Applied Microbiology and Biotechnology

, Volume 102, Issue 9, pp 4217–4229 | Cite as

The biomineralization process of uranium(VI) by Saccharomyces cerevisiae — transformation from amorphous U(VI) to crystalline chernikovite

  • Yanghao Shen
  • Xinyan Zheng
  • Xiaoyu Wang
  • Tieshan Wang
Environmental biotechnology
First Online:
Received:
Revised:
Accepted:
  • 100 Downloads

Abstract

Microorganisms play a significant role in uranium(VI) biogeochemistry and influence U(VI) transformation through biomineralization. In the present work, the process of uranium mineralization was investigated by Saccharomyces cerevisiae. The toxicity experiments showed that the viability of cell was not significantly affected by 100 mg L−1 U(VI) under 4 days of exposure time. The batch experiments showed that the phosphate concentration and pH value increased over time during U(VI) adsorption. Meanwhile, thermodynamic calculations demonstrated that the adsorption system was supersaturated with respect to UO2HPO4. The X-ray powder diffraction spectroscopy (XRD), field emission scanning electron microscopy (FE-SEM) equipped with energy dispersive spectroscopy (EDX), Fourier transform infrared spectroscopy (FTIR), and X-ray photoelectron spectroscopy (XPS) analyses indicated that the U(VI) was first attached onto the cell surface and reacted with hydroxyl, carboxyl, and phosphate groups through electrostatic interactions and complexation. As the immobilization of U(VI) transformed it from the ionic to the amorphous state, lamellar uranium precipitate was formed on the cell surface. With the prolongation of time, the amorphous uranium compound disappeared, and there were some crystalline substances observed extracellularly, which were well-characterized as tetragonal-chernikovite. Furthermore, the size of chernikovite was regulated at nano-level by cells, and the perfect crystal was formed finally. These findings provided an understanding of the non-reductive transformation process of U(VI) from the amorphous to crystalline state within microbe systems, which would be beneficial for the U(VI) treatment and reuse of nuclides and heavy metals.

Keywords

Biomineralization Uranium(VI) Saccharomyces cerevisiae Nano-chernikovite Transformation 
This is a preview of subscription content, log in to check access

