Abstract
The aim of this study was to characterize the yield and chemical compositions of sulfated polysaccharides (SP) from the brown seaweed Silvetia compressa collected off the Pacific coast of Baja California, Mexico. SP yield was evaluated from basal and apical tissues and fruiting bodies. Chemical heterogeneity was evaluated by ethanol fractionation and anion-exchange chromatography and characterized by FTIR spectra. Geographic differences in yield (11–12.1%) and sulfate content (15–16%) were minimal. Basal thallus had a higher yield, while fruiting bodies contained more fucose and sulfates. The SP of S. compressa are composed of variable amounts of fucose, sulfates, and uronic acids (fucoidan type). The heterogeneity of SP was demonstrated by fractionation with ethanol at 50% which yields a soluble fraction, composed of fucose with high sulfate content devoid of uronic acids. Similarly, the anion-exchange chromatography separated fractions composed of molecules differing in fucose content. FTIR spectra showed characteristic signals for SP: a strong peak at 1240–1250 cm−1 (S=O), a peak at 840–850 cm−1 (axial sulfate C-4), and peaks at 1625 and 1417 cm−1 (carboxylic group of uronic acids). These results indicate that SP of S. compressa correspond to a fucoidan-type polysaccharides with sulfates occurring mainly on C-4 of the fucose units and containing low amounts of uronic acids.
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References
Abbott IA, Hollenberg GJ (1976) Marine algae of California. Stanford University Press, Stanford
Ale MT, Meyer AS (2013) Fucoidans from brown seaweeds: an update on structures, extraction techniques and use of enzymes as tools for structural elucidation. RSC Adv 3:8131–8141
Ale MT, Mikkelsen JD, Meyer AS (2011) Important determinants for fucoidan bioactivity: a critical review of structure–function relations and extraction methods for fucose–containing sulfated polysaccharides from brown seaweeds. Mar Drugs 9:2106–2130
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 13:29–40
Bilan MI, Grachev AA, Ustuzhanina NE, Shashkov AS, Nifantiev NE, Usov AI (2002) Structure of a fucoidan from the brown seaweed Fucus evanescens C. Ag Carbohydr Res 337:719–730
Bisgrove SR, Kropf DL (2001) Cell wall deposition during morphogenesis in fucoid algae. Planta 212:648–658
Bitter T, Muir HM (1962) A modified uronic acid carbazole reaction. Anal Biochem 4:330–334
Black WAP (1954) The seasonal variation in the combined L-fucose content of the common British Laminariaceae and Fucaceae. J Sci Food Agric 5:445–448
Bruhn A, Janicek T, Manns D, Nielsen MM, Balsby TJ, Meyer AS, Rasmussen MB, Hou X, Saake B, Göke C, Bjerre AB (2017) Crude fucoidan content in two North Atlantic kelp species, Saccharina latissima and Laminaria digitata seasonal variation and impact of environmental factors. J Appl Phycol 29:3121–3137
Chizhov AO, Dell A, Morris HR, Haslam SM, McDowell RA, Shashkov AS, Nifantev NE, Khatuntseva EA, Usov AI (1999) A study of fucoidan from the brown seaweed Chorda filum. Carbohydr Res 320:108–119
Colliec S, Boisson-Vidal C, Jozefonvicz J (1994) A low molecular weight fucoidan fraction from the brown seaweed Pelvetia canaliculata. Phytochemistry 35:697–700
Craigie JS, Wen ZC (1984) Effects of temperature and tissue age on gel strength and composition of agar from Gracilaria tikvahiae (Rhodophyceae). Can J Bot 62:665–1670
Cumashi A, Ushakova NA, Preobrazhenskaya ME, D’Incecco A, Piccoli A, Totani L, Tinari N, Morozevich GE, Berman AE, Bilan MI, Usov AI, Ustyuzhanina NE, Grachev AA, Sanderson CJ, Kelly M, Rabinovich GA, Iacobelli S, Nifantiev NE (2007) A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology 17:541–552
Dische Z (1955) Sugars in polysaccharides. Methods Biochem Anal 2:31–338
Duarte MER, Cardoso MA, Noseda MD, Cerezo AS (2001) Structural studies on fucoidans from the brown seaweed Sargassum stenophyllum. Carbohydr Res 333:281–293
