Skip to main content

Advertisement

SpringerLink
Log in

Microalgal bio-flocculation: present scenario and prospects for commercialization

  • Review Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The need for sustainable production of renewable biofuel has been a global concern in the recent times. Overcoming the tailbacks of the first- and second-generation biofuels, third-generation biofuel using microalgae as feedstock has emerged as a plausible alternative. It has an added advantage of preventing any greenhouse gas (GHG) emissions with simultaneous carbon dioxide sequestration. Dewatering of microalgal culture is one of the many concerns regarding industrial-scale biofuel production. The small size of microalgae and dilute nature of its growth cultures creates huge operational cost during biomass separation, limiting economic feasibility of algae-based fuels. Considering the recovery efficiency, operation economics, technological feasibility and cost-effectiveness, bio-flocculation is a promising method of harvesting. Moreover, advantage of bio-flocculation over other conventional methods is that it does not incur the addition of any external chemical flocculants. This article reviews the current status of bio-flocculation technique for harvesting microalgae at industrial scale. The various microbial strains that can be prospective bioflocculants have been reviewed along with its application and advantages over chemical flocculants. Also, this article proposes that the primary focus of an appropriate harvesting technique should depend on the final utilization of the harvested biomass. This review article attempts to bring forth the beneficial aspects of microbial aided microalgal harvesting with a special attention on genetically modified self-flocculation microalgae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Availability of data and material

Not applicable

References

  • Abdullah B, Muhammad SAFAS, Shokravi Z, Ismail S, Kassim KA, Mahmood AN, Aziz MMA (2019) Fourth generation biofuel: a review on risks and mitigation strategies. Renew Sust Energ Rev 107:37–50

    Article  Google Scholar 

  • Alam MA, Wan C, Guo SL, Zhao XQ, Huang ZY, Yang YL, Bai FW (2014) Characterization of the flocculating agent from the spontaneously flocculating microalga Chlorella vulgaris JSC-7. J Biosci Bioeng 118:29–33

    Article  CAS  Google Scholar 

  • Alam F, Mobin S, Chowdhury H (2015) Third generation biofuel from Algae. Procedia Eng 105:763–768

    Article  CAS  Google Scholar 

  • 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 

  • Al-Hothaly KA, Adetutu EM, Taha M, Fabbri D, Lorenzetti C, Conti R, Ball AS (2015) Bio-harvesting and pyrolysis of the microalgae Botryococcus braunii. Bioresour Technol 191:117–123

    Article  CAS  Google Scholar 

  • Alrubaie G, Al-Shammari RH (2018) Microalgae Chlorella vulgaris harvesting via co-pelletization with filamentous fungus. Baghdad Sci J 15:31–36. https://doi.org/10.21123/bsj.2018.15.1.0031

    Article  Google Scholar 

  • Andrew LK, David LM, Ashman PJ (2013) Harvesting of marine microalgae by electroflocculation: the energetics, plant design, and economics. Appl Energy 108:45–53

    Article  Google Scholar 

  • Atiku H, Mohamed RMSR, Al-Gheethi AA, Wurochekke AA, Kassim AHM (2016) Harvesting of microalgae biomass from the phycoremediation process of greywater. Environ Sci Pollut Res 23(24):24624–24641

    Article  CAS  Google Scholar 

  • 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 92:675–681

    Article  CAS  Google Scholar 

  • Banerjee S, Banerjee S, Ghosh AK, Das D (2020a) Maneuvering the genetic and metabolic pathway for improving biofuel production in algae: present status and future prospective. Renew Sust Energ Rev 133:110155. https://doi.org/10.1016/j.rser.2020.110155

    Article  CAS  Google Scholar 

  • Banerjee S, Ray A, Das D (2021) Optimization of Chlamydomonas reinhardtii cultivation with simultaneous CO2 sequestration and biofuels production in a biorefinery framework. Sci Total Environ 762:143080. https://doi.org/10.1016/j.scitotenv.2020.143080 

  • Barros AI, Gonçalves AL, Simões M, Pires JC (2015) Harvesting techniques applied to microalgae: a review. Renewable Sustainable Energy Rev 41:1489–500

  • Barrut B, Blancheton J-P, Muller-Feuga A, René F, Narváez C, Champagne JY, Grasmick A (2013) Separation efficiency of a vacuum gas lift for microalgae harvesting. Bioresour Technol 128:235–240

    Article  CAS  Google Scholar 

  • Bayona KCD, Garcés LA (2014) Effect of different media on exopolysaccharide and biomass production by the green microalga Botryococcus braunii. J Appl Phycol 26(5):2087–2095

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bhattacharya A, Mathur M, Kumar P, Prajapati SK, Malik A (2017) A rapid method for fungal assisted algal flocculation: critical parameters and mechanism insights. Algal Res 21:42–51

