Advertisement

Journal of Applied Phycology

, Volume 30, Issue 6, pp 3271–3283 | Cite as

Comparison study of bioactive substances and nutritional components of brown algae Sargassum fusiforme strains with different vesicle shapes

  • Yajing Li
  • Xiaoting FuEmail author
  • Delin Duan
  • Jiachao Xu
  • Xin Gao
8th Asian Pacific Phycological Forum

Abstract

In this study, variations in the biochemical composition of two Sargassum fusiforme strains (SF-1 and SF-2) with different vesicle shapes collected during harvest period were analyzed. Compared with several other algae, S. fusiforme (commonly known as Hijiki) can be recommended as a nutritious food for its high levels of minerals, polyunsaturated fatty acids, phlorotannins, fucoidan, and alginate. Comparison of the two strains indicated that there were significant differences between the contents and characteristics of some components. The alginate content of SF-1 (15.46–26.30%) was higher than that of SF-2 (14.97–24.40%), while the alginate with highest molecular weight and viscosity was obtained from SF-2 (3.77 × 106 g mol−1, 226.2 mPa s). The content of fucoidan of SF-2 (5.30–11.60%) was higher than that of SF-1 (6.11–7.87%). On the other hand, the phlorotannin content of SF-1 (17.55–48.91 mg g−1) was higher than that of SF-2 (28.28–39.76 mg g−1), and a higher purity of fucoxanthin could be obtained from SF-1 (80.59–92.40%) than that from SF-2 (72.50–84.14%). Analysis of fatty acid composition indicated that EPA and α-linolenic acid were more abundant in SF-1, whereas arachidonic acid was more abundant in SF-2. The highest content of various nutrients existed in different strains and different periods. So, strain and the time of harvest can be selected according to the purpose of utilization.

Keywords

Nutritional components Bioactive substances Alginate Fucoidan Phaeophyta Sargassum fusiforme 

Notes

Acknowledgements

We especially thank Culture Collection of Seaweed at the Ocean University of China for their help in providing S. fusiforme.

Funding information

This work was founded by the grant of International Science and Technology Cooperation Program of China (No. 2015DFG32290), the grant of Public Science and Technology Research Funds Projects of Ocean (No. 201405040), and Jiangsu Provincial Key R & D Project (BE2015335).

