Advertisement

From Current Algae Products to Future Biorefinery Practices: A Review

  • Michel H. M. Eppink
  • Giuseppe Olivieri
  • Hans Reith
  • Corjan van den Berg
  • Maria J. Barbosa
  • Rene H. Wijffels
Chapter
Part of the Advances in Biochemical Engineering/Biotechnology book series (ABE, volume 166)

Abstract

Microalgae are considered to be one of the most promising next generation bio-based/food feedstocks with a unique lipid composition, high protein content, and an almost unlimited amount of other bio-active molecules. High-value components such as the soluble proteins, (poly) unsaturated fatty acids, pigments, and carbohydrates can be used as an important ingredient for several markets, such as the food/feed/chemical/cosmetics and health industries. Although cultivation costs have decreased significantly in the last few decades, large microalgae production processes become economically viable if all complex compounds are optimally valorized in their functional state. To isolate these functional compounds from the biomass, cost-effective, mild, and energy-efficient biorefinery techniques need to be developed and applied. In this review we describe current microalgae biorefinery strategies and the derived products, followed by new technological developments and an outlook toward future products and the biorefinery philosophy.

Keywords

Biorefinery Cell disruption Cell wall composition Cellular structure Extraction Fractionation Harvesting Microalgae 

References

  1. 1.
    Langeveld JWA, Dixon J, Jaworski JF (2010) Development perspectives of the biobased economy: A review. Crop Sci 50:S-142–S-151Google Scholar
  2. 2.
    Becker EW (2007) Micro-algae as a source of proteins. Biotech Adv 25:207–210Google Scholar
  3. 3.
    Carioca JOB, Hiluy Filho JJ, Leal MRLV, Macambira FS (2009) The hard choice for alternative biofuels to diesel in Brazil. Biotechnol Adv 27:1043–1050PubMedGoogle Scholar
  4. 4.
    Eppink MHM, Barbosa MJ, Wijffels RH (2012) Biorefinery of microalgae: production of high value products, bulk chemicals and biofuels. In: Posten C, Walter C (eds) Microalgal biotechnology. De Gruyter, Berlin Google Scholar
  5. 5.
    Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microb Biotechnol 65:635–648Google Scholar
  6. 6.
    Chisti Y (2007) Biodiesel from microalgae. Biotech Adv 25:294–306Google Scholar
  7. 7.
    Schenk PM, Thomas-Hall RS, Stephens E, Marx UC, et al. (2008) Second generation biofuels: high-efficiency microalgae for biodiesel production. Bioenergy Res 1:20–43Google Scholar
  8. 8.
    Priyararshani I, Rath B (2012) Commercial and industrial applications of micro algae—a review. J Algal Biomass Utln 3:89–100Google Scholar
  9. 9.
    Ho S-H, Ye X, Hasunuma T, Chang J-S, Kondo A (2014) Perspectives on engineering strategies for improving biofuel production from microalgae—a critical review. Biotech Adv 32:1448–1459Google Scholar
  10. 10.
    Rawat I, Ranjith R, Mutanda T, Bux F (2013) Biodiesel from microalgae: a critical evaluation from laboratory to large scale production. Appl Energy 103:444–467Google Scholar
  11. 11.
    Wijffels RH, Barbosa MJ (2010) An outlook on microalgal biofuels. Science 329:796–799PubMedGoogle Scholar
  12. 12.
    Chisti Y (2013) Contraints to commercialization of algal fuels. J Biotechnol 167:201–214PubMedGoogle Scholar
  13. 13.
    Torres CM, Rios SD (2013) Microalgae-based biodiesel: a multicriteria analysis of the production process using realistic scenarios. Bioresour Technol 147:7–16PubMedGoogle Scholar
  14. 14.
    Norsker NH, Barbosa MJ, Vermue MH, Wijffels RH (2011) Microalgal production—a close look at the economics. Biotechnol Adv 29:24–27PubMedGoogle Scholar
  15. 15.
    Demirbas MF (2011) Biofuels from microalgae for sustainable development. Appl Energy 88:3473–3480Google Scholar
  16. 16.
    Wijffels RH, Barbosa MJ, Eppink MHM (2010) Microalgae for the production of bulk chemicals and biofuels. Biofuels Bioprod Biorefin 4:287–295Google Scholar
  17. 17.
    Vanthoor-Koopmans M, Wijffels RH, Barbosa MJ, Eppink MHM (2013) Biorefinery of microalgae for food and fuel. Bioresour Technol 135:142–149PubMedGoogle Scholar
  18. 18.