    Article  Google Scholar 

  • Bhattacharya A, Mathur M, Kumar P, Malik A (2019) Potential role of N-acetyl glucosamine in Aspergillus fumigatus-assisted Chlorella pyrenoidosa harvesting. Biotechnol Biofuels 12:178

    Article  CAS  Google Scholar 

  • Borowitzka MA (2008) Marine and halophilic algae for the production of biofuels. J Biotechnol 136:S7

    Article  Google Scholar 

  • Bosma R, Van Spronsen WA, Tramper J, Wijffels RH (2003) Ultrasound, a new separation technique to harvest microalgae. J Appl Phycol 15:143–153

    Article  Google Scholar 

  • Brennan L, Owende P (2010) Biofuels from microalgae – a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sust Energ Rev 14:557–577

    Article  CAS  Google Scholar 

  • Brostow W, Hagg Lobland HE, Pal S, Singh RP (2009) Polymeric flocculants for wastewater and industrial effluent treatment. J Mater Educ 31(3–4):157–166

  • Cadoret J-P, Bernard O (2008) La production de biocarburant lipidique avec des microalgues: promesses et défis. J Soc Biol 202(3):201–211

    Article  CAS  Google Scholar 

  • 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 102:71–81

    Article  CAS  Google Scholar 

  • Chen J, Leng L, Ye C, Lu Q, Addy M, Wang J, Liu J, Chen P, Ruan R, Zhou W (2018) A comparative study between fungal pellet- and spore-assisted microalgae harvesting methods for algae bioflocculation. Bioresour Technol 259:181–190

    Article  CAS  Google Scholar 

  • Cho K, Hur SP, Lee CH, Ko K, Lee YJ, Kim KN, Kim MS, Chung YH, Kim D, Oda T (2015) Bioflocculation of the oceanic microalga Dunaliella salina by the bloom-forming dinoflagellate Heterocapsa circularisquama, and its effect on biodiesel properties of the biomass. Bioresour Technol 202:257–261

    Article  CAS  Google Scholar 

  • Christenson L, Sims R (2011) Production and harvesting of microalgae for wastewater treatment, biofuels, and bioproducts. Biotechnol Adv 29:686–702

    Article  CAS  Google Scholar 

  • Collotta M, Champagne P, Mabee W, Tomasoni G, Leite GB, Busi L, Alberti M (2017) Comparative LCA of flocculation for the harvesting of microalgae for biofuels production. Procedia CIRP 61:756–760

    Article  Google Scholar 

  • Connolly MP (2014) Introduction of Yeast Genes into the Green Alga, Chlamydomonas reinhardtii, to Promote Algal Flocculation. Honors Theses 41. https://digitalcommons.esf.edu/honors/41

  • Coons JE, Kalb DM, Dale T, Marrone BL (2014) Getting to low-cost algal biofuels: A monograph on conventional and cutting-edge harvesting and extraction technologies. Algal Res 6:250–270

    Article  Google Scholar 

  • 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 84(7):1078–1083

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Díaz-Santos E, Vila M, Vigara J, León R (2016) A new approach to express transgenes in microalgae and its use to increase the flocculation ability of Chlamydomonas reinhardtii. J Appl Phycol 28(3):1611–1621

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • El-Sheekh MM, Gheda SF, El-Sayed AEKB, Shady AMA, El-Sheikh ME, Schagerl M (2019) Outdoor cultivation of the green microalga Chlorella vulgaris under stress conditions as a feedstock for biofuel. Environ Sci Pollut Res 26(18):18520–18532

    Article  CAS  Google Scholar 

  • Fasaei F, Bitter JH, Slegers PM, van Boxtel AJB (2018) Techno-economic evaluation of microalgae harvesting and dewatering systems. Algal Res 31:347–362

    Article  Google Scholar 

  • Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633

    Article  CAS  Google Scholar 

  • Gao Z, Jiang C, Lyu R, Yang Z, Zhang T (2020) Optimization of the preparation of fungal-algal pellets for use in the remediation of arsenic-contaminated water. Environ Sci Pollut Res 27(29):36789–36798

    Article  CAS  Google Scholar 

  • Godos ID, Guzman HO, Soto R, García-Encina PA, Becares E, Muñoz R, Vargas VA (2011) Coagulation/flocculation-based removal of algal-bacterial biomass from piggery wastewater treatment. Bioresour Technol 102:923–927

    Article  CAS  Google Scholar 

  • Goldin E, Erickson L, Natarajan B et al (2009) Settling and bioflocculation of two species of algae used in wastewater treatment and algae biomass production. Environ Prog 28:404–409. https://doi.org/10.1002/ep

  • Gómez R, Schnabel I, Garrido J (1988) Pellet growth and citric acid yield of Aspergillus niger 110. Enzyme Microb Technol 10(3):188–191

    Article  Google Scholar 

  • González-Fernández C, Ballesteros M (2013) Microalgae autoflocculation: an alternative to high-energy consuming harvesting methods. J Appl Phycol 25:991–999

