A sustainable perspective of microalgal biorefinery for co-production and recovery of high-value carotenoid and biofuel with CO2 valorization
Ramalingam Dineshkumar
Applied Phycology and Biotechnology Division, CSIR–Central Salt and Marine Chemicals Research Institute, Bhavnagar, India
Search for more papers by this authorCorresponding Author
Ramkrishna Sen
Department of Biotechnology, Indian Institute of Technology Kharagpur, Kharagpur, India
Correspondence to: Ramkrishna Sen, Department of Biotechnology, Indian Institute of Technology Kharagpur, West Bengal 721 302, India.
E-mail: rksen@yahoo.com; rksen@bt.iitkgp.ac.in
Search for more papers by this authorRamalingam Dineshkumar
Applied Phycology and Biotechnology Division, CSIR–Central Salt and Marine Chemicals Research Institute, Bhavnagar, India
Search for more papers by this authorCorresponding Author
Ramkrishna Sen
Department of Biotechnology, Indian Institute of Technology Kharagpur, Kharagpur, India
Correspondence to: Ramkrishna Sen, Department of Biotechnology, Indian Institute of Technology Kharagpur, West Bengal 721 302, India.
E-mail: rksen@yahoo.com; rksen@bt.iitkgp.ac.in
Search for more papers by this authorAbstract
Process biotechnology can play a very important role in addressing contemporary global challenges in the areas of energy, the environment, and healthcare. This review discusses the development of a biorefinery model using sustainable feedstocks such as microalgal biomass, with multiple benefits. As a case study, it demonstrates the development of a microalgal biorefinery to produce lipid for biofuel and carotenoids like lutein for healthcare applications, along with CO2 mitigation. However, there has been a question mark regarding the economic viability of microalgal biorefinery, mainly for low biomass and product yields and discrete downstream processing steps. To provide sustainable solutions for these technological challenges, process intensification strategies can be implemented to enhance the yields of biomass-derived biofuels and value-added products. This article investigates the design aspects of photo-bioreactors to enhance biomass productivity and CO2 sequestration. Despite efforts made by researchers to improve product yields, there is ample scope to improve the economic viability of lutein and lipid production by integrating upstream and downstream operations to reduce the cost associated with the process. The future of algal biorefineries will rely on the development of rationally integrated genome and process-scale engineering strategies to improve further the production of lipid and carotenoids. This review critically analyzes the current state of the art and presents the future prospects for microalgal biorefinery to address some of the challenges in the areas of healthcare, energy, and the environment. © 2020 Society of Chemical Industry and John Wiley & Sons, Ltd
References
- 1 Central Electricity Authority. Operation performance of generating stations in the country during the year 2010-11-an overview. pp. 1–45 (2012).
- 2 International Energy Agency Statistics (IEA). CO2 Emissions from Fuel Combustion: Highlights. pp. 1–139 (2015).
- 3 Inter-governmental Panel on Climate Change (IPCC). Climate Change: Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (2007).
- 4 Sevigné Itoiz E, Fuentes-Grünewald C, Gasol CM, Garcés E, Alacid E, Rossi S et al., Energy balance and environmental impact analysis of marine microalgal biomass production for biodiesel generation in a photobioreactor pilot plant. Biomass Bioenergy 39: 324–335 (2012).
- 5 McMichael AJ and Woodruff RE, Climate Change and Human Health, ed. by, Oliver JE, Encyclopedia of World Climatology. Encyclopedia of Earth Sciences Series, Springer, Dordrecht, (2005).
- 6 Remoundou K and Koundouri P, Environmental Effects on Public Health: An Economic Perspective. Int J Environ Res Public Health 6: 2160–2178 (2009).
- 7 Kamm B and Kamm M, Principles of biorefineries. Appl Microbiol Biotechnol 64: 137–145 (2004).
- 8 Cherubini F, Jungmeier G, Wellisch M, Willke T, Skiadas I, Van Ree R et al., Toward a common classification approach for biorefinery systems. Biofuels Bioprod Biorefin 3: 534–546 (2009).
- 9 Pires JCM, Alvim-Ferraz MCM, Martins FG and Simoes M, Carbon dioxide capture from flue gases using microalgae: Engineering aspects and biorefinery concept. Renew Sustain Energy Rev 16: 3043–3053 (2012).
