Abstract
Pollution and climate change induced by fossil fuel usage are calling for the development of a circular bioeconomy based on carbon neutral resources such as marine macroalgae, also named seaweeds. Macroalgal biomass can generate biofuels and valuable bioproducts such as hydrocolloids and other unique biomolecules. Biorefinery of marine macroalgae involves a minimum use of energy and chemicals, and low waste generation, as demonstrated in recent laboratory-scale studies. Here, we review biorefinery of marine macroalgae with focus on non-energy bioproducts and advances in the separation of biomolecules. We found that metabolites with bioactive properties are in high demand for food, cosmetic, medicine and pharmaceutical industries. These metabolites can be obtained together with energy products to improve macroalgae valorization. Emerging extraction methods facilitate the generation of more qualitative bioproducts in higher yields with less energy.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abraham RE, Su P, Puri M, Raston CL, Zhang W (2019) Optimisation of biorefinery production of alginate, fucoidan and laminarin from brown seaweed Durvillaea potatorum. Algal Res 38:101389. https://doi.org/10.1016/j.algal.2018.101389
Abreu MH, Varela DA, Henríquez L, Villarroel A, Yarish C, Sousa-Pinto I, Buschmann AH (2009) Traditional vs. integrated multi-trophic aquaculture of Gracilaria chilensis C. J. Bird, J. McLachlan & E. C. Oliveira: productivity and physiological performance. Aquaculture 293:211–220. https://doi.org/10.1016/j.aquaculture.2009.03.043
Agregán R, Munekata PES, Franco D, Dominguez R, Carballo J, Lorenzo JM (2017) Phenolic compounds from three brown seaweed species using LC-DAD-ESI-MS/MS. Food Res Int 99:979–985. https://doi.org/10.1016/j.foodres.2017.03.043
Agregán R, Munekata PES, Franco D, Carballo J, Barba FJ, Lorenzo JM (2018) Antioxidant potential of extracts obtained from macro- (Ascophyllum nodosum, Fucus vesiculosus and Bifurcaria bifurcata) and micro-algae (Chlorella vulgaris and Spirulina platensis) assisted by ultrasound. Medicines 5:33–41. https://doi.org/10.3390/medicines5020033
Aitken D, Bulboa C, Godoy-Faundez A, Turrion-Gomez JL, Antizar-Ladislao B (2014) Life cycle assessment of macroalgae cultivation and processing for biofuel production. J Clean Prod 75:45–56. https://doi.org/10.1016/j.jclepro.2014.03.080
Akalin MK, Tekin K, Karagöz S (2017) Supercritical fluid extraction of biofuels from biomass. Environ Chem Lett 15:29–41. https://doi.org/10.1007/s10311-016-0593-z
Ali H, Khan E (2017) Environmental chemistry in the twenty-first century. Environ Chem Lett 15:329–346. https://doi.org/10.1007/s10311-016-0601-3
Alvarado-Morales M, Boldrin A, Karakashev AB, Holdt SL, Angelidaki I, Astrup T (2013) Life cycle assessment of biofuel production from brown seaweed in Nordic conditions. Bioresour Technol 129:92–99. https://doi.org/10.1016/j.biortech.2012.11.029
Alvarado-Morales M, Gunnarsson IB, Fotidis IA, Vasilakou E, Lyberatos G, Angelidaki I (2015) Laminaria digitata as a potential carbon source for succinic acid and bioenergy production in a biorefinery perspective. Algal Res 9:126–132. https://doi.org/10.1016/j.algal.2015.03.008
Anand KGV, Eswaran K, Ghosh A (2018) Life cycle impact assessment of a seaweed product obtained from Gracilaria edulis—a potent plant biostimulant. J Clean Prod 170:1621–1627. https://doi.org/10.1016/j.jclepro.2017.09.241
Andriamanantoanina H, Rinaudo M (2010) Characterization of the alginates from five madagascan brown algae. Carbohydr Polym 82:555–560. https://doi.org/10.1016/j.carbpol.2010.05.002
Aravind S, Senthil Kumar P, Kumar NS, Siddarth N (2020) Conversion of green algal biomass into bioenergy by pyrolysis. A review Environ Chem Lett 18:829–849. https://doi.org/10.1007/s10311-020-00990-2
Armenta S, Garrigues S, de la Guardia M (2015) The role of green extraction techniques in green analytical chemistry. TRAC-Trend Anal Chem 71:2–8. https://doi.org/10.1016/j.trac.2014.12.011
Aroso IM, Paiva A, Reis RL, Duarte ARC (2017) Natural deep eutectic solvents from choline chloride and betaine—physicochemical properties. J Mol Liq 241:654–661. https://doi.org/10.1016/j.molliq.2017.06.051
Aryee ANA, Agyei D, Akanbi TO (2018) Recovery and utilization of seaweed pigments in food processing. Curr Opin Food Sci 19:113–119. https://doi.org/10.1016/j.cofs.2018.03.013
Atashrazm F, Lowenthal RM, Woods GM, Holloway AF, Dickinson JL (2015) Fucoidan and cancer: a multifunctional molecule with anti-tumor potential. Mar Drugs 13(4):2327–2346. https://doi.org/10.3390/md13042327
Baghel RS, Trivedi N, Gupta V, Neori A, Reddy CRK, Lali A, Jha B (2015) Biorefining of marine macroalgal biomass for production of biofuel and commodity chemicals. Green Chem 17:2436–2443. https://doi.org/10.1039/c4gc02532f
Baghel RS, Trivedi N, Reddy CRK (2016) A simple process for recovery of a stream of products from marine macroalgal biomass. Bioresour Technol 203:160–165. https://doi.org/10.1016/j.biortech.2015.12.051
Bak UG, Mols-Mortensen A, Gregersen O (2018) Production method and cost of commercial-scale offshore cultivation of kelp in the Faroe Islands using multiple partial harvesting. Algal Res 33:36–47. https://doi.org/10.1016/j.algal.2018.05.001
Balboa EM, Moure A, Domínguez H (2015) Valorization of Sargassum muticum biomass according to the biorefinery concept. Mar Drugs 13:3745–3760. https://doi.org/10.3390/md13063745
Barba FJ, Parniakov O, Pereira SA, Wiktor A, Grimi N, Boussetta N, Saraiva JA, Raso J, Martin-Belloso O, Witrowa-Rajchert D, Lebovka N, Vorobiev E (2015) Current applications and new opportunities for the use of pulsed electric fields in food science and industry. Food Res Int 77:773–798. https://doi.org/10.1016/j.foodres.2015.09.015
Barbosa M, Lopes G, Andrade PB, Valentão P (2019) Bioprospecting of brown seaweeds for biotechnological applications: phlorotannin actions in inflammation and allergy network. Trends Food Sci Technol 86:153–171. https://doi.org/10.1016/j.tifs.2019.02.037
Barbosa-Pereira L, Guglielmetti A, Zeppa G (2018) Pulsed electric field assisted extraction of bioactive compounds from cocoa bean shell and coffee silverskin. Food Bioprocess Tech 11:818–835. https://doi.org/10.1007/s11947-017-2045-6
Ben-Ari T, Neori A, Ben-Ezra D, Shauli L, Odintsov V, Shpigel M (2014) Management of Ulva lactuca as a biofilter of mariculture effluents in IMTA system. Aquaculture 434:493–498. https://doi.org/10.1016/j.aquaculture.2014.08.034
Benvenutti L, Ferreira Zielinski AA, Salvador Ferreira SR (2019) Which is the best food emerging solvent: IL, DES or NADES? Trends Food Sci Technol 90:133–146. https://doi.org/10.1016/j.tifs.2019.06.003