    Article  CAS  Google Scholar 

  • 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):491–515

    Article  Google Scholar 

  • Grima E, González MJ, Giménez A (2013) Solvent extraction for microalgae lipids. In: Borowitzka MA, Moheimani NR (eds) Algae for Biofuels and Energy 5:187–205. Springer, Netherlands

  • Gu Q, Jin WB, Chen YQ, Guo SD, Wan CF (2017) Highly efficient bioflocculation of microalgae using Mucor circinelloides. Huan Jing Ke Xue 38:688–696. https://doi.org/10.13227/j.hjkx.201607217

    Article  Google Scholar 

  • Guo SL, Zhao XQ, Wan C, Huang ZY, Yang YL, Alam MA, Ho SH, Bai FW, Chang JS (2013) Characterization of flocculating agent from the self-flocculating microalga Scenedesmus obliquus AS-6-1 for efficient biomass harvest. Bioresour Technol 145:285–289

    Article  CAS  Google Scholar 

  • Guo H, Hong C, Zhang C, Zheng B, Jiang D, Qin W (2018) Bioflocculants’ production from a cellulase-free xylanase-producing Pseudomonas boreopolis G22 by degrading biomass and its application in cost-effective harvest of microalgae. Bioresour Technol 255:171–179

    Article  CAS  Google Scholar 

  • Henderson R, Parsons S, Jefferson B (2008) Successful removal of algae through the control of zeta potential. Sep Sci Technol 43(7):1653–1666

    Article  CAS  Google Scholar 

  • Höök M, Tang X (2013) Depletion of fossil fuels and anthropogenic climate change - a review. Energy Policy 52:797–809

    Article  CAS  Google Scholar 

  • Jang M, Lee HJ, Shim Y (2010) Rapid removal of fine particles from mine water using sequential processes of coagulation and flocculation. Environ Technol 31:423–432

    Article  CAS  Google Scholar 

  • Kaushik P, Malik A (2013) Comparative performance evaluation of Aspergillus lentulus for dye removal through bioaccumulation and biosorption. Environ Sci Pollut Res 20(5):2882–2892

    Article  CAS  Google Scholar 

  • Kim DG, La HJ, Ahn CY, Park YH, Oh HM (2011) Harvest of Scenedesmus sp. with bioflocculant and reuse of culture medium for subsequent high-density cultures. Bioresour Technol 102:3163–3168

    Article  CAS  Google Scholar 

  • Koyun G (2015) Production of microalgal exopolysaccharides by Dictyosphaerium chlorelloides. Master Thesis University of Chemistry and Technology, Prague, Czech Republic

  • Kubiňáková E, Híveš J, Gál M, Fašková A (2017) Effect of ferrate on green algae removal. Environ Sci Pollut Res 24(27):21894–21901

    Article  CAS  Google Scholar 

  • Kumar V, Othman N, Asharuddin S (2017) Applications of natural coagulants to treat wastewater − a review. MATEC Web Conf 103:06016. https://doi.org/10.1051/matecconf/201710306016

    Article  CAS  Google Scholar 

  • Lal A, Das D (2016) Biomass production and identification of suitable harvesting technique for Chlorella sp. MJ 11/11 and Synechocystis PCC 6803. 3 Biotech 6(1):41

    Article  Google Scholar 

  • Lavoie A, Noüe J (1987) Harvesting of Scenedesmus obliquusin wastewaters: auto- or bioflocculation. Biotechnol Bioeng 30:852–859

    Article  CAS  Google Scholar 

  • Lee AK, Lewis DM, Ashman PJ (2010) Energy requirements and economic analysis of a full-scale microbial flocculation system for microalgal harvesting. Chem Eng Res Des 88(8):988–996

    Article  CAS  Google Scholar 

  • Lee M, Woo SG, Ten LN (2011) Shinella daejeonensis sp. nov., a nitrate-reducing bacterium isolated from sludge of a leachate treatment plant. Int J Syst Evol Micrbiol 61(9):2123–2128

    Article  CAS  Google Scholar 

  • Lee CS, Chong MF, Robinson JP, Binner ER (2014) A review on development and application of plant-based bio-flocculants and grafted bioflocculants. Ind Eng Chem Res 53:18357–18369. https://doi.org/10.1021/ie5034045

    Article  CAS  Google Scholar 

  • Lei X, Chen Y, Shao Z, Chen Z, Li Y, Zhu H, Zhang J, Zheng W, Zheng T (2015) Effective harvesting of the microalgae Chlorella vulgaris via flocculation-flotation with bioflocculant. Bioresour Technol 198:922–925

    Article  CAS  Google Scholar 

  • Lei X, Zheng W, Ding H, Zhu X, Chen Q, Xu H, Zheng T, Tian Y (2018) Effective harvesting of the marine microalga Thalassiosira pseudonana by Marinobacter sp. FL06. Bioresour Technol 269:127–133

