Bioethanol production from microalgae polysaccharides

  • Gergely Ernő LakatosEmail author
  • Karolína Ranglová
  • João Câmara Manoel
  • Tomáš Grivalský
  • Jiří Kopecký
  • Jiří Masojídek


The worldwide growing demand for energy permanently increases the pressure on industrial and scientific community to introduce new alternative biofuels on the global energy market. Besides the leading role of biodiesel and biogas, bioethanol receives more and more attention as first- and second-generation biofuel in the sustainable energy industry. Lately, microalgae (green algae and cyanobacteria) biomass has also remarkable potential as a feedstock for the third-generation biofuel production due to their high lipid and carbohydrate content. The third-generation bioethanol production technology can be divided into three major processing ways: (i) fermentation of pre-treated microalgae biomass, (ii) dark fermentation of reserved carbohydrates and (iii) direct “photo-fermentation” from carbon dioxide to bioethanol using light energy. All three technologies provide possible solutions, but from a practical point of view, traditional fermentation technology from microalgae biomass receives currently the most attention. This study mainly focusses on the latest advances in traditional fermentation processes including the steps of enhanced carbohydrate accumulation, biomass pre-treatment, starch and glycogen downstream processing and various fermentation approaches.



Acetyl coenzyme A


Alcohol dehydrogenase I and II


Adenosine triphosphate


Consolidated bioprocess


Carbon dioxide concentrating mechanism


Dry mass


Generally recognized as safe




Pyruvate decarboxylase




Photosystem I, II




Separate hydrolysis and fermentation


Simultaneous saccharification and fermentation


Sodium bicarbonate



The authors thank Ms. Soňa Pekařová for the technical assistance and Dr. Kateřina Bišová for the discussion.

Author contribution statement

Gergely Lakatos took the leading role in the writing of the manuscript. Karolína Ranglová, Jiří Kopecký, Tomáš Grivalský and João Câmara Manoel contributed during the manuscript preparation. Jiří Masojídek revised and finalized the manuscript.