- 10 Yen HW, Ho SH, Chen CY and Chang JS, CO2, NOx and SOx removal from flue gas via microalgae cultivation: A critical review. Biotechnol J 10: 829–839 (2015).
- 11 Hognon C, Delrue F, Texier J, Grateau M, Thiery S, Miller H et al., Comparison of pyrolysis and hydrothermal liquefaction of Chlamyclomonas reinharcltii growth studies on the recovered hydrothermal aqueous phase. Biomass Bioenerg 73: 23–31 (2015).
- 12 Elliott DC, Biller P, Ross AB, Schmidt AJ and Jones SB, Hydrothermal liquefaction of biomass: Developments from batch to continuous process. Bioresour Technol 178: 147–156 (2015).
- 13 Barreiro DL, Prins W, Ronsse F and Brilman W, Hydrothermal liquefaction (HTL) of microalgae for biofuel production: State of the art review and future prospects. Biomass Bioenergy 53: 113–127 (2013).
- 14 Brennan L and Owende P, Biofuels from microalgae-A review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sustain Energy Rev 14: 557–577 (2010).
- 15 Courchesne NMD, Parisien A, Wang B and Lan CQ, Enhancement of lipid production using biochemical, genetic and transcription factor engineering approaches. J Biotechnol 141: 31–41 (2009).
- 16 Lam MK and Lee KT, Microalgae biofuels: A critical review of issues, problems and the way forward. Biotechnol Adv 30: 673–690 (2012).
- 17 Razzak SA, Hossain MM, Lucky RA, Bassi AS and de Lasa H, Integrated CO2 capture, wastewater treatment and biofuel production by microalgae culturing-A review. Renew Sustain Energy Rev 27: 622–653 (2013).
- 18 Olguin EJ, Dual purpose microalgae-bacteria-based systems that treat wastewater and produce biodiesel and chemical products within a Biorefinery. Biotechnol Adv 30: 1031–1046 (2012).
- 19 Chisti Y, Biodiesel from microalgae. Biotechnol Adv 25: 294–306 (2007).
- 20 Markou G and Nerantzis E, Microalgae for high-value compounds and biofuels production: a review with focus on cultivation under stress conditions. Biotechnol Adv 31: 1532–1542 (2013).
- 21 Fernández-Sevilla JM, Acién Fernández FG and Molina GE, Biotechnological production of lutein and its applications. Appl Microbiol Biotechnol 86: 27–40 (2010).
- 22 Pulz O and Gross W, Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65: 635–648 (2004).
- 23 Borowitzka MA, High-value products from microalgae-their development and commercialisation. J Appl Phycol 25: 743–756 (2013).
- 24 Spolaore P, Joannis-Cassan C, Duran E and Isambert A, Commercial applications of microalgae. J Biosci Bioeng 101: 87–96 (2006).
- 25 Grima EM, Belarbi EH, Fernandez FGA, Medina AR and Chisti Y, Recovery of microalgal biomass and metabolites: process options and economics. Biotechnol Adv 20: 491–515 (2003).
- 26 Mata TM, Martins AA and Caetano NS, Microalgae for biodiesel production and other applications: A review. Renew Sustain Energy Rev 14: 217–232 (2010).
- 27 De Philippis R, Sili C, Paperi R and Vincenzini M, Exopolysaccharide-producing cyanobacteria and their possible exploitation: A review. J Appl Phycol 13: 293–299 (2001).
- 28 Becker EW, Micro-algae as a source of protein. Biotechnol Adv 25: 207–210 (2007).
- 29
Araya B, Gouveia L, Nobre B, Reis A, Chamy R and Poirrier P, Evaluation of the simultaneous production of lutein and lipids using a vertical alveolar panel bioreactor for three Chlorella species. Algal Res 6: 218–222 (2014).
10.1016/j.algal.2014.06.003 Google Scholar
- 30 Minhas AK, Hodgson P, Barrow CJ, Sashidhar B and Adholeya A, The isolation and identification of new microalgal strains producing oil and carotenoid simultaneously with biofuel potential. Bioresour Technol 211: 556–565 (2016).
