Plant-based biopolymers: emerging bio-flocculants for microalgal biomass recovery

Abstract

The production of microalgal biomass and its derived products on a large-scale requires the development of sustainable and cost-effective harvesting technologies. Biomass recovery is the primary step in the downstream processing of microalgae and it is a costly operation because microalgal cultures are stable hydrophilic colloidal suspensions. Bio-flocculation has been proposed as a low-cost technology that can be employed to dewater microalgal cultures thus making secondary harvesting methods like filtration and centrifugation less energy-intensive. This review provides an overview of increasing applications of plant-based biopolymers in microalgal biomass harvesting on laboratory and pilot-scale culture volumes. The structure, preparation, and flocculation activity of natural and chemically cationized plant biopolymers are presented. Recent studies demonstrating microalgal biomass recovery have been summarized discussing the advantages and limitations of plant-based biopolymers as emerging bio-flocculants. Future perspectives on biopolymers with special attention to studies reported on nutrient medium recycling, environmental impact assessment and techno-economic analysis of plant-based bio-flocculants facilitated bio-flocculation have been discussed.

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Reprinted with permission from Branyikova et al. (2018)

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References

  1. Agarwal M, Srinivasan R, Mishra A (2001) Study on flocculation efficiency of okra gum in sewage waste water. Macromol Mater Eng 286(9):560–563

    CAS  Article  Google Scholar 

  2. Agarwal M, Rajani S, Mishra A, Rai JSP (2003) Utilization of okra gum for treatment of tannery effluent. Int J Polym Mater 52(11–12):1049–1057

    CAS  Article  Google Scholar 

  3. Ahmad AL, Yasin NM, Derek CJ, Lim JK (2011) Optimization of microalgae coagulation process using chitosan. Chem Eng J 173(3):879–882

    CAS  Article  Google Scholar 

  4. Ajala SO, Alexander ML (2020) Application of bio-based alkali to induce flocculation of microalgae biomass. Biomass Bioenergy 132:105431

    CAS  Article  Google Scholar 

  5. Alam MA, Vandamme D, Chun W, Zhao X, Foubert I, Wang Z, Muylaert K, Yuan Z (2016) Bioflocculation as an innovative harvesting strategy for microalgae. Rev Environ Sci Biotechnol 15(4):573–583

    Article  Google Scholar 

  6. Alenazi M, Hashim KS, Hassan AA, Muradov M, Kot P, Abdulhadi B (2020) Turbidity removal using natural coagulants derived from the seeds of Strychnos potatorum: statistical and experimental approach. In: IOP conference series: materials science and engineering, vol 888, no 1. IOP Publishing, p 012064

  7. Amid BT, Mirhosseini H (2012) Influence of different purification and drying methods on rheological properties and viscoelastic behaviour of durian seed gum. Carbohydr Polym 90(1):452–461

    CAS  Article  Google Scholar 

  8. Anastasakis K, Kalderis D, Diamadopoulos E (2009) Flocculation behaviour of mallow and okra mucilage in treating wastewater. Desalination 249(2):786–791

    CAS  Article  Google Scholar 

  9. Arunkumar P, Sadish Kumar V, Saran S, Bindun H, Devipriya SP (2019) Isolation of active coagulant protein from the seeds of Strychnos potatorum—a potential water treatment agent. Environ Technol 40(12):1624–1632

    CAS  Article  Google Scholar 

  10. Baharuddin NN, Aziz NS, Sohif HN, Karim WA, Al-Obaidi JR, Basiran M (2016) Marine microalgae flocculation using plant: the case of Nannochloropsis oculata and Moringa oleifera. Pak J Bot 48(2):831–842

    CAS  Google Scholar 

  11. Banerjee C, Gupta P, Mishra S, Sen G, Shukla P, Bandopadhyay R (2012) Study of polyacrylamide grafted starch based algal flocculation towards applications in algal biomass harvesting. Int J Biol Macromol 51(4):456–461

    CAS  Article  Google Scholar 

  12. Banerjee C, Ghosh S, Sen G, Mishra S, Shukla P, Bandopadhyay R (2013) Study of algal biomass harvesting using cationic guar gum from the natural plant source as flocculant. Carbohydr Polym 92(1):675–681

    CAS  Article  Google Scholar 

  13. Banerjee C, Ghosh S, Sen G, Mishra S, Shukla P, Bandopadhyay R (2014) Study of algal biomass harvesting through cationic cassia gum, a natural plant-based biopolymer. Bioresour Technol 151:6–11

    CAS  Article  Google Scholar 

  14. Barbosa M, Israel B, Wijffels RH (2010) Microalgae for production of bulk chemicals and biofuels. Biofuels Bioprod Biorefin 4(3):287–295

    Article  CAS  Google Scholar 

  15. Barrado-Moreno MM, Beltran-Heredia J, Martín-Gallardo J (2016a) Microalgae removal with Moringa oleifera. Toxicon 110:68–73

    CAS  Article  Google Scholar 

  16. Barrado-Moreno MM, Beltrán-Heredia J, Martín-Gallardo J (2016b) Removal of Oocystis algae from freshwater by means of tannin-based coagulant. J Appl Phycol 28(3):1589–1595

    CAS  Article  Google Scholar 

  17. Beach ES, Eckelman MJ, Cui Z, Brentner L, Zimmerman JB (2012) Preferential technological and life cycle environmental performance of chitosan flocculation for harvesting of the green algae Neochloris oleoabundans. Bioresour Technol 121:445–449

    CAS  Article  Google Scholar 

  18. Behera B, Balasubramanian P (2019) Natural plant extracts as an economical and eco-friendly alternative for harvesting microalgae. Bioresour Technol 283:45–52

    CAS  Article  Google Scholar 

  19. Behloul S, Zertal A (2020) Cinnamon mucilage as a natural flocculant for dyestuff removal. Int J Environ Anal Chem 24:1–4

    Article  CAS  Google Scholar 

  20. Beltran-Heredia J, Sanchez Martin J (2008) Azo dye removal by Moringa oleifera seed extract coagulation. Color Technol 124(5):310–317

