1887

Abstract

To investigate the metabolic biochemistry of iron-oxidizing extreme acidophiles, a proteomic analysis of chemomixotrophic and chemo-organotrophic growth, as well as protein expression in the absence of organic carbon, was carried out in species. Electron transport chain inhibitor studies, spectrophotometric analysis and proteomic results suggest that oxidation of ferrous iron may be mediated by the blue copper-haem protein sulfocyanin and the derived electron passes to a terminal electron acceptor. Despite previous suggestions of a putative carbon dioxide fixation pathway, no up-regulation of proteins typically associated with carbon dioxide fixation was evident during incubation in the absence of organic carbon. Although a lack of known carbon dioxide fixation proteins does not constitute proof, the results suggest that these strains are not autotrophic. Proteins putatively involved in central metabolic pathways, a probable sugar permease and flavoproteins were up-regulated during chemo-organotrophic growth in comparison to the protein complement during chemomixotrophic growth. These results reflect a higher energy demand to be derived from the organic carbon during chemo-organotrophic growth. Proteins with suggested function as central metabolic enzymes were expressed at higher levels during chemomixotrophic growth by Y compared to ‘’ Fer1. This study addresses some of the biochemical and bioenergetic questions fundamental for survival of these organisms in extreme acid-leaching environments.

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2005-12-01
2024-03-28
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References

  1. Alexander B., Leach S., Ingledew W. J. 1987; The relationship between chemiosmotic parameters and sensitivity to anions and organic acids in the acidophile Thiobacillus ferrooxidans . J Gen Microbiol 133:1171–1179
    [Google Scholar]
  2. Andrews S. C., Robinson A. K., Rodriguez-Quinones F. 2003; Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237 [CrossRef]
    [Google Scholar]
  3. Appia-Ayme C., Guiliani N., Ratouchniak J., Bonnefoy V. 1999; Characterization of an operon encoding two c -type cytochromes, an aa 3-type cytochrome oxidase, and rusticyanin in Thiobacillus ferrooxidans ATCC 33020. Appl Environ Microbiol 65:4781–4787
    [Google Scholar]
  4. Barr D. W., Ingledew W. J., Norris P. R. 1990; Respiratory-chain components of iron-oxidizing, acidophilic bacteria. FEMS Microbiol Lett 70:85–89 [CrossRef]
    [Google Scholar]
  5. Baumler D. J., Jeong K.-W., Fox B. G., Banfield J. F., Kaspar C. W. 2005; Sulfate requirement for heterotrophic growth of “ Ferroplasma acidarmanus ” strain fer1. Res Microbiol 156:492–498 [CrossRef]
    [Google Scholar]
  6. Blake R. C., Shute E. A., Greenwood M. M., Spencer G. H., Ingledew W. J. 1993; Enzymes of aerobic respiration on iron. FEMS Microbiol Rev 11:9–18 [CrossRef]
    [Google Scholar]
  7. Blum H., Beier H., Gross H. J. 1987; Improved silver staining of plant-proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 8:93–99 [CrossRef]
    [Google Scholar]
  8. Brasseur G., Levican G., Bonnefoy V., Holmes D., Jedlicki E., Lemesle-Meunier D. 2004; Apparent redundancy of electron transfer pathways via bc 1 complexes and terminal oxidases in the extremophilic chemolithoautotrophic. Acidithiobacillus ferrooxidans Biochim Biophys Acta; 1656114–126 [CrossRef]
    [Google Scholar]
  9. Cannio R., Fiorentino G., Morana A., Rossi M., Bartolucci S. 2000; Oxygen: friend or foe? Archaeal superoxide dismutases in the protection of intra- and extracellular oxidative stress. Front Biosci 5:768–779 [CrossRef]
