Skip to main content

Advertisement

SpringerLink
Log in

Microalgae autoflocculation: an alternative to high-energy consuming harvesting methods

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

With increasing concerns regarding energy and environment, algae biofuel is generating considerable interest around the world. Nevertheless, the harvesting step required before downstream biomass processing is a major bottleneck. Commonly employed methods include addition of chemicals or use of mechanical equipment that increase dramatically the biofuel production cost. This review deals with naturally occurring processes that can help offset those costs by causing microalgae flocculation. Interaction theories are briefly reviewed. In addition, operational parameters such as pH, irradiance, nutrients, dissolved oxygen, and temperature effect on microalgae flocculation are evaluated. Finally, microalgae flocculation is also considered from an ecological point of view by taking advantage of their interaction with other microorganisms.

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

Similar content being viewed by others

References

  • Acien FG, González CV, Fernández JM, García-González M, Moreno J, Sierra E, Guerrero MG, Molina E (2008) Removal of CO2 from flue gases coupled to the photosynthetic generation of biomass and exopolysaccharides by cyanobacteria. In: Proceedings 11th International Conference on Applied Phycology, Galway, Ireland

  • Andreadakis AD (1993) Physical and chemical properties of activated sludge floc. Water Res 27:1707–1714

    Article  CAS  Google Scholar 

  • Ayoub GM, Lee SI, Koopman B (1986) Seawater induced algal flocculation. Water Res 20:1265–1271

    Article  CAS  Google Scholar 

  • Barsky EL, Gusev MV, Kazennova NV, Samuilov VD (1984) Surface charge on thylakoid membranes: regulation of photosynthetic electron transfer in cyanobacteria. Arch Microbiol 138:54–57

    Article  Google Scholar 

  • Belkin S, Boussiba S (1991) Resistance of Spirulina platensis to ammonia at high pH values. Plant Cell Physiol 32:953–958

    CAS  Google Scholar 

  • Benemann JR (2008) Opportunities and challenges in algae biofuel production. FAO, Algae World, Singapore

    Google Scholar 

  • Bilad MR, Vandamme D, Foubert I, Muylaert K, Vankelecom IFJ (2012) Harvesting microalgal biomass using submerged microfiltration membranes. Bioresource Technol 111:343–352

    Article  CAS  Google Scholar 

  • Borowitzka MA (1992) Algal biotechnology products and processes—matching science and economics. J Appl Phycol 4:267–279

    Article  Google Scholar 

  • Borowitzka MA (1999) Economic evaluation of microalgal processes and products. In: Cohen Z (ed) Chemicals from microalgae. Taylor & Francis, London, pp 387–409

    Google Scholar 

  • Borowitzka MA, Moheimani NR (2010) Sustainable biofuels from algae. Mitig Adapt Strat Glob Chang. doi:10.1007/s11027-010-9271-9

  • 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 

  • Cordoba-Castro NM, Gonzalez-Marino GE, Montenegro Jaramillo AM, Prieto Correa RE (2012) Analysis of the effect of the interactions among three processing variables for the production of exopolysaccharides in the microalgae Scenedesmus obliquus (UTEX 393). Vitae 19:60–69

    CAS  Google Scholar 

  • Craggs RJ, Davies-Colley RJ, Tanner CC, Sukias JP (2003) Advanced pond system: performance with high rate ponds of different depths and areas. Water Sci Technol 48:259–267

    PubMed  CAS  Google Scholar 

  • Davis R, Aden A, Pienkos PT (2011) Techno-economic analysis of autotrophic microalgae for fuel production. Appl Energy 88:3524–3531

    Article  Google Scholar 

  • De Benardi R, Guissani G (1990) Are blue-green algae suitable food for zooplankton? An overview. Hydrobiologia 200/201:29–41

    Article  Google Scholar 

  • Dismukes GC, Carrieri D, Bennette N, Ananyev GM, Posewitz MC (2008) Aquatic phototrophs: efficient alternatives to land-based crops for biofuels. Curr Opin Biotechnol 19:235–240

