Using microalgae in the circular economy to valorise anaerobic digestate: challenges and opportunities

Abinandan, 2015, Challenges and opportunities in application of microalgae (Chlorophyta) for wastewater treatment: a review, Renew. Sustain. Energy Rev., 52, 123, 10.1016/j.rser.2015.07.086 AHDB, 2017. Nutrient Management Guide (RB209). Section 2: Organic Materials. Agriculture and Horticulture Development Board (AHDB), Warwickshire. AHDB, 2018. UK Fertiliser Price Series, May 2018 report. Available at: https://ahdb.org.uk/documents/UK_Fertiliser_Price_Series_report-May2018.pdf. Barry, 2016 Becker, 2007, Micro-algae as a source of protein, Biotechnol. Adv., 25, 207, 10.1016/j.biotechadv.2006.11.002 Blake, C., Lupatsch, I., 2012. Nutritional assessment of algae-based feeds for tilapia in intensive aquaculture. In: Proceedings of the Europe Aquaculture Society Conference, Prague, Czech Republic. BORRG (Bioenergy and Organic Resources Research Group, University of Southampton) (2015). Anaerobic Digestion Assessment Tool (ADAT), Version 2 dated 4 July 2015. Available at: http://www.bioenergy.soton.ac.uk/AD_software_tool.htm. Budzianowski, 2016, A review of potential innovations for production, conditioning and utilization of biogas with multiple-criteria assessment, Renew. Sustain. Energy Rev., 54, 1148, 10.1016/j.rser.2015.10.054 Burr, 2011, Apparent digestibility of macro-nutrients and phosphorus in plant-derived ingredients for Atlantic salmon, Salmo salar and Arctic charr, Salvelinus alpinus., Aquaculture Nutrition, 17, 570, 10.1111/j.1365-2095.2011.00855.x Cardinaletti, 2018, Effects of graded levels of a blend of Tisochrysis lutea and Tetraselmis suecica dried biomass on growth and muscle tissue composition of European sea bass (Dicentrarchus labrax) fed diets low in fish meal and oil, Aquaculture, 485, 173, 10.1016/j.aquaculture.2017.11.049 Carpenter, 1998, Nonpoint pollution of surface waters with phosphorus and nitrogen, Ecol. Appl., 8, 559, 10.1890/1051-0761(1998)008[0559:NPOSWW]2.0.CO;2 Chadwick, 2011, Manure management: implications for greenhouse gas emissions, Anim. Feed Sci. Technol., 166, 514, 10.1016/j.anifeedsci.2011.04.036 Cho, 2013, Microalgae cultivation for bioenergy production using wastewaters from a municipal WWTP as nutritional sources, Bioresour. Technol., 131, 515, 10.1016/j.biortech.2012.12.176 Choubert, 1993, Carotenoid pigments of the green alga Haematococcus pluvialis: assay on rainbow trout, Oncorhynchus mykiss, pigmentation in comparison with synthetic astaxanthin and canthaxanthin, Aquaculture, 112, 217, 10.1016/0044-8486(93)90447-7 Coelho, 2018, Physical-chemical traits, phytotoxicity and pathogen detection in liquid anaerobic digestates, Waste Manage. (Oxford), 78, 8, 10.1016/j.wasman.2018.05.017 Commichau, 2006, Regulatory links between carbon and nitrogen metabolism, Current Opinion Microbiol., 9, 167, 10.1016/j.mib.2006.01.001 Cordell, 2009, The story of phosphorus: Global food security and food for thought, Global Environ. Change, 19, 292, 10.1016/j.gloenvcha.2008.10.009 de Visser, 2014, The EU’s dependency on soya bean import for the animal feed industry and potential for EU produced alternatives, Ocl, 21, D407, 10.1051/ocl/2014021 Ebrahim, 2013, COBRApy: constraints-based reconstruction and analysis for python, BMC Syst. Biol., 7, 74, 10.1186/1752-0509-7-74 Ekvall, 2004, System boundaries and input data in consequential life cycle inventory