    Yena HW, Hub IC, Chen CY (2013) Microalgae-based biorefinery—from biofuels to natural products. Bioresour Technol 135:166–174Google Scholar
  19. 19.
    Draaisma RB, Wijffels RH, Slegers PM, Brentner LB, et al. (2013) Food commodities from microalgae. Curr Opin Biotechnol 24:169–177PubMedGoogle Scholar
  20. 20.
    Cuellar-Bermudez SP, Aguilar-Hernandez I, Cardenas-Chavez DL, Ornelas-Soto N, et al. (2015) Extraction and purification of high-value metabolites from microalgae: essential lipids, astaxanthin and phycobiliproteins. Microb Biotechnol 8:190–209PubMedGoogle Scholar
  21. 21.
    Hariskos I, Posten C (2014) Biorefinery of microalgae—opportunities and constraints for different production scenarios. Biotechnol J 9:739–752PubMedGoogle Scholar
  22. 22.
    Borowitzka MA (2013) High-value products from microalgae—their development and commercialization. J Appl Phycol 25:743–756Google Scholar
  23. 23.
    Bharathiraja B, Chakravarthy M, Ranjith Kumar R, Yogendran D, et al. (2015) Aquatic biomass (algae) as a future feedstock for bio-refineries: a review on cultivation, processing and products. Renewable Sustainable Energy Rev 47:634–653Google Scholar
  24. 24.
    Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2016) Commercial applications of microalgae. J Biosci Bioeng 101:87–96Google Scholar
  25. 25.
    Koller M, Muhr A, Braunegg G (2014) Microalgae as versatile cellular factories for valued products. Algal Res 6:52–63Google Scholar
  26. 26.
    Ginzberg A, Cohen M, Sod-Moriah UA, Shany S, et al. (2000) Chickens fed with biomass of the red microalga Porphyridium sp have reduced blood cholesterol level and modified fatty acid composition in egg yolk. J Appl Phycol 12:325–330Google Scholar
  27. 27.
    Lu J, Takeuchi T, Satoh H (2014) Ingestion and assimilation of three species of freshwater algae by larval tilapia Oreochromis niloticus. Aquaculture 238:437–449Google Scholar
  28. 28.
    Mandal S, Mallick N (2009) Microalga Scenedesmus obliquus as a potential source for biodiesel production. Appl Microbiol Biotechnol 84:281–291PubMedGoogle Scholar
  29. 29.
    Chen HY, Tang HZ, Ma TC, Holland KY, Ng S, Salley SO (2011) Effect of nutrients on growth and lipid accumulation in the green algae Dunaliella tertiolecta. Bioresour Technol 102:1649–1655PubMedGoogle Scholar
  30. 30.
    Voort MPJ, Vulsteke E, Visser CLM. Macro-economics of algae products, Public Output report WP2A7.02 of the EnAlgae Project, Swansea, June 2015, 47 pGoogle Scholar
  31. 31.
    Benneman J (2013) Microalgae for biofuels and animal feeds. Energies 6:5869–5886Google Scholar
  32. 32.
    Gouveia L (2008) Microalgae in novel food products. In: Papa-doupoulos K (ed) Food chemistry research developments. Nova Science Publishers, New York, pp. 75–112Google Scholar
  33. 33.
    Kovac DJ, Simeunovic JB, Babic OB, Misan AC, Milovanovic IL (2013) Algae in food and feed. Food Feed Res 40:21–31Google Scholar
  34. 34.
    Chacon-lee TL, Gonzalez-Marino GE (2010) Microalgae for “healthy” foods—possibilities and challenges. Compr Rev Food Sci Food Saf 9:655–675Google Scholar
  35. 35.
    Ben-Amotz A (1995) New mode of Dunaliella biotechnology: two-phase growth for β-carotene production. J Appl Phycol 7:65–68Google Scholar
  36. 36.
    Kumar D, Dhar DW, Pabbi S, Kumar N, Walia S (2014) Extraction and purification of C-phycocyanin from Spirulina platensis (CCC540). Ind J Plant Physiol 19:184–188Google Scholar
  37. 37.
    Leu S, Boussiba S (2014) Advances in the production of high-value products by microalgae. Ind Biotechnol 10:169–183Google Scholar
  38. 38.
    Raposo MF, Morais RMSC (2013) Bioactivity and applications of sulphated polysaccharides from marine microalgae. Mar Drugs 11:233–252Google Scholar
  39. 39.