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
Fitton JH, Stringer DN, Karpiniec SS (2015) Therapies from fucoidan: an update. Mar Drugs 13:5920–5946
Fletcher HR, Biller P, Ross AB, Adams JMM (2017) The seasonal variation of fucoidan within three species of brown macroalgae. Algal Res 22:79–86
Ghosh T, Chattopadhyay K, Marschall M, Karmakar P, Mandal P, Ray B (2009) Focus on antivirally active sulfated polysaccharides: from structure–activity analysis to clinical evaluation. Glycobiology 19:2–15
Hogsett WE, Quatrano RS (1975) Isolation of polysaccharides sulfated during early embryogenesis in Fucus. Plant Physiol 55:25–29
Hogsett WE, Quatrano RS (1978) Sulfation of fucoidan in Fucus embryos: III. Required for localization in the rhizoid wall. J Cell Biol 78:866–873
Honya M, Mori M, Anzai M, Araki Y, Nisizawa K (1999) Monthly changes in the content of fucans, their constituent sugars and sulphate in cultured Laminaria japonica. Hydrobiologia 398:411–416
Kloareg B (1981) Structure et rôle écophysiologique des parois des algues littorales: Contribution á la résistance aux variations de salinité. Physiol Vég 17:731–747
Kloareg B, Quatrano R (1988) Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr Mar Biol Annu Rev 26:259–315
Kloareg B, Demarty M, Mabeau S (1986) Polyanionic characteristic of purified sulphated homofucans from brown algae. Int J Biol Macromol 8:380–386
Kraan S (2012) Algal polysaccharides, novel applications and outlook. In: Chang CF (ed) Carbohydrates-comprehensive studies on glycobiology and glycotechnology. InTech, Rijeka, pp 489–532
Kylin H (1913) Zur Biochemie der Meeresalgen. Hoppe Seylers Z Physiol Chem 83:171–197
Larsen B (1967) Sulphated polysaccharides in brown algae. II. Isolation of 3-O-β-D-xylopyranosyl-L-fucose from ascophyllan. Acta Chem Scand 21:1395–1396
Larsen B (1978) Brown seaweeds: analysis of ash, fiber, iodine and mannitol. In: Hellebust JA, Craigie JS (eds) Handbook of phycological methods. Cambridge University Press, Cambridge, pp 181–188
Larsen B, Haug A, Painter TJ (1966) Sulphated polysaccharides in brown algae. Isolation and preliminary characterization of three sulphated polysaccharides from Ascophyllum nodosum (L.). Acta Chem Scand 20:219–230
Li N, Zhang QB, Song JM (2005) Toxicological evaluation of fucoidan extracted from Laminaria japonica in Wistar rats. Food Chem Toxicol 43:421–426
Lobban SC, Harrison JP (1994) Seaweed ecology and physiology. Cambridge University Press, Cambridge
Mak W, Hamid N, Liu T, Lu J, White WL (2013) Fucoidan from New Zealand Undaria pinnatifida: monthly variations and determination of antioxidant activities. Carbohydr Polym 95:606–614
McCandless EL, Craigie JS (1979) Sulfated polysaccharides in red and brown algae. Annu Rev Plant Physiol 30:41–67
Medcalf DG, Schneider TL, Barnett RW (1978) Structural features of a novel glucuronogalactofucan from Ascophyllum nodosum. Carbohydr Res 66:167–171
Mian J, Percival E (1973) Carbohydrates of the brown seaweeds Himanthalia lorea and Bifurcaria bifurcata Part II. Structural studies of the “fucans”. Carbohydr Res 26:147–161
Murray SN, Bray RB (1993) Benthic macrophytes. In: Dailey MD, Reish DJ, Anderson JW (eds) Ecology of the Southern California Bight: a synthesis and interpretation. University of California Press, Berkeley, pp 304–368
Painter TJ (1983) Algal polysaccharides. In: Aspinall GO (ed) The polysaccharides, vol 2. Academic Press, New York, pp 195–285
Patankar MS, Oehninger S, Barnett T, Williams R, Clark GF (1993) A revised structure for fucoidan may explain some of its biological activities. J Biol Chem 268:21770–21776
Pedroche FF, Silva PC, Aguilar-Rosas LE, Dreckmann KM, Aguilar-Rosar R (2008) Catálogo de las Algas Marinas Bentónicas del Pacífico de México II. Phaeophycota, UNAM-UABC-UC, Berkeley