    Article  CAS  Google Scholar 

  • Li Y, Moore R, Qin J, Scott A, Ball A (2013) Extractable liquid, its energy and hydrocarbon content in the green alga Botryococcus braunii. Biomass Bioenergy 52:103–112

    Article  CAS  Google Scholar 

  • Li Y, Xu Y, Liu L, Jiang X, Zhang K, Zheng T, Wang H (2016) First evidence of bioflocculant from Shinella albus with flocculation activity on harvesting of Chlorella vulgaris biomass. Bioresour Technol 218:807–815

    Article  CAS  Google Scholar 

  • Li Y, Xu Y, Liu L, Li P, Yan Y, Chen T, Zheng T, Wang H (2017a) Flocculation mechanism of Aspergillus niger on harvesting of Chlorella vulgaris biomass. Algal Res 25:402–412

    Article  Google Scholar 

  • Li Y, Xu Y, Zheng T, Wang H (2017b) Flocculation mechanism of the actinomycete Streptomyces sp. hsn06 on Chlorella vulgaris. Bioresour Technol 239:137–143

    Article  CAS  Google Scholar 

  • Li Y, Xu Y, Song R, Tian C, Liu L, Zheng T, Wang H (2018) Flocculation characteristics of a bioflocculant produced by the actinomycete Streptomyces sp. hsn06 on microalgae biomass. BMC Biotechnol 18:58

    Article  CAS  Google Scholar 

  • Liao W, Liu Y, Frear C, Chen S (2007) A new approach of pellet formation of a filamentous fungus-Rhizopus oryzae. Bioresour Technol 98:3415–3423

    Article  CAS  Google Scholar 

  • Lim JK, Chieh DCJ, Jalak SA, Toh PY, Yasin NHM, Ng BW, Ahmad AL (2012) Rapid Magnetophoretic Separation of Microalgae. Small 8:1683–1692

    Article  CAS  Google Scholar 

  • Liu WJ, Wang K, Li BZ, Yuan HL, Yang JS (2010) Production and characterization of an intercellular bioflocculant by Chryseobacterium daeguense W6 cultured in low nutrition medium. Bioresour Technol 101:1044–1048

    Article  CAS  Google Scholar 

  • Liu W, Zhao C, Jiang J, Lu Q, Hao Y, Wang L, Liu C (2015) Bioflocculant production from untreated corn stover using Cellulosimicrobium cellulans L804 isolate and its application to harvesting microalgae. Biotechnol Biofuels 8:170

    Article  CAS  Google Scholar 

  • Luo S, Wu X, Jiang H, Yu M, Liu Y, Min A, Li W, Ruan R (2019) Edible fungi-assisted harvesting system for efficient microalgae bioflocculation. Bioresour Technol 282:325–330

    Article  CAS  Google Scholar 

  • Ma X, Pawlik M (2007) Intrinsic viscosities and Huggins constants of guar gum in alkali metal chloride solutions. Carbohydr Polym 70:15–24

    Article  CAS  Google Scholar 

  • Ma X, Gao M, Gao Z, Wang J, Zhang M, Ma Y, Wang Q (2018) Past, current, and future research on microalga-derived biodiesel: a critical review and bibliometric analysis. Environ Sci Pollut Res 25:10596–10610. https://doi.org/10.1007/s11356-018-1453-0

    Article  Google Scholar 

  • Mackay S, Gomes E, Holliger C, Bauer R, Schwitzguebel JP (2015) Harvesting of Chlorella sorokiniana by co-culture with the filamentous fungus Isaria fumosorosea: a potential sustainable feedstock for hydrothermal gasification. Bioresour Technol 185:353–361. https://doi.org/10.1016/j.biortech.03.026

    Article  CAS  Google Scholar 

  • Mahapatra S, Banerjee D (2013) Fungal exopolysaccharide: production, composition and applications. Microbiol Insights 6:1–16

    Article  CAS  Google Scholar 

  • Matsui T, Shinzato N, Tamaki H, Muramatsu M, Hanada S (2009) Shinella yambaruensis sp. nov., a 3-methyl-sulfolane-assimilating bacterium isolated from soil. Int J Syst Evol Microbiol 59(3):536–539

    Article  CAS  Google Scholar 

  • Matter, Bui, Jung, Seo, Kim, Lee, Oh (2019) Flocculation Harvesting Techniques for Microalgae: A Review. Appl Sci 9:3069

    Article  CAS  Google Scholar 

  • Mauseth JD (2017) Plant anatomy laboratory micrograps of plant cells and tissues, with explonatory text

  • Milledge JJ, Heaven S (2013) A review of the harvesting of micro-algae for biofuel production. Rev Environ Sci Biotechnol 12(2):165–178

