Cell Biochemistry and Biophysics

, Volume 67, Issue 3, pp 829–835

Comparable Effects of Low-intensity Electromagnetic Irradiation at the Frequency of 51.8 and 53 GHz and Antibiotic Ceftazidime on Lactobacillus acidophilus Growth and Survival

Original Paper

Abstract

The effects of low-intensity electromagnetic irradiation (EMI) with the frequencies of 51.8 and 53 GHz on Lactobacillus acidophilus growth and survival were revealed. These effects were compared with antibacterial effects of antibiotic ceftazidime. Decrease in bacterial growth rate by EMI was comparable with the inhibitory effect of ceftazidime (minimal inhibitory concentration—16 μM) and no enhanced action was observed with combined effects of EMI and the antibiotic. However, EMI-enhanced antibiotic inhibitory effect on bacterial survival. The kinetics of the bacterial suspension oxidation–reduction potential up to 24 h of the growth was changed by EMI and ceftazidime. The changes were more strongly expressed by combined effects of EMI and antibiotic especially up to 12 h. Moreover, EMI did not change overall energy (glucose)-dependent H+ efflux across the membrane but it increased N,N′-dicyclohexylcarbodiimide (DCCD)-inhibited H+ efflux. In contrast, this EMI in combination with ceftazidime decreased DCCD-sensitive H+ efflux. Low-intensity EMI had inhibitory effect on L. acidophilus bacterial growth and survival. The effect on bacterial survival was more significant in the combination with ceftazidime. The H+-translocating F0F1-ATPase, for which DCCD is specific inhibitor, might be a target for EMI and ceftazidime. The revealed bactericide effects on L. acidophilus can be applied in biotechnology, food producing and safety technology.

Keywords

Electromagnetic irradiation Ceftazidime Bacterial growth and survival Proton transport Food producing and safety technology Lactobacillus 