Percival E (1968) Glucuronoxylofucan, a cell-wall component of Ascophyllum nodosum. Part I. Carbohydr Res 7:272–283
Percival E (1979) The polysaccharides of green, red and brown seaweeds: their basic structure, biosynthesis and function. Br Phycol J 14:103–117
Percival E, McDowell RH (1967) Chemistry and enzymology of marine algal polysaccharides. Academic Press, London
Pereira L, Gheda SF, Ribeiro-Claro PJ (2013) Analysis by vibrational spectroscopy of seaweed polysaccharides with potential use in food, pharmaceutical, and cosmetic industries. Int J Carbohydr Chem 2013:1–7
Ricketts EF, Calvin J, Hedgpeth JW (1985) Between Pacific Tides. Stanford University Press, Stanford, California
Setchell WA, Gardner NL (1925) The marine algae of the Pacific coast of North America. Part III Melanophyceae. University of California Publications in Botany 8:34-107
Silva TMA, Alves LG, Queiroz KCS, Santos MGL, Marques CT, Chavante SF, Rocha HAO, Leite EL (2005) Partial characterization and anticoagulant activity of a heterofucan from the brown seaweed Padina gymnospora. Braz J Med Biol Res 38:523–533
Skriptsova AV (2015) Fucoidans of brown algae: biosynthesis, localization, and physiological role in thallus. Russ J Mar Biol 41:145–156
Skriptsova AV (2016) Seasonal variations in the fucoidan content of brown algae from Peter the Great Bay, Sea of Japan. Russ J Mar Biol 42:351–356
Skriptsova AV, Shevchenko NM, Tarbeeva DV, Zvyagintseva TN (2012) Comparative study of polysaccharides from reproductive and sterile tissues of five brown seaweeds. Mar Biotechnol 14:304–311
Synytsya A, Čopı́ková J, Matějka P, Machovič V (2003) Fourier transform Raman and infrared spectroscopy of pectins. Carbohydr Polym 54:97–106
Tabatabai MA (1974) Determination of sulfate in water samples. J Sulphur Inst 10:11–13
Tako M, Nakada T, Hongou F (1999) Chemical characterization of fucoidan from commercially cultured Nemacystus decipiens (Itomozuku). Biosci Biotechnol Biochem 63:1813–1815
Ushakova NA, Morozevich GE, Ustyuzhanina NE, Bilan MI, Usov AI, Nifantiev NE, Preobrazhenskaya ME (2009) Anticoagulant activity of fucoidans from brown algae. Biochemistry (Moscow) Suppl Ser B 3:77–83
Usoltseva RV, Anastyuk SD, Ishina IA, Isakov VV, Zvyagintseva TN, Thinh PD, Zadorozhny PA, Dmitrenok PS, Ermakova SP (2018) Structural characteristics and anticancer activity in vitro of fucoidan from brown alga Padina boryana. Carbohydr Polym 184:260–268
Usov AI, Smirnova GP, Klochkova NG (2001) Algae polysaccharides. 55. Polysaccharide composition of some brown Kamchatka algae. Bioorg Khim 27:444–448
Usov AI, Smirnova GP, Klochkova NG (2005) Polysaccharides of algae 58. The polysaccharide composition of the Pacific brown alga Alaria fistulosa P. et R. (Alariaceae, Laminariales). Russ Chem Bull Int Ed 54:1282–1286
Ustyuzhanina NE, Bilan MI, Ushakova NA, Usov AI, Kiselevskiy MV, Nifantiev NE (2014) Fucoidans: pro- or antiangiogenic agents? Glycobiology 24:1265–1274
Wang CY, Chen YC (2016) Extraction and characterization of fucoidan from six brown macroalgae. J Mar Sci Technol 24:319–328
Wang P, Zhao X, Lv Y, Liu Y, Lang Y, Wua J, Liu X, Li M, Yua G (2012) Analysis of structural heterogeneity of fucoidan from Hizikia fusiforme by ES-CID-MS/MS. J Appl Phycol 20:431–436
Zhao X, Xue CH, Li BF (2008) Study of antioxidant activities of sulfated polysaccharides from Laminaria japonica. J Appl Phycol 20:431–436
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
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Hernández-Garibay, E., Zertuche-González, J.A. & Pacheco-Ruiz, I. Sulfated polysaccharides (fucoidan) from the brown seaweed Silvetia compressa (J. Agardh) E. Serrão, T.O. Cho, S.M. Boo & Brawley. J Appl Phycol 31, 3841–3847 (2019). https://doi.org/10.1007/s10811-019-01870-1
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DOI: https://doi.org/10.1007/s10811-019-01870-1