Notes

Acknowledgements

This study was supported by the Fundamental Research Funds for the Central Universities (Grant Number: lzujbky-2017-it37). The authors also acknowledge Fanrui Kong, Yu Luo, and Chen Zeng, for the great help in designing the cellular graphics, thermodynamic calculations, and English proofreading of this manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Achbergerová L, Nahálka J (2011) Polyphosphate—an ancient energy source and active metabolic regulator. Microb Cell Factories 10:63.  https://doi.org/10.1186/1475-2859-10-63 CrossRefGoogle Scholar
  2. Asic A, Kurtovic-kozaric A, Besic L, Mehinovic L, Hasic A, Kozaric M, Hukic M, Marjanovicaf D (2017) Chemical toxicity and radioactivity of depleted uranium: the evidence from in vivo and in vitro studies. Environ Res 156:665–673.  https://doi.org/10.1016/j.envres.2017.04.032 CrossRefPubMedGoogle Scholar
  3. Barrett CA, Chouyyok W, Speakman RJ, Olsen KB, Addleman RS (2017) Rapid extraction and assay of uranium from environmental surface samples. Talanta 173:69–78.  https://doi.org/10.1016/j.talanta.2017.05.052
  4. Bernier-Latmani R, Veeramani H, Vecchia ED, Junier P, Lezama-Pacheco JS, Suvorova EI, Sharp JO, Wigginton NS, Bargar JR (2010) Non-uraninite products of microbial U(VI) reduction. Environ Sci Technol 44:9456–9462.  https://doi.org/10.1021/es101675a CrossRefPubMedGoogle Scholar
  5. Bjørklund G, Christophersen OA, Chirumbolo S, Selinus O, Aaseth J (2017) Recent aspects of uranium toxicology in medical geology. Environ Res 156:526–533.  https://doi.org/10.1016/j.envres.2017.04.010 CrossRefPubMedGoogle Scholar
  6. Boyanov MI, Latta DE, Scherer MM, O'Loughlin EJ, Kemner KM (2017) Surface area effects on the reduction of UVI in the presence of synthetic montmorillonite. Chem Geol 464:110–117.  https://doi.org/10.1016/j.chemgeo.2016.12.016 CrossRefGoogle Scholar
  7. Clavier N, Crétaz F, Szenknect S, Mesbah A, Poinssot C, Descostes M, Dacheux N (2016) Vibrational spectroscopy of synthetic analogues of ankoleite, chernikovite and intermediate solid solution. Spectrochim Acta A 156:143–150.  https://doi.org/10.1016/j.saa.2015.11.035 CrossRefGoogle Scholar
  8. Cumberland SA, Douglas G, Grice K, Moreau JW (2016) Uranium mobility in organic matter-rich sediments: a review of geological and geochemical processes. Earth-Sci Rev 159:160–185.  https://doi.org/10.1016/j.earscirev.2016.05.010 CrossRefGoogle Scholar
  9. Du ZJ, Zhang Y, Li ZJ, Chen H, Wang Y, Wang GT, Zou P, Chen HP, Zhang YS (2017) Facile one-pot fabrication of nano-Fe3O4/carboxyl-functionalized baker's yeast composites and their application in methylene blue dye adsorption. Appl Surf Sci 392:312–320.  https://doi.org/10.1016/j.apsusc.2016.09.050 CrossRefGoogle Scholar
  10. Fabrizio P, Longo VD (2003) The chronological life span of Saccharomyces cerevisiae. Aging Cell 2:73–81.  https://doi.org/10.1046/j.1474-9728.2003.00033.x CrossRefPubMedGoogle Scholar
  11. Fleet GH, Manners DJ (1976) Isolation and composition of an alkali-soluble glucan from the cell walls of Saccharomyces cerevisiae. J Gen Microbiol 94:180–192.  https://doi.org/10.1099/00221287-94-1-180 CrossRefPubMedGoogle Scholar
  12. Galichet A, Sockalingum GD, Belarbi A, Manfait M (2001) FTIR spectroscopic analysis of Saccharomyces cerevisiae cell walls: study of an anomalous strain exhibiting a pink-colored cell phenotype. FEMS Microbiol Lett 197:179–186.  https://doi.org/10.1016/S0378-1097(01)00101-X CrossRefPubMedGoogle Scholar
