Extremophiles

, 12:789 | Cite as

Sulfobacillus benefaciens sp. nov., an acidophilic facultative anaerobic Firmicute isolated from mineral bioleaching operations

  • D. Barrie Johnson
  • Catherine Joulian
  • Patrick d’Hugues
  • Kevin B. Hallberg
Original Paper

Abstract

Gram-positive bacteria found as the sole Firmicutes present in two mineral bioleaching stirred tanks, and a third bacterium isolated from a heap leaching operation, were shown to be closely related to each other but distinct from characterized acidophilic iron- and sulfur-oxidizing bacteria of the genus Sulfobacillus, to which they were affiliated. One of the isolates (BRGM2) was shown to be a thermo-tolerant (temperature optimum 38.5°C, and maximum 47°C) obligate acidophile (pH optimum 1.5, and minimum 0.8), and also noted to be a facultative anaerobe, growing via ferric iron respiration in the absence of oxygen. Although isolates BRGM2 and TVK8 were able to metabolize many monomeric organic substrates, their propensity for autotrophic growth was found to be greater than that of Sulfobacillus thermosulfidooxidans and the related acidophile, Sb. acidophilus. Faster growth rates of the novel isolates in the absence of organic carbon was considered to be a major reason why they, rather than Sb. thermosulfidooxidans (which shared many physiological characteristics) more successfully exploited conditions in the stirred tanks. Based on their phylogenetic and phenotypic characteristics, the isolates are designated strains of the proposed novel species, Sulfobacillus benefaciens, with isolate BRGM2 nominated as the type strain.

Keywords

Acidophiles Bioleaching Biomining Firmicute Iron Pyrite Sulfobacillus Sulfur 

Notes

Acknowledgments

This work was carried out in the frame of Bioshale (European project contract NMP2-CT-2004 505710) and in the frame of BioMinE (European project contract NMP1-CT-500329-1). The authors acknowledge the financial support given to these projects by the European Commission under the Sixth Framework Programme for Research and Development. We also wish to thank our various partners on the projects for their contributions to the work reported in this paper. The authors would like to thank Hafida El Achbouni for her technical support, Dr D.H. Morin (of BRGM) for providing the BRGM-KCC mixed culture, and Professor Jean Euzéby for his expert advice on bacterial nomenclature. DBJ is grateful to the Royal Society (UK) for the award of an Industrial Fellowship.

References

  1. Battaglia-Brunet F, Clarens M, d’Hugues P, Godon JJ, Foucher S, Morin D (2002) Monitoring of a pyrite-oxidising bacterial population using DNA single-strand conformation polymorphism and microscopic techniques. Appl Microbiol Biotechnol 60:206–211PubMedCrossRefGoogle Scholar
  2. Bogdanova TI, Tsaplina IA, Kondrat’eva TF, Duda VI, Suzina NE, Melamud VS, Tourova TP, Karavaiko GI (2006) Sulfobacillus thermotolerans sp. nov., a thermotolerant, chemolithotrophic bacterium. Int J Syst Evol Microbiol 56:1039–1042PubMedCrossRefGoogle Scholar
  3. Bond PL, Banfield JF (2001) Design and performance of rRNA targeted oligonucleotide probes for in situ detection and phylogenetic identification of microorganisms inhabiting acid mine drainage environments. Microbial Ecol 41:149–161Google Scholar
  4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254PubMedCrossRefGoogle Scholar
  5. 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
  6. d’Hugues P, Joulian C, Spolaore P, Michel C, Garrido F, Morin D (2008) Continuous bioleaching of a pyrite in stirred reactors: population dynamics and exopolysaccharides production vs. bioleaching performances. Hydrometallurgy (in press)Google Scholar
  7. De Ley J, Cattoir H, Reynaerts A (1970) The quantitative measurement of DNA hybridization from renaturation rates. Eur J Biochem 12:133–142PubMedCrossRefGoogle Scholar
  8. Felsenstein J (1985) Confidence-limits on phylogenies—an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  9. Ghauri MA, Johnson DB (1991) Physiological diversity amongst some moderately thermophilic iron-oxidising bacteria. FEMS Microbiol Ecol 85:327–334CrossRefGoogle Scholar
  10. Goebel BM, Stackebrandt E (1994) The biotechnological importance of molecular biodiversity studies for metal bioleaching. In: Priest FG, Ramos-Cormenzana A, Tindall BJ (eds) Bacterial diversity and systematics (FEMS Symposium No. 75). Plenum Press, New York, pp 259–273Google Scholar
  11. Golovacheva RS, Karavaiko GI (1978) Sulfobacillus, a new genus of spore forming thermophilic bacteria. Mikrobiologiya 47:815–822Google Scholar
  12. Hallberg KB, Coupland K, Kimura S, Johnson DB (2006) Macroscopic streamer growths in acidic, metal-rich mine waters in north Wales consist of novel and remarkably simple bacterial communities. Appl Environ Microbiol 72:2022–2030PubMedCrossRefGoogle Scholar
  13. Huss VAR, Festl H, Schleifer KH (1983) Studies on the spectrophotometric determination of DNA hybridization from renaturation rate. Syst Appl Microbiol 4:184–192Google Scholar
  14. Johnson DB, Hallberg KB (2007) Techniques for detecting and identifying acidophilic mineral-oxidizing microorganisms. In: Rawlings DE, Johnson DB (eds) Biomining. Springer, Berlin, pp 237–261CrossRefGoogle 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. Melamud VS, Pivovarova TA, Tourova TP, Kalganova TV, Osipov GA, Lysenko AM, Kondrat’eva TF, Karavaiko GI (2003) Sulfobacillus sibiricus sp. nov., a new moderately thermophilic bacterium. Microbiology (English translation of Mikrobiologiya) 72:605–612Google Scholar
  17. Mikkelsen D, Kappler U, McEwan AG, Sly LI (2006) Archaeal diversity in two thermophilic chalcopyrite bioleaching reactors. Environ Microbiol 8:2050–2056PubMedCrossRefGoogle Scholar
  18. 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
  19. 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
  20. Rawlings DE, Johnson DB (eds) (2007a) Biomining. Springer, BerlinGoogle Scholar
  21. Rawlings DE, Johnson DB (2007b) The microbiology of biomining: development and optimization of mineral-oxidizing microbial consortia. Microbiology 153:315–324PubMedCrossRefGoogle Scholar
  22. Riekkola-Vanhanen M (2007) Talvivaara black schist bioheap-leaching demonstration plant. Adv Mater Res 20–21:30–33Google Scholar
  23. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  24. Schnaitman CA, Korczynski MS, Lundgren DG (1969) Kinetic studies of iron oxidation by whole cells of Ferrobacillus ferrooxidans. J Bacteriol 99:552–557PubMedGoogle Scholar
  25. 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. Nuc Acids Res 25:4876–4882CrossRefGoogle Scholar
  26. Watling HR, Perrot FA, Shiers DW (2008) Comparison of selected characteristics of Sulfobacillus species and review of their occurrence in acidic and bioleaching environments. Hydrometallurgy 93:57–65CrossRefGoogle Scholar
  27. 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

Copyright information

© Springer 2008

Authors and Affiliations

  • D. Barrie Johnson
    • 1
  • Catherine Joulian
    • 2
  • Patrick d’Hugues
    • 2
  • Kevin B. Hallberg
    • 1
  1. 1.School of Biological Sciences, College of Natural SciencesBangor UniversityBangorUK
  2. 2.Bureau des Recherches Géologique et MinièresOrléans Cedex 2France

Personalised recommendations