    CAS  Article  Google Scholar 

  21. Beltran-Heredia J, Sanchez-Martín J, Solera-Hernandez C (2009) Anionic surfactants removal by natural coagulant/flocculant products. Ind Eng Chem Res 48(10):5085–5092

    CAS  Article  Google Scholar 

  22. Beltrán-Heredia J, Sánchez-Martín J, Dávila-Acedo MA (2011) Optimization of the synthesis of a new coagulant from a tannin extract. J Hazard Mater 186(2–3):1704–1712

    Article  CAS  Google Scholar 

  23. Bhatia S, Othman Z, Ahmad AL (2006) Palm oil mill effluent pre-treatment using Moringa oleifera seeds as an environmentally friendly coagulant: laboratory and pilot plant studies. J Chem Technol Biotechnol 81(12):1852–1858

    CAS  Article  Google Scholar 

  24. Blockx J, Verfaillie A, Eyley S, Deschaume O, Bartic C, Muylaert K, Thielemans W (2019) Cationic cellulose nanocrystals for flocculation of microalgae: effect of degree of substitution and crystallinity. ACS Appl Nano Mater 2(6):3394–3403

    CAS  Article  Google Scholar 

  25. Bouatay F, Mhenni F (2014) Use of the cactus cladodes mucilage (Opuntia Ficus Indica) as an eco-friendly flocculant: process development and optimization using statical analysis. Int J Environ Res 8(4):1295–1308

    Google Scholar 

  26. Branyikova I, Prochazkova G, Potocar T, Jezkova Z, Branyik T (2018) Harvesting of microalgae by flocculation. Fermentation 4(4):93

    CAS  Article  Google Scholar 

  27. Brentner LB, Eckelman MJ, Zimmerman JB (2011) Combinatorial life cycle assessment to inform process design of industrial production of algal biodiesel. Environ Sci Technol 45(16):7060–7067

    CAS  Article  Google Scholar 

  28. Camacho FP, Sousa VS, Bergamasco R, Teixeira MR (2017) The use of Moringa oleifera as a natural coagulant in surface water treatment. Chem Eng J 313:226–237

    CAS  Article  Google Scholar 

  29. Carvalho MS, Alves BR, Silva MF, Bergamasco R, Coral LA, Bassetti FJ (2016) CaCl2 applied to the extraction of Moringa oleifera seeds and the use for Microcystis aeruginosa removal. Chem Eng J 304:469–475

    CAS  Article  Google Scholar 

  30. Chatsungnoen T, Chisti Y (2016) Harvesting microalgae by flocculation–sedimentation. Algal Res 13:271–283

    Article  Google Scholar 

  31. Chen L, Li P, Liu Z, Jiao Q (2009) The released polysaccharide of the cyanobacterium Aphanothece halophytica inhibits flocculation of the alga with ferric chloride. J Appl Phycol 21(3):327–331

    CAS  Article  Google Scholar 

  32. Chen CY, Yeh KL, Aisyah R, Lee DJ, Chang JS (2011) Cultivation, photobioreactor design and harvesting of microalgae for biodiesel production: a critical review. Bioresour Technol 102(1):71–81

    CAS  Article  Google Scholar 

  33. Chi FH, Cheng WP (2006) Use of chitosan as coagulant to treat wastewater from milk processing plant. J Polym Environ 14(4):411–417

    CAS  Article  Google Scholar 

  34. Chiu SY, Kao CY, Tsai MT, Ong SC, Chen CH, Lin CS (2009) Lipid accumulation and CO2 utilization of Nannochloropsis oculata in response to CO2 aeration. Bioresour Technol 100(2):833–838

    CAS  Article  Google Scholar 

  35. Choy SY, Prasad KMN, Wu TY, Raghunandan ME, Ramanan RN (2014) Utilization of plant-based natural coagulants as future alternatives towards sustainable water clarification. J Environ Sci 26(11):2178–2189

    Article  Google Scholar 

  36. Chua ET, Eltanahy E, Jung H, Uy M, Thomas-Hall SR, Schenk PM (2018) Efficient harvesting of Nannochloropsis microalgae via optimized chitosan-mediated flocculation. Glob Chall 3(1):1800038

    Article  Google Scholar 

  37. Chua ET, Shekh AY, Eltanahy E, Thomas-Hall SR, Schenk PM (2020) Effective harvesting of Nannochloropsis microalgae using Mushroom chitosan: a pilot-scale study. Front Bioeng Biotechnol 8:771

    Article  Google Scholar 

  38. Chung CY, Selvarajoo A, Sethu V, Koyande AK, Arputhan A, Lim ZC (2018) Treatment of palm oil mill effluent (POME) by coagulation flocculation process using peanut–okra and wheat germ–okra. Clean Technol Environ Policy 20(9):1951–1970

    CAS  Article  Google Scholar 

  39. Crini G (2005) Recent developments in polysaccharide-based materials used as adsorbents in wastewater treatment. Prog Polym Sci 30(1):38–70

    CAS  Article  Google Scholar 

  40. Danquah MK, Ang L, Uduman N, Moheimani N, Forde GM (2009) Dewatering of microalgal culture for biodiesel production: exploring polymer flocculation and tangential flow filtration. J Chem Technol Biotechnol Int Res Process Environ Clean Technol 84(7):1078–1083

    CAS  Google Scholar 

  41. Dassey AJ, Theegala CS (2013) Harvesting economics and strategies using centrifugation for cost effective separation of microalgae cells for biodiesel applications. Bioresour Technol 128:241–245

    CAS  Article  Google Scholar 

  42. De Jesus E, Cruz PV, Pacífico JA, Silva AS (2013) Removal of turbidity, suspended solids and ions of Fe from aqueous solution using okra powder by coagulation–flocculation process. Am J Water Resour 1(3):20–24

    Article  Google Scholar 

  43. Debruyn A, Alvarez AP, Sandra P, De Leenheer L (1992) Isolation and identification of β-d-fructofuranosyl-(2, 1)-d-fructose, a product of the enzymatic hydrolysis of the inulin from Cichorium intybus. Carbohydr Res 235:303–308