    Wijesekara I, Pangestuti R, Kim S-K (2011) Biological activities and potential health benefits of sulfated polysaccharides derived from marine algae. Carbohydr Polym 84:14–21Google Scholar
  40. 40.
    Arad SM, Rapoport L, Moshkovich A, van Moppes D, et al. (2006) Superior biolubricant from a species of red microalgae. Langmuir 2:7313–7317Google Scholar
  41. 41.
    Arad SM, Levy-Ontman O (2010) Red microalgal cell-wall polysaccharides: biotechnological aspects. Curr Opin Biotechnol 21:358–364PubMedGoogle Scholar
  42. 42.
    Laurienzo P (2010) Marine polysaccharides in pharmaceutical applications: an overview. Mar Drugs 8:2435–2465PubMedGoogle Scholar
  43. 43.
    Radakovitz R, Jinkerson RE, Darzins A, Posewitz MC (2010) Genetic engineering of algae for enhanced biofuel production. Eukaryotic Cell 9:486–501Google Scholar
  44. 44.
    Mendez RL, Fernandes HL, Coelho JAP, Palavra AF (1995) Supercritical CO2 extraction of carotenoids and other lipids from Chlorella vulgaris. Food Chem 53:99–103Google Scholar
  45. 45.
    Ju A (2012) Defatted microalgae (Haematococcus pluvialis) meal as a protein ingredient to partially replace fishmeal in diets of Pacific white shrimp (Litopenaeus vannamei, Boone, 1931). Aquaculture 354–355:50Google Scholar
  46. 46.
    Boussiba S, Richmond AE (1979) Isolation and characterization of phycocyanins from the blue-green alga Spirulina platensis. Arch Microbiol 120:155–159Google Scholar
  47. 47.
    Minkova KM (2013) Purification of C-phycocyanin from Spirulina (Arthrospira) fusiformis. J Biotechnol 102:55–59Google Scholar
  48. 48.
    Yan S, Zhu L, Su H, Zhang X, et al. (2011) Single-step chromatography for simultaneous purification of C-phycocyanin and allophycocyanin with high purity and recovery from Spirulina (Arthrospira) platensis. J Appl Phycol 23:1–6Google Scholar
  49. 49.
    Jubeau S, Marchal J, Pruvost J, Jaouen P, et al. (2013) High pressure disruption: a two-step treatment for selective extraction of intracellular components from the microalgae Porphyridium cruentum. J Appl Phycol 25:983–989Google Scholar
  50. 50.
    Postma PR, Miron TL, Olivier G, Barbosa MJ, et al. (2015) Mild disintegration of the green microalgae Chlorella Vulgaris using bead milling. Bioresour Technol 184:297–304PubMedGoogle Scholar
  51. 51.
    Krienitz L, Takeda H, Hepperle D (1999) Ultrastructure, cell wall composition, and phylogenetic position of Pseudodictyosphaerium jurisii (Chlorococcales, Chlorophyta) including a comparison with other picoplanktonic green algae. Phycologia 38:100–107Google Scholar
  52. 52.
    Domozych DS, Ciancia M, Fangel JU, Mikkelsen MD, et al. (2012) The cell walls of green algae: a journey through evolution and diversity. Front Plant Sci 3:1–7Google Scholar
  53. 53.
    Gerken HG, Donohoe B, Knoshaug EP (2013) Enzymatic cell wall degradation of Chlorella vulgaris and other microalgae for biofuels production. Planta 237:239–253PubMedGoogle Scholar
  54. 54.
    Scholz MJ, Weiss TL, Jinkerson RE, Jing J, et al. (2014) Ultrastructure and composition of the Nannochloropsis gaditana cell wall. Eukaryotic Cell 13:1450–1464PubMedGoogle Scholar
  55. 55.
    Popper ZA, Tuohy MG (2010) Beyond the green: understanding the evolutionary puzzle of plant and algal cell walls. Plant Physiol 153:373–383PubMedGoogle Scholar
  56. 56.
    Yamada T, Sakaguchi K (1982) Comparative studies on Chlorella cell walls: induction of protoplast formation. Arch Microbiol 132:10–13Google Scholar
  57. 57.
    Takeda H (1991) Sugar composition of the cell wall and the taxonomy of Chlorella (Chlorophyceae). J Phycol 27:224–232Google Scholar
  58. 58.