analysis, Int. J. Life Cycle Assess., 9, 161, 10.1007/BF02994190 Erisman, 2008, Agricultural air quality in Europe and the future perspectives, Atmos. Environ., 42, 3209, 10.1016/j.atmosenv.2007.04.004 Farazi, 2018, Ontology-based faceted semantic search with automatic sense disambiguation for bioenergy domain, Int. J. Big Data Intelligence, 5, 62, 10.1504/IJBDI.2018.088286 Fait, 2018, Metabolomics approaches to advance understanding of nitrogen assimilation and carbon–nitrogen interactions, Ann. Plant Rev., 249, 10.1002/9781119312994.apr0457 Fedorniak, 2017 Fenton, 2012, Agricultural nutrient surpluses as potential input sources to grow third generation biomass (microalgae): a review, Algal Research, 1, 49, 10.1016/j.algal.2012.03.003 Finkbeiner, 2006, The new international standards for life cycle assessment: ISO 14040 and ISO 14044, Int. J. Life Cycle Assess., 11, 80, 10.1065/lca2006.02.002 Fishman, 2010 FNR, 2012. Guide to Biogas: From production to use, Gülzow. Available from: https://mediathek.fnr.de/media/downloadable/files/samples/g/u/guide_biogas_engl_2012.pdf. Accessed June 14, 2017. Fuchs, W., Drosg, B., 2010. Technologiebewertung von Gärrestbehandlungs- und Verwertungskonzepten, Universität für Bodenkultur. Wien. ISBN 3900962863, 9783900962869. Gao, 2011, Using thermophilic anaerobic digestate effluent to replace freshwater for bioethanol production, Bioresour. Technol., 102, 2126, 10.1016/j.biortech.2010.08.088 Gasparri, 2013, Linkages between soybean and neotropical deforestation: coupling and transient decoupling dynamics in a multi-decadal analysis, Global Environ. Change, 23, 1605, 10.1016/j.gloenvcha.2013.09.007 Gbadamosi, 2018, Effects of dietary Nannochloropsis salina on the nutritional performance and fatty acid profile of Nile tilapia, Oreochromis niloticus, Algal Research, 33, 48, 10.1016/j.algal.2018.04.030 Gerardo, 2014, Integration of membrane technology in microalgae biorefineries, J. Membr. Sci., 464, 86, 10.1016/j.memsci.2014.04.010 Gerardo, 2013, Strategies for the recovery of nutrients and metals from anaerobically digested dairy farm sludge using cross-flow microfiltration, Water Res., 47, 4833, 10.1016/j.watres.2013.04.019 Gonçalves, 2017, A review on the use of microalgal consortia for wastewater treatment, Algal Res., 24, 403, 10.1016/j.algal.2016.11.008 González-Fernández, 2010, Nitrogen transformations under different conditions in open ponds by means of microalgae–bacteria consortium treating pig slurry, Bioresour. Technol., 102, 960, 10.1016/j.biortech.2010.09.052 Gouveia, 2002, Pigmentation of gilthead seabream, Sparus aurata (L. 1875), using Chlorella vulgaris (Chlorophyta, Volvocales) microalga, Aquac. Res., 33, 987, 10.1046/j.1365-2109.2002.00751.x Hanserud, 2017, Redistributing phosphorus in animal manure from a livestock-intensive region to an arable region: exploration of environmental consequences, Sustainability, 9, 595, 10.3390/su9040595 Hopkins, 2007, Implications of climate change for grassland in Europe: impacts, adaptations and mitigation options: a review, Grass Forage Sci., 62, 118, 10.1111/j.1365-2494.2007.00575.x Janczyk, 2007, Nutritional value of Chlorella vulgaris: effects of ultrasonication and electroporation on digestibility in rats, Animal Feed Sci. Technol., 132, 163, 10.1016/j.anifeedsci.2006.03.007 Kang, 2018, Nutrient removal and community structure of wastewater-borne algal-bacterial consortia grown in raw wastewater with