    [Google Scholar]
  10. Dawson M. V., Lyle S. J. 1990; Spectrophotometric determination of iron and cobalt with ferrozine and dithizone. Talanta 37:1189–1191 [CrossRef]
    [Google Scholar]
  11. Dopson M., Lindström E. B. 1999; Potential role of Thiobacillus caldus in arsenopyrite bioleaching. Appl Environ Microbiol 65:36–40
    [Google Scholar]
  12. Dopson M., Baker-Austin C., Koppineedi P. R., Bond P. L. 2003; Growth in sulfidic mineral environments: metal resistance mechanisms in acidophilic micro-organisms. Microbiology 149:1959–1970 [CrossRef]
    [Google Scholar]
  13. Dopson M., Baker-Austin C., Bond P. L. 2004a; First use of 2-dimensional polyacrylamide gel electrophoresis to determine phylogenetic relationships. J Microbiol Methods 58:297–302 [CrossRef]
    [Google Scholar]
  14. Dopson M., Baker-Austin C., Hind A., Bowman J. P., Bond P. L. 2004b; 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 [CrossRef]
    [Google Scholar]
  15. Edwards K. J., Bond P. L., Gihring T. M., Banfield J. F. 2000; An archaeal iron-oxidizing extreme acidophile important in acid mine drainage. Science 287:1796–1799 [CrossRef]
    [Google Scholar]
  16. Elbehti A., Nitschke W., Tron P., Michel C., Lemesle-Meunier D. 1999; Redox components of cytochrome bc -type enzymes in acidophilic prokaryotes. I. Characterization of the cytochrome bc 1-type complex of the acidophilic ferrous ion-oxidizing bacterium Thiobacillus ferrooxidans . J Biol Chem 274:16760–16765 [CrossRef]
    [Google Scholar]
  17. Ferry J. G. 1995; CO dehydrogenase. Annu Rev Microbiol 49:305–333 [CrossRef]
    [Google Scholar]
  18. Golyshina O. V., Timmis K. N. 2005; Ferroplasma and relatives, recently discovered cell wall-lacking archaea making a living in extremely acid, heavy metal-rich environments. Environ Microbiol 7:1277–1288 [CrossRef]
    [Google Scholar]
  19. Golyshina O. V., Pivovarova T. A., Karavaiko G. I. 7 other authors 2000; 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 50:997–1006 [CrossRef]
    [Google Scholar]
  20. Gonzalez-Toril E., Llobet-Brossa E., Casamayor E. O., Amann R., Amils R. 2003; Microbial ecology of an extreme acidic environment, the Tinto River. Appl Environ Microbiol 69:4853–4865 [CrossRef]
    [Google Scholar]
  21. Hallberg K. B., Johnson D. B. 2001; Biodiversity of acidophilic prokaryotes. Adv Appl Microbiol 49:37–84
    [Google Scholar]
  22. Hart A., Murrell J. C., Poole R. K., Norris P. R. 1991; An acid-stable cytochrome in iron-oxidizing Leptospirillum-ferrooxidans . FEMS Microbiol Lett 81:89–94 [CrossRef]
    [Google Scholar]
  23. Hawkes R. B., Franzman P. D., Plumb J. J. 2005; Microbiology of an industrial-scale chalcocite heap bioleaching operation. In Bac-Min Conference pp 11–17 Bendigo, Victoria, Australia: AusIMM;
    [Google Scholar]
  24. Hesketh A., Fink D., Gust B., Rexer H. U., Scheel B., Chater K., Wohlleben W., Engels A. 2002; The GlnD and GlnK homologues of Streptomyces coelicolor A3(2) are functionally dissimilar to their nitrogen regulatory system counterparts from enteric bacteria. Mol Microbiol 46:319–330 [CrossRef]
    [Google Scholar]
  25. Kinnunen P. H. M., Puhakka J. A. 2004; High-rate ferric sulfate generation by a Leptospirillum ferriphilum -dominated biofilm and the role of jarosite in biomass retainment in a fluidized-bed reactor. Biotechnol Bioeng 85:697–705 [CrossRef]
    [Google Scholar]
  26. Klumpp M., Baumeister W. 1998; The thermosome: archetype of group II chaperonins. FEBS Lett 430:73–77 [CrossRef]
