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Evidence of cell surface iron speciation of acidophilic iron-oxidizing microorganisms in indirect bioleaching process

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Abstract

While indirect model has been widely accepted in bioleaching, but the evidence of cell surface iron speciation has not been reported. In the present work the iron speciation on the cell surfaces of four typically acidophilic iron-oxidizing microorganism (mesophilic Acidithiobacillus ferrooxidans ATCC 23270, moderately thermophilic Leptospirillum ferriphilum YSK and Sulfobacillus thermosulfidooxidans St, and extremely thermophilic Acidianus manzaensis YN25) grown on different energy substrates (chalcopyrite, pyrite, ferrous sulfate and elemental sulfur (S0)) were studied in situ firstly by using synchrotron-based micro- X-ray fluorescence analysis and X-ray absorption near-edge structure spectroscopy. Results showed that the cells grown on iron-containing substrates had apparently higher surface iron content than the cells grown on S0. Both ferrous iron and ferric iron were detected on the cell surface of all tested AIOMs, and the Fe(II)/Fe(III) ratios of the same microorganism were affected by different energy substrates. The iron distribution and bonding state of single cell of A. manzaensis were then studied in situ by scanning transmission soft X-ray microscopy based on dual-energy contrast analysis and stack analysis. Results showed that the iron species distributed evenly on the cell surface and bonded with amino, carboxyl and hydroxyl groups.

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References

  • Bonnefoy V (2010) Bioinformatics and genomics of iron- and sulfur-oxidizing acidophiles. In: Barton LL, Mandl M, Loy A (eds) Geomicrobiology: molecular and environmental perspective. Springer, Berlin, pp 169–192

    Chapter  Google Scholar 

  • Brierley CL (2010) Biohydrometallurgical prospects. Hydrometallurgy 104:324–328

    Article  CAS  Google Scholar 

  • Chi A, Valenzuela L, Beard S, Mackey AJ, Shabanowitz J, Hunt DF, Jerez C (2007) Periplasmic proteins of the extremophile Acidithiobacillus ferrooxidans. Mol Cell Proteomics 6:2239–2251

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Crundwell FK (2003) How do bacteria interact with minerals? Hydrometallurgy 71:75–81

    Article  CAS  Google Scholar 

  • Ding JN, Gao J, Wu XL, Zhang CG, Wang DZ, Qiu GZ (2007) Jarosite-type precipitates mediated by YN22, Sulfobacillus thermosulfidooxidans, and their influences on strain. Trans Nonferrous Met Soc China 17:1038–1044

    Article  CAS  Google Scholar 

  • Emerson D, Fleming EJ, McBeth JM (2010) Iron-oxidizing bacteria: an environmental and genomic perspective. Annu Rev Microbiol 64:561–583

    Article  CAS  PubMed  Google Scholar 

  • Flemming HC, Wingnder J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633

    CAS  PubMed  Google Scholar 

  • Gehrke T, Telegdi J, Thierry D, Sand W (1998) Importance of extracellular polymeric substances from Thiobacillus ferrooxidans for bioleaching. Appl Environ Microbiol 64:2743–2747

    CAS  PubMed Central  PubMed  Google Scholar 

  • He H, Xia JL, Jiang HC, Yan Y, Liang CL, Ma CY, Zheng L, Zhao YD, Qiu GZ (2010) Sulfur species investigation in extra- and intracellular sulfur globules of Acidithiobacillus ferrooxidans and Acidithiobacillus caldus. Geomicrobiol J 27:707–713

    Article  CAS  Google Scholar 

  • Ide-Ektessabi A, Kawakami T, Watt F (2004) Distribution and chemical state analysis of iron in the Parkinsonian substantia nigra using synchrotron radiation micro beams. Nucl Instrum Meth B 213:590–594

    Article  CAS  Google Scholar 

  • Katsikini M, Pinakidou F, Mavromati E, Paloura EC, Gioulekas D, Grolimund D (2010) Fe distribution and speciation in human nails. Nucl Instrum Meth B 268:420–424

    Article  CAS  Google Scholar 

  • Lai B, Yun W, Xiao Y, Yang L, Legnini D, Cai Z, Krasnoperova A, Cerrina F, DiFabrizio E, Grella L, Gentili M (1995) Development of a hard x-ray imaging microscope. Rev Sci Instrum 66:2287–2289