various wavelengths of light, International Biodeteriotation Biodegradation, 126, 10, 10.1016/j.ibiod.2017.09.022 Kerckhof, 2014, Optimized cryopreservation of mixed microbial communities for conserved functionality and diversity, PLoS One, 9, e99517, 10.1371/journal.pone.0099517 Kousoulaki, 2016, Microalgae and organic minerals enhance lipid retention efficiency and fillet quality in Atlantic salmon (Salmo salar L.), Aquaculture, 451, 47, 10.1016/j.aquaculture.2015.08.027 Kumi, 2016, Volatile fatty acids platform from thermally hydrolysed secondary sewage sludge enhanced through recovered micronutrients from digested sludge, Water Res., 100, 267, 10.1016/j.watres.2016.05.030 Lahel, 2016, Effect of process parameters on the bioremediation of diesel contaminated soil by mixed microbial consortia, Int. Biodeter. Biodegrad., 113, 375, 10.1016/j.ibiod.2016.05.005 Levine, 2011, Neochloris oleoabundans grown on anaerobically digested dairy manure for concomitant nutrient removal and biodiesel feedstock production, Biomass Bioenergy, 35, 40, 10.1016/j.biombioe.2010.08.035 Lukehurst, 2010, Utilisation of digestate from biogas plants as biofertiliser, IEA Bioenergy, 1 Lulacat, 1984, Utilization of light for the assimilation of organic matter in Chlorella sp. VJ79, Biotechnol. Bioeng., 26, 677, 10.1002/bit.260260707 Mahapatra, 2014, Bioremediation and lipid synthesis through mixotrophic algal consortia in municipal wastewater, Biores. Technol., 168, 142, 10.1016/j.biortech.2014.03.130 Marcato, 2008, Particle size and metal distributions in anaerobically digested pig slurry, Bioresour. Technol., 99, 2340, 10.1016/j.biortech.2007.05.013 Mata, 2010, Microalgae for biodiesel production and other applications: a review, Renew. Sustain. Energy Rev., 14, 217, 10.1016/j.rser.2009.07.020 Mayhead, 2018, Comparing nutrient removal from membrane filtered and unfiltered domestic wastewater using Chlorella vulgaris, Biology, 7, 12, 10.3390/biology7010012 Medina, 2007, Symbiotic algal bacterial wastewater treatment: effect of food to microorganism ratio and hydraulic retention time on the process performance, Water Sci. Technol., 55, 165, 10.2166/wst.2007.351 Mezzari, 2013, Assessment of N2O emission from a photobioreactor treating ammonia-rich swine wastewater digestate, Bioresour. Technol., 149, 327, 10.1016/j.biortech.2013.09.065 Michiels, 2012, Intact brown seaweed (Ascophyllum nodosum) in diets of weaned piglets: effects on performance, gut bacteria and morphology and plasma oxidative status, J. Animal Physiol. Animal Nutrition, 96, 1101, 10.1111/j.1439-0396.2011.01227.x Misselbrook, T.H., Chadwick, D.R., Gilhespy, S.L., Chambers, B.J., Smith, K.A., Williams, J., Dragosits, U., 2010. Inventory of ammonia emissions from UK agriculture 2009. Defra Contract AC0112. Möller, 2015, Effects of anaerobic digestion on soil carbon and nitrogen turnover, N emissions, and soil biological activity. A review, Agronomy Sustainable Develop., 35, 1021, 10.1007/s13593-015-0284-3 Möller, 2012, Effects of anaerobic digestion on digestate nutrient availability and crop growth: A review, Eng. Life Sci., 12, 242, 10.1002/elsc.201100085 Monson, K.D., Esteves, S.R., Guwy, A.J., Dinsdale, R.M., 2007. Anaerobic Digestion of Biodegradable Municipal Wastes – A Review, University of Glamorgan ISBN 978-1-84054-156-5. Mulbry, 2005, Recycling of manure nutrients: use of algal biomass from dairy manure treatment as a slow release