Environmental Science and Pollution Research

, Volume 26, Issue 16, pp 16708–16715 | Cite as

Comparison and optimization of different methods for Microcystis aeruginosa’s harvesting and the role of zeta potential on its efficiency

  • Pedro GeadaEmail author
  • Francisca Oliveira
  • Luís Loureiro
  • Diogo Esteves
  • José A. Teixeira
  • Vítor Vasconcelos
  • António A. Vicente
  • Bruno D. Fernandes
Research Article


This study has compared the harvesting efficiency of four flocculation methods, namely, induced by pH, FeCl3, AlCl3 and chitosan. No changes were observed on M. aeruginosa cells. Flocculation assays performed at pH 3 and 4 have shown the best harvesting efficiency among the pH-induced tests, reaching values above 90% after 8 h. The adjustment of zeta potential (ZP) to values comprised between − 6.7 and − 20.7 mV enhanced significantly the settling rates using flocculant agents, being FeCl3 the best example where increments up to 88% of harvesting efficiency were obtained. Although all the four methods tested have presented harvesting efficiencies above 91% within the first 8 h after the optimization process, the highest performance was obtained using 3.75 mg L−1 of FeCl3, which allowed reaching 92% in 4 h.


Induced flocculation Zeta potential Harvesting efficiency Microcystis aeruginosa 


Funding information

This research work was supported by the grants SFRH/BPD/98694/2013 (Bruno Fernandes) and SFRH/BD/52335/2013 (Pedro Geada) from Fundação para a Ciência e a Tecnologia (Portugal). Luís Loureiro is recipient of a fellowship supported by a doctoral advanced training (call NORTE-69-2015-15) funded by the European Social Fund under the scope of Norte2020 - Programa Operacional Regional do Norte. This study was supported by the Portuguese Foundation for Science and Technology (FCT) under the scope of the FCT Strategic funding of UID/BIO/04469/2013 unit and COMPETE 2020 (POCI-01-0145-FEDER-006684) and BioTecNorte operation (NORTE-01-0145-FEDER-000004) funded by the European Regional Development Fund under the scope of Norte2020 - Programa Operacional Regional do Norte. This study was also supported by the Project UID/Multi/04423/2013, the Project RECI/BBB-EBI/0179/2012 (FCOMP-01-0124-FEDER-027462), and the project NOVELMAR (reference NORTE-01-0145-FEDER-000035) co-financed by the North Portugal Regional Operational Programme (Norte 2020) under the National Strategic Reference Framework (NSRF) through the ERDF.


