Cultivation of Microalgae on Anaerobically Digested Agro-industrial Wastes and By-Products



Anaerobic digestion (AD) is a widely used technology for the treatment of organic wastes and by-products. Through AD, the organic matter is degraded producing a gaseous stream (biogas, which is a mixture of mainly methane and carbon dioxide) and a liquid/slurry stream (digestates) that contains most of the mineralized elements originating in the feedstock. Digestates are a very interesting source of nutrients for growing microalgae to produce valuable biomass with a simultaneous further treatment of the digestates. The performance of microalgae grown using digestates is influenced by various cultivation parameters, such as the physicochemical characteristics of the digestates (nutrient profile, content of inhibitory compounds, etc.), light penetration (turbidity and colored dissolved compounds), mixing regime, and hydraulic retention time (HRT). Digestates are characterized by their high content in ammoniacal nitrogen, suspended solids, and several inhibitors that might limit growth, and therefore pretreatment of digestates is likely to have a positive effect on biomass production. Microalgal cultivation is proven as an efficient technology for the removal of nitrogen, phosphorus, organic load, and other contaminants (heavy metals, pathogens). The produced biomass could be used as feedstock for the production of various commodities (biofuels, feed, etc.); however there are some concerns about the potential contamination of microalgal biomass with unwanted hazardous pollutants. This book chapter aims to give an overview on the cultivation of microalgae utilizing digestates derived from agro-industrial wastes and by-products, discussing the potentials and the drawbacks of such an approach.


Microalgae  Cultivation  Anaerobic digestion  Agro-industrial wastewater  Contaminants Recycling 


  1. Abeliovich A, Azov Y (1976) Toxicity of ammonia to algae in seawage oxidation ponds. Appl Environ Microbiol 31:801–806Google Scholar
  2. Akhiar A (2017) Characterization of liquid fraction of digestates after solid-liquid separation from anaerobic co-digestion plants. PhD Thesis, Université Montpellier, MontpellierGoogle Scholar
  3. Akhiar A, Battimelli A, Torrijos M, Carrere H (2017) Comprehensive characterization of the liquid fraction of digestates from full-scale anaerobic co-digestion. Waste Manag 59:118–128. Scholar
  4. Aki T, Hachida K, Yoshinaga M, Katai Y, Yamasaki T, Kawamoto S, Kakizono T, Maoka T, Shigeta S, Suzuki O (2003) Thraustochytrid as a potential source of carotenoids. J Am Oil Chem Soc 80(8):789CrossRefGoogle Scholar
  5. Al-Gheethi A, Mohamed R, Jais N, Efaq A, Halid AA, Wurochekke A, Amir-Hashim M (2017) Influence of pathogenic bacterial activity on growth of Scenedesmus sp. and removal of nutrients from public market wastewater. J Water Health 15:741. wh2017080CrossRefGoogle Scholar
  6. Anastopoulos I, Kyzas GZ (2015) Progress in batch biosorption of heavy metals onto algae. J Mol Liq 209:77–86. Scholar
  7. Azov Y, Goldman JC (1982) Free ammonia inhibition of algal photosynthesis in intensive cultures. Appl Environ Microbiol 43(4):735–739Google Scholar
  8. Bachmann S, Uptmoor R, Eichler-Löbermann B (2016) Phosphorus distribution and availability in untreated and mechanically separated biogas digestates. Sci Agric 73:9–17CrossRefGoogle Scholar
  9. Bagge E, Persson M, Johansson KE (2010) Diversity of spore-forming bacteria in cattle manure, slaughterhouse waste and samples from biogas plants. J Appl Microbiol 109(5):1549–1565Google Scholar
  10. Bártíková H, Podlipná R, Skálová L (2016) Veterinary drugs in the environment and their toxicity to plants. Chemosphere 144:2290–2301CrossRefGoogle Scholar
  11. Basile A, Sorbo S, Conte B, Cobianchi RC, Trinchella F, Capasso C, Carginale V (2012) Toxicity, accumulation, and removal of heavy metals by three aquatic macrophytes. Int J Phytoremediation 14(4):374–387CrossRefGoogle Scholar
  12. Becker EW (2007) Micro-algae as a source of protein. Biotechnol Adv 25(2):207–210. Scholar
  13. Beuckels A, Smolders E, Muylaert K (2015) Nitrogen availability influences phosphorus removal in microalgae-based wastewater treatment. Water Res 77 (0):98–106. Scholar
