Skip to main content
SpringerLink
Log in

Stimulation of Saccharomyces cerevisiae Cultures by Pulsed Electric Fields

  • Original Paper
  • Published:
Food and Bioprocess Technology Aims and scope Submit manuscript

Abstract

The effects of stimulation of Saccharomyces cerevisiae cells in an aqueous suspension by pulsed electric field (PEF) with electric field strength E = 20–2,000 V cm−1 and effective PEF treatment time t PEF = 10−5–1 s were investigated. At relatively high electric field strengths (E > 1,000 V cm−1) and moderate times of PEF treatment (t PEF > 100 μs), the extraction of ionic components from yeast was observed, which can be related to electroporation of cell membranes. Petri dishes counting revealed dependency of the colony sizes on the time of preliminary fermentation t f and power consumption W. The “logarithmic” and “saturated” types of electrostimulation were distinguished. At “logarithmic” electrostimulation (10−7 J mL−1 < W < 10−1 J mL−1), the viability of yeast cells increased with the increase of power consumption and was higher for longer fermentation (t f  = 24 h). However, at “saturated” electrostimulation (10−1 J mL−1 < W < 101 J mL−1), the viability of yeast cells was noticeably higher for t f  = 1 h than for t f  = 24 h. The impact of preliminary fermentation time and PEF protocol on biological activity of cells and consumption of nutrients was also discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Araújo, O. Q. F., Coelho, M. A. Z., Margarit, I. C. P., Vaz-Junior, C. A., & Rocha-Leão, M. H. M. (2004). Electrical stimulation of Saccharomyces cerevisiae cultures. Brazilian Journal of Microbiology, 35, 97–103.

    Article  Google Scholar 

  • Araújo, O. Q. F., Oliveira, A. A. C., Torres, C. C. O., Rocha-Leão, M. H., Margarit, I. C. P., & Coelho, M. A. Z. (2007). Glucose uptake in electrically stimulated cultures of Saccharomyces cerevisiae. In: Proceedings of European Congress of Chemical Engineering (ECCE-6) Copenhagen, 16-20 September 2007 (pp. 1–9).

  • Barbosa-Cánovas, G. V., Fernández-Molina, J. J., & Swanson, B. G. (2001). Pulsed electric fields: a novel technology for food preservation. Agro Food Industry Hi Tech, 12(2), 9–14.

    Google Scholar 

  • Berg, H. (1995). Possibilities and problems of low frequency weak electromagnetic fields in cell biology. Bioelectrochemistry and Bioenergetics, 38(1), 153–159.

    Article  CAS  Google Scholar 

  • Bluhm, H., & Sack, M. (2008). Industrial-scale treatment of biological tissues with pulsed electric fields. In E. Vorobiev & N. Lebovka (Eds.), Electrotechnologies for extraction from food plants and biomaterials (pp. 237–269). New York: Springer.

    Google Scholar 

  • Castro, I., Teixeira, J. A., & Vicente, A. A. (2012). The effect of the electric field on lag-phase, ethanol and β-galactosidase production of a recombinant S. cerevisiae growing on lactose. Food and Bioprocess Technology, 5(8), 3014–3020.

    Article  CAS  Google Scholar 

  • Cserhalmi, Z., Vidacs, I., Beczner, J., & Czukor, B. (2002). Inactivation of Saccharomyces cerevisiae and Bacillus cereus by pulsed electric fields technology. Innovative Food Science & Emerging Technologies, 3(1), 41–45.

    Article  CAS  Google Scholar 

  • Dimitrov, D. S., & Sowers, A. E. (1990). Membrane electroporation: fast molecular exchange by electroosmosis. Biochimica et Biophysica Acta, 1022, 381–392.

    Article  CAS  Google Scholar 

  • Donsi, F., Ferrari, G., & Pataro, G. (2010). Applications of pulsed electric field treatments for the enhancement of mass transfer from vegetable tissue. Food Engineering Reviews, 2(2), 109–130. doi:10.1007/s12393-010-9015-3.