    Article  Google Scholar 

  • Miranda AF, Taha M, Wrede D, Morrison P, Ball AS, Stevenson T, Mouradov A (2015) Lipid production in association of filamentous fungi with genetically modified cyanobacterial cells. Biotechnol Biofuels 8:179. https://doi.org/10.1186/s13068-015-0364-2

    Article  CAS  Google Scholar 

  • Mishra A, Kavita K, Jha B (2011) Characterization of extracellular polymeric substances produced by micro-algae Dunaliella salina. Carbohydr Polym 83(2):852–857

    Article  CAS  Google Scholar 

  • Mofijur M, Rasul MG, Hassan NMS, Nabi MN (2019) Recent Development in the Production of Third Generation Biodiesel from Microalgae. Energy Procedia 156:53–58. https://doi.org/10.1016/j.egypro.2018.11.088

    Article  CAS  Google Scholar 

  • Muradov N, Taha M, Miranda AF, Wrede D, Kadali K, Gujar A, Stevenson T, Ball AS, Mouradov A (2015) Fungal-assisted algal flocculation: application in wastewater treatment and biofuel production. Biotechnol Biofuels 8:24

    Article  CAS  Google Scholar 

  • Nagarajan D, Lee DJ, Chen CY, Chang JS (2020) Resource recovery from wastewaters using microalgae-based approaches: a circular bioeconomy perspective. Bioresour Technol 302:122817. https://doi.org/10.1016/j.biortech.2020.122817

    Article  CAS  Google Scholar 

  • Nasir NM, Bakar NSA, Lananan F, Hamid SHA, Lam SS, Jusoh A (2015) Treatment of African catfish, Clarias gariepinus wastewater utilizing phytoremediation of microalgae, Chlorella sp. with Aspergillus niger bio-harvesting. Bioresour Technol 190:492–498

    Article  CAS  Google Scholar 

  • Nazari MT, Freitag JF, Cavanhi VAF, Colla LM (2020) Microalgae harvesting by fungal-assisted bioflocculation. Rev Environ Sci Biotechnol. https://doi.org/10.1007/s11157-020-09528-y

    Article  Google Scholar 

  • Ndikubwimana T, Zeng X, Liu Y, Chang JS, Lu Y (2014) Harvesting of microalgae Desmodesmus sp. F51 by bioflocculation with bacterial bioflocculant. Algal Res 6:186–193

    Article  Google Scholar 

  • Ndikubwimana T, Zeng X, Murwanashyaka T, Manirafasha E, He N, Shao W, Lu Y (2016) Harvesting of freshwater microalgae with microbial bioflocculant: a pilot-scale study. 19 489. Biotechnol Biofuels 9:1–11

    Article  CAS  Google Scholar 

  • Nharingo T, Zivurawa MT, Guyo U (2015) Exploring the use of cactus Opuntia ficus indica in the biocoagulation–flocculation of Pb (II) ions from wastewaters. Int J Environ Sci Technol 12:3791–3802

    Article  CAS  Google Scholar 

  • Oh HM, Lee SJ, Park MH, Kim HS, Kim HC, Yoon JH, Kwon GS, Yoon BD (2001) Harvesting of Chlorella vulgaris using a bioflocculant from Paenibacillus sp. AM49. Biotechnol Lett 23:1229–1234

    Article  CAS  Google Scholar 

  • Okoro V, Azimov U, Munoz J, Hernandez HH, Phan AN (2019) Microalgae cultivation and harvesting: Growth performance and use of flocculants - A review. Renewable Sustainable Energy Rev 115:109364

    Article  CAS  Google Scholar 

  • Papagianni M (2004) Fungal morphology and metabolite production in submerged mycelial processes. Biotechnol Adv 22:189–259

    Article  CAS  Google Scholar 

  • Parker CL (2013) The effects of environmental stressors on biofilm formation of Chlorella Vulgaris (Doctoral dissertation, Appalachian State University)

  • Paulsen BS, Aslaksen T, Freire-Nordi CS, Vieira AA (1998) Extracellular polysaccharides from Ankistrodesmus densus (Chlorophyceae). J Phycol 34(4):638–641

    Article  CAS  Google Scholar 

  • Pires JCM, Alvim-Ferraz MCM, Martins FG, Simões M (2013) Wastewater treatment to enhance the economic viability of microalgae culture. Environ Sci Pollut Res 20(8):5096–5105

    Article  CAS  Google Scholar 

  • Powell RJ, Hill RT (2013) Rapid aggregation of biofuel-producing algae by the bacterium Bacillus sp. strain RP1137. Appl Environ Microbiol 79:6093–6101

    Article  CAS  Google Scholar 

  • Powell RJ, Hill RT (2014) Mechanism of algal aggregation by Bacillus sp. strain RP1137. Appl Environ Microbiol 80(13):4042–4050

