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Bioleaching in brackish waters—effect of chloride ions on the acidophile population and proteomes of model species

  • Genomics, transcriptomics, proteomics
  • Published:
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Abstract

High concentrations of chloride ions inhibit the growth of acidophilic microorganisms used in biomining, a problem particularly relevant to Western Australian and Chilean biomining operations. Despite this, little is known about the mechanisms acidophiles adopt in order to tolerate high chloride ion concentrations. This study aimed to investigate the impact of increasing concentrations of chloride ions on the population dynamics of a mixed culture during pyrite bioleaching and apply proteomics to elucidate how two species from this mixed culture alter their proteomes under chloride stress. A mixture consisting of well-known biomining microorganisms and an enrichment culture obtained from an acidic saline drain were tested for their ability to bioleach pyrite in the presence of 0, 3.5, 7, and 20 g L−1 NaCl. Microorganisms from the enrichment culture were found to out-compete the known biomining microorganisms, independent of the chloride ion concentration. The proteomes of the Gram-positive acidophile Acidimicrobium ferrooxidans and the Gram-negative acidophile Acidithiobacillus caldus grown in the presence or absence of chloride ions were investigated. Analysis of differential expression showed that acidophilic microorganisms adopted several changes in their proteomes in the presence of chloride ions, suggesting the following strategies to combat the NaCl stress: adaptation of the cell membrane, the accumulation of amino acids possibly as a form of osmoprotectant, and the expression of a YceI family protein involved in acid and osmotic-related stress.

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References

  • Alexander B, Leach S, Ingledew WJ (1987) The relationship between chemiosmotic parameters and sensitivity to anions and organic acids in the acidophile Thiobacillus ferrooxidans. J Gen Microbiol 133:1171–1179

    CAS  Google Scholar 

  • Bendtsen JD, Nielsen H, von Heijne G, Brunak S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340:783–795

    Article  Google Scholar 

  • Bergler H, Wallner P, Ebeling A, Leitinger B, Fuchsbichler S, Aschauer H, Kollenz G, Hogenauer G, Turnowsky F (1994) Protein EnvM is the NADH-dependent enoyl-ACP reductase (FabI) of Escherichia coli. J Biol Chem 269:5493–5496

    CAS  Google Scholar 

  • Dopson M, Lindström EB (1999) Potential role of Thiobacillus caldus in arsenopyrite bioleaching. Appl Environ Microbiol 65:36–40

    CAS  Google Scholar 

  • Dopson M, Baker-Austin C, Hind A, Bowman JP, Bond PL (2004) Characterization of Ferroplasma isolates and Ferroplasma acidarmanus sp. nov., extreme acidophiles from acid mine drainage and industrial bioleaching environments. Appl Environ Microbiol 70:2079–2088

    Article  CAS  Google Scholar 

  • Dopson M, Halinen A-K, Rahunen N, Boström D, Sundkvist J-E, Riekkola-Vanhanen M, Kaksonen AH, Puhakka JA (2008) Silicate mineral dissolution during heap bioleaching. Biotechnol Bioeng 99:811–820

    Article  CAS  Google Scholar 

  • Gahan CS, Sundkvist J-E, Sandström Å (2009) A study on the toxic effects of chloride on the biooxidation efficiency of pyrite. J Hazard Mat 172:1273–1281

    Article  CAS  Google Scholar 

  • Gahan CS, Sundkvist J-E, Dopson M, Sandström Å (2010) Effect chloride ferrous iron oxidation Leptospirillum ferriphilum-dominated chemostat culture. Biotechnol Bioeng 106:422–431

    CAS  Google Scholar 

  • Garwin JL, Klages AL, Cronan JE Jr (1980) Structural, enzymatic, and genetic studies of beta-ketoacyl-acyl carrier protein synthases I and II of Escherichia coli. J Biol Chem 255:11949–11956

    CAS  Google Scholar 

  • Ghauri MA, Okibe N, Johnson DB (2007) Attachment of acidophilic bacteria to solid surfaces: the significance of species and strain variations. Hydrometallurgy 85:72–80

