Skip to main content
Log in

Performance evaluation of green and integrated extraction approaches for the recovery of fatty acids, polysaccharides, and proteins from brown macroalgae for a sustainable biorefinery

  • Research
  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

This work centered on the valorization of brown macroalgae by sequentially extracting multiple value-added compounds using emerging green extraction techniques. Supercritical fluid extraction (SFE) was used to extract lipids (up to 8%) from Padina tetrastromatica and Turbinaria conoides biomass, which was found to be rich in polyunsaturated fatty acids with multiple potential nutraceutical applications. Using the subcritical water (ScW) technique, 48 wt % sodium alginate and 11 wt % protein were then recovered from the SFE residual biomass. The alginate derived from ScW contained mannuronic (M) and guluronic acids (G) with M/G ratio greater than 1, fulfilling WHO and FAO guidelines for the nutraceutical and pharmaceutical industries. Alginate extracted using ScW exhibited up to 80% in vitro 2,2-diphenyl-1-picrylhydrazyl scavenging activity and 2,2'-azino-bis (3-ethylbenzothiazoline-6-sulfonic acid) radical scavenging activity. Thus, an integrated method has been designed to valorize biomass by extracting commercially relevant valuable compounds from macroalgae utilizing green and sustainable technologies, which could be used to scale-up extraction of these compounds by a variety of industrial sectors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data availability

The data supporting the findings of this study are available from the corresponding author, Dr. Satyanarayan Naik, upon reasonable request.

References

  • Abka-khajouei R, Tounsi L, Shahabi N, Patel AK, Abdelkafi S, Michaud P (2022) Structures, properties and applications of alginates. Mar Drugs 20:364

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aida TM, Yamagata T, Watanabe M, Smith RL (2010) Depolymerization of sodium alginate under hydrothermal conditions. Carbohydr Polym 80:296–302

    CAS  Google Scholar 

  • Alboofetileh M, Rezaei M, Tabarsa M, Rittà M, Donalisio M, Mariatti F, You SG, Lembo D, Cravotto G (2019) Effect of different non-conventional extraction methods on the antibacterial and antiviral activity of fucoidans extracted from Nizamuddinia zanardinii. Int J Biol Macromol 124:131–137

    CAS  PubMed  Google Scholar 

  • Angell AR, Mata L, de Nys R, Paul NA (2016) The protein content of seaweeds: a universal nitrogen-to-protein conversion factor of five. J Appl Phycol 28:511–524

    CAS  Google Scholar 

  • Arnao MB, Cano A, Acosta M (2001) The hydrophilic and lipophilic contribution to total antioxidant activity. Food Chem 73:239–244

    CAS  Google Scholar 

  • Bi D, Yang X, Yao L, Hu Z, Li H, Xu X, Lu J (2022) Potential food and nutraceutical applications of alginate: A review. Mar Drugs 20:564

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bittkau KS, Neupane S, Alban S (2020) Initial evaluation of six different brown algae species as source for crude bioactive fucoidans. Algal Res 45:101759

  • Blois MS (1958) Antioxidant determinations by the use of a stable free radical. Nature 181:1199–1200

    CAS  ADS  Google Scholar 

  • Borazjani NJ, Tabarsa M, You SG, Rezaei M (2017) Effects of extraction methods on molecular characteristics, antioxidant properties and immunomodulation of alginates from Sargassum angustifolium. Int J Biol Macromol 101:703–711

    CAS  PubMed  Google Scholar 

  • Bordoloi A, Goosen NJ (2020) A greener alternative using subcritical water extraction to valorize the brown macroalgae Ecklonia maxima for bioactive compounds. J Appl Phycol 32:2307–2319

    CAS  Google Scholar 

  • Bouissil S, El Alaoui-Talibi Z, Pierre G, Michaud P, El Modafar C, Delattre C (2020) Use of alginate extracted from moroccan brown algae to stimulate natural defense in date palm roots. Molecules 25:720

    CAS  PubMed  PubMed Central  Google Scholar 

  • Caf F, Yilmaz Ö, Durucan F, Özdemir NŞ (2015) Biochemical components of three marine macroalgae (Padina pavonica, Ulva lactuca and Taonia atomaria) from the Levantine Sea coast of Antalya, Turkey. J Biodivers Env Sci 6:401–411

    Google Scholar 

  • Chattopadhyay N, Ghosh T, Sinha S, Chattopadhyay K, Karmakar P, Ray B (2010) Polysaccharides from Turbinaria conoides: Structural features and antioxidant capacity. Food Chem 118:823–829