References

  1. 1.
    Beresford, T. P., Fitzsimons, N. A., Brennan, N. L., et al. (2001). Recent advances in cheese microbiology. International Dairy Journal, 11, 259–274.CrossRefGoogle Scholar
  2. 2.
    Topisirovic, L., Veljovic, K., Terzic-Vidojevic, A., et al. (2007). Comparative analysis of antimicrobial and proteolytic activity of lactic acid bacteria isolated from zlatar cheese. Genetika, 39, 125–138.CrossRefGoogle Scholar
  3. 3.
    Altermann, E., Russel, W. M., Azcarate-Peril, M. A., et al. (2005). Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proceedings of National Academy of Sciences of USA, 102, 3906–3912.CrossRefGoogle Scholar
  4. 4.
    Gonzalez, S. N., Apella, M. C., Romero, N., et al. (1989). Superoxide dismutase activity in some strains of Lactobacilli: Induction by manganese. Chemical & Pharmaceutical Bulletin, 37, 3026–3028.CrossRefGoogle Scholar
  5. 5.
    Geveke, D. J., Gurtler, J., & Zhang, H. Q. (2009). Inactivation of Lactobacillus plantarum in apple cider, using radio frequency electric fields. Journal of Food Protection, 72, 656–661.PubMedGoogle Scholar
  6. 6.
    Torgomyan, H., & Trchounian, A. (2013). Bactericidal effects of low-intensity extremely high frequency electromagnetic field: An overview with phenomenon, mechanisms, targets and consequences. Critical Reviews on Microbiology, 39, 102–111.CrossRefGoogle Scholar
  7. 7.
    Zand, N., Foroudi, F., Mailova, E., et al. (2010). Sterilization of flexible pouch by high frequency electromagnetic induction, using cooked chick and chick meal. African Journal of Microbiological Research, 4, 2011–2021.Google Scholar
  8. 8.
    Belyaev, I. Y., Scheglov, V. S., Alipov, Y. D., et al. (1996). Resonance effect of millimeter waves in the power range from 10−19 to 3 × 10−3 W/cm2 on Escherichia coli cells at different concentrations. Bioelectromagnetics, 17, 312–321.PubMedCrossRefGoogle Scholar
  9. 9.
    Reguera, G. (2011). When microbial conversations get physical. Trends in Microbiology, 19, 105–116.PubMedCrossRefGoogle Scholar
  10. 10.
    Trushin, M. (2003). The possible role of electromagnetic fields in bacterial communication. Journal of Microbiology, Immunology, and Infection, 36, 153–160.PubMedGoogle Scholar
  11. 11.
    Tadevosyan, H., Kalantaryan, V., & Trchounian, A. (2007). The effects of electromagnetic radiation of extremely high frequency and low intensity on the growth rate of Escherichia coli and the role of medium pH. Biophysics, 52, 893–898.Google Scholar
  12. 12.
    Tadevosyan, H., Kalantaryan, V., & Trchounian, A. (2008). Extremely high frequency electromagnetic radiation enforces bacterial effects of inhibitors and antibiotics. Cell Biochemistry and Biophysics, 51, 97–103.PubMedCrossRefGoogle Scholar
  13. 13.
    Torgomyan, H., Tadevosyan, H., & Trchounian, A. (2011). Extremely high frequency electromagnetic irradiation in combination with antibiotics enhances antibacterial effects on Escherichia coli. Current Microbiology, 62, 962–967.PubMedCrossRefGoogle Scholar
  14. 14.
    Torgomyan, H., Kalantaryan, V., & Trchounian, A. (2011). Low intensity electromagnetic irradiation with 70.6 and 73 GHz frequencies affects Escherichia coli growth and changes water properties. Cell Biochemistry and Biophysics, 60, 275–281.PubMedCrossRefGoogle Scholar
  15. 15.
    Ohanyan, V., Sarkisyan, A., Tadevosyan, H., et al. (2008). The action of low-intensity extremely high frequency electromagnetic radiation on growth parameters for bacteria Enterococcus hirae. Biophysics, 53, 406–408.CrossRefGoogle Scholar
  16. 16.
    Torgomyan, H., Ohanyan, V., Blbulyan, S., et al. (2012). Electromagnetic irradiation of Enterococcus hirae at low-intensity 51.8 and 53.0 GHz frequencies: Changes in bacterial cell membrane properties and enhanced antibiotics effects. FEMS Microbiology Letters, 329, 131–137.PubMedCrossRefGoogle Scholar
  17. 17.
    Torgomyan, H., & Trchounian, A. (2012). Escherichia coli membrane-associated energy-dependent processes and sensitivity toward antibiotics changes as responses to low-intensity electromagnetic irradiation of 70.6 and 73 GHz frequencies. Cell Biochemistry and Biophysics, 62, 451–461.PubMedCrossRefGoogle Scholar
  18. 18.
    Jeanson, S., Hilgert, N., Coquillard, M., et al. (2009). Milk acidification by Lactococcus lactis is improved by decreasing the level of dissolved oxygen rather than decreasing redox potential in the milk prior to inoculation. International Journal of Food Microbiology, 131, 75–81.PubMedCrossRefGoogle Scholar