    Article  CAS  Google Scholar 

  • Li Y, Kawashima N, Li J, Chandra AP, Gerson AR (2013) A review of the structure, and fundamental mechanisms and kinetics of the leaching of chalcopyrite. Adv Colloid Interface 197–198:1–32

    Google Scholar 

  • Liu HC, Xia JL, Nie ZY, Peng AA, Ma CY, Zheng L, Zhao YD (2013) Comparative study of sulfur utilization and speciation transformation of two elemental sulfur species by thermoacidophilic Archaea Acidianus manzaensis YN-25. Process Biochem 48:1855–1860

    Article  CAS  Google Scholar 

  • Lobinski R, Moulin C, Ortega R (2006) Imaging and speciation of trace elements in biological environment. Biochimie 88:1591–1604

    Article  CAS  PubMed  Google Scholar 

  • Melcher F, Oberthür T, Rammlmair D (2006) Geochemical and mineralogical distribution of germanium in the Khusib Springs Cu–Zn–Pb–Ag sulfide deposit, Otavi Mountain Land, Namibia. Ore Geol Rev 28:32–56

    Article  Google Scholar 

  • Mosselmans J, Pattrick R, Van der Laan G, Charnock J, Vaughan D, Henderson C, Garner CD (1995) X-ray absorption near-edge spectra of transition metal disulfides FeS2 (pyrite and marcasite), CoS2, NiS2 and CuS2, and their isomorphs FeAsS and CoAsS. Phys Chem Miner 22:311–317

    Article  CAS  Google Scholar 

  • Nie ZY, Liu HC, Xia JL, Zhu HR, Ma CY, Zheng L, Zhao YD, Qiu GZ (2014) Differential utilization and transformation of sulfur allotropes, μ-S and α-S8, by moderate thermoacidophile Sulfobacillus thermosulfidooxidans. Res Microbiol 165:639–646

    Article  CAS  PubMed  Google Scholar 

  • Peng AA, Xia JL, Liu HC, Nie ZY, Yang Y, Zhu W (2014) Differential utilization of cyclic, orthorhombic α and chain-like polymeric μ-sulfur by Acidithiobacillus ferrooxidans. Trans Nonferrous Met Soc China 24:1562–1570

    Article  CAS  Google Scholar 

  • Pradhan N, Nathsarma KC, Srinivasa Rao K, Sukla LB, Mishra BK (2008) Heap bioleaching of chalcopyrite: a review. Miner Eng 21:355–365

    Article  CAS  Google Scholar 

  • Prange A (2008) Speciation analysis of microbiologically produced sulfur by X-ray absorption near edge structure spectroscopy. In: Dahl C, Friedrich C (eds) Microbial sulfur metabolism. Springer, Berlin, pp 259–272

    Chapter  Google Scholar 

  • Quatrini R, Appia-Ayme C, Denis Y, Jedlicki E, Holmes DS, Bonnefoy V (2009) Extending the models for iron and sulfur oxidation in the extreme Acidophile Acidithiobacillus ferrooxidans. BMC Genom 10:394

    Article  Google Scholar 

  • Ravel B, Newville M (2005) ATHENA, ARTEMIS, HEPHAESTUS: data analysis for X-ray absorption spectroscopy using IFEFFIT. J Synchrotron Radiat 12:537–541

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sand W, Gehrke T, Hallmann R, Schippers A (1995) Sulfur chemistry, biofilm, and the (in)direct attack mechanism—a critical evaluation of bacterial leaching. Appl Microbiol Biotechnol 43:961–966

    Article  CAS  Google Scholar 

  • Schippers A, Sand W (1999) Bacterial leaching of metal sulfides proceeds by two indirect mechanisms via thiosulfate or via polysulfides and sulfur. Appl Microbiol Biotechnol 65:319–321

    CAS  Google Scholar 

  • Thole B, Van der Laan G (1988) Branching ratio in x-ray absorption spectroscopy. Phys Rev B 38:3158

    Article  CAS  Google Scholar 

  • Valdés J, Pedroso I, Quatrini R, Dodson RJ, Tettelin H, Blake R, Eisen JA, Holmes DS (2008) Acidithiobacillus ferrooxidans metabolism: from genome sequence to industrial applications. BMC Genom 9:597