  13. Ganesh R, Robinson KG, Reed GD, Sayler GS (1997) Reduction of hexavalent uranium from organic complexes by sulfate- and iron-reducing bacteria. Appl Environ Microbiol 63:4385–4391PubMedPubMedCentralGoogle Scholar
  14. Ganesh S, Khan F, Ahmed MK, Velavendan P, Pandey NK, Mudali UK, Pandey SK (2012) Determination of ultra traces amount of uranium in raffinates of Purex process by laser fluorimetry. J Radioanal Nucl Chem 292:331–334.  https://doi.org/10.1007/s10967-011-1431-1 CrossRefGoogle Scholar
  15. Gilson ER, Huang S, Jaffé PR (2015) Biological reduction of uranium coupled with oxidation of ammonium by Acidimicrobiaceae bacterium A6 under iron reducing conditions. Biodegradation 26:475–482.  https://doi.org/10.1007/s10532-015-9749-y CrossRefPubMedGoogle Scholar
  16. Goksungur Y, Uren S, Guvenc U (2005) Biosorption of cadmium and lead ions by ethanol treated waste baker’s yeast biomass. Bioresour Technol 96:103–109.  https://doi.org/10.1016/j.biortech.2003.04.002
  17. Gorman-Lewis D, Burns PC, Fein JB (2008) Review of uranyl mineral solubility measurements. J Chem Thermodyn 40:335–352.  https://doi.org/10.1016/j.jct.2007.12.004 CrossRefGoogle Scholar
  18. Grenthe I, Fuger J, Konings RJM, Lemire RJ, Muller AB, Nguyen-Trung C, Wanner H (1992) Chemical thermodynamics of uranium. Elsevier, Amsterdam, pp 605–606Google Scholar
  19. Gu BH, Wu WM, Ginder-Vogel MA, Yan H, Fields MW, Zhou JZ, Fendorf S, Criddle CS, Jardine PM (2005) Bioreduction of uranium in a contaminated soil column. Environ Sci Technol 39:4841–4847.  https://doi.org/10.1021/es050011y CrossRefPubMedGoogle Scholar
  20. Haverbeke LV, Vochte R, Springe KV (1996) Solubility and spectrochemical characteristics of synthetic chernikovite and meta-ankoleite. Mineral Mag 60:759–766.  https://doi.org/10.1180/minmag.1996.060.402.05 CrossRefGoogle Scholar
  21. Huang WB, Cheng WC, Nie XQ, Dong FQ, Ding CC Liu MX, Li Z, Hayat T, Alharbi NS (2017) Microscopic and spectroscopic insights into uranium phosphate mineral precipitated by Bacillus mucilaginosus. ACS Earth Space Chem 1:483–492.  https://doi.org/10.1021/acsearthspacechem.7b00060 CrossRefGoogle Scholar
  22. Istok JD, Senko JM, Krumholz LR, Watson D, Bogle MA, Peacock A, Chang YJ, White DC (2004) In situ bioreduction of technetium and uranium in a nitrate-contaminated aquifer. Environ Sci Technol 38:468–475.  https://doi.org/10.1021/es034639p CrossRefPubMedGoogle Scholar
  23. Johnson J (2000) Geochemist’s workbench, database thermocom Lawrence Livermore National Laboratory, Livermore, California V8R6230Google Scholar
  24. Kushwaha S, Sreedhar B, Padmaja P (2012) XPS, EXAFS, and FTIR as tools to probe the unexpected adsorption-coupled reduction of U(VI) to U(V) and U(IV) on Borassus flabellifer-based adsorbents. Langmuir 28:16038–16048.  https://doi.org/10.1021/la3013443 CrossRefPubMedGoogle Scholar
  25. Lee SY, Cha WS, Kim J-G, Baik MH, Jung EC, Jeong JT, Kim K, Chung SY, Lee YJ (2014) Uranium(IV) remobilization under sulfate reducing conditions. Chem Geol 370:40–48.  https://doi.org/10.1016/j.chemgeo.2014.01.020 CrossRefGoogle Scholar
  26. Li FZ, Li DM, Li XL, Liao JL, Li SJ, Yang JJ, Yang YY, Tang J, Liu N (2016) Microorganism-derived carbon microspheres for uranium removal from aqueous solution. Chem Eng J 284:630–639.  https://doi.org/10.1016/j.cej.2015.09.015 CrossRefGoogle Scholar
  27. Li JQ, Gong LL, Feng XF, Zhang L, Wu HQ, Yan CS, Xiong YY, Gao HY, Luo F (2017) Direct extraction of U(VI) from alkaline solution and seawater via anion exchange by metal-organic framework. Chem Eng J 316:154–159.  https://doi.org/10.1016/j.cej.2017.01.046 CrossRefGoogle Scholar