    Article  CAS  Google Scholar 

  • El Zakhem, H., Lanoiselle, J. L., Lebovka, N. I., Nonus, M., & Vorobiev, E. (2006a). Behavior of yeast cells in aqueous suspension affected by pulsed electric field. Journal of Colloid and Interface Science, 300(2), 553–563.

    Article  Google Scholar 

  • El Zakhem, H., Lanoiselle, J.-L., Lebovka, N. I., Nonus, M., & Vorobiev, E. (2006b). The early stages of Saccharomyces cerevisiae yeast suspensions damage in moderate pulsed electric fields. Colloids and Surfaces B Biointerfaces, 47(2), 189–197.

    Article  Google Scholar 

  • Fiedler, U., Gröbner, U., & Berg, H. (1995). Electrostimulation of yeast proliferation. Bioelectrochemistry and Bioenergetics, 38(2), 423–425.

    Article  CAS  Google Scholar 

  • Fologea, D., Vassu-Dimov, T., Stoica, I., Csutak, O., & Radu, M. (1998). Increase of Saccharomyces cerevisiae plating efficiency after treatment with bipolar electric pulses. Bioelectrochemistry and Bioenergetics, 46(2), 285–287.

    Article  CAS  Google Scholar 

  • Fologea, D., Vassu, T., Stoica, I., Csutak, O., Sasarman, E., Smarandache, D., et al. (2004). Efficient electrotransformation of yeast using bipolar electric pulses. Romanian Biotechnological Letters, 9, 1505–1510.

    Google Scholar 

  • Ganeva, V., Galutzov, B., & Teissié, J. (2003). High yield electroextraction of proteins from yeast by a flow process. Analytical Biochemistry, 315(1), 77–84.

    Article  CAS  Google Scholar 

  • Ganeva, V., Galutzov, B., & Teissie, J. (2004). Flow process for electroextraction of intracellular enzymes from the fission yeast, Schizosaccharomyces pombe. Biotechnology Letters, 26(11), 933–937. doi:10.1023/B:bile.0000025906.95694.1a.

    Article  CAS  Google Scholar 

  • Jin, Y., Wang, M., Lin, S., Guo, Y., Liu, J., & Yin, Y. (2011). Optimization of extraction parameters for trehalose from beer waste brewing yeast treated by high-intensity pulsed electric fields (PEF). African Journal of Biotechnology, 10(82), 19144–19152. doi:10.5897/AJB11.2687.

    CAS  Google Scholar 

  • Knorr, D., Engel, K.-H., Vogel, R., Kochte-Clemens, B., & Eisenbrand, G. (2008). Statement on the treatment of food using a pulsed electric field. Molecular Nutrition & Food Research, 52(12), 1539–1542. doi:10.1002/mnfr.200800391.

    Article  CAS  Google Scholar 

  • Liu, Z., Yang, R., & Zhao, W. (2007). Extraction of protein and nucleic acid from waste beer yeast with pulsed electric fields. Shipin Gongye Keji, 28(3), 85–88.

    Google Scholar 

  • Liu, M., Zhang, M., Lin, S., Liu, J., Yang, Y., & Jin, Y. (2012). Optimization of extraction parameters for protein from beer waste brewing yeast treated by pulsed electric fields (PEF). African Journal of Microbiology Research, 6(22), 4739–4746. doi:10.5897/AJMR12.117.

    CAS  Google Scholar 

  • Liu, D., Lebovka, N. I., & Vorobiev, E. (2013). Impact of electric pulse treatment on selective extraction of intracellular compounds from Saccharomyces cerevisiae yeasts. Food and Bioprocess Technology, 6(2), 576–584.

    Article  CAS  Google Scholar 

  • Lustrato, G., Alfano, G., Belli, C., Grazia, L., Iorizzo, M., Maiuro, L., et al. (2003). Controlling grape must fermentation in early winemaking phases: the role of electrochemical treatment. Journal of Applied Microbiology, 95(5), 1087–1095.