    Article  PubMed  CAS  Google Scholar 

  • Dugdale TM, Willis A, Wetherbee R (2006) Adhesive modular proteins occur in the extracellular mucilage of the motile, pennate diatom Phaeodactylum tricornutum. Biophys J 90:L58–L60

    Article  PubMed  CAS  Google Scholar 

  • Fon Sing S, Isdepsky A, Borowitzka MA, Moheimani NR (2011) Production of biofuels from microalgae. Mitig Adapt Strateg Glob Chang. doi:10.1007/s11027-011-9294-x

  • Golueke CG, Oswald WJ (1970) Surface properties and ion exchange in algae removal. J Water Pollut Control Fed 42:R304–R314

    CAS  Google Scholar 

  • González-Fernández C, Molinuevo-Salces B, García-González MC (2010) Nitrogen transformations under different conditions in open ponds by means of microalgae–bacteria consortium treating pig slurry. Bioresource Technol 102:960–966

    Article  Google Scholar 

  • González-Fernández C, Sialve B, Bernet N, Steyer J-P (2012) Impact of microalgae characteristics on their conversion to biofuel. Part I: Focus Cultivation Biofuel Biofuels Bioprod Bioref 6:105–113

    Article  Google Scholar 

  • Granados MR, Acién FG, Gómez C, Fernández-Sevilla JM, Molina Grima E (2012) Evaluation of flocculants for the recovery of freshwater microalgae. Bioresource Technol 118:102–110

    Article  CAS  Google Scholar 

  • Gutzeit G, Lorch D, Weber A, Engels M, Neis U (2005) Bioflocculent algal–bacterial biomass improves low-cost wastewater treatment. Water Sci Technol 52:9–18

    PubMed  CAS  Google Scholar 

  • Frølund B, Palmgren R, Keiding K, Nielsen PH (1996) Extraction of extracellular polymers from activated sludge using a cation exchange resin. Water Res Oxf 30:1749. doi:10.1016/0043-1354(95)00323-1

    Article  Google Scholar 

  • Hallenbeck PC, Benemann J (2002) Biological hydrogen production; fundamentals and limiting processes. Int J Hydrogen Energ 27:1185–1193

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Horiuchi J-I, Ohba I, Tada K, Kobayashi M, Kanno T, Kishimoto M (2003) Effective cell harvesting of the halotolerant microalga Dunaliella tertiolecta with pH control. J Biosci Bioeng 95:412–415

    PubMed  CAS  Google Scholar 

  • Janssen M, Tramper J, Mur LR, Wijffels RH (2003) Enclosed outdoor photobioreactors: light regime, photosynthetic efficiency, scale up, and future prospects. Biotechnol Bioeng 81:193–210

    Article  PubMed  CAS  Google Scholar 

  • Johnson MR, Montero CI, Conners SB, Shockley KR, Bridger SL, Kelly RM (2005) Population density-dependent regulation of exopolysaccharide formation in the hyperthermophilic bacterium Thermotoga maritima. Mol Microbiol 55:664–674

    Article  PubMed  CAS  Google Scholar 

  • Jorand F, Boué-Bigne F, Block JC, Urbain V (1998) Hydrophobic/hydrophilic properties of activated sludge exopolymeric substances. Water Sci Technol 37:307–315

    CAS  Google Scholar 

  • Kim DG, La HJ, Ahn CY, Park YH, Oh HM (2010) Harvest of Scenedesmus sp. with bioflocculant and reuse of culture medium for subsequent high-density cultures. Bioresource Technol 102:3163–3168

    Article  Google Scholar 

  • Kurane R, Nohata Y (1991) Microbial flocculation of waste liquids and oil emulsion by a bioflocculant from Alcaligenes latus. Agric Biol Chem 55:1127–1129

