High-value products from macroalgae: the potential uses of the invasive brown seaweed, Sargassum muticum

  • John J. Milledge
  • Birthe V. Nielsen
  • David Bailey
Review Paper


Marine seaweeds represent an abundant source of natural products and may harbour valuable chemicals. The brown seaweed Sargassum muticum is an invasive species to the coasts of the British Isles, mainland Europe and North America. Attempts at its eradication and control have generally not been successful, although time-consuming and costly. Commercial exploration of this biomass for food, fuel and pharmaceutical products could encourage its harvesting and control. Though S. muticum might be unsuitable as a source of biofuel due to high ash and water content, this rapidly growing macroalga has a naturally high content of antioxidants, carotenoids and phenols, including the well-known anti-cancer compound fucoxanthin, making this species a potential source of a range of pharmaceutically relevant materials.


Sargassum muticum Seaweed Invasive species Algae Macroalgae Japanese wireweed 



Funding for this project was by a Business Interaction Voucher from the High Value Chemicals from Plants Network (HVCfP a Biotechnology and Biological Sciences Research Council (BBSRC) funded network in industrial biotechnology and bioenergy) supported by IOTA Pharmaceuticals Ltd.


  1. Abidov M, Ramazanov Z, Seifulla R, Grachev S (2010) The effects of Xanthigen in the weight management of obese premenopausal women with non-alcoholic fatty liver disease and normal liver fat. Diabetes Obes Metab 12:72–81. doi: 10.1111/j.1463-1326.2009.01132.x CrossRefGoogle Scholar
  2. Ahn EK, Lee JA, Baik SH, Hong SS, Oh JS (2012) Inhibitory effect of Sargassum muticum (Yendo) Fensholt on adipogenesis in 3T3-L1 cells. J Immunol 188(44):29Google Scholar
  3. Ahn EK, Lee JA, Ko HJ, Hong SS, Oh JS (2013) Anti-obesity effect of Sargassum muticum (Yendo) Fensholt in high fat diet-induced obese mice. J Immunol 190:180Google Scholar
  4. Ale MT, Maruyama H, Tamauchi H, Mikkelsen JD, Meyer AS (2011a) Fucoidan from Sargassum sp. and Fucus vesiculosus reduces cell viability of lung carcinoma and melanoma cells in vitro and activates natural killer cells in mice in vivo. Int J Biol Macromol 49:331–336. doi: 10.1016/j.ijbiomac.2011.05.009 CrossRefGoogle Scholar
  5. Ale MT, Maruyama H, Tamauchi H, Mikkelsen JD, Meyer AS (2011b) Fucose-containing sulfated polysaccharides from brown seaweeds inhibit proliferation of melanoma cells and induce apoptosis by activation of caspase-3 in vitro. Mar Drugs 9:2605–2621. doi: 10.3390/md9122605 CrossRefGoogle Scholar
  6. Alvarado-Morales M, Boldrin A, Karakashev DB, Holdt SL, Angelidaki I, Astrup T (2013) Life cycle assessment of biofuel production from brown seaweed in Nordic conditions. Bioresour Technol 129:92–99. doi: 10.1016/j.biortech.2012.11.029 CrossRefGoogle Scholar
  7. Anastasakis K, Ross AB (2011) Hydrothermal liquefaction of the brown macro-alga Laminaria saccharina: effect of reaction conditions on product distribution and composition. Bioresour Technol 102:4876–4883. doi: 10.1016/j.biortech.2011.01.031 CrossRefGoogle Scholar
  8. Astals S, Musenze RS, Bai X, Tannock S, Tait S, Pratt S, Jensen PD (2015) Anaerobic co-digestion of pig manure and algae: impact of intracellular algal products recovery on co-digestion performance. Bioresour Technol 181:97–104. doi: 10.1016/j.biortech.2015.01.039 CrossRefGoogle Scholar
  9. Azizi S, Ahmad MB, Namvar F, Mohamad R (2014) Green biosynthesis and characterization of zinc oxide nanoparticles using brown marine macroalga Sargassum muticum aqueous extract. Mater Lett 116:275–277. doi: 10.1016/j.matlet.2013.11.038 CrossRefGoogle Scholar
  10. Bae DY, Ang PO, Boo SM (2013) Mitochondrial cox3 and trnW-I sequence diversity of Sargassum muticum. Aqua Bot 104:220–223. doi: 10.1016/j.aquabot.2012.09.007 CrossRefGoogle Scholar
  11. Baghel RS, Trivedi N, Gupta V, Neori A, Chennur RR, Lali AM, Jha B (2015) Biorefining of marine macroalgal biomass for production of biofuel and commodity chemicals. Green Chem. doi: 10.1039/C4GC02532F Google Scholar
  12. Bahadar A, Bilal Khan MB (2013) Progress in energy from microalgae: a review. Renew Sustain Energy Rev 27:128–148. doi: 10.1016/j.rser.2013.06.029 CrossRefGoogle Scholar
  13. Balboa EM, Rivas S, Moure A, Dominguez H, Parajo JC (2013) Simultaneous extraction and depolymerization of fucoidan from Sargassum muticum in aqueous media. Mar Drugs 11:4612–4627. doi: 10.3390/md11114612 CrossRefGoogle Scholar
  14. Balboa EM et al (2014) Potential of antioxidant extracts produced by aqueous processing of renewable resources for the formulation of cosmetics. Ind Crops Prod 58:104–110. doi: 10.1016/j.indcrop.2014.03.041 CrossRefGoogle Scholar
  15. Balboa E, Moure A, Domínguez H (2015) Valorization of Sargassum muticum biomass according to the biorefinery concept. Mar Drugs 13:3745CrossRefGoogle Scholar
  16. Banks C, Zhang Y (2010) Optimising inputs and outputs from anaerobic digestion processes. Technical report. DefraGoogle Scholar