References

  1. Aguilera-Morales M, Casas-Valdez M, Carrillo-Domínguez S, González-Acosta B, Pérez-Gil F (2005) Chemical composition and microbiological assays of marine algae Enteromorpha spp. as a potential food source. J Food Compos Anal 18:79–88CrossRefGoogle Scholar
  2. Albana C, Natalia AU, Marina EP, Armida DI, Antonio P, Licia T, Nicola T, Galina EM, Albert EB, Maria I, Bilan AIU, Nadezhda EU, Alexey AG, Craig JS, Maeve K, Gabriel AR, Stefano I, Nikolay EN (2007) A comparative study of the anti-inflammatory, anticoagulant, antiangiogenic, and antiadhesive activities of nine different fucoidans from brown seaweeds. Glycobiology 17:541–541CrossRefGoogle Scholar
  3. Balboa EM, Conde E, Moure A, Falque E, Dominguez H (2013) In vitro antioxidant properties of crude extracts and compounds from brown algae. Food Chem 138:1764–1785CrossRefGoogle Scholar
  4. Balboa EM, Gallego-Fábrega C, Moure A, Domínguez H (2016) Study of the seasonal variation on proximate composition of oven-dried Sargassum muticum biomass collected in Vigo Ria, Spain. J Appl Phycol 28:1943–1953CrossRefGoogle Scholar
  5. Chen LM, Li DM, Yushan Z, Naihao Y (2009) Content and gelling properties of alginate from different region of Laminaria. China Food Addit 2:124–142Google Scholar
  6. Chen X, Nie W, Yu G, Li Y, Hu Y, Lu J, Jin L (2012) Antitumor and immunomodulatory activity of polysaccharides from Sargassum fusiforme. Food Chem Toxicol 50:695–700CrossRefGoogle Scholar
  7. Clementi F, Mancini M, Moresi M (1998) Rheology of alginate from Azotobacter vinelandii in aqueous dispersions. J Food Eng 36:51–62CrossRefGoogle Scholar
  8. Denis C, Morancais M, Li M, Deniaud E, Gaudin P, Wielgosz CG, Barnathan G, Jaouen P, Fleurence J (2010) Study of the chemical composition of edible red macroalgae Grateloupia turuturu from Brittany (France). Food Chem 119:913–917CrossRefGoogle Scholar
  9. Dobashi K, Nishino T, Fujihara M, Nagumo T (1989) Isolation and preliminary characterization of fucose-containing sulfated polysaccharides with blood-anticoagulant activity from the brown seaweed Hizikia fusiforme. Carbohydr Res 194:315–320CrossRefGoogle Scholar
  10. Dodgson KS (1961) Determination of inorganic sulphate in studies on the enzymic and non-enzymic hydrolysis of carbohydrate and other sulphate esters. Biochem J 78:312–319CrossRefGoogle Scholar
  11. Dos Santos RR, Moreira DM, Kunigami CN, Aranda DA, Teixeira CM (2015) Comparison between several methods of total lipid extraction from Chlorella vulgaris biomass. Ultrason Sonochem 22:95–99CrossRefGoogle Scholar
  12. Foley SA, Szegezdi E, Mulloy B, Samali A, Tuohy MG (2011) An unfractionated fucoidan from Ascophyllum nodosum: extraction, characterization, and apoptotic effects in vitro. J Nat Prod 74:1851–1861CrossRefGoogle Scholar
  13. Gerasimenko NI, Busarova NG, Moiseenko OP (2010) Seasonal changes in the content of lipids, fatty acids, and pigments in brown alga Costaria costata. Rus J Plant Physiol 57:205–211CrossRefGoogle Scholar
  14. Gosch BJ, Magnusson M, Paul NA, de Nys R (2012) Total lipid and fatty acid composition of seaweeds for the selection of species for oil-based biofuel and bioproducts. GCB Bioenergy 4:919–930CrossRefGoogle Scholar
  15. Gosch BJ, Paul NA, de Nys R, Magnusson M (2015) Seasonal and within-plant variation in fatty acid content and composition in the brown seaweed Spatoglossum macrodontum (Dictyotales, Phaeophyceae). J Appl Phycol 27:387–398CrossRefGoogle Scholar
  16. Guo F, Xu S, Lin Z (2003) Study on decoloration, purification and structure of sodium alginate from Sargassum fusiforme. J Wuxi Univ Light Ind 22:52–56Google Scholar
  17. Heffernan N, Brunton NP, Fitzgerald RJ, Smyth TJ (2015) Profiling of the molecular weight and structural isomer abundance of macroalgae-derived phlorotannins. Mar Drugs 13:509–528CrossRefGoogle Scholar
  18. Hernández-Carmona G, McHugh DJ, López-Gutiérrez F (1999) Pilot plant scale extraction of alginates from Macrocystis pyrifera. 2. Studies on extraction conditions and methods of separating the alkaline-insoluble residue. J Appl Phycol 11:493–502CrossRefGoogle Scholar