    Article  CAS  Google Scholar 

  • Kyong H, Jang MH, Joo GJ, Takamura N (2001) Growth and morphological changes in Scenedesmus dimorphus induced by substances released from grazers, Daphnia magna and Moina macrocopa. Korean J Limnol 34:285–291

    Google Scholar 

  • Lavoie A, de la Noue J, Serodes JB (1984) Recovery of microalgae in wastewater: a comparative study of different flocculating agents. Can J Civil Eng 11:266–272

    Article  Google Scholar 

  • Lavoie A, de la Noüe J (1987) Harvesting of Scenedesmus obliquus in wastewaters: auto- or bioflocculation? Biotechnol Bioeng 30:852–859

    Article  PubMed  CAS  Google Scholar 

  • Lee SJ, Kim SB, Kim JE, Kwon GS, Yoon BD, Oh HM (1998) Effects of harvesting method and growth stage on the flocculation of the green alga Botryococcus braunii. Lett Appl Microbiol 27:14–18

    Article  Google Scholar 

  • Lee AK, Lewis DM, Ashman PJ (2009) Microbial flocculation, a potentially low-cost harvesting technique for marine microalgae for the production of biodiesel. J Appl Phycol 21:559–567

    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 88:988–996

    Article  CAS  Google Scholar 

  • Leflaive J, Lacroix G, Nicaise Y, Ten-Hage L (2008) Colony induction and growth inhibition in Desmodesmus quadrispina (Chlorococcales) by allelochemicals released from the filamentous alga Uronema confervicolum (Ulotrichales). Environ Microbiol 10:1536–1546

    Article  PubMed  CAS  Google Scholar 

  • Liao BQ, Allen DG, Droppo IG, Leppard GG, Liss SN (2001) Surface properties of sludge and their role in bioflocculation and settleability. Water Res 35:339–350

    Article  PubMed  CAS  Google Scholar 

  • Lupi FM, Fernandes HML, Sá-Correia I, Novais JM (1991) Temperature profiles of cellular growth and exopolysaccharide synthesis by Botryococus braunii Kütz. UC 58. J Appl Phycol 3:35–42

    Article  CAS  Google Scholar 

  • Lurling M, van Donk E (1997) Morphological changes in Scenedesmus induced by infochemicals released in situ from zooplankton grazers. Limnol Oceanogr 42:783–788

    Article  Google Scholar 

  • Lurling M, de Lange HJ, van Donk E (1997) Changes in food quality of the green alga Scenedesmus induced by Daphnia infochemicals: biochemical composition and morphology. Freshwat Biol 38:619–628

    Article  CAS  Google Scholar 

  • Moheimani NR, Borowitzka MA (2011) Increased CO2 and the effect of pH on growth and calcification of Pleurochrysis carterae and Emiliania huxleyi (Haptophyta) in semicontinuous cultures. Appl Microbiol Biotechnol 90:1399–1407

    Article  PubMed  CAS  Google Scholar 

  • Moheimani N (2012) Long term outdoor growth and lipid productivity of Tetraselmis suecica, Dunaliella tertiolecta, and Chlorella sp (Chlorophyta) in bag photobioreactors. J Appl Phycol. doi:10.1007/s10811-012-9850-0

  • Mohn FH (1988) Harvesting of micro-algal biomass. In: Borowitzka MA, Borowitzka LJ (eds) Micro-algal Biotechnology. Cambridge University Press, Cambridge, pp 395–414

    Google Scholar 

  • Molina Grima E, Belarbi E, Acien Fernandez F, Robles Medina A, Chisti Y (2003) Recovery of microalgal biomass and metabolites: process options and economics. Biotechnol Adv 20:491–515

    Article  PubMed  CAS  Google Scholar 

  • Molinuevo-Salces B, García-González MC, González-Fernández C (2010) Performance comparison of two photobioreactors configurations (open and closed to the atmosphere) treating anaerobically degraded swine manure. Bioresource Technol 101:5144–5149

