Skip to main content
SpringerLink
Log in

Effect of Light Metal Ions and Chloride on Activity of Moderately Thermophilic Acidophilic Iron-Oxidizing Microorganisms

  • EXPERIMENTAL ARTICLES
  • Published:
Microbiology Aims and scope Submit manuscript

Abstract—

The effect of sodium, potassium, magnesium, and aluminum ions, as well as of the chloride ion on the growth and ferrous iron oxidation by moderately thermophilic acidophilic iron-oxidizing microorganisms was studied. Strains of the microorganisms predominant in biohydrometallurgical processes (bacteria of genus Sulfobacillus and archaea of the genus Acidiplasma) were the subjects of the study. Ability of the studied strains to grow and oxidize ferrous iron in the media containing different concentrations of sodium, potassium, magnesium, and aluminum (up to 1000 mM) was determined. The experiments were conducted in two variants, in which the studied metals were added to the medium as sulfates and chlorides, respectively. It was revealed that inhibitory effects of the studied metals on the studied strains differed insignificantly and that high concentrations all studied salts inhibited growth and ferrous iron oxidation. The studied Acidiplasma strains were shown to be more tolerant to the cations than the Sulfobacillus strains. The inhibitory effect of chloride ion on the studied strains was the most significant, which were probably adapted to the habitats characterized by high concentrations of metals and sulfates, but not of chloride ions. The mechanisms of action of the studied light metal ions on growth of iron-oxidizing acidophilic microorganisms are 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

  1. Bakker E.P., The role of alkali-cation transport in energy coupling of neutrophilic and acidophilic bacteria: an assessment of methods and concepts, FEMS Microbiol. Lett., 1990, vol. 75, pp. 319–334.

    Article  CAS  Google Scholar 

  2. Bevilaqua, D., Lahti, H., Suegama, P.H., Garcia, O., Benedetti, A.V., Puhakka, J.A., and Tuovinen, O.H., Effect of Na-chloride on the bioleaching of a chalcopyrite concentrate in shake flasks and stirred tank bioreactors, Hydrometallurgy, 2013, vol. 138, pp. 1–13.

    Article  CAS  Google Scholar 

  3. Bhatti, T.M., Vuorinen, A., and Tuovinen, O.H., Dissolution of non-sulfide phases during the chemical and bacterial leaching of a sulfidic black schist, Hydrometallurgy, 2012, vol. 117–118, pp. 32–35.

    Article  CAS  Google Scholar 

  4. Bond, P.L., Druschel, G.K., and Banfield, J.F., Comparison of acid mine drainage microbial communities in physically and geochemically distinct ecosystems, Appl. Environ. Microbiol., 2000, vol. 66, pp. 4962–4971.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Bobadilla-Fazzini, R.A., Cortes, M.P., Maaas, A., and Parada, P. Sulfobacillus thermosulfidooxidans strain Cutipay enhances chalcopyrite bioleaching under moderate thermophilic conditions in the presence of chloride ion, AMB Express, 2014, vol. 4, p. 84.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Cardenas, J.-P., Ortiz, R., Norris, P.R., Watkin, E., and Holmes, D.S., Reclassification of ‘Thiobacillus prosperus’ (Huber and Stetter 1989) as Acidihalobacter prosperus gen. nov., sp. nov., a member of the family Ectothiorhodospiraceae, Int. J. Syst. Evol. Microbiol., vol. 65, pp. 3641–3644.

  7. Davis-Belmar, C.S., Cautivo, D., Rautenbach, G., and Demergasso, C.S., Biologically assisted copper secondary sulfide ore leaching in the presence of chloride, Adv. Mater. Res., 2013, vol. 825, pp. 292–295.

    Article  CAS  Google Scholar 

  8. Davis-Belmar, C.S., Nicolle, J.L.C., and Norris, P.R., Ferrous iron oxidation and leaching of copper ore with halotolerant bacteria in ore columns, Hydrometallurgy, 2008, vol. 94. nos. 1–4, pp. 144–147.

  9. Dopson, M., Baker-Austin, C., Koppineedi, P.R., and Bond, P.L., Growth in sulfidic mineral environments: metal resistance mechanisms in acidophilic micro-organisms, Microbiology (UK), 2003, vol. 149, pp. 1959–1970.

    Article  PubMed  CAS  Google Scholar 

  10. Dopson, M. and Holmes, D.S., Metal resistance in acidophilic microorganisms and its significance for biotechnologies, Appl. Microbiol. Biotechnol., 2014, vol. 98, pp. 8133–8144.

    Article  PubMed  CAS  Google Scholar 

  11. Dopson, M., Holmes, D.S., Lazcano, M., McCredden, T.J., Bryan, C.G., Mulroney, K.T., Steuart, R., Jackaman, C., and Watkin, E.L., Multiple osmotic stress responses in Acidihalobacter prosperus result in tolerance to chloride ions, Front. Microbiol., 2017, vol. 7. Article 2132.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Epstein, W., The roles and regulation of potassium in bacteria, Prog. Nucl. Acid Res Mol. Biol., vol. 75., Moldave, K., Ed., Oxford: Academic, 2003, pp. 293–320.