Bharathiraja B, Chakravarthy M, Kumar RR, Yogendran D, Yuvaraj D, Jayamuthunagai J, Kumar RP, Palani S (2015) Aquatic biomass (algae) as a future feed stock for bio-refineries: a review on cultivation, processing and products. Renew Sust Energ Rev 47:634–653. https://doi.org/10.1016/j.rser.2015.03.047
Billakanti JM, Catchpole OJ, Fenton TA, Mitchell KA, MacKenzie AD (2013) Enzyme-assisted extraction of fucoxanthin and lipids containing polyunsaturated fatty acids from Undaria pinnatifida using dimethyl ether and ethanol. Process Biochem 48:1999–2008. https://doi.org/10.1016/j.procbio.2013.09.015
BP Global (2013) BP Energy Outlook 2030. https://www.bp.com/content/dam/bp/business-sites/en/global/corporate/pdfs/energy-economics/energy-outlook/bp-energy-outlook-2013.pdf
Bruhn A, Dahl J, Nielsen HB, Nikolaisen L, Rasmussen MB, Markager S, Olesen B, Arias C, Jensen PD (2011) Bioenergy potential of Ulva lactuca: Biomass yield, methane production and combustion. Bioresour Technol 102:2595–2604. https://doi.org/10.1016/j.biortech.2010.10.010
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. Sustainable Energy Ireland. https://www.leanbusinessireland.ie/includes/documents/SEIalgae%20Report.pdf
Bubalo MC, Vidović S, Redovniković IR, Jokić S (2018) New perspective in extraction of plant biologically active compounds by green solvents. Food Bioprod Process 109:52–73. https://doi.org/10.1016/j.fbp.2018.03.001
Budhiyanti SA, Raharjo S, Marseno DW, Lelana IYB (2012) Antioxidant activity of brown algae Sargassum species extract from the coastline of Java Island. AJABS 7(3):337–346. https://doi.org/10.3844/ajabssp.2012.337.346
Campo VL, Kawano DF, da Silva Jr. DB, Carvalho I, (2009) Carrageenans: biological properties, chemical modifications and structural analysis—a review. Carbohydr Polym 77(2):167–180. https://doi.org/10.1016/j.carbpol.2009.01.020
Cao C, Huang Q, Zhang B, Li C, Fu X (2018) Physicochemical characterization and in vitro hypoglycemic activities of polysaccharides from Sargassum pallidum by microwave-assisted aqueous two-phase extraction. Int J Biol Macromol 109:357–368. https://doi.org/10.1016/j.ijbiomac.2017.12.096
Castillo ASR, Guihéneuf S, Le Guével R, Biard P-F, Paquin L, Amrane A, Couvert A (2016) Synthesis and toxicity evaluation of hydrophobic ionic liquids for volatile organic compounds biodegradation in a two-phase partitioning bioreactor. J Hazard Mater 307:221–230. https://doi.org/10.1016/j.jhazmat.2015.12.043
Cesário MT, da Fonseca MMR, Marques MM, de Almeida MCMD (2018) Marine algal carbohydrates as carbon sources for the production of biochemicals and biomaterials. Biotechnol Adv 36:798–817. https://doi.org/10.1016/j.biotechadv.2018.02.006
Charoensiddhi S, Franco C, Su P, Zhang W (2015) Improved antioxidant activities of brown seaweed Ecklonia radiata extracts prepared by microwave-assisted enzymatic extraction. J Appl Phycol 27(5):2049–2058. https://doi.org/10.1007/s10811-014-0476-2
Chemat F, Vian MA, Cravotto G (2012) Green extraction of natural products: concept and principles. Int J Mol Sci 13:8615–8627. https://doi.org/10.3390/ijms13078615
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
Crini G, Lichtfouse E, Wilson LD, Morin-Crini N (2019) Conventional and non-conventional adsorbents for wastewater treatment. Environ Chem Lett 17:195–213. https://doi.org/10.1007/s10311-018-0786-8
Czyrnek-Delêtre MM, Rocca S, Agostini A, Giuntoli J, Murphy JD (2017) Life cycle assessment of seaweed biomethane, generated from seaweed sourced from integrated multi-trophic aquaculture in temperate oceanic climates. Appl Energy 196:34–50. https://doi.org/10.1016/j.apenergy.2017.03.129
da Costa E, Melo T, Moreira ASP, Alves E, Domingues P, Calado R, Abreu MH, Domingues MR (2015) Decoding bioactive polar lipid profile of the macroalgae Codium tomentosum from a sustainable IMTA system using a lipidomic approach. Algal Res 12:388–397. https://doi.org/10.1016/j.algal.2015.09.020
Dai Y, Meng Q, Mu W, Zhang T (2017) Recent advances in the applications and biotechnological production of mannitol. J Funct Foods 36:404–409. https://doi.org/10.1016/j.jff.2017.07.022
Dang TT, Vuong QV, Schreider MJ, Bowyer MC, Van Altena IA, Scarlett CJ (2017) Optimisation of ultrasound-assisted extraction conditions for phenolic content and antioxidant activities of the alga Hormosira banksii using response surface methodology. J Appl Phycol 29:3161–3173. https://doi.org/10.1007/s10811-017-1162-y
Deniaud-Bouët E, Kervarec N, Michel G, Tonon T, Kloareg B, Hervé C (2014) Chemical and enzymatic fractionation of cell walls from Fucales: Insights into the structure of the extracellular matrix of brown algae. Ann Bot 114(6):1203–1216. https://doi.org/10.1093/aob/mcu096
de Quirós ARB, Frecha-Ferreiro S, Vidal-Pérez AM, López-Hernández J (2010) Antioxidant compounds in edible brown seaweeds. Eur Food Res Technol 231:495–498. https://doi.org/10.1007/s00217-010-1295-6
Dinh TV, Saravana PS, Woo HC, Chun BS (2018) Ionic liquid-assisted subcritical water enhances the extraction of phenolics from brown seaweed and its antioxidant activity. Sep Purif Technol 196:287–299. https://doi.org/10.1016/j.seppur.2017.06.009
Domingues B, Abreu MH, Sousa-Pinto I (2015) On the bioremediation efficiency of Mastocarpus stellatus (Stackhouse) Guiry, in an integrated multi-trophic aquaculture system. J Appl Phycol 27:1289–1295. https://doi.org/10.1007/s10811-014-0414-3
Dumay J, Clément N, Morançais M, Fleurence J (2013) Optimization of hydrolysis conditions of Palmaria palmata to enhance R-phycoerythrin extraction. Bioresour Technol 131:21–27. https://doi.org/10.1016/j.biortech.2012.12.146
Eom SH, Kim YM, Kim SK (2012) Antimicrobial effect of phlorotannins from marine brown algae. Food Chem Toxicol 50(9):3251–3255. https://doi.org/10.1016/j.fct.2012.06.028
Ertem FC, Neubauer P, Junne S (2017) Environmental life cycle assessment of biogas production from marine macroalgal feedstock for the substitution of energy crops. J Clean Prod 140:977–985. https://doi.org/10.1016/j.jclepro.2016.08.041
FAO (2012) The state of world fisheries and aquaculture. https://www.fao.org/3/i2727e/i2727e.pdf
Fauster T, Schlossnikl D, Rath F, Ostermeier R, Teufel F, Toepfl S, Jaeger H (2018) Impact of pulsed electric field (PEF) pretreatment on process performance of industrial French fries production. J Food Eng 235:16–22. https://doi.org/10.1016/j.jfoodeng.2018.04.023
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. https://doi.org/10.1016/j.carbpol.2016.11.077
Fawzy S, Osman AI, Doran J, Rooney DW (2020) Strategies for mitigation of climate change. Environ Chem Lett. https://doi.org/10.1007/s10311-020-01059-w
Ferreres F, Lopes G, Gil-Izquierdo A, Andrade PB, Sousa C, Mouga T, Valentão P (2012) Phlorotannin extracts from Fucales characterized by HPLC-DAD-ESI-MSn: approaches to Hyaluronidase inhibitory capacity and antioxidant Properties. Mar Drugs 10(12):2766–2781. https://doi.org/10.3390/md10122766