  14. Bicudo J, Goyal S (2003) Pathogens and manure management systems: a review. Environ Technol 24(1):115–130CrossRefGoogle Scholar
  15. Biller P, Ross AB, Skill S, Lea-Langton A, Balasundaram B, Hall C, Riley R, Llewellyn C (2012) Nutrient recycling of aqueous phase for microalgae cultivation from the hydrothermal liquefaction process. Algal Res 1(1):70–76CrossRefGoogle Scholar
  16. Bjornsson WJ, Nicol RW, Dickinson KE, McGinn PJ (2013) Anaerobic digestates are useful nutrient sources for microalgae cultivation: functional coupling of energy and biomass production. J Appl Phycol 25(5):1523–1528. Scholar
  17. Borowitzka MA (2013) High-value products from microalgae-their development and commercialisation. J Appl Phycol 25(3):743–756. Scholar
  18. Brulé M, Bolduan R, Seidelt S, Schlagermann P, Bott A (2013) Modified batch anaerobic digestion assay for testing efficiencies of trace metal additives to enhance methane production of energy crops. Environ Technol 34(13):1–12Google Scholar
  19. Camiro-Vargas TK, Hernández-Ayón JM, Valenzuela-Espinoza E, Delgadillo-Hinojosa F, Cajal-Medrano R (2005) Dissolved inorganic carbon uptake by Rhodomonas sp. and Isochrysis aff. galbana determined by a potentiometric technique. Aquac Eng 33(2):83–95. Scholar
  20. Certik M, Shimizu S (1999) Biosynthesis and regulation of microbial polyunsaturated fatty acid production. J Biosci Bioeng 87(1):1–14CrossRefGoogle Scholar
  21. Chen F, Johns MR (1995) A strategy for high cell density culture of heterotrophic microalgae with inhibitory substrates. J Appl Phycol 7(1):43–46. Scholar
  22. Chen F, Johns MR (1996a) Heterotrophic growth of Chlamydomonas reinhardtii on acetate in chemostat culture. Process Biochem 31(6):601–604. Scholar
  23. Chen F, Johns MR (1996b) Relationship between substrate inhibition and maintenance energy ofChlamydomonas reinhardtii in heterotrophic culture. J Appl Phycol 8(1):15–19. Scholar
  24. Chew KW, Yap JY, Show PL, Suan NH, Juan JC, Ling TC, Lee D-J, Chang J-S (2017) Microalgae biorefinery: high value products perspectives. Bioresour Technol 229:53–62CrossRefGoogle Scholar
  25. Chiranjeevi P, Venkata Mohan S (2017) Diverse acidogenic effluents as feedstock for microalgae cultivation: dual phase metabolic transition on biomass growth and lipid synthesis. Bioresour Technol 242(Supplement C):191–196. Scholar
  26. Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25(3):294–306. Scholar
  27. Chojnacka K, Marquez-Rocha FJ (2004) Kinetic and stoichiometric relationships of the energy and carbon metabolism in the culture of microalgae. Biotechnology 3:21–34CrossRefGoogle Scholar
  28. Christaki E, Florou-Paneri P, Bonos E (2011) Microalgae: a novel ingredient in nutrition. Int J Food Sci Nutr 62(8):794–799CrossRefGoogle Scholar
  29. Cuellar-Bermudez SP, Aleman-Nava GS, Chandra R, Garcia-Perez JS, Contreras-Angulo JR, Markou G, Muylaert K, Rittmann BE, Parra-Saldivar R (2017) Nutrients utilization and contaminants removal. A review of two approaches of algae and cyanobacteria in wastewater. Algal Res 24:438–449. Scholar
  30. Cuellar-Bermudez SP, Aguilar-Hernandez I, Cardenas-Chavez DL, Ornelas-Soto N, Romero-Ogawa MA, Parra-Saldivar R (2015) Extraction and purification of high-value metabolites from microalgae: essential lipids, astaxanthin and phycobiliproteins. Microb Biotechnol 8(2):190–209CrossRefGoogle Scholar
  31. Curtis T, Mara DD, Dixo N, Silva SA (1994) Light penetration in waste stabilization ponds. Water Res 28(5):1031–1038CrossRefGoogle Scholar
  32. de Farias Silva CE, Bertucco A (2016) Bioethanol from microalgae and cyanobacteria: a review and technological outlook. Process Biochem 51(11):1833–1842. Scholar
  33. Delrue F, Imbert Y, Fleury G, Peltier G, Sassi J-F (2015) Using coagulation–flocculation to harvest Chlamydomonas reinhardtii: coagulant and flocculant efficiencies, and reuse of the liquid phase as growth medium. Algal Res 9(Supplement C):283–290. Scholar
  34. Deng X-Y, Gao K, Addy M, Li D, Zhang R-C, Lu Q, Ma Y-W, Cheng Y-L, Chen P, Liu Y-H, Ruan R (2018) Cultivation of Chlorella vulgaris on anaerobically digested swine manure with daily recycling of the post-harvest culture broth. Bioresour Technol 247(Supplement C):716–723. Scholar
