Skip to main content

Towards determining details of anaerobic growth coupled to ferric iron reduction by the acidophilic archaeon ‘Ferroplasma acidarmanus’ Fer1

Extremophiles volume 11, pages 159–168 (2007)Cite this article

Abstract

Elucidation of the different growth states of Ferroplasma species is crucial in understanding the cycling of iron in acid leaching sites. Therefore, a proteomic and biochemical study of anaerobic growth in ‘Ferroplasma acidarmanus’ Fer1 has been carried out. Anaerobic growth in Ferroplasma spp. occurred by coupling oxidation of organic carbon with the reduction of Fe3+; but sulfate, nitrate, sulfite, thiosulfate, and arsenate were not utilized as electron acceptors. Rates of Fe3+ reduction were similar to other acidophilic chemoorganotrophs. Analysis of the ‘F. acidarmanus’ Fer1 proteome by 2-dimensional polyacrylamide gel electrophoresis revealed ten key proteins linked with central metabolic pathways ≥4 fold up-regulated during anaerobic growth. These included proteins putatively identified as associated with the reductive tricarboxylic acid pathway used for anaerobic energy production, and others including a putative flavoprotein involved in electron transport. Inhibition of anaerobic growth and Fe3+ reduction by inhibitors suggests the involvement of electron transport in Fe3+ reduction. This study has increased the knowledge of anaerobic growth in this biotechnologically and environmentally important acidophilic archaeon.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Abbreviations

AMD:

Acid mine drainage

S0 :

Elemental sulfur

RISC:

Reduced inorganic sulfur compound

MSM:

Mineral salts medium

2D-PAGE:

2-Dimensional polyacrylamide gel electrophoresis

MALDI-TOF:

Matrix-assisted laser desorption ionization time-of-flight

1D-PAGE:

1-Dimensional polyacrylamide gel electrophoresis

TCA:

Tricarboxylic acid

HQNO:

2-Heptyl-4-Hydroxyquinoline N-oxide

References

  • Altschul SF et al (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Andrews SC, Robinson AK, Rodriguez-Quinones F (2003) Bacterial iron homeostasis. FEMS Microbiol Rev 27:215–237

    Article  PubMed  CAS  Google Scholar 

  • Baker-Austin C, Dopson M, Wexler M, Sawers G, Bond PL (2005) Molecular insight into extreme copper resistance in the extremophilic archaeon “Ferroplasma acidarmanus” Fer1. Microbiology 151:2637–2646

    Article  PubMed  CAS  Google Scholar 

  • 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 1656:114–126

    Article  PubMed  CAS  Google Scholar 

  • Bridge TAM, Johnson DB (1998) Reduction of soluble iron and reductive dissolution of ferric iron-containing minerals by moderately thermophilic iron-oxidizing bacteria. Appl Environ Microbiol 64:2181–2186

    PubMed  CAS  Google Scholar 

  • Brierley CL (2001) Bacterial succession in bioheap leaching. Hydrometallurgy 59:249–255

    Article  CAS  Google Scholar 

  • Cecchini G, Schroder I, Gunsalus RP, Maklashina E (2002) Succinate dehydrogenase and fumarate reductase from Escherichia coli. Biochim Biophys Acta Bioenerg 1553:140–157

    Article  CAS  Google Scholar 

  • Dawson MV, Lyle SJ (1990) Spectrophotometric determination of iron and cobalt with ferrozine and dithizone. Talanta 37:1189–1191

    Article  CAS  Google Scholar 

  • Degli Esposti M (1998) Inhibitors of NADH-ubiquinone reductase: an overview. Biochim Biophys Acta Bioenerg 1364:222–235

    Article  CAS  Google Scholar 

  • Dopson M, Baker-Austin C, Bond PL (2004a) First use of 2-dimensional polyacrylamide gel electrophoresis to determine phylogenetic relationships. J Microbiol Methods 58:297–302

    Article  CAS  Google Scholar 

  • Dopson M, Baker-Austin C, Bond PL (2005) Analysis of differential protein expression during growth states of Ferroplasma strains and insights into electron transport for iron oxidation. Microbiology 151:4127–4137

    Article  PubMed  CAS  Google Scholar 

  • Dopson M, Baker-Austin C, Hind A, Bowman JP, Bond PL (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

    Article  CAS  Google Scholar 

  • Dopson M, Baker-Austin C, Koppineedi PR, Bond PL (2003) Growth in sulfidic mineral environments: metal resistance mechanisms in acidophilic micro-organisms. Microbiology 149:1959–1970

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Edwards KJ, Bond PL, Gihring TM, Banfield JF (2000) An archaeal iron-oxidizing extreme acidophile important in acid mine drainage. Science 287:1796–1799

    Article  PubMed  CAS  Google Scholar 

  • Golyshina OV et al (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

    PubMed  CAS  Google Scholar 

  • Golyshina OV, Timmis KN (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

    Article  PubMed  CAS  Google Scholar 

  • Hallberg KB, Thomson HEC, Boeselt I, Johnson DB (2001) Aerobic and anaerobic sulfur metabolism by acidophilic bacteria. In: Ciminelli VST, Garcia O Jr (eds) International biohydrometallurgy symposium. Elselvier, Ouro Preto, Brazil, pp 423–431

  • Hesketh A et al (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

    Article  PubMed  CAS  Google Scholar 

  • Huynen MA, Dandekar T, Bork P (1999) Variation and evolution of the citric-acid cycle: a genomic perspective. Trends Microbiol 7:281–291

