Skip to main content
SpringerLink
Log in

The Effects of Manganese (II) But Not Nickel (II) Ions on Enterococcus hirae Cell Growth, Redox Potential Decrease, and Proton-Coupled Membrane Transport

  • Original Paper
  • Published:
Cell Biochemistry and Biophysics Aims and scope Submit manuscript

Abstract

Enterococcus hirae grow well under anaerobic conditions by fermenting glucose, accompanied with the decrease of oxidation–reduction potential (E h) from positive values to negative ones. It was shown that heavy metals—copper and iron ions—affect E. hirae growth and alter E h and proton-potassium ions fluxes through the cell membrane. The aim of this study was to establish the effects of manganese (II) ions on bacterial growth within the concentration range of 0.01–1 mM and compare with nickel (II) ions’ effect. The presence of Mn2+ during E. hirae ATCC9790 growth had significant effects: The lag phase duration decreased while the specific growth rate was increased; decrease in E h was shifted. In contrast, no visible changes in bacterial growth and E h were observed in the case of Ni2+. The effects of these ions on proton-potassium ions fluxes through the cell membrane were estimated in the presence and absence of N,N′-dicyclohexylcarbodiimide (DCCD), inhibitor of the FoF1 ATPase. Stronger effect of Mn2+ on H+–K+ exchange was detected in the presence of DCCD that can be explained by a possible complex formation between these substances and its direct influence on membrane transport proteins.

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

Similar content being viewed by others

References

  1. Giller, K., Witter, E., & Mcgrath, S. (1998). Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: A review. Soil Biology & Biochemistry, 30, 1389–1414.

    Article  CAS  Google Scholar 

  2. Audry, S., Schafer, J., Blanc, G., & Jouanneau, J. (2004). Fifty-year sedimentary record of heavy metal pollution (Cd, Zn, Cu, Pb) in the Lot River reservoirs (France). Environmental Pollution, 132, 413–426.

    Article  PubMed  CAS  Google Scholar 

  3. Spain, A. (2003). Implications of microbial heavy metal tolerance in the environment. Reviews Undergraduate Research, 2, 1–6.

    Google Scholar 

  4. Nies, D. (1999). Microbial heavy metal resistance. Applied Microbiology and Biotechnology, 51, 730–750.

    Article  PubMed  CAS  Google Scholar 

  5. Kakinuma, Y. (1998). Inorganic cation transport and energy transduction in Enterococcus hirae and other Streptococci. Microbiology and Molecular Biology Reviews, 62, 1021–1045.

    PubMed  CAS  Google Scholar 

  6. Poladyan, A., Kirakosyan, G., & Trchounian, A. (2006). Growth and proton-potassium exchange in the bacterium Enterococcus hirae: The effect of protonophore and the role of redox potential. Biophysics, 51, 447–451.

    Article  Google Scholar 

  7. Bagramyan, K., Galstyan, A., & Trchounian, A. (2000). Redox potential is a determinant in the Escherichia coli anaerobic growth and survival: Effects of impermeable oxidant. Bioelectrochemistry, 51, 151–156.

    Article  PubMed  CAS  Google Scholar 

  8. Kirakosyan, G., Trchounian, K., Vardanyan, Z., & Trchounian, A. (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.

    Article  PubMed  CAS  Google Scholar 

  9. Vardanyan, Z., & Trchounian, A. (2010). The effects of copper (II) ions on Enterococcus hirae cell growth and the proton-translocating FoF1 ATPase activity. Cell Biochemistry and Biophysics, 57, 19–26.

    Article  PubMed  CAS  Google Scholar 

  10. Vardanyan, Z., & Trchounian, A. (2012). Fe(III) and Fe(II) ions different effects on Enterococcus hirae cell growth and membrane-associated ATPase activity. Biochemical Biophysical Research Communications, 417, 541–545.

    Article  PubMed  CAS  Google Scholar 

  11. Kirakosyan, G., & Trchounian, A. (2007). Redox sensing by Escherichia coli: Effects of copper ions as oxidizers on proton-coupled membrane transport. Bioelectrochemistry, 70, 58–63.

    Article  PubMed  CAS  Google Scholar 

  12. Langenhoff, A., Bronwers-Ceiler, D., Engelberting, J., Quist, J., Wolkenfelt, J., & Zehnder, A. (1997). Microbial reduction of manganese coupled to toluene oxidation. FEMS Microbiology Ecology, 22, 119–127.

    Article  CAS  Google Scholar 

  13. Gaechter, T., Wunderlin, C., Schmidheini, T., & Soliozb, M. (2012). Genome sequence of Enterococcus hirae (Streptococcus faecalis) ATCC9790, a model organism for the study of ion transport, bioenergetics, and copper homeostasis. Journal of Bacteriology, 194, 5126–5127.

    Article  PubMed  CAS  Google Scholar 

  14. Poyart, C., Quesnes, G., & Trieu-Cuot, P. (2000). Sequencing the gene encoding manganese-dependent superoxide dismutase for rapid species identification of enterococci. Journal of Clinical Microbiology, 38, 415–418.

    PubMed  CAS  Google Scholar 

  15. Crowley, J., Traynor, D., & Weatherburn, D. (1999). Enzymes and proteins containing manganese: An overview. In A. Sigel & H. Sigel (Eds.), Manganese and its role in biological processes. Metal ions in biological systems (Vol. 37, pp. 209–257). New York, NY: Marcel Dekker.