  19. 19.
    Kojic, M., Fira, D., Bojovic, B., et al. (1995). Comparative study on cell envelope-associated proteinases in natural isolates of mesophilic lactobacilli. Journal of Applied Bacteriology, 79, 61–68.CrossRefGoogle Scholar
  20. 20.
    De Man, J. C., Rogosa, M., & Sharpe, M. E. (1960). A medium for the cultivation of lactobacilli. Journal of Applied Bacteriology, 23, 130–135.CrossRefGoogle Scholar
  21. 21.
    Soghomonyan, D., Akopyan, K., & Trchounian, A. (2011). pH and oxidation–reduction potential change of environment during growth of lactic acid bacteria: Effects of oxidizers and reducers. Applied Biochemistry and Microbiology, 47, 27–31.CrossRefGoogle Scholar
  22. 22.
    Betskii, O. V., Devyatkov, N. D., & Kislov, V. V. (2000). Low intensity millimeter waves in medicine and biology. Critical Reviews on Biomedical Engineering, 28, 247–268.CrossRefGoogle Scholar
  23. 23.
    Hedges, A. J. (2002). Estimating the precision of serial dilutions and viable bacterial counts. International Journal of Food Microbiology, 76, 207–214.PubMedCrossRefGoogle Scholar
  24. 24.
    Kirakosyan, G., Trchounian, K., Vardanyan, Z., et al. (2008). Copper (II) Ions affect Escherichia coli membrane vesicles’ SH-groups and a disulfide-dithiol interchange between membrane proteins. Cell Biochemistry and Biophysics, 51, 45–50.PubMedCrossRefGoogle Scholar
  25. 25.
    Bauer, A. W., Kirby, M. M., Sherris, J. C., et al. (1966). Antibiotic susceptibility testing by a standardized single disk method. American Journal of Clinical Pathology, 45, 493–496.PubMedGoogle Scholar
  26. 26.
    Ocana V., Silva C., & Nader-Macıas M. E. (2006) Antibiotic susceptibility of potentially probiotic vaginal Lactobacilli. Infection Diseases in Obstetric Gynecology, 2006, 18182.Google Scholar
  27. 27.
    Trchounian, A., Ogandzhanyan, E., Sarkisyan, E., et al. (2001). Membranotropic effects of electromagnetic radiation of extremely high frequency in Escherichia coli. Biophysics, 46, 69–76.Google Scholar
  28. 28.
    Trchounian, A. A., & Vassilian, A. V. (1994). Relationship between the F 0 F 1-ATPase and the K+-transport system within the membrane of anaerobically grown Escherichia coli. N,N′-Dicyclohexylcarbodiimide-sensitive ATPase activity in mutants with defects in K+-transport. Journal of Bioenergetics and Biomembranes, 26, 563–571.PubMedCrossRefGoogle Scholar
  29. 29.
    Bagramyan, K., Galstyan, A., & Trchounian, A. (2000). Redox potential is a determinant in the Escherichia coli anaerobic fermentative growth and survival: Effects of impermeable oxidant. Bioelectrochemistry, 51, 151–156.PubMedCrossRefGoogle Scholar
  30. 30.
    Bagramyan, K., & Trchounian, A. (1997). Decrease of redox potential in the anaerobic growing Escherichia coli suspension and proton-potassium exchange. Bioelectrochemistry and Bioenergetics, 43, 129–134.CrossRefGoogle Scholar
  31. 31.
    Vassilian, A., & Trchounian, A. (2009). Environment oxidation-reduction potential and redox sensing by bacteria. In A. Trchounian (Ed.), Bacterial Membranes (pp. 163–195). Trivandrum: Research Signpost.Google Scholar
  32. 32.
    Waché, Y., Riondet, C., Diviès, C., et al. (2002). Effect of reducing agents on the acidification capacity and the proton motive force of Lactococcus lactis ssp. cremoris resting cells. Bioelectrochemistry, 57, 113–118.PubMedCrossRefGoogle Scholar
  33. 33.
    Trchounian, A. (2004). Escherichia coli proton-translocating F 0 F 1-ATP synthase and its association with solute secondary transporters and/or enzymes of anaerobic oxidation-reduction under fermentation. Biochemical and Biophysical Research Communications, 315, 1051–1057.PubMedCrossRefGoogle Scholar
  34. 34.
    Lee, S., Hinz, A., Bauerle, E., et al. (2009). Targeting a bacterial stress response to enhance antibiotic action. Proceedings of National Academy of Sciences of USA, 106, 14570–14575.CrossRefGoogle Scholar
  35. 35.
    Ohanyan, V. (2012). Combined effects of extremely high frequency electromagnetic field and antibiotics on Enterococcus hirae growth and survival. Reports of National Academy of Sciences of Armenia, 112, 87–94.Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Department of Biophysics, Biology FacultyYerevan State UniversityYerevanArmenia
  2. 2.Department of Microbiology, Plants and Microbes Biotechnology, Biology FacultyYerevan State UniversityYerevanArmenia

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