Abstract
Botryococcus braunii is a microalga considered for biofuel production and may require physical disruption of cells/colonies for efficient hydrocarbon extraction. In this study, the strength of individual cells of B. braunii was measured using a nanoindenter. From the load and cell size, the pressure for bursting the cell was calculated to be 56.9 MPa. This value is 2.3–10 times those of Saccharomyces cerevisiae and Chlorella vulgaris found in another research, because B. braunii has two types of cell walls with different thicknesses. The energy required to disrupt 1 g of dry B. braunii cells, estimated by load-displacement curves, is 3.19 J g−1 which is 0.19–1.2 times higher than those of S. cerevisiae and C. vulgaris. When using a high-pressure homogenizer for disrupting B. braunii cells, the cell disruption degree increased with the treatment pressure at above 30 MPa, and 70% of cells were disrupted at 80 MPa.
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References
Arfsten J, Bradtmöller C, Kampen I, Kwade A (2011) Compressive testing of single yeast cells in liquid environment using a nanoindentation system. J Mater Res 23:3153–3160
Arfsten J, Kampen I, Kwade A (2009) Mechanical testing of single yeast cells in liquid environment: effect of the extracellular osmotic conditions on the failure behavior. Int J Mater Res 100:978–983
Balasubramanian S, Allen JD, Kanitkar A, Boldor D (2011) Oil extraction from Scenedesmus obliquus using a continuous microwave system—design, optimization, and quality characterization. Bioresour Technol 102:3396–3403
Banerjee A, Sharma R, Chisti Y, Banerjee UC (2002) Botryococcus braunii: a renewable source of hydrocarbons and other chemicals. Crit Rev Biotechnol 22:245–279
Berkaloff C, Casadevall E, Largeau C, Peracca MS, Virlet J (1983) The resistant polymer of the walls of the hydrocarbon-rich alga Botryococcus braunii. Phytochemistry 22:389–397
Blackburn KB, Temperley BN (1936) Botryococcus and the algal coals. Trans R Soc Edinburgh 58:841–868
Brennan L, Owende P (2010) Biofuels from microalgae—a review of technologies for production, processing, and extractions of biofuels and co-products. Renew Sustain Energy Rev 14:557–577
Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25:294–306
Chisti Y, Mooyoung M (1986) Disruption of microbial-cells for intracellular products. Enzym Microb Technol 8:194–204 6
Cooney M, Young G, Nagle N (2009) Extraction of bio-oils from microalgae. Separat Purif Rev 38:291–325
de Jesus SS, Moreira Neto J, Santana A, Maciel Filho R (2015) Influence of impeller type on hydrodynamics and gas-liquid mass-transfer in stirred airlift bioreactor. AIChE J 61:3159–3171
Eroglu E, Melis A (2010) Extracellular terpenoid hydrocarbon extraction and quantitation from the green microalgae Botryococcus braunii var. showa. Bioresour Technol 101:2359–2366
Furuhashi K, Saga K, Okada S, Imou K (2013) Seawater-cultured Botryococcus braunii for efficient hydrocarbon extraction. PLoS One 8:e66483
Günther S, Gernat D, Overbeck A, Kampen I, Kwade A (2016) Micromechanical properties and energy requirements of the microalgae Chlorella vulgaris for cell disruption. Chem Eng Technol 39:1693–1699
Greenwell HC, Laurens LM, Shields RJ, Lovitt RW, Flynn KJ (2010) Placing microalgae on the biofuels priority list: a review of the technological challenges. J R Soc Interface 7:703–726
Griehl C, Kleinert C, Griehl C, Bieler S (2015) Design of a continuous milking bioreactor for non-destructive hydrocarbon extraction from Botryococcus braunii. J Appl Phycol 27:1833–1841
Guionet A, Hosseini B, Teissie J, Akiyama H, Hosseini H (2017) A new mechanism for efficient hydrocarbon electro-extraction from Botryococcus braunii. Biotechnol Biofuels 10:39
