Winery wastewater treatment by microalgae Chlorella sorokiniana and characterization of the produced biomass for value-added products.

Eirini Zkeri, Maria Mastori, Argyri Xenaki, Evangelia Kritikou, Marios Kostakis, Marilena Dasenaki, Niki Maragou, Michail S Fountoulakis, Nikolaos S Thomaidis, Athanasios S Stasinakis
Author Information
  1. Eirini Zkeri: Department of Environment, University of the Aegean, 81100, Mytilene, Greece.
  2. Maria Mastori: Department of Environment, University of the Aegean, 81100, Mytilene, Greece.
  3. Argyri Xenaki: Department of Environment, University of the Aegean, 81100, Mytilene, Greece.
  4. Evangelia Kritikou: Laboratory of Analytical Chemistry, Department of Chemistry, National and Kapodistrian University of Athens, 15771, Athens, Greece.
  5. Marios Kostakis: Laboratory of Analytical Chemistry, Department of Chemistry, National and Kapodistrian University of Athens, 15771, Athens, Greece.
  6. Marilena Dasenaki: Laboratory of Food Chemistry, Department of Chemistry, National and Kapodistrian University of Athens, Panepistimiopolis Zographou, 15771, Athens, Greece.
  7. Niki Maragou: Laboratory of Analytical Chemistry, Department of Chemistry, National and Kapodistrian University of Athens, 15771, Athens, Greece.
  8. Michail S Fountoulakis: Department of Environment, University of the Aegean, 81100, Mytilene, Greece.
  9. Nikolaos S Thomaidis: Laboratory of Analytical Chemistry, Department of Chemistry, National and Kapodistrian University of Athens, 15771, Athens, Greece.
  10. Athanasios S Stasinakis: Department of Environment, University of the Aegean, 81100, Mytilene, Greece. astas@env.aegean.gr. ORCID

Abstract

The microalgae Chlorella sorokiniana was used for the treatment of winery wastewater (WWW). Batch experiments were initially conducted to investigate how biomass acclimatization in different media, dilution of wastewater, and addition of ammonium nitrogen (NH-N) affect the growth of microalgae and the removal of major pollutants. Afterwards, two sequencing batch reactor (SBR) systems were tested applying different configurations and hydraulic retention times. The biomass collected at the end of the experiments was characterized for proteins, lipids, carbohydrates, amino acid profile, and the existence of lutein, ��-carotene, chlorophyll a, and tocopherols. Batch experiments showed that Chlorella sorokiniana acclimatization to urban wastewater enhanced the removal of NH-N and total phosphorus (TP). The operation of a two-stage SBR system achieved COD and NH-N removal equal to 85��������9% and 91��������20%, respectively, while the use of a single-stage system feeding with anaerobically pretreated WWW resulted to COD and NH-N removal of 78��������9% and 95��������9%, respectively. Analyses of biomass showed higher protein content (up to 58.8%) in batch experiments with NH-N addition as well as in SBR experiments. The cultivation of microalgae under SBR conditions enhanced the production of pigments and tocopherols. The maximum concentrations of 1075 mg kg, 45.5 mg kg, and 131.2 mg kg were achieved for lutein, ��-carotene, and tocopherols, respectively, in the one-stage system. Our findings suggested that Chlorella sorokiniana cultivation in WWW not only removed nutrients from WWW but also could potentially serve for the production of value-added ingredients used in food industry, cosmetics, and animal feedstock.