  17. Bazes A et al (2009) Investigation of the antifouling constituents from the brown alga Sargassum muticum (Yendo) Fensholt. J Appl Phycol 21:395–403. doi: 10.1007/s10811-008-9382-9 CrossRefGoogle Scholar
  18. Becker EW (2007) Micro-algae as a source of protein. Biotechnol Adv 25:207–210. doi: 10.1016/j.biotechadv.2006.11.002 CrossRefGoogle Scholar
  19. 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. doi: 10.1093/glycob/cwg058 CrossRefGoogle Scholar
  20. Biomara (2014) A short history of seaweed exploitation in the western British Isles http://www.biomara.org/understanding-seaweed/the-importance-of-seaweed-across-the-ages. Accessed 27 Jan 2014
  21. Bixler H, Porse H (2011) A decade of change in the seaweed hydrocolloids industry. J Appl Phycol 23:321–335. doi: 10.1007/s10811-010-9529-3 CrossRefGoogle Scholar
  22. Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR (2015) Marine natural products. Nat Prod Rep 32:116–211. doi: 10.1039/c4np00144c CrossRefGoogle Scholar
  23. Boonstra AS (2014) A comprehensive review and a prospective study of future macroalgae-based biorefinery systems. Utrecht University, UtrechtGoogle Scholar
  24. Booth E (1969) The manufacture and properties of liquid seaweed extracts. Paper presented at the Proceedings of the International Seaweed Symposium Google Scholar
  25. Borowitzka MA (1995) Microalgae as sources of pharmaceuticals and other biologically active compounds. J Appl Phycol 7:3–15CrossRefGoogle Scholar
  26. Brennan L, Owende P (2010) Biofuels from microalgae—a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sustain Energy Rev 14:557–577. doi: 10.1016/j.rser.2009.10.009 CrossRefGoogle Scholar
  27. Brkljača R, Urban S (2014) Chemical profiling (HPLC-NMR & HPLC-MS), isolation, and identification of bioactive meroditerpenoids from the Southern Australian marine brown alga Sargassum paradoxum. Mar Drugs 13:102–127CrossRefGoogle Scholar
  28. Bruton T, Lyons H, Lerat Y, Stanley M, Rasmussen MB (2009) A review of the potential of marine algae as a source of biofuel in Ireland. Sustain Energy Ireland, DublinGoogle Scholar
  29. CABI (2011) Sargassum muticum in invasive species compendium. CAB International, WallingfordGoogle Scholar
  30. Carro L, Barriada JL, Herrero R, de Vicente MES (2015) Interaction of heavy metals with Ca-pretreated Sargassum muticum algal biomass: characterization as a cation exchange process. Chem Eng J 264:181–187. doi: 10.1016/j.cej.2014.11.079 CrossRefGoogle Scholar
  31. Chae D et al (2013) Apo-9′-Fucoxanthinone, Isolated from Sargassum muticum, inhibits CpG-induced inflammatory response by attenuating the mitogen-activated protein kinase pathway. Mar Drugs 11:3272–3287. doi: 10.3390/md11093272 CrossRefGoogle Scholar
  32. Chen SH, Zhao Y, Zhang Y, Zhang DH (2014a) Fucoidan induces cancer cell apoptosis by modulating the endoplasmic reticulum stress cascades. PLoS ONE. doi: 10.1371/journal.pone.0108157 Google Scholar
  33. Chen Z et al (2014b) 24(S)-saringosterol from edible marine seaweed Sargassum fusiforme is a novel selective LXR beta agonist. J Agric Food Chem 62:6130–6137. doi: 10.1021/jf500083r CrossRefGoogle Scholar
  34. Chen H, Zhou D, Luo G, Zhang S, Chen J (2015) Macroalgae for biofuels production: progress and perspectives. Renew Sustain Energy Rev 47:427–437. doi: 10.1016/j.rser.2015.03.086 CrossRefGoogle Scholar
  35. Cheow WS, Hadinoto K (2013) Biofilm-like Lactobacillus rhamnosus probiotics encapsulated in alginate and carrageenan microcapsules exhibiting enhanced thermotolerance and freeze-drying resistance. Biomacromolecules 14:3214–3222. doi: 10.1021/bm400853d CrossRefGoogle Scholar
  36. Cherubini F (2010) The biorefinery concept: using biomass instead of oil for producing energy and chemicals. Energy Conv Manag 51:1412–1421. doi: 10.1016/j.enconman.2010.01.015 CrossRefGoogle Scholar
  37. Chynoweth DP (2002) Review of biomethane from marine biomass. Department of Agricultural and Biological Engineering, University of Florida, GainesvilleGoogle Scholar
  38. Chynoweth DP (2005) Renewable biomethane from land and ocean energy crops and organic wastes. HortScience 40:283–286Google Scholar
  39. Clifton P (2009) Lowering cholesterol—a review on the role of plant sterols. Aust Fam Phys 38:218–221Google Scholar
  40. Cock JM et al (2010) The Ectocarpus genome and the independent evolution of multicellularity in brown algae. Nature 465:617–621. doi: 10.1038/nature09016 CrossRefGoogle Scholar
  41. Commission European (2014) Eurostat handbook for annual crop statistics. Eurostat, LuxembourgGoogle Scholar
  42. Cook EJ, Jenkins S, Maggs C, Minchin D, Mineur F, Nall C, Sewell J (2013) Impacts of climate change on non-native species. MCCIP Sci Rev. doi: 10.14465/2013.arc17.155-166 Google Scholar
  43. Critchley AT, Farnham WF, Morrell SL (1986) An account of the attempted control of an introduced marine alga, Sargassum-muticum, in southern England. Biol Conserv 35:313–332. doi: 10.1016/0006-3207(86)90092-3 CrossRefGoogle Scholar
  44. Critchley AT, Devisscher PRM, Nienhuis PH (1990) Canopy characteristics of the brown alga Sargassum-muticum (fucales, phaeophyta) in lake Grevelingen, southwest Netherlands. Hydrobiologia 204:211–217. doi: 10.1007/bf00040236 CrossRefGoogle Scholar