  19. Hu P, Li Z, Chen M, Sun Z, Ling Y, Jiang J, Huang C (2016) Structural elucidation and protective role of a polysaccharide from Sargassum fusiforme on ameliorating learning and memory deficiencies in mice. Carbohydr Polym 139:150–158CrossRefGoogle Scholar
  20. Hwang PA, Chien SY, Chan YL, Lu MK, Wu CH, Kong ZL, Wu CJ (2011) Inhibition of lipopolysaccharide (LPS)-induced inflammatory responses by Sargassum hemiphyllum sulfated polysaccharide extract in RAW 264.7 macrophage cells. J Agric Food Chem 59:2062–2068CrossRefGoogle Scholar
  21. Ito K, Hori K (1989) Seaweed: chemical composition and potential food uses. Food Rev Int 5:101–144CrossRefGoogle Scholar
  22. Jin W, Zhang W, Wang J (2014) A study of neuroprotective and antioxidant activities of heteropolysaccharides from six Sargassum species. Int J Biol Macromol 67:336–342CrossRefGoogle Scholar
  23. Jung HA, Jung HJ, Jeong HY, Kwon HJ, Ali MY, Choi JS (2014) Phlorotannins isolated from the edible brown alga Ecklonia stolonifera exert anti-adipogenic activity on 3T3-L1 adipocytes by downregulating C/EBPα and PPARγ. Fitoterapia 92:260–269CrossRefGoogle Scholar
  24. Jurković N, Kolb N, Colić I (1995) Nutritive value of marine algae Laminaria japonica and Undaria pinnatifida. Die Nahrung 39:63–66CrossRefGoogle Scholar
  25. Kang SM, Cha SH, Ko JY, Kang MC, Kim DK, Heo SJ, Kim JS, Heu MS, Kim YT, Jung WK, Jeon YJ (2012) Neuroprotective effects of phlorotannins isolated from a brown alga, Ecklonia cava, against H2O2-induced oxidative stress in murine hippocampal HT22 cells. Environ Toxicol Pharmacol 34:96–105CrossRefGoogle Scholar
  26. Kim JC (2014) Solvent extraction of fucoxanthin from Phaeodactylum tricornutum. Sep Sci Technol 49:410–415CrossRefGoogle Scholar
  27. Kim KN, Ahn G, Heo SJ, Kang SM, Kang MC, Yang HM, Dk K, Roh SW, Kim SK, Jeon BT, Park PJ, Jung WK, Jeon YJ (2013) Inhibition of tumor growth in vitro and in vivo by fucoxanthin against melanoma B16F10 cells. Environ Toxicol Pharmacol 35:39–46CrossRefGoogle Scholar
  28. Kordjazi M, Shabanpour B, Zabihi E, Faramarzi MA, Feizi F, Gavlighi HA, Feghhi MA, Hosseini SA (2013) Sulfated polysaccharides purified from two species of Padina improve collagen and epidermis formation in the rat. Int J Mol Cell Med 2:156–163PubMedPubMedCentralGoogle Scholar
  29. Kumar S, Sahoo D, Levine I (2015) Assessment of nutritional value in a brown seaweed Sargassum wightii and their seasonal variations. Algal Res 9:117–125CrossRefGoogle Scholar
  30. Landa-Cansigno C, Hernández-Carmona G, Arvizu-Higuera DL, Muñoz-Ochoa M, Hernández-Guerrero CJ (2017) Bimonthly variation in the chemical composition and biological activity of the brown seaweed Eisenia arborea (Laminariales: Ochrophyta) from Bahía Magdalena, Baja California Sur, Mexico. J Appl Phycol 29:2605–2615CrossRefGoogle Scholar
  31. Lee SH, Jeon YJ (2013) Anti-diabetic effects of brown algae derived phlorotannins, marine polyphenols through diverse mechanisms. Fitoterapia 86:129–136CrossRefGoogle Scholar
  32. Lee DG, Park SY, Chung WS, Park JH, Hwang E, Mavlonov GT, Kim IH, Kim KY, Yi TH (2015) Fucoidan prevents the progression of osteoarthritis in rats. J Med Food 18:1032–1041CrossRefGoogle Scholar
  33. Li B, Lu F, Wei X, Zhao R (2008) Fucoidan: structure and bioactivity. Molecules 13:1671–1695CrossRefGoogle Scholar
  34. Li L, Ma W, Zhou G (2012) The chemical analysis of S. kjellmanianum in Shandong peninsula. Adv Mater Res 554–556:1884–1888CrossRefGoogle Scholar
  35. Li YJ, Fan JX, Cheng LK, Xu JC, Gao X, Fu XT (2017) Co-extraction and characterization of alginate and fucoidan from two Sargassum fusiforme strains. Sci Technol Food Ind 38:90–95Google Scholar
  36. Liu H, Gu L (2012) Phlorotannins from brown algae (Fucus vesiculosus) inhibited the formation of advanced glycation endproducts by scavenging reactive carbonyls. J Agric Food Chem 60:1326–1334CrossRefGoogle Scholar
  37. Liu N, Fu X, Duan D, Xu J, Gao X, Zhao L (2018) Evaluation of bioactivity of phenolic compounds from the brown seaweed of Sargassum fusiforme and development of their stable emulsion. J Appl Phycol 30:1955–1970CrossRefGoogle Scholar
  38. Lorbeer AJ, Lahnstein J, Fincher GB, Su P, Zhang W (2015) Kinetics of conventional and microwave-assisted fucoidan extractions from the brown alga, Ecklonia radiata. J Appl Phycol 27:2079–2087CrossRefGoogle Scholar