    Article  PubMed  CAS  Google Scholar 

  • Johnson DB, Bridge TAM (2002) Reduction of ferric iron by acidophilic heterotrophic bacteria: evidence for constitutive and inducible enzyme systems in Acidiphilium spp. J Appl Microbiol 92:315–321

    Article  PubMed  CAS  Google Scholar 

  • Johnson DB, McGinness S (1991) Ferric iron reduction by acidophilic heterotrophic bacteria. Appl Environ Microbiol 57:207–211

    PubMed  CAS  Google Scholar 

  • Kolthoff JM, Sandell EB (1963) Textbook of quantitative inorganic chemistry. MacMillan Publishing Co., New York

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kusel K, Dorsch T, Acker G, Stackebrandt E (1999) Microbial reduction of Fe(III) in acidic sediments: isolation of Acidiphilium cryptum JF-5 capable of coupling the reduction of Fe(III) to the oxidation of glucose. Appl Environ Microbiol 65:3633–3640

    PubMed  CAS  Google Scholar 

  • Kusel K, Roth U, Drake HL (2002) Microbial reduction of Fe(III) in the presence of oxygen under low pH conditions. Environ Microbiol 4:414–421

    Article  PubMed  CAS  Google Scholar 

  • Lombardo MJ, Bagga D, Miller CG (1991) Mutations in rpoA affect expression of anaerobically regulated genes in Salmonella typhimurium. J Bacteriol 173:7511–7518

    PubMed  CAS  Google Scholar 

  • Nordstrom DK, Alpers CN, Ptacek CJ, Blowes DW (2000) Negative pH and extremely acidic mine waters from Iron Mountain, California. Environ Sci Technol 34:254–258

    Article  CAS  Google Scholar 

  • Ohmura N, Sasaki K, Matsumoto N, Saiki H (2002) Anaerobic respiration using Fe3+, S0, and H2 in the chemolithoautotrophic bacterium Acidithiobacillus ferrooxidans. J Bacteriol 184:2081–2087

    Article  PubMed  CAS  Google Scholar 

  • Okibe N, Gericke M, Hallberg KB, Johnson DB (2003) Enumeration and characterization of acidophilic microorganisms isolated from a pilot plant stirred-tank bioleaching operation. Appl Environ Microbiol 69:1936–1943

    Article  PubMed  CAS  Google Scholar 

  • Pritchard RH, Tempest DW (1982) Growth: cells and populations. In: Mandelstam J, McQuillen K, Dawes I (eds) Biochemistry of bacterial growth, 3rd edn. Blackwell Scientific Publications, Oxford

  • Richardson DJ (2000) Bacterial respiration: a flexible process for a changing environment. Microbiology 146:551–571

    PubMed  CAS  Google Scholar 

  • Schröder I, Johnson E, de Vries S (2003) Microbial ferric iron reductases. FEMS Microbiol Rev 27:427–447

    Article  PubMed  Google Scholar 

  • Suzuki I (2001) Microbial leaching of metals from sulfide minerals. Biotechnol Adv 19:119–132

    Article  PubMed  CAS  Google Scholar 

  • Thomas PE, 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

    Article  PubMed  CAS  Google Scholar 

  • Tolkatchev D, Yu L, Yu CA (1996) Potential induced redox reactions in mitochondrial and bacterial cytochrome b-c 1 complexes. J Biol Chem 271:12356–12363

    Article  PubMed  CAS  Google Scholar 

  • Tyson GW et al (2004) Community structure and metabolism through reconstruction of microbial genomes from the environment. Nature 428:37–43

    Article  PubMed  CAS  Google Scholar 

  • Walt A, Kahn ML (2002) The fixA and fixB genes are necessary for anaerobic carnitine reduction in Escherichia coli. J Bacteriol 184:4044–4047

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank JF Banfield and KJ Edwards for provision of ‘F. acidarmanus’ Fer1 and helpful discussions. DJ Richardson is acknowledged for assistance in interpreting electron transport data. Trypsin digests and MALDI-TOF analysis of excised proteins was carried out at the John Innes Centre, Norwich. The technical assistance of M Maidment and L Flegg was greatly appreciated and R Evans-Gowing is acknowledged for taking the electron micrographs. This work was funded by a BBSRC Research grant.

Author information

Author notes

  1. Philip Bond

    Present address: Advanced Wastewater Management Centre, University of Queensland, Queensland, 4072, Australia

  2. Craig Baker-Austin

    Present address: Savannah River Ecology Laboratory, University of Georgia, Aiken, SC, USA

Authors and Affiliations

  1. School of Biological Sciences, University of East Anglia, Norwich, NR4 7TJ, UK

    Mark Dopson, Craig Baker-Austin & Philip Bond

  2. Molecular Biology, Umeå University, 901 87, Umea, Sweden

    Mark Dopson

  3. Centre for Ecology, Evolution and Conservation, University of East Anglia, Norwich, NR4 7TJ, UK

    Philip Bond

Authors
  1. Mark Dopson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Craig Baker-Austin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Philip Bond
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Philip Bond.

Additional information

Communicated by G. Antranikian.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Dopson, M., Baker-Austin, C. & Bond, P. Towards determining details of anaerobic growth coupled to ferric iron reduction by the acidophilic archaeon ‘Ferroplasma acidarmanus’ Fer1. Extremophiles 11, 159–168 (2007). https://doi.org/10.1007/s00792-006-0029-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-006-0029-y

Keywords

  • Ferroplasma
  • Proteomics
  • Anaerobic
  • Electron transport
  • Metabolism