    Google Scholar 

  13. Golyshina, O.V., Pivovarova, T.A., Karavaiko, G.I., Kondrat’eva, T.F., Moore, E.R., Abraham, W.R., Lünsdorf, H., Timmis, K.N., Yakimov, M.M., and Golyshin, P.N., Ferroplasma acidiphilum gen. nov., sp. nov., an acidophilic, autotrophic, ferrous-iron-oxidizing, cell-wall-lacking, mesophilic member of the Ferroplasmaceae fam. nov., comprising a distinct lineage of the Archaea, Int. J. Syst. Evol. Microbiol., 2000, vol. 50, pp. 997–1006.

  14. Golyshina, O.V. and Timmis, K.N., Ferroplasma and relatives, recently discovered cell wall-lacking archaea making a living in extremely acid, heavy metal-rich environments, Environ. Microbiol., 2005, vol. 7, pp. 1277–1288.

    Article  PubMed  CAS  Google Scholar 

  15. Golyshina, O.V., Yakimov, M.M., Lünsdorf, H., Ferrer, M., Nimtz, M., Timmis, K.N., Wray, V., Tindall, B.J., and Golyshin, P.N., Acidiplasma aeolicum gen. nov., sp. nov., a euryarchaeon of the family Ferroplasmaceae isolated from a hydrothermal pool, and transfer of Ferroplasma cupricumulans to Acidiplasma cupricumulans comb. nov., Int. J. Syst. Evol. Microbiol., 2009, vol. 59, pp. 2815–2824.

    Article  PubMed  CAS  Google Scholar 

  16. Groisman, E.A., Hollands, K., Kriner, M.A., Lee, E.J., Park, S.Y., and Pontes, M.H., Bacterial Mg2+ homeostasis, transport, and virulence, Annu. Rev. Genet., 2013, vol. 47, pp. 625–646.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Hallberg, K.B., Hedrich, S., and Johnson, D.B. Acidiferrobacter thiooxydans, gen. nov. sp. nov.; an acidophilic, thermo-tolerant, facultatively anaerobic iron- and sulfur-oxidizer of the family Ectothiorhodospiraceae, Extremophiles, 2011, vol. 15, pp. 271–279.

    Article  PubMed  CAS  Google Scholar 

  18. Hawkes, R.B., Franzmann, P.D., O’Hara, G., and Plumb, J.J., Ferroplasma cupricumulans sp. nov., a novel moderately thermophilic, acidophilic archaea isolated from an industrial-scale chalcocite bioleach heap, Extremophiles, 2006, vol. 10, pp. 525–530.

    Article  PubMed  CAS  Google Scholar 

  19. Huber, H. and Stetter, K.O., Thiobacillus prosperus sp. nov., represents a new group of halotolerant metal-mobilizing bacteria isolated from a marine geothermal field, Arch. Microbiol, vol. 151, pp. 479–485.

  20. Johnson, D.B., Hallberg, K.B., and Hedrich, S., Uncovering a microbial enigma: isolation and characterization of the streamer-generating, iron-oxidizing, acidophilic bacterium “Ferrovum myxofaciens,” Appl. Environ. Microbiol., 2014, vol. 80, pp. 672–680.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Keeling, S.E, Davies, K.L., Palmer, M.-L., Town-send, D.E., Watkin, E., Johnson, J.A., and Watling, H.R., Utilization of native microbes from a spent chalcocite test heap, Hydrometallurgy, 2006, vol. 83, pp. 124–131.

    Article  CAS  Google Scholar 

  22. Kondrat’eva, T.F., Bulaev, A.G., and Muravyov, M.I., Mikrooganizmy v biotecknologiyakh pererabotki sul’fidnykh rud (Microorganisms in Biotechnologies of Sulfide Ores Processing), Moscow: Nauka, 2015.

    Google Scholar 

  23. Korehi, H., Blöthe, M., Sitnikova, M.A., Dold, B., and Schippers, A., Metal mobilization by iron- and sulfur-oxidizing bacteria in a multiple extreme mine tailings in the Atacama Desert, Chile, Environ. Sci. Technol., 2013, vol. 47, pp. 2189−2196.

    Article  PubMed  CAS  Google Scholar 

  24. Muravyov, M.I. and Bulaev, A.G., Two-step oxidation of a refractory gold-bearing sulfidic concentrate and the effect of organic nutrients on its biooxidation, Min. Eng., 2013, vol. 45, pp. 108–114.

    Article  CAS  Google Scholar 

  25. Pina, R.G. and Cervantes, C., Microbial interactions with aluminium, Biometals, 1996, vol. 9, pp. 311–316.

    Google Scholar 

  26. Pakostova, E., Grail, B.M., and Johnson, D.B., Column bioleaching of a saline, calcareous copper sulfide ore, Solid State Phenom., 2017, vol. 262, pp. 7–11.