- 31 Xie Y, Ho SH, Chen CN, Chen CY, Ng IS, Jing KJ et al., Phototrophic cultivation of a thermo-tolerant Desmodesmus sp. for lutein production: effects of nitrate concentration, light intensity and fed-batch operation. Bioresour Technol 144: 435–444 (2013).
- 32 Ho SH, Chan MC, Liu CC, Chen CY, Lee WL, Lee DJ et al., Enhancing lutein productivity of an indigenous microalga Scenedesmus obliquus FSP-3 using light-related strategies. Bioresour Technol 152: 275–282 (2014).
- 33 Mujtaba G, Choi W, Lee CG and Lee K, Lipid production by Chlorella vulgaris after a shift from nutrient-rich to nitrogen starvation conditions. Bioresour Technol 123: 279–283 (2012).
- 34 Huang Y, Cheng J, Lu HX, Huang R, Zhou JH and Cen KF, Simultaneous enhancement of microalgae biomass growth and lipid accumulation under continuous aeration with 15% CO2. RSC Adv 5: 50851–50858 (2015).
- 35 Ho SH, Chen CY, Lee DJ and Chang JS, Perspectives on microalgal CO2-emission mitigation systems - A review. Biotechnol Adv 29: 189–198 (2011).
- 36 Zhao B and Su Y, Process effect of microalgal-carbon dioxide fixation and biomass production: A review. Renew Sustain Energy Rev 31: 121–132 (2014).
- 37 Becker EW, Microalgae: Biotechnology and Microbiology. Cambridge University Press, Cambridge, ISBN 0-521-35020-4 (1994).
- 38 Polle JE, Neofotis P, Huang A, Chang W, Sury K and Wiech EM, Carbon partitioning in green algae (Chlorophyta) and the enolase enzyme. Metabolites 4: 612–628 (2014).
- 39 Chakraborty N, Mukheriee I, Santra AK, Chowdhury S, Chakraborty S, Bhattacharya S et al., Measurement of CO2, CO, SO2, and NO emissions from coal-based thermal power plants in India. Atmos Environ 42: 1073–1082 (2008).
- 40 Van den Hende S, Vervaeren H and Boon N, Flue gas compounds and microalgae: (Bio-)chemical interactions leading to biotechnological opportunities. Biotechnol Adv 30: 1405–1424 (2012).
- 41 Cheah WY, Show PL, Chang JS, Ling TC and Juan JC, Biosequestration of atmospheric CO2 and flue gas-containing CO2 by microalgae. Bioresour Technol 184: 190–201 (2015).
- 42 Kumar A, Ergas S, Yuan X, Sahu A, Zhang QO, Dewulf J et al., Enhanced CO2 fixation and biofuel production via microalgae: recent developments and future directions. Trends Biotechnol 28: 371–380 (2010).
- 43 Matsumoto H, Hamasaki A, Sioji N and Ikuta Y, Influence of CO2, SO2 and NO in flue gas on microalgae productivity. J Chem Eng Jpn 30: 620–624 (1997).
- 44 Ryu HJ, Oh KK and Kim YS, Optimization of the influential factors for the improvement of CO2 utilization efficiency and CO2 mass transfer rate. J Ind Eng Chem 15: 471–475 (2009).
- 45 Sydney EB, Sturm W, de Carvalho JC, Thomaz-Soccol V, Larroche C, Pandey A et al., Potential carbon dioxide fixation by industrially important microalgae. Bioresour Technol 101: 5892–5896 (2010).
- 46 Borkenstein CG, Knoblechner J, Frühwirth H and Schagerl M, Cultivation of Chlorella emersonii with flue gas derived from a cement plant. J Appl Phycol 23: 131–135 (2011).
- 47 Jiang Y, Zhang W, Wang J, Chen Y, Shen S and Liu T, Utilization of simulated flue gas for cultivation of Scenedesmus dimorphus. Bioresour Technol 128: 359–364 (2013).
- 48 Kumar K, Banerjee D and Das D, Carbon dioxide sequestration from industrial flue gas by Chlorella sorokiniana. Bioresour Technol 152: 225–233 (2014).
- 49
De Bhowmick G, Subramanian G, Mishra S and Sen R, Raceway pond cultivation of a marine microalga of Indian origin for biomass and lipid production: A case study. Algal Res 6: 201–209 (2014).