    Article  CAS  Google Scholar 

  • Prajapati SK, Kumar P, Malik A, Choudhary P (2014) Exploring pellet forming filamentous fungi as tool for harvesting non-flocculating unicellular microalgae. Bioenergy Res 7:1430–1440

    Article  CAS  Google Scholar 

  • Prajapati SK, Bhattacharya A, Kumar P, Malik A, Vijay VK (2016) A method for simultaneous bioflocculation and pretreatment of algal biomass targeting improved methane production. Green Chem 18:5230–5238. https://doi.org/10.1039/C6GC01483F

    Article  CAS  Google Scholar 

  • Prochazkova G, Safarik I, Branyik T (2013) Harvesting microalgae with microwave synthesized magnetic microparticles. Bioresour Technol 130:472–477

    Article  CAS  Google Scholar 

  • Rao AR, Dayananda C, Sarada R, Shamala TR, Ravishankar GA (2007) Effect of salinity on growth of green alga Botryococcus braunii and its constituents. Bioresour Technol 98(3):560–564

    Article  CAS  Google Scholar 

  • Rashid N, Rehman SU, Han JI (2013) Rapid harvesting of freshwater microalgae using chitosan. Process Biochem 48(7):1107–1110. https://doi.org/10.1016/j.procbio.2013.04.018

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Roselet F, Vandamme D, Muylaert K, Abreu PC (2019) Harvesting of Microalgae for Biomass Production. In: Alam M., Wang Z. (eds) Microalgae Biotechnology for Development of Biofuel and Wastewater Treatment. Springer, Singapore. https://doi.org/10.1007/978-981-13-2264-8_10

  • Sahin ÜA, Onat B, Ayvaz C (2019) Climate Change and Greenhouse Gases in Turkey. In: Balkaya N, Guneysu S (eds) Recycling and reuse approaches for better sustainability. Environmental Science and Engineering. Springer, Cham, pp 201–214. https://doi.org/10.1007/978-3-319-95888-0_17

    Chapter  Google Scholar 

  • 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 

  • Salim S, Vermuë MH, Wijffels RH (2012) Ratio between autoflocculating and target microalgae affects the energy-efficient harvesting by bio-flocculation. Bioresour Technol 118:49–55

    Article  CAS  Google Scholar 

  • Salim S, Kosterink NR, Tchetkoua Wacka ND, Vermuë MH, Wijffels RH (2014) Mechanism behind autoflocculation of unicellular green microalgae Ettlia texensis. J Biotechnol 174:34–38

    Article  CAS  Google Scholar 

  • Santos-Ballardo DU, Rossi S, Reyes-Moreno C, Valdez-Ortiz A (2016) Microalgae potential as a biogas source: current status, restraints and future trends. Rev Environ Sci Biotechnol 15(2):243–264

    Article  CAS  Google Scholar 

  • Selbmann L, Stingele F, Petruccioli M (2003) Exopolysaccharide production by filamentous fungi: the example of Botryosphaeria rhodina. Anton Leeuw Int J G 84:135–145

    Article  CAS  Google Scholar 

  • Selesu NF, de Oliveira TV, Corrêa DO, Miyawaki B, Mariano AB, Vargas JV, Vieira RB (2015) Maximum microalgae biomass harvesting via flocculation in large scale photobioreactor cultivation. Can J Chem Eng 94:304–309. https://doi.org/10.1002/cjce.22391

    Article  CAS  Google Scholar 

  • Shahid A, Malik S, Zhu H, Xu J, Nawaz MZ, Nawaz S, Alam MA, Mehmood MA (2020) Cultivating microalgae in wastewater for biomass production, pollutant removal, and atmospheric carbon mitigation: a review. Sci Total Environ 704:135303. https://doi.org/10.1016/j.scitotenv.2019.135303

    Article  CAS  Google Scholar 

  • Sheng GP, Yu HQ (2006) Chemical-equilibrium-based model for describing the strength of sludge: taking hydrogen producing sludge as an example. Environ Sci Technol 40:1280–1285

    Article  CAS  Google Scholar 

  • Shuman TR, Mason G, Marsolek MD et al (2014) An ultra-low energy method for rapidly pre-concentrating microalgae. Bioresour Technol 158C:217–224. https://doi.org/10.1016/j.biortech.2014.02.033

  • Singh G, Patidar SK (2018) Microalgae harvesting techniques: A review. J Environ Manage 217:499–508

    Article  Google Scholar 

  • Sirin S, Trobajo R, Ibanez C, Salvadó J (2012) Harvesting the microalgae Phaeodactylum tricornutum with polyaluminum chloride, aluminium sulphate, chitosan and alkalinity-induced flocculation. J Appl Phycol 24:1067–1080

    Article  CAS  Google Scholar 

  • Sitanggang AB, Wu H-S, Wang SS, Ho Y-C (2010) Effect of pellet size and stimulating factor on the glucosamine production using Aspergillus sp. BCRC 31742. Bioresour Technol 101(10):3595–3601

