Journal of Applied Phycology

, Volume 29, Issue 6, pp 2937–2946 | Cite as

Effects of biological and physical properties of microalgae on disruption induced by a low-frequency ultrasound

  • Zhipeng Duan
  • Xiao TanEmail author
  • Jiujia Guo
  • Christine Wairimu Kahehu
  • Hanpei Yang
  • Xueying Zheng
  • Feng Zhu


Ultrasonication has drawn an increasing attention as one of cell disruption methods for extracting cellular compounds or controlling algal blooms. However, the effects of biological and physical properties of microalgae on cell disruption were not well understood. In this work, cell disruption of six microalgae, namely, Chlamydomonas reinhardtii, Chlorella pyrenoidosa, Microcystis aeruginosa (three strains: PCC 7806, FACHB 469, and FACHB 1343), and Synechococcus elongatus, was compared mutually based on their characteristics induced by a low-frequency ultrasound (35 kHz, 0.043 W mL−1). Results showed that the most sensitive strain was C. reinhardtii which has a hydroxyproline-rich-glycoproteins cell wall and a larger cell size (normally 10 μm in diameter). More than 80% of the cells of C. reinhardtii were ruptured after sonication for 5 min. In comparison, C. pyrenoidosa, a cellulose-rich-wall algal species with a medium size of 4–6 μm, and M. aeruginosa FACHB 1343, a peptidoglycan-wall species with a smaller average size of 2.3 μm, were highly resistant to ultrasound. Only 7.5 and 7.7% of cell disruption were achieved for C. pyrenoidosa and M. aeruginosa FACHB 1343, respectively, when they were sonicated for 60 min. Declumping effect was dominant in these strains. This suggested that cellulose-rich-wall algal species might be much more resistant than hydroxyproline-rich glycoproteins, and peptidoglycan-wall species to sonication. It also revealed that the larger cell size was more susceptible to sonication the cell would be. This research provides useful insights into choosing the low-cost microalgae for extraction or controlling specific microalgal blooms in water systems using ultrasound.


Microalgae Cell wall structure Cell size Ultrasonic disruption 



This work was supported by the Fundamental Research Funds for the Central Universities (2013B32414), National Natural Science Foundation of China (31470507), Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD) and Top-notch Academic Programs Project of Jiangsu Higher Education Institutions (TAPP).