    Article  CAS  Google Scholar 

  • He Z, Zhou A, Baidoo E, He Q, Joachimiak MP, Benke P, Phan R, Mukhopadhyay A, Hemme CL, Huang K, Alm EJ, Fields MW, Wall J, Stahl D, Hazen TC, Keasling JD, Arkin AP, Zhou J (2010) Global transcriptional, physiological, and metabolite analyses of the responses of Desulfovibrio vulgaris hildenborough to salt adaptation. Appl Environ Microbiol 76:1574–1586

    Article  CAS  Google Scholar 

  • Huber H, Stetter KO (1989) Thiobacillus prosperus sp. nov., represents a new group of halotolerant metal-mobilizing bacteria isolated from a marine geothermal field. Arch Microbiol 151:479–485

    Article  CAS  Google Scholar 

  • Johnson DB, Hallberg KB (2009) Carbon, iron and sulfur metabolism in acidophilic micro-organisms. Adv Microb Physiol 54:201–255

    CAS  Google Scholar 

  • Kamimura K, Higashino E, Kanao T, Sugio T (2005) Effects of inhibitors and NaCl on the oxidation of reduced inorganic sulfur compounds by a marine acidophilic, sulfur-oxidizing bacterium, Acidithiobacillus thiooxidans strain SH. Extremophiles 9:45–51

    Article  CAS  Google Scholar 

  • Kinnunen PHM, Puhakka JA (2004) Chloride-promoted leaching of chalcopyrite concentrate by biologically-produced ferric sulfate. J Chem Tech Biotechnol 79:830–834

    Article  CAS  Google Scholar 

  • Lane DJ (1985) 16S/23S sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematic. Wiley, New York, pp 115–176

    Google Scholar 

  • Lloubes R, Cascales E, Walburger A, Bouveret E, Lazdunski C, Bernadac A, Journet L (2001) The Tol-Pal proteins of the Escherichia coli cell envelope: an energized system required for outer membrane integrity? Res Microbiol 152:523–529

    Article  CAS  Google Scholar 

  • Mangold S, Valdes J, Holmes DS, Dopson M (2011) Sulfur metabolism in the extreme acidophile Acidithiobacillus caldus. Front Microbio 2:17. doi:10.3389/fmicb.2011.00017

    Article  Google Scholar 

  • Mutch LA, Watling H, Watkin ELJ (2010) Microbial population dynamics of inoculated low-grade chalcopyrite bioleaching columns. Hydrometallurgy 104:391–398

    Article  CAS  Google Scholar 

  • Nicolle JLC, Simmons S, Bathe S, Norris PR (2009) Ferrous iron oxidation and rusticyanin in halotolerant, acidophilic 'Thiobacillus prosperus'. Microbiology 155:1302–1309

    Article  CAS  Google Scholar 

  • Noriko H, Takaho T, Yukiko D-H, Hiroshi H, Jeremy RHT, Sam-Yong P, Seiki K, Mikako S, Shigeyuki Y (2005) Crystal structure of a novel polyisoprenoid binding protein from Thermus thermophilus HB8. Protein Sci 14:1004–1010

    Article  Google Scholar 

  • Norris PR, Nicolle JLC, Calvo-Bado L, Angelatou V (2009) Pyrite oxidation by halotolerant, thermotolerant bacteria. Adv Mat Res 71–73:75–78

    Article  Google Scholar 

  • Orphan VJ, Taylor LT, Hafenbradl D, Delong EF (2000) Culture-dependent and culture-independent characterization of microbial assemblages associated with high-temperature petroleum reservoirs. Appl Environ Microbiol 66:700–711

    Article  CAS  Google Scholar 

  • Potrykus J, Rao Jonna V, Dopson M (2011) Iron homeostasis and responses to iron limitation in extreme acidophiles from the Ferroplasma genus. Proteomics 11:52–63

    Article  CAS  Google Scholar 

  • Rohwerder T, Gehrke T, Kinzler K, Sand W (2003) Bioleaching review part A. Progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation. Appl Microbiol Biotechnol 63:239–248

    Article  CAS  Google Scholar 

  • Romantsov T, Guan ZQ, Wood JM (2009) Cardiolipin and the osmotic stress responses of bacteria. Biochim Biophys Acta-Biomembr 1788:2092–2100