    CAS  Article  Google Scholar 

  44. Demirbas A (2008) Production of biodiesel from algae oils. Energy Sources Part A Recov Util Environ Eff 31(2):163–168

    Article  CAS  Google Scholar 

  45. Divakaran R, Pillai VS (2002) Flocculation of algae using chitosan. J Appl Phycol 14(5):419–422

    CAS  Article  Google Scholar 

  46. Dkhissi O, El Hakmaoui A, Souabi S, Chatoui M, Jada A, Akssira M (2018) Treatment of vegetable oil refinery wastewater by coagulation–flocculation process using the cactus as a bio-flocculant. J Mater Environ Sci 9(1):18–25

    CAS  Google Scholar 

  47. El-Mashad H (2014) Growth kinetics and chitosan flocculation of Spirulina platensis algae. J Environ Sci Eng A 3:150–162

    Google Scholar 

  48. El-Naggar ME, Samhan FA, Salama AA, Hamdy RM, Ali GH (2018) Cationic starch: safe and economic harvesting flocculant for microalgal biomass and inhibiting E. coli growth. Int J Biol Macromol 116:1296–1303

    CAS  Article  Google Scholar 

  49. Endut A, Hamid S, Lananan F, Kathoon H (2016) Moringa oleifera seed derivatives as potential bio-coagulant for microalgae Chlorella sp. harvesting. Malaysian Journal of Analytical Sciences 20(2):401–412

    Article  Google Scholar 

  50. Erdawati MK, Saefurahman G, Hidayatuloh S, Kawaroe M (2020) Effect of pH culture and dosage of chitosan nanoemulsion on the effectiveness of bio-flocculation in harvesting Chlorella sp. biomass. In: IOP Conference Series: Earth and Environmental Science vol 460. IOP Publishing, p 012005

  51. Farid MS, Shariati A, Badakhshan A, Anvaripour B (2013) Using nano-chitosan for harvesting microalga Nannochloropsis sp. Bioresour Technol 131:555–559

    CAS  Article  Google Scholar 

  52. Freitas TK, Oliveira VM, De Souza MT, Geraldino HC, Almeida VC, Fávaro SL, Garcia JC (2015) Optimization of coagulation–flocculation process for treatment of industrial textile wastewater using okra (A. esculentus) mucilage as natural coagulant. Ind Crops Prod 76:538–544

    CAS  Article  Google Scholar 

  53. Fuad N, Omar R, Kamarudin S, Harun R, Idris A, Azlina WW (2018) Effective use of tannin based natural biopolymer, AFlok-BP1 to harvest marine microalgae Nannochloropsis sp. J Environ Chem Eng 6(4):4318–4328

    CAS  Article  Google Scholar 

  54. Galal TM, Shedeed ZA, Hassan LM (2019) Hazards assessment of the intake of trace metals by common mallow (Malva parviflora K.) growing in polluted soils. Int J Phytoremediat 21(14):1397–1406

    CAS  Article  Google Scholar 

  55. Garcia-Fayos B, Arnal JM, Ruiz V, Sancho M (2015) Use of Moringa oleifera in drinking water treatment: study of storage conditions and performance of the coagulant extract. Desalin Water Treat 57(48–49):23365–23371

    Google Scholar 

  56. Gautam S, Arora AS, Singh AK, Ekka P, Daniel H, Gokul B, Toppo S, Chockalingam P, Kumar H, Lyngdoh JF (2020) Coagulation influencing parameters investigation on textile industry discharge using Strychnos potatorum seed powders. Environ Dev Sustain 28:1–8

    Google Scholar 

  57. Georgianna DR, Mayfield SP (2012) Exploiting diversity and synthetic biology for the production of algal biofuels. Nature 488(7411):329–335

    CAS  Article  Google Scholar 

  58. Gonzalez-Fernandez C, Ballesteros M (2013) Microalgae auto-flocculation: an alternative to high-energy consuming harvesting methods. J Appl Phycol 25(4):991–999

    CAS  Article  Google Scholar 

  59. Gouveia L, Oliveira AC (2009) Microalgae as a raw material for biofuels production. J Ind Microbiol Biotechnol 36(2):269–274

    CAS  Article  Google Scholar 

  60. Granados MR, Acién FG, Gomez C, Fernández-Sevilla JM, Grima EM (2012) Evaluation of flocculants for the recovery of freshwater microalgae. Bioresour Technol 118:102–110

    CAS  Article  Google Scholar 

  61. Grenda K, Arnold J, Hunkeler D, Gamelas JAF, Rasteiro MG (2018) Tannin-based coagulants from laboratory to pilot plant scales for coloured wastewater treatment. BioResources 13(2):2727–2747

    CAS  Article  Google Scholar 

  62. Grima EM, Belarbi EH, Fernández FA, Medina AR, Chisti Y (2003) Recovery of microalgal biomass and metabolites: process options and economics. Biotechnol Adv 20(7–8):491–515

    Article  Google Scholar 

  63. Gupta BS, Ako JE (2005) Application of guar gum as a flocculant aid in food processing and potable water treatment. Eur Food Res Technol 221(6):746–751

    Article  CAS  Google Scholar 

  64. Gutiérrez R, Ferrer I, García J, Uggetti E (2015) Influence of starch on microalgal biomass recovery, settleability and biogas production. Bioresour Technol 185:341–345

    Article  CAS  Google Scholar 

  65. Hameed YT, Idris A, Hussain SA, Abdullah N (2016) A tannin-based agent for coagulation and flocculation of municipal wastewater: chemical composition, performance assessment compared to polyaluminium chloride, and application in a pilot plant. J Environ Manage 184:494–503

    CAS  Article  Google Scholar 

  66. Hamid SHA, Lananan F, Din WNS, Lam SS, Khatoon H, Endut A, Jusoh A (2014) Harvesting microalgae, Chlorella sp. by bio-flocculation of Moringa oleifera seed derivatives from aquaculture wastewater phytoremediation. Int Biodeterior Biodegrad 95:270–275