    Kapaun E, Reisser W (1995) A., Chitin-like glycan in the cell wall of a Chlorella sp. (Chlorococcales, Chlorophyceae). Planta 195:577–582Google Scholar
  59. 59.
    Blumreisinger M, Meindl D, Loos E (1983) Cell wall composition of chlorococcal algae. Phytochremistry 1603–1604:22Google Scholar
  60. 60.
    Klein U, Chen C, Gibbs M, Platt-Aloia KA (1983) Cellular fractionation of Chlamydomonas reinhardii with emphasis on the isolation of the chloroplast. Plant Physiol 72:481–487PubMedGoogle Scholar
  61. 61.
    Tardiff M, Atteia A, Specht M, Cogne G, et al. (2012) PredAlgo: a new subcellular localization prediction tool dedicated to green algae. Mol Biol Evol 29:3625–3639Google Scholar
  62. 62.
    Vandamme D, Foubert I, Muylaert K (2012) Flocculation as a low-cost method for harvesting microalgae for bulk biomass production. Trends Biotechnol 31:233–239Google Scholar
  63. 63.
    Gonzalez-Fernandez C, Ballesteros M (2013) Microalgae autoflocculation: an alternative to high-energy consuming harvesting methods. J Appl Phycol 25:991–999Google Scholar
  64. 64.
    Milledge JJ, Heaven S (2013) A review of the harvesting of micro-algae for biofuel production. Rev Environ Sci Biotechnol 12:165–178Google Scholar
  65. 65.
    Kim DY, Oh YK, Park JY, Kim B, et al. (2015) An integrated process for microalgae harvesting and cell disruption by the use of ferric ions. Bioresour Technol 191:469–474PubMedGoogle Scholar
  66. 66.
    Gerardo ML, van den Hende S, Vervaeren H, Coward T, Skill SC (2015) Harvesting of microalgae within a biorefinery approach: a review of the developments and case studies from pilot-plants. Algal Res 11:248–262Google Scholar
  67. 67.
    De Carvalho Neto RG, do Nascimento JG, Costa MC, Lopes AC, et al. (2014) Microalgae harvesting and cell disruption: a preliminary evaluation of the technology electroflotation by alternating current. Water Sci Technol 70:315–320PubMedGoogle Scholar
  68. 68.
    Dassey AJ, Theegala CS (2013) Harvesting economics and strategies using centrifugation for cost effective separation of microalgae cells for biodiesel applications. Bioresour Technol 128:241–245PubMedGoogle Scholar
  69. 69.
    Rossignol N, Vandanjon L, Jaouen P, Quemeneur F (1999) Membrane technology for the continuous separation microalgae/culture medium: compared performances of cross-flow microfiltration and ultrafiltration. Aquacult Eng 20:191–208Google Scholar
  70. 70.
    Gerardo ML, Oatley-Radcliffe DL, Lovitt RW (2014) Integration of membrane technology in microalgae biorefineries. J Membr Sci 464:86–99Google Scholar
  71. 71.
    Hwang T, Park S-J, Oh Y-K, Rashid N, Han J-I (2013) Harvesting of Chlorella sp. KR-1 using a cross-flow membrane filtration system equipped with an anti-fouling membrane. Bioresour Tech 139:379–382Google Scholar
  72. 72.
    Kang S, Kim S, Lee J (2015) Optimization of cross flow filtration system for Dunaliella tertiolecta and Tetraselmis sp. microalgae harvest. Korean J Chem. Eng 32:1377–1380Google Scholar
  73. 73.
    Safi C, Charton M, Pignolet O, Silvestre F, et al. (2013) Influence of microalgae cell wall characteristics on protein extractability and determination of nitrogen-to-protein conversion factors. J Appl Phycol 25:523–529Google Scholar
  74. 74.
    Nurra C, Clavero E, Salvado J, Torras C (2014) Vibrating membrane filtration as improved technology for microalgae dewatering. Bioresour Technol 157:247–253PubMedGoogle Scholar
  75. 75.
    Bilad MR, Vandamme D, Foubert I, Muylaert K, Vankelecom IFJ (2012) Harvesting microalgal biomass using submerged microfiltration membranes. Bioresour Technol 111:343–352PubMedGoogle Scholar
  76. 76.
    Bilad MR, Discart V, Vandamme D, Foubert I, et al. (2013) Harvesting microalgal biomass using a magnetically induced membrane vibration (MMV) system: filtration performance and energy consumption. Bioresour Technol 138:329–338PubMedGoogle Scholar
  77. 77.