Fidelis GP, Camara RBG, Queiroz MF, Costa MSSP, Santos PC, Rocha HAO, Costa LS (2014) Proteolysis, NaOH and ultrasound-enhanced extraction of anticoagulant and antioxidant sulfated polysaccharides from the edible seaweed, Gracilaria birdiae. Molecules 19:18511–18526. https://doi.org/10.3390/molecules191118511
Filote C, Popa VI, Volf I (2017) Marine algae biomass potential for obtaining biofuels and bioproducts. In: Strategic Synergies in the Black Sea Basin, proceedings of the XIIth edition of the annual conference “The Academic Days of A.T.S.R.”, pp 452–457
Filote C, Volf I, Santos SCR, Botelho CMS (2019) Bioadsorptive removal of Pb(II) from aqueous solution by the biorefinery waste of Fucus spiralis. Sci Total Environ 648:1201–1209. https://doi.org/10.1016/j.scitotenv.2018.08.210
Fleurence J, Le Coeur C, Mabeau S, Maurice M, Landrein A (1995) Comparison of different extractive procedures for proteins from the edible seaweeds Ulva rigida and Ulva rotundata. J Appl Phycol 7(6):577–582
Florindo C, Branco LC, Marrucho IM (2017) Development of hydrophobic deep eutectic solvents for extraction of pesticides from aqueous environments. Fluid Phase Equilib 448:135–142. https://doi.org/10.1016/j.fluid.2017.04.002
Flórez-Fernández N, López-García M, González-Muñoz MJ, Vilariño JML, Domínguez H (2017) Ultrasound-assisted extraction of fucoidan from Sargassum muticum. J Appl Phycol 29:1553–1561. https://doi.org/10.1007/s10811-016-1043-9
Francavilla M, Manara P, Kamaterou P, Monteleone M, Zabaniotou A (2015) Cascade approach of red macroalgae Gracilaria gracilis sustainable valorization by extraction of phycobiliproteins and pyrolysis of residue. Bioresour Technol 184:305–313. https://doi.org/10.1016/j.biortech.2014.10.147
Fung A, Hamid N, Lu J (2013) Fucoxanthin content and antioxidant properties of Undaria pinnatifida. Food Chem 136:1055–1062. https://doi.org/10.1016/j.foodchem.2012.09.024
Gajaria TK, Suthar P, Baghel RS, Balar NB, Sharnagat P, Mantri VA, Reddy CRK (2017) Integration of protein extraction with a stream of byproducts from marine macroalgae: a model forms the basis for marine bioeconomy. Bioresour Technol 243:867–873. https://doi.org/10.1016/j.biortech.2017.06.149
Gammone MA, D’Orazio N (2015) Anti-obesity activity of the marine carotenoid fucoxanthin. Mar Drugs 13:2196–2214. https://doi.org/10.3390/md13042196
Ganesan AR, Tiwari U, Rajauria G (2019) Seaweed nutraceuticals and their therapeutic role in disease prevention. Food Sci Hum Wellness 8:252–263. https://doi.org/10.1016/j.fshw.2019.08.001
Gao G, Clare AS, Rose C, Caldwell GS (2017) Eutrophication and warming-driven green tides (Ulva rigida) are predicted to increase under future climate change scenarios. Mar Pollut Bull 114:439–447. https://doi.org/10.1016/j.marpolbul.2016.10.003
Gereniu CRN, Saravana PS, Chun BS (2018) Recovery of carrageenan from Solomon Islands red seaweed using ionic liquid-assisted subcritical water extraction. Sep Purif Technol 196:309–317. https://doi.org/10.1016/j.seppur.2017.06.055
Getachew AT, Saravana PS, Cho YJ, Woo HC, Chun BS (2018) Concurrent extraction of oil from roasted coffee (Coffea arabica) and fucoxanthin from brown seaweed (Saccharina japonica) using supercritical carbon dioxide. J CO2 Util 25:137–146. https://doi.org/https://doi.org/10.1016/j.jcou.2018.03.018
Ghadiryanfar M, Rosentrater KA, Keyhani A, Omid M (2016) A review of macroalgae production, with potential applications in biofuels and bioenergy. Renew Sust Energ Rev 54:473–481. https://doi.org/10.1016/j.rser.2015.10.022
Ghosh A, Anand KGV, Seth A (2015) Life cycle impact assessment of seaweed based biostimulant production from onshore cultivated Kappaphycus alvarezii (Doty) Doty ex Silva—is it environmentally sustainable? Algal Res 12:513–521. https://doi.org/10.1016/j.algal.2015.10.015
Goto M, Kanda H, Wahyudiono MS (2015) Extraction of carotenoids and lipids from algae by supercritical CO2 and subcritical dimethyl ether. J Supercrit Fluids 96:245–251. https://doi.org/10.1016/j.supflu.2014.10.003
Grosso C, Valentão P, Ferreres F, Andrade PB (2015) Alternative and efficient extraction methods for marine-derived compounds. Mar Drugs 13(5):3182–3230. https://doi.org/10.3390/md13053182
Gude VG, Martinez-Guerra E (2018) Green chemistry with process intensification for sustainable biodiesel production. Environ Chem Lett 16:327–341. https://doi.org/10.1007/s10311-017-0680-9
Hahn T, Lang S, Ulber R, Muffler K (2012) Novel procedures for the extraction of fucoidan from brown algae. Process Biochem 47(12):1691–1698. https://doi.org/10.1016/j.procbio.2012.06.016
Hardouin K, Bedoux G, Burlot AS, Donnay-Moreno C, Bergé JP, Nyvall-Collén P, Bourgougnon N (2016) Enzyme-assisted extraction (EAE) for the production of antiviral and antioxidant extracts from the green seaweed Ulva armoricana (Ulvales, Ulvophyceae). Algal Res 16:233–239. https://doi.org/10.1016/j.algal.2016.03.013
Heo SJ, Jeon YJ, Lee JH, Kim HT, Lee KW (2003) Antioxidant effect of enzymatic hydrolyzate from a kelp. Ecklonia cava Algae 18(4):341–347. https://doi.org/10.4490/ALGAE.2003.18.4.341
Heo SJ, Park EJ, Lee KW, Jeon YJ (2005) Antioxidant activities of enzymatic extracts from brown seaweeds. Bioresour Technol 96:1613–1623. https://doi.org/10.1016/j.biortech.2004.07.013
Heo SJ, Ko SC, Cha SH, Kang DH, Park HS, Choi YU, Jeon YJ (2009) Effect of phlorotannins isolated from Ecklonia cava on melanogenesis and their protective effect against photo-oxidative stress induced by UV-B radiation. Toxicol Vitr 23(6):1123–1130. https://doi.org/10.1016/j.tiv.2009.05.013
Heo SJ, Yoon WJ, Kim KN, Ahn GN, Kang SM, Kang DH, Affan A, Oh C, Jung WK, Jeon YJ (2010) Evaluation of anti-inflammatory effect of fucoxanthin isolated from brown algae in lipopolysaccharide-stimulated RAW 264.7 macrophages. Food Chem Toxicol 48:2045–2051. https://doi.org/10.1016/j.fct.2010.05.003
Herrero M, Ibañez E (2018) Green extraction processes, biorefineries and sustainability: Recovery of high added-value products from natural sources. J Supercrit Fluids 134:252–259. https://doi.org/10.1016/j.supflu.2017.12.002
Hmelkov AB, Zvyagintseva TN, Shevchenko NM, Rasin AB, Ermakova SP (2018) Ultrasound-assisted extraction of polysaccharides from brown alga Fucus evanescens. Structure and biological activity of the new fucoidan fractions. J Appl Phycol 30:2039–2046. https://doi.org/10.1007/s10811-017-1342-9
Holdt SL, Kraan S (2011) Bioactive compounds in seaweed: functional food applications and legislation. J Appl Phycol 23:543–597. https://doi.org/10.1007/s10811-010-9632-5
Hosokawa M, Miyashita T, Nishikawa S, Emi S, Tsukui T, Beppu F, Okada T, Miyashita K (2010) Fucoxanthin regulates adipocytokine mRNA expression in white adipose tissue of diabetic/obese KK-AY mice. Arch Biochem Biophys 504:17–25. https://doi.org/10.1016/j.abb.2010.05.031