    Article  CAS  Google Scholar 

  67. Hamid SHA, Lananan F, Khatoon H, Jusoh A, Endut A (2016) A study of coagulating protein of Moringa oleifera in microalgae bio-flocculation. Int Biodeterior Biodegrad 113:310–317

    Article  CAS  Google Scholar 

  68. Hauwa A, Mohamed RM, Al-Gheethi AA, Wurochekke AA, Hashim MA (2018) Harvesting of Botryococcus sp. biomass from greywater by natural coagulants. Waste Biomass Valorization 9(10):1841–1853

    CAS  Article  Google Scholar 

  69. Haveren JV, Scott EL, Sanders J (2008) Bulk chemicals from biomass. Biofuels Bioprod Biorefin Innov Sustain Econ 2(1):41–57

    Article  CAS  Google Scholar 

  70. Heasman M, Diemar J, O’connor W, Sushames T, Foulkes L (2000) Development of extended shelf-life microalgae concentrate diets harvested by centrifugation for bivalve molluscs—a summary. Aquacult Res 31(8–9):637–659

    Google Scholar 

  71. Hellsing MS, Kwaambwa HM, Nermark FM, Nkoane BB, Jackson AJ, Wasbrough MJ, Rennie AR (2014) Structure of flocs of latex particles formed by addition of protein from Moringa seeds. Colloids Surf A Physicochem Eng Asp 460:460–467

    CAS  Article  Google Scholar 

  72. Henderson RK, Baker A, Parsons SA, Jefferson B (2008) Characterisation of algogenic organic matter extracted from cyanobacteria, green algae and diatoms. Water Res 42(13):3435–3445

    CAS  Article  Google Scholar 

  73. Henderson RK, Parsons SA, Jefferson B (2010) The impact of differing cell and algogenic organic matter (AOM) characteristics on the coagulation and flotation of algae. Water Res 44(12):3617–3624

    CAS  Article  Google Scholar 

  74. Hernes PJ, Hedges JI (2000) Determination of condensed tannin monomers in environmental samples by capillary gas chromatography of acid depolymerization extracts. Anal Chem 72(20):5115–5124

    CAS  Article  Google Scholar 

  75. Hesse MC, Santos B, Selesu NF, Correa DO, Mariano AB, Vargas JV, Vieira RB (2017) Optimization of flocculation with tannin-based flocculant in the water reuse and lipidic production for the cultivation of Acutodesmus obliquus. Sep Sci Technol 52(5):936–942

    CAS  Article  Google Scholar 

  76. Huang C, Chen Y (1996) Coagulation of colloidal particles in water by chitosan. J Chem Technol Biotechnol Int Res Process Environ Clean Technol 66(3):227–232

    CAS  Google Scholar 

  77. Huang Y, Wei C, Liao Q, Xia A, Zhu X, Zhu X (2019) Biodegradable branched cationic starch with high C/N ratio for Chlorella vulgaris cells concentration: regulating microalgae flocculation performance by pH. Bioresour Technol 276:133–139

    CAS  Article  Google Scholar 

  78. Hulatt CJ, Thomas DN (2010) Dissolved organic matter (DOM) in microalgal photobioreactors: a potential loss in solar energy conversion? Bioresour Technol 101(22):8690–8697

    CAS  Article  Google Scholar 

  79. Ives KJ (1956) Electrokinetic phenomena of planktonic algae. Proc Soc Water Treat Exam 5:41–58

    Google Scholar 

  80. Jain A, Subramanian R, Manohar B, Radha C (2019) Preparation, characterization and functional properties of Moringa oleifera seed protein isolate. J Food Sci Technol 56(4):2093–2104

    CAS  Article  Google Scholar 

  81. Jethani H, Patel P, Mudliar SN, Ravi S, Chauhan VS (2019a) Growth and biochemical response of an indigenous oleaginous microalga Scenedesmus obtusus cultivated in outdoor open ponds. Indian J Exp Biol 57(1):40–49

    CAS  Google Scholar 

  82. Jethani H, Nair S, Radha C, Chauhan VS, Sarada R, Hebbar HU (2019b) Plant-based bio-flocculant assisted microalgal biomass recovery. In: 7th Bioprocessing India Conference, Advances in bioprocessing of agri-food resources (BBT-025, p 118), CSIR-CFTRI, India

  83. Junior AT, Hasan SD, Sebastien NY (2019) Optimization of coagulation/flocculation treatment of brewery wastewater employing organic flocculant based of vegetable tannin. Water Air Soil Pollut 230(8):202

    Article  CAS  Google Scholar 

  84. Kandasamy G, Shaleh SRM (2017) Harvesting of the microalga Nannochloropsis sp. by bioflocculation with mung bean protein extract. Appl Biochem Biotechnol 182(2):586–597

    CAS  Article  Google Scholar 

  85. Kanza M, Saefurahman G, Hidayatuloh S, Kawaroe M (2020) Effect of pH culture and dosage of chitosan nanoemulsion on the effectiveness of bio-flocculation in harvesting Chlorella sp. biomass. In: IOP conference series: earth and environmental science, vol 460, no 1. IOP Publishing, p 012005

  86. Kaur N, Gupta AK (2002) Applications of inulin and oligofructose in health and nutrition. J Biosci 27(7):703–714

    CAS  Article  Google Scholar 

  87. Khiari R, Dridi-Dhaouadi S, Aguir C, Mhenni MF (2010) Experimental evaluation of eco-friendly flocculants prepared from date palm rachis. J Environ Sci 22(10):1539–1543

    CAS  Article  Google Scholar 

  88. Kim MS, Kwak DH (2020) Auto/bio-flocculation conditions to separate algal particles without chemical coagulants for flotation and sedimentation processes. Sep Sci Technol 55(6):1185–1196

    CAS  Article  Google Scholar 

  89. Kim IT, Sethu V, Arumugasamy SK, Selvarajoo A (2020) Fenugreek seeds and okra for the treatment of palm oil mill effluent (POME)—characterization studies and modeling with backpropagation feedforward neural network (BFNN). J Water Process Eng 37:101500