    Bilad MR, Discart V, Vandamme D, Foubert I, et al. (2014) Coupled cultivation and pre-harvesting of microalgae in a membrane photobioreactor (MPBR). Bioresour Technol 155:410–417PubMedGoogle Scholar
  78. 78.
    Salim S, Bosma R, Vermue MH, Wijffels RH (2011) Harvesting of microalgae by bio-flocculation. J Appl Phycol 23:849–855PubMedGoogle Scholar
  79. 79.
    ’t Lam G, Vermue MH, Olivieri G, van den Broek LA, et al. (2014) Cationic polymers for successful flocculation of marine microalgae. Bioresour Technol 169:804–807PubMedGoogle Scholar
  80. 80.
    ’t Lam G, Zegeye EK, Vermue MH, Kleinegris DM, et al. (2015) Dosage effect of cationic polymers on the flocculation efficiency of the marine microalgae Neochloris oleoabundans. Bioresour Technol 198:797–802PubMedGoogle Scholar
  81. 81.
    ’t Lam G, Giraldo JB, Vermue MH, Olivieri G, et al. (2016) Understanding the salinity effect on cationic polymers in inducing flocculation of the microalga Neochloris oleoabundans. J Biotechnol 18:10–17Google Scholar
  82. 82.
    Brentner LB, Eckelman MJ, Zimmerman JB (2011) Combinatorial life cycle assessment to inform process design of industrial production of algal biodiesel. Environ Sci Technol 45:7060–7067PubMedGoogle Scholar
  83. 83.
    Pienkos PT, Darzins A (2009) The promise and challenges of microalgal-derived biofuels. Biofuels Bioprod Biorefin 4:287–295Google Scholar
  84. 84.
    Wileman A, Ozkan A, Berberoglu H (2011) Rheological properties of algae slurries for minimizing harvesting energy requirements in biofuel production. Bioresour Technol 104:432–439PubMedGoogle Scholar
  85. 85.
    Schlesinger A, Eisenstadt D, Bar-Gil A, Carmely H, et al. (2012) Inexpensive non-toxic flocculation of microalgae contradicts theories; overcoming a major hurdle to bulk algal production. Biotechnol Adv 30:1023–1030PubMedGoogle Scholar
  86. 86.
    Morrissey KL, Keirn MI, Inaba Y, Denham AJ, et al. (2015) Recyclable polyampholyte flocculants for the cost-effective dewatering of microalgae and cyanobacteria. Algal Res 11:304–312Google Scholar
  87. 87.
    Gunerken E, d’Hondt E, Eppink MHM, Garcia-Gonzalez L, et al. (2015) Cell disruption for microalgae biorefineries. Biotechnol Adv 33:243–260PubMedGoogle Scholar
  88. 88.
    Lee J-Y, Yoo C, Jun S, Ahn C, Oh H-M (2010) Comparison of several methods for effective lipid extraction from microalgae. Bioresour Technol 101:S75–S77PubMedGoogle Scholar
  89. 89.
    Safi C, Ursu AV, Laroche C, Zebib B, et al. (2014) Aqueous extraction of proteins from microalgae: effect of different cell disruption methods. Algal Res 3:61–61Google Scholar
  90. 90.
    Safi C, Charton M, Ursu AV, Laroche C, et al. (2014) Release of hydro-soluble microalgal proteins using mechanical and chemical treatments. Algal Res 3:55–60Google Scholar
  91. 91.
    Mutanda T, Ramesh D, Karthikeyan S, Kumari S, et al. (2011) Bioprospecting for hyper-lipid producing microalgal strains for sustainable biofuel production. Bioresour Technol 102:57–70PubMedGoogle Scholar
  92. 92.
    Grimi N, Dubois A, Marchal L, Jubeau S, et al. (2014) Selective extraction from microalgae Nannochloropsis sp. using different methods of cell disruption. Bioresour Technol. 153:254–259PubMedGoogle Scholar
  93. 93.
    Goettel M, Eing C, Gusbeth C, Straessner R, Frey W (2013) Pulsed electric field assisted extraction of intracellular valuables from microalgae. Algal Res 2:401–408Google Scholar
  94. 94.
    Zbinden MD, Sturm BS, Nord RD, Carey WJ, et al. (2013) Pulsed electric field (PEF) as an intensification pretreatment for greener solvent lipid extraction from microalgae. Biotechnol Bioeng 110:1605–1615PubMedGoogle Scholar
  95. 95.