  1. Adair WS, Snell WJ (1990) The Chlamydomonas reinhardtii cell wall: structure, biochemistry, and molecular biology. In: Adair WS (ed) Organization and assembly of plant and animal extracellular matrix. Academic, San Diego, pp 15–84CrossRefGoogle Scholar
  2. Ahn C-Y, Park M-H, Joung S-H, Kim H-S, Jang K-Y, Oh H-M (2003) Growth inhibition of cyanobacteria by ultrasonic radiation: laboratory and enclosure studies. Environ Sci Technol 37:3031–3037CrossRefPubMedGoogle Scholar
  3. Bigelow TA, Xu J, Stessman DJ, Yao L, Spalding MH, Wang T (2014) Lysis of Chlamydomonas reinhardtii by high-intensity focused ultrasound as a function of exposure time. Ultrason Sonochem 21:1258–1264CrossRefPubMedGoogle Scholar
  4. Bold HC, Parker BC (1962) Some supplementary attributes in the classification of Chlorococcum species. Arch Mikrobiol 42:267–288CrossRefPubMedGoogle Scholar
  5. Borowitzka MA (2013a) High-value products from microalgae—their development and commercialisation. J Appl Phycol 25:743–756CrossRefGoogle Scholar
  6. Borowitzka MA (2013b) Energy from microalgae: a short history. In: Borowitzka MA, Moheimani NR (eds) Algae for biofuels and energy. Springer, Dordrecht, pp 1–15CrossRefGoogle Scholar
  7. Callieri C (2010) Single cells and microcolonies of freshwater picocyanobacteria: a common ecology. J Limnol 69:257–277CrossRefGoogle Scholar
  8. Cameron M (2007) Impact of low-frequency high-power ultrasound on spoilage and potentially pathogenic dairy microbes. PhD Thesis, Stellenbosch University, South AfricaGoogle Scholar
  9. Domozych DS (2011) Algal cell walls. In: Pettis G (ed) eLS. John Wiley & Sons, Ltd, ChichesterGoogle Scholar
  10. Furuki T, Maeda S, Imajo S, Hiroi T, Amaya T, Hirokawa T, Ito K, Nozawa H (2003) Rapid and selective extraction of phycocyanin from Spirulina platensis with ultrasonic cell disruption. J Appl Phycol 15:319–324CrossRefGoogle Scholar
  11. Gao S, Hemar Y, Ashokkumar M, Paturel S, Lewis GD (2014a) Inactivation of bacteria and yeast using high-frequency ultrasound treatment. Water Res 60:93–104CrossRefPubMedGoogle Scholar
  12. Gao S, Lewis GD, Ashokkumar M, Hemar Y (2014b) Inactivation of microorganisms by low-frequency high-power ultrasound: 1. Effect of growth phase and capsule properties of the bacteria. Ultrason Sonochem 21:446–453CrossRefPubMedGoogle Scholar
  13. Görs M, Schumann R, Hepperle D, Karsten U (2010) Quality analysis of commercial Chlorella products used as dietary supplement in human nutrition. J Appl Phycol 22:265–276CrossRefGoogle Scholar
  14. Greenly JM, Tester JW (2015) Ultrasonic cavitation for disruption of microalgae. Bioresource Technol 184:276–279CrossRefGoogle Scholar
  15. Hao H, Wu M, Chen Y, Tang J, Wu Q (2004) Cavitation mechanism in cyanobacterial growth inhibition by ultrasonic irradiation. Colloid Surface B 33:151–156CrossRefGoogle Scholar
  16. Jacobs SE, Thornley MJ (1954) The lethal action of ultrasonic waves on bacteria suspended in milk and other liquids. J Appl Bacteriol 17:38–56CrossRefGoogle Scholar
  17. Joyce EM, Wu X, Mason TJ (2010) Effect of ultrasonic frequency and power on algae suspensions. J Environ Sci Health A 45:863–866CrossRefGoogle Scholar
  18. Joyce EM, King PM, Mason TJ (2014) The effect of ultrasound on the growth and viability of microalgae cells. J Appl Phycol 26:1741–1748CrossRefGoogle Scholar
  19. Keris-Sen UD, Sen U, Soydemir G, Gurol MD (2014) An investigation of ultrasound effect on microalgal cell integrity and lipid extraction efficiency. Bioresource Technol 152:407–413CrossRefGoogle Scholar
  20. Kurokawa M, King PM, Wu X, Joyce EM, Mason TJ, Yamamoto K (2016) Effect of sonication frequency on the disruption of algae. Ultrason Sonochem 31:157–162CrossRefPubMedGoogle Scholar
  21. Lee J-Y, Yoo C, Jun S-Y, Ahn C-Y, Oh H-M (2010) Comparison of several methods for effective lipid extraction from microalgae. Bioresource Technol 101:S75–S77CrossRefGoogle Scholar
  22. 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
  23. Lee AK, Lewis DM, Ashman PJ (2015) Microalgal cell disruption by hydrodynamic cavitation for the production of biofuels. J Appl Phycol 27:1881–1889CrossRefGoogle Scholar
  24. Li M, Zhu W, Gao L (2014) Analysis of cell concentration, volume concentration, and colony size of Microcystis via laser particle analyzer. Environ Manag 53:947–958CrossRefGoogle Scholar