Hou X, Hansen JH, Bjerre AB (2015) Integrated bioethanol and protein production from brown seaweed Laminaria digitata. Bioresour Technol 197:310–317. https://doi.org/10.1016/j.biortech.2015.08.091
Hu X, Li Y, Li C, Fu Y, Cai F, Chen Q, Li D (2012) Combination of fucoxanthin and conjugated linoleic acid attenuates body weight gain and improves lipid metabolism in high-fat diet-induced obese rats. Arch Biochem Biophys 519:59–65. https://doi.org/10.1016/j.abb.2012.01.011
Huang J, Guo X, Xu T, Fan L, Zhou X, Wu S (2019) Ionic deep eutectic solvents for the extraction and separation of natural products. J Chromatogr A 1598:1–19. https://doi.org/10.1016/j.chroma.2019.03.046
Huang D, Quan Q, Zheng Y, Tang W, Zhang Z, Qiang X (2020) Dual-network design to enhance the properties of agar aerogel adsorbent by incorporating in situ ion cross-linked alginate. Environ Chem Lett 18:251–255. https://doi.org/10.1007/s10311-019-00932-7
Jung KA, Lim SR, Kim Y, Park JM (2013) Potentials of macroalgae as feedstocks for biorefinery. Bioresour Technol 135:182–190. https://doi.org/10.1016/j.biortech.2012.10.025
Kadam SU, Tiwari BK, O’Donnell CP (2013) Application of novel extraction technologies for bioactives from marine algae. J Agric Food Chem 61(20):4667–4675. https://doi.org/10.1021/jf400819p
Kadam SU, Tiwari BK, O’Donnell CP (2015) Extraction, structure and biofunctional activities of laminarin from brown algae. Int J Food Sci Technol 50:24–31. https://doi.org/10.1111/ijfs.12692
Kadam SU, O’Donnell CP, Rai DK, Hossain MB, Burgess CM, Walsh D, Tiwari BK (2015) Laminarin from Irish brown seaweeds Ascophyllum nodosum and Laminaria hyperborea: Ultrasound assisted extraction, characterization and bioactivity. Mar Drugs 13:4270–4280. https://doi.org/10.3390/md13074270
Kadam SU, Tiwari BK, Smyth TJ, O’Donnell CP (2015) Optimization of ultrasound assisted extraction of bioactive components from brown seaweed Ascophyllum nodosum using response surface methodology. Ultrason Sonochem 23:308–316. https://doi.org/10.1016/j.ultsonch.2014.10.007
Kadam SU, Álvarez C, Tiwari BK, O’Donnell CP (2017) Extraction and characterization of protein from Irish brown seaweed Ascophyllum nodosum. Food Res Int 99:1021–1027. https://doi.org/10.1016/j.foodres.2016.07.018
Kawai S, Murata K (2016) Biofuel production based on carbohydrates from both brown and red macroalgae: recent developments in key biotechnologies. Int J Mol Sci 17:145–161. https://doi.org/10.3390/ijms17020145
Kazir M, Abuhassira Y, Robin A, Nahor O, Luo J, Israel A, Golberg A, Livney YD (2019) Extraction of proteins from two marine macroalgae, Ulva sp. and Gracilaria sp., for food application, and evaluating digestibility, amino acid composition and antioxidant properties of the protein concentrates. Food Hydrocoll 87:194–203. https://doi.org/10.1016/j.foodhyd.2018.07.047
Keyrouz R, Abasq ML, Le Bourvellec C, Blanc N, Audibert L, ArGall E, Hauchard D (2011) Total phenolic contents, radical scavenging and cyclic voltammetry of seaweeds from Brittany. Food Chem 126(3):831–836. https://doi.org/10.1016/j.foodchem.2010.10.061
Khandelwal S, Tailor YK, Kumar M (2016) Deep eutectic solvents (DESs) as eco-friendly and sustainable solvent/catalyst systems in organic transformations. J Mol Liq 215:345–386. https://doi.org/10.1016/j.molliq.2015.12.015
Kim KN, Heo SJ, Kang SM, Ahn G, Jeon YJ (2010) Fucoxanthin induces apoptosis in human leukemia HL-60 cells through a ROS-mediated Bcl-xL pathway. Toxicol in Vitro 24:1648–1654. https://doi.org/10.1016/j.tiv.2010.05.023
Kim GY, Seo YH, Kim I, Han JI (2019) Co-production of biodiesel and alginate from Laminaria japonica. Sci Total Environ 673:750–755. https://doi.org/10.1016/j.scitotenv.2019.04.049
Klejdus B, Lojková L, Plaza M, Šnóblová M, Štěrbová D (2010) Hyphenated technique for the extraction and determination of isoflavones in algae: Ultrasound-assisted supercritical fluid extraction followed by fast chromatography with tandem mass spectrometry. J Chromatogr A 1217:7956–7965. https://doi.org/10.1016/j.chroma.2010.07.020
Kostas ET, White DA, Cook DJ (2017) Development of a bio-refinery process for the production of specialty chemical, biofuel and bioactive compounds from Laminaria digitata. Algal Res 28:211–219. https://doi.org/10.1016/j.algal.2017.10.022
Kostić MD, Divac VM (2019) Green solvents in organoselenium chemistry. Environ Chem Lett 17:897–915. https://doi.org/10.1007/s10311-018-00848-8
Kraan S (2013) Mass-cultivation of carbohydrate rich macroalgae, a possible solution for sustainable biofuel production. Mitig Adapt Strat Gl 18:27–46. https://doi.org/10.1007/s11027-010-9275-5
Krishnan A, Gopinath KP, Vo DVN, Malolan R, Nagarajan VM, Arun J (2020) Ionic liquids, deep eutectic solvents and liquid polymers as green solvents in carbon capture technologies: a review. Environ Chem Lett. https://doi.org/10.1007/s10311-020-01057-y
Kulshreshtha G, Burlot AS, Marty C, Critchley A, Hafting J, Bedoux G, Bourgougnon N, Prithiviraj B (2015) Enzyme-assisted extraction of bioactive material from Chondrus crispus and Codium fragile and its effect on Herpes simplex virus (HSV-1). Mar Drugs 13:558–580. https://doi.org/10.3390/md13010558
Kumar S, Gupta R, Kumar G, Sahoo D, Kuhad RC (2013) Bioethanol production from Gracilaria verrucosa, a red alga, in a biorefinery approach. Bioresour Technol 135:150–156. https://doi.org/10.1016/j.biortech.2012.10.120
Kumari P, Kumar M, Gupta V, Reddy CRK, Jha B (2010) Tropical marine macroalgae as potential sources of nutritionally important PUFAs. Food Chem 120:749–757. https://doi.org/10.1016/j.foodchem.2009.11.006
Kumari P, Reddy CRK, Jha B (2011) Comparative evaluation and selection of a method for lipid and fatty acid extraction from macroalgae. Anal Biochem 415:134–144. https://doi.org/10.1016/j.ab.2011.04.010
Langlois J, Sassi JF, Jard G, Steyer JP, Delgenes JP, Hélias A (2012) Life cycle assessment of biomethane from offshore-cultivated seaweed. Biofuel Bioprod Bior 6:387–404. https://doi.org/10.1002/bbb.1330
Lazar L, Talmaciu AI, Volf I, Popa VI (2016) Kinetic modeling of the ultrasound-assisted extraction of polyphenols from Picea abies bark. Ultrason Sonochem 32:191–197. https://doi.org/10.1016/j.ultsonch.2016.03.009
Lee KY, Mooney DJ (2012) Alginate: properties and biomedical applications. Prog Polym Sci 37:106–126. https://doi.org/10.1016/j.progpolymsci.2011.06.003
Lee SH, Jeon YJ (2013) Anti-diabetic effects of brown algae derived phlorotannins, marine polyphenols through diverse mechanisms. Fitoterapia 86(1):129–136. https://doi.org/10.1016/j.fitote.2013.02.013
Lee OK, Lee EY (2016) Sustainable production of bioethanol from renewable brown algae biomass. Biomass Bioenergy 92:70–75. https://doi.org/10.1016/j.biombioe.2016.03.038