  39. Mackie AR, Macierzanka A, Aarak K (2016) Sodium alginate decreases the permeability of intestinal mucus. Food Hydrocoll 52:749–755CrossRefGoogle Scholar
  40. Marinho-Soriano E, Fonseca PC, Carneiro MA, Moreira WS (2006) Seasonal variation in the chemical composition of two tropical seaweeds. Bioresour Technol 97:2402–2406CrossRefGoogle Scholar
  41. Marudhupandi T, Kumar TTA (2013) Antibacterial effect of fucoidan from Sargassum wightii against the chosen human bacterial pathogens. Int J Curr Pharm Res 2:155–158Google Scholar
  42. Matanjun P, Mohamed S, Mustapha NM, Muhammad K (2009) Nutrient content of tropical edible seaweeds, Eucheuma cottonii, Caulerpa lentillifera and Sargassum polycystum. J Appl Phycol 21:75–80CrossRefGoogle Scholar
  43. Men'shova RV, Ermakova SP, Rachidi SM, Al-Hajje AH, Zvyagintseva TN, Kanaan HM (2012) Seasonal variations of the composition, structural features, and antitumor properties of polysaccharides from Padina pavonica (Lebanon) as a function of composition. Chem Nat Compd 47:870–875CrossRefGoogle Scholar
  44. Ministry of Health of the People’s Republic of China (2013) National food safety standards on maximum levels of contaminants in foods. Standardization Administration of the People's Republic of China, BeijingGoogle Scholar
  45. Miyashita K, Nishikawa S, Beppu F, Tsukui T, Abe M, Hosokawa M (2011) The allenic carotenoid fucoxanthin, a novel marine nutraceutical from brown seaweeds. J Sci Food Agric 91:1166–1174CrossRefGoogle Scholar
  46. Miyashita K, Mikami N, Hosokawa M (2013) Chemical and nutritional characteristics of brown seaweed lipids: a review. J Funct Foods 5:1507–1517CrossRefGoogle Scholar
  47. Murakami K, Yamaguchi Y, Noda K (2011) Seasonal variation in the chemical composition of a marine brown alga, Sargassum horneri (Turner) C. Agardh. J Food Compos Anal 24:231–236CrossRefGoogle Scholar
  48. Nagappan T, Vairappan CS (2014) Nutritional and bioactive properties of three edible species of green algae, genus Caulerpa (Caulerpaceae). J Appl Phycol 26:1019–1027CrossRefGoogle Scholar
  49. Nomura M, Kamogawa H, Susanto E, Kawagoe C, Yasui H, Saga N, Hosokawa M, Miyashita K (2013) Seasonal variations of total lipids, fatty acid composition, and fucoxanthin contents of Sargassum horneri (Turner) and Cystoseira hakodatensis (Yendo) from the northern seashore of Japan. J Appl Phycol 25:1159–1169CrossRefGoogle Scholar
  50. Noviendri D, Jaswir I, Salleh HM, Taher M, Miyashita K, Ramli N (2011) Fucoxanthin extraction and fatty acid analysis of Sargassum binderi and S. duplicatum. J Med Plant Res 5:2405–2412Google Scholar
  51. O’Connell E, Murray P, Piggott C, Hennequart F, Tuohy M (2008) Purification and characterization of a N-acetylglucosaminidase produced by Talaromyces emersonii during growth on algal fucoidan. J Appl Phycol 20:557–565CrossRefGoogle Scholar
  52. Pena-Rodriguez A, Mawhinney TP, Ricque-Marie D, Cruz-Suarez LE (2011) Chemical composition of cultivated seaweed Ulva clathrata(Roth) C. Agardh. Food Chem 129:491–498CrossRefGoogle Scholar
  53. Praiboon J, Palakas S, Noiraksa T, Miyashita K (2018) Seasonal variation in nutritional composition and anti-proliferative activity of brown seaweed, Sargassum oligocystum. J Appl Phycol 30:101–111CrossRefGoogle Scholar
  54. Rioux LE, Turgeon SL, Beaulieu M (2007) Characterization of polysaccharides extracted from brown seaweeds. Carbohydr Polym 69:530–537CrossRefGoogle Scholar
  55. Schiener P, Black KD, Stanley MS, Green DH (2015) The seasonal variation in the chemical composition of the kelp species Laminaria digitata, Laminaria hyperborea, Saccharina latissima and Alaria esculenta. J Appl Phycol 27:363–373CrossRefGoogle Scholar
  56. Simopoulos AP (2002) The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed Pharmacother 56:365–379CrossRefGoogle Scholar
  57. Taboada MC, Millán R, Miguez MI (2013) Nutritional value of the marine algae wakame (Undaria pinnatifida) and nori (Porphyra purpurea) as food supplements. J Appl Phycol 25:1271–1276CrossRefGoogle Scholar