  45. Dang VT, Li Y, Speck P, Benkendorff K (2011) Effects of micro and macroalgal diet supplementations on growth and immunity of greenlip abalone, Haliotis laevigata. Aquaculture 320:91–98. doi: 10.1016/j.aquaculture.2011.08.009 CrossRefGoogle Scholar
  46. Davison DM (2009) Sargassum muticum in Scotland 2008: a review of information, issues and implications. vol Commissioned Report No.324 (ROAME No. R07AC707). Scottish Natural HeritageGoogle Scholar
  47. Edwards M, Watson L (2011) Aquaculture explained cultivating Laminaria digitata. Irish Sea Fisheries Board, DunlaoghaireGoogle Scholar
  48. Edwards M et al (2014) Microalgae fact-sheets. NUI, GalwayGoogle Scholar
  49. Engelen A, Santos R (2009) Which demographic traits determine population growth in the invasive brown seaweed Sargassum muticum? J Ecol 97:675–684. doi: 10.1111/j.1365-2745.2009.01501.x CrossRefGoogle Scholar
  50. Enquist-Newman M et al (2014) Efficient ethanol production from brown macroalgae sugars by a synthetic yeast platform. Nature 505:239. doi: 10.1038/nature12771 CrossRefGoogle Scholar
  51. Environment and Heritage Service NI (2007) Environmentally sustainable seaweed harvesting in Northern Ireland. Environment and Heritage Service, BelfastGoogle Scholar
  52. Farvin KHS, Jacobsen C (2013) Phenolic compounds and antioxidant activities of selected species of seaweeds from Danish coast. Food Chem 138:1670–1681. doi: 10.1016/j.foodchem.2012.10.078 CrossRefGoogle Scholar
  53. Fletcher RL, Fletcher SM (1975) Studies on the recently introduced brown Alga Sargassum muticum (Yendo) fensholt I. Ecology and reproduction. Bot Mar 18:149–156. doi: 10.1515/botm.1975.18.3.149 Google Scholar
  54. Gammone MA, Riccioni G, D’Orazio N (2015) Carotenoids: potential allies of cardiovascular health? Food Nutr Res 59:26762. doi: 10.3402/fnr.v59.26762 CrossRefGoogle Scholar
  55. Genser B et al (2012) Plant sterols and cardiovascular disease: a systematic review and meta-analysis (dagger). Eur Heart J 33:444–451. doi: 10.1093/eurheartj/ehr441 CrossRefGoogle Scholar
  56. Gerasimenko NI, Martyyas EA, Logvinov SV, Busarova NG (2014) Biological activity of lipids and photosynthetic pigments of Sargassum pallidum C. Agardh. Appl Biochem Microbiol 50:73–81. doi: 10.1134/S0003683814010037 CrossRefGoogle Scholar
  57. Gibbs BF, Kermasha S, Alli I, Mulligan CN (1999) Encapsulation in the food industry: a review. Int J Food Sci Nutr 50:213–224CrossRefGoogle Scholar
  58. Gibson CE (2011) Northern Ireland State of the seas report. Agri-Food and Biosciences Institute, BelfastGoogle Scholar
  59. Golueke CG, Oswald WJ, Gotaas HB (1957) Anaerobic digestion of algae. Appl Microbiol 5:47–55Google Scholar
  60. Gonzalez-Delgado AD, Kafarov V (2011) Microalgae based biorefinery: issues to consider. CT&F Cienc Tecnol Futuro 4:5–21Google Scholar
  61. Gonzalez-Lopez N, Moure A, Dominguez H (2012) Hydrothermal fractionation of Sargassum muticum biomass. J Appl Phycol 24:1569–1578. doi: 10.1007/s10811-012-9817-1 CrossRefGoogle Scholar
  62. Gorham J, Lewey SA (1984) Seasonal changes in the chemical composition of Sargassum muticum. Mar Biol 80:103–107. doi: 10.1007/BF00393133 CrossRefGoogle Scholar
  63. Guiry MD (2014) The seaweed site: information on marine algae. http://www.seaweed.ie/uses_general/agars.php. Accessed 27 Feb 2014
  64. Gupta S, Abu-Ghannam N (2011) Bioactive potential and possible health effects of edible brown seaweeds. Trends Food Sci Technol 22:315–326. doi: 10.1016/j.tifs.2011.03.011 CrossRefGoogle Scholar
  65. Hannon M, Gimpel J, Tran M, Rasala B, Mayfield S (2010) Biofuels from algae: challenges and potential. Biofuels 1:763–784CrossRefGoogle Scholar
  66. Hardouin K et al (2014) Biochemical and antiviral activities of enzymatic hydrolysates from different invasive French seaweeds. J Appl Phycol 26:1029–1042. doi: 10.1007/s10811-013-0201-6 CrossRefGoogle Scholar
  67. Hellio C, De La Broise D, Dufosse L, Le Gal Y, Bourgougnon N (2001) Inhibition of marine bacteria by extracts of macroalgae: potential use for environmentally friendly antifouling paints. Mar Environ Res 52:231–247. doi: 10.1016/s0141-1136(01)00092-7 CrossRefGoogle Scholar
  68. Holdt S, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597. doi: 10.1007/s10811-010-9632-5 CrossRefGoogle Scholar
  69. Horn SV (2000) Bioenergy from brown seaweeds. Norwegian University of Science and Technology NTNU, TrondheimGoogle Scholar
  70. Horn SJ, Aasen IM, Ostgaard K (2000) Ethanol production from seaweed extract. J Ind Microbiol Biotechnol 25:249–254. doi: 10.1038/sj.jim.7000065 CrossRefGoogle Scholar
  71. Huang G, Chen F, Wei D, Zhang X, Chen G (2010) Biodiesel production by microalgal biotechnology. Appl Energy 87:38–46. doi: 10.1016/j.apenergy.2009.06.016 CrossRefGoogle Scholar
  72. Hughes A (2014) Scottish seaweed aquaculture; research, development and commercialisation. Paper presented at the Seaweed for Biofuel: towards a sustainable seaweed supply chain, ObanGoogle Scholar