Lee SY, Khoiroh I, Vo DVN, Kumar PS, Show PL (2020) Techniques of lipid extraction from microalgae for biofuel production: a review. Environ Chem Lett. https://doi.org/10.1007/s10311-020-01088-5
Le Guillard C, Bergé JP, Donnay-Moreno C, Bruzac S, Ragon JY, Baron R, Fleurence J, Dumay J (2016) Soft liquefaction of the red seaweed Grateloupia turuturu Yamada by ultrasound-assisted enzymatic hydrolysis process. J Appl Phycol 28:2575–2585. https://doi.org/10.1007/s10811-015-0788-x
Li Z, Wang B, Zhang Q, Qu Y, Xu H, Li G (2012) Preparation and antioxidant property of extract and semipurified fractions of Caulerpa racemosa. J Appl Phycol 24:1527–1536. https://doi.org/10.1007/s10811-012-9813-5
Liu J, Zhan X, Wan J, Wang Y, Wang C (2015) Review for carrageenan-based pharmaceutical biomaterials: favourable physical features versus adverse biological effects. Carbohydr Polym 121:27–36. https://doi.org/10.1016/j.carbpol.2014.11.063
Lorbeer AJ, Lahnstein J, Bulone V, Nguyen T, Zhang W (2015) Multiple-response optimization of the acidic treatment of the brown alga Ecklonia radiata for the sequential extraction of fucoidan and alginate. Bioresour Technol 197:302–309. https://doi.org/10.1016/j.biortech.2015.08.103
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 27:2079–2087. https://doi.org/10.1007/s10811-014-0446-8
Lorbeer AJ, Charoensiddhi S, Lahnstein J, Lars C, Franco CMM, Bulone V, Zhang W (2017) Sequential extraction and characterization of fucoidans and alginates from Ecklonia radiata, Macrocystis pyrifera, Durvillaea potatorum, and Seirococcus axillaris. J Appl Phycol 29:1515–1526. https://doi.org/10.1007/s10811-016-0990-5
Magnusson M, Yuen AKL, Zhang R, Wright JT, Taylor RB, Maschmeyer T, de Nys R (2017) A comparative assessment of microwave assisted (MAE) and conventional solid-liquid (SLE) techniques for the extraction of phloroglucinol from brown seaweed. Algal Res 23:28–36. https://doi.org/10.1016/j.algal.2017.01.002
Manuhara GJ, Praseptiangga D, Riyanto RA (2016) Extraction and characterization of refined K-carrageenan of Red Algae [Kappaphycus alvarezii (Doty ex P.C. Silva, 1996)] originated from Karimun Jawa Islands. Aquat Procedia 7:106–111. https://doi.org/10.1016/j.aqpro.2016.07.014
Marinho G, Nunes C, Sousa-Pinto I, Pereira R, Rema P, Valente LMP (2013) The IMTA-cultivated Chlorophyta Ulva spp. as a sustainable ingredient in Nile tilapia (Oreochromis niloticus) diets. J Appl Phycol 25:1359–1367. https://doi.org/10.1007/s10811-012-9965-3
Marinho GS, Holdt SL, Birkeland MJ, Angelidaki I (2015) Commercial cultivation and bioremediation potential of sugar kelp, Saccharina latissima, in Danish waters. J Appl Phycol 27:1963–1973. https://doi.org/10.1007/s10811-014-0519-8
Marinho GS, Holdt SL, Angelidaki I (2015) Seasonal variations in the amino acid profile and protein nutritional value of Saccharina latissima cultivated in a commercial IMTA system. J Appl Phycol 27(5):1991–2000. https://doi.org/10.1007/s10811-015-0546-0
Martínez JM, Delso C, Álvarez I, Raso J (2019) Pulsed electric field permeabilization and extraction of phycoerythrin from Porphyridium cruentum. Algal Res 37:51–56. https://doi.org/10.1016/j.algal.2018.11.005
Masarin F, Cedeno FRP, Chavez EGS, de Oliveira LE, Gelli VC, Monti R (2016) Chemical analysis and biorefinery of red algae Kappaphycus alvarezii for efficient production of glucose from residue of carrageenan extraction process. Biotechnol Biofuels 9:122. https://doi.org/10.1186/s13068-016-0535-9
Masri MA, Jurkowski W, Shaigani P, Haack M, Mehlmer N, Brück T (2018) A waste-free, microbial oil centered cyclic bio-refinery approach based on flexible macroalgae biomass. Appl Energy 224:1–12. https://doi.org/10.1016/j.apenergy.2018.04.089
Matsson S, Christie H, Fieler R (2019) Variation in biomass and biofouling of kelp, Saccharina latissima, cultivated in the Arctic, Norway. Aquaculture 506:445–452. https://doi.org/10.1016/j.aquaculture.2019.03.068
McHugh DJ (2003) A Guide to the Seaweed Industry. FAO Fisheries Technical Paper. https://www.fao.org/3/a-y4765e.pdf
Menshova RV, Ermakova SP, Anastyuk SD, Isakov VV, Dubrovskaya YV, Kusaykin MI, Zvyagintseva TN (2014) Structure, enzymatic transformation and anticancer activity of branched high molecular weight laminaran from brown alga Eisenia bicyclis. Carbohydr Polym 99:101–109. https://doi.org/10.1016/j.carbpol.2013.08.037
Mezghani S, Csupor D, Bourguiba I, Hohmann J (2016) Characterization of phenolic compounds of Ulva rigida (Chlorophycae) and its antioxidant activity. Euro J Med Plants 12(1):1–9. https://doi.org/10.9734/ejmp/2016/22935
Mhatre A, Gore S, Mhatre A, Trivedi N, Sharma M, Pandit R, Anil A, Lali A (2019) Effect of multiple products extraction on bio-methane potential of marine macrophytic green alga Ulva lactuca. Renew Energy 132:742–751. https://doi.org/10.1016/j.renene.2018.08.012
Michalak I, Chojnacka K (2014) Algal extracts: technology and advances. Eng Life Sci 14:581–591. https://doi.org/10.1002/elsc.201400139
Michalak I, Tuhy Ł, Chojnacka K (2015) Seaweed extract by microwave assisted extraction as plant growth biostimulant. Open Chem 13(1):1183–1195. https://doi.org/10.1515/chem-2015-0132
Mihranyan A (2011) Cellulose from Cladophorales Green Algae: from environmental problem to high-tech composite materials. J Appl Polym Sci 119:2449–2460. https://doi.org/10.1002/app.32959
Milledge JJ, Smith B, Dyer PW, Harvey P (2014) Macro-algae derived biofuel: a review of methods of energy extraction from seaweed biomass. Energies 7:7194–7222. https://doi.org/10.3390/en7117194
Mineur F, Arenas F, Assis J, Davies AJ, Engelen AH, Fernandes F, Malta EJ, Thibaut T, Nguyen TV, Vaz-Pinto F, Vranken S, Serrão EA, De Clerck O (2015) European seaweeds under pressure: consequences for communities and ecosystem functioning. J Sea Res 98:91–108. https://doi.org/10.1016/j.seares.2014.11.004
Mittal R, Tavanandi HA, Mantri VA, Raghavarao KSMS (2017) Ultrasound assisted methods for enhanced extraction of phycobiliproteins from marine macro-algae Gelidium pusillum (Rhodophyta). Ultrason Sonochem 38:92–103. https://doi.org/10.1016/j.ultsonch.2017.02.030
Miyashita K, Mikami M, Hosokawa M (2013) Chemical and nutritional characteristics of brown seaweed lipids: a review. J Funct Foods 5:1507–1517. https://doi.org/10.1016/j.jff.2013.09.019
Nakazawa Y, Sashima T, Hosokawa M, Miyashita K (2009) Comparative evaluation of growth inhibitory effect of stereoisomers of fucoxanthin in human cancer cell lines. J Funct Foods 1(1):88–97. https://doi.org/10.1016/j.jff.2008.09.015
Nishikawa S, Hosokawa M, Miyashita K (2012) Fucoxanthin promotes translocation and induction of glucose transporter 4 in skeletal muscles of diabetic/obese KK-AY mice. Phytomedicine 19:389–394. https://doi.org/10.1016/j.phymed.2011.11.001