    Google Scholar 

  16. Meargeay, M., Nies, D., Schlegel, H., Gerits, J., Charles, P., & Van Gijsegem, F. (1985). Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-borne resistance to heavy metals. Journal of Bacteriology, 162, 328–334.

    Google Scholar 

  17. Dunning, J., Ma, Y., & Marquis, R. (1998). Anaerobic killing of oral Streptococci by reduced, transition metal cations. Applied and Environmental Microbiology, 64, 27–33.

    PubMed  CAS  Google Scholar 

  18. Nakipoğlu, Y., Gümüş, D., SertelSelale, D., & Küçüker, M. (2009). Enterokok suşlarinin yűksek dűzeyde aminoglikozidilere ve ağir matellere karşi in vitro duyarliliklarinin araştirilmasi (In vitro susceptibility of Enterococcus strains to high level aminoglycosides and heavy metals). Mikrobiyolog Bullitin, 43, 545–551. (article in Turkish).

    Google Scholar 

  19. Trchounian, A., & Kobayashi, H. (1998). Relationship of K+-uptaking system with H+-translocating ATPase in Enterococcus hirae, growth at a high or low alkaline pH. Current Microbiology, 36, 114–118.

    Article  PubMed  CAS  Google Scholar 

  20. Mobley, H., Island, M., & Hausinger, R. (1995). Molecular biology of microbial ureases. Microbiology and Molecular Biology Reviews, 59, 451–480.

    CAS  Google Scholar 

  21. Kim, E., Chung, H., Suh, B., Hah, Y., & Roe, J. (1998). Transcriptional and posttranscriptional regulation by nickel of sodN gene encoding nickel-containing superoxide dismutase from Streptomyces coelicolor Müller. Molecular Microbiology, 27, 187–195.

    Article  PubMed  CAS  Google Scholar 

  22. Wu, L., Yu, J., Sun, X., & Li, B. (2009). The effect of nickel (II) ions on the growth and bioaccumulation properties of Escherichia coli. Environmental Progress in Sustainable Energy, 28, 234–239.

    Article  CAS  Google Scholar 

  23. Kirakosyan, G., Bagramyan, K., & Trchounian, A. (2004). Redox sensing by Escherichia coli: Effects of dithiothreitol, a redox reagent reducing disulphides, on bacterial growth. Biochemical and Biophysical Research Communications, 325, 803–806.

    Article  PubMed  CAS  Google Scholar 

  24. Vassilian, A., & Trchounian, A. (2009). Environment oxidation-reduction potential and redox sensing by bacteria. In A. Trchounian (Ed.), Bacterial Membranes (pp. 163–195). Kerala (India): Research Signpost.

    Google Scholar 

  25. Bauda, P., Garsot, P., & Block, J. (1987). Cadmium uptake by Pseudomonas fluorescens cells. Environmental Toxicology and Water, 2, 63–78.

    Article  CAS  Google Scholar 

  26. Breznak, J., & Costilow, R. (1994). Physicochemical factors in growth. In P. Gerhardt, R. Nurrey, W. Wood, et al. (Eds.), Methods for general and molecular bacteriology (pp. 137–155). Washington, DC: ASM Press.

    Google Scholar 

  27. Mnatsakanyan, N., Bagramyan, K., Vassilian, A., Nakamoto, R., & Trchounian, A. (2002). Fo cysteine, bCys21, in the Escherichia coli ATP synthase is involved in regulation of potassium uptake and molecular hydrogen production in anaerobic conditions. Bioscience Reports, 22, 421–430.

    Article  PubMed  CAS  Google Scholar 

  28. Ali, S., & Stokes, J. (1971). Stimulation of heterotrophic and autotrophic growth of Sphaerotilus discophorus by manganeous ions. Anton Van Leewenhouk Journal of Microbiology, 37, 519–528.

    Article  CAS  Google Scholar 

  29. Daly, M. (2009). A new perspective on radiation resistance based on Deinococcus radioduran. Nature Reviews in Microbiology, 7, 237–245.

    Article  CAS  Google Scholar 

  30. Kawano, M., Igarashi, K., & Kakinuma, Y. (2002). Isolation of Enterococcus hirae mutant deficient in low-affinity potassium uptake at alkaline pH. Bioscience, Biotechnology, and Biochemistry, 66, 1597–1600.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Prof. H. Kobayashi for supplying E. hirae strain. The authors thank Dr. V. Ohanyan for helping to edit this manuscript. This study was supported by the Ministry of Education and Science of Armenia (Research Grant #1012-2008 and Basic support).

Conflict of interest

There is no conflict of interest to declare.

Author information

Authors and Affiliations

  1. Department of Biophysics, Faculty of Biology, Yerevan State University, 1 A. Manoukian Str., 0025, Yerevan, Armenia

    Zaruhi Vardanyan

  2. Department of Microbiology and Plants and Microbes Biotechnology, Faculty of Biology, Yerevan State University, 1 A. Manoukian Str., 0025, Yerevan, Armenia

    Armen Trchounian

Authors
  1. Zaruhi Vardanyan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Armen Trchounian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Armen Trchounian.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Vardanyan, Z., Trchounian, A. The Effects of Manganese (II) But Not Nickel (II) Ions on Enterococcus hirae Cell Growth, Redox Potential Decrease, and Proton-Coupled Membrane Transport. Cell Biochem Biophys 67, 1301–1306 (2013). https://doi.org/10.1007/s12013-013-9662-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12013-013-9662-0

Keywords

Search

Navigation