This study was funded partly by the National Sustainability Program of the Czech Ministry of Education, Youth and Sports (project Algatech Plus LO1416), and by cross-border InterReg projects between Austria and the Czech Republic (Algenetics No. ATCZ15) and Bavaria and the Czech Republic (CZ-BAV 41).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abreu AP, Fernandes B, Vicente AA, Teixeira J, Dragone G (2012) Mixotrophic cultivation of Chlorella vulgaris using industrial dairy waste as organic carbon source. Bioresour Technol 118:61–66CrossRefPubMedGoogle Scholar
  2. Aikawa S, Inokuma K, Wakai S, Sasaki K, Ogino C, Chang JS, Hasunuma T, Kondo A (2018) Direct and highly productive conversion of cyanobacteria Arthrospira platensis to ethanol with CaCl2 addition. Biotechnol Biofuels 11:50CrossRefPubMedPubMedCentralGoogle Scholar
  3. Aikawa S, Izumi Y, Matsuda F, Hasunuma T, Chang J-S, Kondo A (2012) Synergistic enhancement of glycogen production in Arthrospira platensis by optimization of light intensity and nitrate supply. Bioresour Technol 108:211–215CrossRefPubMedGoogle Scholar
  4. Aikawa S et al (2013) Direct conversion of Spirulina to ethanol without pretreatment or enzymatic hydrolysis processes. Energy Environ Sci 6:1844–1849CrossRefGoogle Scholar
  5. Ajit A, Sulaiman AZ, Chisti Y (2017) Production of bioethanol by Zymomonas mobilis in high-gravity extractive fermentations. Food Bioprod Process 102:123–135CrossRefGoogle Scholar
  6. Arad SM, Lerental YB, Dubinsky O (1992) Effect of nitrate and sulfate starvation on polysaccharide formation in Rhodella reticulata. Bioresour Technol 42:141–148CrossRefGoogle Scholar
  7. Arias DM, Uggetti E, García-Galán MJ, García J (2018) Production of polyhydroxybutyrates and carbohydrates in a mixed cyanobacterial culture: effect of nutrients limitation and photoperiods. New BiotechnolGoogle Scholar
  8. Ariño X, Ortega-Calvo J-J, Hernandez-Marine M, Saiz-Jimenez C (1995) Effect of sulfur starvation on the morphology and ultrastructure of the cyanobacterium Gloeothece sp. PCC 6909. Arch Microbiol 163:447–453CrossRefGoogle Scholar
  9. Bachmann B, Hofmann R, Follmann H (1983) Tight coordination of ribonucleotide reduction and thymidylate synthesis in synchronous algae. FEBS Lett 152:247–250CrossRefGoogle Scholar
  10. Behera S, Singh R, Arora R, Sharma NK, Shukla M, Kumar S (2015) Scope of algae as third generation biofuels. Front Bioeng Biotechnol 2:90CrossRefPubMedPubMedCentralGoogle Scholar
  11. Bellou S, Aggelis G (2013) Biochemical activities in Chlorella sp. and Nannochloropsis salina during lipid and sugar synthesis in a lab-scale open pond simulating reactor. J Biotechnol 164:318–329CrossRefGoogle Scholar
  12. Bellou S, Baeshen MN, Elazzazy AM, Aggeli D, Sayegh F, Aggelis G (2014) Microalgal lipids biochemistry and biotechnological perspectives. Biotechnol Adv 32:1476–1493CrossRefPubMedGoogle Scholar
  13. Ben-Amotz A (1975) Adaptation of the unicellular alga Dunaliella parva to a saline environment. J Phycol 11:50–54Google Scholar
  14. Benavides AMS, Ranglová K, Malapascua JR, Masojídek J, Torzillo G (2017) Diurnal changes of photosynthesis and growth of Arthrospira platensis cultured in a thin-layer cascade and an open pond. Algal Res 28:48–56CrossRefGoogle Scholar
  15. Bennamoun L, Afzal MT, Léonard A (2015) Drying of alga as a source of bioenergy feedstock and food supplement–a review. Renew Sust Energ Rev 50:1203–1212CrossRefGoogle Scholar
  16. Berges JA, Charlebois DO, Mauzerall DC, Falkowski PG (1996) Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. Plant Physiol 110:689–696CrossRefPubMedPubMedCentralGoogle Scholar
  17. Bharathiraja B et al (2015) Aquatic biomass (algae) as a future feed stock for bio-refineries: a review on cultivation, processing and products. Renew Sust Energ Rev 47:634–653CrossRefGoogle Scholar
  18. Bibi R, Ahmad Z, Imran M, Hussain S, Ditta A, Mahmood S, Khalid A (2017) Algal bioethanol production technology: a trend towards sustainable development. Renew Sust Energ Rev 71:976–985CrossRefGoogle Scholar
  19. Boboescu IZ, Gherman VD, Lakatos G, Pap B, Bíró T, Maroti G (2016) Surpassing the current limitations of biohydrogen production systems: the case for a novel hybrid approach. Bioresour Technol 204:192–201CrossRefPubMedGoogle Scholar
  20. Bracken ME et al (2015) Signatures of nutrient limitation and co-limitation: responses of autotroph internal nutrient concentrations to nitrogen and phosphorus additions. Oikos, 124:113–121Google Scholar
  21. Brányiková I, Maršálková B, Doucha J, Brányik T, Bišová K, Zachleder V, Vítová M (2011) Microalgae - novel highly efficient starch producers. Biotechnol Bioeng 108:766–776CrossRefPubMedGoogle Scholar
  22. Brennan L, Owende P (2010a) Biofuels from microalgae—a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sust Energ Rev 14:557–577CrossRefGoogle Scholar
  23. Brennan L, Owende P (2010b) Biofuels from microalgae - a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sust Energ Rev 14:557–577CrossRefGoogle Scholar
  24. Brown M, Jeffrey S, Volkman J, Dunstan G (1997) Nutritional properties of microalgae for mariculture. Aquaculture 151:315–331CrossRefGoogle Scholar
  25. Buléon A, Colonna P, Planchot V, Ball S (1998) Starch granules: structure and biosynthesis. Int J Biol Macromol 23:85–112CrossRefPubMedGoogle Scholar