    Parniakov O, Barba FJ, Grimi N, Marchal L, et al. (2015) Pulsed electric field and pH assisted selective extraction of intracellular components from microalgae Nannochloropsis. Algal Res 8:128–134Google Scholar
  96. 96.
    Lai YS, Parameswaran P, Li A, Baez M, Rittman BE (2014) Effect of pulsed electric field treatment on enhancing lipid recovery from the microalga Scenedesmus. Bioresour Technol 173:457–461PubMedGoogle Scholar
  97. 97.
    Barba FJ, Grimi N, Vorobiev E (2015) New approaches for the use of non-conventional cell disruption technologies to extract potential food additives and nutraceuticals from microalgae. Food Eng Rev 7:45–62Google Scholar
  98. 98.
    Postma R, Capitoli M, Barbosa M, Wijffels RH, et al. (2016) Selective extraction of intracellular components from the microalgae Chlorella vulgaris by combined pulsed electric field-temperature treatment. Bioresour Technol 203:80–88PubMedGoogle Scholar
  99. 99.
    Echevarria Parres AJ (2011) Process and apparatus for extracting biodiesel from algae, (Ed.) E.P. Application, 2011Google Scholar
  100. 100.
    Wang M, Yuan W, Jiang X, Jing Y, Wang Z (2014) Disruption of microalgal cells using high frequency focused ultrasound. Bioresour Technol 153:315–321PubMedGoogle Scholar
  101. 101.
    Yoo G, Yoo Y, Kwon J, Darpito C, et al. (2014) An effective, cost-efficient extraction method of biomass from wet microalgae with a functional polymeric membrane. Green Chem 16:312–319Google Scholar
  102. 102.
    Boussetta N, Lesaint O, Vorobiev E (2013) A study of mechanisms involved during the extraction of polyphenols from grape seeds by pulsed electrical discharges. Innovation Food Sci Emerging Technol 19:124–132Google Scholar
  103. 103.
    Dierkes H, Steinhagen V, Bork M, Lütge C, Knez Z (2012) Inventor; Uhde High Pressure Technologies GmbH, assignee. Cell lysis of plant or animal starting materials by a combination of a spray method and decompression for the selective extraction and separation of valuable intracellularmaterials. European Patent EP2315825 (B1)Google Scholar
  104. 104.
    Middelberg APJ (1995) Process scale disruption of microorganisms. Biotechnol Adv 13:491–551PubMedGoogle Scholar
  105. 105.
    Demuez M, Mahdy A, Tomas-Pejo E, Gonzalez-Fernandez C, Ballesteros M (2015) Enzymatic cell disruption of microalgae biomass in biorefinery processes. Biotechnol Bioeng 112:1955–1966PubMedGoogle Scholar
  106. 106.
    Halim R, Danquah MK, Webley PA (2012) Extraction of oil from microalgae for biodiesel production: a review. Biotechnol Adv 30:709–732PubMedGoogle Scholar
  107. 107.
    Kim J, Yoo G (2013) Methods of downstream processing for the production of biodiesel from microalgae. Biotechnol Adv 31:862–876PubMedGoogle Scholar
  108. 108.
    Grosso C, Valentao P, Ferreres F, Andrade PB (2015) Alternative and efficient extraction methods for marine-derived compounds. Mar Drugs 13:3182–3230PubMedGoogle Scholar
  109. 109.
    Yen H-W, Yang S-C, Chen C-H, Jesisca, Chang J-S (2015) Supercritical fluid extraction of valuable compounds from microalgal biomass. Bioresour Technol 184:291–296PubMedGoogle Scholar
  110. 110.
    Azevedo AM, Rosa PA, Ferreira IF, Aires-Barros MR (2009) Chromatography-free recovery of biopharmaceuticals through aqueous two-phase processing. Trends Biotechnol 27:240–247PubMedGoogle Scholar
  111. 111.
    Aquilar O, Rito-Palomares M (2010) Aqueous two-phase systems strategies for the recovery and characterization of biological products from plants. J Sci Food Agric 90:1385–1392Google Scholar
  112. 112.
    Rosa PA, Azevedo AM, Sommerfeld S, Backer W, Aires-Barros MR (2011) Aqueous two-phase extraction as a platform in the biomanufacturing industry: economical and environmental sustainability. Biotechnol Adv 29:559–567PubMedGoogle Scholar
  113. 113.
    Ruiz-Ruiz F, Benavides J, Aguilar O, Rito-Palomares M (2012) Aqueous two-phase affinity partitioning systems: Current applications and trends. J Chromatogr A 1244:1–13PubMedGoogle Scholar
  114. 114.