  28. Liang K, Ricco R, Doherty CM, Styles MJ, Bell S, Kirby N, Mudie S, Haylock D, Hill AJ, Doonan CJ, Falcaro P (2015a) Biomimetic mineralization of metal-organic frameworks as protective coatings for biomacromolecules. Nat Commun 6:1–8.  https://doi.org/10.1038/ncomms8240 Google Scholar
  29. Liang XJ, Hillier S, Pendlowski H, Gray N, Ceci A, Gadd GM (2015b) Uranium phosphate biomineralization by fungi. Environ Microbiol 17:2064–2075.  https://doi.org/10.1111/1462-2920.12771 CrossRefPubMedGoogle Scholar
  30. Liang XJ, Csetenyi L, Gadd GM (2016) Uranium bioprecipitation mediated by yeasts utilizing organic phosphorus substrates. Appl Microbiol Biotechnol 100:5141–5151.  https://doi.org/10.1007/s00253-016-7327-9 CrossRefPubMedGoogle Scholar
  31. Liu MX, Dong FQ, Yan XY, Zeng WM, Hou LY, Pang XF (2010) Biosorption of uranium by Saccharomyces cerevisiae, and surface interactions under culture conditions. Bioresour Technol 101:8573–8580.  https://doi.org/10.1016/j.biortech.2010.06.063 CrossRefPubMedGoogle Scholar
  32. Lovley DR, Phillips EJ (1992) Reduction of uranium by Desulfovibrio desulfuricans. Appl Environ Microbiol 58:850–856PubMedPubMedCentralGoogle Scholar
  33. Lu X, Zhou XJ, Wang TS (2013) Mechanism of uranium(VI) uptake by Saccharomyces cerevisiae, under environmentally relevant conditions: batch, HRTEM, and FTIR studies. J Hazard Mater 262:297–303.  https://doi.org/10.1016/j.jhazmat.2013.08.051 CrossRefPubMedGoogle Scholar
  34. Macaskie LE, Empson RM, Cheetham AK, Grey CP, Skarnulis AJ (1992) Uranium bioaccumulation by a Citrobacter sp as a result of enzymically mediated growth of polycrystalline HUO2PO4. Science 257:782–784.  https://doi.org/10.1126/science.1496397 CrossRefPubMedGoogle Scholar
  35. Martinez RJ, Beazley MJ, Taillefert M, Arakaki AK, Skolnick J, Sobecky PA (2007) Aerobic uranium (VI) bioprecipitation by metal-resistant bacteria isolated from radionuclide and metal-contaminated subsurface soils. Environ Microbiol 9:3122–3133.  https://doi.org/10.1111/j.1462-2920.2007.01422.x CrossRefPubMedGoogle Scholar
  36. Mehta VS, Maillot F, Wang ZM, Catalano JG, Giammar DE (2014) Effect of co-solutes on the products and solubility of uranium(VI) precipitated with phosphate. Chem Geol 364:66–75.  https://doi.org/10.1016/j.chemgeo.2013.12.002 CrossRefGoogle Scholar
  37. Merroun ML, Nedelkova M, Ojeda JJ, Reitz T, Fernández ML, Arias JM, Romero-González M, Selenska-Pobella S (2011) Bio-precipitation of uranium by two bacterial isolates recovered from extreme environments as estimated by potentiometric titration, TEM and X-ray absorption spectroscopic analyses. J Hazard Mater 197:1–10.  https://doi.org/10.1016/j.jhazmat.2011.09.049 CrossRefPubMedGoogle Scholar
  38. Moon EM, Ogden MD, Griffith CS, Wilson A, Mata JP (2017) Impact of chloride on uranium(VI) speciation in acidic sulfate ion exchange systems: towards seawater-tolerant mineral processing circuits. J Ind Eng Chem 51:255–263.  https://doi.org/10.1016/j.jiec.2017.03.009 CrossRefGoogle Scholar
  39. Newsome L, Morris K, Trivedi D, Bewsher A, Lloyd JR (2015) Biostimulation by glycerol phosphate to precipitate recalcitrant uranium(IV) phosphate. Environ Sci Technol 49:11070–11078.  https://doi.org/10.1021/acs.est.5b02042 CrossRefPubMedGoogle Scholar
  40. Ohnuki T, Ozaki T, Yoshida T, Sakamoto F, Kozai N, Wakai E, Francis AJ, Iefuji H (2005) Mechanisms of uranium mineralization by the yeast Saccharomyces cerevisiae. Geochim Cosmochim Acta 69:5307–5316.  https://doi.org/10.1016/j.gca.2005.06.023 CrossRefGoogle Scholar
