Surface physicochemical properties of selected single and mixed cultures of microalgae and cyanobacteria and their relationship with sedimentation kinetics

Abstract

Background

Microalgae are photosynthetic microorganisms presenting a diversity of biotechnological applications. However, microalgal cultivation systems are not energetically and economically feasible. Possible strategies that can be applied to improve the feasibility of microalgal production include biofouling control in photobioreactors, the use of attached growth systems and bioflocculation. These processes are ruled by surface physicochemical properties. Accordingly, the surface physicochemical properties of Chlorella vulgaris, Pseudokirchneriella subcapitata, Synechocystis salina and Microcystis aeruginosa were determined through contact angle and zeta potential measurements. Additionally, mixed cultures of the selected microorganisms were performed. Sedimentation kinetics of the studied cultures was also evaluated to understand how surface physicochemical properties influence microalgal recovery.

Results

All studied microorganisms, except S. salina, presented a hydrophilic surface. The co-culture of S. salina with the other studied microorganisms resulted in a more hydrophobic algal suspension. Regarding zeta potential determinations, all studied suspensions presented a negatively charged surface (approximately -40.8 ± 4.4 mV). Sedimentation experiments have shown that all microalgal suspensions presented low microalgal recovery efficiencies. However, a negative linear relationship between microalgal removal percentage and free energy of hydrophobic interaction was obtained.

Conclusions

The evidence of a relationship between microalgal removal percentage and free energy of hydrophobic interaction demonstrates the importance of surface physicochemical properties on microalgal settling. However, the low recovery efficiencies achieved, as well as the high net zeta potential values determined, indicate that another factor to consider in microalgal settling is the ionic strength of the culture medium, which play an important role in suspensions’ stability.

Keywords

Cyanobacteria / Microalgae / Mixed cultures / Sedimentation kinetics / Surface physicochemical properties

References

[1] Brennan L, Owende P. Biofuels from microalgae - a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sust Energ Rev, 2010, 14: 557-77.

[2] Demirbas A. Biodiesel from oilgae, biofixation of carbon dioxide by microalgae: a solution to pollution problems. Appl Energy, 2011, 88: 3541-7.

[3] Bilanovic D, Andargatchew A, Kroeger T, Shelef G. Freshwater and marine microalgae sequestering of CO₂ at different C and N concentrations - response surface methodology analysis. Energy Conv Manag, 2009, 50: 262-7.

[4] Gonçalves AL, Simões M, Pires JCM. The effect of light supply on microalgal growth, CO₂ uptake and nutrient removal from wastewater. Energy Conv Manag, 2014, 85: 530-6.

[5] Ho S-H, Chen C-Y, Lee D-J, Chang J-S. Perspectives on microalgal CO₂-emission mitigation systems - a review. Biotechnol Adv, 2011, 29: 189-98.

[6] Sayre R. Microalgae: the potential for carbon capture. Bioscience, 2010, 60: 722-7.

[7] Boelee N, Temmink H, Janssen M, Buisman C, Wijffels R. Nitrogen and phosphorus removal from municipal wastewater effluent using microalgal biofilms. Water Res, 2011, 45: 5925-33.

[8] Park JBK, Craggs RJ, Shilton AN. Wastewater treatment high rate algal ponds for biofuel production. Bioresour Technol, 2011, 102: 35-42.

[9] Rawat I, Ranjith Kumar R, Mutanda T, Bux F. Dual role of microalgae: phycoremediation of domestic wastewater and biomass production for sustainable biofuels production. Appl Energy, 2011, 88: 3411-24.

[10] Silva-Benavides A, Torzillo G. Nitrogen and phosphorus removal through laboratory batch cultures of microalga Chlorella vulgaris and cyanobacterium Planktothrix isothrix grown as monoalgal and as co-cultures. J Appl Phycol, 2012, 24: 267-76.

[11] Hu Q. Richmond A. Industrial production of microalgal cell-mass and secondary products - major industrial species. Handbook of microalgal culture: biotechnology and applied phycology, 2004, Oxford, UK: Blackwell Science Ltd., 268-71.

[12] Singh S, Kate B, Banerjee U. Bioactive compounds from cyanobacteria and microalgae: an overview. Crit Rev Biotechnol, 2005, 25: 73-95.

[13] Spolaore P, Joannis-Cassan C, Duran E, Isambert A. Commercial applications of microalgae. J Biosci Bioeng, 2006, 101: 87-96.