Gunerken E, D'Hondt E, Eppink MH, Garcia-Gonzalez L, Elst K, Wijffels RH (2015) Cell disruption for microalgae biorefineries. Biotechnol Adv 33:243–260
Halim R, Danquah MK, Webley PA (2012) Extraction of oil from microalgae for biodiesel production: a review. Biotechnol Adv 30:709–732
He JY, Helland T, Zhang ZL, Kristiansen H (2009a) Fracture of micrometre-sized Ni/Au coated polymer particles. J Phys D 42:085405
He JY, Zhang ZL, Kristiansen H (2009b) Compression properties of individual micron-sized acrylic particles. Mater Lett 63:1696–1698
Ishimatsu A, Matsuura H, Sano T, Kaya K, Watanabe MM (2012) Biosynthesis of isoprene units in the C34 botryococcene molecule produced by Botryococcus braunii strain Bot-22. Procedia Environ Sci 15:56–65
Kleinig AR, Middelberg APJ (1996) The correlation of cell disruption with homogenizer valve pressure gradient determined by computational fluid dynamics. Chem Eng Sci 51:5103–5110
Kleinig AR, Middelberg APJ (1997) Numerical and experimental study of a homogenizer impinging jet. AIChE J 43:1100–1107
Lardon L, He'lias A, Sialve B, Steyer J-P, Bernard O (2009) Life-cycle assessment of biodiesel production from microalgae. Environ Sci Technol 43:6475–6481
Largeau C, Casadevall E, Berkaloff C, Dhamelincourt P (1980) Sites of accumulation and composition of hydrocarbons in Botryococcus braunii. Phytochemistry 19:1043–1051
Lee AK, Lewis DM, Ashman PJ (2012) Disruption of microalgal cells for the extraction of lipids for biofuels: processes and specific energy requirements. Biomass Bioenergy 46:89–101
Lee AK, Lewis DM, Ashman PJ (2013) Force and energy requirement for microalgal cell disruption: an atomic force microscope evaluation. Bioresour Technol 128:199–206
Lee AK, Lewis DM, Ashman PJ (2014) Microalgal cell disruption by hydrodynamic cavitation for the production of biofuels. J Appl Phycol 27:1881–1889
Lin C-C, Hong PKA (2013) A new processing scheme from algae suspension to collected lipid using sand filtration and ozonation. Algal Res 2:378–384
Louise Meyer R, Zhou X, Tang L, Arpanaei A, Kingshott P, Besenbacher F (2010) Immobilisation of living bacteria for AFM imaging under physiological conditions. Ultramicroscopy 110:1349–1357
McMillan JR, Watson IA, Ali M, Jaafar W (2013) Evaluation and comparison of algal cell disruption methods: microwave, waterbath, blender, ultrasonic and laser treatment. Appl Energy 103:128–134
Mercer P, Armenta RE (2011) Developments in oil extraction from microalgae. Eur J Lipid Sci Technol 113:539–547
Metzger P, Largeau C (2005) Botryococcus braunii: a rich source for hydrocarbons and related ether lipids. Appl Microbiol Biotechnol 66:486–496
Moheimani NR, Cord-Ruwisch R, Raes E, Borowitzka MA (2013) Non-destructive oil extraction from Botryococcus braunii (Chlorophyta). J Appl Phycol 25:1653–1661
Moheimani NR, Matsuura H, Watanabe MM, Borowitzka MA (2014) Non-destructive hydrocarbon extraction from Botryococcus braunii BOT-22 (race B). J Appl Phycol 26:1453–1463
Molina Grima E, Belarbi EH, Acien Fernandez FG, Robles Medina A, Chisti Y (2003) Recovery of microalgal biomass and metabolites: process options and economics. Biotechnol Adv 20:491–515
Olmstead IL, Kentish SE, Scales PJ, Martin GJ (2013) Low solvent, low temperature method for extracting biodiesel lipids from concentrated microalgal biomass. Bioresour Technol 148:615–619
Overbeck A, Gunther S, Kampen I, Kwade A (2017) Compression testing and modeling of spherical cells—comparison of yeast and algae. Chem Eng Technol 40:1158–1164
Overbeck A, Kampen I, Kwade A (2015) Mechanical characterization of yeast cells: effects of growth conditions. Lett Appl Microbiol 61:333–338
Pragya N, Pandey KK, Sahoo PK (2013) A review on harvesting, oil extraction and biofuels production technologies from microalgae. Renew Sustain Energy Rev 24:159–171