  41. Pan XH, Chen Z, Chen FB, Cheng YJ, Lin Z, Guan X (2015) The mechanism of uranium transformation from U(VI) into nano-uramphite by two indigenous Bacillus thuringiensis strains. J Hazard Mater 297:313–319.  https://doi.org/10.1016/j.jhazmat.2015.05.019 CrossRefPubMedGoogle Scholar
  42. Pande S, Kumar Ghosh S, Nath S, Praharaj S, Jana S, Panigrahi S, Basu S, Pal T (2006) Reduction of methylene blue by thiocyanate: kinetic and thermodynamic aspects. J Colloid Interf Sci 299:421–427.  https://doi.org/10.1016/j.jcis.2006.01.052 CrossRefGoogle Scholar
  43. Pidchenko I, Kvashnina KO, Yokosawa T, Finck N, Bahl S, Schild D, Polly R, Bohnert E, Rossberg A, Göttlicher J, Dardenne K, Rothe J, Schäfer T, Geckeis H, Vitova T (2017) Uranium redox transformations after U(VI) coprecipitation with magnetite nanoparticles. Environ Sci Technol 51:2217–2225.  https://doi.org/10.1021/acs.est.6b04035 CrossRefPubMedGoogle Scholar
  44. Pierrefite-Carle V, Santucci-Darmanin S, Breuil V, Gritsaenko T, Vidaud C, Creff G, Solari PL, Pagnotta S, Al-Sahlanee R, Auwer CD, Carle GF (2017) Effect of natural uranium on the UMR-106 osteoblastic cell line: impairment of the autophagic process as an underlying mechanism of uranium toxicity. Arch Toxicol 91:1903–1914.  https://doi.org/10.1007/s00204-016-1833-5 CrossRefPubMedGoogle Scholar
  45. Rui X, Kwon MJ, O’Loughlin EJ, Dunham-Cheatham S, Fein JB, Bunker B, Kemner KM, Boyanov MI (2013) Bioreduction of hydrogen uranyl phosphate: mechanisms and U(IV) products. Environ Sci Technol 47:5668–5678.  https://doi.org/10.1021/es305258p CrossRefPubMedGoogle Scholar
  46. Schulte-Herbrüggen HMA, Semião AJC, Chaurand P, Graham MC (2016) Effect of pH and pressure on uranium removal from drinking water using NF/RO membranes. Environ Sci Technol 50:5817–5824.  https://doi.org/10.1021/acs.est.5b05930 CrossRefPubMedGoogle Scholar
  47. Shelobolina ES, Konishi H, Xu HF, Roden EE (2009) U(VI) sequestration in hydroxyapatite produced by microbial glycerol 3-phosphate metabolism. Appl Environ Microbiol 75:5773–5778.  https://doi.org/10.1128/AEM.00628-09 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Shyla B, Mahadevaiah, Nagendrappa G (2011) A simple spectrophotometric method for the determination of phosphate in soil, detergents, water, bone and food samples through the formation of phosphomolybdate complex followed by its reduction with thiourea. Spectrochim Acta A 78:497–502.  https://doi.org/10.1016/j.saa.2010.11.017 CrossRefGoogle Scholar
  49. Singhal P, Jha SK, Pandey SP, Neogy S (2017) Rapid extraction of uranium from sea water using Fe3O4 and humic acid coated Fe3O4 nanoparticles. J Hazard Mater 335:152–161.  https://doi.org/10.1016/j.jhazmat.2017.04.043 CrossRefPubMedGoogle Scholar
  50. Sousa T, Chung AP, Pereira A, Piedade AP, Morais PV (2013) Aerobic uranium immobilization by Rhodanobacter A2-61 through formation of intracellular uranium-phosphate complexes. Metallomics 5:390–397.  https://doi.org/10.1039/c3mt00052d CrossRefPubMedGoogle Scholar
  51. Sun YB, Zhang R, Ding CC, Wang XX, Cheng WC, Chen CL, Wang XK (2016) Adsorption of U(VI) on sericite in the presence of Bacillus subtilis: a combined batch, EXAFS and modeling techniques. Geochim Cosmochim Acta 180:51–65.  https://doi.org/10.1016/j.gca.2016.02.012 CrossRefGoogle Scholar
  52. Theodorakopoulos N, Chapon V, Coppin F, Floriani M, Vercouter T, Sergeant C, Camilleri V, Berthomieu C, Février L (2015) Use of combined microscopic and spectroscopic techniques to reveal interactions between uranium and Microbacterium sp A9, a strain isolated from the Chernobyl exclusion zone. J Hazard Mater 285:285–293.  https://doi.org/10.1016/j.jhazmat.2014.12.018 CrossRefPubMedGoogle Scholar