    Article  Google Scholar 

  90. Konig RB, Sales R, Roselet F, Abreu PC (2014) Harvesting of the marine microalga Conticribra weissflogii (Bacillariophyceae) by cationic polymeric flocculants. Biomass Bioenergy 68:1–6

    CAS  Article  Google Scholar 

  91. Kothari R, Pathak VV, Pandey A, Ahmad S, Srivastava C, Tyagi VV (2016) A novel method to harvest Chlorella sp. via low cost bioflocculant: influence of temperature with kinetic and thermodynamic functions. Bioresour Technol 225:84–89

    Article  CAS  Google Scholar 

  92. Kumar N, Banerjee C, Kumar N, Jagadevan S (2019) A novel non-starch based cationic polymer as flocculant for harvesting microalgae. Bioresour Technol 271:383–390

    CAS  Article  Google Scholar 

  93. Kurniawati HA, Ismadji S, Liu JC (2014) Microalgae harvesting by flotation using natural saponin and chitosan. Bioresour Technol 166:429–434

    CAS  Article  Google Scholar 

  94. Lama S, Muylaert K, Karki TB, Foubert I, Henderson RK, Vandamme D (2016) Flocculation properties of several microalgae and a cyanobacterium species during ferric chloride, chitosan and alkaline flocculation. Bioresour Technol 220:464–470

    CAS  Article  Google Scholar 

  95. Larkum AW, Ross IL, Kruse O, Hankamer B (2012) Selection, breeding and engineering of microalgae for bioenergy and biofuel production. Trends Biotechnol 30(4):198–205

    CAS  Article  Google Scholar 

  96. Lee CS, Chong MF, Robinson J, Binner E (2014) A review on development and application of plant-based bio-flocculants and grafted bio-flocculants. Ind Eng Chem Res 53(48):18357–18369

    CAS  Article  Google Scholar 

  97. Leon-Martínez FM, Rodriguez-Ramirez J, Medina-Torres LL, Lagunas LM, Bernad-Bernad MJ (2011) Effects of drying conditions on the rheological properties of reconstituted mucilage solutions (Opuntia ficus-indica). Carbohydr Polym 84(1):439–445

    Article  CAS  Google Scholar 

  98. Letelier-Gordo CO, Holdt SL, De Francisci D, Karakashev DB, Angelidaki I (2014) Effective harvesting of the microalgae Chlorella protothecoides via bio-flocculation with cationic starch. Bioresour Technol 167:214–218

    CAS  Article  Google Scholar 

  99. Levy N, Garti N, Magdassi S (1995) Flocculation of bentonite suspensions with cationic guar. Colloids Surf A Physicochem Eng Asp 97(2):91–99

    CAS  Article  Google Scholar 

  100. Maghfiroh W, Saefurahman G, Hidayatuloh S, Kawaroe M (2018) Harvesting effectiveness of Chlorella sp. biomass using different flocculation treatments of Moringa oleifera extract and pH conditions. In: IOP conference series: earth and environmental science, vol 209, no 1, p 012-014

  101. Makur MM, Duraisamy R, Birhanu T (2019) Clarifying capacity of eco-friendly nano CaO and okra (Abelmoschus esculentus) extract on the processing of sugarcane juice: a review. Int Res J Sci Technol 1(1):21–30

    Article  Google Scholar 

  102. Mezzari MP, Da Silva ML, Pirolli M, Perazzoli S, Steinmetz RL, Nunes EO, Soares HM (2014) Assessment of a tannin-based organic polymer to harvest Chlorella vulgaris biomass from swine wastewater digestate phycoremediation. Water Sci Technol 70(5):888–894

    CAS  Article  Google Scholar 

  103. Mirzaei S, Javanbakht V (2019) Dye removal from aqueous solution by a novel dual cross-linked bio-composite obtained from mucilage of Plantago Psyllium and eggshell membrane. Int J Biol Macromol 134:1187–1204

    CAS  Article  Google Scholar 

  104. Mishra A, Bajpai M (2006a) Graft copolymerization of polyacrylamide onto tamarind mucilage. J Macromol Sci Part A Pure Appl Chem 43(2):315–326

    CAS  Article  Google Scholar 

  105. Mishra A, Bajpai M (2006b) The flocculation performance of Tamarindus mucilage in relation to removal of vat and direct dyes. Bioresour Technol 97(8):1055–1059

    CAS  Article  Google Scholar 

  106. Mishra S, Kundu K (2019) Synthesis, characterization and applications of polyacrylamide grafted fenugreek gum (FG-g-PAM) as flocculant: microwave vs thermal synthesis approach. Int J Biol Macromol 141:792–808

    CAS  Article  Google Scholar 

  107. Mishra A, Agarwal M, Bajpai M, Rajani S, Mishra RP (2002a) Plantago psyllium mucilage for sewage and tannery effluent treatment. Iran Polym J 11(6):381–386

    CAS  Google Scholar 

  108. Mishra A, Srinivasan R, Dubey R (2002b) Flocculation of textile wastewater by Plantago psyllium mucilage. Macromol Mater Eng 287(9):592–596

    CAS  Article  Google Scholar 

  109. Mishra A, Agarwal M, Yadav A (2003) Fenugreek mucilage as a flocculating agent for sewage treatment. Colloid Polym Sci 281(2):164–167

    CAS  Article  Google Scholar 

  110. Mishra A, Srinivasan R, Bajpai M, Dubey R (2004a) Use of polyacrylamide-grafted Plantago psyllium mucilage as a flocculant for treatment of textile wastewater. Colloid Polym Sci 282(7):722–727

    CAS  Article  Google Scholar 

  111. Mishra A, Yadav A, Agarwal M, Bajpai M (2004b) Fenugreek mucilage for solid removal from tannery effluent. React Funct Polym 59(1):99–104

    CAS  Article  Google Scholar 

  112. Mishra S, Sinha S, Dey KP, Sen G (2014) Synthesis, characterization and applications of polymethylmethacrylate grafted psyllium as flocculant. Carbohydr Polym 99:462–468