10.1016/j.algal.2014.07.005 Google Scholar
- 50 Kao C-Y, Chen T-Y, Chang Y-B, Chiu T-W, Lin H-Y, Chen C-D et al., Utilization of carbon dioxide in industrial flue gases for the cultivation of microalga Chlorella sp. Bioresour Technol 166: 485–493 (2014).
- 51 Subramanian G, Dineshkumar R and Sen R, Modelling of oxygen-evolving-complex ionization dynamics for energy-efficient production of microalgal biomass, pigment and lipid with carbon capture: an engineering vision for a biorefinery. RSC Adv 6: 51941–51956 (2016).
- 52 Nayak M, Karemore A and Sen R, Sustainable valorization of flue gas CO2 and wastewater for the production of microalgal biomass as a biofuel feedstock in closed and open reactor systems. RSC Adv 6: 91111–91120 (2016).
- 53 Christenson L and Sims R, Production and harvesting of microalgae for wastewater treatment, biofuels, and bioproducts. Biotechnol Adv 29: 686–702 (2011).
- 54 Chaumont D, Biotechnology of algal biomass production – A review of systems for outdoor mass-culture. J Appl Phycol 5: 593–604 (1993).
- 55 Lee YK, Microalgal mass culture systems and methods: Their limitation and potential. J Appl Phycol 13: 307–315 (2001).
- 56 Pulz O, Photobioreactors: production systems for phototrophic microorganisms. Appl Microbiol Biotechnol 57: 287–293 (2001).
- 57 Wang B, Lan CQ and Horsman M, Closed photobioreactors for production of microalgal biomasses. Biotechnol Adv 30: 904–912 (2012).
- 58 Ugwu CU, Aoyagi H and Uchiyama H, Photobioreactors for mass cultivation of algae. Bioresour Technol 99: 4021–4028 (2008).
- 59 Molina E, Fernández J, Acién FG and Chisti Y, Tubular photobioreactor design for algal cultures. J Biotechnol 92: 113–131 (2001).
- 60 Singh RN and Sharma S, Development of suitable photobioreactor for algae production – A review. Renew Sustain Energy Rev 16: 2347–2353 (2012).
- 61 Suh IS and Lee SB, A light distribution model for an internally radiating photobioreactor. Biotechnol Bioeng 82: 180–189 (2003).
- 62 Barbosa MJ, Janssen M, Ham N, Tramper J and Wijffels RH, Microalgae cultivation in air-lift reactors: Modeling biomass yield and growth rate as a function of mixing frequency. Biotechnol Bioeng 82: 170–179 (2003).
- 63 Kumar K, Dasgupta CN, Nayak B, Lindblad P and Das D, Development of suitable photobioreactors for CO2 sequestration addressing global warming using green algae and cyanobacteria. Bioresour Technol 102: 4945–4953 (2011).
- 64 Hu Q, Kurano N, Kawachi M, Iwasaki I and Miyachi S, Ultrahigh-cell-density culture of a marine green alga Chlorococcum littorale in a flat-plate photobioreactor. Appl Microbiol Biotechnol 49: 655–662 (1998).
- 65 Cuaresma M, Janssen M, Vílchez C and Wijffels RH, Productivity of Chlorella sorokiniana in a short light-path (SLP) panel photobioreactor under high irradiance. Biotechnol Bioeng 104: 352–359 (2009).
- 66 Jacobi A, Bucharsky EC, Schell KG, Habisreuther P, Oberacker R, Hoffmann MJ et al., The application of transparent glass sponge for improvement of light distribution in photobioreactors. J Bioprocess Biotechniq 2: 113 (2012).
- 67 Benson BC, Gutierrez-Wing MT and Rusch KA, Optimization of the lighting system for a Hydraulically Integrated Serial Turbidostat Algal Reactor (HISTAR): Economic implications. Aquacult Eng 40: 45–53 (2009).
- 68 Grobbelaar JU and Kurano N, Use of photoacclimation in the design of a novel photobioreactor to achieve high yields in algal mass cultivation. J Appl Phycol 15: 121–126 (2003).
- 69 Bergmann P, Ripplinger P, Beyer L and Trösch W, Disposable Flat Panel Airlift Photobioreactors. Chemie Ingenieur Technik 85: 202–205 (2013).
