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Water, Air, & Soil Pollution

, 229:395 | Cite as

Effect of the Simultaneous Action of Zinc and Chromium on Arthrobacter spp.

  • Nino AsatianiEmail author
  • Tamar Kartvelishvili
  • Nelly Sapojnikova
  • Marina Abuladze
  • Lali Asanishvili
  • Mariam Osepashvili
Article
  • 94 Downloads

Abstract

Bacteria are regarded as the most effective in the detoxification of heavy metals, being environmental compatible. Metalloresistant bacteria are usually found in nature in highly contaminated environment where they interact with a combination of several toxic metals. For the present research, Arthrobacter oxydans and Arthrobacter globiformis have been isolated from the soil samples of the most polluted regions of Georgia, rich with manganese and iron, and contain co-produced toxic metals such as Cr, V, Zn, Ni, Pb, and Mo. We have studied the effects of the metals with different valence/charge on the metalloresistant Arthrobacter spp., the divalent cation—Zn(II) and the hexavalent anion—Cr(VI). The permanent presence of a nontoxic concentration of zinc alone or zinc together with the subtoxic concentration of chromium at the growth of A. oxydans and A. globiformis as batch culture causes the activation of the zinc primary uptake system transporters from the ZIP family (Zrt1). Chromium does not affect the process. The studied Arthrobacter spp. differ by the character of the activation of the antioxidant defense system. Chromium and zinc concomitant action causes the strongest oxidative stress in the case of A. globiformis that is demonstrated by the increased activity of superoxide dismutase (SOD) and catalase. In the case of A. oxydans, the zinc separate action, and the joint action of zinc and chromium decreases the activity of SOD and catalase. The antioxidant system is active in A. globiformis at the prolonged action of metals (96 h), whereas the cells of A. oxyidans activate the other defense mechanisms to survive.

Keywords

Metal toxicity Arthrobacter species Catalase Superoxide dismutase 

Notes

Funding Information

This work was supported by grants (#2016-39) from the Shota Rustaveli National Science Foundation (SRNSF) and (#6304) from the Science and Technology Center in Ukraine (STCU).