  35. Depraetere O, Foubert I, Muylaert K (2013) Decolorisation of piggery wastewater to stimulate the production of Arthrospira platensis. Bioresour Technol 148:366–372. Scholar
  36. Deublein D, Steinhauser A (2008) Biogas from waste and renewable resources: an introduction. Willey-VCH, WeinheimCrossRefGoogle Scholar
  37. Díaz M, Pérez C, Sánchez C, Lauzurica S, Cañeque V, González C, De La Fuente J (2017) Feeding microalgae increases omega 3 fatty acids of fat deposits and muscles in light lambs. J Food Compos Anal 56:115–123CrossRefGoogle Scholar
  38. Dickinson KE, Bjornsson WJ, Garrison LL, Whitney CG, Park KC, Banskota AH, McGinn PJ (2015) Simultaneous remediation of nutrients from liquid anaerobic digestate and municipal wastewater by the microalga Scenedesmus sp. AMDD grown in continuous chemostats. J Appl Microbiol 118(1):75–83CrossRefGoogle Scholar
  39. Drath M, Kloft N, Batschauer A, Marin K, Novak J, Forchhammer K (2008) Ammonia triggers photodamage of photosystem II in the cyanobacterium Synechocystis sp. strain PCC 6803. Plant Physiol 147(1):206–215CrossRefGoogle Scholar
  40. Drosg B, Fuchs W, Al Seadi T, Madsen M, Linke B (2015) Nutrient recovery by biogas digestate processing. IEA Bioenergy, pp 7–11Google Scholar
  41. Dyhrman ST, Ruttenberg KC (2006) Presence and regulation of alkaline phosphatase activity in eukaryotic phytoplankton from the coastal ocean: implications for dissolved organic phosphorus remineralization. Limnol Oceanogr 51(3):1381–1390CrossRefGoogle Scholar
  42. Eich-Greatorex S, Vivekanand V, Estevez MM, Schnürer A, Børresen T, Sogn TA (2018) Biogas digestates based on lignin-rich feedstock – potential as fertilizer and soil amendment. Arch Agron Soil Sci 64(3):347–359. Scholar
  43. Eriksen NT (2008) The technology of microalgal culturing. Biotechnol Lett 30(9):1525–1536CrossRefGoogle Scholar
  44. Farno E, Baudez JC, Parthasarathy R, Eshtiaghi N (2014) Rheological characterisation of thermally-treated anaerobic digested sludge: impact of temperature and thermal history. Water Res 56:156–161. Scholar
  45. Farooq W, Moon M, Ryu B-G, Suh WI, Shrivastav A, Park MS, Mishra SK, Yang J-W (2015) Effect of harvesting methods on the reusability of water for cultivation of Chlorella vulgaris, its lipid productivity and biodiesel quality. Algal Res 8(Supplement C):1–7. Scholar
  46. Fernandez E, Galvan A (2007) Inorganic nitrogen assimilation in Chlamydomonas. J Exp Bot 58(9):2279–2287. Scholar
  47. Fernández-Sevilla J, Acién Fernández F, Molina Grima E (2010) Biotechnological production of lutein and its applications. Appl Microbiol Biotechnol 86(1):27–40CrossRefGoogle Scholar
  48. Flores E, Herrero A (2005) Nitrogen assimilation and nitrogen control in cyanobacteria. Biochem Soc Trans 33(1):164–167CrossRefGoogle Scholar
  49. Franchino M, Comino E, Bona F, Riggio VA (2013) Growth of three microalgae strains and nutrient removal from an agro-zootechnical digestate. Chemosphere 92(6):738–744CrossRefGoogle Scholar
  50. Fu F, Wang Q (2011) Removal of heavy metal ions from wastewaters: a review. J Environ Manag 92(3):407–418. Scholar
  51. Günerken E, D’Hondt E, Eppink MHM, Garcia-Gonzalez L, Elst K, Wijffels RH (2015) Cell disruption for microalgae biorefineries. Biotechnol Adv 33(2):243–260. Scholar
  52. Georgacakis D, Sievers DM, Iannotti EL (1982) Buffer stability in manure digesters. Agric Wastes 4(6):427–441. Scholar
  53. Gerardi MH (2003) The microbiology of anaerobic digesters, Wastwater microbiology series. Willey, Hoboken, New JerseyGoogle Scholar
  54. Gerardo ML, Oatley-Radcliffe DL, Lovitt RW (2014) Integration of membrane technology in microalgae biorefineries. J Membr Sci 464:86–99CrossRefGoogle Scholar
  55. González-Fernández C, Molinuevo-Salces B, García-González MC (2011) Nitrogen transformations under different conditions in open ponds by means of microalgae–bacteria consortium treating pig slurry. Bioresour Technol 102(2):960–966CrossRefGoogle Scholar
  56. Gonzalez-Fernandez C, Sialve B, Molinuevo-Salces B (2015) Anaerobic digestion of microalgal biomass: challenges, opportunities and research needs. Bioresour Technol 198:896–906CrossRefGoogle Scholar
  57. González-López CV, Cerón-García MC, Fernández-Sevilla JM, González-Céspedes AM, Camacho-Rodríguez J, Molina-Grima E (2013) Medium recycling for Nannochloropsis gaditana cultures for aquaculture. Bioresour Technol 129(Supplement C):430–438. Scholar