- 70 Kliphuis AMJ, de Winter L, Vejrazka C, Martens DE, Janssen M and Wijffels RH, Photosynthetic efficiency of Chlorella sorokiniana in a turbulently mixed short light-path photobioreactor. Biotechnol Prog 26: 687–696 (2010).
- 71 Olivieri G, Salatino P and Marzocchella A, Advances in photobioreactors for intensive microalgal production: configurations, operating strategies and applications. J Chem Technol Biotechnol 89: 178–195 (2014).
- 72 Chen C-Y, Saratale GD, Lee C-M, Chen P-C and Chang J-S, Phototrophic hydrogen production in photobioreactors coupled with solar-energy-excited optical fibers. Int J Hydrogen Energy 33: 6886–6895 (2008).
- 73 Chen C-Y, Yeh K-L, Aisyah R, Lee D-J and Chang J-S, Cultivation, photobioreactor design and harvesting of microalgae for biodiesel production: a critical review. Bioresour Technol 102: 71–81 (2011).
- 74 Cheng J, Yang Z, Huang Y, Huang L, Hu L, Xu D et al., Improving growth rate of microalgae in a 1191 m2 raceway pond to fix CO2 from flue gas in a coal-fired power plant. Bioresour Technol 190: 235–241 (2015).
- 75 de Morais MG and JAV C, Biofixation of carbon dioxide by Spirulina sp and Scenedesmus obliquus cultivated in a three-stage serial tubular photobioreactor. J Biotechnol 129: 439–445 (2007).
- 76 Fan L-H, Zhang Y-T, Zhang L and Chen H-L, Evaluation of a membrane-sparged helical tubular photobioreactor for carbon dioxide biofixation by Chlorella vulgaris. J Membrane Sci 325: 336–345 (2008).
- 77 Del Campo JA, Garcia-Gonzalez M and Guerrero MG, Outdoor cultivation of microalgae for carotenoid production: current state and perspectives. Appl Microbiol Biotechnol 74: 1163–1174 (2007).
- 78 Ribaya-Mercado JD and Blumberg JB, Lutein and zeaxanthin and their potential roles in disease prevention. J Am Coll Nutr 23: 567S–587S (2004).
- 79 Xie Y-P, Ho S-H, Chen C-Y, Chen C-NN, Liu C-C, Ng IS et al., Simultaneous enhancement of CO2 fixation and lutein production with thermo-tolerant Desmodesmus sp. F51 using a repeated fed-batch cultivation strategy. Biochem Eng J 86: 33–40 (2014).
- 80 Lin JH, Lee DJ and Chang JS, Lutein production from biomass: marigold flowers versus microalgae. Bioresour Technol 184: 421–428 (2015).
- 81 Cha KH, Koo SY and Lee D-U, Antiproliferative Effects of Carotenoids Extracted from Chlorella ellipsoidea and Chlorella vulgaris on Human Colon Cancer Cells. J Agric Food Chem 56: 10521–10526 (2008).
- 82 Park JS, Chew BP and Wong TS, Dietary lutein from marigold extract inhibits mammary tumor development in BALB/c mice. J Nutr 128: 1650–1656 (1998).
- 83 Lari Z, Moradi-kheibari N, Ahmadzadeh H, Abrishamchi P, Moheimani NR and Murry MA, Bioprocess engineering of microalgae to optimize lipid production through nutrient management. J Appl Phycol 28: 3235–3250 (2016).
- 84 Heydarizadeh P, Poirier I, Loizeau D, Ulmann L, Mimouni V, Schoefs B et al., Plastids of marine phytoplankton produce bioactive pigments and lipids. Mar Drugs 11: 3425–3471 (2013).
- 85 Casal Bejarano C, Cuaresma Franco M, Vílchez Lobato C and Vega Piqueres JM, Enhanced productivity of a lutein-enriched novel acidophile microalgae grown on urea. Mar Drugs 9(1): 29–42 (2011).
- 86 Cordero BF, Obraztsova I, Couso I, Leon R, Vargas MA and Rodriguez H, Enhancement of lutein production in Chlorella sorokiniana (Chorophyta) by improvement of culture conditions and random mutagenesis. Mar Drugs 9: 1607–1624 (2011).