    [Google Scholar]
  27. Komorowski L., Schafer G. 2001; Sulfocyanin and subunit II, two copper proteins with novel features, provide new insight into the archaeal SoxM oxidase supercomplex. FEBS Lett 487:351–355 [CrossRef]
    [Google Scholar]
  28. Komorowski L., Verheyen W., Schafer G. 2002; The archaeal respiratory supercomplex SoxM from S. acidocaldarius combines features of quinole and cytochrome c oxidases. Biol Chem 383:1791–1799
    [Google Scholar]
  29. Nordstrom D. K., Alpers C. N. 1999; Negative pH, efflorescent mineralogy, and consequences for environmental restoration at the iron mountain superfund site, California. Proc Natl Acad Sci U S A 96:3455–3462 [CrossRef]
    [Google Scholar]
  30. Okibe N., Johnson D. B. 2004; Biooxidation of pyrite by defined mixed cultures of moderately thermophilic acidophiles in pH-controlled bioreactors: significance of microbial interactions. Biotechnol Bioeng 87:574–583 [CrossRef]
    [Google Scholar]
  31. Okibe N., Gericke M., Hallberg K. B., Johnson D. B. 2003; Enumeration and characterization of acidophilic microorganisms isolated from a pilot plant stirred-tank bioleaching operation. Appl Environ Microbiol 69:1936–1943 [CrossRef]
    [Google Scholar]
  32. Patel M. S., Roche T. E. 1990; Molecular biology and biochemistry of pyruvate dehydrogenase complexes. FASEB J 4:3224–3233
    [Google Scholar]
  33. Pivovarova T. A., Kondrat'eva T. F., Batrakov S. G., Esipov S. E., Sheichenko V. I., Bykova S. A., Lysenko A. M., Karavaiko G. I. 2002; Phenotypic features of Ferroplasma acidiphilum strains Y-T and Y-2. Microbiology 71:698–706 [CrossRef]
    [Google Scholar]
  34. Sambrook J., Fritsch E. F., Maniatas T. 1989 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor;
    [Google Scholar]
  35. Schafer G., Purschke W., Schmidt C. L. 1996; On the origin of respiration: electron transport proteins from archaea to man. FEMS Microbiol Rev 18:173–188 [CrossRef]
    [Google Scholar]
  36. Seaver L. C., Imlay J. A. 2001; Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli . J Bacteriol 183:7173–7181 [CrossRef]
    [Google Scholar]
  37. Singer P. C., Stumm W. 1970; Acid mine drainage: the rate-determining step. Science 167:1121–1123 [CrossRef]
    [Google Scholar]
  38. Smith R. D. 2000; Probing proteomes – seeing the whole picture?. Nat Biotechnol 18:1041–1042 [CrossRef]
    [Google Scholar]
  39. Thomas P. E., Ryan D., Levin W. 1976; An improved staining procedure for the detection of the peroxidase activity of cytochrome P-450 on sodium dodecyl sulfate polyacrylamide gels. Anal Biochem 75:168–176 [CrossRef]
    [Google Scholar]
  40. Tyson G. W., Chapman J., Hugenholtz P. 7 other authors 2004; Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43 [CrossRef]
    [Google Scholar]
  41. Yarzabal A., Brasseur G., Ratouchniak J., Lund K., Lemesle-Meunier D., DeMoss J. A., Bonnefoy V. 2002; The high-molecular-weight cytochrome c cyc2 of Acidithiobacillus ferrooxidans is an outer membrane protein. J Bacteriol 184:313–317 [CrossRef]
    [Google Scholar]
  42. Yarzabal A., Duquesne K., Bonnefoy V. 2003; Rusticyanin gene expression of Acidithiobacillus ferrooxidans ATCC 33020 in sulfur- and in ferrous iron media. Hydrometallurgy 71:107–114 [CrossRef]
    [Google Scholar]
  43. Yarzabal A., Appia-Ayme C., Ratouchniak J., Bonnefoy V. 2004; Regulation of the expression of the Acidithiobacillus ferrooxidans rus operon encoding two cytochromes c 1 a cytochrome oxidase and rusticyanin. Microbiology 150:2113–2123 [CrossRef]
    [Google Scholar]
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