  26. Busi MV, Barchiesi J, Martín M, Gomez-Casati DF (2014) Starch metabolism in green algae. Starch-Stärke 66:28–40CrossRefGoogle Scholar
  27. Cade-Menun BJ, Paytan A (2010) Nutrient temperature and light stress alter phosphorus and carbon forms in culture-grown algae. Mar Chem 121:27–36CrossRefGoogle Scholar
  28. Caporgno M, Taleb A, Olkiewicz M, Font J, Pruvost J, Legrand J, Bengoa C (2015) Microalgae cultivation in urban wastewater: nutrient removal and biomass production for biodiesel and methane. Algal Res 10:232–239CrossRefGoogle Scholar
  29. Carvalho AP, Monteiro CM, Malcata FX (2009) Simultaneous effect of irradiance and temperature on biochemical composition of the microalga Pavlova lutheri. J Appl Phycol 21:543–552CrossRefGoogle Scholar
  30. Catalanotti C, Yang W, Posewitz MC, Grossman AR (2013) Fermentation metabolism and its evolution in algae. Front Plant Sci 4:150CrossRefPubMedPubMedCentralGoogle Scholar
  31. Champigny M (1985) Regulation of photosynthetic carbon assimilation at the cellular level: a review. Photosynth Res 6:273–286CrossRefPubMedGoogle Scholar
  32. Chen C-Y et al (2013) Microalgae-based carbohydrates for biofuel production. Biochem Eng J 78:1–10CrossRefGoogle Scholar
  33. Cheng D, He Q (2014) Assessment of environmental stresses for enhanced microalgal biofuel production–an overview. Front Energy Res 2:26CrossRefGoogle Scholar
  34. Chew KW, Yap JY, Show PL, Suan NH, Juan JC, Ling TC, Lee DJ, Chang JS (2017) Microalgae biorefinery: high value products perspectives. Bioresour Technol 229:53–62CrossRefPubMedGoogle Scholar
  35. Choi W et al (2012) Bioethanol production from Ulva pertusa Kjellman by high-temperature liquefaction. Chem Biochem Eng Q 26:15–21Google Scholar
  36. Choix FJ, de Bashan LE, Bashan Y (2012) Enhanced accumulation of starch and total carbohydrates in alginate-immobilized Chlorella spp. induced by Azospirillum brasilense: II. Heterotrophic conditions. Enzym Microb Technol 51:300–309CrossRefGoogle Scholar
  37. Chojnacka K, Marquez-Rocha F-J (2004) Kinetic and stoichiometric relationships of the energy and carbon metabolism in the culture of microalgae. Biotechnology 3:21–34CrossRefGoogle Scholar
  38. Cisneros RJ, Zapf JW, Dunlap RB (1993) Studies of 5-fluorodeoxyuridine 5′-monophosphate binding to carboxypeptidase A-inactivated thymidylate synthase from Lactobacillus casei. J Biol Chem 268:10102–10108PubMedGoogle Scholar
  39. D'Souza FM, Kelly GJ (2000) Effects of a diet of a nitrogen-limited alga (Tetraselmis suecica) on growth, survival and biochemical composition of tiger prawn (Penaeus semisulcatus) larvae. Aquaculture 181:311–329CrossRefGoogle Scholar
  40. de Castro AS, Garcia VMT (2005) Growth and biochemical composition of the diatom Chaetoceros cf. wighamii brightwell under different temperature, salinity and carbon dioxide levels. I. Protein, carbohydrates and lipids. Aquaculture 246:405–412CrossRefGoogle Scholar
  41. de Farias Silva CE, Bertucco A (2016) Bioethanol from microalgae and cyanobacteria: a review and technological outlook. Process Biochem 51:1833–1842CrossRefGoogle Scholar
  42. de Farias Silva CE, Sforza E, Bertucco A (2018) Stability of carbohydrate production in continuous microalgal cultivation under nitrogen limitation: effect of irradiation regime and intensity on Tetradesmus obliquus. J Appl Phycol 30:261–270CrossRefGoogle Scholar
  43. De Oliveira M, Monteiro M, Robbs P, Leite S (1999) Growth and chemical composition of Spirulina maxima and Spirulina platensis biomass at different temperatures. Aquac Int 7:261–275CrossRefGoogle Scholar
  44. De Philippis R, Sili C, Vincenzini M (1992) Glycogen and poly-β-hydroxybutyrate synthesis in Spirulina maxima. Microbiology 138:1623–1628Google Scholar
  45. De Porcellinis A, Frigaard N-U, Sakuragi Y (2017) Determination of the glycogen content in cyanobacteria. J Vis Exp:e56068Google Scholar
  46. Dean AP, Estrada B, Nicholson JM, Sigee DC (2008a) Molecular response of Anabaena flos-aquae to differing concentrations of phosphorus: a combined Fourier transform infrared and X-ray microanalytical study. Phycol Res 56:193–201CrossRefGoogle Scholar
  47. Dean AP, Nicholson JM, Sigee DC (2008b) Impact of phosphorus quota and growth phase on carbon allocation in Chlamydomonas reinhardtii: an FTIR microspectroscopy study. Eur J Phycol 43:345–354CrossRefGoogle Scholar
  48. Deng M-D, Coleman JR (1999) Ethanol synthesis by genetic engineering in cyanobacteria. Appl Environ Microbiol 65:523–528PubMedPubMedCentralGoogle Scholar
  49. Dexter J, Armshaw P, Sheahan C, Pembroke J (2015) The state of autotrophic ethanol production in cyanobacteria. J Appl Microbiol 119:11–24CrossRefPubMedGoogle Scholar
  50. Dexter J, Fu P (2009) Metabolic engineering of cyanobacteria for ethanol production. Energy Environ Sci 2:857–864CrossRefGoogle Scholar
  51. Dienst D et al (2014) Transcriptomic response to prolonged ethanol production in the cyanobacterium Synechocystis sp. PCC6803. Biotechnol Biofuels 7:21CrossRefPubMedPubMedCentralGoogle Scholar
  52. Dourou M, Tsolcha ON, Tekerlekopoulou AG, Bokas D, Aggelis G (2018) Fish farm effluents are suitable growth media for Nannochloropsis gaditana, a polyunsaturated fatty acid producing microalga. Eng Life Sci 18:851–860CrossRefGoogle Scholar
  53. Dragone G, Fernandes BD, Abreu AP, Vicente AA, Teixeira JA (2011) Nutrient limitation as a strategy for increasing starch accumulation in microalgae. Appl Energy 88:3331–3335CrossRefGoogle Scholar