    Goja AM, Yang H, Cul M, Li C (2013) Aqueous two-phase extraction advances for bioseparation. J. Bioprocess Biotech 4:1–8Google Scholar
  115. 115.
    Raja S, Murty V, Thivaharan R, Rajasekar V, Ramesh V (2011) Aqueous two phase systems for the recovery of biomolecules—a review. Sci Technol 1:7–16Google Scholar
  116. 116.
    Molino JVD, Marques DAV, Junior AP, Mazzola PG, Gatti MSV (2013) Different types of aqueous two-phase systems for biomolecule and bioparticle extraction and purification. Biotechnol Progr 29:1343–1353Google Scholar
  117. 117.
    Mourao T, Tome LC, Florindo C, Rebelo LPN, Marrucho IM (2014) Understanding the role of cholinium carboxylate ionic liquids in PEG-based aqueous biphasic systems. ACS Sustainable Chem Eng 2:2426–2434Google Scholar
  118. 118.
    Quental MV, Caban M, Pereira MM, Stepnowski P, et al. (2015) Enhanced extraction of proteins using cholinium-based ionic liquids as phase-forming components of aqueous biphasic systems. Biotechnol J 10:1–10Google Scholar
  119. 119.
    Berthod A, Ruiz-Ángel MJ, Carda-Broch S (2008) Ionic liquids in separation techniques. J Chromatogr A 1184:6–18PubMedGoogle Scholar
  120. 120.
    Vidal L, Riekkola M-L, Canals A (2012) Ionic liquid-modified materials for solid-phase extraction and separation: a review. Anal Chim Acta 715:19–41PubMedGoogle Scholar
  121. 121.
    Desai RK, Streefland M, Wijffels RH, Eppink MHM (2016) Novel astaxanthin extraction from Haematococcus pluvialis using cell permeabilising ionic liquids. Green Chem 18:1261–1267Google Scholar
  122. 122.
    Dreyer S, Kragl U (2008) Ionic liquids for aqueous two-phase extraction and stabilization of enzymes. Biotechnol Bioeng 99:1416–1424PubMedGoogle Scholar
  123. 123.
    Desai RK, Streefland M, Wijffels RH, Eppink MHM (2014) Extraction and stability of selected proteins in ionic liquid based aqueous two phase systems. Green Chem 16:2670–2679Google Scholar
  124. 124.
    Richard BR, Deutscher MP (2009) Methods in enzymology, vol 463: Guide to protein purification. Elsevier. ISBN: 978-0-12-374536-1. http://store.elsevier.com/Guide-to-Protein-Purification/isbn-9780123745361/
  125. 125.
    Carta G, Jungbauer A (2010) Protein chromatography and scale-up. Wiley-VCH Verlag GmbH & Co KGaA. Weinheim. ISBN: 978-3-527-31819-3Google Scholar
  126. 126.
    Cavonius LR, Albert E, Undeland I (2015) pH-shift processing of Nannochloropsis oculata microalgal biomass to obtain a protein-enriched food or feed ingredients. Algal Res 11:95–102Google Scholar
  127. 127.
    Schwenzfeier A, Wierenga PA, Gruppen H (2011) Isolation and characterization of soluble protein from the green microalgae Tetraselmis sp. Bioresour Technol 102:9121–9127PubMedGoogle Scholar
  128. 128.
    Van Reis R, Zydney AL (2001) Membrane separations in biotechnology. Curr Opin Biotechnol 12:208–211PubMedGoogle Scholar
  129. 129.
    Schwenzfeier A, Wierenga PA, Eppink MHM, Gruppen HA (2014) Effect of charged polysaccharides on the techno-functional properties of fractions obtained from algae soluble protein isolate. Food Hydrocolloids 35:9–18Google Scholar
  130. 130.
    Urzu AV, Marcati A, Sayd T, Sante-Lhoutellier V, et al. (2014) Extraction, fractionation and functional properties of proteins from the microalgae Chlorella Vulgaris. Bioresour Technol 157:134–139Google Scholar
  131. 131.
    Demmer W, Fischer-Fruehholz S, Kocourek A, Nusbaumer D, Wuenn E (2005) Adsorption membrane comprising microporous polymer membrane with adsorbent particles embedded in pores, useful in analysis, for purification or concentration. Patent DE10344820 A1Google Scholar
  132. 132.