- 87 Vaquero I, Ruiz-Domínguez MC, Márquez M and Vílchez C, Cu-mediated biomass productivity enhancement and lutein enrichment of the novel microalga Coccomyxa onubensis. Process Biochem 47: 694–700 (2012).
- 88 Fu W, Paglia G, Magnúsdóttir M, Steinarsdóttir EA, Gudmundsson S, Palsson BØ et al., Effects of abiotic stressors on lutein production in the green microalga Dunaliella salina. Microb Cell Fact 13: 1–9 (2014).
- 89 Ho S-H, Chen C-Y and Chang J-S, Effect of light intensity and nitrogen starvation on CO2 fixation and lipid/carbohydrate production of an indigenous microalga Scenedesmus obliquus CNW-N. Bioresour Technol 113: 244–252 (2012).
- 90 Ruangsomboon S, Effect of light, nutrient, cultivation time and salinity on lipid production of newly isolated strain of the green microalga, Botryococcus braunii KMITL 2. Bioresour Technol 109: 261–265 (2012).
- 91 Yeh K-L and Chang J-S, Effects of cultivation conditions and media composition on cell growth and lipid productivity of indigenous microalga Chlorella vulgaris ESP-31. Bioresour Technol 105: 120–127 (2012).
- 92 Chen C-Y, Chang J-S, Chang H-Y, Chen T-Y, Wu J-H and Lee W-L, Enhancing microalgal oil/lipid production from Chlorella sorokiniana CY1 using deep-sea water supplemented cultivation medium. Biochem Eng J 77: 74–81 (2013).
- 93 Nakanishi A, Aikawa S, Ho S-H, Chen C-Y, Chang J-S, Hasunuma T et al., Development of lipid productivities under different CO2 conditions of marine microalgae Chlamydomonas sp. JSC4. Bioresour Technol 152: 247–252 (2014).
- 94 Converti A, Casazza AA, Ortiz EY, Perego P and Del Borghi M, Effect of temperature and nitrogen concentration on the growth and lipid content of Nannochloropsis oculata and Chlorella vulgaris for biodiesel production. Chem Eng Process 48: 1146–1151 (2009).
- 95 Del Campo JA, Moreno J, Rodriguez H, Vargas MA, Rivas J and Guerrero MG, Carotenoid content of chlorophycean microalgae: factors determining lutein accumulation in Muriellopsis sp (Chlorophyta). J Biotechnol 76: 51–59 (2000).
- 96 Liu J, Yuan C, Hu G and Li F, Effects of Light Intensity on the Growth and Lipid Accumulation of Microalga Scenedesmus sp. 11-1 Under Nitrogen Limitation. Appl Biochem Biotechnol 166: 2127–2137 (2012).
- 97 Desai KM, Survase SA, Saudagar PS, Lele SS and Singhal RS, Comparison of artificial neural network (ANN) and response surface methodology (RSM) in fermentation media optimization: Case study of fermentative production of scleroglucan. Biochem Eng J 41: 266–273 (2008).
- 98 Huang J, Mei LH and Xia J, Application of artificial neural network coupling particle swarm optimization algorithm to biocatalytic production of GABA. Biotechnol Bioeng 96: 924–931 (2007).
- 99 Dhanarajan G, Mandal M and Sen R, A combined artificial neural network modeling–particle swarm optimization strategy for improved production of marine bacterial lipopeptide from food waste. Biochem Eng J 84: 59–65 (2014).
- 100
Dineshkumar R, Dhanarajan G, Dash SK and Sen R, An advanced hybrid medium optimization strategy for the enhanced productivity of lutein in Chlorella minutissima. Algal Res 7: 24–32 (2015).
10.1016/j.algal.2014.11.010 Google Scholar
- 101 Dineshkumar R, Dash SK and Sen R, Process integration for microalgal lutein and biodiesel production with concomitant flue gas CO2 sequestration: a biorefinery model for healthcare, energy and environment. RSC Adv 5: 73381–73394 (2015).
- 102 Sánchez J, Fernández J, Acién F, Rueda A, Pérez-Parra J and Molina E, Influence of culture conditions on the productivity and lutein content of the new strain Scenedesmus almeriensis. Process Biochem 43: 398–405 (2008).
