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Uranium speciation and distribution in Shewanella putrefaciens and anaerobic granular sludge in the uranium immobilization process

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Abstract

The uranium (U) in Shewanella putrefaciens (S. putrefaciens) and anaerobic granular sludge (AnGS) were fractionated, and the contents and forms of U in each fraction were investigated. The functional groups of microorganisms for U binding and the deposition of U in microbial aggregates were also analyzed. Four main approaches were found involved in U immobilization, including biosorption/complexation by microbial cells and their extracellular polymeric substances (EPS), non-reductive biomineralization, bioreduction and intracellular accumulation. Results show that non-reductive biomineralization was found to be dominated in the U(VI) immobilization process. Besides, the contribution of EPS to U removal could not be ignored.

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References

  1. Thomas B, Ruben K, Andreas K, Philippe VC, Matthew GV, Andreas V, Kate C (2009) Biogeochemical redox processes and their impact on contaminant dynamics. Environ Sci Technol 44:15–23

    Google Scholar 

  2. Liu P, Yu Q, Xue Y, Chen J, Ma F (2020) Adsorption performance of U(VI) by amidoxime-based activated carbon. J Radioanal Nucl Chem. https://doi.org/10.1007/s10967-020-07111-x

    Article  PubMed  PubMed Central  Google Scholar 

  3. Wei H, Dong F, Chen M, Zhang W, He M, Liu M (2020) Removal of uranium by biogenetic jarosite coupled with photoinduced reduction in the presence of oxalic acid: a low-cost remediation technology. J Radioanal Nucl Chem. https://doi.org/10.1007/s10967-020-07125-5

    Article  Google Scholar 

  4. Newsome L, Morris K, Lloyd JR (2014) The biogeochemistry and bioremediation of uranium and other priority radionuclides. Chem Geol 363:164–184

    Article  CAS  Google Scholar 

  5. Spear JR, Figueroa LA, Honeyman BD (1999) Modeling the removal of uranium U(VI) from aqueous solutions in the presence of sulfate reducing bacteria. Environ Sci Technol 33:2667–2675

    Article  CAS  Google Scholar 

  6. Finneran KT, Anderson RT, Nevin KP, Lovley DR (2002) Potential for bioremediation of uranium-contaminated aquifers with microbial U(VI) reduction. J Soil Contam 11:339–357

    Article  CAS  Google Scholar 

  7. Anderson RT, Vrionis HA, Ortiz-Bernad I, Resch CT, Long PE, Dayvault R, Karp K, Marutzky S, Metzler DR, Peacock A, White DC, Lowe M, Lovley DR (2003) Stimulating the in situ activity of geobacter species to remove uranium from the groundwater of a uranium-contaminated aquifer. Appl Environ Microbiol 69:5884–5891

    Article  CAS  Google Scholar 

  8. Renshaw JC, Lloyd JR, Livens FR (2003) Microbial interactions with actinides and long-lived fission products. C R Chim 10:1067–1077

    Article  Google Scholar 

  9. Lovley DR, Phillips EJP, Gorby YA, Landa ER (1991) Microbial reduction of uranium. Nature 350:413–416

    Article  CAS  Google Scholar 

  10. Mumtaz S, Streten-Joyce C, Parry DL, Mcguinness KA, Lu P, Gibb KS (2013) Fungi outcompete bacteria under increased uranium concentration in culture media. J Environ Radioact 120:39–44

    Article  CAS  Google Scholar 

  11. Sheng L, Fein JB (2014) Uranium reduction by Shewanella oneidensis MR-1 as a function of NaHCO3 concentration: surface complexation control of reduction kinetics. Environ Sci Technol 48:3768–3775

    Article  CAS  Google Scholar 

  12. Newsome L, Morris K, Lloyd JR (2015) Uranium biominerals precipitated by an environmental isolate of serratia under anaerobic conditions. PLoS ONE 10:1–14

    Article  CAS  Google Scholar 

  13. Nancharaiah YV, Joshi HM, Mohan TVK, Venugopalan VP, Narasimhan SV (2006) Aerobic granular biomass: a novel biomaterial for efficient uranium removal. Curr Sci 91:503–509

    CAS  Google Scholar 

  14. Tapia-Rodriguez A, Luna-Velasco A, Field JA, Sierra-Alvarez R (2010) Anaerobic bioremediation of hexavalent uranium in groundwater by reductive precipitation with methanogenic granular sludge. Water Res 44:2153–2162

    Article  CAS  Google Scholar 

  15. Vaideeswaran S, Maxim IB, Brent MP, Sridhar V, Robin G, William AA, Rajesh KS, Alice D, Kenneth MK, Thomas B (2011) Multiple mechanisms of uranium immobilization by cellulomonas sp. strain es6. Biotechnol Bioeng 108:264–276

    Article  Google Scholar 

  16. Lloyd JR, Macaskie LE (2002) Chapter 11 biochemical basis of microbe-radionuclide interactions. Radioact Environ 2:313–342

    Article  CAS  Google Scholar 

  17. Merroun ML, Selenska-Pobell S (2008) Bacterial interactions with uranium: an environmental perspective. J Contam Hydrol 102:285–295

