JWARP  Vol.11 No.7 , July 2019
Impact on Wastewater Quality of Biopellets Composed of Chlorella vulgaris and Aspergillus niger and Lipid Content in the Harvested Biomass
Abstract: Filamentous fungi can be used to form easily harvested pellets with microalgae (fungal-assisted algal harvesting) in order to advance the sustainability and economic feasibility of wastewater treatment using microalgae. In experiments employing the microalga Chlorella vulgaris and using the filamentous fungus Aspergillus niger for harvesting, this study investigated the effect on water quality and the quantity and quality of lipids in the biomass produced. Major reductions in the concentrations of total nitrogen, ammonium-nitrogen and total phosphorus were observed after addition of the fungal spores (day 5) and during fungal growth and entrapment of the algal cells. At harvest (day 8), the decrease in total nitrogen was 47.4% ± 18.4% of the initial value, corresponding to a reduction of 41.9 ± 17.1 mg·nitrogen·L-1. For total phosphorus, the decrease was 94.4% ± 3.2%, corresponding to a reduction of 6.4 ± 0.2 mg·phosphorus·L-1. A significant decrease in concentration of the micropollutant diclofenac was observed at harvest, to 5.1 ± 4.0 μg·L-1 compared with an initial concentration of 9.5 ± 0.6 μg·L-1. A significant decrease in total lipids in the biomass was observed after fungal-assisted algal harvesting, from 58.7 ± 2.7 μg·mg-1 at day 5 (algal biomass only) to 34.2 ± 2.7 μg·mg-1 at day 8 (fungal-algal biomass). However, because of high biomass production, the amount of lipids produced per litre of wastewater increased from 5.6 ± 0.9 mg on day 5 to 20.6 ± 4.9 mg on day 8.
Cite this paper: Hultberg, M. , Bodin, H. and Birgersson, G. (2019) Impact on Wastewater Quality of Biopellets Composed of Chlorella vulgaris and Aspergillus niger and Lipid Content in the Harvested Biomass. Journal of Water Resource and Protection, 11, 831-843. doi: 10.4236/jwarp.2019.117050.

[1]   Oswald, W.J. (1988) Microalgae and Wastewater Treatment. In: Borowitzka, M.A., Borowitzka, L.J., Eds, Microalgal Biotechnology, Cambridge University Press, Cambridge, 305-328.

[2]   Islam, M.A., Magnusson, M., Brown, R.J., Ayoko, G.A., Nabi, M.N. and Heimann, K. (2013) Microalgal Species Selection for Biodiesel Production Based on Fuel Properties Derived from Fatty Acid Profiles. Energies, 6, 5676-5702.

[3]   Singh, G. and Patidar, S.K. (2018) Microalgal Harvesting Techniques: A Review. Journal of Environmental Management, 217, 499-508.

[4]   Zhang, J. and Hu, B. (2012) A Novel Method to Harvest Microalgae via Co-Culture of Filamentous Fungi to Form Cell Pellets. Bioresource Technology, 114, 529-535.

[5]   Bhattacharya, A., Mathur, M., Kumar, P., Kumar Prajapati, S. and Malik, A. (2017) A Rapid Method for Fungal Assisted Algal Flocculation: Critical Parameters and Mechanism Insights. Algal Research, 21, 42-51.

[6]   Hollender, J., Zimmermann, S.G., Koepke, S., Krauss, M., Mcardell, C.S., Oer, C., Singer, H., Von Guten, U. and Siegrist, H. (2009) Elimination of Organic Micropollutants in a Municipal Wastewater Treatment Plant Upgraded with a Full-Scale Post-Ozonation Followed by Sand Filtration. Environmental Science & Technology, 43, 7862-7869.

[7]   Loos, R., Gawlik, B.M., Locoro, G., Rimaviciute, E., Contini, S. and Bidoglio, G. (2009) EU-Wide Survey of Polar Organic Persistent Pollutants in European River Waters. Environmental Pollution, 157, 561-568.