    Article  CAS  Google Scholar 

  • McCabe, A., Barron, N., McHale, L., & McHale, A. P. (1995). Increased efficiency of substrate utilization by exposure of the thermotolerant yeast strain, Kluyveromyces marxianus IMB3 to electric-field stimulation. Biotechnology Techniques, 9(2), 133–136.

    Article  CAS  Google Scholar 

  • Nakanishi, K., Tokuda, H., Soga, T., Yoshinaga, T., & Takeda, M. (1998). Effect of electric current on growth and alcohol production by yeast cells. Journal of Fermentation and Bioengineering, 85(2), 250–253.

    Article  CAS  Google Scholar 

  • Nawarathna, D., Miller, J. H., Claycomb, J. R., Cardenas, G., & Warmflash, D. (2005). Harmonic response of cellular membrane pumps to low frequency electric fields. Physical Review Letters, 95(15), 158103. doi:10.1103/PhysRevLett.95.158103.

    Article  CAS  Google Scholar 

  • Nawarathna, D., Claycomb, J. R., Cardenas, G., Gardner, J., Warmflash, D., Miller, J. H., et al. (2006). Harmonic generation by yeast cells in response to low-frequency electric fields. Physical Review E, 73(5), 51914. doi:10.1103/PhysRevE.73.051914.

    Article  CAS  Google Scholar 

  • Ohshima, T., & Sato, M. (2004). Bacterial sterilization and intracellular protein release by a pulsed electric field. Advances in Biochemical Engineering/Biotechnology, 90, 113–133.

    Article  CAS  Google Scholar 

  • Ohshima, T., Sato, M., & Saito, M. (1995). Selective release of intracellular protein using pulsed electric field. Journal of Electrostatics, 35(1), 103–112.

    Article  CAS  Google Scholar 

  • Pakhomov, A. G., Miklavcic, D., & Markov, M. S. (Eds.). (2010). Advanced electroporation techniques in biology and medicine Food and biomaterials processing assisted by electroporation. New York: CRC Press.

    Google Scholar 

  • Palaniappan, S., Sastry, S. K., & Richter, E. R. (1990). Effects of electricity on microorganisms: a review. Journal of Food Processing and Preservation, 14(5), 393–414. doi:10.1111/j.1745-4549.1990.tb00142.x.

    Article  Google Scholar 

  • Pankiewicz, U., & Jamroz, J. (2008). Accumulation of selenium and catalase activity changes in the cells of Saccharomyces cerevisiae on pulsed electric field (PEF) treatment. Annals of Microbiology (Milano, Italy), 58(2), 239–243. doi:10.1007/BF03175323.

    Article  CAS  Google Scholar 

  • Pankiewicz, U., & Jamroz, J. (2010). Effect of pulsed electric fields upon accumulation of magnesium in Saccharomyces cerevisiae. European Food Research and Technology, 231(5), 663–668.

    Article  CAS  Google Scholar 

  • Pankiewicz, U., & Jamroz, J. (2011). Effect of pulsed electric fields upon accumulation of zinc in Saccharomyces cerevisiae. Journal of Microbiology and Biotechnology, 21(6), 646–651.

    CAS  Google Scholar 

  • Pataro, G., Senatore, B., Donsì, G., & Ferrari, G. (2011). Effect of electric and flow parameters on PEF treatment efficiency. Journal of Food Engineering, 105(1), 79–88.

    Article  Google Scholar 

  • Peng, L., & Zeng, X. (2011). Effect of ultrasonic, PEF and microwave on the extraction of trehalose from yeast cells. Shipin Keji, 36(7), 161–165.

    CAS  Google Scholar 

  • Petrofsky, J., Laymon, M., Chung, W., Collins, K., & Yang, T.-N. (2006). Effect of electrical stimulation on bacterial growth. The Journal of Neurological and Orthopaedic Medicine and Surgery(archive of reprints),1-21. Web address: http://aanos.org/wpcontent/uploads/2014/02/Eff-of-Elect-Stim-on-Bact-Grwth.pdf

  • Raso, J., & Heinz, V. (Eds.). (2006). Pulsed electric field technology for the food industry. Fundamentals and applications. New York: Springer.