    Article  Google Scholar 

  • Van Aken P, Liebscher B (2002) Quantification of ferrous/ferric ratios in minerals: new evaluation schemes of Fe L 23 electron energy-loss near-edge spectra. Phys Chem Miner 29:188–200

    Article  Google Scholar 

  • Van der Laan G, Kirkman I (1992) The 2p absorption spectra of 3d transition metal compounds in tetrahedral and octahedral symmetry. J Phys-Condens Mat 4:4189

    Article  Google Scholar 

  • Vera M, Schippers A, Sand W (2013) Progress in bioleaching: fundamentals and mechanisms of bacterial metal sulfide oxidation—part A. Appl Microbiol Biotechnol 97:7529–7541

    Article  CAS  PubMed  Google Scholar 

  • Wang HJ, Wang M, Wang B, Meng XY, Wang Y, Li M, Feng WY, Zhao YL, Chai ZF (2010) Quantitative imaging of element spatial distribution in the brain section of a mouse model of Alzheimer’s disease using synchrotron radiation X-ray fluorescence analysis. J Anal At Spectrom 25:328

    Article  CAS  Google Scholar 

  • Wang ZW, Zhang LJ, Guo Z, Liu L, Ji J, Zhang JN, Chen XH, Liu BY, Zhang J, Ding QL, Wang XF, Zhao W, Zhu ZG, Yu YY (2012) A unique feature of iron loss via close adhesion of Helicobacter pylori to host erythrocytes. PLoS ONE 7:e50314

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xia JL, Liu HC, Nie ZY, Peng AA, Zhen XJ, Yang Y, Zhang XL (2013) Synchrotron radiation based STXM analysis and micro-XRF mapping of differential expression of extracellular thiol groups by Acidithiobacillus ferrooxidans grown on Fe2+ and S0. J Microbiol Meth 94:257–261

    Article  CAS  Google Scholar 

  • Xue CF, Wang Y, Guo Z, Wu YQ, Zhen XJ, Chen M, Chen JH, Xue S, Peng ZQ, Lu QP, Tai RZ (2010) High-performance soft X-ray spectromicroscopy beamline at SSRF. Rev Sci Instrum 81:103502

    Article  PubMed  Google Scholar 

  • Yang Y, Liu W, Chen M (2013) A copper and iron K-edge XANES study on chalcopyrite leached by mesophiles and moderate thermophiles. Miner Eng 48:31–35

    Article  CAS  Google Scholar 

  • Zhang CG, Zhang RY, Xia JL, Zhang Q, Nie ZY (2008) Sulfur activation-related extracellular proteins of Acidithiobacillus ferrooxidans. Trans Nonferrous Met Soc China 18:1398–1402

    Article  CAS  Google Scholar 

  • Zhang XZ, Xu ZJ, Tai RZ, Zhen XJ, Wang Y, Guo Z, Yan R, Chang R, Wang B, Li M, Zhao J, Gao F (2010) Ratio-contrast imaging of dual-energy absorption for element mapping with a scanning transmission X-ray microscope. J Synchrotron Radiat 17:804–809

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to the staff at beamlines BL08U1A and BL15U1 of Shanghai Synchrotron Radiation Facility (SSRF) for their help in beamlines operation and data collection. This work is supported by the National Natural Science Foundation of China (Grant No.51274257), the Joint Funds of National Natural Science Foundation of China and Large Scientific Facility Foundation of Chinese Academy of Sciences (Grant No.U1232103), and the Open Funds of SSRF, Shanghai Institute of Applied Physics, Chinese Academy of Sciences, Shanghai, China (Grants No. 13SRBL08U1A3016, Z13sr0026, 13SRBL15U13024, and 13SRBL15U15653).

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Correspondence to Jin-lan Xia.

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Zhen-yuan Nie and Hong-chang Liu have equally contributed to this work.

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Nie, Zy., Liu, Hc., Xia, Jl. et al. Evidence of cell surface iron speciation of acidophilic iron-oxidizing microorganisms in indirect bioleaching process. Biometals 29, 25–37 (2016). https://doi.org/10.1007/s10534-015-9893-1

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  • DOI: https://doi.org/10.1007/s10534-015-9893-1

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