1887

Abstract

It has been postulated that inorganic polyphosphate (polyP) and transport of metal–phosphate complexes could participate in heavy metal tolerance in some bacteria. To study if such a system exists in archaea, the presence of polyP was determined by the electron energy loss spectroscopy (EELS) procedure and quantified by using specific enzymic methods in , and . All three micro-organisms synthesized polyP during growth, but only greatly accumulated polyP granules. The differences in the capacity to accumulate polyP between these archaea may reflect adaptive responses to their natural environment. Thus, could grow in and tolerate up to 200 mM copper sulfate, with a concomitant decrease in its polyP levels with increasing copper concentrations. On the other hand, could not grow in or tolerate more than 1–5 mM copper sulfate, most likely due to its low levels of polyP. Shifting cells to copper sulfate concentrations up to 100 mM led to a rapid increase in their exopolyphosphatase (PPX) activity which was concomitant in time with a decrease in their polyP levels and a stimulation of phosphate efflux. Furthermore, copper in the range of 10 μM greatly stimulated PPX activity in cell-free extracts from . The results strongly suggest that a metal tolerance mechanism mediated through polyP is functional in members of the genus . This ability to accumulate and hydrolyse polyP may play an important role not only in the survival of these micro-organisms in sulfidic mineral environments containing high toxic metals concentrations, but also in their applications in biomining.

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2006-01-01
2024-03-28
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References