    Article  Google Scholar 

  27. Rea, S.M., McSweeney, N.J., Degens, B.P., Morrisa, C., Siebert, H.M., and Kaksonen, A.H., Salt-tolerant microorganisms potentially useful for bioleaching operations where fresh water is scarce, Miner. Engin., 2015, vol. 75, pp. 126–132.

    Article  CAS  Google Scholar 

  28. Reznikov, A.A., Mulikovskaya, E.P., and Sokolov, I.Yu., Metody analiza pripornykh vod (Methods for Analysis of Natural Waters), Moscow: Nedra, 1970.

    Google Scholar 

  29. Schippers, A., Microorganisms involved in bioleaching and nucleic acid-based molecular methods for their identification and quantification, in Microbial Processing of Metal Sulfides, Donati, E.R. and Sand, W., Eds, New York: Springer, 2007, pp. 3–33.

    Google Scholar 

  30. Simmons, S. and Norris, P.R., Acidophiles of saline water at thermal vents of Vulcano, Italy, Extremophiles, 2002, vol. 6, pp. 201–207.

    Article  PubMed  CAS  Google Scholar 

  31. Suzuki, I., Lee, D., Mackay, B., Harahuc, L., and Oh, J.K., Effect of various ions, pH, and osmotic pressure on oxidation of elemental sulfur by Thiobacillus thiooxidans, Appl. Environ. Microbiol., 1999, vol. 65, pp. 5163–5168.

    PubMed  PubMed Central  CAS  Google Scholar 

  32. van Hille, R.P., van Wyk, N., Froneman, T., and Harrison, S.T.L., Dynamic evolution of the microbial community in BIOX leaching tanks, Adv. Mater. Res., 2013, vol. 825, pp. 331–334.

    Article  Google Scholar 

  33. Wang, Y., Su, L., Zhang, L., Zeng, W., Wu, J., Wan, L., Qiu, G., and Chen, X.Z.H., Bioleaching of chalcopyrite by defined mixed moderately thermophilic consortium including a marine acidophilic halotolerant bacterium, Bioresour. Technol., 2012, vol. 121, pp. 348–354.

    Article  PubMed  CAS  Google Scholar 

  34. Watling, H.R., Watkin, E.J.L., and Ralph, D.E., The resilience and versatility of acidophiles that contribute to the bio-assisted extraction of metals from mineral sulfides, Environ. Technol., 2010, vol. 31, pp. 915–933.

    Article  CAS  Google Scholar 

  35. Watling, H.R., Chalcopyrite hydrometallurgy at atmospheric pressure: Review of acidic chloride process options, Hydrometallurgy. 2014, vol. 146, pp. 96–110.

    Article  CAS  Google Scholar 

  36. Zammit, C.M., Mangold, S., Jonna, V., Mutch, L.A., Watling, H.R., Dopson, M., and Watkin, E.L. Bioleaching in brackish waters—effect of chloride ions on the acidophile population and proteomes of model species, Appl. Microbiol. Biotechnol., 2012, vol. 93, pp. 319–329.

    Article  PubMed  CAS  Google Scholar 

  37. Zammit, C.M. and Watkin, E.L.J., Adaptation to extreme acidity and osmotic stress, in Acidophiles. Life in Extremely Acidic Environments, Quatrini, R. and Johnson, D.B., Eds., Norfolk: Caister Academic, 2016, pp. 49–62.

  38. Zhou, H., Zhang, R., Hu, P., Zeng, W., Xie, Y., Wu, C., and Qiu, G., Isolation and characterization of Ferroplasma thermophilum sp. nov., a novel extremely acidophilic, moderately thermophilic archaeon and its role in bioleaching of chalcopyrite, J. Appl. Microbiol., 2008, vol. 105, pp. 591–601.

    Article  PubMed  CAS  Google Scholar 

Download references

ACKNOWLEDGMENTS

The work was supported by the Russian Foundation for Basic Research, project no. 16-34-60053 mol_a_dk.

Author information

Authors and Affiliations

  1. Biological Faculty, Lomonosov Moscow State University, Moscow, Russia

    A. G. Bulaev

  2. Winogradsky Institute of Microbiology, Research Center of Biotechnology of the Russian Academy of Sciences, Moscow, Russia

    A. G. Bulaev & A. N. Chernyshov

Authors
  1. A. G. Bulaev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. N. Chernyshov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. G. Bulaev.

Additional information

Translated by A. Bulaev

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bulaev, A.G., Chernyshov, A.N. Effect of Light Metal Ions and Chloride on Activity of Moderately Thermophilic Acidophilic Iron-Oxidizing Microorganisms. Microbiology 87, 621–634 (2018). https://doi.org/10.1134/S0026261718050053

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0026261718050053

Keywords:

Search

Navigation