  54. Dragone G, Fernandes BD, Vicente AA, Teixeira JA (2010) Third generation biofuels from microalgae, Current research, technology and education topics in applied microbiology and microbial biotechnology. 2:1355–1366Google Scholar
  55. Eriksen NT, Riisgård FK, Gunther WS, Iversen JJL (2007) On-line estimation of O2 production, CO2 uptake, and growth kinetics of microalgal cultures in a gas-tight photobioreactor. J Appl Phycol 19:161CrossRefPubMedGoogle Scholar
  56. Eshaq FS, Ali MN, Mohd MK (2011) Production of bioethanol from next generation feed-stock alga Spirogyra species. Int J Eng Sci Technol 3:1749–1755Google Scholar
  57. Fernandes BD, Dragone GM, Teixeira JA, Vicente AA (2010) Light regime characterization in an airlift photobioreactor for production of microalgae with high starch content. Appl Biochem Biotechnol 161:218–226CrossRefPubMedGoogle Scholar
  58. Figueroa-Torres GM, Pittman JK, Theodoropoulos C (2017) Kinetic modelling of starch and lipid formation during mixotrophic, nutrient-limited microalgal growth. Bioresour Technol 241:868–878CrossRefPubMedGoogle Scholar
  59. Fouchard S et al (2005) Autotrophic and mixotrophic hydrogen photoproduction in sulfur-deprived Chlamydomonas cells. Appl Environ Microbiol 71:6199–6205CrossRefPubMedPubMedCentralGoogle Scholar
  60. Friedman O, Dubinsky Z, Arad SM (1991) Effect of light intensity on growth and polysaccharide production in red and blue-green rhodophyta unicells. Bioresour Technol 38:105–110CrossRefGoogle Scholar
  61. Gaffron H, Rubin J (1942) Fermentative and photochemical production of hydrogen in algae. J Gen Physiol 26:219–240CrossRefPubMedPubMedCentralGoogle Scholar
  62. Gao Z, Zhao H, Li Z, Tan X, Lu X (2012) Photosynthetic production of ethanol from carbon dioxide in genetically engineered cyanobacteria. Energy Environ Sci 5:9857–9865CrossRefGoogle Scholar
  63. Geider RJ, La Roche J (2002) Redfield revisited: variability of C/N/P in marine microalgae and its biochemical basis. Eur J Phycol 37:1–17CrossRefGoogle Scholar
  64. Giordano M (2001) Interactions between C and N metabolism in Dunaliella salina cells cultured at elevated CO2 and high N concentrations. J Plant Physiol 158:577–581CrossRefGoogle Scholar
  65. Giordano M, Bowes G (1997) Gas exchange and C allocation in Dunaliella salina cells in response to the N source and CO2 concentration used for growth. Plant Physiol 115:1049–1056CrossRefPubMedPubMedCentralGoogle Scholar
  66. Grossman AR, Croft M, Gladyshev VN, Merchant SS, Posewitz MC, Prochnik S, Spalding MH (2007) Novel metabolism in Chlamydomonas through the lens of genomics. Curr Opin Plant Biol 10:190–198CrossRefPubMedGoogle Scholar
  67. Guerrini F, Cangini M, Boni L, Trost P, Pistocchi R (2000) Metabolic responses of the diatom Achnanthes brevipes (Bacillariophyceae) to nutrient limitation. J Phycol 36:882–890CrossRefGoogle Scholar
  68. Gupta PL, Lee S-M, Choi H-J (2015) A mini review: photobioreactors for large scale algal cultivation. World J Microbiol Biotechnol 31:1409–1417CrossRefPubMedGoogle Scholar
  69. Harun R, Jason W, Cherrington T, Danquah MK (2011) Exploring alkaline pre-treatment of microalgal biomass for bioethanol production. Appl Energy 88:3464–3467CrossRefGoogle Scholar
  70. Hasunuma T, Kondo A (2012) Consolidated bioprocessing and simultaneous saccharification and fermentation of lignocellulose to ethanol with thermotolerant yeast strains. Process Biochem 47:1287–1294CrossRefGoogle Scholar
  71. Hemschemeier A, Happe T (2005) The exceptional photofermentative hydrogen metabolism of the green alga Chlamydomonas reinhardtii. Portland Press LimitedGoogle Scholar
  72. Hena S, Znad H, Heong K, Judd S (2018) Dairy farm wastewater treatment and lipid accumulation by Arthrospira platensis. Water Res 128:267–277CrossRefPubMedGoogle Scholar
  73. Hernández D, Riaño B, Coca M, García-González M (2015) Saccharification of carbohydrates in microalgal biomass by physical, chemical and enzymatic pre-treatments as a previous step for bioethanol production. Chem Eng J 262:939–945CrossRefGoogle Scholar
  74. Heyer H, Krumbein WE (1991) Excretion of fermentation products in dark and anaerobically incubated cyanobacteria. Arch Microbiol 155:284–287CrossRefGoogle Scholar
  75. Hirano A, Ueda R, Hirayama S, Ogushi Y (1997) CO2 fixation and ethanol production with microalgal photosynthesis and intracellular anaerobic fermentation. Energy 22:137–142CrossRefGoogle Scholar
  76. Ho S-H et al (2017) Feasibility of CO2 mitigation and carbohydrate production by microalga Scenedesmus obliquus CNW-N used for bioethanol fermentation under outdoor conditions: effects of seasonal changes. Biotechnol Biofuels 10:27CrossRefPubMedPubMedCentralGoogle Scholar
  77. Ho S-H, Huang S-W, Chen C-Y, Hasunuma T, Kondo A, Chang J-S (2013) Bioethanol production using carbohydrate-rich microalgae biomass as feedstock. Bioresour Technol 135:191–198CrossRefPubMedGoogle Scholar
  78. Hosono H et al (1994) Effect of culture temperature shift on the cellular sugar accumulation of Chlorella vulgaris SO-26. J Ferment Bioeng 78:235–240CrossRefGoogle Scholar
  79. Hossain MNB, Basu JK, Mamun M (2015) The production of ethanol from micro-algae Spirulina. Procedia Eng 105:733–738CrossRefGoogle Scholar
  80. Hu Q (2004) Environmental effects on cell composition vol 1. Blackwell Science Ltd., OxfordGoogle Scholar