References

  1. Ackerley, D. F., Barak, Y., Lynch, S. V., Curtin, J., & Matin, A. (2006). Effect of chromate stress on Escherichia coli K-12. Journal of Bacteriolology, 188, 3371–3381.CrossRefGoogle Scholar
  2. Akshata, J. N., Udayashankara, T. H., & Lokesh, K. S. (2014). Review on bioremediation of heavy metals with microbial isolates and amendments on soil residue. International Journal of Science and Research, 3, 118–123.Google Scholar
  3. Ayangbenro, A. S., & Babalola, O. O. (2017). A new strategy for heavy metal polluted environments: a review of microbial biosorbents. International Journal of Environmental Research and Public Health.  https://doi.org/10.3390/ijerph14010094.
  4. Beard, S. J., Hughes, M. N., & Poole, R. K. (1995). Inhibition of the cytochrome M-terminated NADH oxidase system in Escherichia coli K-12 by divalent metal cations. FEMS Microbiology Letters, 131(2), 205–210.CrossRefGoogle Scholar
  5. Beers, R. F., & Sizer, J. W. (1952). A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. The Journal of Biological Chemistry, 195, 133–140.Google Scholar
  6. Brocklehurst, K. R., Megit, S. J., & Morby, A. P. (2003). Characterization of CadR from Pseudomonas aeruginosa: a Cd(II)-responsive MerR homologue. Biochemical and Biophysical Research Communications, 308, 234–239.CrossRefGoogle Scholar
  7. Brown, S. D., Thompson, M. R., Verberkmoes, N. C., Chourey, K., Shah, M., Zhou, J. Z., Hettich, R. L., & Thompson, D. K. (2006). Molecular dynamics of the Shewanella oneidensis response to chromate stress. Molecular & Cellular Proteomics, 5, 1054–1071.CrossRefGoogle Scholar
  8. Camargo, F., Bento, F., Okeke, B., & Frankenberger, W. T. (2003). Hexavalent chromium reduction by an actinomycete, Arthrobacter crystallopoietes ES 32. Biological Trace Element Research, 97, 183–194.CrossRefGoogle Scholar
  9. Cervantes, C., & Campos-Garcıa, J. (2007). Reduction and efflux of chromate by bacteria. In D. H. Nies & S. Silver (Eds.), Molecular microbiology of heavy metals (pp. 407–419). New York: Springer.CrossRefGoogle Scholar
  10. Daud, M. K., Mei, L., Variath, M. T., Ali, S., Li, C., Rafiq, M. T., & Zhu, S. J. (2014). Chromium (VI) uptake and tolerance potential in cotton cultivars: effect on their root physiology, ultramorphology, and oxidative metabolism. BioMed Research International.  https://doi.org/10.1155/2014/975946.
  11. Eide, D. J. (2006). Zinc transporters and the cellular trafficking of zinc. Biochimica et Biophysica Acta (Molecular Cell Research), 1763, 711–722.CrossRefGoogle Scholar
  12. Eng, B. H., Guerinot, M. L., Eide, D., & Saier, M. H., Jr. (1998). Sequence analyses and phylogenetic characterization of the ZIP family of metal ion transport proteins. Journal of Membrane Biology, 166, 1–7.CrossRefGoogle Scholar
  13. Ercal, N., Gurer-Orhan, H., & Aykin-Burns, N. (2001). Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Current Topics in Medical Chemistry, 1, 529–539.CrossRefGoogle Scholar
  14. Girard, B., & Snell, E. (1983). Biochemical factors. In P. Gerhardt (Ed.), Manual of methods for general bacteriology (pp. 198–276). Moscow: Mir.Google Scholar
  15. Gitan, R. S., Luo, H., Rodgers, J., Broderius, M., & Eide, D. (1998). Zinc-induced inactivation of the yeast ZRT1 zinc transporter occurs through endocytosis and vacuolar degradation. The Journal of Biological Chemistry, 273, 28617–28624.CrossRefGoogle Scholar
  16. Guerinot, M. L. (2000). The ZIP family of metal transporters. Biochimica et Biophysica Acta, 1465, 190–198.CrossRefGoogle Scholar
  17. Gupta, A., Joia, J., Sood, A., Sood, R., Sidhu, C., & Kaur, G. (2016). Microbes as potential tool for remediation of heavy metals: a review. Journal of Microbial & Biochemical Technology, 8(4), 364–372.CrossRefGoogle Scholar
  18. Hynninen, A. (2010). Zinc, cadmium and lead resistance mechanisms in bacteria and their contribution to biosensing. Dissertation, University of Helsinki.Google Scholar
  19. Joutey, N. T., Bahafid, W., Sayel, H., Ananou, S., & El Ghachtouli, N. (2013). Hexavalent chromium removal by a novel Serratia proteamaculans isolated from the bank of Sebou river (Morocco). Environmental Science and Pollution Research, 21(4), 3060–3072.CrossRefGoogle Scholar
  20. Joutey, N. T., Sayel, H., Bahafid, W., & El Ghachtouli, N. (2015). Mechanisms of hexavalent chromium resistance and removal by microorganisms. Reviews of Environmental Contamination and Toxicology, 233, 45–69.Google Scholar