Noreen A, Zia KM, Zuber M, Ali M, Mujahid M (2016) A critical review of algal biomass: a versatile platform of bio-base polyesters from renewable resources. Int J Biol Macromol 86:937–949. https://doi.org/10.1016/j.ijbiomac.2016.01.067
Obluchinskaya ED, Daurtseva AV, Pozharitskaya ON, Flisyuk EV, Shihov AN (2019) Natural deep eutectic solvents as alternatives for extracting phlorotannins from brown algae. Pharm Chem J 53:243–247. https://doi.org/10.1007/s11094-019-01987-0
Okolie CL, Akanbi TO, Mason B, Udenigwe CC, Aryee ANA (2019) Influence of conventional and recent extraction technologies on physicochemical properties of bioactive macromolecules from natural sources: a review. Food Res Int 116:827–839. https://doi.org/10.1007/s11094-019-01987-0
Park JN, Shin TS, Lee JH, Chun BS (2012) Production of reducing sugars from Laminaria japonica by subcritical water hydrolysis. APCBEE Procedia 2:17–21. https://doi.org/10.1016/j.apcbee.2012.06.004
Parsons S, Allen MJ, Abeln F, McManus M, Chuck CJ (2019) Sustainability and life cycle assessment (LCA) of macroalgae-derived single cell oils. J Clean Prod 232:1272–1281. https://doi.org/10.1016/j.jclepro.2019.05.315
Patle DS, Pandey A, Srivastava S, Sawarkar AN, Kumar S (2020) Ultrasound-intensified biodiesel production from algal biomass: a review. Environ Chem Lett. https://doi.org/10.1007/s10311-020-01080-z
Pechsiri JS, Thomas JBE, Risén E, Ribeiro MS, Malmström ME, Nylund GM, Jansson A, Welander U, Pavia H, Gröndahl F (2016) Energy performance and greenhouse gas emissions of kelp cultivation for biogas and fertilizer recovery in Sweden. Sci Total Environ 573:347–355. https://doi.org/10.1016/j.scitotenv.2016.07.220
Peng L, Fu D, Chu H, Wang Z, Qi H (2019) Biofuel production from microalgae: a review. Environ Chem Lett 18:285–297. https://doi.org/10.1007/s10311-019-00939-0
Pérez MJ, Falqué E, Domínguez H (2016) Antimicrobial action of compounds from Marine Seaweed. Mar Drugs 14:52. https://doi.org/10.3390/md14030052
Pérez-López P, Balboa EM, González-García S, Domínguez H, Feijoo G, Moreira MT (2014) Comparative environmental assessment of valorization strategies of the invasive macroalgae Sargassum muticum. Bioresour Technol 161:137–148. https://doi.org/10.1016/j.biortech.2014.03.013
Pham TPT, Cho CW, Yun YS (2010) Environmental fate and toxicity of ionic liquids: a review. Water Res 44:352–372. https://doi.org/10.1016/j.watres.2009.09.030
Polikovsky M, Fernand F, Sack M, Frey W, Müller G, Golberg A (2016) Towards marine biorefineries: selective proteins extractions from marine macroalgae Ulva with pulsed electric fields. Innov Food Sci Emerg Technol 37:194–200. https://doi.org/10.1016/j.ifset.2016.03.013
Polikovsky M, Fernand F, Sack M, Frey W, Müller G, Golberg A (2019) In silico food allergenic risk evaluation of proteins extracted from macroalgae Ulva sp. with pulsed electric fields. Food Chem 276:735–744. https://doi.org/10.1016/j.foodchem.2018.09.134
Pollet P, Davey EA, Ureña-Benavides EE, Eckert CA, Liotta CL, Sheldon RA, Liotta CL (2014) Solvents for sustainable chemical processes. Green Chem 16:1034–1055. https://doi.org/10.1039/c3gc42302f
Popa V, Rusan V, Simionescu C (1974) Chimia algelor marine. Editura Academiei Republicii Socialiste România.
Popa V (1975) Cercetări în domeniul chimiei algelor marine (PhD Thesis). Institutul Politehnic “Gh Asachi”, Facultatea de Chimie și Inginerie Chimică, p.14.
Ragonese C, Tedone L, Beccaria M, Torre G, Cichello F, Cacciola F, Mondello L (2014) Characterisation of lipid fraction of marine macroalgae by means of chromatography techniques coupled to mass spectrometry. Food Chem 145:932–940. https://doi.org/10.1016/j.foodchem.2013.08.130
Rahimi F, Tabarsa M, Rezaei M (2016) Ulvan from green algae Ulva intestinalis: optimization of ultrasound-assisted extraction and antioxidant activity. J Appl Phycol 28:2979–2990. https://doi.org/10.1007/s10811-016-0824-5
Raposo MFJ, Morais AMB, Morais RMSC (2015) Marine polysaccharides from algae with potential biomedical applications. Mar Drugs 13:2967–3028. https://doi.org/10.3390/md13052967
Rhein-Knudsen N, Ale MT, Meyer AS (2015) Seaweed hydrocolloid production: an update on enzyme assisted extraction and modification technologies. Marine Drugs 13:3340–3359. https://doi.org/10.3390/md13063340
Rinaudo M (2014) Biomaterials based on a natural polysaccharide: alginate. TIP 17(1):92–96. https://doi.org/10.1016/S1405-888X(14)70322-5
Robin A, Sack M, Israel A, Frey W, Müller G, Golberg A (2018) Deashing macroalgae biomass by pulsed electric field treatment. Bioresour Technol 255:131–139. https://doi.org/10.1016/j.biortech.2018.01.089
Rodriguez-Jasso RM, Mussatto SI, Pastrana L, Aguilar CN, Teixeira JA (2011) Microwave-assisted extraction of sulfated polysaccharides (fucoidan) from brown seaweed. Carbohydr Polym 86:1137–1144. https://doi.org/10.1016/j.carbpol.2011.06.006
Romero JB, Villanueva RD, Montano MNE (2008) Stability of agar in the seaweed Gracilaria eucheumatoides (Gracilariales, Rhodophyta) during postharvest storage. Bioresour Technol 99(17):8151–8155. https://doi.org/10.1016/j.biortech.2008.03.017
Ryu HJ, Oh KK (2017) Combined de-algination process as a fractionation strategy for valorization of Brown Macroalga Saccharina japonica. Appl Biochem Biotechnol 182:238–249. https://doi.org/10.1007/s12010-016-2323-1
Saluri M, Kaldmäe M, Tuvikene R (2019) Extraction and quantification of phycobiliproteins from the red alga Furcellaria lumbricalis. Algal Res 37:115–123. https://doi.org/10.1016/j.algal.2018.11.013
Sambusiti C, Bellucci M, Zabaniotou A, Beneduce L, Monlau F (2015) Algae as promising feedstocks for fermentative biohydrogen production according to a biorefinery approach: a comprehensive review. Renew Sust Energ Rev 44:20–36. https://doi.org/10.1016/j.rser.2014.12.013
Sanjeewa KKA, Kim EA, Son KT, Jeon YJ (2016) Bioactive properties and potentials cosmeceutical applications of phlorotannins isolated from brown seaweeds: a review. J Photochem Photobiol B 162:100–105. https://doi.org/10.1016/j.jphotobiol.2016.06.027
Santos SCR, Ungureanu G, Volf I, Boaventura RAR, Botelho CMS (2018) Macroalgae biomass as sorbent for metal ions. In: Popa V, Volf I (eds) Biomass as renewable raw material to obtain bioproducts of high-tech value. Elsevier, Amsterdam, The Netherlands, pp 69–112. https://doi.org/10.1016/B978-0-444-63774-1.00003-X
Saravana PS, Cho YJ, Park YB, Woo HC, Chun BS (2016) Structural, antioxidant, and emulsifying activities of fucoidan from Saccharina japonica using pressurized liquid extraction. Carbohydr Polym 153:518–525. https://doi.org/10.1016/j.carbpol.2016.08.014
Saravana PS, Getachew AT, Cho YJ, Choi JH, Park YB, Woo HC, Chun BS (2017) Influence of co-solvents on fucoxanthin and phlorotannin recovery from brown seaweed using supercritical CO2. J Supercrit Fluids 120:295–303. https://doi.org/10.1016/j.supflu.2016.05.037
