, Pierre G, Delattre C, Trica B, Abdelkafi S, Michaud P (2019) Production, extraction and characterization of alginates from seaweeds. In: Ravishankar G, Ambati RR (eds) Handbook of Algal Technologies and Phytochemicals. CRC Press, Boca Raton, pp 33–42
Hifney AF, Fawzy MA, Abdel-Gawad KM, Gomaa M (2016) Industrial optimization of fucoidan extraction from Sargassum sp. and its potential antioxidant and emulsifying activities. Food Hydrocoll 54:77–88
Humayun S, Premarathna AD, Rjabovs V, Howlader MM, Darko CNS, Mok I-K, Tuvikene R (2023) Biochemical characteristics and potential biomedical applications of hydrolyzed carrageenans. Mar Drugs 21:269
January GG, Naidoo RK, Kirby-McCullough B, Bauer R (2019) Assessing methodologies for fucoidan extraction from South African brown algae. Algal Res 40:101517
Johnson FA, Craig DQ, Mercer AD (1997) Characterization of the block structure and molecular weight of sodium alginates. J Pharm Pharmacol 49:639–643
Kang HS, Kim HR, Byun DS, Son BW, Nam TJ, Choi JS (2004) Tyrosinase inhibitors isolated from the edible brown alga Ecklonia stolonifera. Arch Pharm Res 27:1226–1232
Khajouei RA, Keramat J, Hamdami N, Ursu AV, Delattre C, Laroche C, Gardarin C, Lecerf D, Desbrières J, Djelveh G, Michaud P (2018) Extraction and characterization of an alginate from the Iranian brown seaweed Nizimuddinia zanardini. Int J Biol Macromol 118:1073–1081
Kuda T, Taniguchi E, Nishizawa M, Araki Y (2002) Fate of water-soluble polysaccharides in dried Chorda filum a brown alga during water washing. J Food Compos 15:3–9
Kumar Y, Tarafdar A, Badgujar PC (2021) Seaweed as a source of natural antioxidants: Therapeutic activity and food applications. J Food Qual 2021:5753391
Larsen B, Salem DMSA, Sallam MAE, Mishrikey MM, Beltagy AI (2003) Characterization of the alginates from algae harvested at the Egyptian Red Sea Coast. Carbohydr Res 338:2325–2336
Liu J, Wu SY, Chen L, Li QJ, Shen YZ, Jin L, Zhang X, Chen PC, Wu MJ, Choi JI, Tong HB (2020) Different extraction methods bring about distinct physicochemical properties and antioxidant activities of Sargassum fusiforme fucoidans. Int J Biol Macromol 155:1385–1392
Lorbeer AJ, Charoensiddhi S, Lahnstein J, Lars C, Franco CM, Bulone V, Zhang W (2016) Sequential extraction and characterization of fucoidans and alginates from Ecklonia radiata, Macrocystis pyrifera, Durvillaea potatorum, and Seirococcus axillaris. J Appl Phycol 29:1515–1526
Milledge JJ, Nielsen BV, Bailey D (2016) High-value products from macroalgae: the potential uses of the invasive brown seaweed, Sargassum muticum. Environ Sci Biotechnol 15:67–88
Mohammed A, Rivers A, Stuckey DC, Ward K (2020) Alginate extraction from Sargassum seaweed in the Caribbean region: Optimization using response surface methodology. Carbohydr Polym 245:116419
Msuya FE, Bolton J, Pascal F, Narrain K, Nyonje B, Cottier-Cook EJ (2022) Seaweed farming in Africa: current status and future potential. J Appl Phycol 34:985–1005
Nøkling-Eide K, Langeng AM, Åslund A, Aachmann FL, Sletta H, Arlov Ø (2023) An assessment of physical and chemical conditions in alginate extraction from two cultivated brown algal species in Norway: Alaria esculenta and Saccharina latissima. Algal Res 69:10295
O’Sullivan AM, O’Callaghan YC, O’Grady MN, Queguineur B, Hanniffy D, Troy DJ, Kerry JP, O’Brien NM (2011) In vitro and cellular antioxidant activities of seaweed extracts prepared from five brown seaweeds harvested in spring from the west coast of Ireland. Food Chem 126:1064–1070
Oyesiku OO, Egunyomi A (2014) Identification and chemical studies of pelagic masses of Sargassum natans (Linnaeus) Gaillon and S. fluitans (Borgessen) Borgesen (brown algae), found offshore in Ondo state, Nigeria. Afr J Biotechnol 13:1188–1193
Palanisamy S, Vinosha M, Marudhupandi T, Rajasekar P, Prabhu NM (2017) Isolation of fucoidan from Sargassum polycystum brown algae: Structural characterization, in vitro antioxidant and anticancer activity. Int J Biol Macromol 102:405–412
Percival E, McDowell RH (1967) Chemistry and enzymology of marine algal polysaccharides. Academic Press, London
Pereira L, Sousa A, Coelho H, Amado AM, Ribeiro-Claro PJ (2003) Use of FTIR, FT-Raman and 13C-NMR spectroscopy for identification of some seaweed phycocolloids. Biomol Eng 20:223–228
Premarathna AD, Tuvikene R, Fernando PHP, Adhikari R, Perera MCN, Ranahewa TH, Howlader MM, Wangchuk P, Jayasooriya AP Rajapakse RPVJ (2022) Comparative analysis of proximate compositions, mineral and functional chemical groups of 15 different seaweed species. Sci Rep 12:19610
Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237
Rehm BH (ed) (2009) Alginates: Biology and Applications. Springer, Berlin
Rhein-Knudsen N, Ale MT, Ajalloueian F, Meyer AS (2017) Characterization of alginates from Ghanaian brown seaweeds: Sargassum spp. and Padina spp. Food Hydrocoll 71:236–244
Rioux LE, Turgeon SL, Beaulieu M (2007) Characterisation of polysaccharides extracted from brown seaweeds. Carbohydr Polym 69:530–537
Saluri K, Tuvikene R (2020) Anticoagulant and antioxidant activity of lambda-and theta-carrageenans of different molecular weights. Bioact Carbohydr Dietary Fibre 24:100243
Schwaeble CF, Pott RW, Goosen NJ (2021) The effect of sodium alginate, lignosulfonate and bentonite binders on agglomeration performance and mechanical strength of micro-fine agricultural lime pellets. Part Sci Technol 39:820–831
Serfor-Armah Y, Nyarko BJB, Osae E K, Carboo D, Seku F (1999) Elemental analysis of some green and brown seaweeds from the coastal belt of Ghana. J Radioanalyt Nuclear Chem 242:193e197
Shobharani P, Nanishankar VH, Halami PM, Sachindra NM (2014) Antioxidant and anticoagulant activity of polyphenol and polysaccharides from fermented Sargassum sp. Int Biol Macromol 65:542–548
Sluiter A, Hames B, Ruiz RO, Scarlata C, Sluiter J, Templeton D (2004) Determination of ash in biomass. Laboratory Analytical Procedure. National Renewable Energy Laboratory, Golden, Colorado. Technical Report NREL/TP-510–42622
Sluiter A, Hames B, Hyman D, Payne C, Ruiz R, Scarlata C, Sluiter J, Templeton D, Wolfe J (2008) Determination of total solids in biomass and total dissolved solids in liquid process samples.National Renewable Energy Laboratory, Golden, Colorado. Technical Report NREL/TP-510–42621
Smirnoff N, Cumbes QJ (1989) Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry 28:1057–1060
Torabi P, Hamdami N, Keramat J (2022) Microwave-assisted extraction of sodium alginate from brown macroalgae Nizimuddinia zanardini, optimization and physicochemical properties. Sep Sci Technol 57:872–885
Torres MR, Sousa AP, Silva Filho EA, Melo DF, Feitosa JP, de Paula RC, Lima MG (2007) Extraction and physicochemical characterization of Sargassum vulgare alginate from Brazil. Carbohydr Res 342:2067–2074
Tuvikene R, Robal M, Fujita D, Saluri K, Truus K, Tashiro Y, Ogawa H, Matsukawa S (2015) Funorans from Gloiopeltis species. Part I. Extraction and structural characteristics. Food Hydrocoll 43:481–492
Wang HMD, Chen CC, Huynh P, Chang JS (2015) Exploring the potential of using algae in cosmetics. Bioresour Technol 184:355–436
Zayed A, El-Aasr M, Ibrahim ARS, Ulber R (2020) Fucoidan characterization: Determination of purity and physicochemical and chemical properties. Mar Drugs 18:71
Zhang X, Border A, Goosen N, Thomsen M (2021) Environmental life cycle assessment of cascade valorisation strategies of South African macroalga Ecklonia maxima using green extraction technologies. Algal Res 58:102348
Zvyagintseva TN, Shevchenko NM, Chizhov AO, Krupnova TN, Sundukova EV, Isakov VV (2003) Water-soluble polysaccharides of some far-eastern brown seaweeds. Distribution, structure, and their dependence on the developmental conditions. J Exp Mar Biol Ecol 294:1–13
Acknowledgements
The authors are grateful to Keemilise ja Bioloogilise Füüsika Instituut (KBFI), Tallinn Estonia for the 1H-NMR analysis and spectra acquisition of all the different extracted fractions.
Funding
Research funding was provided by the Estonian Ministry of Foreign Affairs grant TYA21090 and the Estonian Research Council grant PRG1808. 1H-NMR spectra were acquired on the instrumentation of the Estonian Centre of Analytical Chemistry (AKKI, TT4).
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All co-authors contributed and approved the final version of the manuscript for publication. CNSD: Conceptualization, investigation, writing, interpretation and analysis of data. ADP and SH: investigation, data analysis, review and editing. BAT and NJG: conceptualization, provision of seaweed samples, review and editing. RT: conceptualization, project administration, supervision, funding acquisition, review and editing.
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Darko, C.N.S., Premarathna, A.D., Humayun, S. et al. Physico- and biochemical properties of alginates extracted from Ecklonia maxima and Sargassum fluitans using a simple cascade process. J Appl Phycol (2023). https://doi.org/10.1007/s10811-023-03023-x
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DOI: https://doi.org/10.1007/s10811-023-03023-x