    Weaver J, Husson MS, Murphy L, Wickramasinghe SR (2013) Anion exchange membrane absorbers for flow-through polishing steps: part II. Virus, host cell protein, DNA clearance and antibody recovery. Biotechnol. Bioeng 110:500–510PubMedGoogle Scholar
  133. 133.
    Schwenzfeier A, Lech FJ, Wierenga PA, Eppink MHM, Gruppen HA (2013) Foam properties of algae soluble protein isolate: effect of pH and ionic strength. Food Hydrocolloids 33(1):111–117Google Scholar
  134. 134.
    Conde E, Balboa EM, Parada M, Falque E (2013) Algal proteins, peptides and amino acids. Funct Ingredients Algae Foods Nutraceuticals:135. doi: 10.1533/9780857098689.1.135 Google Scholar
  135. 135.
    Bermejo R, Felipe MA, Talavera EM, Alvarez-Pez JM (2006) Expanded bed absorption chromatography for recovery of Phycocyanins from the microalgae Spirulina platentis. Chromatographia 63:59–66Google Scholar
  136. 136.
    Schwenzfeier A, Helbig A, Wierenga PA, Eppink MHM, Gruppen HA (2013) Emulsion properties of algae soluble protein isolate from Tetraselmis sp. Food Hydrocolloids 30:258–263Google Scholar
  137. 137.
    Gilbert-Lopez B, Mendiola JA, Fontecha J, van den Broek LAM, et al. (2015) Downstream processing of Isochrysis galbana: a step towards microalgal biorefinery. Green Chem 17:4599–4609Google Scholar
  138. 138.
    Kumar RR, Rao PH, Arumugam M (2015) Lipid extraction methods for microalgae: a comprehensive review. Front Energy Res 2:1–9Google Scholar
  139. 139.
    Taher H, Al-Zuhair S, Al-Marzouqi AH, Haik Y, Farid M (2014) Effective extraction of microalgae lipids from wet biomass for biodiesel production. Biomass Bioenergy 66:159–167Google Scholar
  140. 140.
    Kim K, Shin H, Moon M, Ryu B-G, et al. (2015) Evaluation of various harvesting methods for high-density microalgae Aurantiochytrium sp. Bioresour Technol 198:828–835PubMedGoogle Scholar
  141. 141.
    Halim R, Webley PA, Martin GJO (2016) The CIDES process: fractionation of concentrated microalgal paste for co-production of biofuel, nutraceuticals, and high-grade protein feed. Algal Res 19:299. doi: 10.1016/j/algal.2015.09.018 CrossRefGoogle Scholar
  142. 142.
    Gendy TS, El-Temtamy SA (2013) Commercialization potential of microalgae for biofuel production: an overview. Egypt J Pet 22:43–51Google Scholar
  143. 143.
    Dominguez H (2013) Functional ingredients from algae for foods and nutraceuticals, Food science, technology and nutrition. Woodhead Publishing Limited, (Oxford). ISBN:978-0-85709-512-1Google Scholar
  144. 144.
    Buono S, Langellotti AL, Martello A, Rinna F, Fogliano V (2014) Functional ingredients from microalgae. Food Funct 5:1669–1685PubMedGoogle Scholar
  145. 145.
    Martin AH, Nieuwland M, de Jong GAH (2014) Characterization of heat-set gels from RuBisCO in comparison to those from other proteins. JAFC 62:10783–10791Google Scholar
  146. 146.
    Chen C-Y, Zhao X-Q, Yen H-W, Ho SH, et al. (2013) Microalgae-based carbohydrates for biofuel production. Biochem Eng J 78:1–10Google Scholar
  147. 147.
    De Jesus Raposo MF, Morais RMSC, Morais AMMB (2013) Bioactivity and applications of sulphated polysaccharides from marine microalgae. Mar Drugs 11:233–252Google Scholar
  148. 148.
    Misurcova L, Skrovankova S, Samek D, Ambrozova J, Machu L (2012) Health benefits of algal polysaccharides in human nutrition. Adv Food Nutr Res 66:75–145Google Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  • Michel H. M. Eppink
    • 1
  • Giuseppe Olivieri
    • 1
  • Hans Reith
    • 1
  • Corjan van den Berg
    • 1
  • Maria J. Barbosa
    • 1
  • Rene H. Wijffels
    • 1
    • 2
  1. 1.Bioprocess Engineering, AlgaePARCWageningen UniversityWageningenThe Netherlands
  2. 2.University of NordlandBodøNorway

Personalised recommendations