[14] Molina Grima E, Belarbi EH, Acién Fernández FG, Robles Medina A, Chisti Y. Recovery of microalgal biomass and metabolites: process options and economics. Biotechnol Adv, 2003, 20: 491-515.

[15] Lardon L, Hélias A, Sialve B, Steyer J-P, Bernard O. Life-cycle assessment of biodiesel production from microalgae. Environ Sci Technol, 2009, 43: 6475-81.

[16] Ozkan A, Berberoglu H. Adhesion of algal cells to surfaces. Biofouling, 2013, 29: 469-82.

[17] Posten C. Design principles of photo-bioreactors for cultivation of microalgae. Eng Life Sci, 2009, 9: 165-77.

[18] Pulz O. Photobioreactors: production systems for phototrophic microorganisms. Appl Microbiol Biotechnol, 2001, 57: 287-93.

[19] Irving TE, Allen DG. Species and material considerations in the formation and development of microalgal biofilms. Appl Microbiol Biotechnol, 2011, 92: 283-94.

[20] Roeselers G, Van Loosdrecht M, Muyzer G. Phototrophic biofilms and their potential applications. J Appl Phycol, 2008, 20: 227-35.

[21] Finlay JA, Bennett SM, Brewer LH, Sokolova A, Clay G, Gunari N, . Barnacle settlement and the adhesion of protein and diatom microfouling to xerogel films with varying surface energy and water wettability. Biofouling, 2010, 26: 657-66.

[22] Ista LK, Callow ME, Finlay JA, Coleman SE, Nolasco AC, Simons RH, . Effect of substratum surface chemistry and surface energy on attachment of marine bacteria and algal spores. Appl Environ Microbiol, 2004, 70: 4151-7.

[23] Mercer P, Armenta RE. Developments in oil extraction from microalgae. Eur J Lipid Sci Technol, 2011, 113: 539-47.

[24] Christenson L, Sims R. Production and harvesting of microalgae for wastewater treatment, biofuels, and bioproducts. Biotechnol Adv, 2011, 29: 686-702.

[25] Uduman N, Qi Y, Danquah MK, Forde GM, Hoadley A. Dewatering of microalgal cultures: a major bottleneck to algae-based fuels. J Renew Sustain Energy, 2010, 2: 012701-15.

[26] Vandamme D, Foubert I, Muylaert K. Flocculation as a low-cost method for harvesting microalgae for bulk biomass production. Trends Biotechnol, 2013, 31: 233-9.

[27] van Oss C, Chaudhury M, Good R. Monopolar surfaces. Adv Colloid Interface Sci, 1987, 28: 35-64.

[28] van Oss C, Ju L, Chaudhury M, Good R. Estimation of the polar parameters of the surface tension of liquids by contact angle measurements on gels. J Colloid Interface Sci, 1989, 128: 313-9.

[29] van Oss CJ, Good RJ, Chaudhury MK. Additive and nonadditive surface tension components and the interpretation of contact angles. Langmuir, 1988, 4: 884-91.

[30] Chinnasamy S, Ramakrishnan B, Bhatnagar A, Das KC. Biomass production potential of a wastewater alga Chlorella vulgaris ARC 1 under elevated levels of CO₂ and temperature. Int J Mol Sci, 2009, 10: 518-32.

[31] McLarnon-Riches CJ, Rolph CE, Greenway DL, Robinson PK. Effects of environmental factors and metals on Selenastrum capricornutum lipids. Phytochemistry, 1998, 49: 1241-7.

[32] Philippis R, Vincenzini M. Exocellular polysaccharides from cyanobacteria and their possible applications. FEMS Microbiol Rev, 1998, 22: 151-75.

[33] Wahlen BD, Willis RM, Seefeldt LC. Biodiesel production by simultaneous extraction and conversion of total lipids from microalgae, cyanobacteria, and wild mixed-cultures. Bioresour Technol, 2011, 102: 2724-30.

[34] OECD. Freshwater alga and cyanobacteria, growth inhibition test. Test Guideline 201: Organisation for Economic Co-operation and Development, 2011

[35] Busscher H, Weerkamp A, van der Mei H, van Pelt A, de Jong H, Arends J. Measurement of the surface free energy of bacterial cell surfaces and its relevance for adhesion. Appl Environ Microbiol, 1984, 48: 980-3.