Saravana PS, Cho YN, Woo HC, Chun BS (2018) Green and efficient extraction of polysaccharides from brown seaweed by adding deep eutectic solvent in subcritical water hydrolysis. J Clean Prod 198:1474–1484. https://doi.org/10.1016/j.jclepro.2018.07.151
Saravana PS, Shanmugapriya K, Gereniu CRN, Chae SJ, Kang HW, Woo HC, Chun BS (2019) Ultrasound-mediated fucoxanthin rich oil nanoemulsions stabilized by κ-carrageenan: process optimization, bio-accessibility and cytotoxicity. Ultrason Sonochem 55:105–116. https://doi.org/10.1016/j.ultsonch.2019.03.014
Sathya R, Kanaga N, Sankar P, Jeeva S (2017) Antioxidant properties of phlorotannins from brown seaweed Cystoseira trinodis (Forsskål) C. Agardh Arab J Chem 10:2608–2614. https://doi.org/10.1016/j.arabjc.2013.09.039
Scaife MA, Merkx-Jacques A, Woodhall DL, Armenta RE (2015) Algae biofuels in Canada: status and potential. Renew Sust Energ Rev 44:620–642. https://doi.org/10.1016/j.rser.2014.12.024
Schiener P, Atack T, Wareing R, Kelly MS, Hughes AD (2016) The by-products from marine biofuels as a feed source for the aquaculture industry: a novel example of the biorefinery approach. Biomass Convers Biorefinery 6:281–287. https://doi.org/10.1007/s13399-015-0190-6
Schmid M, Guihéneuf F, Stengel DB (2016) Evaluation of food grade solvents for lipid extraction and impact of storage temperature on fatty acid composition of edible seaweeds Laminaria digitata (Phaeophyceae) and Palmaria palmata (Rhodophyta). Food Chem 208:161–168. https://doi.org/10.1016/j.foodchem.2016.03.123
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. https://doi.org/10.1016/j.foodchem.2018.05.060
Seghetta M, Hou X, Bastianoni S, Bjerre AB, Thomsen M (2016) Life cycle assessment of macroalgal biorefinery for the production of ethanol, proteins and fertilizers—a step towards a regenerative bioeconomy. J Clean Prod 137:1158–1169. https://doi.org/10.1016/j.jclepro.2016.07.195
Shang YF, Kim SM, Lee WJ, Um BH (2011) Pressurized liquid method for fucoxanthin extraction from Eisenia bicyclis (Kjellman) Setchell. J Biosci Bioeng 111(2):237–241. https://doi.org/10.1016/j.jbiosc.2010.10.008
Shao P, Qin M, Han L, Sun P (2014) Rheology and characteristics of sulfated polysaccharides from chlorophytan seaweeds Ulva fasciata. Carbohydr Polym 113:365–372. https://doi.org/10.1016/j.carbpol.2014.07.008
Shi Q, Wang A, Lu Z, Qin C, Hu J, Yin J (2017) Overview on the antiviral activities and mechanisms of marine polysaccharides from seaweeds. Carbohydr Res 453–454:1–9. https://doi.org/10.1016/j.carres.2017.10.020
Silva TH, Alves A, Popa EG, Reys LL, Gomes ME, Sousa RA, Silva SS, Mano JF, Reis RL (2012) Marine algae sulphated polysaccharides for tissue engineering and drug delivery approaches. Biomatter 2(4):278–289. https://doi.org/10.4161/biom.22947
Silva M, Gomes F, Oliveira F, Morais S, Delerue-Matos C (2015) Microwave-assisted alginate extraction from Portuguese Saccorhiza polyschides—influence of acid pretreatment. Int J Chem Nucl Metall Mater Eng 9(1):30–33. https://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.688.198&rep=rep1&type=pdf
Singh S, Gaikwad KK, Park SI, Lee YS (2017) Microwave-assisted step reduced extraction of seaweed (Gelidiella aceroso) cellulose nanocrystals. Int J Biol Macromol 99:506–510. https://doi.org/10.1016/j.ijbiomac.2017.03.004
Skjermo J, Aasen IM, Arff J, Broch OJ, Carvajal A, Christie H, Forbord S, Olsen Y, Reitan KI, Rustad T, Sandquist J, Solbakken R, Steinhovden KB, Wittgens B, Wolff R, Handå A (2014) A new Norwegian bioeconomy based on cultivation and processing of seaweeds: opportunities and R&D needs. SINTEF Fish Aquacult. https://sintef.brage.unit.no/sintef-xmlui/handle/11250/2448125
Smit AJ (2004) Medicinal and pharmaceutical uses of seaweed natural products: a review. JAppl Phycol 16:245–262. https://doi.org/10.1023/B:JAPH.0000047783.36600.ef
Sousa AMM, Alves VD, Morais S, Delerue-Matos C, Gonçalves MP (2010) Agar extraction from integrated multitrophic aquacultured Gracilaria vermiculophylla: evaluation of a microwave-assisted process using response surface methodology. Bioresour Technol 101(9):3258–3267. https://doi.org/10.1016/j.biortech.2009.12.061
Stabili L, Acquaviva MI, Biandolino F, Cavallo RA, De Pascali SA, Fanizzi FP, Narracci M, Petrocelli A, Cecere E (2012) The lipidic extract of the seaweed Gracilariopsis longissima (Rhodophyta, Gracilariales): a potential resource for biotechnological purposes? N Biotechnol 29(3):443–450. https://doi.org/10.1016/j.nbt.2011.11.003
Stabili L, Acquaviva MI, Biandolino F, Cavallo RA, De Pascali SA, Fanizzi FP, Narracci M, Cecere E, Petrocelli A (2014) Biotechnological potential of the seaweed Cladophora repestris (Chlorophyta, Cladophorales) lipidic extract. N Biotechnol 31(5):436–444. https://doi.org/10.1016/j.nbt.2014.05.002
Sudhakar K, Mamat R, Samykano M, Azmi WH, Ishak WFW, Yusaf T (2018) An overview of marine macroalgae as bioresource. Renew Sust Energ Rev 91:165–179. https://doi.org/10.1016/j.rser.2018.03.100
Sunwoo IY, Ra CH, Jeong G, Jeong GT, Kim SK (2016) Evaluation of ethanol production and bioadsorption of heavy metals by various red seaweeds. Bioprocess Biosyst Eng 39:915–923. https://doi.org/10.1007/s00449-016-1571-3
Talmaciu AI, Volf I, Popa VI (2015) A comparative analysis of the “Green” techniques applied for polyphenols extraction from bioresources. Chem Biodivers 12:1635–1651. https://doi.org/10.1002/cbdv.201400415
Tang DYY, Yew GY, Koyande AK, Chew KW, Vo DVN, Show PL (2020) Green technology for the industrial production of biofuels and bioproducts from microalgae: a review. Environ Chem Lett. https://doi.org/10.1007/s10311-020-01052-3
Tedesco S, Stokes J (2017) Valorisation to biogas of macroalgal waste streams: a circular approach to bioproducts and bioenergy in Ireland. Chem Pap 71:721–728. https://doi.org/10.1007/s11696-016-0005-7
Tedesco S, Daniels S (2018) Optimisation of biogas generation from brown seaweed residues: compositional and geographical parameters affecting the viability of a biorefinery concept. Appl Energy 228:712–723. https://doi.org/10.1016/j.apenergy.2018.06.120
Thamke VR, Chaudhari AU, Tapase SR, Paul D, Kodam KM (2019) In vitro toxicological evaluation of ionic liquids and development of effective bioremediation process for their removal. Environ Pollut 250:567–577. https://doi.org/10.1016/j.envpol.2019.04.043
Thomas NV, Kim SK (2013) Beneficial effects of marine algal compounds in cosmeceuticals. Mar Drugs 11(1):146–164. https://doi.org/10.3390/md11010146
Tierney MS, Smyth TJ, Rai DK, Soler-Vila A, Croft AK, Brunton N (2013) Enrichment of polyphenol contents and antioxidant activities of Irish brown macroalgae using food-friendly techniques based on polarity and molecular size. Food Chem 139(1–4):753–761. https://doi.org/10.1016/j.foodchem.2013.01.019