- 103 Ho S-H, Xie Y, Chan M-C, Liu C-C, Chen C-Y, Lee D-J et al., Effects of nitrogen source availability and bioreactor operating strategies on lutein production with Scenedesmus obliquus FSP-3. Bioresour Technol 184: 131–138 (2015).
- 104 Dineshkumar R, Subramanian G, Dash SK and Sen R, Development of an optimal light-feeding strategy coupled with semi-continuous reactor operation for simultaneous improvement of microalgal photosynthetic efficiency, lutein production and CO2 sequestration. Biochem Eng J 113: 47–56 (2016).
- 105 Rodolfi L, Chini Zittelli G, Bassi N, Padovani G, Biondi N, Bonini G et al., Microalgae for oil: Strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol Bioeng 102: 100–112 (2009).
- 106 Hsieh C-H and Wu W-T, Cultivation of microalgae for oil production with a cultivation strategy of urea limitation. Bioresour Technol 100: 3921–3926 (2009).
- 107 Su C-H, Chien L-J, Gomes J, Lin Y-S, Yu Y-K, Liou J-S et al., Factors affecting lipid accumulation by Nannochloropsis oculata in a two-stage cultivation process. J Appl Phycol 23: 903–908 (2011).
- 108 Praveenkumar R, Shameera K, Mahalakshmi G, Akbarsha MA and Thajuddin N, Influence of nutrient deprivations on lipid accumulation in a dominant indigenous microalga Chlorella sp., BUM11008: Evaluation for biodiesel production. Biomass Bioenerg 37: 60–66 (2012).
- 109 Ho S-H, Chen C-NN, Lai Y-Y, Lu W-B and Chang J-S, Exploring the high lipid production potential of a thermotolerant microalga using statistical optimization and semi-continuous cultivation. Bioresour Technol 163: 128–135 (2014).
- 110 Martin GJ, Energy requirements for wet solvent extraction of lipids from microalgal biomass. Bioresour Technol 205: 40–47 (2016).
- 111
Yap BH, Martin GJ and Scales PJ, Rheological manipulation of flocculated algal slurries to achieve high solids processing. Algal Res 14: 1–8 (2016).
10.1016/j.algal.2015.12.007 Google Scholar
- 112 Lee NJG, Seo JY, Shim TS, Kim B, Praveenkumar R et al., Magnetic-Nanoflocculant-Assisted Water-Nonpolar Solvent Interface Sieve for Microalgae Harvesting. ACS Appl Mater Interfaces 7: 18336–18343 (2015).
- 113 Kim J, Yoo G, Lee H, Lim J, Kim K, Kim CW et al., Methods of downstream processing for the production of biodiesel from microalgae. Biotechnol Adv 31: 862–876 (2013).
- 114 Pragya N, Pandey KK and Sahoo PK, A review on harvesting, oil extraction and biofuels production technologies from microalgae. Renew Sustain Energy Rev 24: 159–171 (2013).
- 115 Rashid N, Rehman SU and Han J-I, Rapid harvesting of freshwater microalgae using chitosan. Process Biochem 48: 1107–1110 (2013).
- 116 Farid MS, Shariati A, Badakhshan A and Anvaripour B, Using nano-chitosan for harvesting microalga Nannochloropsis sp. Bioresour Technol 131: 555–559 (2013).
- 117 Vandamme D, Foubert I, Meesschaert B and Muylaert K, Flocculation of microalgae using cationic starch. J Appl Phycol 22: 525–530 (2010).
- 118 Wang SK, Stiles AR, Guo C and Liu CZ, Harvesting microalgae by magnetic separation: A review. Algal Res 9: 178–185 (2015).
- 119 Toh PY, Ng BW, Chong CH, Ahmad AL, Yang J-W, Chieh Derek CJ et al., Magnetophoretic separation of microalgae: the role of nanoparticles and polymer binder in harvesting biofuel. RSC Adv 4: 4114–4121 (2014).
- 120 Lee K, Lee SY, Na JG, Jeon SG, Praveenkumar R, Kim DM et al., Magnetophoretic harvesting of oleaginous Chlorella sp by using biocompatible chitosan/magnetic nanoparticle composites. Bioresour Technol 149: 575–578 (2013).