    Article  CAS  Google Scholar 

  • Sivasankara P, Poongodi S, Lobo AO, Pugazhendhi A (2020) Characterization of a novel polymeric bioflocculant from marine actinobacterium Streptomyces sp. and its application in recovery of microalgae. Int Biodeterior Biodegradation 148:104883

    Article  CAS  Google Scholar 

  • Srinuanpan S, Chawpraknoi A, Chantarit S, Cheirsilp B, Prasertsan P (2018) A rapid method for harvesting and immobilization of oleaginous microalgae using pellet-forming filamentous fungi and the application in phytoremediation of secondary effluent. Int J Phytoremediation 20:1017–1024

    Article  CAS  Google Scholar 

  • Stratford M (1992) Yeast flocculation: a new perspective. Adv Microb Physiol 33:1–71 Academic Press

    Article  CAS  Google Scholar 

  • Surendhiran D, Vijay M (2014) Exploration on bioflocculation of Nannochloropsis oculata using response surface methodology for biodiesel production. Sci World J.

    Google Scholar 

  • Sutherland IW (1996) Extracellular polysaccharides. In: Rhem HJ, Reed G (eds) Biotechnology, vol 6. VCH, Weinheim, pp 615–657

    Google Scholar 

  • Thomas DM, Mechery J, Paulose SV (2016) Carbon dioxide capture strategies from flue gas using microalgae: a review. Environ Sci Pollut Res 23:16926–16940. https://doi.org/10.1007/s11356-016-7158-3

    Article  CAS  Google Scholar 

  • Uduman N, Qi Y, Danquah MK, Hoadley AF (2010) Marine microalgae flocculation and focused beam reflectance measurement. Chem Eng J 162:935–940

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Vandamme D, Pontes SCV, Goiris K, Foubert I, Pinoy LJJ, Muylaert K (2011) Evaluation of electro-coagulation-flocculation for harvesting marine and freshwater microalgae. Biotechnol Bioeng 108:2320–2329

    Article  CAS  Google Scholar 

  • Verstrepen KJ, Derdelinckx G, Verachtert H, Delvaux FR (2003) Yeast flocculation: what brewers should know. Appl Microbiol Biotechnol 61(3):197–205

    Article  CAS  Google Scholar 

  • Vishali S, Karthikeyan R (2014) Cactus opuntia (ficus-indica): an eco-friendly alternative coagulant in the treatment of paint effluent. Desalin Water Treat 56:1489–1497. https://doi.org/10.1080/19443994.2014.945487

    Article  CAS  Google Scholar 

  • Vogelaar JCT, Keizer AD, Spijker S, Lettinga G (2005) Bioflocculation of mesophilic and thermophilic activated sludge. Water Res 39(1):37–46

    Article  CAS  Google Scholar 

  • Wan C, Zhao XQ, Guo SL, Alam MA, Bai FW (2013) Bioflocculant production from Solibacillus silvestris W01 and its application in cost-effective harvest of marine microalga Nannochloropsis oceanica by flocculation. Bioresour Technol 135:207–212

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wang L, Ma F, Qu Y, Sun D, Li A, Guo J, Yu B (2011) Characterization of a 515 compound bioflocculant produced by mixed culture of Rhizobium radiobacter F2 and Bacillus sphaeicus F6. World J Microbiol Biotechnol 27:2559–2565

    Article  CAS  Google Scholar 

  • Wang H, Laughinghouse HD IV, Anderson MA, Chen F, Willliams E, Place AR, Zmora O, Zohar Y, Zheng T, Hill RT (2012) Novel bacterial isolate from Permian groundwater, capable of aggregating potential biofuel-producing microalga Nannochloropsis oceanica IMET1. Appl Environ Microbiol 78(5):1445–1453

    Article  CAS  Google Scholar 

  • Wang M, Kuo-Dahab WC, Dolan S, Park C (2014) Kinetics of nutrient removal and expression of extracellular polymeric substances of the microalgae, Chlorella sp. and Micractinium sp., in wastewater treatment. Bioresour Technol 154:131–137

    Article  CAS  Google Scholar 

  • Wang H, Qi B, Jiang X, Jiang Y, Yang H, Xiao Y, Jiang N, Deng L, Wang W (2019) Microalgal interstrains differences in algal-bacterial biofloc formation during liquid digestate treatment. Bioresour Technol 289:121741

    Article  CAS  Google Scholar 

  • Wrede D, Taha M, Miranda AF, Kadali K, Stevenson T, Ball AS, 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

    Article  CAS  Google Scholar 

  • Xia CJ, Zhang JG, Zhang WD, Hu B (2011) A new cultivation method for microbial oil production: cell pelletization and lipid accumulation by Mucor circinelloides. Biotechnol Biofuels 4:15

    Article  Google Scholar 

  • Xiao R, Zheng Y (2016) Overview of microalgal extracellular polymeric substances (EPS) and their applications. Biotechnol Adv 34(7):1225–1244

