Archives of Microbiology

, Volume 189, Issue 4, pp 305–312 | Cite as

Iron and carbon metabolism by a mineral-oxidizing Alicyclobacillus-like bacterium

  • Adibah Yahya
  • Kevin B. Hallberg
  • D. Barrie Johnson
Original Paper

Abstract

A novel iron-oxidizing, moderately thermophilic, acidophilic bacterium (strain “GSM”) was isolated from mineral spoil taken from a gold mine in Montana. Biomolecular analysis showed that it was most closely related to Alicyclobacillus tolerans, although the two bacteria differed in some key respects, including the absence (in strain GSM) of ϖ-alicyclic fatty acids and in their chromosomal base compositions. Isolate GSM was able to grow in oxygen-free media using ferric iron as terminal electron acceptor confirming that it was a facultative anaerobe, a trait not previously described in Alicyclobacillus spp.. The acidophile used both organic and inorganic sources of energy and carbon, although growth and iron oxidation by isolate GSM was uncoupled in media that contained both fructose and ferrous iron. Fructose utilization suppressed iron oxidation, and oxidation of ferrous iron occurred only when fructose was depleted. In contrast, fructose catabolism was suppressed when bacteria were harvested while actively oxidizing iron, suggesting that both ferrous iron- and fructose-oxidation are inducible in this acidophile. Isolate GSM accelerated the oxidative dissolution of pyrite in liquid media either free of, or amended with, organic carbon, although redox potentials were significantly different in these media. The potential of this isolate for commercial mineral processing is discussed.

Keywords

Acidophile Alicyclobacillus Firmicute Iron oxidation Iron reduction Mixotroph Pyrite 

Notes

Acknowledgments

AY is grateful to the Universiti Teknologi Malaysia for providing and research studentship, and DBJ to the Royal Society, UK, for providing an Industrial Research Fellowship.