  58. Grobbelaar JU (2000) Physiological and technological considerations for optimising mass algal cultures. J Appl Phycol 12(3–5):201–206CrossRefGoogle Scholar
  59. Guo Y, Yeh T, Song W, Xu D, Wang S (2015) A review of bio-oil production from hydrothermal liquefaction of algae. Renew Sust Energ Rev 48:776–790CrossRefGoogle Scholar
  60. Gupta RK, Gangoliya SS, Singh NK (2015) Reduction of phytic acid and enhancement of bioavailable micronutrients in food grains. J Food Sci Technol 52(2):676–684CrossRefGoogle Scholar
  61. Gupta VK, Ali I, Saleh TA, Nayak A, Agarwal S (2012) Chemical treatment technologies for waste-water recycling—an overview. RSC Adv 2(16):6380–6388CrossRefGoogle Scholar
  62. Hansen KH, Angelidaki I, Ahring BK (1998) Anaerobic digestion of swine manure: inhibition by ammonia. Water Res 32(1):5–12. Scholar
  63. Hartley AM, House WA, Callow ME, Leadbeater BSC (1997) Coprecipitation of phosphate with calcite in the presence of photosynthesizing green algae. Water Res 31(9):2261–2268. Scholar
  64. Heubeck S, Craggs R, Shilton A (2007) Influence of CO2 scrubbing from biogas on the treatment performance of a high rate algal pond. Water Sci Technol 55(11):193–200CrossRefGoogle Scholar
  65. Hjorth M, Christensen KV, Christensen ML, Sommer SG (2010) Solid–liquid separation of animal slurry in theory and practice. A review. Agron Sustain Dev 30(1):153–180CrossRefGoogle Scholar
  66. Hoffmann JP (1998) Wastewater treatment with suspended and nonsuspended algae. J Phycol 34(5):757–763. Scholar
  67. Holman B, Kashani A, Malau-Aduli A (2012) Growth and body conformation responses of genetically divergent Australian sheep to Spirulina (Arthrospira platensis) supplementation. Am J Exp Agric 2:160–173Google Scholar
  68. Hua-sheng H, Hai-li W, Bang-qin H (1995) The availability of dissolved organic phosphorus compounds to marine phytoplankton. Chin J Oceanol Limnol 13(2):169–176. Scholar
  69. Huang B, Hong H (1999) Alkaline phosphatase activity and utilization of dissolved organic phosphorus by algae in subtropical coastal waters. Mar Pollut Bull 39(1–12):205–211. Scholar
  70. Jorquera M, Martínez O, Maruyama F, Marschner P, de la Luz Mora M (2008) Current and future biotechnological applications of bacterial Phytases and Phytase-producing bacteria. Microbes Environ 23(3):182–191. Scholar
  71. Kamalanathan M, Gleadow R, Beardall J (2015) Impacts of phosphorus availability on lipid production by Chlamydomonas reinhardtii. Algal Res 12:191–196. Scholar
  72. Kao C-Y, Chiu S-Y, Huang T-T, Dai L, Hsu L-K, Lin C-S (2012) Ability of a mutant strain of the microalga chlorella sp. to capture carbon dioxide for biogas upgrading. Appl Energy 93:176–183CrossRefGoogle Scholar
  73. Khajepour F, Hosseini SA, Ghorbani Nasrabadi R, Markou G (2015) Effect of light intensity and photoperiod on growth and biochemical composition of a local isolate of Nostoc calcicola. Appl Biochem Biotechnol 176(8):2279–2289. Scholar
  74. Khan S, Roser D, Davies C, Peters G, Stuetz R, Tucker R, Ashbolt N (2008) Chemical contaminants in feedlot wastes: concentrations, effects and attenuation. Environ Int 34(6):839–859CrossRefGoogle Scholar
  75. Kim B-H, Kang Z, Ramanan R, Choi J-E, Cho D-H, Oh H-M, Kim H-S (2014a) Nutrient removal and biofuel production in high rate algal pond using real municipal wastewater. J Microbiol Biotechnol 24(8):1123–1132CrossRefGoogle Scholar
  76. Kim H-C, Choi WJ, Maeng SK, Kim HJ, Kim HS, Song KG (2014b) Ozonation of piggery wastewater for enhanced removal of contaminants by S. Quadricauda and the impact on organic characteristics. Bioresour Technol 159(Supplement C):128–135. Scholar
  77. Kleinman PJ, Wolf AM, Sharpley AN, Beegle DB, Saporito LS (2005) Survey of water-extractable phosphorus in livestock manures. Soil Sci Soc Am J 69(3):701–708CrossRefGoogle Scholar
  78. Kovač DJ, Simeunović JB, Babić OB, Mišan AČ, Milovanović IL (2013) Algae in food and feed. Food Feed Res 40(1):21–31Google Scholar
  79. Kulpys J, Paulauskas E, Pilipavicius V, Stankevicius R (2009) Influence of cyanobacteria Arthrospira (Spirulina) platensis biomass additive towards the body condition of lactation cows and biochemical milk indexes. Agron Res 7:823–835Google Scholar