Keywords

References

  1. AOAC International (2002) AOAC Official Method 2001.11: Protein (crude) in animal feed, forage (plant tissue), grain and oilseeds
  2. APHA (2005) Standard methods for the examination of water and wastewater, 21st ed., 507 American Public Health Association, USA
  3. Asadi P, Rad HA, Qaderi F (2019) Comparison of Chlorella vulgaris and Chlorella sorokiniana pa.91 in post treatment of dairy wastewater treatment plant effluents. Environ Sci Pollut Res 26:29473���29489. https://doi.org/10.1007/s11356-019-06051-8 [DOI: 10.1007/s11356-019-06051-8]
  4. D���oca MGM, Vi��gas CV, Lem��es JS, Miyasaki EK, Mor��n-Villarreyes JA, Primel EG, Abreu PC (2011) Production of FAMEs from several microalgal lipidic extracts and direct transesterification of the Chlorella pyrenoidosa. Biomass Bioenerg 35:1533���1538. https://doi.org/10.1016/j.biombioe.2010.12.047 [DOI: 10.1016/j.biombioe.2010.12.047]
  5. Davididou K, Frontistis Z (2021) Advanced oxidation processes for the treatment of winery wastewater: a review and future perspectives. J Chem Technol Biotechnol 96:2436���2450. https://doi.org/10.1002/jctb.6772 [DOI: 10.1002/jctb.6772]
  6. Durmaz Y (2007) Vitamin E (��-tocopherol) production by the marine microalgae Nannochloropsis oculata (Eustigmatophyceae) in nitrogen limitation. Aquaculture 272:717���722. https://doi.org/10.1016/j.aquaculture.2007.07.213 [DOI: 10.1016/j.aquaculture.2007.07.213]
  7. Ganeshkumar V, Subashchandrabose SR, Dharmarajan R, Venkateswarlu K, Naidu R, Megharaj M (2018) Use of mixed wastewaters from piggery and winery for nutrient removal and lipid production by Chlorella sp. MM3. Biores Technol 256:254���258. https://doi.org/10.1016/j.biortech.2018.02.025 [DOI: 10.1016/j.biortech.2018.02.025]
  8. Gatidou G, Anastopoulou P, Aloupi M, Stasinakis AS (2019) Growth inhibition and fate of benzotriazoles in Chlorella sorokiniana cultures. Sci Total Environ 663:580���586. https://doi.org/10.1016/j.scitotenv.2019.01.384 [DOI: 10.1016/j.scitotenv.2019.01.384]
  9. Hansen J, M��ller I (1975) Percolation of starch and soluble carbohydrates from plant tissue for quantitative determination with anthrone. Anal Biochem 68:87���94. https://doi.org/10.1016/0003-2697(75)90682-X [DOI: 10.1016/0003-2697(75)90682-X]
  10. Idenyi NJ, Eya CJ, Nwankwegu SA, Nwoba GE (2022) Aquaculture sustainability through alternative dietary ingredients: microalgal value-added products. Eng Microbiol 2:100049. https://doi.org/10.1016/j.engmic.2022.100049 [DOI: 10.1016/j.engmic.2022.100049]
  11. Iliopoulou A, Zkeri E, Panara A, Dasenaki M, Fountoulakis MS, Thomaidis NS, Stasinakis AS (2022) Treatment of different dairy wastewater with Chlorella sorokiniana: removal of pollutants and biomass characterization. J Chem Technol Biotechnol 97:3193���3201. https://doi.org/10.1002/jctb.7188 [DOI: 10.1002/jctb.7188]
  12. Imchen T, Singh SK (2023) Marine algae colorants: antioxidant, anti-diabetic properties and applications in food industry. Algal Res 69:102898. https://doi.org/10.1016/j.algal.2022.102898 [DOI: 10.1016/j.algal.2022.102898]
  13. Ioannou LA, Li Puma G, Fatta-Kassinos D (2015) Treatment of winery wastewater by physicochemical, biological and advanced processes: a review. J Hazard Mater 286:343���368. https://doi.org/10.1016/j.jhazmat.2014.12.043 [DOI: 10.1016/j.jhazmat.2014.12.043]
  14. Kotoula D, Iliopoulou A, Irakleous-Palaiologou E, Gatidou G, Aloupi M, Antonopoulou P, Fountoulakis MS, Stasinakis AS (2020) Municipal wastewater treatment by combining in series microalgae Chlorella sorokiniana and macrophyte Lemna minor: preliminary results. J Clean Prod 271:122704. https://doi.org/10.1016/j.jclepro.2020.122704 [DOI: 10.1016/j.jclepro.2020.122704]
