Measurement of individual cell strength of Botryococcus braunii in cell culture

  • Shun Tsutsumi
  • Yasuhiro Saito
  • Yohsuke Matsushita
  • Hideyuki Aoki
Article

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.

Keywords

Microalgae Botryococcus braunii Cell strength Cell disruption Nanoindentation 

Notes

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.

References

  1. 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 23:3153–3160CrossRefGoogle Scholar
  2. 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 100:978–983CrossRefGoogle Scholar
  3. 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 102:3396–3403CrossRefPubMedGoogle Scholar
  4. Banerjee A, Sharma R, Chisti Y, Banerjee UC (2002) Botryococcus braunii: a renewable source of hydrocarbons and other chemicals. Crit Rev Biotechnol 22:245–279CrossRefPubMedGoogle Scholar
  5. 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 22:389–397CrossRefGoogle Scholar
  6. Blackburn KB, Temperley BN (1936) Botryococcus and the algal coals. Trans R Soc Edinburgh 58:841–868Google Scholar
  7. 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 14:557–577CrossRefGoogle Scholar
  8. Chisti Y (2007) Biodiesel from microalgae. Biotechnol Adv 25:294–306CrossRefPubMedGoogle Scholar
  9. Chisti Y, Mooyoung M (1986) Disruption of microbial-cells for intracellular products. Enzym Microb Technol 8:194–204 6CrossRefGoogle Scholar
  10. Cooney M, Young G, Nagle N (2009) Extraction of bio-oils from microalgae. Separat Purif Rev 38:291–325CrossRefGoogle Scholar
  11. 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 61:3159–3171CrossRefGoogle Scholar
  12. Eroglu E, Melis A (2010) Extracellular terpenoid hydrocarbon extraction and quantitation from the green microalgae Botryococcus braunii var. showa. Bioresour Technol 101:2359–2366CrossRefPubMedGoogle Scholar
  13. Furuhashi K, Saga K, Okada S, Imou K (2013) Seawater-cultured Botryococcus braunii for efficient hydrocarbon extraction. PLoS One 8:e66483CrossRefPubMedPubMedCentralGoogle Scholar
  14. 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 39:1693–1699CrossRefGoogle Scholar
  15. 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 7:703–726CrossRefPubMedGoogle Scholar
  16. 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 27:1833–1841CrossRefGoogle Scholar
  17. Guionet A, Hosseini B, Teissie J, Akiyama H, Hosseini H (2017) A new mechanism for efficient hydrocarbon electro-extraction from Botryococcus braunii. Biotechnol Biofuels 10:39CrossRefPubMedPubMedCentralGoogle Scholar
  18. Gunerken E, D'Hondt E, Eppink MH, Garcia-Gonzalez L, Elst K, Wijffels RH (2015) Cell disruption for microalgae biorefineries. Biotechnol Adv 33:243–260CrossRefPubMedGoogle Scholar
  19. Halim R, Danquah MK, Webley PA (2012) Extraction of oil from microalgae for biodiesel production: a review. Biotechnol Adv 30:709–732CrossRefPubMedGoogle Scholar
  20. He JY, Helland T, Zhang ZL, Kristiansen H (2009a) Fracture of micrometre-sized Ni/Au coated polymer particles. J Phys D 42:085405CrossRefGoogle Scholar
  21. He JY, Zhang ZL, Kristiansen H (2009b) Compression properties of individual micron-sized acrylic particles. Mater Lett 63:1696–1698CrossRefGoogle Scholar
  22. 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 15:56–65CrossRefGoogle Scholar
  23. Kleinig AR, Middelberg APJ (1996) The correlation of cell disruption with homogenizer valve pressure gradient determined by computational fluid dynamics. Chem Eng Sci 51:5103–5110CrossRefGoogle Scholar
  24. Kleinig AR, Middelberg APJ (1997) Numerical and experimental study of a homogenizer impinging jet. AIChE J 43:1100–1107CrossRefGoogle Scholar
  25. Lardon L, He'lias A, Sialve B, Steyer J-P, Bernard O (2009) Life-cycle assessment of biodiesel production from microalgae. Environ Sci Technol 43:6475–6481CrossRefPubMedGoogle Scholar
  26. Largeau C, Casadevall E, Berkaloff C, Dhamelincourt P (1980) Sites of accumulation and composition of hydrocarbons in Botryococcus braunii. Phytochemistry 19:1043–1051CrossRefGoogle Scholar
  27. 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 46:89–101CrossRefGoogle Scholar