  1. Ahn K, Kornberg A. 1990; Polyphosphate kinase from Escherichia coli . Purification and demonstration of a phosphoenzyme intermediate. J Biol Chem 256:11734–11739
    [Google Scholar]
  2. Aiking H, Stijnman A, van Garderen C, van Heerikhuizen H, van't Riet J. 1984; Inorganic phosphate accumulation and cadmium detoxification in Klebsiella aerogenes CTC 418 growing in continuous culture. Appl Environ Microbiol 47:374–377
    [Google Scholar]
  3. Akiyama M, Crooke E, Kornberg A. 1992; The polyphosphate kinase gene of Escherichia coli . Isolation and sequence of the ppk gene and membrane location of the protein. J Biol Chem 267:22556–22561
    [Google Scholar]
  4. Akiyama M, Crooke E, Kornberg A. 1993; An exopolyphosphatase of Escherichia coli . The enzyme and its ppx gene in a polyphosphate operon. J Biol Chem 268:633–639
    [Google Scholar]
  5. Alvarez S, Jerez C. A. 2004; Copper ions stimulate polyphosphate degradation and phosphate efflux in Acidithiobacillus ferrooxidans . Appl Environ Microbiol 70:5177–5182 [CrossRef]
    [Google Scholar]
  6. Amend J. P, Shock E. L. 2001; Energetics of overall metabolic reactions of thermophilic and hyperthermophilic Archaea and Bacteria. FEMS Microbol Rev 25:175–243 [CrossRef]
    [Google Scholar]
  7. Ault-Riché D, Fraley C. D, Tzeng C.-M, Kornberg A. 1998; A novel assay reveals multiple pathways regulating stress-induced accumulations of inorganic polyphosphate in Escherichia coli . J Bacteriol 180:1841–1847
    [Google Scholar]
  8. Baker-Austin C, Dopson M, Wexler M, Sawers R. G, Bond P. L. 2005; Molecular insight into extreme copper resistance in the extremophilic archaeon Ferroplasma acidarmanus Fer1. Microbiology 151:2637–2646 [CrossRef]
    [Google Scholar]
  9. Cardona S. T, Remonsellez F, Guiliani N, Jerez C. A. 2001; The glycogen-bound polyphosphate kinase from Sulfolobus acidocaldarius is actually a glycogen synthase. Appl Environ Microbiol 67:4773–4780 [CrossRef]
    [Google Scholar]
  10. Cardona S. T, Chávez F. P, Jerez C. A. 2002; The exopolyphosphatase gene from Sulfolubus solfataricus : characterization of the first gene found to be involved in polyphosphate metabolism in Archaea . Appl Environ Microbiol 68:4812–4819 [CrossRef]
    [Google Scholar]
  11. Chávez F. P, Lünsdorf H, Jerez C. A. 2004; Growth of polychlorinated-biphenyl-degrading bacteria in the presence of biphenyl and chlorobiphenyls generates oxidative stress and massive accumulation of inorganic polyphosphate. Appl Environ Microbiol 70:3064–3072 [CrossRef]
    [Google Scholar]
  12. Deigweiher K, Drell I. V. T. L, Prutsch A, Scheidig A. J, Lübben M. 2004; Expression, isolation, and crystallization of the catalytic domain of CopB, a putative copper transporting ATPase from the thermoacidophilic archaeon Sulfolobus solfataricus . J Bioenerg Biomemr 36:151–159 [CrossRef]
    [Google Scholar]
  13. Dopson M, Baker-Austin C, Koppineedi P. R, Bond P. L. 2003; Growth in sulfidic mineral environments: metal resistance mechanisms in acidophilic microorganisms. Microbiology 149:1959–1970 [CrossRef]
    [Google Scholar]
  14. Ettema T. J, Huynen M. A, de Vos W. M, van der Oost J. 2003; TRASH: a novel metal-binding domain predicted to be involved in heavy-metal sensing, trafficking and resistance. Trends Biochem Sci 28:170–173 [CrossRef]
    [Google Scholar]
  15. Gonzalez H, Jensen T. E. 1998; Nickel sequestering by polyphosphate bodies in Staphylococcus aureus . Microbios 106:179–185
    [Google Scholar]
  16. Harwood V. J, Gordon A. S. 1994; Regulation of extracellular copper-binding proteins in copper-resistant and copper-sensitive mutants of Vibrio alginolyticus . Appl Environ Microbiol 60:1749–1753
    [Google Scholar]
  17. Keasling J. D. 1997; Regulation of intracellular toxic metals and other cations by hydrolysis of polyphosphate. Ann N Y Acad Sci 829:242–249 [CrossRef]
    [Google Scholar]
  18. Keasling J. D, Hupf G. A. 1996; Genetic manipulation of polyphosphate metabolism affects cadmium tolerance in Escherichia coli . Appl Environ Microbiol 62:743–746
    [Google Scholar]
  19. Keasling J. D, Bertsch L, Kornberg A. 1993; Guanosine pentaphosphate phosphohydrolase of Escherichia coli is a long-chain exopolyphosphatase. Proc Natl Acad Sci U S A 90:7029–7033 [CrossRef]
    [Google Scholar]
  20. Kornberg A, Rao N. N, Ault-Riché D. 1999; Inorganic polyphosphate: a molecule of many functions. Annu Rev Biochem 68:89–125 [CrossRef]
    [Google Scholar]
  21. Kumble K. D, Ahn K, Kornberg A. 1996; Phosphohistidyl active sites in polyphosphate kinase of Escherichia coli . Proc Natl Acad Sci U S A 93:14391–14395 [CrossRef]
    [Google Scholar]
  22. Lünsdorf H, Strömpl C, Osborn A. M, Bennasar A, Moore E. R. B, Abraham W.-R, Kenneth N. T. 2000; Approach to analyze interactions of microorganisms, hydrophobic substrates, biofilms and to study initial events in microbiogeological processes. Methods Enzymol 336:317–331
    [Google Scholar]
  23. Miller K. W, Risanico S. S, Risatti J. B. 1992; Differential tolerance of Sulfolobus strains to transition metals. FEMS Microbiol Lett 93:69–74 [CrossRef]
    [Google Scholar]
  24. Ogawa N, Tzeng C. M, Fraley C. D, Kornberg A. 2000; Inorganic polyphosphate in Vibrio cholerae : genetic, biochemical and physiologic features. J Bacteriol 182:6687–6693 [CrossRef]
    [Google Scholar]
  25. Pao S. S, Paulsen I. T, Saier M. H Jr. 1998; Major facilitator superfamily. Microbiol Mol Biol Rev 62:1–34
    [Google Scholar]
  26. Pedone E, Bartolucci S, Fiorentino G. 2004; Sensing and adapting to environmental stress: the archaeal tactic. Front Biosci 9:2909–2926 [CrossRef]
    [Google Scholar]
  27. Persson B. L, Lagerstedt J. O, Pratt J. R, Pattison-Granberg J, Lundh K, Shokrollahzadeh S, Lundh F. 2003; Regulation of phosphate acquisition in Saccharomyces cerevisiae . Curr Genet 43:225–244 [CrossRef]
    [Google Scholar]
  28. Rouch D. R, Lee B. T, Camakaris J. 1989; Genetics and molecular basis of copper resistance in Escherichia coli. In Metal Homeostasis pp  439–446 Edited by Hamer D. H., Winge D. R. New York: Alan Liss;
    [Google Scholar]
  29. Scherer P. A, Bochem H. P. 1983; Ultrastructural investigation of 12 Methanosarcinae and related species grown on methanol for occurrence of polyphosphatelike inclusions. Can J Microbiol 29:1190–1199 [CrossRef]
    [Google Scholar]
  30. Silver S, Phung L. T. 1996; Bacterial heavy metal resistance: new surprises. Annu Rev Microbiol 50:753–789 [CrossRef]
    [Google Scholar]
  31. Skórko R, Osipiuk J., Stetter K. O. 1989; Glycogen-bound polyphosphate kinase from the archaebacterium Sulfolobus acidocaldarius . J Bacteriol 171:5162–5164
    [Google Scholar]
  32. van Veen H. W. 1997; Phosphate transport in prokaryotes: molecules, mediators and mechanisms. Antonie van Leeuwenhoek 72:299–315 [CrossRef]
    [Google Scholar]
  33. van Veen H. W, Abee T, Kortstee G. J. J, Konings W. N, Zehnder A. J. B. 1994; Translocation of metal phosphate via phosphate inorganic transport system of Escherichia coli . Biochemistry 33:1766–1770 [CrossRef]
    [Google Scholar]
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