  15. Latessa SH, Hanley L, Tao W (2023) Characteristics and practical treatment technologies of winery wastewater: a review for wastewater management at small wineries. J Environ Manage 342:118343. https://doi.org/10.1016/j.jenvman.2023.118343 [DOI: 10.1016/j.jenvman.2023.118343]
  16. Lee JC, Joo JH, Chun BH, Moon K, Song SH, Kim YJ, Lee SM, Lee AH (2022) Isolation and screening of indigenous microalgae species for domestic and livestock wastewater treatment, biodiesel production, and carbon sequestration. J Environ Manage 318:115648. https://doi.org/10.1016/j.jenvman.2022.115648 [DOI: 10.1016/j.jenvman.2022.115648]
  17. Louren��o-Lopes C, Fraga-Corral M, Garcia-Perez P, Carreira-Casais A, Silva A, Simal-Gandara J, Prieto MA (2022) A HPLC-DAD method for identifying and estimating the content of fucoxanthin, ��-carotene and chlorophyll a in brown algal extracts. Food Chemistry Advances 1:100095. https://doi.org/10.1016/j.focha.2022.100095 [DOI: 10.1016/j.focha.2022.100095]
  18. Mader AE, Holtman GA, Welz PJ (2022) Treatment wetlands and phyto-technologies for remediation of winery effluent: challenges and opportunities. Sci Total Environ 807:150544. https://doi.org/10.1016/j.scitotenv.2021.150544 [DOI: 10.1016/j.scitotenv.2021.150544]
  19. Makaroglou G, Marakas H, Fodelianakis S, Axaopoulou VA, Koumi I, Kalogerakis N, Gikas P (2021) Optimization of biomass production from Stichococcous sp. biofilms coupled to wastewater treatment. Biochem Eng J 169:107964. https://doi.org/10.1016/j.bej.2021.107964 [DOI: 10.1016/j.bej.2021.107964]
  20. Mamais D, Noutsopoulos C, Dimopoulou A, Stasinakis A, Lekkas TD (2015) Wastewater treatment process impact on energy savings and greenhouse gas emissions. Water Sci Technol 71:303���308. https://doi.org/10.2166/wst.2014.521 [DOI: 10.2166/wst.2014.521]
  21. March��o L, Fernandes JR, Sampaio A, Peres JA, Tavares PB, Lucas MS (2021) Microalgae and immobilized TiO/UV-a LEDs as a sustainable alternative for winery wastewater treatment. Water Res 203:117464. https://doi.org/10.1016/j.watres.2021.117464 [DOI: 10.1016/j.watres.2021.117464]
  22. Marshall JD (1986) Drought and shade interact to cause fine-root mortality in Douglas-fir seedlings. Plant Soil 91:51���60 [DOI: 10.1007/BF02181818]
  23. Martakos I, Kostakis M, Dasenaki M, Thomaidis N (2019) Simultaneous determination of pigments, tocopherols, and squalene in Greek olive oils: a study of the influence of cultivation and oil-production parameters. Foods 9:31. https://doi.org/10.3390/foods9010031 [DOI: 10.3390/foods9010031]
  24. Mastoras P, Zkeri E, Panara A, Dasenaki ME, Maragou NC, Vakalis S, Fountoulakis M, Thomaidis NS, Stasinakis AS (2023) Application of a pilot-scale solar still for wine lees management: characterization of by-products and valorization potential. J Environ Chem Eng 11:111227. https://doi.org/10.1016/j.jece.2023.111227 [DOI: 10.1016/j.jece.2023.111227]
  25. Matsukawa R, Hotta M, Masuda Y, Chihara M, Karube I (2000) Antioxidants from carbon dioxide fixing Chlorella sorokiniana. J Appl Phycol 12:263���267. https://doi.org/10.1023/A:1008141414115 [DOI: 10.1023/A]
  26. Muhammad G, Butler OT, Chen B, Lv Y, Xiong W, Zhao X, Solovchenko EA, Zhao A, Mofijur M, Xu J, Alam AMd (2024) Sustainable production of lutein���an underexplored commercially relevant pigment from microalgae. Biomass Conversion and Biorefinery 14:7255���7276. https://doi.org/10.1007/s13399-022-03349-5 [DOI: 10.1007/s13399-022-03349-5]