    CAS  Google Scholar 

  • Chen H, Zhang L, Long X, Li P, Chen S, Kuang W, Guo J (2017) Sargassum fusiforme polysaccharides inhibit VEGF-A-related angiogenesis and proliferation of lung cancer in vitro and in vivo. Biomed Pharmacother 85:22–27

    CAS  PubMed  Google Scholar 

  • Conde E, Moure A, Domínguez H (2015) Supercritical CO2 extraction of fatty acids, phenolics and fucoxanthin from freeze-dried Sargassum muticum. J Appl Phycol 27:957–964

    CAS  Google Scholar 

  • Dawczynski C, Schubert R, Jahreis G (2007) Amino acids, fatty acids, and dietary fibre in edible seaweed products. Food Chem 103:891–899

    CAS  Google Scholar 

  • El-Shenody RA, Ashour M, Ghobara MME (2019) Evaluating the chemical composition and antioxidant activity of three Egyptian seaweeds: Dictyota dichotoma, Turbinaria decurrens, and Laurencia obtusa. Braz J Food Technol 22:e2018203

    CAS  Google Scholar 

  • El Atouani S, Bentiss F, Reani A, Zrid R, Belattmania Z, Pereira L, Mortadi A, Cherkaoui O, Sabour B (2016) The invasive brown seaweed Sargassum muticum as new resource for alginate in Morocco: Spectroscopic and rheological characterization. Phycol Res 64:185–193

    Google Scholar 

  • Esquivel-Hernández DA, López VH, Rodríguez-Rodríguez J, Alemán-Nava GS, Cuéllar-Bermúdez SP, Rostro-Alanis M, Parra-Saldívar R (2016) Supercritical carbon dioxide and microwave-assisted extraction of functional lipophilic compounds from Arthrospira platensis. Int J Mol Sci 17:658

    PubMed  PubMed Central  Google Scholar 

  • Faidi A, Farhat F, Boina DA, Touati M, Le-Nouen D, Stumbé JF (2020) Physico-chemical characterization of alginates isolated from a Tunisian Padina pavonica algae as a sustainable biomaterial. Polym Int 69:1130–1139

    CAS  Google Scholar 

  • Fawzy MA, Gomaa M (2021) Optimization of citric acid treatment for the sequential extraction of fucoidan and alginate from Sargassum latifolium and their potential antioxidant and FE(III) chelation properties. J Appl Phycol 33:2523–2535

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Fertah M, Belfkira A, Dahmane E montassir, Taourirte M, Brouillette F (2017) Extraction and characterization of sodium alginate from Moroccan Laminaria digitata brown seaweed. Arab J Chem 10:S3707–S3714

  • Fletcher HR, Biller P, Ross AB, Adams JMM (2017) The seasonal variation of fucoidan within three species of brown macroalgae. Algal Res 22:79–86

    Google Scholar 

  • Flórez-Fernández N, Domínguez H, Torres MD (2019) A green approach for alginate extraction from Sargassum muticum brown seaweed using ultrasound-assisted technique. Int J Biol Macromol 124:451–459

    PubMed  Google Scholar 

  • Ganapathy S, Lingappa S, Naidu K, Selvaraj U, Ramachandiran S, Ponnusamy S, Somasundaram ST (2019) Isolation and bioactive potential of fucoidan from marine macroalgae Turbinaria conoides. ChemistrySelect 4:14114–14119

    CAS  Google Scholar 

  • Gerde JA, Wang T, Yao L, Jung S, Johnson LA, Lamsal B (2013) Optimizing protein isolation from defatted and non-defatted Nannochloropsis microalgae biomass. Algal Res 2:145–153

    Google Scholar 

  • Gómez-Ordóñez E, Rupérez P (2011) FTIR-ATR spectroscopy as a tool for polysaccharide identification in edible brown and red seaweeds. Food Hydrocoll 25:1514–1520

    Google Scholar 

  • Gomez LP, Alvarez C, Zhao M, Tiwari U, Curtin J, Garcia-Vaquero M, Tiwari BK (2020) Innovative processing strategies and technologies to obtain hydrocolloids from macroalgae for food applications. Carbohydr Polym 248:116784

    CAS  PubMed  Google Scholar 

  • Gupta SC, Kunnumakkara AB, Aggarwal S, Aggarwal BB (2018) Inflammation, a double-edge sword for cancer and other age-related diseases. Front Immunol 9:2160

