Electrical characterization of phytoplankton suspensions using impedance spectroscopy

Abstract

This study used impedance spectroscopy measurements to extract the electrical properties of phytoplankton cells in suspension. Experimental measurements were acquired, and the single-shell model was applied to extract the specific membrane capacitance, cytoplasm permittivity, and conductivity of assumingly spherical cells in suspension utilizing Maxwell’s mixture theory of a controlled volume fraction of cells. The impedance of suspensions of algae was measured at different frequencies ranging from 3 kHz to 10 MHz and impedance values were compared to investigate differences between two types of cells by characterizing their change in cytoplasm permittivity and specific membrane capacitance. Differentiation between healthy control and nitrogen-depleted cultured algae was attempted. The extracted specific membrane capacitances of Chlamydomonas and Selenastrum were 15.5 ± 3.6 and 40.6 ± 12.6 mF m− 2 respectively. Successful differentiation based on the specific membrane capacitance of different algae species was achieved. However, no significant difference was noticed between nitrogen-abundant and nitrogen-depleted cultures.

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References

  1. Abt V, Gringel F, Han A, Neubauer P, Birkholz M (2020) Separation, characterization, and handling of microalgae by dielectrophoresis. Microorganisms 9:540

    Article  Google Scholar 

  2. Andersen RA (ed.) (2005) Algal culturing techniques. Elsevier, Amsterdam

  3. Das D, Kamil FA, Biswas K, Das S (2014) Evaluation of single cell electrical parameters from bioimpedance of a cell suspension. RSC Adv 4:18178–18185

    CAS  Article  Google Scholar 

  4. Deng YL, Juang CJS JY (2013) Separation of microalgae with different lipid contents by dielectrophoresis. Bioresour Technol 135:137–141

    CAS  Article  Google Scholar 

  5. Domozych DS, Ciancia M, Fangel JU, Mikkelsen MD, Ulvskov P, Willats WGT (2012) The cell walls of green algae: a journey through evolution and diversity. Front Plant Sci 3:82

    CAS  Article  Google Scholar 

  6. Donk EV, Lürling M, Hessen D, Lokhorst G (1997) Altered cell wall morphology in nutrient-deficient phytoplankton and its impact on grazers. Limnol Oceanogr 42:357–364

    Article  Google Scholar 

  7. Foster K, Schwan H (1989) Dielectric properties of tissues and biological materials: a critical review. CRC Biomed Eng 17:25–104

    CAS  Google Scholar 

  8. Graham L, Wilcox L (2000) Algae. Prentice-Hall. Upper Saddle River

  9. Hadady H, Wong JJ, Hiibel SR, Redelman D, Geiger EJ (2014) High frequency dielectrophoretic response of microalgae over time. Electrophoresis 35:3533–3540

    CAS  Article  Google Scholar 

  10. Jang LS, Wang MH (2007) Microfluidic device for cell capture and impedance measurement. Biomed Microdevices 9:737–743

    Article  Google Scholar 

  11. Kumar RTK, Kanchustambham P, Kinnamon D, Prasad S (2017) 2D dielectrophoretic signature of Coscinodiscus wailesii algae in non-uniform electric fields. Algal Res 27:109–114

    Article  Google Scholar 

  12. Lasia A (2014) Electrochemical impedance spectroscopy and its applications. Springer, New York

    Google Scholar 

  13. Lindsey R, Scott M (2010) What are Phytoplankton?. https://earthobservatory.nasa.gov/features/Phytoplankton

  14. Mata TM, Martins AA, Caetano NS (2010) Microalgae for biodiesel production and other applications: a review. Renew Sust Energy Rev 14:217–232

    CAS  Article  Google Scholar 

  15. Maxwell J (1954) Treatise on Electricity and Magnetism. 2 vols. Dover, New York

    Google Scholar 

  16. Morgan H, Green NG (1997) Dielectrophoretic manipulation of rod-shaped viral particles. J Electrost 42:279–293

    Article  Google Scholar 

  17. Morgan H, Sun T, Holmes D, Gawad S, Green NG (2007) Single cell dielectric spectroscopy. J Phys D 40:61–70

    CAS  Article  Google Scholar 

  18. Petchakup C, Li KHH, Hou HW (2017) Advances in single cell impedance cytometry for biomedical applications. Micromachines 8:87

    Article  Google Scholar 

  19. Sancho M, Martínez G, Martín C (2003) Accurate dielectric modelling of shelled particles and cells. J Electrost 57:143–156

    Article  Google Scholar 

  20. Searchinger T, Heimlich R, Houghton RA, Dong F, Elobeid A, Fabiosa J, Tokgoz S, Hayes D, Yu TH (2008) Use of U.S. croplands for biofuels increases greenhouse gases through emissions from land-use change. Science 319:1238–1240

    CAS  Article  Google Scholar 

  21. Siebman C, Velev O, Slaveykova V (2017) Alternating current-dielectrophoresis collection and chaining of phytoplankton on chip: Comparison of individual species and artificial communities. Biosensors 7:4–4

    Article  Google Scholar 

  22. Sun T, Morgan H (2010) Single-cell microfluidic impedance cytometry: a review. Mircrofluid Nanofluid 8:423–443

    CAS  Article  Google Scholar 

  23. Wang B, Li Y, Wu N, Lan CQ (2008) CO2 biomitigation using microalgae. Appl Microbiol Biotechnol 79:707–718

    CAS  Article  Google Scholar 

  24. Wanichapichart P, Bunthawin S, Kaewpaiboon A, Kanchanapoom K (2001) Determination of cell dielectric properties using dielectrophoretic technique. ScienceAsia 28:113–119

    Article  Google Scholar 

  25. Weaver JC, Chizmadzhev YA (1996) Theory of electroporation: A review. Bioelectrochem Bioenerg 41:135–160

    CAS  Article  Google Scholar 

  26. Zabara MA, Ulgut B (2020) Electrochemical Impedance Spectroscopy based voltage modeling of lithium thionyl chloride (Li∖SOCL2) primary battery at arbitrary discharge. Electrochim Acta 334:135584–135584

    CAS  Article  Google Scholar 

  27. Zhu L (2015) Biorefinery as a promising approach to promote microalgae industry: An innovative framework. Renew Sust Energ Rev 41:1376–1384

    Article  Google Scholar 

Download references

Funding

The authors would like to acknowledge the support from National Science Foundation under grant No. 1550509 “Isomotive dielectrophoresis for enhanced analyses of cell subpopulations.”

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S. J. W. and S. P. H. obtained funding for the project. S. P. H. provided cells from various cultures for the experiments.

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Correspondence to Stuart J. Williams.

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The authors declare that they have no conflict of interest.

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M. R. J and M. Z. R contributed equally to this work.

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Jett, M.R., Rashed, M.Z., Hendricks, S.P. et al. Electrical characterization of phytoplankton suspensions using impedance spectroscopy. J Appl Phycol (2021). https://doi.org/10.1007/s10811-020-02363-2

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Keywords

  • Electrochemical impedance spectroscopy
  • Cell-in-suspension analysis
  • Phytoplankton differentiation
  • Cell characterization