  27. Napolitano G, Fasciolo G, Salbitani G, Venditti P (2020) Chlorella sorokiniana dietary supplementation increases antioxidant capacities and reduces ROS release in mitochondria of hyperthyroid rat liver. Antioxidants 9:883. https://doi.org/10.3390/antiox9090883 [DOI: 10.3390/antiox9090883]
  28. OECD (2011) Guidelines for the testing of chemicals, Section 2, Test No. 201: Freshwater Alga and Cyanobacteria, Growth Inhibition Test, 1���25. https://www.oecdilibrary.org/environment/test-no-201-alga-growth-inhibition-test_9789264069923-en . Accessed 21 Sep 2023
  29. Ort��z-S��nchez E, Guill��n-Garc��s RA, Morales-Arrieta S, Okoye PU, Olvera-Vergas H, Sebastian PJ, Arias DM (2023) Cultivation of carbohydrate-rich microalgae with great settling properties using cooling tower wastewater. Environ Sci Pollut Res (in Press). https://doi.org/10.1007/s11356-023-28432-w [DOI: 10.1007/s11356-023-28432-w]
  30. Papastavropoulou K, Koupa A, Kritikou E, Kostakis M, Proestos C (2022) Edible insects: benefits and potential risk for consumers and the food industry. Biointerface Res Appl Chem 12:5131���5149. https://doi.org/10.33263/BRIAC124.51315149 [DOI: 10.33263/BRIAC124.51315149]
  31. Salbitani G, Carfagna S (2021) Ammonium utilization in microalgae: a sustainable method for wastewater treatment. Sustainability 13:956. https://doi.org/10.3390/su13020956 [DOI: 10.3390/su13020956]
  32. Spennati E, Mirizadeh S, Casazza AA, Solisio C, Converti A (2021) Chlorella vulgaris and Arthrospira platensis growth in a continuous membrane photobioreactor using industrial winery wastewater. Algal Res 60:102519. https://doi.org/10.1016/j.algal.2021.102519 [DOI: 10.1016/j.algal.2021.102519]
  33. Spennati E, Casazza AA, Converti A, Padula MP, Dehghani F, Perego P, Valtchev P (2022) Winery waste valorisation as microalgae culture medium: a step forward for food circular economy. Sep Purif Technol 293:121088. https://doi.org/10.1016/j.seppur.2022.121088 [DOI: 10.1016/j.seppur.2022.121088]
  34. Thiex NJ, Manson H, Anderson S, Persson JA (2002) Determination of crude protein in animal feed, forage, grain, and oilseeds by using block digestion with a copper catalyst and steam distillation into boric acid: collaborative study. J AOAC Int 85:309���317. https://doi.org/10.1093/jaoac/85.2.309 [DOI: 10.1093/jaoac/85.2.309]
  35. 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���193. https://doi.org/10.1016/j.jclepro.2017.02.026 [DOI: 10.1016/j.jclepro.2017.02.026]
  36. Tsolcha ON, Tekerlekopoulou AG, Akratos CS et al (2018) A Leptolyngbya-based microbial consortium for agro-industrial wastewaters treatment and biodiesel production. Environ Sci Pollut Res 25:17957���17966. https://doi.org/10.1007/s11356-018-1989-z [DOI: 10.1007/s11356-018-1989-z]
  37. Yust MM, Pedroche J, Giron-Calle J, Vioque J, Millan F, Alaiz M (2004) Determination of tryptophan by high-performance liquid chromatography of alkaline hydrolysates with spectrophotometric detection. Food Chem 85:317���320. https://doi.org/10.1016/j.foodchem.2003.07.026 [DOI: 10.1016/j.foodchem.2003.07.026]
  38. Zkeri E, Iliopoulou A, Katsara A, Korda A, Aloupi M, Gatidou G, Fountoulakis M, Stasinakis AS (2021) Comparing the use of a two-stage MBBR system with a methanogenic MBBR coupled with a microalgae reactor for medium-strength dairy wastewater treatment. Biores Technol 323:124629. https://doi.org/10.1016/j.biortech.2020.124629 [DOI: 10.1016/j.biortech.2020.124629]

Grants

  1. MIS 5046750/European Regional Development Fund

MeSH Term

Chlorella
Wastewater
Microalgae
Biomass
Waste Disposal, Fluid
Nitrogen

Chemicals

Wastewater
Nitrogen

Word Cloud

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