[8]   Loos, R., Locoro, G., Comero, S., Contini, S., Schwesig, D., Werres, F., Balsaa, P., Gans, O., Weiss, S., Blaha, L., Bolchi, M. and Gawlik, B.M. (2010) Pan-European Survey on the Occurrence of Selected Polar Organic Persistent Pollutants in Ground Water. Water Research, 44, 4115-4126.

[9]   Fomina, M. and Gadd, G.M. (2014) Biosorption: Current Perspectives on Concept, Definition and Application. Bioresource Technology, 160, 3-14.

[10]   Matamoros, V., Gutiérrez, R., Ferrer, I., García, J. and Bayona, J.M. (2015) Capability of Microalgae-Based Wastewater Treatment Systems to Remove Emerging Contaminates: A Pilot-Scale Study. Journal of Hazardous Materials, 288, 34-42.

[11]   Hultberg, M., Bodin, H., Ardal, E. and Asp, H. (2016) Effect of Microalgal Treatments on Pesticides in Water. Environmental Technology, 37, 893-898.

[12]   Mir-Tutsaus, J.A., Parladé, E., Llorca, M., Villagrasa, M., Barceló, D., Rodriguez-Mozaz, S., Martinez-Alonso, M., Gaju, N., Caminal, G. and Sarra, M. (2017) Pharmaceutical Removal and Microbial Community Assessment in a Continuous Fungal Treatment of Non-Sterile Real Hospital Wastewater after a Coagulation-Flocculation Pretreatment. Water Research, 116, 65-75.

[13]   Barbosa, M.O., Moreira, N.F.F., Ribeiro, A.R., Pereira, M.F.R. and Silva, A.M.T. (2016) Occurrence and Removal of Organic Micropollutants: An Overview of the Watch List of EU Decision 2015/495. Water Research, 94, 257-279.

[14]   OECD (2001) OECD Guidelines for Testing of Chemicals. Simulation Test-Aerobic Sewage Treatment 303A.

[15]   Gago-Ferrero, P., Gros, M., Ahrens, L. and Wiberg, K. (2017) Impact of on-Site, Small and Large Scale Wastewater Treatment Facilities on Levels and Fate of Pharmaceuticals, Personal Care Products, Artificial Sweeteners, Pesticides, and Perfluoroalkyl Substances in Recipient Waters. Science of The Total Environment, 601-602, 1289-1297.

[16]   Hultberg, M., Olsson, L.E., Birgersson, G., Gustafsson, S. and Sievertsson, B. (2016) Microalgal Growth in Municipal Wastewater Treated in an Anaerobic Moving Bed Biofilm Reactor. Bioresource Technology, 207, 19-23.

[17]   Ummalyma, S.B., Gnansounou, E., Sukumaran, R.K., Sindhu, R., Pandey, A. and Sahoo, D. (2017) Bioflocculation: An Alternative Strategy for Harvesting of Microalgae—An Overview. Bioresource Technology, 242, 227-235.

[18]   Li, Y., Xu, Y., Liu, L., Li, Yan, Y., Chen, T., Zheng, T. and Wang, H. (2017) Flocculation Mechanism of Aspergillus niger on Harvesting of Chlorella Vulgaris Biomass. Algal Research, 25, 402-412.

[19]   Larsdotter, K., La Cour Jansen, J. and Dalhammar, G. (2007) Biological Mediated Phosphorus Precipitation in Wastewater Treatment with Microalgae. Environmental Technology, 28, 953-960.

[20]   Yakout, S.M. (2014) Review on the Bioremediation by Aspergillus niger. Journal of Pure and Applied Microbiology, 8, 109-116.

[21]   Zhang, J. and Elser, J.J. (2017) Carbon:nitrogen: Phosphorus Stoichiometry in Fungi: A Meta-Analysis. Frontiers in Microbiology, 8, 1281.

[22]   Cleuvers, M. (2004) Mixture Toxicity of the Anti-Inflammatory Drugs Diclofenac, Ibuprofen, Naproxen, and Acetylsalicylic Acid. Ecotoxicology and Environmental Safety, 59, 309-315.

[23]   Paiga, P., Santos, L.H.M.L.M., Ramos, S., Jorge, S., Silva, J.G. and Delerue-Matos, C. (2016) Presence of Pharmaceuticals in the Lis River (Portugal): Source, Fate and Seasonal Variation. Science of the Total Environment, 573, 164-177.

