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The cellular machinery of Ferroplasma acidiphilum is iron-protein-dominated

Nature volume 445, pages 91–94 (2007)Cite this article

Abstract

Ferroplasma is a genus of the Archaea, one of the three branches of the tree of life, and belongs to the order Thermoplasmatales (Euryarchaeota), which contains the most acidophilic microbes yet known. Ferroplasma species live in acid mine drainage, acidic pools and environments containing sulphidic ores such as pyrite and characterized by pH values of 0–2 and high concentrations of ferrous iron and other heavy metals1,2,3. F. acidiphilum strain YT is a chemoautotroph that grows optimally at pH 1.7 and gains energy by oxidizing ferrous iron and carbon by the fixation of carbon dioxide1. Here we show that 86% of 189 investigated cellular proteins of F. acidiphilum are iron-metalloproteins. These include proteins with deduced structural, chaperone and catalytic roles, not described as iron-metalloproteins in any other organism so far investigated. The iron atoms in the proteins seem to organize and stabilize their three-dimensional structures, to act as ‘iron rivets’. Analysis of proteins of the phylogenetic neighbour Picrophilus torridus and of the habitat neighbour Acidithiobacillus ferrooxidans revealed far fewer and only typical metalloproteins. F. acidiphilum therefore has a currently unique iron-protein-dominated cellular machinery and biochemical phylogeny.

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Figure 1: ‘Luminal metalloproteome’ of F. acidiphilum YT.

References

  1. Golyshina, O. V. et al. 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. 3, 997–1006 (2000)

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  3. Dopson, M., Baker-Austin, C., Hind, A., Bowman, J. P. & Bond, P. C. 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 (2004)

    Article  CAS  Google Scholar 

  4. Ferrer, M., Golyshina, O. V., Plou, F. J., Timmis, K. N. & Golyshin, P. N. A novel α-glucosidase from the acidophilic archaeon Ferroplasma acidiphilum strain Y with high transglycosylation activity and an unusual catalytic nucleophile. Biochem. J. 391, 269–276 (2005)

    Article  CAS  Google Scholar 

  5. Agarwalla, S., Stroud, R. M. & Gaffney, B. J. Redox reactions of the iron–sulfur clusters in a ribosomal RNA methyltransferase, RumA: optical and EPR studies. J. Biol. Chem. 279, 34123–34129 (2004)

    Article  CAS  Google Scholar 

  6. Boal, A. K. et al. DNA-bound redox activity of DNA repair glycosylases containing [4Fe-4S] clusters. Biochemistry 44, 8397–8407 (2005)

    Article  CAS  Google Scholar 

  7. Pierrel, F., Bjork, G. R., Fontecave, M. & Atta, M. Enzymatic modification of tRNAs: MiaB is an iron–sulfur protein. J. Biol. Chem. 277, 13367–13370 (2002)

    Article  CAS  Google Scholar 

  8. Watson, A. J., Bakker, D. C., Ridgwell, A. J., Bord, P. W. & Law, C. S. Effect of iron supply on Southern Ocean CO2 uptake and implications for glacial atmospheric CO2 . Nature 407, 730–733 (2000)

    Article  ADS  CAS  Google Scholar 

  9. Buesseler, K. O., Andrews, J. E., Pike, S. M. & Charetter, M. A. The effect of iron fertilization on carbon sequestration in the Southern Ocean. Science 304, 414–417 (2004)

    Article  ADS  CAS  Google Scholar 

  10. Imlay, J. A. Iron–sulphur clusters and the problem with oxygen. Mol. Microbiol. 59, 1073–1082 (2006)

    Article  Google Scholar 

  11. Blochl, E., Keller, M., Wächterhauser, G. & Stetter, K. O. Reactions depending on iron sulfde and linking geochemistry with biochemistry. Proc. Natl Acad. Sci. USA 89, 8117–8120 (1992)

    Article  ADS  CAS  Google Scholar 

  12. Wächtershäuser, G. Discussing the origin of life. Science 296, 1982–1983 (2002)

    Article  Google Scholar 

  13. Major, T. A., Burd, H. & Whitman, W. B. Abundance of 4Fe-4S motifs in the genomes of methanogens and other prokaryotes. FEMS Microbiol. Lett. 239, 117–123 (2004)

    Article  CAS  Google Scholar 

  14. Schneider, D. & Schmidt, C. L. Multiple Rieske proteins in prokaryotes: where and why? Biochim. Biophys. Acta 1710, 1–12 (2005)

    Article  CAS  Google Scholar 

  15. Giometti, C. S. et al. Analysis of the Shewanella oneidensis proteome by two-dimensional gel electrophoresis under non-denaturing conditions. Proteomics 3, 777–785 (2003)

    Article  CAS  Google Scholar 

  16. Golyshina, O. V., Golyshin, P. N., Timmis, K. N. & Ferrer, M. The ‘pH optimum anomaly’ of intracellular enzymes of Ferroplasma acidiphilum. Environ. Microbiol. 8, 416–425 (2006)

    Article  CAS  Google Scholar 

  17. Högbom, M. et al. A high-throughput method for the detection of metalloproteins on a milligram scale. Mol. Cell. Proteomics 4, 827–834 (2005)

    Article  Google Scholar 

Download references

Acknowledgements

We thank G. Wächtershäuser, R. Thauer, M. Wilson, A. Böck and A. Ballesteros for discussions. This research was supported by the Spanish Ministerio de Educación y Ciencia (MEC) (Ramón y Cajal contract to M.F. and a FPU Fellowship to A.B.), European Community Project ‘BIOMELI’, the Microbial Genomic Network Programme (GenoMik Plus) of the German Ministry for Education and Research (BMBF), and the DFG Priority Program ‘Mars and Terrestrial Planets’. K.N.T. thanks the Fonds der Chemischen Industrie for generous support.

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Author notes

  1. Peter N. Golyshin and Kenneth N. Timmis: These authors contributed equally to this work.

Authors and Affiliations

  1. CSIC, Institute of Catalysis, Cantoblanco, 28049, Madrid, Spain

    Manuel Ferrer & Ana Beloqui

  2. Department of Environmental Microbiology, HZI-Helmholtz Centre for Infection Research, 38124, Braunschweig, Germany

    Olga V. Golyshina, Peter N. Golyshin & Kenneth N. Timmis

  3. Institute of Microbiology, Carolo-Wilhelmina Technical University of Braunschweig, 38106, Braunschweig, Germany

    Peter N. Golyshin & Kenneth N. Timmis

  4. Department of Biological Sciences, University of Essex, Colchester, CO4 3SQ, UK

    Kenneth N. Timmis

Authors
  1. Manuel Ferrer
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  2. Olga V. Golyshina
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  4. Peter N. Golyshin
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Correspondence to Manuel Ferrer.

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This file contains Supplementary Methods, Supplementary Figures S1 and S2 with legends and Supplementary Tables S1-S5. (PDF 1623 kb)

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Ferrer, M., Golyshina, O., Beloqui, A. et al. The cellular machinery of Ferroplasma acidiphilum is iron-protein-dominated. Nature 445, 91–94 (2007). https://doi.org/10.1038/nature05362

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