Trivedi TJ, Kumar A (2014) Efficient extraction of agarose from red algae using ionic liquids. Green Sustain Chem 4:190–201. https://doi.org/10.4236/gsc.2014.44025
Trivedi J, Aila M, Bangwal DP, Kaul S, Garg MO (2015) Algae based biorefinery—how to make sense? Renew Sust Energ Rev 47:295–307. https://doi.org/10.1016/j.rser.2015.03.052
Trivedi N, Baghel RS, Bothwell J, Gupta V, Reddy CRK, Lali AM, Jha B (2016) An integrated process for the extraction of fuel and chemicals from marine macroalgal biomass. Sci Rep 6:30728. https://doi.org/10.1038/srep30728
Uy SF, Easteal AJ, Farid MM, Keam RB, Conner GT (2005) Seaweed processing using industrial single-mode cavity microwave heating: a preliminary investigation. Carbohydr Res 340(7):1357–1364. https://doi.org/10.1016/j.carres.2005.02.008
Vanda H, Dai Y, Wilson EG, Verpoorte R, Choi YH (2018) Green solvents from ionic liquids and deep eutectic solvents to natural deep eutectic solvents. C R Chim 21:628–638. https://doi.org/10.1016/j.crci.2018.04.002
van Ginneken VJT, Helsper JPFG, de Visser W, van Keulen H (2011) Brandenburg WA Polyunsaturated fatty acids in various macroalgal species from north Atlantic and tropical seas. Lipids Health Dis 10(1):104. https://doi.org/10.1186/1476-511X-10-104
Vieira EF, Soares C, Machado S, Correia M, Ramalhosa MJ, Oliva-teles MT, Carvalho AP, Domingues VF, Antunes F, Oliveira TAC, Morais S, Delerue-Matos C (2018) Seaweeds from the Portuguese coast as a source of proteinaceous material: total and free amino acid composition profile. Food Chem 269:264–275. https://doi.org/10.1016/j.foodchem.2018.06.145
Vishchuk OS, Ermakova SP, Zvyagintseva TN (2011) Sulfated polysaccharides from brown seaweeds Saccharina japonica and Undaria pinnatifida: isolation, structural characteristics, and antitumor activity. Carbohydr Res 346:2769–2776. https://doi.org/10.1016/j.carres.2011.09.034
Vo T, Ngo D, Kim S (2012) Marine algae as a potential pharmaceutical source for anti-allergic therapeutics. Process Biochem 47:386–394. https://doi.org/10.1016/j.procbio.2011.12.014
Wan P, Yang X, Cai B, Chen H, Sun H, Chen D, Pan J (2015) Ultrasonic extraction of polysaccharides from Laminaria japonica and their antioxidative and glycosidase inhibitory activities. J Ocean Univ China 14(4):651–662. https://doi.org/10.1007/s11802-015-2648-3
Wang T, Jónsdóttir R, Ólafsdóttir G (2009) Total phenolic compounds, radical scavenging and metal chelation of extracts from Icelandic seaweeds. Food Chem 116(1):240–248. https://doi.org/10.1016/j.foodchem.2009.02.041
Wang T, Jónsdóttir R, Kristinsson HG, Hreggvidsson GO, Jónsson JÓ, Thorkelsson G, Ólafsdóttir G (2010) Enzyme-enhanced extraction of antioxidant ingredients from red algae Palmaria palmata. LWT Food Sci Technol 43:1387–1393. https://doi.org/10.1016/j.lwt.2010.05.010
Wang D, Yun EJ, Kim S, Kim DH, Seo N, An HJ, Kim J-H, Cheong NY, Kim KH (2016) Efficacy of acidic pretreatment for the saccharification and fermentation of alginate from brown macroalgae. Bioprocess Biosyst Eng 39:959–966. https://doi.org/10.1007/s00449-016-1575-z
Wei N, Quarterman J, Jin YS (2013) Marine macroalgae: an untapped resource for producing fuels and chemicals. Trends Biotechnol 31(2):70–77. https://doi.org/10.1016/j.tibtech.2012.10.009
Wijesekara I, Pangestuti R, Kim S-K (2011) Biological activities and potential health benefits of sulfated polysaccharides derived from marine algae. Carbohydr Polym 84:14–21. https://doi.org/10.1016/j.carbpol.2010.10.062
Wijesinghe WAJP, Jeon YJ (2012) Enzyme-assistant extraction (EAE) of bioactive components: a useful approach for recovery of industrially important metabolites from seaweeds: a review. Fitoterapia 83:6–12
Woo MN, Jeon SM, Kim HJ, Lee MK, Shin SK, Shin YC, Park YB, Choi MS (2010) Fucoxanthin supplementation improves plasma and hepatic lipid metabolism and blood glucose concentration in high-fat fed C57BL/6N mice. Chem Biol Interact 186:316–322. https://doi.org/10.1016/j.cbi.2010.05.006
Xia A, Jacob A, Herrmann C, Tabassum MR, Murphy JD (2015) Production of hydrogen, ethanol and volatile fatty acids from the seaweed carbohydrate mannitol. Bioresour Technol 193:488–497. https://doi.org/10.1016/j.biortech.2015.06.130
Yi YB, Lee JW, Chung Ch (2015) Conversion of plant materials into hydroxymethylfurfural using ionic liquids. Environ Chem Lett 13:173–190. https://doi.org/10.1007/s10311-015-0503-9
Youssouf L, Lallemand L, Giraud P, Soulé F, Bhaw-Luximon A, Meilhac O, D’Hellencourt CL, Jhurry D, Couprie J (2017) Ultrasound-assisted extraction and structural characterization by NMR of alginates and carrageenans from seaweeds. Carbohydr Polym 166:55–63. https://doi.org/10.1016/j.carbpol.2017.01.041
Yuan Y, Macquarrie DJ (2015a) Microwave assisted step-by-step process for the production of fucoidan, alginate sodium, sugars and biochar from Ascophyllum nodosum through a biorefinery concept. Bioresour Technol 198:819–827. https://doi.org/10.1016/j.biortech.2015.09.090
Yuan Y, Macquarrie D (2015b) Microwave assisted extraction of sulfated polysaccharides (fucoidan) from Ascophyllum nodosum and its antioxidant activity. Carbohydr Polym 129:101–107. https://doi.org/10.1016/j.carbpol.2015.04.057
Zaharudin N, Staerk D, Dragsted LO (2019) Inhibition of α-glucosidase activity by selected edible seaweeds and fucoxanthin. Food Chem 270:481–486. https://doi.org/10.1016/j.foodchem.2018.07.142
Zhang Z, Zhang Q, Wang J, Song H, Zhang H, Niu X (2010) Regioselective syntheses of sulphated porphyrans from Porphyra haitanensis and their antioxidant and anticoagulant activities in vitro. Carbohydr Polym 79:1124–1129. https://doi.org/10.1016/j.carbpol.2009.10.055
Funding
This study is part of the Ph.D. thesis carried out by the first author within the Laboratory of Bioresources (Med-Res) at “Gheorghe Asachi” Technical University of Iasi. Ph.D. scholarship was awarded by Romanian Government. This work was also partially financed by: Base Funding—UIDB/50,020/2020 of the Associate Laboratory LSRE-LCM—funded by national funds through FCT/MCTES (PIDDAC). S. Santos acknowledges postdoctoral scholarship (SFRH/BPD/117,387/2016), awarded by the Portuguese Science and Technology Foundation (FCT) and financed by National Funds and by the European Social Fund (ESF) through the Human Capital Operational Programme (POCH).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflict of interest to declare related to the content of this article.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Filote, C., Santos, S.C.R., Popa, V.I. et al. Biorefinery of marine macroalgae into high-tech bioproducts: a review. Environ Chem Lett 19, 969–1000 (2021). https://doi.org/10.1007/s10311-020-01124-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10311-020-01124-4