[24]   Rosales, E., Diaz, S., Pazos, M. and Sanromán, M.A. (2019) Comprehensive Strategy for the Degradation of Anti-Inflammatory Drug Diclofenac by Different Advanced Oxidation Processes. Separation and Purification Technology, 208, 130-141.

[25]   de Wilt, A., Butkovskyi, A., Tuantet, K., Leal, L.H., Fernandes, T.V., Langenhoff, A. and Zeeman, G. (2016) Micropollutant Removal in an Algal Treatment System Fed with Source Separated Wastewater Streams. Journal of Hazardous Materials, 304, 84-92.

[26]   Lucas, D., Castellet-Rovira, F., Villagrasa, M., Badia-Fabregat, M., Barceló, D., Vicent, T., Caminal, G., Sarra, M. and Rodriguez-Mozaz, S. (2018) The Role of Sorption Processes in the Removal of Pharmaceuticals by Fungal Treatment of Wastewater. Science of the Total Environment, 610-611, 1147-1153.

[27]   Viswanath, B., Rajesh, B., Janardhan, A., Kumar, A.P. and Narasimha, G. (2014) Fungal Laccases and Their Application in Bioremediation. Enzyme Research, 2014, Article ID: 163242.

[28]   Hahn, V., Meister, M., Hussy, S., Cordes, A., Enderle, G., Saningong, A. and Schauer, F. (2018) Enhanced Laccase-Mediated Transformation of Diclofenac and Fufenamic Acid in the Presence of Bisphenol A and Testing of an Enzymatic Membrane Reactor. AMB Express, 8, 28.

[29]   Tamayo Ramos, J.A., Barends, S., Verhaert, R.M.D. and de Graff, L.H. (2011) The Aspergillus niger Multicopper Oxidase Family: Analysis and Overexpression of Laccase Like Encoding Genes. Microbial Cell Factories, 10, 78.

[30]   Hultberg, M. and Bodin, H. (2018) Effects of Fungal-Assisted Algal Harvesting through Biopellet Formation on Pesticides in Water. Biodegradation, 29, 557-565.

[31]   Frisvad, J.C., Moller, L.L.H., Larsen, T.O., Kumar, R. and Arnau, J. (2018) Safety of the Fungal Workhorses of Industrial Biotechnology: Update on the Mycotoxin and Secondary Metabolites Potential of Aspergillus niger, Aspergillus oryzae, and Trichoderma reesei. Applied Microbiology and Biotechnology, 102, 9481-9515.

[32]   Sharma, K.K., Schuhmann, H. and Schenk, P.M. (2012) High Lipid Induction in Microalgae for Biodiesel Production. Energies, 5, 1532-1553.

[33]   Singh, A. (1992) Lipid Accumulation by a Cellolytic Strain of Aspergillus niger. Experientia, 48, 234-236.

[34]   Wrede, D., Taha, M., Miranda, A.F., Kadali, K., Stevenson, T., Ball, A.S. and Mouradov, A. (2014) Co-Cultivation of Fungal and Microalgal Cells as an Efficient System for Harvesting Microalgal Cells, Lipid Production and Wastewater Treatment. PLoS ONE, 9, e113497.

[35]   Hempel, N., Petric, I. and Behrendt, F. (2012) Biomass Productivity and Productivity of Fatty Acids and Amino Acids of Microalgae Strains as Key Characteristics of Suitability for Biodiesel Production. Journal of Applied Phycology, 24, 1407-1418.

[36]   Gushina, L.A. and Harwood, J.L. (2006) Lipids and lipid metabolism in eukaryotic algae. Progress in Lipid Research, 45, 160-185.

[37]   Chen, J., Leng, L., Ye, C., Lu, Q., Addy, M., Wang, J., Liu, J., Chen, P., Ruan, R. and Zhou, W. (2018) A Comparative Study between Fungal Pellet- and Spore-Assisted Microalgae Harvesting Methods for Algae Bioflocculation. Bioresource Technology, 259, 181-190.