  73. Hur S, Lee H, Kim Y, Lee B-H, Shin J, Kim T-Y (2008) Sargaquinoic acid and sargachromenol, extracts of Sargassum sagamianum, induce apoptosis in HaCaT cells and mice skin: its potentiation of UVB-induced apoptosis. Eur J Pharmacol 582:1–11. doi: 10.1016/j.ejphar.2007.12.025 CrossRefGoogle Scholar
  74. Iofina (2011) Iodine. http://www.iofina.com/mid-stream-iodine-business/iodine. Accessed 27 Jan 2014
  75. Jard G, Marfaing H, Carrere H, Delgenes JP, Steyer JP, Dumas C (2013) French Brittany macroalgae screening: composition and methane potential for potential alternative sources of energy and products. Bioresour Technol 144:492–498. doi: 10.1016/j.biortech.2013.06.114 CrossRefGoogle Scholar
  76. Joana Gil-Chávez G, Villa JA, Fernando Ayala-Zavala J, Basilio Heredia J, Sepulveda D, Yahia EM, González-Aguilar GA (2013) Technologies for extraction and production of bioactive compounds to be used as nutraceuticals and food ingredients: an overview. Compr Rev Food Sci Food Saf 12:5–23. doi: 10.1111/1541-4337.12005 CrossRefGoogle Scholar
  77. Jung KA, Lim SR, Kim Y, Park JM (2013) Potentials of macroalgae as feedstocks for biorefinery. Bioresour Technol 135:182–190. doi: 10.1016/j.biortech.2012.10.025 CrossRefGoogle Scholar
  78. Kelly MS, Dworjanyn S (2008) The potential of marine biomass for anaerobic biogas production a feasibility study with recommendations for further research. The Crown Estate on Behalf of the Marine Estate, ScotlandGoogle Scholar
  79. Kent Wildlife Trust (2006) Have you seen you seen these species on the shores around Kent or Sussex? Available at http://www.pevenseybay.co.uk/resources/pdf/BAR%20Have%20you%20seen%20these.pdf
  80. Kozak LP, Anunciado-Koza R (2008) UCP1: its involvement and utility in obesity. Int J Obes 32:S32–S38CrossRefGoogle Scholar
  81. Kraan S (2013) Mass-cultivation of carbohydrate rich macroalgae, a possible solution for sustainable biofuel production. Mitig Adapt Strateg Glob Change 18:27–46. doi: 10.1007/s11027-010-9275-5 CrossRefGoogle Scholar
  82. Kumar SR, Hosokawa M, Miyashita K (2013) Fucoxanthin: a marine carotenoid exerting anti-cancer effects by affecting multiple mechanisms. Mar Drugs 11:5130–5147. doi: 10.3390/md11125130 CrossRefGoogle Scholar
  83. Le Lann K, Jegou C, Stiger-Pouvreau V (2008) Effect of different conditioning treatments on total phenolic content and antioxidant activities in two Sargassacean species: comparison of the frondose Sargassum muticum (Yendo) Fensholt and the cylindrical Bifurcaria bifurcata R. Ross Phycol Res 56:238–245. doi: 10.1111/j.1440-1835.2008.00505.x CrossRefGoogle Scholar
  84. Leal MC et al (2013) Biogeography and biodiscovery hotspots of macroalgal marine natural products. Nat Prod Rep 30:1380–1390. doi: 10.1039/c3np70057g CrossRefGoogle Scholar
  85. Liu F, Pang S (2014) Complete mitochondrial genome of the invasive brown alga Sargassum muticum (Sargassaceae, Phaeophyceae). Mitochondrial DNA. doi: 10.3109/19401736.2014.933333 Google Scholar
  86. Liu L, Heinrich M, Myers S, Dworjanyn SA (2012) Towards a better understanding of medicinal uses of the brown seaweed Sargassum in Traditional Chinese Medicine: a phytochemical and pharmacological review. J Ethnopharmacol 142:591–619. doi: 10.1016/j.jep.2012.05.046 CrossRefGoogle Scholar
  87. Liu F, Pang SJ, Gao SQ, Shan TF (2013) Intraspecific genetic analysis, gamete release performance, and growth of Sargassum muticum (Fucales, Phaeophyta) from China. Chin J Ocean Limnol 31:1268–1275. doi: 10.1007/s00343-013-2314-9 CrossRefGoogle Scholar
  88. Liu F, Pang S, Luo M (2014) Complete mitochondrial genome of the brown alga Sargassum fusiforme (Sargassaceae, Phaeophyceae): genome architecture and taxonomic consideration. Mitochondrial DNA. doi: 10.3109/19401736.2014.936417 Google Scholar
  89. Lodeiro P, Cordero B, Grille Z, Herrero R, de Vicente MES (2004) Physicochemical studies of cadmium(II) biosorption by the invasive alga in Europe, Sargassum muticum. Biotechnol Bioeng 88:237–247. doi: 10.1002/bit.20229 CrossRefGoogle Scholar
  90. Lundquist TJ, Woertz IC, Quinn NWT, Benemann JR (2010) A realistic technology and engineering assessment of algae biofuel production. Energy Biosciences Inst, BerkeleyGoogle Scholar
  91. Maeda H (2015) Nutraceutical effects of fucoxanthin for obesity and diabetes therapy: a review. J Oleo Sci 64:125–132. doi: 10.5650/jos.ess14226 CrossRefGoogle Scholar
  92. Marquez GPB, Santianez WJE, Trono GC, Montano MNE, Araki H, Takeuchi H, Hasegawa T (2014) Seaweed biomass of the Philippines: sustainable feedstock for biogas production. Renew Sust Energ Rev 38:1056–1068. doi: 10.1016/j.rser.2014.07.056 CrossRefGoogle Scholar
  93. Mattio L, Payri CE (2011) 190 years of Sargassum taxonomy, facing the advent of DNA phylogenies. Bot Rev 77:31–70. doi: 10.1007/s12229-010-9060-x CrossRefGoogle Scholar
  94. McHugh DJ (2003) A guide to the seaweed industry. FAO, RomeGoogle Scholar
  95. McLaren J (2009) Sugarcane as a feedstock for biofuels: an analytical white paper. Medway Swale Estuary Partnership (ND) In: The water. Accessed 22 April 2014Google Scholar