    Article  CAS  Google Scholar 

  • Moreno J, Vargas MA, Olivares H, Rivas J, Guerrero MG (1998) Exopolysaccharide production by the cyanobacterium Anabaena sp. ATCC 33047 in batch and continuous culture. J Biotechnol 60:175–182

    Article  CAS  Google Scholar 

  • Norsker NH, Barbosa MJ, Vermuë MH, Wijffels RH (2011) Microalgal production—a close look at economics. Biotechnol Adv 29:24–27

    Article  PubMed  CAS  Google Scholar 

  • Ntsaluba L, Agundiade O, Mabinya L, Okoh A (2011) Studies on bioflocculant production by Methylobacterium sp. Obi isolated from a freshwater environment in South Africa. Afr J Microbiol Res 5:4533–4540

    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 

  • Park JBK, Craggs RJ (2010) Wastewater treatment and algal production in high rate algal ponds with carbon dioxide addition. Water Sci Technol 61:633–639

    Article  PubMed  CAS  Google Scholar 

  • Park JB, Craggs RJ, Shilton AN (2011) Recycling algae to improve species control and harvest efficiency from a high rate algal pond. Water Res 15:6637–6649

    Article  Google Scholar 

  • Petrusevski B, van Breemen AN, Alaerts GJ, Bolier G (1995) Tangential flow filtration: a method to concentrate freshwater algae. Water Res 29:1419–1424

    Article  CAS  Google Scholar 

  • Poelman E, de Pauw N, Jeurissen B (1997) Potential of electrolytic flocculation for recovery of micro-algae. Res Conserv Rec 19:1–10

    Article  Google Scholar 

  • Posten C (2009) Design principles of photo-bioreactors for cultivation of microalgae. Eng Life Sci 9:165–177

    Article  CAS  Google Scholar 

  • Pulz O (2001) Photobioreactors: production systems for phototrophic microorganisms. Appl Microbiol Biot 57:287–293

    Article  CAS  Google Scholar 

  • Rebolloso-Fuentes MM, García Sánchez JL, Fernández Sevilla JM, Acien Fernández FG, Sánchez Pérez JA, Molina Grima E (1999) Outdoor continuous culture of Porphyridium cruentum in a tubular photobioreactor: quantitative analysis of the daily cyclic variation of culture parameters. J Biotechnol 70:271–288

    Article  CAS  Google Scholar 

  • Salehizadeh H, Shojaosadati S (2001) Extracellular biopolymeric flocculants: recent trends and biotechnological importance. Biotechnol Adv 19:371–385

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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. Biotechnology Adv 30:1023–1030

    Article  CAS  Google Scholar 

  • Schryver PD, Crab R, Defoirdt T, Boon N, Verstraete W (2008) The basics of bio-flocs technology: the added value for aquaculture. Aquaculture 277:125–137

    Article  Google Scholar 

  • Shelef G, Sukenik A, Green M (1984) Microalgae harvesting and processing: a literature review. Subcontract report, no. XK-3-03031-01. U.S. Department of Energy

  • Shin HS, Kang ST, Nam SY (2001) Effect of carbohydrate and protein in the EPS on sludge settling characteristics. Water Sci Technol 43:193–196

    PubMed  CAS  Google Scholar 

  • Schnoor JL, Di Toro DM (1980) Differential phytoplankton sinking- and growth-rates: an eigenvalue analysis. Ecol Model 9:233–245

    Article  Google Scholar 

  • Sigee DC (2005) Freshwater microbiology: biodiversity and dynamic interactions of microorganisms in the aquatic environment. Wiley, UK

    Google Scholar 

  • Şirin 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

    Google Scholar 

  • Smith BT, Davis RH (2012) Sedimentation of algae flocculated using naturally-available, magnesium-based flocculants. Algal Res 1:32–39

    Article  CAS  Google Scholar 

  • Spilling K, Seppälä J, Tamminen T (2011) Inducing autoflocculation in the diatom Phaeodactylum tricornutum through CO2 regulation. J Appl Phycol 23:959–966