- 121 Ge S, Agbakpe M, Zhang W, Kuang L, Wu Z and Wang X, Recovering Magnetic Fe3O4–ZnO Nanocomposites from Algal Biomass Based on Hydrophobicity Shift under UV Irradiation. ACS Appl Mater Interfaces 7: 11677–11682 (2015).
- 122 Wang SK, Wang F, Hu YR, Stiles AR, Guo C and Liu CZ, Magnetic Flocculant for High Efficiency Harvesting of Microalgal Cells. ACS Appl Mater Interfaces 6: 109–115 (2014).
- 123 Lee AK, Lewis DM and Ashman PJ, Disruption of microalgal cells for the extraction of lipids for biofuels: Processes and specific energy requirements. Biomass Bioenergy 46: 89–101 (2012).
- 124 Braun E and Aach HG, Enzymatic degradation of the cell wall of Chlorella. Planta 126: 181–185 (1975).
- 125 Fu C-C, Hung T-C, Chen J-Y, Su C-H and Wu W-T, Hydrolysis of microalgae cell walls for production of reducing sugar and lipid extraction. Bioresour Technol 101: 8750–8754 (2010).
- 126 Lee YC, Lee HU, Lee K, Kim B, Lee SY, Choi MH et al., Aminoclay-conjugated TiO2 synthesis for simultaneous harvesting and wet-disruption of oleaginous Chlorella sp. Chem Eng J 245: 143–149 (2014).
- 127 Huang WC and Kim JD, Cationic surfactant-based method for simultaneous harvesting and cell disruption of a microalgal biomass. Bioresour Technol 149: 579–581 (2013).
- 128 Seo JY, Praveenkumar R, Kim B, Seo J-C, Park J-Y, Na J-G et al., Downstream integration of microalgae harvesting and cell disruption by means of cationic surfactant-decorated Fe3O4 nanoparticles. Green Chem 18(14): 3981–3989 (2016).
- 129 Dineshkumar R, Paul A, Gangopadhyay M, Singh NP and Sen R, Smart and reusable biopolymer nanocomposite for simultaneous microalgal biomass harvesting and disruption: Integrated downstream processing for a sustainable biorefinery. ACS Sust Chem Eng 5: 852–861 (2016).
- 130 Bligh EG and Dyer WJ, A rapid method of total lipid extraction and purification. Can J Biochem Phys 37: 911–917 (1959).
- 131 Folch J, Lees M and Sloane-Stanley G, A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226: 497–509 (1957).
- 132 Bai M-D, Cheng C-H, Wan H-M and Lin Y-H, Microalgal pigments potential as byproducts in lipid production. J Taiwan Inst Chem Eng 42: 783–786 (2011).
- 133 Nobre BP, Villalobos F, Barragan BE, Oliveira AC, Batista AP, Marques PA et al., A biorefinery from Nannochloropsis sp microalga–Extraction of oils and pigments Production of biohydrogen from the leftover biomass. Bioresour Technol 135: 128–136 (2013).
- 134 Prommuak C, Pavasant P, Quitain AT, Goto M and Shotipruk A, Simultaneous production of biodiesel and free lutein from Chlorella vulgaris. Chem Eng Technol 36: 733–739 (2013).
- 135 Craft, Soares, Relative solubility, stability, and absorptivity of lutein and beta.-carotene in organic solvents. J Agric Food Chem 40: 431–434 (1992).
- 136 Yang F, Cheng C, Long L, Hu Q, Jia Q, Wu H et al., Extracting lipids from several species of wet microalgae using ethanol at room temperature. Energ Fuel 29: 2380–2386 (2015).
- 137 Li Y, Naghdi FG, Garg S, Adarme-Vega TC, Thurecht KJ, Ghafor WA et al., A comparative study: the impact of different lipid extraction methods on current microalgal lipid research. Microb Cell Fact 13: 1 (2014).
- 138 Maurya R, Paliwal C, Ghosh T, Pancha I, Chokshi K, Mitra M et al., Applications of de-oiled microalgal biomass towards development of sustainable biorefinery. Bioresour Technol 214: 787–796 (2016).
- 139 Gattrel S, Lum K, Kim J and Lei X, Potential of defatted microalgae from biofuel industry as an ingredient to replace corn and soybean meal in swine and poultry diets. J Anim Sci 92: 1306–1314 (2014).