Abstract
The speciation transformation of elemental sulfur mediated by the leaching bacterium Acidithiobacillus ferrooxidans was investigated using an integrated approach including scanning electron microscopy, transmission electron microscopy, Fourier transform infrared spectroscopy, energy dispersive X-ray spectroscopy, and X-ray absorption near edge spectroscopy (XANES). Our results showed that when grown on elemental sulfur powder, At. ferrooxidans ATCC23270 cells were first attached to sulfur particles and modified the surface sulfur with some amphiphilic compounds. In addition, part of the elemental sulfur powder might be converted to polysulfides. Furthermore, sulfur globules were accumulated inside the cells. XANES spectra of these cells suggested that these globules consisted of elemental sulfur bound to thiol groups of protein.
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Bevilaqua D, Leite ALLC, Garcia O Jr, Tuovinen OH (2002) Oxidation of chalcopyrite by Acidithiobacillus ferrooxidans and Acidithiobacillus thiooxidans in shake flasks. Process Biochem 38:587–592
Bruce DC (1995) Isolation and characterization of sulfur globule proteins from Chromatium vinosum and Thiocapsa roseopersiciana. Arch Microbiol 163:391–399
Devasia P, Natarajan KA, Sathyanarayana DN, Rao GR (1993) Surface chemistry of Thiobacillus ferrooxidans relevant to adhesion on mineral surfaces. Appl Environ Microbiol 59:4051–4055
Fowler TA, Crundwell FK (1999) Leaching of zinc sulfide by Thiobacillus ferrooxidans: bacterial oxidation of the sulfur product layer increases the rate of zinc sulfide dissolution at high concentrations of ferrous ions. Appl Environ Microbiol 12:5285–5292
Friedrich CG, Bardischewsky F, Rother D, Quentmeier A, Fisher J (2005) Prokaryotic sulfur oxidation. Curr Opin Microbiol 8:253–259
George GN, Gnida M, Bazylinski DA, Prince RC, Pickering IJ (2008) X-Ray absorption spectroscopy as a probe of microbial sulfur biochemistry: the nature of bacterial sulfur globules revisited. J Bacteriol 19:6376–6383
Hazeu W, Batenburg-van der Vegte WH, Bos P, van der Pas RK, Kuenen JG (1988) The production and utilization of intermediary elemental sulfur during the oxidation of reduced sulfur compounds by Thiobacillus ferrooxidans. Arch Microbiol 150:574–579
Kanaoa T, Kamimurab K, Sugio T (2007) Identification of a gene encoding a tetrathionate hydrolase in Acidithiobacillus ferrooxidans. J Biotech 132:16–22
Lee YJ, Prange A, Lichtenberg H, Rohde M, Dashti M, Wiegel J (2007) In situ analysis of sulfur species in sulfur globules produced from thiosulfate by Thermoanaerobacter sulfurigignens and Thermoanaerobacterium thermosulfurigenes. J Bacteriol 189:7525–7529
Mangold S, Harneit K, Rohwerder T, Claus G, Sand W (2008) Novel combination of atomic force microscopy and epifluorescence microscopy for visualization of leaching bacteria on pyrite. Appl Environ Microbiol 74:410–415
Pickering IJ, George GN, Eileen YY, Brune DC, Tuschak C, Overmann J, Beatty T, Prince RC (2001) Analysis of sulfur biochemistry of sulfur bacteria using X-ray absorption spectroscopy. Biochemistry 40:8138–8145
Prange A, Arzberger I, Engemann C, Modrow H, Schumann O, Truper HG, Steudel R, Dahl C, Hormes J (1998) In situ analysis of sulfur in the sulfur globules of phototrophic sulfur bacteria by X-ray absorption near edge spectroscopy. Biochim Biophys Acta 1428:446–454
Prange A, Chauvistré R, Modrow H, Trueper HG, Dahl C (2002) Quantitative speciation of sulfur in bacterial sulfur globules: X-ray absorption spectroscopy reveals at least three different species of sulfur. Microbiology 248:267–276
Prange A, Dahl C, Behnke M, Hahn J, Modrow H, Hormes J (2002) Investigation of S-H bonds in biologically important compounds by sulfur K-edge X-ray absorption spectroscopy. Eur Phys J D 20:589–596
Prange A, Dahl C (2006) Bacterial sulfur globules: occurrence, structure and metabolism. In: Steinbüchel A (ed) Microbiology monographs. Springer-Verlag, New York, pp 21–51
Rohwerder T, Gehrke T, Kinzler K, Sand W (2003) Bioleaching review part A: progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation. Appl Microbiol Biotechnol 63:239–248
Rohwerder T, Sand W (2007) Oxidation of inorganic sulfur compounds in acidophilic prokaryotes. Eng Life Sci 7:301–309
Rohwerder T, Sand W (2003) The sulfane sulfur of persulfides is the actual substrate of the sulfur-oxidizing enzymes from Acidithiobacillus and Acidiphilium spp. Microbiology 149:1699–1709
Rojas J, Giersig M, Tributsch H (1995) Sulfur colloids as temporary energy reservoirs for Thiobacillus ferrooxidans during pyrite oxidation. Arch Microbiol 163:352–356
Rompel A, Cinco RM, Latimer MJ, McDermott AE, Guiles RD, Quintanilha A, Krauss RM, Sauer K, Yachandra VK (1998) Sulfur K-edge X-ray absorption spectroscopy: a spectroscopic tool to examine the redox state of S-containing metabolites in vivo. Proc Natl Acad Sci USA 95:6122–6127
Sand W, Gehrke T (2006) Extracellular polymeric substances mediate bioleaching/biocorrosion via interfacial processes involving iron (III) ions and acidophilic bacteria. Res Microbiol 157:49–56
Sharma PK, Das A, Rao KH, Forssberg KSE (2003) Surface characterization of Acidithiobacillus ferrooxidans cells grown under different conditions. Hydrometallurgy 71:285–292
Takeuchi T, Suzuki I (1997) Cell hydrophobicity and sulfur adhesion of Thiobacillus thiooxidans. Appl Environ Microbiol 63:2058–2061
Sugio T, Ochi K, Muraoka T (2005) Isolation and some properties of sulfur dioxygenase from Acidithiobacillus thiooxidans NB1-3. In: Harrison STL, Rawlings DE, Petersen (eds) Proceedings of the 16th International Biohydromet. Symposium, Cape Town, South Africa. Compress, pp 25–29
Wakai A, Kikumoto M, Kanao T, Kamimura K (2004) Involvement of sulfide: quinone oxidoreductase in sulfur oxidation of an acidophilic iron-oxidizing bacterium, Acidithiobacillus ferrooxidans NASF-1. Biosci Biotech Biochem 68:2519–2528
Acknowledgments
This work was supported by the National Natural Science Foundation of China (No. 50674101), the National Basic Research Program of China (No. 2004CB619201), and the Chinese Science Foundation for Distinguished Groups (No. 50621063). The authors are indebted to the staff at the Beijing Synchrotron Radiation Facility (BSRF) medium-energy beam-line station for their generous assistance. Measurements at BSRF were supported by the public user program.
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Huan He and Cheng-Gui Zhang made equal contributions to this paper.
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He, H., Zhang, CG., Xia, JL. et al. Investigation of Elemental Sulfur Speciation Transformation Mediated by Acidithiobacillus ferrooxidans . Curr Microbiol 58, 300–307 (2009). https://doi.org/10.1007/s00284-008-9330-6
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DOI: https://doi.org/10.1007/s00284-008-9330-6