  80. Lam MK, Lee KT (2012) Microalgae biofuels: a critical review of issues, problems and the way forward. Biotechnol Adv 30(3):673–690. Scholar
  81. Lamminen M, Halmemies-Beauchet-Filleau A, Kokkonen T, Simpura I, Jaakkola S, Vanhatalo A (2017) Comparison of microalgae and rapeseed meal as supplementary protein in the grass silage based nutrition of dairy cows. Anim Feed Sci Technol 234:295–311CrossRefGoogle Scholar
  82. Li B, Brett MT (2013) The influence of dissolved phosphorus molecular form on recalcitrance and bioavailability. Environ Pollut 182 (0):37–44. Scholar
  83. Lin H, Gan J, Rajendran A, Reis CER, Hu B (2015) Phosphorus removal and recovery from Digestate after biogas production, Ch. 24. In: Biernat K (ed) Biofuels - status and perspective. InTech, Rijeka. Scholar
  84. Lora Grando R, de Souza Antune AM, da Fonseca FV, Sánchez A, Barrena R, Font X (2017) Technology overview of biogas production in anaerobic digestion plants: a European evaluation of research and development. Renew Sust Energ Rev 80(Supplement C):44–53. Scholar
  85. Lukehurst C, Frost P, Al Seadi T (2010) Utilisation of digestate from biogas plants as biofertiliser. IEA Bioenergy, Hoboken, New JerseyGoogle Scholar
  86. Macías-Sánchez MD, Robles-Medina A, Hita-Peña E, Jiménez-Callejón MJ, Estéban-Cerdán L, González-Moreno PA, Molina-Grima E (2015) Biodiesel production from wet microalgal biomass by direct transesterification. Fuel 150:14–20. Scholar
  87. Maes HM, Maletz SX, Ratte HT, Hollender J, Schaeffer A (2014) Uptake, elimination, and biotransformation of 17α-ethinylestradiol by the freshwater alga Desmodesmus subspicatus. Environ Sci Technol 48(20):12354–12361CrossRefGoogle Scholar
  88. Marazzi F, Sambusiti C, Monlau F, Cecere SE, Scaglione D, Barakat A, Mezzanotte V, Ficara E (2017) A novel option for reducing the optical density of liquid digestate to achieve a more productive microalgal culturing. Algal Res 24(Part A):19–28. Scholar
  89. Marcilhac C, Sialve B, Pourcher A-M, Ziebal C, Bernet N, Béline F (2014) Digestate color and light intensity affect nutrient removal and competition phenomena in a microalgal-bacterial ecosystem. Water Res 64:278–287CrossRefGoogle Scholar
  90. Markou G (2015) Fed-batch cultivation of Arthrospira and Chlorella in ammonia-rich wastewater: optimization of nutrient removal and biomass production. Bioresour Technol 193 (0):35–41. Scholar
  91. Markou G, Agriomallou M, Georgakakis D (2017) Forced ammonia stripping from livestock wastewater: the influence of some physico-chemical parameters of the wastewater. Water Sci Technol 75(3):686–692CrossRefGoogle Scholar
  92. Markou G, Depraetere O, Muylaert K (2016) Effect of ammonia on the photosynthetic activity of Arthrospira and Chlorella: a study on chlorophyll fluorescence and electron transport. Algal Res 16:449–457. Scholar
  93. Markou G, Depraetere O, Vandamme D, Muylaert K (2015) Cultivation of Chlorella vulgaris and Arthrospira platensis with recovered phosphorus from wastewater by means of zeolite sorption. Int J Mol Sci 16(2):4250–4264. Scholar
  94. Markou G, Muylaert K (2016) Effect of light intensity on the degree of ammonia toxicity on PSII activity of Arthrospira platensis and Chlorella vulgaris. Bioresour Technol 216:453–461. Scholar
  95. Markou G, Vandamme D, Muylaert K (2014a) Ammonia inhibition on Arthrospira platensis in relation to the initial biomass density and pH. Bioresour Technol 166:259–265. Scholar
  96. Markou G, Vandamme D, Muylaert K (2014b) Using natural zeolite for ammonia sorption from wastewater and as nitrogen releaser for the cultivation of Arthrospira platensis. Bioresour Technol 155 (0):373–378. Scholar
  97. Marshall JS, Huang Y (2010) Simulation of light-limited algae growth in homogeneous turbulence. Chem Eng Sci 65(12):3865–3875. Scholar
  98. Marshall KC (1985) Mechanisms of bacterial adhesion at solid-water interfaces. In: Savage DC, Fletcher M (eds) Bacterial adhesion: mechanisms and physiological significance. Springer US, Boston, pp 133–161. Scholar
  99. Marti N, Bouzas A, Seco A, Ferrer J (2008) Struvite precipitation assessment in anaerobic digestion processes. Chem Eng J 141(1):67–74. Scholar