  25. Luo J, Fang Z, Richard L, Smith J, Qi X (2011) Fundamentals of acoustic cavitation and sonochemistry. In: Ashokkumar M (ed) Theoretical and experimental sonochemistry involving inorganic systems. Springer, Dordrecht, pp 1–29Google Scholar
  26. Ma B, Chen Y, Hao H, Wu M, Wang B, Lv H, Zhang G (2005) Influence of ultrasonic field on microcystins produced by bloom-forming algae. Colloid Surface B 41:197–201CrossRefGoogle Scholar
  27. Mason T, Lorimer J, Bates D (1992) Quantifying sonochemistry: casting some light on a ‘black art’. Ultrasonics 30:40–42CrossRefGoogle Scholar
  28. Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sust Energ Rev 14:217–232CrossRefGoogle Scholar
  29. Northcote DH, Goulding KJ, Horne RW (1958) The chemical composition and structure of the cell wall of Chlorella pyrenoidosa. Biochem J 70:391–397CrossRefPubMedPubMedCentralGoogle Scholar
  30. Purcell D (2009) Control of algal growth in reservoirs with ultrasound. PhD Thesis, Cranfield University, UKGoogle Scholar
  31. Purcell D, Parsons SA, Jefferson B (2013) The influence of ultrasound frequency and power, on the algal species Microcystis aeruginosa, Aphanizomenon flos-aquae, Scenedesmus subspicatus and Melosira sp. Environ Technol 34:2477–2490CrossRefPubMedGoogle Scholar
  32. Raja R, Hemaiswarya S, Kumar NA, Sridhar S, Rengasamy R (2008) A perspective on the biotechnological potential of microalgae. Crit Rev Microbiol 34:77–88CrossRefPubMedGoogle Scholar
  33. Rajasekhar P, Fan L, Nguyen T, Roddick FA (2012a) Impact of sonication at 20 kHz on Microcystis aeruginosa, Anabaena circinalis and Chlorella sp. Water Res 46:1473–1481CrossRefPubMedGoogle Scholar
  34. Rajasekhar P, Fan L, Nguyen T, Roddick FA (2012b) A review of the use of sonication to control cyanobacterial blooms. Water Res 46:4319–4329CrossRefPubMedGoogle Scholar
  35. Scanlan DJ, Ostrowski M, Mazard S, Dufresne A, Garczarek L, Hess WR, Post AF, Hagemann M, Paulsen I, Partensky F (2009) Ecological genomics of marine picocyanobacteria. Microbiol Mol Biol Rev 73:249–299CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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
  37. Spiden EM, Yap BHJ, Hill DRA, Kentish SE, Scales PJ, Martin GJO (2013b) Quantitative evaluation of the ease of rupture of industrially promising microalgae by high pressure homogenization. Bioresource Technol 140:165–171CrossRefGoogle Scholar
  38. Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. Biosci Bioeng 101:87–96CrossRefGoogle Scholar
  39. Suslick KS (1989) The chemical effects of ultrasound. Sci Am 260:80–86CrossRefGoogle Scholar
  40. Tan X, Kong FX, Zeng QF, Cao HS, Qian SQ, Zhang M (2009) Seasonal variation of Microcystis in Lake Taihu and its relationships with environmental factors. J Environ Sci 21:892–899CrossRefGoogle Scholar
  41. Tang J, Wu Q, Hao H, Chen Y, Wu M (2003) Growth inhibition of the cyanobacterium Spirulina (Arthrospira) platensis by 1.7 MHz ultrasonic irradiation. J Appl Phycol 15:37–43CrossRefGoogle Scholar
  42. Tang JW, Wu QY, Hao HW, Chen Y, Wu M (2004) Effect of 1.7 MHz ultrasound on a gas-vacuolate cyanobacterium and a gas-vacuole negative cyanobacterium. Colloid Surface B 36:115–121CrossRefGoogle Scholar
  43. Voigt J (1988) The lithium-chloride-soluble cell-wall layers of Chlamydomonas reinhardii contain several immunologically related glycoproteins. Planta 173:373–384CrossRefPubMedGoogle Scholar
  44. Wang M, Yuan W, Jiang X, Jing Y, Wang Z (2014) Disruption of microalgal cells using high-frequency focused ultrasound. Bioresource Technol 153:315–321CrossRefGoogle Scholar
  45. Wu X, Joyce EM, Mason TJ (2012) Evaluation of the mechanisms of the effect of ultrasound on Microcystis aeruginosa at different ultrasonic frequencies. Water Res 46:2851–2858CrossRefPubMedGoogle Scholar
  46. Yamamoto K, King PM, Wu X, Mason TJ, Joyce EM (2015) Effect of ultrasonic frequency and power on the disruption of algal cells. Ultrason Sonochem 24:165–171CrossRefPubMedGoogle Scholar
  47. 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

Copyright information

© Springer Science+Business Media Dordrecht 2017

Authors and Affiliations

  • Zhipeng Duan
    • 1
  • Xiao Tan
    • 1
    Email author
  • Jiujia Guo
    • 1
  • Christine Wairimu Kahehu
    • 1
  • Hanpei Yang
    • 1
  • Xueying Zheng
    • 1
  • Feng Zhu
    • 1
  1. 1.Key Laboratory of Integrated Regulation and Resource Development on Shallow Lakes of Ministry of Education, College of EnvironmentHohai UniversityNanjingChina

Personalised recommendations