  96. Mikami K, Hosokawa M (2013) Biosynthetic pathway and health benefits of fucoxanthin, an algae-specific xanthophyll in brown seaweeds. Int J Mol Sci 14:13763–13781CrossRefGoogle Scholar
  97. Milledge JJ (2011) Commercial application of microalgae other than as biofuels: a brief review. Rev Environ Sci Biotechnol 10:31–41. doi: 10.1007/s11157-010-9214-7 CrossRefGoogle Scholar
  98. Milledge JJ (2012) Microalgae—commercial potential for fuel, food and feed. Food Sci Technol 26:26–28Google Scholar
  99. Milledge JJ, Heaven S (2014) Methods of energy extraction from microalgal biomass: a review. Rev Environ Sci Biotechnol 13:301–320. doi: 10.1007/s11157-014-9339-1 CrossRefGoogle Scholar
  100. Milledge JJ, Smith B, Dyer P, Harvey P (2014) Macroalgae-derived biofuel: a review of methods of energy extraction from seaweed. Biomass Energ 7:7194–7222Google Scholar
  101. Milledge JJ, Staple A, Harvey P (2015) Slow pyrolysis as a method for the destruction of Japanese wireweed, Sargassum muticum. Environ Nat Resour Res 5:28–36. doi: 10.5539/enrr.v5n1p28 Google Scholar
  102. Misra MK, Ragland KW, Baker AJ (1993) Wood ash composition as a function of furnace temperature. Biomass Bioenergy 4:103–116. doi: 10.1016/0961-9534(93)90032-y CrossRefGoogle Scholar
  103. 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 91:1166–1174. doi: 10.1002/jsfa.4353 CrossRefGoogle Scholar
  104. Miyoshi E, Moriwaki K, Nakagawa T (2008) Biological function of fucosylation in cancer biology. J Biochem 143:725–729. doi: 10.1093/jb/mvn011 CrossRefGoogle Scholar
  105. Moorthi PV, Balasubramanian C, Mohan S (2015) An improved insecticidal activity of silver nanoparticle synthesized by using Sargassum muticum. Appl Biochem Biotechnol 175:135–140. doi: 10.1007/s12010-014-1264-9 CrossRefGoogle Scholar
  106. Murphy F, Devlin G, Deverell R, McDonnell K (2013) Biofuel production in Ireland—an approach to 2020 targets with a focus on algal biomass. Energies 6:6391–6412CrossRefGoogle Scholar
  107. Murphy C, Hotchkiss S, Worthington J, McKeown S (2014) The potential of seaweed as a source of drugs for use in cancer chemotherapy. J Appl Phycol. doi: 10.1007/s10811-014-0245-2 Google Scholar
  108. Nallathambi Gunaseelan V (1997) Anaerobic digestion of biomass for methane production: a review. Biomass Bioenergy 13:83–114. doi: 10.1016/S0961-9534(97)00020-2 CrossRefGoogle Scholar
  109. Namvar F, Mohamad R, Baharara J, Zafar-Balanejad S, Fargahi F, Rahman HS (2013) Antioxidant, antiproliferative, and antiangiogenesis effects of polyphenol-rich seaweed (Sargassum muticum). BioMed Res Int 2013:9. doi: 10.1155/2013/604787 CrossRefGoogle Scholar
  110. Namvar F et al (2014) Cytotoxic effect of magnetic iron oxide nanoparticles synthesized via seaweed aqueous extract. Int J Nanomed 9:2479–2488. doi: 10.2147/ijn.s59661 CrossRefGoogle Scholar
  111. Necas J, Bartosikova L (2013) Carrageenan: a review. Vet Med 58:187–205Google Scholar
  112. Nguyen H, Heaven S, Banks C (2014) Energy potential from the anaerobic digestion of food waste in municipal solid waste stream of urban areas in Vietnam. Int J Energy Environ Eng 5:365–374. doi: 10.1007/s40095-014-0133-1 CrossRefGoogle Scholar
  113. Oak JH, Suh Y, Lee IK (2002) Phylogenetic relationships of Sargassum subgenus Bactrophycus (Sargassaceae, Phaeophyceae) inferred from rDNA ITS sequences. Algae 17:235–247CrossRefGoogle Scholar
  114. Olguin EJ (2012) Dual purpose microalgae–bacteria-based systems that treat wastewater and produce biodiesel and chemical products within a biorefinery. Biotechnol Adv 30:1031–1046. doi: 10.1016/j.biotechadv.2012.05.001 CrossRefGoogle Scholar
  115. Oliveira JV, Alves MM, Costa JC (2015) Optimization of biogas production from Sargassum sp. using a design of experiments to assess the co-digestion with glycerol and waste frying oil. Bioresour Technol 175:480–485. doi: 10.1016/j.biortech.2014.10.121 CrossRefGoogle Scholar
  116. Oswald WJ (1988) Large-scale algal culture systems (Engineering aspects). In: Borowitzka MA, Borowitzka LJ (eds) Micro-algal biotechnology. Cambridge University Press, CambridgeGoogle Scholar
  117. Pagliaro M, Rossi M, Royal Society of C (2008) The future of glycerol: new uses of a versatile raw material. Royal Society of Chemistry, CambridgeGoogle Scholar
  118. Pang ZC, Otaka K, Maoka T, Hidaka K, Ishijima S, Oda M, Ohnishi M (2005) Structure of ss-glucan oligomer from laminarin and its effect on human monocytes to inhibit the proliferation of U937 cells. Biosci Biotechnol Biochem 69:553–558. doi: 10.1271/bbb.69.553 CrossRefGoogle Scholar
  119. Park YS, Seo IS, Lee SJ, Lee SP (2015) Study on the health benefits of brown algae (Sargassum muticum) in volunteers. J Food Nutr Res 3:126–130. doi: 10.12691/jfnr-3-2-9 CrossRefGoogle Scholar
  120. Pereira L (2011) A review of the nutrient composition of selected edible seaweeds. In: Pomin VH (ed) Seaweed. Nova Science Publishers, HauppaugeGoogle Scholar
  121. Perez-Lopez P, Balboa EM, Gonzalez-Garcia S, Dominguez H, Feijoo G, Moreira MT (2014) Comparative environmental assessment of valorization strategies of the invasive macroalgae Sargassum muticum. Bioresour Technol 161:137–148. doi: 10.1016/j.biortech.2014.03.013 CrossRefGoogle Scholar