  28. Lee AK, Lewis DM, Ashman PJ (2013) Force and energy requirement for microalgal cell disruption: an atomic force microscope evaluation. Bioresour Technol 128:199–206CrossRefPubMedGoogle Scholar
  29. Lee AK, Lewis DM, Ashman PJ (2014) Microalgal cell disruption by hydrodynamic cavitation for the production of biofuels. J Appl Phycol 27:1881–1889CrossRefGoogle Scholar
  30. Lin C-C, Hong PKA (2013) A new processing scheme from algae suspension to collected lipid using sand filtration and ozonation. Algal Res 2:378–384CrossRefGoogle Scholar
  31. 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 110:1349–1357CrossRefPubMedGoogle Scholar
  32. 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 103:128–134CrossRefGoogle Scholar
  33. Mercer P, Armenta RE (2011) Developments in oil extraction from microalgae. Eur J Lipid Sci Technol 113:539–547CrossRefGoogle Scholar
  34. Metzger P, Largeau C (2005) Botryococcus braunii: a rich source for hydrocarbons and related ether lipids. Appl Microbiol Biotechnol 66:486–496CrossRefPubMedGoogle Scholar
  35. Moheimani NR, Cord-Ruwisch R, Raes E, Borowitzka MA (2013) Non-destructive oil extraction from Botryococcus braunii (Chlorophyta). J Appl Phycol 25:1653–1661CrossRefGoogle Scholar
  36. Moheimani NR, Matsuura H, Watanabe MM, Borowitzka MA (2014) Non-destructive hydrocarbon extraction from Botryococcus braunii BOT-22 (race B). J Appl Phycol 26:1453–1463CrossRefGoogle Scholar
  37. 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 20:491–515CrossRefPubMedGoogle Scholar
  38. Olmstead IL, Kentish SE, Scales PJ, Martin GJ (2013) Low solvent, low temperature method for extracting biodiesel lipids from concentrated microalgal biomass. Bioresour Technol 148:615–619CrossRefPubMedGoogle Scholar
  39. Overbeck A, Gunther S, Kampen I, Kwade A (2017) Compression testing and modeling of spherical cells—comparison of yeast and algae. Chem Eng Technol 40:1158–1164CrossRefGoogle Scholar
  40. Overbeck A, Kampen I, Kwade A (2015) Mechanical characterization of yeast cells: effects of growth conditions. Lett Appl Microbiol 61:333–338CrossRefPubMedGoogle Scholar
  41. Pragya N, Pandey KK, Sahoo PK (2013) A review on harvesting, oil extraction and biofuels production technologies from microalgae. Renew Sustain Energy Rev 24:159–171CrossRefGoogle Scholar
  42. 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 15:80–89CrossRefGoogle Scholar
  43. 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 70:120–126CrossRefGoogle Scholar
  44. 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 140:165–171CrossRefPubMedGoogle Scholar
  45. 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 55:909–941CrossRefGoogle Scholar
  46. 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:e81626CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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 26:1–8CrossRefGoogle Scholar
  48. 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 63:1494–1502CrossRefGoogle Scholar
  49. 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 12:454–467CrossRefGoogle Scholar
  50. 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 2:012701CrossRefGoogle Scholar
  51. Wijihastuti RS, Moheimani NR, Bahri PA, Cosgrove JJ, Watanabe MM (2017) Growth and photosynthetic activity of Botryococcus braunii biofilms. J Appl Phycol 29:1123–1134CrossRefGoogle Scholar
  52. 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 43:1671–1680CrossRefPubMedGoogle Scholar
  53. Yap BH, Dumsday GJ, Scales PJ, Martin GJ (2015) Energy evaluation of algal cell disruption by high pressure homogenisation. Bioresour Technol 184:280–285CrossRefPubMedGoogle Scholar
  54. 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 5:112–120CrossRefGoogle Scholar
  55. 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 154:281–284CrossRefPubMedGoogle Scholar
  56. 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 165:22–29CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Chemical Engineering, Graduate School of EngineeringTohoku UniversitySendaiJapan

Personalised recommendations