  58. Tanniou A, andanjon L, Incera M, Leon ES, Husa V, Grand JL, Nicolas JL, Poupart N, Kervarec N, Engelen A, Walsh R, Guerard F, Bourgougnon N, Stiger-Pouvreau S (2013) Assessment of the spatial variability of phenolic contents and associated bioactivities in the invasive alga Sargassum muticum sampled along its European range from Norway to Portugal. J Appl Phycol 26:1215–1230Google Scholar
  59. Terasaki M, Hirose A, Narayan B, Baba Y, Kawagoe C, Yasui H, Saga N, Hosokawa M, Miyashita K (2009) Evaluation of recoverable functional lipid components of several brown seaweeds (Phaeophyta) from Japan with special reference to fucoxanthin and fucosterol contents. J Phycol 45:974–980CrossRefGoogle Scholar
  60. Thiex N, Novotny L, Crawford A (2012) Determination of ash in animal feed: AOAC official method 942.05 revisited. J AOAC Int 95:1392–1397CrossRefGoogle Scholar
  61. 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 342:2067–2074CrossRefGoogle Scholar
  62. Wang T, Jonsdottir R, Liu H, Gu L, Kristinsson HG, Raghavan S, Olafsdottir G (2012a) Antioxidant capacities of phlorotannins extracted from the brown algae Fucus vesiculosus. J Agric Food Chem 60:5874–5883CrossRefGoogle Scholar
  63. Wang PP, Zhao XL, Lv YJ, Liu YN, Lang YZ, Wu JD, liu X, Li MM, Yu GL (2012b) Analysis of structural heterogeneity of fucoidan from Hizikia fusiforme by ES-CID-MS/MS. Carbohydr Polym 90:602–607CrossRefGoogle Scholar
  64. Wang C, Liu Y, Lin M (2014) Antitumor effect of phlorotannins from Sargassum fusiforme in S180 sarcoma-bearing mice. J Guangdong Med College 32:614–616Google Scholar
  65. Westermeier R, Murúa P, Patiño DJ, Muñoz L, Ruiz A, Müller DG (2011) Variations of chemical composition and energy content in natural and genetically defined cultivars of Macrocystis from Chile. J Appl Phycol 24:1191–1201CrossRefGoogle Scholar
  66. Wijesinghe W, Jeon YJ (2012) Biological activities and potential industrial applications of fucose rich sulfated polysaccharides and fucoidans isolated from brown seaweeds: a review. Carbohydr Polym 88:13–20CrossRefGoogle Scholar
  67. Wu X, Jiang W, Lu J, Yu Y, Wu B (2014a) Analysis of the monosaccharide composition of water-soluble polysaccharides from Sargassum fusiforme by high performance liquid chromatography/electrospray ionisation mass spectrometry. Food Chem 145:976–983CrossRefGoogle Scholar
  68. Wu X, Wang G, Fu X (2014b) Variations in the chemical composition of Costaria costata during harvest. J Appl Phycol 26:2389–2396CrossRefGoogle Scholar
  69. Wu MT, Su HM, Cui Y, Windust A, Chou HN, Huang CJ (2015) Fucoxanthin enhances chain elongation and desaturation of alpha-linolenic acid in HepG2 cells. Lipids 50:945–953CrossRefGoogle Scholar
  70. Yaich H, Garna H, Besbes S, Paquot M, Blecker C, Attia H (2011) Chemical composition and functional properties of Ulva lactuca seaweed collected in Tunisia. Food Chem 128:895–901CrossRefGoogle Scholar
  71. Yang X, Lu H, Li Y, Liu Y (2013) Antioxidative activities of phlorotannins with different molecular weight extracted from Sargassum fusiforme. Mar Sci 37:47–51Google Scholar
  72. Yin S, Woo H-C, Choi J-H, Park Y-B, Chun B-S (2015) Measurement of antioxidant activities and phenolic and flavonoid contents of the brown seaweed Sargassum horneri: comparison of supercritical CO2 and various solvent extractions. Fish Aquat Sci 18:123–130Google Scholar
  73. Yong YS, Yong WTL, Ng SE, Anton A, Yassir S (2015) Chemical composition of farmed and micropropagated Kappaphycus alvarezii (Rhodophyta, Gigartinales), a commercially important seaweed in Malaysia. J Appl Phycol 27:1271–1275CrossRefGoogle Scholar
  74. Zhang YP, Fang H, Xie QL, Sun JP, Liu R, Hong Z, Yi RZ, Wu H, Yi RZ (2014) Comparative evaluation of the radical-scavenging activities of fucoxanthin and its stereoisomers. Molecules 19:2100–2113CrossRefGoogle Scholar
  75. Zhao XL, Liu XX, Li CX, Yu GL (2016) In vitro and in vivo hypoglycemic effects of brown algal fucoidans. Int J Biol Macromol 82:249–255CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.College of Food Science & EngineeringOcean University of ChinaQingdaoChina
  2. 2.Key Laboratory of Experimental Marine BiologyInstitute of Oceanology, Chinese Academy of SciencesQingdaoChina
  3. 3.State Key Lab of Seaweed Bioactive SubstancesQingdaoChina

Personalised recommendations