  1. Braithwaite SP, Voronkov M, Stock JB, Mouradian MM (2012) Targeting phosphatases as the next generation of disease modifying therapeutics for Parkinson’s disease. Neurochem Int 61:899–906. CrossRefGoogle Scholar
  2. Chen G, Zhao L, Qi Y, Cui Y-L (2014) Chitosan and its derivatives applied in harvesting microalgae for biodiesel production: an outlook. J Nanomat 2014:217537. Google Scholar
  3. Chow CWK, House J, Velzeboer RMA, Drikas M, Burch MD, Steffensen DA (1998) The effect of ferric chloride flocculation on cyanobacterial cells. Water Res 32:808–814. CrossRefGoogle Scholar
  4. Geada P, Gkelis S, Teixeira J, Vasconcelos V, Vicente A, Fernandes B (2017) Chapter 17: Cyanobacterial toxins as a high added-value product. In: Muñoz R, Gonzalez C (eds) Microalgae-based biofuels and bioproducts. Woodhead Publishing, Cambridge, pp 405–432Google Scholar
  5. Giannuzzi L, Sedan D, Echenique R, Andrinolo D (2011) An acute case of intoxication with cyanobacteria and cyanotoxins in recreational water in Salto Grande Dam, Argentina. Mar Drugs 9:2164–2175. CrossRefGoogle Scholar
  6. Gonzalez-Torres A, Putnam J, Jefferson B, Stuetz RM, Henderson RK (2014) Examination of the physical properties of Microcystis aeruginosa flocs produced on coagulation with metal salts. Water Res 60:197–209. CrossRefGoogle Scholar
  7. Griffiths MJ, Garcin C, van Hille RP, Harrison ST (2011) Interference by pigment in the estimation of microalgal biomass concentration by optical density. J Microbiol Methods 85:119–123. CrossRefGoogle Scholar
  8. Hadjoudja S, Deluchat V, Baudu M (2010) Cell surface characterisation of Microcystis aeruginosa and Chlorella vulgaris. J Colloid Interface Sci 342:293–299. CrossRefGoogle Scholar
  9. Harke MJ, Stefffen MM, Gobler CJ, Otten TG, Wilhelm SW, Wood SA, Paerl HW (2016) A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium, Microcystis spp. Harmful Algae 54:4–20. CrossRefGoogle Scholar
  10. Ilić M, Svirčev Z, Baltić V (2011) Microcystins—potent xenobiotics. Arch Oncol 19:67–72. CrossRefGoogle Scholar
  11. Jiang C, Wang R, Ma W (2010) The effect of magnetic nanoparticles on Microcystis aeruginosa removal by a composite coagulant. Colloids Surf A Physicochem Eng Asp 369:260–267. CrossRefGoogle Scholar
  12. Jochimsen EM, Carmichael WW, Cardo D, Cookson ST, Holmes CEM, Antunes BC, Filho DAM, Lyra TM, Barreto VS, Azevedo SMFO, Jarvis W (1998) Liver failure and death after exposure to microcystins at a hemodialysis center in Brazil. N Engl J Med 338:873–878CrossRefGoogle Scholar
  13. Kotai J (1972) Instructions for preparation of modified nutrient solution Z8 for algae. Norwegian Institute for Water Research, Blindern, p 5Google Scholar
  14. Li L, Zhang H, Pan G (2015) Influence of zeta potential on the flocculation of cyanobacteria cells using chitosan modified soil. J Environ Sci (China) 28:47–53. CrossRefGoogle Scholar
  15. Lin Z, Xu Y, Zhen Z, Fud Y, Liu Y, Li W, Luo C, Ding A, Zhang D (2015) Application and reactivation of magnetic nanoparticles in Microcystis aeruginosa harvesting. Bioresour Technol 190:82–88. CrossRefGoogle Scholar
  16. Liu J, Zhu Y, Tao Y, Zhang Y, Li A, Li T, Sang M, Zhang C (2013) Freshwater microalgae harvested via flocculation induced by pH decrease. Biotechnol Biofuels 6:98–108. CrossRefGoogle Scholar
  17. Lürling M, Noymac NP, Magalhães L, Miranda M, Mucci M, van Oosterhout F, Huszar VLM, Marinho MM (2017) Critical assessment of chitosan as coagulant to remove cyanobacteria. Harmful Algae 66:1–12. CrossRefGoogle Scholar
  18. Ma M, Liu R, Liu H, Qu J, Jefferson W (2012) Effects and mechanisms of pre-chlorination on Microcystis aeruginosa removal by alum coagulation: significance of the released intracellular organic matter. Sep Purif Technol 86:19–25. CrossRefGoogle Scholar
  19. Ma C, Hu W, Pei H, Xu H, Pei R (2016) Enhancing integrated removal of Microcystis aeruginosa and adsorption of microcystins using chitosan-aluminum chloride combined coagulants: effect of chemical dosing orders and coagulation mechanisms. Colloids Surf A Physicochem Eng Asp 490:258–267. CrossRefGoogle Scholar