    Article  CAS  Google Scholar 

  • Stephens E, Ross IL, King Z, Mussgnug JH, Kruse O, Posten C, Borowitzka MA, Hankamer B (2010) An economic and technical evaluation of microalgal biofuels. Nature Biotechnol 28:126–128

    Article  CAS  Google Scholar 

  • Sukenik A, Shelef G (1984) Algal autoflocculation—verification and proposed mechanism. Biotechnol Bioeng 26:142–147

    Article  PubMed  CAS  Google Scholar 

  • 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 Energ 2:012701–012701

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Vonshak A, Richmond A (1988) Mass production of the blue green algae Spirulina: an overview. Biomass 15:233–247

    Article  Google Scholar 

  • Wilén BM, Balmér P (1999) The effect of dissolved oxygen concentration on the structure, size and size distribution of activated sludge flocs. Water Res 33:391–400

    Article  Google Scholar 

  • Wiltshire KH, Lampert W (1999) Urea excretion by Daphnia: a colony-inducing factor in Scenedesmus? Limnol Oceanogr 44:1894–1903

    Article  CAS  Google Scholar 

  • Wu Z, Zhu Y, Huang W, Zhang C, Li T, Zhang Y, Li A (2012) Evaluation of flocculation induced by pH increase for harvesting microalgae and reuse of flocculated medium. Bioresource Technol 110:496–502

    Article  CAS  Google Scholar 

  • Wyatt NB, Gloe LM, Brady PV, Hewson JC, Grillet AM, Hankins MG, Pohl PI (2012) Critical conditions for ferric chloride-induced flocculation of freshwater algae. Biotechnol Bioeng 109:493–501

    Article  PubMed  CAS  Google Scholar 

  • Xia S, Zhang Z, Wang X, Yang A, Chen L, Zhao J, Leonard D, Jaffrezic-Renault N (2008) Production and characterization of a bioflocculant by Proteus mirabilis TJ-1. Bioresource Technol 99:6520–6527

    Article  CAS  Google Scholar 

  • Yahi H, Elmaleh S, Coma J (1994) Algal flocculation–sedimentation by pH increase in a continuous reactor. Water Sci Technol 30:259–267

    CAS  Google Scholar 

  • Yang Z, Kong F, Yang Z, Zhang M, Yu Y, Qian S (2009) Benefits and costs of the grazer-induced colony formation in Microcystis aeruginosa. Ann Limnol- Int J Lim 45:203–208

    Article  Google Scholar 

  • Young KD (2006) The selective value of bacterial shape. Microbiol Mol Biol Rev 70:660–703

    Article  PubMed  Google Scholar 

  • Zhang X, Amendola P, Hewson JC, Sommerfeld M, Hu Q (2012) Influence of growth phase on harvesting of Chlorella zofingiensis by dissolved air flotation. Bioresource Technol 116:477–484

    Article  CAS  Google Scholar 

  • Zitelli GC, Rodolfi L, Biondi N, Tredici MR (2006) Productivity and photosynthetic efficiency of outdoor cultures of Tetraselmis suecica in annular columns. Aquaculture 261:932–943

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. IMDEA Energy, Avda. Ramón de la Sagra 3, 28935, Móstoles, Madrid, Spain

    Cristina González-Fernández & Mercedes Ballesteros

  2. CIEMAT, Avda Complutense, 28040, Madrid, Spain

    Mercedes Ballesteros

Authors
  1. Cristina González-Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mercedes Ballesteros
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Cristina González-Fernández.

Rights and permissions

Reprints and permissions

About this article

Cite this article

González-Fernández, C., Ballesteros, M. Microalgae autoflocculation: an alternative to high-energy consuming harvesting methods. J Appl Phycol 25, 991–999 (2013). https://doi.org/10.1007/s10811-012-9957-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-012-9957-3

Keywords

Search

Navigation