  21. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680–685.CrossRefGoogle Scholar
  22. Li, S., Zhou, X., Huang, Y., Zhu, L., Zhang, S., Zhao, Y., Guo, J., Chen, J., & Chen, R. (2013) Identification and characterization of the zinc-regulated transporters, iron-regulated transporter-like protein (ZIP) gene family in maize. BMC Plant Biology.  https://doi.org/10.1186/1471-2229-13-114.
  23. McCall, K. A., Huang, C., & Fierke, C. A. (2000). Function and mechanism of zinc metalloenzymes. The Journal of Nutrition.  https://doi.org/10.1093/jn/130.5.1437S.
  24. Ngwenya, N., & Chirwa, E. M. N. (2011). Biological removal of cationic fission products from nuclear wastewater. Water Science and Technology, 63, 124–128.CrossRefGoogle Scholar
  25. Opperman, D. J., & van Heerden, E. (2008). A membrane-associated protein with Cr(VI)-reducing activity from Thermus scotoductus SA-01. FEMS Microbiology Letters, 280, 210–218.CrossRefGoogle Scholar
  26. Scheublin, T. R., & Leveau, J. H. J. (2013). Isolation of Arthrobacter species from the phylloshere and demonstration of their epiphytic fitness. MicrobiologyOpen, 2, 205–213.CrossRefGoogle Scholar
  27. Schutzendubel, A., & Polle, A. (2002). Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. Journal of Experimental Botany, 53(372), 1351–1365.Google Scholar
  28. Steinman, H. M. (1985). Bacteriocuprein superoxide dismutases in pseudomonads. Journal of Bacteriology, 162, 1255–1260.Google Scholar
  29. Stoyanov, J. V., & Brown, N. L. (2003). The Escherichia coli copper-responsive copA promoter is activated by gold. The Journal of Biological Chemistry, 278, 1407–1410.CrossRefGoogle Scholar
  30. Stoyanov, J. V., Hobman, J. L., & Brown, N. L. (2001). CueR (YbbI) of Escherichia coli is a MerR family regulator controlling expression of the copper exporter CopA. Molecular Microbiology, 39, 502–511.CrossRefGoogle Scholar
  31. Tang, M., Chen, J., Sun, Y., Tong, Y., & Liu, Y. (2014). The absorption and scavenging ability of a bacillus in heavy metal contaminated soils (Pb, Zn and Cr). African Journal of Environmental Science and Technology, 8, 476–481.CrossRefGoogle Scholar
  32. Tchounwou, P. B., Yedjou, C. G., Patlolla, A. K., & Sutton, D. J. (2012). Heavy metals toxicity and the environment. In A. Luch (Ed.), Molecular, clinical and environmental toxicology, volume 3: Environmental toxicology (pp. 133–164). New York: Springer.CrossRefGoogle Scholar
  33. Tsibakhashvili, N. Y., Kalabegishvili, T. L., Rcheulishvili, A. N., Ginturi, E. N., Lomidze, L. G., Gvarjaladze, D. N., & Rcheulishvili, O. A. (2011). Effect of Zn(II) on the reduction and accumulation of Cr(VI) by Arthrobacter species. Journal of Industrial Microbiology and Biotechnology, 38(11), 1803–1808.CrossRefGoogle Scholar
  34. Valko, M., Jomova, K., Rhodes, C. J., Kuca, K., & Musilek, K. (2016). Redox- and non-redox-metal-induced formation of free radicals and their role in human disease. Archives of Toxicology, 90(1), 1–37.CrossRefGoogle Scholar
  35. Viti, C., Marchi, E., Decorosi, F., & Giovannetti, L. (2014). Molecular mechanisms of Cr(VI) resistance in bacteria and fungi. FEMS Microbiology Reviews, 38, 633–659.CrossRefGoogle Scholar
  36. Westerberg, K., Elvang, A. M., Stackebrandt, E., & Jansson, J. K. (2000). Arthrobacter chlorophenolicus sp. nov., a new species capable of degrading high concentrations of 4-chlorophenol. International Journal of Systematic and Evolutionary Microbiology, 50(6), 2083–2092.CrossRefGoogle Scholar
  37. Yoon, K. P., Misra, T. K., & Silver, S. (1991). Regulation of the cadA cadmium resistance determinant of Staphylococcus aureus plasmid pI258. Journal of Bacteriology, 173, 7643–7649.CrossRefGoogle Scholar
  38. Zhao, H., & Eide, D. (1996). The yeast ZRT1 gene encodes the zinc transporter protein of a high-affinity uptake system induced by zinc limitation. Proceedings of the National Academy of Sciences of the United States of America, 93, 2454–2458.CrossRefGoogle Scholar
  39. Zhao, H., & Eide, D. J. (1997). Zap1p, a metalloregulatory protein involved in zinc-responsive transcriptional regulation in Saccharomyces cerevisiae. Molecular and Cellular Biology, 17(9), 5044–5052.CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Andronikashvili Institute of PhysicsI. Javakhishvili Tbilisi State UniversityTbilisiGeorgia
  2. 2.Technological Institute of GeorgiaTbilisiGeorgia

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