  81. Huang W-D, Zhang Y-HP (2011) Analysis of biofuels production from sugar based on three criteria: thermodynamics, bioenergetics, and product separation. Energy Environ Sci 4:784–792CrossRefGoogle Scholar
  82. Huo Y-X, Cho KM, Rivera JGL, Monte E, Shen CR, Yan Y, Liao JC (2011) Conversion of proteins into biofuels by engineering nitrogen flux. Nat Biotechnol 29:346CrossRefPubMedGoogle Scholar
  83. Ingram L, Conway T, Clark D, Sewell G, Preston J (1987) Genetic engineering of ethanol production in Escherichia coli. Appl Environ Microbiol 53:2420–2425PubMedPubMedCentralGoogle Scholar
  84. Izumo A, Fujiwara S, Oyama Y, Satoh A, Fujita N, Nakamura Y, Tsuzuki M (2007) Physicochemical properties of starch in Chlorella change depending on the CO2 concentration during growth: comparison of structure and properties of pyrenoid and stroma starch. Plant Sci 172:1138–1147CrossRefGoogle Scholar
  85. Jensen S, Knutsen G (1993) Influence of light and temperature on photoinhibition of photosynthesis in Spirulina platensis. J Appl Phycol 5:495–504CrossRefGoogle Scholar
  86. Jerez CG, Malapascua JR, Sergejevová M, Figueroa FL, Masojídek J (2016) Effect of nutrient starvation under high irradiance on lipid and starch accumulation in Chlorella fusca (Chlorophyta). Mar Biotechnol 18:24–36CrossRefPubMedGoogle Scholar
  87. Ji X, Cheng J, Gong D, Zhao X, Qi Y, Su Y, Ma W (2018) The effect of NaCl stress on photosynthetic efficiency and lipid production in freshwater microalga—Scenedesmus obliquus XJ002. Sci Total Environ 633:593–599CrossRefPubMedGoogle Scholar
  88. John RP, Anisha G, Nampoothiri KM, Pandey A (2011) Micro and macroalgal biomass: a renewable source for bioethanol. Bioresour Technol 102:186–193CrossRefPubMedGoogle Scholar
  89. Jones CS, Mayfield SP (2012) Algae biofuels: versatility for the future of bioenergy. Curr Opin Biotechnol 23:346–351CrossRefPubMedGoogle Scholar
  90. Juneja A, Ceballos RM, Murthy GS (2013) Effects of environmental factors and nutrient availability on the biochemical composition of algae for biofuels production: a review. Energies 6:4607–4638CrossRefGoogle Scholar
  91. Kadouche D et al (2016) Characterization of function of the GlgA2 glycogen/starch synthase in Cyanobacterium sp. Clg1 highlights convergent evolution of glycogen metabolism into starch granule aggregation. Plant Physiol:00049.02016Google Scholar
  92. Kämäräinen J, Knoop H, Stanford NJ, Guerrero F, Akhtar MK, Aro EM, Steuer R, Jones PR (2012) Physiological tolerance and stoichiometric potential of cyanobacteria for hydrocarbon fuel production. J Biotechnol 162:67–74CrossRefPubMedGoogle Scholar
  93. Khalil ZI, Asker MM, El-Sayed S, Kobbia IA (2010) Effect of pH on growth and biochemical responses of Dunaliella bardawil and Chlorella ellipsoidea. World J Microbiol Biotechnol 26:1225–1231CrossRefPubMedGoogle Scholar
  94. Kim HM, Wi SG, Jung S, Song Y, Bae H-J (2015) Efficient approach for bioethanol production from red seaweed Gelidium amansii. Bioresour Technol 175:128–134CrossRefPubMedGoogle Scholar
  95. Klein U, Betz A (1978) Fermentative metabolism of hydrogen-evolving Chlamydomonas moewusii. Plant Physiol 61:953–956CrossRefPubMedPubMedCentralGoogle Scholar
  96. Kopka J et al (2017) Systems analysis of ethanol production in the genetically engineered cyanobacterium Synechococcus sp. PCC 7002. Biotechnol Biofuels 10:56CrossRefPubMedPubMedCentralGoogle Scholar
  97. Kumar D, Murthy GS (2011) Impact of pretreatment and downstream processing technologies on economics and energy in cellulosic ethanol production. Biotechnol Biofuels 4:27CrossRefPubMedPubMedCentralGoogle Scholar
  98. Lakatos G, Balogh D, Farkas A, Ördög V, Nagy PT, Bíró T, Maróti G (2017) Factors influencing algal photobiohydrogen production in algal-bacterial co-cultures. Algal Res 28:161–171CrossRefGoogle Scholar
  99. Lakatos G, Deák Z, Vass I, Rétfalvi T, Rozgonyi S, Rákhely G, Ördög V, Kondorosi É, Maróti G (2014) Bacterial symbionts enhance photo-fermentative hydrogen evolution of Chlamydomonas algae. Green Chem 16:4716–4727CrossRefGoogle Scholar
  100. Lee H-J, Lim W-S, Lee J-W (2013) Improvement of ethanol fermentation from lignocellulosic hydrolysates by the removal of inhibitors. J Ind Eng Chem 19:2010–2015CrossRefGoogle Scholar
  101. Lee SY, Cho JM, Chang YK, Oh Y-K (2017) Cell disruption and lipid extraction for microalgal biorefineries: a review. Bioresour TechnolGoogle Scholar
  102. Li Y, Han D, Hu G, Sommerfeld M, Hu Q (2010) Inhibition of starch synthesis results in overproduction of lipids in Chlamydomonas reinhardtii. Biotechnol Bioeng 107:258–268CrossRefPubMedGoogle Scholar
  103. Lynn SG, Kilham SS, Kreeger DA, Interlandi SJ (2000) Effect of nutrient availability on the biochemical and elemental stoichiometry in the freshwater diatom Stephanodiscus minutulus (Bacillariophyceae). J Phycol 36:510–522CrossRefPubMedGoogle Scholar
  104. Magneschi L, Catalanotti C, Subramanian V, Dubini A, Yang W, Mus F, Posewitz MC, Seibert M, Perata P, Grossman AR (2012) A mutant in the ADH1 gene of Chlamydomonas reinhardtii elicits metabolic restructuring during anaerobiosis. Plant Physiol 158:1293–1305CrossRefPubMedPubMedCentralGoogle Scholar
  105. Malibari R, Sayegh F, Elazzazy AM, Baeshen MN, Dourou M, Aggelis G (2018) Reuse of shrimp farm wastewater as growth medium for marine microalgae isolated from Red Sea–Jeddah. J Clean Prod 198:160–169CrossRefGoogle Scholar
