Extremophiles

, Volume 15, Issue 2, pp 271–279 | Cite as

Acidiferrobacter thiooxydans, gen. nov. sp. nov.; an acidophilic, thermo-tolerant, facultatively anaerobic iron- and sulfur-oxidizer of the family Ectothiorhodospiraceae

  • Kevin B. Hallberg
  • Sabrina Hedrich
  • D. Barrie Johnson
Original Paper

Abstract

A comprehensive physiological and phylogenetic characterisation was carried out of “Thiobacillus ferrooxidans” m-1, an acidophilic iron-oxidizing bacterium first described over 25 years ago. Phylogenetically, strain m-1 is a gammaproteobacterium, most closely related to alkaliphilic Ectothiorhodospira spp. and only distantly to iron-oxidizing acidithiobacilli. Physiological examination confirmed that strain m-1 can grow autotrophically not only by ferrous iron oxidation but also, in contrast to previous reports, by oxidation of elemental sulfur, sulfide and tetrathionate, using either oxygen or ferric iron as terminal electron acceptor. The bacterium was also found to be thermo-tolerant, growing optimally at 38°C and up to a maximum of 47°C. Growth in liquid media required an external osmotic potential of >2 bar, and was optimal at ~5 bar, though no growth occurred where the medium osmotic potential was close to that of sea water (~26 bar). From this, it was concluded that strain m-1 is a moderate osmophile. Strain m-1 was also shown to be diazotrophic and tolerant of elevated concentrations of many metals typically found in mine-impacted environments. On the basis of these data, m-1 is proposed as the type strain of a new genus and species of bacteria, Acidiferrobacter thiooxydans (DSM 2392, JCM 17358).

Keywords

Acidophile Diazotroph Iron oxidation Iron reduction Osmophile Sulfur oxidation Thermo-tolerance 

Notes

Acknowledgments

The authors wish to acknowledge financial support for this work from the Biosciences, Environment and Agriculture Alliance (BEAA) between Bangor and Aberystwyth Universities and the European Union (FP7 project “Promine”). DBJ is grateful to the Royal Society for the provision of an Industrial Fellowship. The authors thank Dr. Tadayoshi Kanao, Okayama University Japan, for his contribution to the measurement of specific rates of iron oxidation and Professor Jean Euzéby for his willingness to share his expertise on nomenclature.

Supplementary material

792_2011_359_MOESM1_ESM.doc (128 kb)
Supplementary material 1 (DOC 128 kb)