    PubMed  PubMed Central  Google Scholar 

  • Hans N, Malik A, Naik S (2021) Antiviral activity of sulfated polysaccharides from marine algae and its application in combating COVID-19: Mini review. Bioresour Technol Rep 13:100623

    CAS  PubMed  Google Scholar 

  • Hans N, Pattnaik F, Malik A, Naik S (2023) Comparison of different green extraction techniques and their influence on chemical characteristics of sulfated polysaccharide (fucoidan) from Padina tetrastromatica and Turbinaria conoides. Algal Res 74:103199

    Google Scholar 

  • Heidaryan E, Hatami T, Rahimi M, Moghadasi J (2011) Viscosity of pure carbon dioxide at supercritical region: Measurement and correlation approach. J Supercrit Fluids 56:144–151

    CAS  Google Scholar 

  • Ismail GA, Gheda SF, Abo-Shady AM, Abdel-Karim OH (2020) In vitro potential activity of some seaweeds as antioxidants and inhibitors of diabetic enzymes. Food Sci Technol 40:681–691

    Google Scholar 

  • Jiao W, Chen W, Mei Y, Yun Y, Wang B, Zhong Q, Chen H, Chen W (2019) Effects of molecular weight and guluronic acid/mannuronic acid ratio on the rheological behavior and stabilizing property of sodium alginate. Molecules 24:4374

    CAS  PubMed  PubMed Central  Google Scholar 

  • Khajouei RA, Keramat J, Hamdami N, Ursu AV, Delattre C, Laroche C, Gardarin C, Lecerf D, Desbrières J, Djelveh G, Michaud P (2018) Extraction and characterization of an alginate from the Iranian brown seaweed Nizimuddinia zanardini. Int J Biol Macromol 118:1073–1081

    CAS  PubMed  Google Scholar 

  • Kokilam G, Vasuki S, Sajitha N (2013) Biochemical composition, alginic acid yield and antioxidant activity of brown seaweeds from mandapam region, gulf of Mannar. J Appl Pharm Sci 3:99–104

    CAS  Google Scholar 

  • Larsen B, Salem DMSA, Sallam MAE, Mishrikey MM, Beltagy AI (2003) Characterization of the alginates from algae harvested at the Egyptian Red Sea coast. Carbohydr Res 338:2325–2336

    CAS  PubMed  Google Scholar 

  • Lee KY, Mooney DJ (2012) Alginate: Properties and biomedical applications. Prog Polym Sci 37:106–126

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SC, Prosky L, De VJW (1992) Determination of total, soluble, and insoluble dietary fiber in foods—Enzymatic-gravimetric method, MES-TRIS buffer: Collaborative study. J AOAC Int 75:395–416

    CAS  Google Scholar 

  • Liu M, Liu Y, Cao MJ, Liu GM, Chen Q, Sun L, Chen H (2017) Antibacterial activity and mechanisms of depolymerized fucoidans isolated from Laminaria japonica. Carbohydr Polym 172:294–305

    CAS  PubMed  Google Scholar 

  • Lopes D, Melo T, Rey F, Meneses J, Monteiro FL, Helguero LA, Abreu MH, Lillebø AI, Calado R, Domingues MR (2020) Valuing bioactive lipids from green, red and brown macroalgae from aquaculture, to foster functionality and biotechnological applications. Molecules 25:3883

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Lorenzen J, Igl N, Tippelt M, Stege A, Qoura F, Sohling U, Brück T (2017) Extraction of microalgae derived lipids with supercritical carbon dioxide in an industrial relevant pilot plant. Bioprocess Biosyst Eng 40:911–918

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Luo X, Duan Y, Yang W, Zhang H, Li C, Zhang J (2017) Structural elucidation and immunostimulatory activity of polysaccharide isolated by subcritical water extraction from Cordyceps militaris. Carbohydr Polym 157:794–802

    CAS  PubMed  Google Scholar 

  • Mathur M, Hans N, Naaz F, Naik SN, Pant KK, Malik A (2022) Valorization of microalgal biomass to value-added products using integrated supercritical CO2 extraction and sub-critical hydrothermal liquefaction. J Clean Prod 373:133925

    CAS  Google Scholar 

  • McKennedy J, Önenç S, Pala M, Maguire J (2016) Supercritical carbon dioxide treatment of the microalgae Nannochloropsis oculata for the production of fatty acid methyl esters. J Supercrit Fluids 116:264–270