  106. Manochio C, Andrade B, Rodriguez R, Moraes B (2017) Ethanol from biomass: a comparative overview. Renew Sust Energ Rev 80:743–755CrossRefGoogle Scholar
  107. Märkl H, Bronnenmeier R, Wittek B (1991) The resistance of microorganisms to hydrodynamic stress. Int Chem Eng 31:185–196Google Scholar
  108. Markou G, Angelidaki I, Georgakakis D (2012a) Microalgal carbohydrates: an overview of the factors influencing carbohydrates production, and of main bioconversion technologies for production of biofuels. Appl Microbiol Biotechnol 96:631–645CrossRefPubMedGoogle Scholar
  109. Markou G, Angelidaki I, Nerantzis E, Georgakakis D (2013) Bioethanol production by carbohydrate-enriched biomass of Arthrospira (Spirulina) platensis. Energies 6:3937–3950CrossRefGoogle Scholar
  110. Markou G, Chatzipavlidis I, Georgakakis D (2012b) Carbohydrates production and bio-flocculation characteristics in cultures of Arthrospira (Spirulina) platensis: improvements through phosphorus limitation process. BioEnergy Res 5:915–925CrossRefGoogle Scholar
  111. Matsubara K (2004) Recent advances in marine algal anticoagulants. Curr Med Chem Cardiovasc Hematol Agents 2:13–19CrossRefPubMedGoogle Scholar
  112. Melendez-Hevia E, Waddell T, Shelton E (1993) Optimization of molecular design in the evolution of metabolism: the glycogen molecule. Biochem J 295:477–483CrossRefPubMedPubMedCentralGoogle Scholar
  113. Melis A (2007) Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (unicellular green algae). Planta 226:1075–1086CrossRefPubMedGoogle Scholar
  114. Möllers KB, Cannella D, Jørgensen H, Frigaard N-U (2014) Cyanobacterial biomass as carbohydrate and nutrient feedstock for bioethanol production by yeast fermentation. Biotechnol Biofuels 7:64CrossRefPubMedPubMedCentralGoogle Scholar
  115. Mühlroth A et al (2013) Pathways of lipid metabolism in marine algae, co-expression network, bottlenecks and candidate genes for enhanced production of EPA and DHA in species of Chromista. Mar Drugs 11:4662–4697CrossRefPubMedPubMedCentralGoogle Scholar
  116. Mulchandani K, Kar JR, Singhal RS (2015) Extraction of lipids from Chlorella saccharophila using high-pressure homogenization followed by three phase partitioning. Appl Biochem Biotechnol 176(6):1613–1626Google Scholar
  117. Mus F, Dubini A, Seibert M, Posewitz MC, Grossman AR (2007) Anaerobic acclimation in Chlamydomonas reinhardtii anoxic gene expression, hydrogenase induction, and metabolic pathways. J Biol Chem 282:25475–25486CrossRefPubMedGoogle Scholar
  118. Nakamura Y, Takahashi JI, Sakurai A, Inaba Y, Suzuki E, Nihei S, Fujiwara S, Tsuzuki M, Miyashita H, Ikemoto H, Kawachi M, Sekiguchi H, Kurano N (2005) Some cyanobacteria synthesize semi-amylopectin type α-polyglucans instead of glycogen. Plant Cell Physiol 46:539–545CrossRefPubMedGoogle Scholar
  119. Namakoshi K, Nakajima T, Yoshikawa K, Toya Y, Shimizu H (2016) Combinatorial deletions of glgC and phaCE enhance ethanol production in Synechocystis sp. PCC 6803. J Biotechnol 239:13–19CrossRefPubMedGoogle Scholar
  120. Nguyen MT, Choi SP, Lee J, Lee JH, Sim SJ (2009) Hydrothermal acid pretreatment of Chlamydomonas reinhardtii biomass for ethanol production. J Microbiol Biotechnol 19:161–166CrossRefPubMedGoogle Scholar
  121. Nigam PS, Singh A (2011) Production of liquid biofuels from renewable resources. Prog Energy Combust Sci 37:52–68CrossRefGoogle Scholar
  122. Norsker N-H, Barbosa MJ, Vermuë MH, Wijffels RH (2011) Microalgal production—a close look at the economics. Biotechnol Adv 29:24–27CrossRefPubMedGoogle Scholar
  123. Nyvall P, Pelloux J, Davies HV, Pedersén M, Viola R (1999) Purification and characterisation of a novel starch synthase selective for uridine 5′-diphosphate glucose from the red alga Gracilaria tenuistipitata. Planta 209:143–152CrossRefPubMedGoogle Scholar
  124. Ogbonda KH, Aminigo RE, Abu GO (2007) Influence of temperature and pH on biomass production and protein biosynthesis in a putative Spirulina sp. Bioresour Technol 98:2207–2211CrossRefPubMedGoogle Scholar
  125. Ogbonna JC, Tanaka H (1996) Night biomass loss and changes in biochemical composition of cells during light/dark cyclic culture of Chlorella pyrenoidosa. J Ferment Bioeng 82:558–564CrossRefGoogle Scholar
  126. Pade N, Mikkat S, Hagemann M (2017) Ethanol, glycogen and glucosylglycerol represent competing carbon pools in ethanol-producing cells of Synechocystis sp. PCC 6803 under high-salt conditions. Microbiology 163:300–307CrossRefPubMedGoogle Scholar
  127. Perez-Garcia O, Escalante FM, de Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45:11–36CrossRefPubMedGoogle Scholar
  128. Poblete R, Cortes E, Macchiavello J, Bakit J (2018) Factors influencing solar drying performance of the red algae Gracilaria chilensis. Renew Energy 126:978–986CrossRefGoogle Scholar
  129. Rastogi M, Shrivastava S (2017) Recent advances in second generation bioethanol production: an insight to pretreatment, saccharification and fermentation processes. Renew Sust Energ Rev 80:330–340CrossRefGoogle Scholar
  130. Raven JA, Beardall J (2003) Carbohydrate metabolism and respiration in algae. In: Photosynthesis in algae. Springer, pp 205–224Google Scholar
  131. Renaud SM, Thinh L-V, Lambrinidis G, Parry DL (2002) Effect of temperature on growth, chemical composition and fatty acid composition of tropical Australian microalgae grown in batch cultures. Aquaculture 211:195–214CrossRefGoogle Scholar