  122. Philippsen A (2013) Energy input, carbon intensity, and cost for ethanol produced from brown seaweed. University of Victoria, VictoriaGoogle Scholar
  123. Phillips N et al (2011) Estimates of nuclear DNA content in 98 species of brown algae (Phaeophyta). Aob Plants. doi: 10.1093/aobpla/plr001 Google Scholar
  124. Piao MJ et al (2011) Protective effect of the ethyl acetate fraction of Sargassum muticum against ultraviolet B-irradiated damage in human keratinocytes. Int J Mol Sci 12:8146–8160. doi: 10.3390/ijms12118146 CrossRefGoogle Scholar
  125. Piao MJ et al (2014) The ethyl acetate fraction of Sargassum muticum attenuates ultraviolet B radiation-induced apoptotic cell death via regulation of MAPK- and caspase-dependent signaling pathways in human HaCaT keratinocytes. Pharm Biol 52:1110–1118. doi: 10.3109/13880209.2013.879186 CrossRefGoogle Scholar
  126. Pires JCM, Alvim-Ferraz MCM, Martins FG, Simoes M (2012) Carbon dioxide capture from flue gases using microalgae: engineering aspects and biorefinery concept. Renew Sust Energy Rev 16:3043–3053. doi: 10.1016/j.rser.2012.02.055 CrossRefGoogle Scholar
  127. Pizzolla P (2008) Sargassum muticum. Wireweed. Marine life information network: biology and sensitivity key information sub-programme. Marine Biological Association of the United Kingdom. http://www.marlin.ac.uk/speciesinformation.php?speciesID=4296. Accessed 02/05 2015 (online)
  128. Plouguerne E, Le Lann K, Connan S, Jechoux G, Deslandes E, Stiger-Pouvreau V (2006) Spatial and seasonal variation in density, reproductive status, length and phenolic content of the invasive brown macroalga Sargassum muticum (Yendo) Fensholt along the coast of Western Brittany (France). Aquat Bot 85:337–344. doi: 10.1016/j.aquabot.2006.06.011 CrossRefGoogle Scholar
  129. Plouguerne E, Hellio C, Deslandes E, Veron B, Stiger-Pouvreau V (2008) Anti-microfouling activities in extracts of two invasive algae: Grateloupia turuturu and Sargassum muticum. Bot Mar 51:202–208. doi: 10.1515/bot.2008.026 CrossRefGoogle Scholar
  130. Plouguerne E et al (2010) Anti-microfouling Activity of Lipidic Metabolites from the Invasive Brown Alga Sargassum muticum (Yendo) Fensholt. Mar Biotechnol 12:52–61. doi: 10.1007/s10126-009-9199-9 CrossRefGoogle Scholar
  131. Plouguerné E, Da Gama BAP, Pereira RC, Barreto-Bergter E (2014) Glycolipids from seaweeds and their potential biotechnological applications Frontiers in cellular and infection. Microbiology. doi: 10.3389/fcimb.2014.00174 Google Scholar
  132. Pomin VH (2014) Marine medicinal glycomics Frontiers in cellular and infection. Microbiology. doi: 10.3389/fcimb.2014.00005 Google Scholar
  133. Rabinovich GA, van Kooyk Y, Cobb BA, Annals NYAS (2012) Glycobiology of immune responses Glycobiology of the Immune. Response 1253:1–15. doi: 10.1111/j.1749-6632.2012.06492.x Google Scholar
  134. Rajkumar R, Yaakob Z, Takriff MS (2014) Potential of the micro and macro algae for biofuel production: a brief review. BioResources 9:1606–1633Google Scholar
  135. Rappleye CA, Eissenberg LG, Goldman WE (2007) Histoplasma capsulatum alpha-(1,3)-glucan blocks innate immune recognition by the beta-glucan receptor. Proc Nat Acad Sci USA 104:1366–1370. doi: 10.1073/pnas.0609848104 CrossRefGoogle Scholar
  136. Rawat I, Ranjith Kumar R, Mutanda T, Bux F (2013) Biodiesel from microalgae: a critical evaluation from laboratory to large scale production. Appl Energy 103:444–467. doi: 10.1016/j.apenergy.2012.10.004 CrossRefGoogle Scholar
  137. Rehm BHA (ed) (2009) Alginates: biology and applications. In: Microbiology monographs, vol 13, Springer, Heidelberg. doi: 10.1007/978-3-540-92679-5
  138. Rodrigues D et al (2015) Chemical composition of red, brown and green macroalgae from Buarcos bay in Central West Coast of Portugal. Food Chem 183:197–207. doi: 10.1016/j.foodchem.2015.03.057 CrossRefGoogle Scholar
  139. Rodriguez-Jasso RM, Mussatto SI, Pastrana L, Aguilar CN, Teixeira JA (2014) Chemical composition and antioxidant activity of sulphated polysaccharides extracted from Fucus vesiculosus using different hydrothermal processes. Chem Pap 68:203–209. doi: 10.2478/s11696-013-0430-9 CrossRefGoogle Scholar
  140. Roesijadi G, Copping AE, Huesemann MH, Foster J, Benemann JR (2010a) Techno-economic feasibility analysis of offshore seaweed farming for bioenergy and biobased products. U.S. Department of Energy, WashingtonGoogle Scholar
  141. Roesijadi G, Jones SB, Snowden-Swan LJ, Zhu Y (2010b) Macroalgae as a biomass feedstock: a preliminary analysis. U.S. Department of Energy, WashingtonCrossRefGoogle Scholar
  142. Rose C (2013) Seaweed: a future food? Actually, a food of the present! Food Sci Technol 27:26–30Google Scholar
  143. Ross AB, Jones JM, Kubacki ML, Bridgeman T (2008) Classification of macroalgae as fuel and its thermochemical behaviour. Bioresour Technol 99:6494–6504. doi: 10.1016/j.biortech.2007.11.036 CrossRefGoogle Scholar