    CAS  Google Scholar 

  • Fauziee NAM, Chang LS, Wan Mustapha WA, MdNor AR, Lim SJ (2021) Functional polysaccharides of fucoidan, laminaran and alginate from Malaysian brown seaweeds (Sargassum polycystum, Turbinaria ornata and Padina boryana). Int J Biol Macromol 167:1135–1145

  • Molino A, Iovine A, Casella P, Mehariya S, Chianese S, Cerbone A, Rimauro J, Musmarra D (2018) Microalgae characterization for consolidated and new application in human food, animal feed and nutraceuticals. Int J Environ Res Public Health 15:2436

    CAS  PubMed  PubMed Central  Google Scholar 

  • Naveen J, Baskaran R, Baskaran V (2021) Profiling of bioactives and in vitro evaluation of antioxidant and antidiabetic property of polyphenols of marine algae Padina tetrastromatica. Algal Res 55:102250

    Google Scholar 

  • Nguyen TT, Mikkelsen MD, Tran VHN, Trang VTD, Rhein-Knudsen N, Holck J, Rasin AB, Cao HTT, Van TTT, Meyer AS (2020) Enzyme-assisted fucoidan extraction from brown macroalgae Fucus distichus subsp. evanescens and Saccharina latissima. Mar Drugs 18:296

  • O’Fallon JV, Busboom JR, Nelson ML, Gaskins CT (2007) A direct method for fatty acid methyl ester synthesis: Application to wet meat tissues, oils, and feedstuffs. J Anim Sci 85:1511–1521

    PubMed  Google Scholar 

  • Okolie CL, Mason B, Mohan A, Pitts N, Udenigwe CC (2020) Extraction technology impacts on the structure-function relationship between sodium alginate extracts and their in vitro prebiotic activity. Food Biosci 37:100672

    CAS  Google Scholar 

  • Olsson J, Toth GB, Albers E (2020) Biochemical composition of red, green and brown seaweeds on the Swedish west coast. J Appl Phycol 32:3305–3317

    CAS  Google Scholar 

  • Parthiban C, Saranya C, Girija K, Hemalatha A, Suresh M, Anantharaman P (2013) Biochemical composition of some selected seaweeds from Tuticorin coast. Pelagia Res Libr 4:362–366

    CAS  Google Scholar 

  • Pattnaik F, Nanda S, Kumar V, Naik S, Dalai AK (2021) Subcritical water hydrolysis of Phragmites for sugar extraction and catalytic conversion to platform chemicals. Biomass Bioenergy 145:105965

    CAS  Google Scholar 

  • Ponce NMA, Flores ML, Pujol CA, Becerra MB, Navarro DA, Córdoba O, Damonte EB, Stortz CA (2019) Fucoidans from the phaeophyta Scytosiphon lomentaria: Chemical analysis and antiviral activity of the galactofucan component. Carbohydr Res 478:18–24

    CAS  PubMed  Google Scholar 

  • Ravi P, Subramanian G (2017) Biochemical studies on marine algal species of Padina (Phaeophyceae) from Mandapam coastline, Tamil Nadu, India. World J Pharm Res 3:5041–5048

  • Remya RR, Rajasree SRR, Suman TY, Aranganathan L, Gayathri S, Gobalakrishnan M, Karthih MG (2019) Studies on proximate composition and phytochemical profiling of Turbinaria ornata and its antiproliferative effect on Y79 cell lines. Thalassas 35:495–502

    Google Scholar 

  • Rhein-Knudsen N, Ale MT, Ajalloueian F, Meyer AS (2017) Characterization of alginates from Ghanaian brown seaweeds: Sargassum spp. and Padina spp. Food Hydrocoll 71:236–244

    CAS  Google Scholar 

  • Sanjeewa KKA, Fernando IPS, Kim SY, Kim HS, Ahn G, Jee Y, Jeon YJ (2018) In vitro and in vivo anti-inflammatory activities of high molecular weight sulfated polysaccharide; containing fucose separated from Sargassum horneri: Short communication. Int J Biol Macromol 107:803–807

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Sellimi S, Younes I, Ayed HB, Maalej H, Montero V, Rinaudo M, Dahia M, Mechichi T, Hajji M, Nasri M (2015) Structural, physicochemical and antioxidant properties of sodium alginate isolated from a Tunisian brown seaweed. Int J Biol Macromol 72:1358–1367