References

  1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402PubMedCrossRefGoogle Scholar
  2. 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 64:2181–2590PubMedGoogle Scholar
  3. Chang S-S, Kang D-K (2004) Alicyclobacillus spp. in the fruit juice industry: history, characteristics, and current isolation/detection procedures. Crit Rev Microbiol 30:55–74PubMedCrossRefGoogle Scholar
  4. Clark DA, Norris PR (1996) Acidimicrobium ferrooxidans gen. nov., sp. nov.: mixed-culture ferrous iron oxidation with Sulfobacillus species. Microbiology 142:785–790Google Scholar
  5. Ehrlich HL (2002) Geomicrobiology, 4th edn. Taylor and Francis, New YorkGoogle Scholar
  6. Germida JJ (1985) Modified sulfur-containing media for studying sulfur-oxidizing microorganisms. In: Caldwell DE, Brierley JA, Brierley CL (eds) Planetary ecology. van Nostrand Reinhold, New York, pp 333–344Google Scholar
  7. Goto K, Mochida K, Asahara M, Suzuki M, Kasai H, Yokota A (2003) Alicyclobacillus pomorum sp. nov., a novel thermo-acidophilic, endospore-forming bacterium that does not possess a-alicyclic fatty acids, and emended description of the genus Alicyclobacillus. Int J Syst Evol Microbiol 53:1537–1544PubMedCrossRefGoogle Scholar
  8. Hallberg KB, Johnson DB (2001) Biodiversity of acidophilic microorganisms. Adv Appl Microbiol 49:37–84PubMedCrossRefGoogle Scholar
  9. Johnson DB (1995) Selective solid media for isolating and enumerating acidophilic bacteria. J Microbiol Methods 23:205–218CrossRefGoogle Scholar
  10. Johnson DB (2007) Physiology and ecology of acidophilic microorganisms. In: Gerday C, Glansdorff N (eds) Physiology and biochemistry of extremophiles. ASM, Washington, DC, pp 257–270Google Scholar
  11. Johnson DB, Body DA, Bridge TAM, Bruhn DF, Roberto FF (2001) Biodiversity of acidophilic moderate thermophiles isolated from two sites in Yellowstone National Park, and their roles in the dissimilatory oxido-reduction of iron. In: Reysenbach AL, Voytek A (eds) Thermophiles: biodiversity, ecology and evolution. Kluwer/Plenum, New York, pp 23–39Google Scholar
  12. Johnson DB, Okibe N, Roberto FF (2003) Novel thermo-acidophilic bacteria isolated from geothermal sites in Yellowstone National Park: physiological and phylogenetic characteristics. Arch Microbiol 180:60–68PubMedCrossRefGoogle Scholar
  13. Johnson DB, Bacelar-Nicolau P, Okibe N, Thomas A, Hallberg KB (2007) Characteristics of Ferrimicrobium acidiphilum gen. nov., sp. nov., and Ferrithrix thermotolerans gen. nov., sp. nov.: heterotrophic iron-oxidizing, extremely acidophilic Actinobacteria. Int J Syst Evol Microbiol (submitted)Google Scholar
  14. Karavaiko GI et al (2005) Reclassification of ‘Sulfobacillus thermosulfidooxidans subsp. thermotolerans’ strain K1 as Alicyclobacillus tolerans sp. nov. and Sulfobacillus disulfidooxidans Dufresne et al. 1996 as Alicyclobacillus disulfidooxidans comb. nov., and emended description of the genus Alicyclobacillus. Int J Syst Evol Microbiol 55:941–947PubMedCrossRefGoogle Scholar
  15. Lovley DR, Phillips EJP (1987) Rapid assay for microbially reduced ferric iron in aquatic sediments. Appl Environ Microbiol 53:1536–1540PubMedGoogle Scholar
  16. Norris PR, Ingledew WJ (1992) Acidophilic bacteria: adaptations and applications. In: Herbert RA, Sharp RJ (eds) Molecular biology and biotechnology of extremophiles. Royal Society for Chemistry, Cambridge, pp 121–131Google Scholar
  17. Norris PR, Clark DA, Owen JP, Waterhouse S (1996) Characteristics of Sulfobacillus acidophilus sp. nov. and other moderately thermophilic mineral-sulphide-oxidizing bacteria. Microbiology 142:775–783PubMedCrossRefGoogle Scholar
  18. 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 69:1936–1943PubMedCrossRefGoogle Scholar
  19. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  20. Third KA, Cord-Ruwisch R, Watling HR (2002) Control of the redox potential by oxygen limitation improves bacterial leaching of chalcopyrite. Biotechnol Bioeng 78:433–441PubMedCrossRefGoogle Scholar
  21. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882PubMedCrossRefGoogle Scholar
  22. Trevelyan WE, Harrison JS (1952) Studies on yeast metabolism: 1. Fractionation and microdetermination of cell carbohydrates. Biochem J 50:298–303PubMedGoogle Scholar
  23. Wilson K (1987) Preparation of genomic DNA from bacteria. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JA, Struhl K (eds) Current protocols in molecular biology. Green & Wiley Interscience, New York, pp 2.4.1–2.4.5Google Scholar
  24. Wisotzkey JD, Jurtshuk P, Fox GE, Deinhard G, Poralla K (1992) Comparative sequence analyses on the 16S ribosomal-RNA (rDNA) of Bacillus acidocaldarius, Bacillus acidoterrestris, and Bacillus cycloheptanicus and proposal for creation of a new genus, Alicyclobacillus gen. nov. Int J Syst Bacteriol 42:263–269PubMedCrossRefGoogle Scholar
  25. Wood AP, Kelly DP (1983) Autotrophic and mixotrophic growth of three thermoacidophilic iron-oxidizing bacteria. FEMS Microbiol Lett 20:107–112CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Adibah Yahya
    • 1
    • 2
  • Kevin B. Hallberg
    • 1
  • D. Barrie Johnson
    • 1
  1. 1.School of Biological Sciences University of WalesBangorUK
  2. 2.Department of Biology, Institute of Environmental and Water Resource ManagementUniversiti Teknologi MalaysiaUTM SkudaiMalaysia

Personalised recommendations