References

  1. 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
  2. Chun J, Lee JH, Jung Y, Kim M, Kim S, Kim BK, Lim YW (2007) EzTaxon: a web-based tool for the identification of prokaryotes based on 16S ribosomal RNA gene sequences. Int J Syst Evol Microbiol 57:2259–2261PubMedCrossRefGoogle Scholar
  3. Davis-Belmar CS, Nicolle JLC, Norris PR (2008) Ferrous iron oxidation and leaching of copper with halotolerant bacteria in ore columns. Hydrometallurgy 94:144–147CrossRefGoogle Scholar
  4. Galleguillos P, Hallberg KB, Johnson DB (2009) Microbial diversity and genetic response to stress conditions of extremophilic bacteria isolated from the Escondida copper mine. Adv Mat Res 71–73:55–58CrossRefGoogle Scholar
  5. Garcia-Moyano A, Gonzalez-Toril E, Aguilera A, Amils R (2007) Prokaryotic community composition and ecology of floating macroscopic filaments from an extreme acidic environment, Rio Tinto (SW, Spain). Syst Appl Microbiol 30:601–614PubMedCrossRefGoogle Scholar
  6. Hallberg KB, Johnson DB (2007) Isolation, enumeration, growth, and preservation of acidophilic prokaryotes. In: Hurst CJ, Crawford RL, Garland JL, Lipson DA, Mills AL, Stetzenbach LD (eds) Manual of environmental microbiology, 3rd edn. American Society of Microbiology Press, Washington, DC, pp 1155–1165Google Scholar
  7. 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
  8. Hallberg KB, González-Toril E, Johnson DB (2010) Acidithiobacillus ferrivorans, sp. nov.; facultatively anaerobic, psychrotolerant iron-, and sulfur-oxidizing acidophiles isolated from metal mine-impacted environments. Extremophiles 14:9–19PubMedCrossRefGoogle Scholar
  9. Harrison AP Jr (1982) Genomic and physiological diversity amongst strains of Thiobacillus ferrooxidans, and genomic comparison with Thiobacillus thiooxidans. Arch Microbiol 131:68–76CrossRefGoogle Scholar
  10. Harrison AP Jr (1984) The acidophilic thiobacilli and other acidophilic bacteria that share their habitat. Annu Rev Microbiol 38:265–292PubMedCrossRefGoogle Scholar
  11. He Z, Xie XH, He ZG, Xiao SM, Liu JS (2007) Microbial diversity of mine water at Zhong Tiaoshan copper mine, China. J Basic Microbiol 47:485–495PubMedCrossRefGoogle Scholar
  12. Imhoff JF (2006) The family Ectothiorhodospiraceae. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) The prokaryotes: a handbook on the biology of bacteria, vol 6, 3rd edn. Springer, New York, pp 874–886Google Scholar
  13. 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
  14. Johnson DB, Hallberg KB (2008) Carbon, iron and sulfur metabolism in acidophilic micro-organisms. Adv Microb Physiol 54:202–256Google Scholar
  15. Johnson DB, Bacelar-Nicolau P, Okibe N, Thomas A, Hallberg KB (2009) 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 59:1082–1089PubMedCrossRefGoogle Scholar
  16. Kelly DP, Wood AP (2000) Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen. nov., Halothiobacillus gen. nov. and Thermithiobacillus gen. nov. Int J Syst Evol Microbiol 50:511–516PubMedCrossRefGoogle Scholar
  17. Kelly DP, Chambers LA, Trudinger PA (1969) Cyanolysis and spectrophotometric estimation of trithionate in mixture with thiosulfate and tetrathionate. Anal Chem 41:898–902CrossRefGoogle Scholar
  18. Kolmert Å, Wikström P, Hallberg KB (2000) A fast and simple turbidimetric method for the determination of sulfate in sulfate-reducing bacterial cultures. J Microbiol Methods 41:179–184PubMedCrossRefGoogle Scholar
  19. Lane DJ, Harrison AP, Stahl D, Pace P, Giovannoni SJ, Olsen GJ, Pace NR (1992) Evolutionary relationships among sulfur- and iron-oxidizing eubacteria. J Bacteriol 174:269–278PubMedGoogle Scholar
  20. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948PubMedCrossRefGoogle Scholar
  21. Lovley DR, Phillips EJP (1987) Rapid assay for microbially reducible ferric iron in aquatic sediments. Appl Environ Microbiol 53:1536–1540PubMedGoogle Scholar
  22. Mendez MO, Neilson JW, Maier RM (2008) Characterization of a bacterial community in an abandoned semiarid lead-zinc mine tailing site. Appl Environ Microbiol 74:3899–3907PubMedCrossRefGoogle Scholar
  23. Mitchell D, Harneit K, Meyer G, Sand W, Stackebrandt E (2004) Systematic analysis of our culture collection for “genospecies” of Acidithiobacillus ferrooxidans, Acidithiobacillus thiooxidans and Leptospirillum ferrooxidans. In: Ciminelli VST, Garcia O Jr (eds) Biohydrometallurgy: fundamentals, technology and sustainable development. Elsevier, Amsterdam, pp 1369–1378Google Scholar
  24. Ñancucheo I, Johnson DB (2010) Production of glycolic acid by chemolithotrophic iron- and sulfur-oxidizing bacteria and its role in delineating and sustaining acidophilic sulfide mineral-oxidizing consortia. Appl Environ Microbiol 76:461–467PubMedCrossRefGoogle Scholar
  25. 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
  26. Schippers A, Sand W (1999) Bacterial leaching of metal sulfides proceeds by two indirect mechanisms via thiosulfate or via polysulfides and sulfur. Appl Environ Microbiol 65:319–321PubMedGoogle Scholar
  27. Tourova TP, Spiridonova EM, Berg IA, Slobodova NV, Boulygina ES, Sorokin DY (2007) Phylogeny and evolution of the family Ectothiorhodospiraceae based on comparison of 16S rRNA, cbbL and nifH gene sequences. Int J Syst Evol Microbiol 57:2387–2398PubMedCrossRefGoogle Scholar
  28. Ueda T, Suga Y, Yahiro N, Matsuguchi T (1995) Remarkable N2-fixing bacterial diversity detected in rice roots by molecular evolutionary analysis of nifH gene sequences. J Bacteriol 177:1414–1417PubMedGoogle Scholar
  29. Wakeman K, Auvinen H, Johnson DB (2008) Microbiological and geochemical dynamics in simulated heap leaching of a polymetallic sulfide ore. Biotechnol Bioeng 101:739–750PubMedCrossRefGoogle Scholar
  30. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2011

Authors and Affiliations

  • Kevin B. Hallberg
    • 1
  • Sabrina Hedrich
    • 1
  • D. Barrie Johnson
    • 1
  1. 1.School of Biological Sciences, College of Natural SciencesBangor UniversityBangorUK

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