  132. Richmond A, Cheng-Wu Z, Zarmi Y (2003) Efficient use of strong light for high photosynthetic productivity: interrelationships between the optical path, the optimal population density and cell-growth inhibition. Biomol Eng 20:229–236CrossRefPubMedGoogle Scholar
  133. Richmond A, Hu Q (2013) Handbook of microalgal culture: applied phycology and biotechnology. John Wiley & SonsGoogle Scholar
  134. Roopnarain A, Gray V, Sym S (2014) Phosphorus limitation and starvation effects on cell growth and lipid accumulation in Isochrysis galbana U4 for biodiesel production. Bioresour Technol 156:408–411CrossRefPubMedGoogle Scholar
  135. Salehi Jouzani G, Taherzadeh MJ (2015) Advances in consolidated bioprocessing systems for bioethanol and butanol production from biomass: a comprehensive review. Biofuel Res J 2:152–195CrossRefGoogle Scholar
  136. Sangar VK, Dugan PR (1972) Polysaccharide produced by Anacystis nidulans: its ecological implication. Appl Microbiol 24:732–734PubMedPubMedCentralGoogle Scholar
  137. Sassano C, Gioielli L, Ferreira L, Rodrigues M, Sato S, Converti A, Carvalho J (2010) Evaluation of the composition of continuously-cultivated Arthrospira (Spirulina) platensis using ammonium chloride as nitrogen source. Biomass Bioenergy 34:1732–1738CrossRefGoogle Scholar
  138. Scott SA, Davey MP, Dennis JS, Horst I, Howe CJ, Lea-Smith DJ, Smith AG (2010) Biodiesel from algae: challenges and prospects. Curr Opin Biotechnol 21:277–286CrossRefPubMedGoogle Scholar
  139. Shang C, Zhu S, Wang Z, Qin L, Alam MA, Xie J, Yuan Z (2017) Proteome response of Dunaliella parva induced by nitrogen limitation. Algal Res 23:196–202CrossRefGoogle Scholar
  140. Shokrkar H, Ebrahimi S, Zamani M (2017) Bioethanol production from acidic and enzymatic hydrolysates of mixed microalgae culture. Fuel 200:380–386CrossRefGoogle Scholar
  141. Show K-Y, Lee D-J, Tay J-H, Lee T-M, Chang J-S (2015) Microalgal drying and cell disruption–recent advances. Bioresour Technol 184:258–266CrossRefPubMedGoogle Scholar
  142. Siaut M, Cuiné S, Cagnon C, Fessler B, Nguyen M, Carrier P, Beyly A, Beisson F, Triantaphylidès C, Li-Beisson Y, Peltier G (2011) Oil accumulation in the model green alga Chlamydomonas reinhardtii: characterization, variability between common laboratory strains and relationship with starch reserves. BMC Biotechnol 11:7CrossRefPubMedPubMedCentralGoogle Scholar
  143. Sigee DC, Bahrami F, Estrada B, Webster RE, Dean AP (2007) The influence of phosphorus availability on carbon allocation and P quota in Scenedesmus subspicatus: a synchrotron-based FTIR analysis. Phycologia 46:583–592CrossRefGoogle Scholar
  144. Singh A, Nigam PS, Murphy JD (2011) Renewable fuels from algae: an answer to debatable land based fuels. Bioresour Technol 102:10–16CrossRefPubMedGoogle Scholar
  145. Skorupskaite V, Makareviciene V, Ubartas M, Karosiene J, Gumbyte M (2017) Green algae Ankistrodesmus fusiformis cell disruption using different modes. Biomass Bioenergy 107:311–316CrossRefGoogle Scholar
  146. Song Z, Chen L, Wang J, Lu Y, Jiang W, Zhang W (2014) A transcriptional regulator Sll0794 regulates tolerance to biofuel ethanol in photosynthetic Synechocystis sp. PCC 6803. Mol Cell Proteomics 13:3519–3532CrossRefPubMedPubMedCentralGoogle Scholar
  147. Suzuki E, Suzuki R (2013) Variation of storage polysaccharides in phototrophic microorganisms. J Appl Glycosci 60:21–27CrossRefGoogle Scholar
  148. Taiz L, Zeiger E (2010) Plant physiology, 5th edn. Sinauer Associates, SunderlandGoogle Scholar
  149. Takahashi H, Kopriva S, Giordano M, Saito K, Hell R (2011) Sulfur assimilation in photosynthetic organisms: molecular functions and regulations of transporters and assimilatory enzymes. Annu Rev Plant Biol 62:157–184CrossRefGoogle Scholar
  150. Taleb A et al (2016) Screening of freshwater and seawater microalgae strains in fully controlled photobioreactors for biodiesel production. Bioresour Technol 218:480–490CrossRefPubMedGoogle Scholar
  151. Taraldsvik M, Myklestad SM (2000) The effect of pH on growth rate, biochemical composition and extracellular carbohydrate production of the marine diatom Skeletonema costatum. Eur J Phycol 35:189–194CrossRefGoogle Scholar
  152. Torzillo G, Sacchi A, Materassi R (1991) Temperature as an important factor affecting productivity and night biomass loss in Spirulina platensis grown outdoors in tubular photobioreactors. Bioresour Technol 38:95–100CrossRefGoogle Scholar
  153. Tredici MR (2010) Photobiology of microalgae mass cultures: understanding the tools for the next green revolution. Biofuels 1:143–162CrossRefGoogle Scholar
  154. Tsolcha O, Tekerlekopoulou A, Akratos C, Aggelis G, Genitsaris S, Moustaka-Gouni M, Vayenas D (2018) Agroindustrial wastewater treatment with simultaneous biodiesel production in attached growth systems using a mixed microbial culture. Water 10:1693CrossRefGoogle Scholar
  155. Tsolcha ON, Tekerlekopoulou AG, Akratos CS, Aggelis G, Genitsaris S, Moustaka-Gouni M, Vayenas DV (2017) Biotreatment of raisin and winery wastewaters and simultaneous biodiesel production using a Leptolyngbya-based microbial consortium. J Clean Prod 148:185–193CrossRefGoogle Scholar
  156. Tsolcha ON et al (2016) Treatment of second cheese whey effluents using a Choricystis-based system with simultaneous lipid production. J Chem Technol Biotechnol 91:2349–2359CrossRefGoogle Scholar