    Article  CAS  Google Scholar 

  • Xu L, Guo C, Wang F, Zheng S, Liu CZ (2011) A simple and rapid harvesting method for microalgae by in situ magnetic separation. Bioresour Technol 102:10047–10051

    Article  CAS  Google Scholar 

  • Yang H, He G (2008) Influence of nutritional conditions on exopolysaccharide production by submerged cultivation of the medicinal fungus Shiraia bambusicola. World J Microbiol Biotechnol 24(12):2903–2907

    Article  CAS  Google Scholar 

  • Yang L, Zhang H, Cheng S, Zhang W, Zhang X (2020) Enhanced microalgal harvesting using microalgae-derived extracellular polymeric substance as flocculation aid. ACS Sustain Chem Eng 8(10):4069–4075

    Article  CAS  Google Scholar 

  • Yokoi H, Arima T, Hirose J, Hayashi S, Takasaki Y (1996) Flocculation properties of poly (γ-glutamic acid) produced by Bacillus subtilis. J Ferment Bioeng 82:84–87

    Article  CAS  Google Scholar 

  • Zhang J, Hu B (2012) A novel method to harvest microalgae via co-culture of filamentous fungi to form cell pellets. Bioresour Technol 114:529–535

    Article  CAS  Google Scholar 

  • Zhao Y, Wang X, Jiang X, Fan Q, Li X, Jiao L, Liang W (2018) Harvesting of Chlorella vulgaris using Fe 3 O 4 coated with modified plant polyphenol. Environ Sci Pollut Res 25(26):26246–26258

    Article  CAS  Google Scholar 

  • Zhao F, Xiao J, Ding W, Cui N, Yu X, Xu JW, Zhao P (2019) An effective method for harvesting of microalga: coculture-induced self-flocculation. J Taiwan Inst Chem Eng 100:117–126

    Article  CAS  Google Scholar 

  • Zheng H, Gao Z, Yin J, Tang X, Ji X, Huang H (2012) Harvesting of microalgae by flocculation with poly (γ-glutamic acid). Bioresour Technol 112:212–220

    Article  CAS  Google Scholar 

  • Zhou W, Cheng Y, Li Y, Wan Y, Liu Y, Lin X, Ruan R (2012) Novel fungal pelletization-assisted technology for algae harvesting and wastewater treatment. Appl Biochem Biotechnol 167:214–228

    Article  CAS  Google Scholar 

  • Zhou W, Min M, Hu B, Ma X, Liu Y, Wang Q, Shi J, Chen P, Ruan R (2013) Filamentous fungi assisted bioflocculation: a novel alternative technique for harvesting heterotrophic and autotrophic microalgal cells. Sep Purif Technol 107:158–165

    Article  CAS  Google Scholar 

  • Sarang MC, Nerurkar AS (2020) Amyloid protein produced by B. cereus CR4 possesses bioflocculant activity and has potential application in microalgae harvest. Biotechnol Lett 42:79–91

    Article  CAS  Google Scholar 

  • Jiang J, Jin W, Tu R, Han S, Ji Y, Zhou X (2021) Harvesting of Microalgae Chlorella pyrenoidosa by Bio-flocculation with Bacteria and Filamentous Fungi. Waste Biomass Valori 12:145–154

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge Department of Biotechnology (DBT), India, for their financial assistance and Indian Institute of Technology Kharagpur, India, for the research facilities.

Funding

The authors thank Department of Biotechnology (DBT), Govt. of India (grant no: BT/EB/PANIIT/2012) for financial support and Indian Institute of Technology Kharagpur, India, for the research facilities.

Author information

Authors and Affiliations

  1. P K Sinha Centre for Bioenergy and Renewables, Indian Institute of Technology Kharagpur, Kharagpur, 721302, India

    Ayusmita Ray & Debabrata Das

  2. Department of Biotechnology, Indian Institute of Technology Kharagpur, Kharagpur, 721302, India

    Sanjukta Banerjee & Debabrata Das

Authors
  1. Ayusmita Ray
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sanjukta Banerjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Debabrata Das
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AR and SB have contributed equally in data collection for microalgal bioflocculation and preparation of this manuscript, and should be treated as joint first authors.

DD was involved in idea conceptualization, manuscript formatting and corrections.

Corresponding author

Correspondence to Debabrata Das.

Ethics declarations

Ethics approval and consent to participate

Not applicable. The authors consent to participate.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Ta Yeong Wu

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Ayusmita Ray and Sanjukta Banerjee are co-first Authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ray, A., Banerjee, S. & Das, D. Microalgal bio-flocculation: present scenario and prospects for commercialization. Environ Sci Pollut Res 28, 26294–26312 (2021). https://doi.org/10.1007/s11356-021-13437-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-13437-0

Keywords

Search

Navigation