fertilizer, Bioresour. Technol., 96, 451, 10.1016/j.biortech.2004.05.026 Nakagawa, 1997, Effect of dietary algae on improvement of lipid metabolism in fish, Biomed. Pharmacother., 51, 345, 10.1016/S0753-3322(97)88053-5 Nath, 2012, Dietary supplementation with the microalgae Parietochloris incisa increases survival and stress resistance in guppy (Poecilia reticulata) fry, Aquac. Nutr., 18, 167, 10.1111/j.1365-2095.2011.00885.x National Non-Food Crops Centre (NNFCC), 2010. Anaerobic Digestion Economic Assessment Tool, Version 2.2 dated July 2010. Available at: http://www.nnfcc.co.uk/publications/tool-ad-cost-calculator. Nicholson, 2013, An enhanced software tool to support better use of manure nutrients: MANNER-NPK, Soil Use Manag., 29, 473, 10.1111/sum.12078 Nkoa, 2014, Agricultural benefits and environmental risks of soil fertilization with anaerobic digestates: a review, Agron. Sustainable Dev., 34, 473, 10.1007/s13593-013-0196-z Oliveira, 2016, The potential use of shear viscosity to monitor polymer conditioning of sewage sludge digestates, Water Res., 105, 320, 10.1016/j.watres.2016.08.007 Orth, 2010, What is flux balance analysis?, Nat. Biotechnol., 28, 245, 10.1038/nbt.1614 Osborne, 2013, Variation in the global-scale impacts of climate change on crop productivity due to climate model uncertainty and adaptation, Agric. For. Meteorol., 170, 183, 10.1016/j.agrformet.2012.07.006 Oswald, 1953, Algae symbiosis in oxidation ponds: III. Photosynthetic oxygenation, Sewage Ind. Wastes, 25, 692 Passanha, 2013, Increasing polyhydroxyalkanoate (PHA) yields from Cupriavidus necator by using filtered digestate liquors, Bioresour. Technol., 147, 345, 10.1016/j.biortech.2013.08.050 Perez-Garcia, 2011, Heterotrophic cultures of microalgae: metabolism and potential products, Water Res., 45, 11, 10.1016/j.watres.2010.08.037 Provenzano, 2011, Qualitative characterization and differentiation of digestates from different biowastes using FTIR and fluorescence spectroscopies, J. Environ. Protection, 2, 83, 10.4236/jep.2011.21009 Rehl, 2011, Life cycle assessment of biogas digestate processing technologies, Resour. Conserv. Recycl., 56, 92, 10.1016/j.resconrec.2011.08.007 Rodhe, 2015, Greenhouse gas emissions from storage and field application of anaerobically digested and non-digested cattle slurry, Agric. Ecosyst. Environ., 199, 358, 10.1016/j.agee.2014.10.004 Scaglia, 2017, The anaerobic digestion process capability to produce biostimulant: the case study of the dissolved organic matter (DOM) vs. auxin-like property, Sci. Total Environ., 589, 36, 10.1016/j.scitotenv.2017.02.223 Schipper, 2014, Phosphorus: too Big to Fail, Eur. J. Inorg. Chem., 2014, 1567, 10.1002/ejic.201400115 Schlarb-Ridley, B., Parker, B., 2013. A UK roadmap for algal technologies. Report for the National Environmental Research Council (NERC) Technology Strategy Board (TSB) Algal Bioenergy-Special Interest Group (AB-SIG). Sharma, 2012, Role of algae and cyanobacteria in sustainable agriculture system, Wudpecker J. Agric. Res, 1, 381 Sheeman, J., Dunahay T., Benemann, J., Roessler, P., 1998. A Look Back at the U.S. Department of Energy’s Aquatic Species Program—Biodiesel from Algae. National Renewable Energy Laboratory. NREL/TP-580-24190. Sheikhzadeh, 2012, Effects of Haematococcus pluvialis supplementation on antioxidant system and metabolism in rainbow trout (Oncorhynchus mykiss), Fish Physiol. Biochem., 38, 413, 10.1007/s10695-011-9519-7 