    CAS  Article  Google Scholar 

  113. Morweiser M, Kruse O, Hankamer B, Posten C (2010) Developments and perspectives of photobioreactors for biofuel production. Appl Microbiol Biotechnol 87(4):1291–1301

    CAS  Article  Google Scholar 

  114. Moulin M, Mossou E, Signor L, Kieffer-Jaquinod S, Kwaambwa HM, Nermark F, Gutfreund P, Mitchell EP, Haertlein M, Forsyth VT, Rennie AR (2019) Towards a molecular understanding of the water purification properties of Moringa seed proteins. J Colloid Interface Sci 554:296–304

    CAS  Article  Google Scholar 

  115. Nayak BR, Singh RP (2001) Development of graft copolymer flocculating agents based on hydroxypropyl guar gum and acrylamide. J Appl Polym Sci 81(7):1776–1785

    CAS  Article  Google Scholar 

  116. Ogbonna CN, Edeh IC (2018) Harvesting Chlorella variabilis biomass using Moringa oleifera seed-induced sedimentation. J Adv Biol Biotechnol 8:1

    Google Scholar 

  117. Okolo BI, Menkiti MC, Nnaji PC, Onukwuli OD, Agu CC (2014) The Performance of okra seed (Hibiscus esculentus L.) extract in removal of suspended particles from brewery effluent by coag-flocculation process. Curr J Appl Sci Technol 23:4791–4806

    Article  Google Scholar 

  118. Oladoja NA (2015) Headway on natural polymeric coagulants in water and wastewater treatment operations. J Water Process Eng 6:174–192

    Article  Google Scholar 

  119. Pal S, Mal D, Singh RP (2005) Cationic starch: an effective flocculating agent. Carbohydr Polym 59(4):417–423

    CAS  Article  Google Scholar 

  120. Pal S, Mal D, Singh RP (2008) Characterization of cationic starch: an efficient flocculating agent. J Appl Polym Sci 108(4):2674–2681

    CAS  Article  Google Scholar 

  121. Pal S, Ghosh S, Sen G, Jha U, Singh RP (2009) Cationic tamarind kernel polysaccharide (Cat TKP): a novel polymeric flocculant for the treatment of textile industry wastewater. Int J Biol Macromol 45(5):518–523

    CAS  Article  Google Scholar 

  122. Pal S, Ghorai S, Dash MK, Ghosh S, Udayabhanu G (2011) Flocculation properties of polyacrylamide grafted carboxymethyl guar gum (CMG-g-PAM) synthesized by conventional and microwave-assisted method. J Hazard Mater 192(3):1580–1588

    CAS  Article  Google Scholar 

  123. Papazi A, Makridis P, Divanach P (2010) Harvesting Chlorella minutissima using cell coagulants. J Appl Phycol 22(3):349–355

    CAS  Article  Google Scholar 

  124. Patel P, Jethani H, Radha C, Vijayendra SVN, Mudliar SN, Sarada R, Chauhan VS (2019) Development of a carotenoid enriched probiotic yogurt from fresh biomass of Spirulina and its characterization. J Food Sci Technol 56(8):3721–3731

    CAS  Article  Google Scholar 

  125. Peng C, Li S, Zheng J, Huang S, Li D (2017) Harvesting microalgae with different sources of starch-based cationic flocculants. Appl Biochem Biotechnol 181(1):112–124

    CAS  Article  Google Scholar 

  126. Pishgar Z, Samimi A, Mohebbi-Kalhori D, Shokrollahzadeh S (2020) Comparative study on the harvesting of marine Chlorella vulgaris microalgae from a dilute slurry using autoflocculation-sedimentation and electrocoagulation-flotation methods. Int J Environ Res 4:1–4

    Google Scholar 

  127. Prabaharan M, Mano JF (2004) Chitosan-based particles as controlled drug delivery systems. Drug Deliv 12(1):41–57

    Article  CAS  Google Scholar 

  128. Pugazhendhi A, Shobana S, Bakonyi P, Nemestóthy N, Xia A, Kumar G (2019) A review on chemical mechanism of microalgae flocculation via polymers. Biotechnol Rep 21:e00302

    Article  Google Scholar 

  129. Pulkkinen E, Mikkonen H (1992) Preparation and performance of tannin-based flocculants. In: Plant polyphenols. Springer, Boston, pp 953–966

  130. Qureshi K, Bhatti I, Shaikh MS (2011) Development of bio-coagulant from mango pit for the purification of turbid water. Sindh Univ Res J 43(1):105–110

    Google Scholar 

  131. Rachdi R, Srarfi F, Shimi NS (2017) Cactus opuntia as natural flocculant for urban wastewater treatment. Water Sci Technol 76(7):1875–1883

    CAS  Article  Google Scholar 

  132. Radin Mohamed RM, Maniam H, Afandi N, Al-Gheethi AA, Mohd Kassim AH (2017) Microalgae biomass recovery grown in wet market wastewater via flocculation method using Moringa oleifera. In: Key engineering materials, vol 744. Trans Tech Publications Ltd, pp 542–545

  133. Rahul R, Kumar S, Jha U, Sen G (2015) Cationic inulin: a plant based natural biopolymer for algal biomass harvesting. Int J Biol Macromol 72:868–874

    CAS  Article  Google Scholar 

  134. Razack SA, Duraiarasan S, Shellomith AS, Muralikrishnan K (2015) Statistical optimization of harvesting Chlorella vulgaris using a novel bio-source, Strychnos potatorum. Biotechnol Rep 7:150–156

    Article  Google Scholar 

  135. Renault F, Sancey B, Badot PM, Crini G (2009) Chitosan for coagulation/flocculation processes—an eco-friendly approach. Eur Polym J 45(5):1337–1348

    CAS  Article  Google Scholar 

  136. Ronke RA, Saidat OG, Abdulwahab G (2016) Coagulation–flocculation treatment of industrial wastewater using tamarind seed powder. Int J ChemTech Res 9(5):771–780