  157. Tsubaki S, Oono K, Hiraoka M, Onda A, Mitani T (2016) Microwave-assisted hydrothermal extraction of sulfated polysaccharides from Ulva spp. and Monostroma latissimum. Food Chem 210:311–316CrossRefPubMedGoogle Scholar
  158. Turpin DH (1991) Effects of inorganic N availability on algal photosynthesis and carbon metabolism. J Phycol 27:14–20CrossRefGoogle Scholar
  159. Ueno Y, Kurano N, Miyachi S (1998) Ethanol production by dark fermentation in the marine green alga, Chlorococcum littorale. J Ferment Bioeng 86:38–43CrossRefGoogle Scholar
  160. Vonshak A (1997) Spirulina platensis arthrospira: physiology, cell-biology and biotechnology. CRC PressGoogle Scholar
  161. Wang H, Ji C, Bi S, Zhou P, Chen L, Liu T (2014) Joint production of biodiesel and bioethanol from filamentous oleaginous microalgae Tribonema sp. Bioresour Technol 172:169–173CrossRefPubMedGoogle Scholar
  162. Wang L, Li Y, Sommerfeld M, Hu Q (2013) A flexible culture process for production of the green microalga Scenedesmus dimorphus rich in protein, carbohydrate or lipid. Bioresour Technol 129:289–295CrossRefPubMedGoogle Scholar
  163. Warr S, Reed R, Stewart W (1985) Carbohydrate accumulation in osmotically stressed cyanobacteria (blue-green algae): interactions of temperature and salinity. New Phytol 100:285–292CrossRefGoogle Scholar
  164. Wirth R, Lakatos G, Böjti T, Maróti G, Bagi Z, Kis M, Kovács A, Ács N, Rákhely G, Kovács KL (2015) Metagenome changes in the mesophilic biogas-producing community during fermentation of the green alga Scenedesmus obliquus. J Biotechnol 215:52–61CrossRefPubMedGoogle Scholar
  165. Wuang SC, Khin MC, Chua PQD, Luo YD (2016) Use of Spirulina biomass produced from treatment of aquaculture wastewater as agricultural fertilizers. Algal Res 15:59–64CrossRefGoogle Scholar
  166. Xia JR, Gao KS (2005) Impacts of elevated CO2 concentration on biochemical composition, carbonic anhydrase, and nitrate reductase activity of freshwater green algae. J Integr Plant Biol 47:668–675CrossRefGoogle Scholar
  167. Yamada R, Tanaka T, Ogino C, Fukuda H, Kondo A (2010) Novel strategy for yeast construction using δ-integration and cell fusion to efficiently produce ethanol from raw starch. Appl Microbiol Biotechnol 85:1491–1498CrossRefPubMedGoogle Scholar
  168. Yang S, Pan C, Tschaplinski TJ, Hurst GB, Engle NL, Zhou W, Dam PA, Xu Y, Rodriguez M, Dice L, Johnson CM, Davison BH, Brown SD (2013) Systems biology analysis of Zymomonas mobilis ZM4 ethanol stress responses. PLoS One 8:e68886CrossRefPubMedPubMedCentralGoogle Scholar
  169. Yao C-H, Ai J-N, Cao X-P, Xue S (2013) Characterization of cell growth and starch production in the marine green microalga Tetraselmis subcordiformis under extracellular phosphorus-deprived and sequentially phosphorus-replete conditions. Appl Microbiol Biotechnol 97:6099–6110CrossRefPubMedGoogle Scholar
  170. Yao C, Ai J, Cao X, Xue S, Zhang W (2012) Enhancing starch production of a marine green microalga Tetraselmis subcordiformis through nutrient limitation. Bioresour Technol 118:438–444CrossRefPubMedGoogle Scholar
  171. Yoshikawa K, Toya Y, Shimizu H (2017) Metabolic engineering of Synechocystis sp. PCC 6803 for enhanced ethanol production based on flux balance analysis. Bioprocess Biosyst Eng 40:791–796CrossRefPubMedGoogle Scholar
  172. Zabed H, Sahu J, Suely A, Boyce A, Faruq G (2017) Bioethanol production from renewable sources: current perspectives and technological progress. Renew Sust Energ Rev 71:475–501CrossRefGoogle Scholar
  173. Zachleder V, Kawano S, Kuroiwa T (1996) Uncoupling of chloroplast reproductive events from cell cycle division processes by 5-fluorodeoxyuridine in the alga Scenedesmus quadricauda. Protoplasma 192:228–234CrossRefGoogle Scholar
  174. Zhang Z, Shrager J, Jain M, Chang C-W, Vallon O, Grossman AR (2004) Insights into the survival of Chlamydomonas reinhardtii during sulfur starvation based on microarray analysis of gene expression. Eukaryot Cell 3:1331–1348CrossRefPubMedPubMedCentralGoogle Scholar
  175. Zhao G, Chen X, Wang L, Zhou S, Feng H, Chen WN, Lau R (2013) Ultrasound assisted extraction of carbohydrates from microalgae as feedstock for yeast fermentation. Bioresour Technol 128:337–344CrossRefPubMedGoogle Scholar
  176. Zhou N, Zhang Y, Wu X, Gong X, Wang Q (2011) Hydrolysis of Chlorella biomass for fermentable sugars in the presence of HCl and MgCl2. Bioresour Technol 102:10158–10161CrossRefPubMedGoogle Scholar
  177. Zhu L, Hiltunen E, Antila E, Zhong J, Yuan Z, Wang Z (2014) Microalgal biofuels: flexible bioenergies for sustainable development. Renew Sust Energ Rev 30:1035–1046CrossRefGoogle Scholar
  178. Zhu Z, Luan G, Tan X, Zhang H, Lu X (2017) Rescuing ethanol photosynthetic production of cyanobacteria in non-sterilized outdoor cultivations with a bicarbonate-based pH-rising strategy. Biotechnol Biofuels 10:93CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Institute of Microbiology, Academy of Sciences of the Czech Republic, v.v.i. 2019

Authors and Affiliations

  1. 1.Centre Algatech, Laboratory of Algal BiotechnologyInstitute of MicrobiologyTřeboňCzech Republic
  2. 2.Faculty of AgricultureUniversity of South BohemiaČeské BudějoviceCzech Republic
  3. 3.Faculty of ScienceUniversity of South BohemiaČeské BudějoviceCzech Republic

Personalised recommendations