Sigurnjak, 2017, Fertilizer performance of liquid fraction of digestate as synthetic nitrogen substitute in silage maize cultivation for three consecutive years, Sci. Total Environ., 599, 1885, 10.1016/j.scitotenv.2017.05.120 Silkina, 2017, Formulation and utilisation of spent anaerobic digestate fluids for the growth and product formation of single cell algal cultures in heterotrophic and autotrophic conditions, Bioresour. Technol., 244, 1445, 10.1016/j.biortech.2017.05.133 Singh, 2017, Uncovering potential applications of cyanobacteria and algal metabolites in biology, agriculture and medicine: current status and future prospects, Fronti. Microbiol., 8, 515, 10.3389/fmicb.2017.00515 Sivakumar, 2012, Integrated green algal technology for bioremediation and biofuel, Bioresour. Technol., 107, 1, 10.1016/j.biortech.2011.12.091 Skrede, 2011, Evaluation of microalgae as sources of digestible nutrients for monogastric animals, J. Animal Feed Sci., 20, 10.22358/jafs/66164/2011 Smith, 2001, Nutrient losses by surface run-off following the application of organic manures to arable land. 1. Nitrogen, Environ. Pollut., 112, 41, 10.1016/S0269-7491(00)00097-X Smith, 2001, Nutrient losses by surface run-off following the application of organic manures to arable land. 2. Phosphorus, Environ. Pollut., 112, 53, 10.1016/S0269-7491(00)00098-1 Spolaore, 2006, Commercial applications of microalgae, J. Biosci. Bioeng., 101, 87, 10.1263/jbb.101.87 Sprague, 2015, Replacement of fish oil with a DHA-rich algal meal derived from Schizochytrium sp. on the fatty acid and persistent organic pollutant levels in diets and flesh of Atlantic salmon (Salmo salar, L.) post-smolts, Food Chem., 185, 413, 10.1016/j.foodchem.2015.03.150 Steffen, 2015, Planetary boundaries: Guiding human development on a changing planet, Science, 347, 1259855, 10.1126/science.1259855 Steinfeld, H., Gerber, P., Wassenaar, T., Castel, V., Rosales, M., de Haan, C., 2007. Livestock’s long shadow. Environmental issues and options. FAO, Rom. Styles, 2018, Climate mitigation by dairy intensification depends on intensive use of spared grassland, Global Change Biol., 24, 681, 10.1111/gcb.13868 Styles, 2016, Environmental balance of the of the UK biogas sector: an evaluation by consequential life cycle assessment, Sci. Total Environ., 560–561, 241, 10.1016/j.scitotenv.2016.03.236 Styles, 2018, Life cycle assessment of biofertilizer production and use compared with conventional liquid digestate management, Environ. Sci. Technol., 10.1021/acs.est.8b01619 Suganya, 2016, Macroalgae and microalgae as a potential source for commercial applications along with biofuels production: a biorefinery approach, Renew. Sustain. Energy Rev., 55, 909, 10.1016/j.rser.2015.11.026 Sutton, 2011, Too much of a good thing, Nature, 472, 159, 10.1038/472159a Tilman, 2014, Global diets link environmental sustainability and human health, Nature, 515, 518, 10.1038/nature13959 Tonini, 2012, Bioenergy production from perennial energy crops: a consequential LCA of 12 bioenergy scenarios including land use changes, Environ. Sci. Technol., 46, 13521, 10.1021/es3024435 Turner, 2002, Effects of Ascophyllum nodosum extract on growth performance and immune function of young pigs challenged with Salmonella typhimurium 1, J. Anim. Sci., 80, 1947, 10.2527/2002.8071947x Uggetti, 2014, Anaerobic digestate as substrate for microalgae culture: the role of ammonium concentration on the microalgae