  53. Wadgaonkar SL, Mal J, Nancharaiah YV, Maheshwari NO, Esposito G, Lens PNL (2018) Formation of Se(0), Te(0), and Se(0)-Te(0) nanostructures during simultaneous bioreduction of selenite and tellurite in a UASB reactor. Appl Microbiol Biotechnol 102:2899–2911.  https://doi.org/10.1007/s00253-018-8781-3
  54. Wang JL, Chen C (2006) Biosorption of heavy metals by Saccharomyces cerevisiae: a review. Biotechnol Adv 24:427–451.  https://doi.org/10.1016/j.biotechadv.2006.03.001 CrossRefPubMedGoogle Scholar
  55. Wang TS, Zheng XY, Wang XY, Lu X, Shen YH (2017a) Different biosorption mechanisms of uranium(VI) by live and heat-killed Saccharomyces cerevisiae under environmentally relevant conditions. J Environ Radioact 167:92–99.  https://doi.org/10.1016/j.jenvrad.2016.11.018 CrossRefPubMedGoogle Scholar
  56. Wang XY, Wang TS, Zheng XY, Shen YH, Lu X (2017b) Isotherms, thermodynamic and mechanism studies of removal of low concentration uranium (VI) by Aspergillus niger. Water Sci Technol 75:2727–2736.  https://doi.org/10.2166/wst.2017.055 CrossRefPubMedGoogle Scholar
  57. Watson DB, Wu WM, Mehlhorn T, Tang GP, Earles J, Lowe K, Gihring TM, Zhang GX, Phillips J, Boyanov MI, Spalding BP, Schadt C, Kemner KM, Criddle CS, Jardine PM, Brooks SC (2013) In situ bioremediation of uranium with emulsified vegetable oil as the electron donor. Environ Sci Technol 47:6440–6448.  https://doi.org/10.1021/es3033555 CrossRefPubMedGoogle Scholar
  58. Wu WM, Carley J, Gentry T, Ginder-Vogel MA, Fienen M, Mehlhorn T, Yan H, Caroll S, Pace MN, Nyman J, Luo J, Gentile ME, Fields MW, Hickey RF, Gu BH, Watson D, Cirpka OA, Zhou JZ, Fendorf S, Kitanidis PK, Jardine PM, Criddle CS (2006) Pilot-scale in situ bioremedation of uranium in a highly contaminated aquifer. 2. Reduction of U(VI) and geochemical control of U(VI) bioavailability. Environ Sci Technol 40:3986–3995.  https://doi.org/10.1021/es051960u CrossRefPubMedGoogle Scholar
  59. Wu WM, Carley J, Luo J, Ginder-Vogel MA, Cardenas E, Leigh MB, Hwang CC, Kelly SD, Ruan CM, Wu LY, Joy VN, Gentry T, Lowe K, Mehlhorn T, Carroll S, Luo WS, Fields MW, Gu BH, Watson D, Kemner KM, Marsh T, Tiedje J, Zhou JZ, Fendorf S, Kitanidis PK, Jardine PM, Criddle CS (2007) In situ bioreduction of uranium (VI) to submicromolar levels and reoxidation by dissolved oxygen. Environ Sci Technol 41:5716–5723.  https://doi.org/10.1021/es062657b CrossRefPubMedGoogle Scholar
  60. Yan X, Luo XG, Zhao M (2016) Metagenomic analysis of microbial community in uranium-contaminated soil. Appl Microbiol Biotechnol 100:299–310.  https://doi.org/10.1007/s00253-015-7003-5 CrossRefPubMedGoogle Scholar
  61. Zheng XY, Wang XY, Shen YH, Lu X, Wang TS (2017) Biosorption and biomineralization of uranium(VI) by Saccharomyces cerevisiae—crystal formation of chernikovite. Chemosphere 175:161–169.  https://doi.org/10.1016/j.chemosphere.2017.02.035 CrossRefPubMedGoogle Scholar
  62. Zhou JL (1999) Zn biosorption by Rhizopus arrhizus and other fungi. Appl Microbiol Biotechnol 51:686–693.  https://doi.org/10.1007/s002530051453 CrossRefGoogle Scholar
  63. Zhou P, Gu BH (2005) Extraction of oxidized and reduced forms of uranium from contaminated soils: effects of carbonate concentration and pH. Environ Sci Technol 39:4435–4440.  https://doi.org/10.1021/es0483443 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Nuclear Science and TechnologyLanzhou UniversityLanzhouChina

Personalised recommendations