    Google Scholar 

  137. Roselet F, Burkert J, Abreu PC (2016) Flocculation of Nannochloropsis oculata using a tannin-based polymer: bench scale optimization and pilot scale reproducibility. Biomass Bioenergy 87:55–60

    CAS  Article  Google Scholar 

  138. Roy M, Mohanty K (2020) Valorization of waste eggshell-derived bio-flocculant for harvesting T. obliquus: process optimization, kinetic studies and recyclability of the spent medium for circular bioeconomy. Bioresour Technol 23:123–205

    Google Scholar 

  139. Ruiz-Marin A, Canedo-Lopez Y, Narvaez-Garcia A, Zavala-Loría JD, Dzul-López LA, Sámano-Celorio ML, Crespo-Álvarez J, García-Villena E, Agudo-Toyos P (2019) Harvesting Scenedesmus obliquus via flocculation of Moringa oleifera seed extract from urban wastewater: proposal for the integrated use of oil and flocculant. Energies 12(20):3996

    CAS  Article  Google Scholar 

  140. Rwehumbiza VM, Harrison R, Thomsen L (2012) Alum-induced flocculation of preconcentrated Nannochloropsis salina: residual aluminium in the biomass, FAMEs and its effects on microalgae growth upon media recycling. Chem Eng J 200:168–175

    Article  CAS  Google Scholar 

  141. Salim S, Bosma R, Vermuë MH, Wijffels RH (2011) Harvesting of microalgae by bio-flocculation. J Appl Phycol 23(5):849–855

    Article  Google Scholar 

  142. Sánchez-Martín J, Beltrán-Heredia J, Solera-Hernández C (2010) Surface water and wastewater treatment using a new tannin-based coagulant. Pilot plant trials. J Environ Manag 10:2051–2058

    Article  CAS  Google Scholar 

  143. Savant VD, Torres JA (2000) Chitosan-based coagulating agents for treatment of cheddar cheese whey. Biotechnol Progr 16(6):1091–1097

    CAS  Article  Google Scholar 

  144. Schenk PM, Thomas-Hall SR, Stephens E, Marx UC, Mussgnug JH, Posten C, Kruse O, Hankamer B (2008) Second generation biofuels: high-efficiency microalgae for biodiesel production. Bioenergy Res 1(1):20–43

    Article  Google Scholar 

  145. Schlesinger A, Eisenstadt D, Bar-Gil A, Carmely H, Einbinder S, Gressel J (2012) Inexpensive non-toxic flocculation of microalgae contradicts theories; overcoming a major hurdle to bulk algal production. Biotechnol Adv 30(5):1023–1030

    CAS  Article  Google Scholar 

  146. Sellamib M, Zarai Z, Khadhraoui M, Jdidi N, Leduc R, Ben Rebah F (2014) Cactus juice as bioflocculant in the coagulation–flocculation process for industrial wastewater treatment: a comparative study with polyacrylamide. Water Sci Technol 70(7):1175–1181

    Article  CAS  Google Scholar 

  147. Sen G, Pal S (2009a) Polyacrylamide grafted carboxymethyl tamarind (CMT-g-PAM): development and application of a novel polymeric flocculant. In: Macromolecular symposia, vol 7, no 1. WILEY-VCH Verlag, Weinheim, pp 100–111

  148. Sen G, Pal S (2009b) Polyacrylamide grafted carboxymethyl tamarind (CMT-g-PAM): development and application of a novel polymeric flocculant. In: Macromolecular symposia, vol 277, no 1. WILEY-VCH Verlag, Weinheim, pp 100–111

  149. Sen G, Mishra S, Rani GU, Rani P, Prasad R (2012) Microwave initiated synthesis of polyacrylamide grafted Psyllium and its application as a flocculant. Int J Biol Macromol 50(2):369–375

    CAS  Article  Google Scholar 

  150. Shabe KM, Salah SE, Janbi MM (2011) Coagulation–flocculation process to treat pulp and paper mill wastewater by fenugreek mucilage coupled with alum and polyaluminium chloride. Al-Khwarizmi Eng J 7(3):39–47

    Google Scholar 

  151. Sharma BR, Dhuldhoya NC, Merchant UC (2006) Flocculants—an ecofriendly approach. J Polym Environ 14(2):195–202

    CAS  Article  Google Scholar 

  152. Sharma KK, Garg S, Li Y, Malekizadeh A, Schenk PM (2013) Critical analysis of current microalgae dewatering techniques. Biofuels 4(4):397–407

    CAS  Article  Google Scholar 

  153. Singh G, Patidar SK (2018) Microalgae harvesting techniques: a review. J Environ Manag 217:499–508

    Article  Google Scholar 

  154. Singh RP, Karmakar GP, Rath SK, Karmakar NC, Pandey SR, Tripathy T, Panda J, Kanan K, Jain SK, Lan NT (2000) Biodegradable drag reducing agents and flocculants based on polysaccharides: materials and applications. Polym Eng Sci 40(1):46–60

    CAS  Article  Google Scholar 

  155. Soomro RR, Ndikubwimana T, Zeng X, Lu Y, Lin L, Danquah MK (2016) Development of a two-stage microalgae dewatering process—a life cycle assessment approach. Front Plant Sci 7:113

    Article  Google Scholar 

  156. Srinivasan R, Mishra A (2008) Okra (Hibiscus esculentus) and fenugreek (Trigonella foenum graceum) mucilage: characterization and application as flocculants for textile effluent treatments. Chin J Polym Sci 26(06):679–687

    CAS  Article  Google Scholar 

  157. Srinivasan R, Agarwal M, Mishra A (2002) Plantago psyllium-grafted-polyacrylonitrile—synthesis, characterization and its use in suspended and dissolved solid removal from textile effluent. Water Qual Res J 37(2):371–378

    CAS  Article  Google Scholar 

  158. Srirama A, Swaminathanb G, Subbarayanb S (2019) Removal of solids from surfactant wastewater through synergetic utilization of Strychnos potatorum and Colocasia esculenta. Desalin Water Treat 156:357–369