    Article  CAS  Google Scholar 

  • Romero J, Yanez C, Vasquez M, Moore ER, Espejo RT (2003) Characterization and identification of an iron-oxidizing, Leptospirillum-like bacterium, present in the high sulfate leaching solution of a commercial bioleaching plant. Res Microbiol 154:353–359

    Article  CAS  Google Scholar 

  • Seaver LC, Imlay JA (2001) Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183:7173–7181

    Article  CAS  Google Scholar 

  • Shiers DW, Blight KR, Ralph DE (2005) Sodium sulphate and sodium chloride effects on batch culture of iron oxidising bacteria. Hydrometallurgy 80:75–82

    Article  CAS  Google Scholar 

  • Sleator RD, Hill C (2002) Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol Rev 26:49–71

    Article  CAS  Google Scholar 

  • Slonczewski JL, Fujisawa M, Dopson M, Krulwich TA (2009) Cytoplasmic pH measurement and homeostasis in bacteria and archaea. Adv Microb Physiol 55:1–79

    Article  Google Scholar 

  • Soda K (1987) Microbial sulfur amino acids: an overview. Methods Enzymol 143:453–459

    Article  CAS  Google Scholar 

  • Stolyar S, He Q, Joachimiak MP, He Z, Yang ZK, Borglin SE, Joyner DC, Huang K, Alm E, Hazen TC, Zhou J, Wall JD, Arkin AP, Stahl DA (2007) Response of Desulfovibrio vulgaris to alkaline stress. J Bacteriol 189:8944–8952

    Article  CAS  Google Scholar 

  • Suzuki I, Lee D, Mackay B, Harahuc L, Oh JK (1999) Effect of various ions, pH, and osmotic pressure on oxidation of elemental sulfur by Thiobacillus thiooxidans. Appl Environ Microbiol 65:5163–5168

    CAS  Google Scholar 

  • Valdes J, Quatrini R, Hallberg K, Dopson M, Valenzuela PD, Holmes DS (2009) Draft genome sequence of the extremely acidophilic bacterium Acidithiobacillus caldus ATCC 51756 reveals metabolic versatility in the genus Acidithiobacillus. J Bacteriol 191:5877–5878

    Article  CAS  Google Scholar 

  • van den Ent F, Amos LA, Lowe J (2001) Prokaryotic origin of the actin cytoskeleton. Nature 413:39–44

    Article  Google Scholar 

  • Weber A, Kogl SA, Jung K (2006) Time-dependent proteome alterations under osmotic stress during aerobic and anaerobic growth in Escherichia coli. J Bacteriol 188(20):7165–7175

    Article  CAS  Google Scholar 

  • Ying-Ying C, John EC (1999) Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol Microbiol 33:249–259

    Article  Google Scholar 

  • Zammit CM, Mutch LA, Watling HR, Watkin ELJ (2008) Evaluation of quantitative real-time polymerase chain reaction for enumeration of biomining microorganisms in culture. Hydrometallurgy 94:185–189

    Article  CAS  Google Scholar 

  • Zammit CM, Mutch LA, Watling H, Watkin E (2009a) The characterization of salt tolerance in biomining microorganisms and the search for novel salt tolerant strains. Adv Mat Res 71–73:283–286

    Article  Google Scholar 

  • Zammit CM, Mutch LA, Watling H, Watkin E (2009b) Nucleic acid extraction from biomining microorganisms. Adv Mat Res 71–73:159–162

    Article  Google Scholar 

Download references

Acknowledgements

The authors express their gratitude for financial support from the Swedish Research Council (Vetenskapsrådet contract number 621-2007-3537) to MD. CZ, LM, HW, and EW would like to thank the support of the Parker CRC for Integrated Hydrometallurgy Solutions (established and supported under the Australian Government’s Cooperative Research Centres Program). Additionally, CZ gratefully acknowledges the financial support from the Minerals and Energy Research Institute of Western Australia and Curtin University.

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Correspondence to Elizabeth L. J. Watkin.

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Zammit, C.M., Mangold, S., rao Jonna, V. et al. Bioleaching in brackish waters—effect of chloride ions on the acidophile population and proteomes of model species. Appl Microbiol Biotechnol 93, 319–329 (2012). https://doi.org/10.1007/s00253-011-3731-3

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  • DOI: https://doi.org/10.1007/s00253-011-3731-3

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