productivity, Bioresour. Technol., 152, 437, 10.1016/j.biortech.2013.11.036 Vigani, 2015, Food and feed products from micro-algae: Market opportunities and challenges for the EU, Trends Food Sci. Technol., 42, 81, 10.1016/j.tifs.2014.12.004 Van Den Hende, 2014, Up-scaling aquaculture wastewater treatment by microalgal bacterial flocs: from lab reactors to an outdoor raceway pond, Biores. Technol., 159, 342, 10.1016/j.biortech.2014.02.113 Van der Werf, 2009, CO2 emissions from forest loss, Nat. Geosci., 2, 737, 10.1038/ngeo671 Vaneeckhaute, 2013, Ecological and economic benefits of the application of bio-based mineral fertilizers in modern agriculture, Biomass Bioenergy, 49, 239, 10.1016/j.biombioe.2012.12.036 Vázquez-Rowe, 2015, Environmental assessment of digestate treatment technologies using LCA methodology, Waste Manage., 43, 442, 10.1016/j.wasman.2015.05.007 Vulsteke, 2017, Economic feasibility of microalgal bacterial floc production for wastewater treatment and biomass valorization: A detailed up-to-date analysis of up-scaled pilot results, Bioresour. Technol., 224, 118, 10.1016/j.biortech.2016.11.090 Walsh, 2012, Replacing inorganic fertilizer with anaerobic digestate may maintain agricultural productivity at less environmental cost, J. Plant Nutr. Soil Sci., 175, 840, 10.1002/jpln.201200214 Wang, 2010, Anaerobic digested dairy manure as a nutrient supplement for cultivation of oil-rich green microalgae Chlorella sp, Bioresour. Technol., 101, 2623, 10.1016/j.biortech.2009.10.062 Weidema, 2000, Avoiding co-product allocation in life-cycle assessment, J. Ind. Ecol., 4, 11, 10.1162/108819800300106366 Weidema, 2010, Avoiding allocation in life cycle assessment revisited, J. Ind. Ecol., 14, 192, 10.1111/j.1530-9290.2010.00236.x Williams, 2013, Monitoring methanogenic population dynamics in a full-scale anaerobic digester to facilitate operational management, Bioresour. Technol., 140, 234, 10.1016/j.biortech.2013.04.089 Withers, 2002, Agricultural nutrient inputs to rivers and groundwaters in the UK: policy, environmental management and research needs, Sci. Total Environ., 282, 9, 10.1016/S0048-9697(01)00935-4 Wollenberg, 2016, Reducing emissions from agriculture to meet the 2 °C target, Glob. Change Biol., 22, 3859, 10.1111/gcb.13340 WRAP, 2012. Using quality anaerobic digestate to benefit crops 1–12. Available from http://www.wrap.org.uk/sites/files/wrap/Using%20quality%20digestate %20to%20benefit%20crops.pdf. Accessed 13/06/18. Xu, 2015, Nutrient removal and biogas upgrading by integrating freshwater algae cultivation with piggery anaerobic digestate liquid treatment, Appl. Microbiol. Biotechnol., 99, 6493, 10.1007/s00253-015-6537-x Yaakob, 2014, An overview: biomolecules from microalgae for animal feed and aquaculture, J. Biol. Res. Thessaloniki, 21, 6, 10.1186/2241-5793-21-6 Zamagni, 2012, Lights and shadows in consequential LCA, Int. J. Life Cycle Assess., 17, 904, 10.1007/s11367-012-0423-x Zheng, 2009, Carbon and nitrogen nutrient balance signalling in plants, Plant Signalling Behav., 4, 584, 10.4161/psb.4.7.8540 Zuliani, 2016, Microalgae cultivation on anaerobic digestate of municipal wastewater, sewage sludge and agro-waste, Int. J. Mol. Sci., 17, 1692, 10.3390/ijms17101692 Zuñiga, 2016, Genome-scale metabolic model for the green alga Chlorella vulgaris UTEX 395 accurately predicts phenotypes under autotrophic, heterotrophic, and mixotrophic growth conditions, Plant Physiol., 00593