  100. Mata-Alvarez J, Dosta J, Romero-Güiza MS, Fonoll X, Peces M, Astals S (2014) A critical review on anaerobic co-digestion achievements between 2010 and 2013. Renew Sust Energ Rev 36(Supplement C):412–427. Scholar
  101. Matamoros V, Gutiérrez R, Ferrer I, García J, Bayona JM (2015) Capability of microalgae-based wastewater treatment systems to remove emerging organic contaminants: a pilot-scale study. J Hazard Mater 288:34–42CrossRefGoogle Scholar
  102. Medina M, Neis U (2007) Symbiotic algal bacterial wastewater treatment: effect of food to microorganism ratio and hydraulic retention time on the process performance. Water Sci Technol 55(11):165–171CrossRefGoogle Scholar
  103. Milledge JJ (2011) Commercial application of microalgae other than as biofuels: a brief review. Rev Environ Sci Biotechnol 10(1):31–41CrossRefGoogle Scholar
  104. Möller K, Müller T (2012) Effects of anaerobic digestion on digestate nutrient availability and crop growth: a review. Eng Life Sci 12(3):242–257CrossRefGoogle Scholar
  105. Monlau F, Sambusiti C, Ficara E, Aboulkas A, Barakat A, Carrere H (2015) New opportunities for agricultural digestate valorization: current situation and perspectives. Energy Environ Sci 8(9):2600–2621CrossRefGoogle Scholar
  106. Mudryk K, Frączek J, Jewiarz M, Wróbel M, Dziedzic K (2016) Analysis of mechanical dewatering of Digestate. Agric Eng 20. Scholar
  107. Munoz R, Guieysse B (2006) Algal-bacterial processes for the treatment of hazardous contaminants: a review. Water Res 40(15):2799–2815. Scholar
  108. Myklestad SM (1995) Release of extracellular products by phytoplankton with special emphasis on polysaccharides. Sci Total Environ 165(1):155–164CrossRefGoogle Scholar
  109. Napan K, Teng L, Quinn JC, Wood BD (2015) Impact of heavy metals from flue gas integration with microalgae production. Algal Res 8:83–88. Scholar
  110. Neilson AH, Larsson T (1980) The utilization of organic nitrogen for growth of algae: physiological aspects. Physiol Plant 48(4):542–553. Scholar
  111. Olguín EJ (2012) Dual purpose microalgae–bacteria-based systems that treat wastewater and produce biodiesel and chemical products within a Biorefinery. Biotechnol Adv 30(5):1031–1046. Scholar
  112. Oliveira I, Reed J, Abu-Orf M, Wilson V, Jones D, Esteves S (2015) Impact of digestate storage conditions and rheological properties: preliminary investigations on conditioning and dewatering. Paper presented at the IWA Specialist conference on sludge management: SludgeTech 2015, United Kingdom, 29/06/15Google Scholar
  113. Pancha I, Chokshi K, George B, Ghosh T, Paliwal C, Maurya R, Mishra S (2014) Nitrogen stress triggered biochemical and morphological changes in the microalgae Scenedesmus sp. CCNM 1077. Bioresour Technol 156:146–154. Scholar
  114. Park J, Jin H-F, Lim B-R, Park K-Y, Lee K (2010) Ammonia removal from anaerobic digestion effluent of livestock waste using green alga Scenedesmus sp. Bioresour Technol 101(22):8649–8657. Scholar
  115. Pastor L, Mangin D, Ferrer J, Seco A (2010) Struvite formation from the supernatants of an anaerobic digestion pilot plant. Bioresour Technol 101(1):118–125. Scholar
  116. Pei H, Jiang L, Hou Q, Yu Z (2017) Toward facilitating microalgae cope with effluent from anaerobic digestion of kitchen waste: the art of agricultural phytohormones. Biotechnol Biofuels 10(1):76CrossRefGoogle Scholar
  117. Perales-Vela HV, Peña-Castro JM, Canizares-Villanueva RO (2006) Heavy metal detoxification in eukaryotic microalgae. Chemosphere 64(1):1–10CrossRefGoogle Scholar
  118. Perez-Garcia O, Escalante FME, de Bashan LE, Bashan Y (2011) Heterotrophic cultures of microalgae: metabolism and potential products. Water Res 45(1):11–36. Scholar
  119. Posadas E, del Mar MM, Gomez C, Acién FG, Muñoz R (2015) Influence of pH and CO 2 source on the performance of microalgae-based secondary domestic wastewater treatment in outdoors pilot raceways. Chem Eng J 265:239–248CrossRefGoogle Scholar
  120. Prajapati SK, Kumar P, Malik A, Vijay VK (2014) Bioconversion of algae to methane and subsequent utilization of digestate for algae cultivation: a closed loop bioenergy generation process. Bioresour Technol 158:174–180CrossRefGoogle Scholar
  121. Priyadarshani I, Rath B (2012) Commercial and industrial applications of micro algae–a review. J Algal Biomass Utln 3(4):89–100Google Scholar