    Google Scholar 

  • Sauer, U. (2001). Evolutionary engineering of industrially important microbial phenotypes. In T. Scheper (Ed.), Advances in biochemical engineering/biotechnology (Vol. 73, pp. 130–167). Berlin: Springer.

    Google Scholar 

  • Schrive, L., Grasmick, A., Moussiere, S., & Sarrade, S. (2006). Pulsed electric field treatment of Saccharomyces cerevisiae suspensions: a mechanistic approach coupling energy transfer, mass transfer and hydrodynamics. Biochemical Engineering Journal, 27(3), 212–224.

    Article  CAS  Google Scholar 

  • Shynkaryk, M. V., Lebovka, N. I., Lanoisellé, J. L., Nonus, M., Bedel-Clotour, C., & Vorobiev, E. (2009). Electrically-assisted extraction of bio-products using high pressure disruption of yeast cells (Saccharomyces cerevisiae). Journal of Food Engineering, 92(2), 189–195.

    Article  Google Scholar 

  • Simpson, J., Brady, D., Rollan, A., Barron, N., McHale, L., & McHale, A. P. (1995). Increased ethanol production during growth of electric-field stimulated Kluweromyces marxianus IMB3 during growth on lactose-containing media at 45 C. Biotechnology Letters, 17(7), 1757–1760.

    Article  Google Scholar 

  • Somolinos, M., Garcia, D., Condon, S., Manas, P., & Pagan, R. (2007). Relationship between sublethal injury and inactivation of yeast cells by the combination of sorbic acid and pulsed electric fields. Applied and Environmental Microbiology, 73(12), 3814–3821.

    Article  CAS  Google Scholar 

  • Somolinos, M., Mañas, P., Condón, S., Pagán, R., & García, D. (2008). Recovery of Saccharomyces cerevisiae sublethally injured cells after pulsed electric fields. International Journal of Food Microbiology, 125(3), 352–356.

    Article  CAS  Google Scholar 

  • Suga, M., & Hatakeyama, T. (2009). Gene transfer and protein release of fission yeast by application of a high voltage electric pulse. Analytical and Bioanalytical Chemistry, 394(1), 13–16.

    Article  CAS  Google Scholar 

  • Suga, M., Goto, A., & Hatakeyama, T. (2006). Control by osmolarity and electric field strength of electro-induced gene transfer and protein release in fission yeast cells. Journal of Electrostatics, 64(12), 796–801. doi:10.1016/j.elstat.2006.01.007.

    Article  CAS  Google Scholar 

  • Tanino, T., Sato, S., Oshige, M., & Ohshima, T. (2012). Analysis of the stress response of yeast Saccharomyces cerevisiae toward pulsed electric field. Journal of Electrostatics, 70(2), 212–216.

    Article  CAS  Google Scholar 

  • Teissié, J., Eynard, N., Vernhes, M. C., Bénichou, A., Ganeva, V., Galutzov, B., et al. (2002). Recent biotechnological developments of electropulsation. A prospective review. Bioelectrochemistry, 55(1–2), 107–112.

    Article  Google Scholar 

  • Tsong, T. Y. (1991). Electroporation of cell membranes. Biophysical Journal, 60(2), 297–306. doi:10.1016/S0006-3495(91)82054-9.

    Article  CAS  Google Scholar 

  • Vassu, T., Fologea, D., Csutak, O., Smarandache, D., Sasarman, E., Stoica, I., et al. (2004). Secondary effects of electroporation with bipolar electric pulses: electrostimulation. Romanian Biotechnological Letters, 9, 1541–1544.