  144. Rubin E, Rodriguez P, Herrero R, Cremades J, Barbara I, de Vicente MES (2005) Removal of methylene blue from aqueous solutions using as biosorbent Sargassum muticum: an invasive macroalga in Europe. J Chem Technol Biotechnol 80:291–298. doi: 10.1002/jctb.1192 CrossRefGoogle Scholar
  145. Rubin E, Rodriguez P, Herrero R, de Vicente MES (2006) Biosorption of phenolic compounds by the brown alga Sargassum muticum. J Chem Technol Biotechnol 81:1093–1099. doi: 10.1002/jctb.1430 CrossRefGoogle Scholar
  146. Ruperez P (2002) Mineral content of edible marine seaweeds. Food Chem 79:23–26. doi: 10.1016/s0308-8146(02)00171-1 CrossRefGoogle Scholar
  147. Saidur R, Abdelaziz EA, Demirbas A, Hossain MS, Mekhilef S (2011) A review on biomass as a fuel for boilers. Renew Sust Energ Rev 15:2262–2289. doi: 10.1016/j.rser.2011.02.015 CrossRefGoogle Scholar
  148. Scottish Natural Heritage (2012) Seaweed harvesting. http://www.snh.gov.uk/land-and-sea/managing-coasts-and-sea/seaweed-harvesting/. Accessed 07 Aug 2015
  149. Service RF (2011) Algae’s second try. Science 333:1238–1239CrossRefGoogle Scholar
  150. Sewell JM, Mayer I, Langdon SP, Smyth JF, Jodrell DI (2005) The mechanism of action of Kahalalide F: variable cell permeability in human hepatoma cell lines. Eur J Cancer (Oxford, England : 1990) 41:1637–1644. doi: 10.1016/j.ejca.2005.04.015 CrossRefGoogle Scholar
  151. Shekhar SHS, Lyons G, McRoberts C, McCall D, Carmichael E, Andrews F, McCormack R (2012) Brown seaweed species from Strangford Lough: compositional analyses of seaweed species and biostimulant formulations by rapid instrumental methods. J Appl Phycol 24:1141–1157. doi: 10.1007/s10811-011-9744-6 CrossRefGoogle Scholar
  152. Silkina A, Bazes A, Vouve F, Le Tilly V, Douzenel P, Mouget JL, Bourgougnon N (2009) Antifouling activity of macroalgal extracts on Fragilaria pinnata (Bacillariophyceae): a comparison with Diuron. Aquat Toxicol 94:245–254. doi: 10.1016/j.aquatox.2009.07.004 CrossRefGoogle Scholar
  153. Silva J, Alves C, Pinteus S, Horta A, Pedrosa R (2013) High antioxidant activity of Sargassum muticum and Padina pavonica collected from Peniche coast (Portugal). Curr Opin Biotechnol 24:S116–S116. doi: 10.1016/j.copbio.2013.05.361 CrossRefGoogle Scholar
  154. Singh U, Ahluwalia A (2013) Microalgae: a promising tool for carbon sequestration. Mitig Adapt Strateg Glob Change 18:73–95. doi: 10.1007/s11027-012-9393-3 CrossRefGoogle Scholar
  155. Smit A (2004) Medicinal and pharmaceutical uses of seaweed natural products: a review. J Appl Phycol 16:245–262. doi: 10.1023/B:JAPH.0000047783.36600.ef CrossRefGoogle Scholar
  156. Smit LE, Schonfeldt HC, de Beer WHJ (2004) Comparison of the energy values of different dairy products obtained by various methods. J Food Compos Anal 17:361–370. doi: 10.1016/j.jfca.2004.02.006 CrossRefGoogle Scholar
  157. Soto M, Vazquez MA, de Vega A, Vilarino JM, Fernandez G, de Vicente ME (2015) Methane potential and anaerobic treatment feasibility of Sargassum muticum. Bioresour Technol 189:53–61. doi: 10.1016/j.biortech.2015.03.074 CrossRefGoogle Scholar
  158. Spolaore P, Joannis-Cassan C, Duran E, Isambet A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96CrossRefGoogle Scholar
  159. Sridhar S, Rengasamy R (2011) Potential of seaweed liquid fertilizers (SLFS) on some agricultural crop with special reference to protein profile of seedlings. Int J Dev Res 1:55–57Google Scholar
  160. Stiger V, Horiguchi T, Yoshida T, Coleman AW, Masuda M (2003) Phylogenetic relationships within the genus Sargassum (Fucales, Phaeophyceae), inferred from ITS-2 nrDNA, with an emphasis on the taxonomic subdivision of the genus. Phycol Res 51:1–10CrossRefGoogle Scholar
  161. Stonik V, Fedorov S (2014) Marine low molecular weight natural products as potential cancer preventive compounds. Mar Drugs 12:636–671CrossRefGoogle Scholar
  162. Suárez Y, González L, Cuadrado A, Berciano M, Lafarga M, Muñoz A (2003) Kahalalide F, a new marine-derived compound, induces oncosis in human prostate and breast cancer cells. Mol Cancer Ther 2:863–872Google Scholar
  163. Sun JC, Tan HP (2013) Alginate-based biomaterials for regenerative medicine applications. Materials 6:1285–1309. doi: 10.3390/ma6041285 CrossRefGoogle Scholar
  164. Sweeney T, Collins CB, Reilly P, Pierce KM, Ryan M, O’Doherty JV (2012) Effect of purified beta-glucans derived from Laminaria digitata, Laminaria hyperborea and Saccharomyces cerevisiae on piglet performance, selected bacterial populations, volatile fatty acids and pro-inflammatory cytokines in the gastrointestinal tract of pigs. Br J Nutr 108:1226–1234. doi: 10.1017/s0007114511006751 CrossRefGoogle Scholar
  165. Tan C-p, Hou Y-h (2014) First evidence for the anti-inflammatory activity of fucoxanthin in high-fat-diet-induced obesity in mice and the antioxidant functions in PC12 cells. Inflammation 37:443–450. doi: 10.1007/s10753-013-9757-1 CrossRefGoogle Scholar
  166. Tanniou A et al (2013) Green improved processes to extract bioactive phenolic compounds from brown macroalgae using Sargassum muticum as model. Talanta. doi: 10.1016/j.talanta.2012.10.088 Google Scholar
  167. Tanniou A et al (2014) 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 26:1215–1230. doi: 10.1007/s10811-013-0198-x Google Scholar