  20. Merel S, Walker D, Chicana R, Snyder S, Baurès E, Thomas O (2013) State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environ Int 59:303–327. CrossRefGoogle Scholar
  21. Moreira C, Vasconcelos V, Antunes A (2013) Phylogeny and biogeography of cyanobacteria and their related toxins. Mar Drugs 11:4350–4369. CrossRefGoogle Scholar
  22. Mucci M, Noyma NP, Magalhães L, Miranda M, van Oosterhout F, Guedes IA, Huszar VLM, Marinho MM, Lürling M (2017) Chitosan as coagulant on cyanobacteria in lake restoration management may cause rapid cell lysis. Water Res 118:121–130. CrossRefGoogle Scholar
  23. Niedermeyer THJ, Daily A, Swiatecka-Hagenbruch M, Moscow JA (2014) Selectivity and potency of microcystin congeners against OATP1B1 and OATP1B3 expressing cancer cells. In: PLos One, vol 9, p e91476. Google Scholar
  24. Oberholster PJ, Botha A-M, Grobbelaar JU (2004) Microcystis aeruginosa: source of toxic microcystins in drinking water. Afr J Biotechnol 3:159–168. CrossRefGoogle Scholar
  25. Paerl HW, Fulton RS, Moisander PH, Dyble J (2001) Harmful freshwater algal blooms with an emphasis on cyanobacteria. Sci World J 1:76–113. CrossRefGoogle Scholar
  26. Pei H-Y, Ma C-X, Hu W-R, Sun F (2014) The behaviors of Microcystis aeruginosa cells and extracellular microcystins during chitosan flocculation and flocs storage processes. Bioresour Technol 151:314–322. CrossRefGoogle Scholar
  27. Qi J, Lan H, Miao S, Xu Q, Liu R, Liu H, Qu J (2016) KMnO4-Fe(II) pretreatment to enhance Microcystis aeruginosa removal by aluminum coagulation: does it work after long distance transportation? Water Res 88:127–134. CrossRefGoogle Scholar
  28. Rodriguez-Molares A, Dickson S, Hobson P, Howard C, Zander A, Burch M (2014) Quantification of the ultrasound induced sedimentation of Microcystis aeruginosa. Ultrason Sonochem 21:1299–1304. CrossRefGoogle Scholar
  29. Shi W, Tan W, Wang L, Pan G (2016) Removal of Microcystis aeruginosa using cationic starch modified soils. Water Res 97:19–25. CrossRefGoogle Scholar
  30. Sun F, Pei H-Y, Hu W-R, Ma C-X (2012) The lysis of Microcystis aeruginosa in AlCl3 coagulation and sedimentation processes. Chem Eng J 193-194:196–202. CrossRefGoogle Scholar
  31. Teixeira MR, Rosa MJ (2007) Comparing dissolved air flotation and conventional sedimentation to remove cyanobacterial cells of Microcystis aeruginosa. Part II. The effect of water background organics. Sep Purif Technol 53:126–134. CrossRefGoogle Scholar
  32. Wang H-Q, Mao T-G, Xi B-D, Zhang L-Y, Zhou Q-H (2015) KMnO4 pre-oxidation for Microcystis aeruginosa removal by a low dosage of flocculant. Ecol Eng 81:298–300. CrossRefGoogle Scholar
  33. 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. Bioresour Technol 110:496–502. CrossRefGoogle Scholar
  34. Yap RKL, Whittaker M, Diao M, Stuetz RM, Jefferson B, Bulmus V, Peirson WL, Nguyen AV, Henderson RK (2014) Hydrophobically-associating cationic polymers as micro-bubble surface modifiers in dissolved air flotation for cyanobacteria cell separation. Water Res 61:253–262. CrossRefGoogle Scholar
  35. Yuan Y, Zhang H, Pan G (2016) Flocculation of cyanobacterial cells using coal fly ash modified chitosan. Water Res 97:11–18. CrossRefGoogle Scholar
  36. Zamyadi A, MacLeod SL, Fan Y, McQuaid N, Dorner S, Sauvé S, Prévost M (2012) Toxic cyanobacterial breakthrough and accumulation in a drinking water plant: a monitoring and treatment challenge. Water Res 46:1511–1523. CrossRefGoogle Scholar
  37. Zanchett G, Oliveira-Filho EC (2013) Cyanobacteria and cyanotoxins: from impacts on aquatic ecosystems and human health to anticarcinogenic effects. Toxins 5:1896–1917. CrossRefGoogle Scholar
  38. Zhou S, Shao Y, Gao N, Zhu S, Li L, Deng J, Zhu M (2014) Removal of Microcystis aeruginosa by potassium ferrate (VI): impacts on cells integrity, intracellular organic matter release and disinfection by-products formation. Chem Eng J 251:304–309. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.CEB-Centre of Biological EngineeringUniversity of MinhoBragaPortugal
  2. 2.Department of Biology, Faculty of Sciences, CIIMAR/CIMAR - Interdisciplinary Centre of Marine and Environmental Research andUniversity of PortoPortoPortugal

Personalised recommendations