  122. Qi G, Pan Z, Andriamanohiarisoamanana FJ, Yamashiro T, Iwasaki M, Kawamoto K, Umetsu K (2017) Isolation and characterization of plant growth promoting bacteria (PGPB) from anaerobic digestate and their effect on common wheat (Triticum aestivum) seedling growth. Int J Environ Agric Res 3(11):46–52Google Scholar
  123. Rajagopal R, Massé DI, Singh G (2013) A critical review on inhibition of anaerobic digestion process by excess ammonia. Bioresour Technol 143:632–641CrossRefGoogle Scholar
  124. Ray P, Zhao Z, Knowlton K (2013) Emerging contaminants in livestock manure: hormones, antibiotics and antibiotic resistance genes. Sustainable Animal Agriculture, Wallingford, pp 268–283Google Scholar
  125. Rincón B, Borja R, González JM, Portillo MC, Sáiz-Jiménez C (2008) Influence of organic loading rate and hydraulic retention time on the performance, stability and microbial communities of one-stage anaerobic digestion of two-phase olive mill solid residue. Biochem Eng J 40(2):253–261. Scholar
  126. Risberg K, Cederlund H, Pell M, Arthurson V, Schnürer A (2017) Comparative characterization of digestate versus pig slurry and cow manure – chemical composition and effects on soil microbial activity. Waste Manag 61:529–538. Scholar
  127. Sahlström L (2003) A review of survival of pathogenic bacteria in organic waste used in biogas plants. Bioresour Technol 87(2):161–166CrossRefGoogle Scholar
  128. Salafudin, Setyobudi RH, Wahono SK, Nindita A, Adinurani PG, Nugroho YA, Sasmito A, Liwang T (2015) Biological purification system: integrated biogas from small anaerobic digestion and natural microalgae. Procedia Chem 14:387–393. Scholar
  129. Salama E-S, Kabra AN, Ji M-K, Kim JR, Min B, Jeon B-H (2014) Enhancement of microalgae growth and fatty acid content under the influence of phytohormones. Bioresour Technol 172:97–103CrossRefGoogle Scholar
  130. Salama E-S, Kurade MB, Abou-Shanab RA, El-Dalatony MM, Yang I-S, Min B, Jeon B-H (2017) Recent progress in microalgal biomass production coupled with wastewater treatment for biofuel generation. Renew Sust Energ Rev 79:1189–1211CrossRefGoogle Scholar
  131. Santaeufemia S, Torres E, Mera R, Abalde J (2016) Bioremediation of oxytetracycline in seawater by living and dead biomass of the microalga Phaeodactylum tricornutum. J Hazard Mater 320:315–325CrossRefGoogle Scholar
  132. Schnürer A, Schnürer J (2006) Fungal survival during anaerobic digestion of organic household waste. Waste Manag 26(11):1205–1211CrossRefGoogle Scholar
  133. Schumacher G, Blume T, Sekoulov I (2003) Bacteria reduction and nutrient removal in small wastewater treatment plants by an algal biofilm. Water Sci Technol 47(11):195–202CrossRefGoogle Scholar
  134. Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101(2):87–96. Scholar
  135. Stasinakis AS (2012) Review on the fate of emerging contaminants during sludge anaerobic digestion. Bioresour Technol 121:432–440CrossRefGoogle Scholar
  136. Suresh Kumar K, Dahms H-U, Won E-J, Lee J-S, Shin K-H (2015) Microalgae – a promising tool for heavy metal remediation. Ecotoxicol Environ Saf 113:329–352. Scholar
  137. Švec P, Kováčik J, Hedbavný J, Babula P, Rotková G, Klejdus B (2016) Impact of anions, cations, and pH on manganese accumulation and toxicity in the green alga Scenedesmus quadricauda. Water Air Soil Pollut 227(5):161CrossRefGoogle Scholar
  138. 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 66:159–167. j.biombioe.2014.02.034CrossRefGoogle Scholar
  139. Tambone F, Genevini P, D’Imporzano G, Adani F (2009) Assessing amendment properties of digestate by studying the organic matter composition and the degree of biological stability during the anaerobic digestion of the organic fraction of MSW. Bioresour Technol 100(12):3140–3142. Scholar
  140. Tian C, Li B, Liu Z, Zhang Y, Lu H (2014) Hydrothermal liquefaction for algal biorefinery: a critical review. Renew Sust Energ Rev 38:933–950CrossRefGoogle Scholar
  141. Torres EM, Hess D, McNeil BT, Guy T, Quinn JC (2017) Impact of inorganic contaminants on microalgae productivity and bioremediation potential. Ecotoxicol Environ Saf 139:367–376. Scholar