  168. Tanniou A, Vandanjon L, Gonçalves O, Kervarec N, Stiger-Pouvreau V (2015) Rapid geographical differentiation of the European spread brown macroalga Sargassum muticum using HRMAS NMR and Fourier-Transform Infrared spectroscopy. Talanta 132:451–456. doi: 10.1016/j.talanta.2014.09.002 CrossRefGoogle Scholar
  169. Taylor G (2008) Biofuels and the biorefinery concept. Energy Policy 36:4406–4409. doi: 10.1016/j.enpol.2008.09.069 CrossRefGoogle Scholar
  170. Thanet District Council (2014) Seaweed removal guidelines. http://thanet.gov.uk/the-thanet-magazine/campaigns/beside-the-seaside/removing-seaweed/seaweed-removal-guidelines/. Accessed 01 Dec 2014
  171. The River Stour (Kent) Internal Drainage Board (2012) Minutes of Board Meeting. Available at http://www.riverstouridb.org.uk/documents/minutes081112.pdf
  172. Ungureanu G, Santos S, Boaventura R, Botelho C (2015) Biosorption of antimony by brown algae S. muticum and A. nodosum. Environ Eng Manag J 14:455–463Google Scholar
  173. Valderrama D, Cai J, Hishamunda N, Ridler N (2014) Social and economic dimensions of carrageenan seaweed farming. FAO, RomeGoogle Scholar
  174. Villarreal-Gomez LJ, Soria-Mercado IE, Guerra-Rivas G, Ayala-Sanchez NE (2010) Antibacterial and anticancer activity of seaweeds and bacteria associated with their surface. Revista De Biologia Marina Y Oceanografia 45:267–275Google Scholar
  175. Wageningen University (2011) Research on microalgae within Wageningen UR http://www.algae.wur.nl/UK/technologies/biorefinery. Accessed 25 Jan 2013
  176. Wang PR, Xu GJ, Bian LZ, Zhang SC, Song FQ (2006) Study on sterols from brown algae (Sargassum muticum). Chin Sci Bull 51:2520–2528. doi: 10.1007/s11434-006-2124-y CrossRefGoogle Scholar
  177. Wang C, Kim J-H, Kim S-W (2014) Synthetic biology and metabolic engineering for marine carotenoids: new opportunities and future prospects. Mar Drugs 12:4810–4832CrossRefGoogle Scholar
  178. Wargacki AJ et al (2012) An engineered microbial platform for direct biofuel production from brown. Macroalgae Sci 335:308–313. doi: 10.1126/science.1214547 Google Scholar
  179. Wernberg T, Thomsen MS, Staehr PA, Pedersen MF (2001) Comparative phenology of Sargassum muticum and Halidrys siliquosa (Phaeophyceae: Fucales) in Limfjorden. Den. Bot Mar. 44:31–39. doi: 10.1515/bot.2001.005 Google Scholar
  180. Wijesinghe W, Jeon YJ (2011) Biological activities and potential cosmeceutical applications of bioactive components from brown seaweeds: a review. Phytochem Rev 10:431–443. doi: 10.1007/s11101-011-9214-4 CrossRefGoogle Scholar
  181. 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 88:13–20. doi: 10.1016/j.carbpol.2011.12.029 CrossRefGoogle Scholar
  182. Wijffels RH (2007) Potential of sponges and microalgae for marine biotechnology. Trends Biotechnol 26:26–31CrossRefGoogle Scholar
  183. Williams FE et al. (2010) The economic cost of invasive non-native species on Great Britain. CABIGoogle Scholar
  184. World Health Organisation (2014) Micronutrient deficiencies. http://www.who.int/nutrition/topics/idd/en/. Accessed 27 Jan 2014
  185. Yang EJ, Ham YM, Lee WJ, Lee NH, Hyun CG (2013) Anti-inflammatory effects of apo-9′-fucoxanthinone from the brown alga, Sargassum muticum. Daru-J Pharm Sci. doi: 10.1186/2008-2231-21-62 Google Scholar
  186. Yende SR, Harle UN, Chaugule BB (2014) Therapeutic potential and health benefits of Sargassum species. Pharmacogn Rev 8:1–7. doi: 10.4103/0973-7847.125514 CrossRefGoogle Scholar
  187. Yeong HY, Phang SM, Reddy CRK, Khalid N (2014) Production of clonal planting materials from Gracilaria changii and Kappaphycus alvarezii through tissue culture and culture of G-changii explants in airlift photobioreactors. J Appl Phycol 26:729–746. doi: 10.1007/s10811-013-0122-4 CrossRefGoogle Scholar
  188. Yoon WJ, Ham YM, Lee WJ, Lee NH, Hyun CG (2010) Brown alga Sargassum muticum inhibits proinflammatory cytokines, iNOS, and COX-2 expression in macrophage RAW 264.7 cells. Turk J Biol 34:25–34. doi: 10.3906/biy-0810-14 Google Scholar
  189. Zhao FJ, Liu FL, Liu JD, Ang PO, Duan DL (2008) Genetic structure analysis of natural Sargassum muticum (Fucales, Phaeophyta) populations using RAPD and ISSR markers. J Appl Phycol 20:191–198. doi: 10.1007/s10811-007-9207-2 CrossRefGoogle Scholar
  190. Zhou D, Zhang L, Zhang S, Fu H, Chen J (2010) Hydrothermal liquefaction of macroalgae Enteromorpha prolifera to bio-oil. Energy Fuels 24:4054–4061. doi: 10.1021/ef100151h CrossRefGoogle Scholar
  191. Zorofchian Moghadamtousi S, Karimian H, Khanabdali R, Razavi M, Firoozinia M, Zandi K, Abdul Kadir H (2014) Anticancer and antitumor potential of fucoidan and fucoxanthin, two main metabolites isolated from brown algae. Sci World J. Article ID 768323 (2014). doi: 10.1155/2014/768323

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© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.Algae Biotechnology Research Group, School of ScienceUniversity of GreenwichKentUK
  2. 2.IOTA Pharmaceuticals Ltd, St Johns Innovation CentreCambridgeUK

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