Shimamura R, Watanabe S, Sakakura Y, Shiho M, Kaya K, Watanabe MM (2012) Development of Botryococcus seed culture system for future mass culture. Procedia Environ Sci 15:80–89
Spiden EM, Scales PJ, Kentish SE, Martin GJO (2013a) Critical analysis of quantitative indicators of cell disruption applied to Saccharomyces cerevisiae processed with an industrial high pressure homogenizer. Biochem Eng J 70:120–126
Spiden EM, Yap BH, Hill DR, Kentish SE, Scales PJ, Martin GJ (2013b) Quantitative evaluation of the ease of rupture of industrially promising microalgae by high pressure homogenization. Bioresour Technol 140:165–171
Suganya T, Varman M, Masjuki HH, Renganathan S (2016) Macroalgae and microalgae as a potential source for commercial applications along with biofuels production: a biorefinery approach. Renew Sust Energy Rev 55:909–941
Suzuki R, Ito N, Uno Y, Nishii I, Kagiwada S, Okada S, Noguchi T (2013) Transformation of lipid bodies related to hydrocarbon accumulation in a green alga, Botryococcus braunii (race B). PLoS One 8:e81626
Tanoi T, Kawachi M, Watanabe MM (2013) Iron and glucose effects on the morphology of Botryococcus braunii with assumption on the colony formation variability. J Appl Phycol 26:1–8
Teymouri A, Kumar S, Barbera E, Sforza E, Bertucco A, Morosinotto T (2017) Integration of biofuels intermediates production and nutrients recycling in the processing of a marine algae. AIChE J 63:1494–1502
Tsutsumi S, Yokomizo M, Saito Y, Matsushita Y, Aoki H (2017) Mechanical cell disruption of microalgae for investigating the effects of degree of disruption on hydrocarbon extraction. Asia Pac J Chem Eng 12:454–467
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 2:012701
Wijihastuti RS, Moheimani NR, Bahri PA, Cosgrove JJ, Watanabe MM (2017) Growth and photosynthetic activity of Botryococcus braunii biofilms. J Appl Phycol 29:1123–1134
Yap BH, Crawford SA, Dagastine RR, Scales PJ, Martin GJ (2016) Nitrogen deprivation of microalgae: effect on cell size, cell wall thickness, cell strength, and resistance to mechanical disruption. J Ind Microbiol Biotechnol 43:1671–1680
Yap BH, Dumsday GJ, Scales PJ, Martin GJ (2015) Energy evaluation of algal cell disruption by high pressure homogenisation. Bioresour Technol 184:280–285
Yap BHJ, Crawford SA, Dumsday GJ, Scales PJ, Martin GJO (2014) A mechanistic study of algal cell disruption and its effect on lipid recovery by solvent extraction. Algal Res 5:112–120
Zhang F, Cheng LH, Gao WL, Xu XH, Zhang L, Chen HL (2011) Mechanism of lipid extraction from Botryococcus braunii FACHB 357 in a biphasic bioreactor. J Biotechnol 154:281–284
Zhang F, Cheng LH, Xu XH, Zhang L, Chen HL (2013) Application of memberane dispersion for enhanced lipid milking from Botryococcus braunii FACHB 357. J Biotechnol 165:22–29
Acknowledgements
The authors would like to thank Prof. H. Inomata and Dr. M. Ota, Department of Chemical Engineering, Tohoku University, for lending us the UV-Vis spectrophotometer.
Funding
This work was supported by the Next-Generation Energies for Tohoku Recovery (NET) project of the Ministry of Education, Culture, Sports, Science, and Technology (MEXT), Japan. The samples of B. braunii were provided by the University of Tsukuba. The cell compression test using nanoindentation was supported by the Kyoto University Nano Technology Hub in “Nanotechnology Platform Project” sponsored by MEXT, Japan.
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Tsutsumi, S., Saito, Y., Matsushita, Y. et al. Measurement of individual cell strength of Botryococcus braunii in cell culture. J Appl Phycol 30, 2287–2296 (2018). https://doi.org/10.1007/s10811-018-1466-6
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DOI: https://doi.org/10.1007/s10811-018-1466-6