    Article  CAS  Google Scholar 

  159. Teixeira CML, Teixeira PCN (2017) Evaluation of the flocculation efficiency of Chlorella vulgaris mediated by Moringa oleifera seed under different forms: flour, seed cake and extracts of flour and cake. Braz J Chem Eng 34(1):65–74

    CAS  Article  Google Scholar 

  160. Teixeira CMLL, Kirsten FV, Teixeira PCN (2012) Evaluation of Moringa oleifera seed flour as a flocculating agent for potential biodiesel producer microalgae. J Appl Phycol 24(3):557–563

    CAS  Article  Google Scholar 

  161. Tork MB, Khalilzadeh R, Kouchakzadeh H (2017) Efficient harvesting of marine Chlorella vulgaris microalgae utilizing cationic starch nanoparticles by response surface methodology. Bioresour Technol 243:583–588

    Article  CAS  Google Scholar 

  162. Uduman N, Qi Y, Danquah MK, Forde GM, Hoadley A (2010) Dewatering of microalgal cultures: a major bottleneck to algae-based fuels. J Renew Sustain Energy 2(1):012701

    Article  CAS  Google Scholar 

  163. Ummalyma SB, Gnansounou E, Sukumaran RK, Sindhu R, Pandey A, Sahoo D (2017) Bioflocculation: an alternative strategy for harvesting of microalgae—an overview. Bioresour Technol 242:227–235

    CAS  Article  Google Scholar 

  164. Vandamme D, Foubert I, Meesschaert B, Muylaert K (2010) Flocculation of microalgae using cationic starch. J Appl Phycol 22(4):525–530

    Article  Google Scholar 

  165. Vandamme D, Foubert I, Fraeye I, Muylaert K (2012) Influence of organic matter generated by Chlorella vulgaris on five different modes of flocculation. Bioresour Technol 124:508–511

    CAS  Article  Google Scholar 

  166. Vandamme D, Foubert I, Muylaert K (2013) Flocculation as a low-cost method for harvesting microalgae for bulk biomass production. Trends Biotechnol 31(4):233–239

    CAS  Article  Google Scholar 

  167. Vijayaraghavan G, Sivakumar T, Kumar AV (2011) Application of plant-based coagulants for waste water treatment. Int J Adv Eng Res Stud 1(1):88–92

    Google Scholar 

  168. Wan C, Alam MA, Zhao XQ, Zhang XY, Guo SL, Ho SH, Chang JS, Bai FW (2015) Current progress and future prospect of microalgal biomass harvest using various flocculation technologies. Bioresour Technol 184:251–257

    CAS  Article  Google Scholar 

  169. Wang L, Liang W, Yu J, Liang Z, Ruan L, Zhang Y (2013) Flocculation of Microcystis aeruginosa using modified larch tannin. Environ Sci Technol 47(11):5771–5777

    CAS  Article  Google Scholar 

  170. Wang X, Zhao Y, Jiang X, Wang Y, Li H, Wang L, Liang W (2018) The growth and physiological activity of Microcystis aeruginosa after flocculation using modified tannin. Int Biodeterior Biodegrad 133:180–186

    CAS  Article  Google Scholar 

  171. Xing GX, Zhang SF, Ju BZ, Yang JZ (2005) Recent advances in modified starch as flocculant. In: Proceedings of the third international conference on functional molecules, pp 13–18

  172. Xu L, Weathers PJ, Xiong XR, Liu CZ (2009) Microalgal bioreactors: challenges and opportunities. Eng Life Sci 9(3):178–189

    CAS  Article  Google Scholar 

  173. Xu Y, Purton S, Baganz F (2013) Chitosan flocculation to aid the harvesting of the microalga Chlorella sorokiniana. Bioresour Technol 129:296–301

    CAS  Article  Google Scholar 

  174. Yuliastri IR, Rohaeti E, Effendi H, Darusman LK (2016) The use of Moringa oleifera seed powder as coagulant to improve the quality of wastewater and ground water. In: IOP conference series: earth and environmental science, vol 31, no 012033. IOP Publishing, p 1755-1315

  175. Yunos FH, Nasir NM, Jusoh HH, Khatoon H, Lam SS, Jusoh A (2017) Harvesting of microalgae (Chlorella sp.) from aquaculture bioflocs using an environmental-friendly chitosan-based bio-coagulant. Int Biodeterior Biodegrad 124:243–249

    Article  CAS  Google Scholar 

  176. Zhang J, Zhang F, Luo Y, Yang H (2006) A preliminary study on cactus as coagulant in water treatment. Process Biochem 41(3):730–733

    CAS  Article  Google Scholar 

  177. Zheng H, Zhu G, Jiang S, Tshukudu T, Xiang X, Zhang P, He Q (2011) Investigations of coagulation–flocculation process by performance optimization, model prediction and fractal structure of flocs. Desalination 269(1–3):148–156

    CAS  Article  Google Scholar 

  178. Zhu LD, Takala J, Hiltunen E, Wang ZM (2013) Recycling harvest water to cultivate Chlorella zofingiensis under nutrient limitation for biodiesel production. Bioresour Technol 144:14–20

    CAS  Article  Google Scholar 

  179. Zhu L, Li Z, Hiltunen E (2018) Microalgae Chlorella vulgaris biomass harvesting by natural flocculant: effects on biomass sedimentation, spent medium recycling and lipid extraction. Biotechnol Biofuels 11(1):183

    Article  CAS  Google Scholar 

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Acknowledgements

The authors thank the Director, CSIR-CFTRI for his constant encouragement and providing the necessary infrastructure. The first author thanks University Grants Commission (UGC), India for the doctoral research fellowship.

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Doctoral research funding was provided by University Grants Commission (UGC), India.

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Jethani, H., Hebbar, U.H. Plant-based biopolymers: emerging bio-flocculants for microalgal biomass recovery. Rev Environ Sci Biotechnol 20, 143–165 (2021). https://doi.org/10.1007/s11157-020-09561-x

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Keywords

  • Bio-flocculation
  • Biopolymer
  • Biomass recovery
  • Cationization
  • Harvesting
  • Microalgae