[36] van Oss C. Hydrophobicity of biosurfaces - origin, quantitative determination and interaction energies. Colloids Surf B Biointerfaces, 1995, 5: 91-110.

[37] Ozkan A, Berberoglu H. Cell to substratum and cell to cell interactions of microalgae. Colloids Surf B Biointerfaces, 2013, 112: 302-9.

[38] van Oss CJ. Long-range and short-range mechanisms of hydrophobic attraction and hydrophilic repulsion in specific and aspecific interactions. J Mol Recognit, 2003, 16: 177-90.

[39] Janczuk B, Chibowski E, Bruque J, Kerkeb M, Caballero FG. On the consistency of surface free energy components as calculated from contact angles of different liquids: an application to the cholesterol surface. J Colloid Interface Sci, 1993, 159: 421-8.

[40] Salim S, Bosma R, Vermuë MH, Wijffels RH. Harvesting of microalgae by bio-flocculation. J Appl Phycol, 2011, 23: 849-55.

[41] Gompertz B. On the nature of the function expressive of the law of human mortality, and on a new mode of determining the value of life contingencies. Philos Trans Royal Soc London, 1825, 115: 513-83.

[42] Simões LC, Simões M, Oliveira R, Vieira MJ. Potential of the adhesion of bacteria isolated from drinking water to materials. J Basic Microbiol, 2007, 47: 174-83.

[43] Volpe CD, Siboni S. Some reflections on acid–base solid surface free energy theories. J Colloid Interface Sci, 1997, 195: 121-36.

[44] Ozkan A, Berberoglu H. Physico-chemical surface properties of microalgae. Colloids Surf B Biointerfaces, 2013, 112: 287-93.

[45] Becker E. Microalgae as a source of protein. Biotechnol Adv, 2007, 25: 207-10.

[46] Latała A, Nędzi M, Stepnowski P. Toxicity of imidazolium and pyridinium based ionic liquids towards algae: Chlorella vulgaris, Oocystis submarina (green algae) and Cyclotella meneghiniana, Skeletonema marinoi (diatoms). Green Chem, 2009, 11: 580-8.

[47] Loos E, Meindl D. Composition of the cell wall of Chlorella fusca. Planta, 1982, 156: 270-3.

[48] Northcote D, Goulding K, Horne R. The chemical composition and structure of the cell wall of Chlorella pyrenoidosa. Biochem J, 1958, 70: 391.

[49] Bos R, Mei HC, Busscher HJ. Physico-chemistry of initial microbial adhesive interactions - its mechanisms and methods for study. FEMS Microbiol Rev, 1999, 23: 179-230.

[50] Ferreira C, Pereira A, Pereira M, Melo L, Simões M. Physiological changes induced by the quaternary ammonium compound benzyldimethyldodecylammonium chloride on Pseudomonas fluorescens. J Antimicrob Chemother, 2011, 66: 1036-43.

[51] González-Fernández C, Ballesteros M. Microalgae autoflocculation: an alternative to high-energy consuming harvesting methods. J Appl Phycol, 2012, 25: 1-9.

[52] Hadjoudja S, Deluchat V, Baudu M. Cell surface characterisation of Microcystis aeruginosa and Chlorella vulgaris. J Colloid Interface Sci, 2010, 342: 293-9.

[53] Stumm W, Morgan JJ. Aquatic chemistry: chemical equilibria and rates in natural waters, 2012, New Jersey: John Wiley & Sons.

[54] de Schryver P, Crab R, Defoirdt T, Boon N, Verstraete W. The basics of bio-flocs technology: the added value for aquaculture. Aquaculture, 2008, 277: 125-37.

[55] Zita A, Hermansson M. Effects of ionic strength on bacterial adhesion and stability of flocs in a wastewater activated sludge system. Appl Environ Microbiol, 1994, 60: 3041-8.

[56] Manheim D, Nelson Y. Settling and bioflocculation of two species of algae used in wastewater treatment and algae biomass production. Environ Prog Sustain Energy, 2013, 32: 946-54.

[57] Papazi A, Makridis P, Divanach P. Harvesting Chlorella minutissima using cell coagulants. J Appl Phycol, 2010, 22: 349-55.

[58] Garzon-Sanabria AJ, Davis RT, Nikolov ZL. Harvesting Nannochloris oculata by inorganic electrolyte flocculation: effect of initial cell density, ionic strength, coagulant dosage, and media pH. Bioresour Technol, 2012, 118: 418-24.