  142. Tsiplakou E, Abdullah M, Mavrommatis A, Chatzikonstantinou M, Skliros D, Sotirakoglou K, Flemetakis E, Labrou N, Zervas G (2017) The effect of dietary Chlorella vulgaris inclusion on goat’s milk chemical composition, fatty acids profile and enzymes activities related to oxidation. J Anim Physiol Anim Nutr 102(1):142–151CrossRefGoogle Scholar
  143. Turon V, Baroukh C, Trably E, Latrille E, Fouilland E, Steyer J-P (2015) Use of fermentative metabolites for heterotrophic microalgae growth: yields and kinetics. Bioresour Technol 175:342–349CrossRefGoogle Scholar
  144. Uggetti E, Sialve B, Latrille E, Steyer J-P (2014) Anaerobic digestate as substrate for microalgae culture: the role of ammonium concentration on the microalgae productivity. Bioresour Technol 152:437–443. Scholar
  145. Van Boeckel TP, Glennon EE, Chen D, Gilbert M, Robinson TP, Grenfell BT, Levin SA, Bonhoeffer S, Laxminarayan R (2017) Reducing antimicrobial use in food animals. Science 357(6358):1350–1352CrossRefGoogle Scholar
  146. Venkata Mohan S, Prathima Devi M (2012) Fatty acid rich effluent from acidogenic biohydrogen reactor as substrate for lipid accumulation in heterotrophic microalgae with simultaneous treatment. Bioresour Technol 123(Supplement C):627–635. Scholar
  147. Verbyla ME, Mihelcic JR (2015) A review of virus removal in wastewater treatment pond systems. Water Res 71:107–124. Scholar
  148. Vílchez C, Vega JM (1994) Nitrite uptake by Chlamydomonas reinhardtii cells immobilized in calcium alginate. Appl Microbiol Biotechnol 41(1):137–141CrossRefGoogle Scholar
  149. Wang H, Xiong H, Hui Z, Zeng X (2012) Mixotrophic cultivation of Chlorella pyrenoidosa with diluted primary piggery wastewater to produce lipids. Bioresour Technol 104:215–220CrossRefGoogle Scholar
  150. Wang K, Yin J, Shen D, Li N (2014) Anaerobic digestion of food waste for volatile fatty acids (VFAs) production with different types of inoculum: effect of pH. Bioresour Technol 161(Supplement C):395–401. Scholar
  151. Wang Y, Guo W, Yen H-W, Ho S-H, Lo Y-C, Cheng C-L, Ren N, Chang J-S (2015) Cultivation of Chlorella vulgaris JSC-6 with swine wastewater for simultaneous nutrient/COD removal and carbohydrate production. Bioresour Technol 198:619–625CrossRefGoogle Scholar
  152. Wang Y, Liu J, Kang D, Wu C, Wu Y (2017) Removal of pharmaceuticals and personal care products from wastewater using algae-based technologies: a review. Rev Environ Sci Biotechnol. Scholar
  153. Weiland P (2010) Biogas production: current state and perspectives. Appl Microbiol Biotechnol 85(4):849–860CrossRefGoogle Scholar
  154. Whitton B (1991) Use of phosphatase assays with algae to assess phosphorus status of aquatic environments. Bioindicators and environmental management Academic Press, London, pp 295–310Google Scholar
  155. Whitton R, Ometto F, Pidou M, Jarvis P, Villa R, Jefferson B (2015) Microalgae for municipal wastewater nutrient remediation: mechanisms, reactors and outlook for tertiary treatment. Environ Technolo Rev 4(1):133–148CrossRefGoogle Scholar
  156. Xia A, Murphy JD (2016) Microalgal cultivation in treating liquid digestate from biogas systems. Trends Biotechnol 34(4):264–275CrossRefGoogle Scholar
  157. Yang S, Xu J, Wang Z-M, Bao L-J, Zeng EY (2017) Cultivation of oleaginous microalgae for removal of nutrients and heavy metals from biogas digestates. J Clean Prod 164:793–803. Scholar
  158. Zhang D, Gersberg RM, Ng WJ, Tan SK (2014) Removal of pharmaceuticals and personal care products in aquatic plant-based systems: a review. Environ Pollut 184:620–639CrossRefGoogle Scholar
  159. Zhang F, Li Y, Yang M, Li W (2012) Content of heavy metals in animal feeds and manures from farms of different scales in Northeast China. Int J Environ Res Public Health 9(8):2658–2668. Scholar
  160. Zuliani L, Frison N, Jelic A, Fatone F, Bolzonella D, Ballottari M (2016) Microalgae cultivation on anaerobic Digestate of municipal wastewater, sewage sludge and agro-waste. Int J Mol Sci 17(10):1692. Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  1. 1.Institute of Technology of Agricultural ProductsHellenic Agricultural Organization - DemeterAthensGreece
  2. 2.Water Research InstituteShanghai Academy of Environmental SciencesShanghaiChina
  3. 3.School of Environmental ScienceMemorial University of NewfoundlandCorner BrookCanada

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