    Google Scholar 

  • Vega-Mercado, H., Belloso, O. M., Qin, B.-L., Chang, F. J., Gongora-Nieto, M. M., Barbosa-Canovas, G. V., et al. (1997). Non-thermal food preservation: pulsed electric fields. Trends in Food Science & Technology, 8(5), 151–157. doi:10.1016/S0924-2244(97)01016-9.

    Article  CAS  Google Scholar 

  • Walther, T., Reinsch, H., Grose, A., Ostermann, K., Deutsch, A., & Bley, T. (2004). Mathematical modeling of regulatory mechanisms in yeast colony development. Journal of Theoretical Biology, 229, 327–338.

    Article  CAS  Google Scholar 

  • Wang, M., Jin, Y., Liu, M., Zhang, M., Yang, Y., & Lin, S. (2011). Activating effect of pulsed electric field treatment on trehalose activity in waste brewing yeast cells. Shipin Kexue (Beijing, China), 32(23), 87–90.

    Google Scholar 

  • Weaver, J. C., & Chizmadzhev, Y. A. (1996). Theory of electroporation: a review. Bioelectrochemistry and Bioenergetics, 41(2), 135–160.

    Article  CAS  Google Scholar 

  • Xie, G., Yang, R., Lu, R., Zhang, W., & Zhao, W. (2008). Release of protein and nucleic acid by inducing brewer yeast cell with high-voltage pulsed electric fields. Shipin Yu Fajiao Gongye, 34(3), 44–47.

    CAS  Google Scholar 

  • Ye, H., Jin, Y., Lin, S., Liu, M., Yang, Y., Zhang, M., et al. (2012). Effect of pulsed electric fields on the activity of neutral trehalase from beer yeast and RSM analysis. International Journal of Biological Macromolecules, 50(5), 1315–1321.

    Article  CAS  Google Scholar 

  • Zhang, Q., Monsalve-Gonzalez, A., Qin, B. L., Barbosa-Canovas, G. V., & Swanson, B. G. (1994). Inactivation of Saccharomyces cerevisiae in apple juice by square-wave and exponential-decay pulsed electric field. Journal of Food Process Engineering, 17(4), 469–478.

    Article  Google Scholar 

Download references

Acknowledgments

The authors appreciate the financial support from the financial support from the CNRS-Lebanon and the support from the COST Action TD1104 (EP4Bio2Med-European Network for Development of Electroporation-based Technologies and treatments). The authors also thank Dr. N.S. Pivovarova for her help with the preparation of the manuscript.

Author information

Authors and Affiliations

  1. Équipe TAI EA TIMR 4297, Université de Technologie de Compiègne, Centre de Recherche de Royallieu, 20529-60205, Compiègne cedex, France

    Jessy R. Mattar, Maurice Nonus, Nikolai I. Lebovka & Eugene Vorobiev

  2. Chemical Engineering Department, University of Balamand, P.O. Box 33, Amioun, North, Lebanon

    Jessy R. Mattar & Henri El Zakhem

  3. Équipe TAI EA TIMR 4297, École Supérieure de Chimie Organique et Minérale, 1 allée du réseau Jean-Marie Buckmaster, 60200, Compiègne cedex, France

    Mohammad F. Turk

  4. Department of Physical Chemistry of Disperse Minerals, Institute of Biocolloidal Chemistry named after F.D. Ovcharenko, NAS of Ukraine, 42 Blvd., Vernadskogo, Kyiv, 03142, Ukraine

    Nikolai I. Lebovka

Authors
  1. Jessy R. Mattar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mohammad F. Turk
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Maurice Nonus
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nikolai I. Lebovka
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Henri El Zakhem
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eugene Vorobiev
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nikolai I. Lebovka.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mattar, J.R., Turk, M.F., Nonus, M. et al. Stimulation of Saccharomyces cerevisiae Cultures by Pulsed Electric Fields. Food Bioprocess Technol 7, 3328–3335 (2014). https://doi.org/10.1007/s11947-014-1336-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11947-014-1336-4

Keywords

Search

Navigation