    CAS  PubMed  Google Scholar 

  • Sereewatthanawut I, Prapintip S, Watchiraruji K, Goto M, Sasaki M, Shotipruk A (2008) Extraction of protein and amino acids from deoiled rice bran by subcritical water hydrolysis. Bioresour Technol 99:555–561

    CAS  PubMed  Google Scholar 

  • Singleton VL, Rossi Jr JA, Rossi Jr JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158

  • Terme N, Boulho R, Kendel M, Kucma JP, Wielgosz-Collin G, Bourgougnon N, Bedoux G (2017) Selective extraction of lipid classes from Solieria chordalis and Sargassum muticum using supercritical carbon dioxide and conventional solid–liquid methods. J Appl Phycol 29:2513–2519

    CAS  Google Scholar 

  • Torabi P, Hamdami N, Keramat J (2022) Microwave-assisted extraction of sodium alginate from brown macroalgae Nizimuddinia zanardini, optimization and physicochemical properties. Sep Sci Technol 57:872–885

    CAS  Google Scholar 

  • Trica B, Delattre C, Gros F, Ursu AV, Dobre T, Djelveh G, Michaud P, Oancea F (2019) Extraction and characterization of alginate from an edible brown seaweed (Cystoseira barbata) harvested in the Romanian Black Sea. Mar Drugs 17:405

    CAS  PubMed  PubMed Central  Google Scholar 

  • Trigueros E, Sanz MT, Alonso-Riaño P, Beltrán S, Ramos C, Melgosa R (2021) Recovery of the protein fraction with high antioxidant activity from red seaweed industrial solid residue after agar extraction by subcritical water treatment. J Appl Phycol 33:1181–1194

    CAS  Google Scholar 

  • Ummat V, Tiwari BK, Jaiswal AK, Condon K, Garcia-Vaquero M, O’Doherty J, O’Donnell C, Rajauria G (2020) Optimisation of ultrasound frequency, extraction time and solvent for the recovery of polyphenols, phlorotannins and associated antioxidant activity from brown seaweeds. Mar Drugs 18:250

    CAS  PubMed  PubMed Central  Google Scholar 

  • Van Wychen S, Laurens LML (2016) Determination of total solids and ash in algal biomass: laboratory analytical procedure (LAP). NREL/TP-5100–60956, National Renewable Energy Laboratory, Golden, p 11

  • Vijayraja D, Jeyaprakash K (2017) Preliminary phytochemical analysis, in vitro antioxidant and anti-inflammatory activity of Turbinaria ornata (Turner). J Agardh Res J Pharm Technol 10:2243–2248

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Zubia M, Payri C, Deslandes E (2008) Alginate, mannitol, phenolic compounds and biological activities of two range-extending brown algae, Sargassum mangarevense and Turbinaria ornata (Phaeophyta: Fucales), from Tahiti (French Polynesia). J Appl Phycol 20:1033–1043

    Google Scholar 

  • Zubia M, Stiger-Pouvreau V, Mattio L, Payri CE, Stewart HL (2020) A comprehensive review of the brown macroalgal genus Turbinaria J.V. Lamouroux (Fucales, Sargassaceae). J Appl Phycol 32:2743–2760

    Google Scholar 

Download references

Acknowledgements

The authors sincerely acknowledge the Indian Institute of Technology Delhi for the financial and technical support to carry out this research work. The authors are grateful to Central Research Facility (CRF), IIT Delhi and Advanced Instrumentation Research Facility (ARIF), JNU Delhi, for help with ICP-MS, FTIR, HPLC, NMR and SEM.

Funding

The authors acknowledge funding from IIT Delhi to carry out the research work.

Author information

Authors and Affiliations

Authors

Contributions

Nidhi Hans: Conceptualization, Methodology, Formal analysis, Investigation, Resources, Software, Data curation, Writing - original draft, Visualization, Experimentation. Anushree Malik: Conceptualization, Supervision, Proofreading and Funding acquisition. Satyanarayan Naik: Conceptualization, Supervision, Proofreading and Funding acquisition.

Corresponding authors

Correspondence to Nidhi Hans or Satyanarayan Naik.

Ethics declarations

Competing interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 1856 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hans, N., Malik, A. & Naik, S. Performance evaluation of green and integrated extraction approaches for the recovery of fatty acids, polysaccharides, and proteins from brown macroalgae for a sustainable biorefinery. J Appl Phycol 36, 341–357 (2024). https://doi.org/10.1007/s10811-023-03126-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-023-03126-5

Keywords

Navigation