    Article  CAS  Google Scholar 

  18. Zhao C, Jun L, Li X, Li F, Tu H, Sun Q, Liao J, Yang J, Yang Y, Liu N (2016) Biosorption and bioaccumulation behavior of uranium on Bacillus sp. dwc-2: investigation by Box-Behenken design method. J Mol Liq 221:156–165

    Article  CAS  Google Scholar 

  19. Merroun M, Nedelkova M, Rossberg A, Hennig C, Scheinost AC, Selenska-pobell S (2006) Interaction mechanisms of uranium with bacterial strains isolated from extreme habitats. Spec Publ R Soc Chem 305:47–49

    CAS  Google Scholar 

  20. Macaskie L, Empson R, Cheetham A, Grey C, Skarnulis A (1992) Uranium bioaccumulation by a citrobacter sp. as a result of enzymically mediated growth of polycrystalline HUO2PO4. Science 257:782–784

    Article  CAS  Google Scholar 

  21. Newsome L, Morris K, Trivedi D, Bewsher AD, Lloyd JR (2015) Biostimulation by glycerol phosphate to precipitate recalcitrant uranium(IV) phosphate. Environ Sci Technol 49:11070–11078

    Article  CAS  Google Scholar 

  22. Cao B, Ahmed B, Kennedy DW, Wang Z, Shi L, Marshall MJ, Fredrickson JK, Isern NG, Majors PD, Beyenal H (2011) Contribution of extracellular polymeric substances from Shewanella sp. HRCR-1 biofilms to U(VI) immobilization. Environ Sci Technol 45:5483–5490

    Article  CAS  Google Scholar 

  23. Zhang H, Cheng M, Liu W, Huang F, Ding H, Li S, Guo W, Wang Y, Huang H (2017) Characterization of uranium in the extracellular polymeric substances of anaerobic granular sludge used to treat uranium-contaminated groundwater. RSC Adv 7:54188–54195

    Article  CAS  Google Scholar 

  24. Haas JR, Dichristina TJ, Wade R Jr (2001) Thermodynamics of U(VI) sorption onto Shewanella putrefaciens. Chem Geol 180:33–54

    Article  CAS  Google Scholar 

  25. Vogt SJ, Stewart BD, Seymour JD, Peyton BM (2012) Detection of biological uranium reduction using magnetic resonance. Biotechnol Bioeng 109:877–883

    Article  CAS  Google Scholar 

  26. Luo W, Wu WM, Yan T, Criddle CS, Jardine PM, Zhou J, Gu B (2007) Influence of bicarbonate, sulfate, and electron donors on biological reduction of uranium and microbial community composition. Appl Microbiol Biotechnol 77:713–721

    Article  CAS  Google Scholar 

  27. Huang W, Nie X, Dong F, Ding C, Huang R, Qin Y, Liu M, Sun S (2017) Kinetics and pH-dependent uranium bioprecipitation by Shewanella putrefaciens under aerobic conditions. J Radioanal Nucl Chem 312:531–541

    Article  CAS  Google Scholar 

  28. Elias DA, Senko JM, Krumholz LR (2003) A procedure for quantitation of total oxidized uranium for bioremediation studies. J Microbiol Methods 53:343–353

    Article  CAS  Google Scholar 

  29. Suzuki Y, Tanaka K, Kozai N, Ohnuki T (2010) Effects of citrate, NTA, and EDTA on the reduction of U(VI) by Shewanellaputrefaciens. Geomicrobiol J 27:245–250

    Article  CAS  Google Scholar 

  30. Ke MH, Murgel GA, Lion LW, Shuler ML (1994) Interactions of microbial biofilms with toxic trace metals: 2. Prediction and verification of an integrated computer model of lead(II) distribution in the presence of microbial activity. Biotechnol Bioeng 44:232–239

    Article  Google Scholar 

  31. Drew GL, Elias PE, Fein JB (2005) Adsorption of aqueous uranyl complexes onto Bacillus subtilis cells. Environ Sci Technol 39:4906–4912

    Article  Google Scholar 

  32. Merroun ML, Nedelkova M, Ojeda JJ, Reitz T, LópezFernández M, Arias JM, MaríaRomero-González S-PS (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

    Article  CAS  Google Scholar 

  33. Islam E, Sar P (2016) Diversity, metal resistance and uranium sequestration abilities of bacteria from uranium ore deposit in deep earth stratum. Ecotoxicol Environ Saf 127:12–21

    Article  CAS  Google Scholar 

  34. Finneran KT, Housewright ME, Lovley DR (2002) Multip, le influences of nitrate on uranium solubility durin ~ 1 bioremediation of uranium-contaminated subsurface sediments. Environ Microbiol 4:510–516

    Article  CAS  Google Scholar 

  35. Brooks SC, Fredrickson JK, Carroll SL, KennedyD W (2003) Inhibition of bacterial U(VI) reduction by Calcium. Environ Sci Technol 37:1850–1858

    Article  CAS  Google Scholar 

  36. Belli KM, Dichristina TJ, Cappellen PV, Taillefert M (2015) Effects of aqueous uranyl speciation on the kinetics of microbial uranium reduction. Geochim Cosmochim Acta 157:109–124

    Article  CAS  Google Scholar 

  37. Suzuki Y, Banfield JF (1999) Geomicrobiology of uranium. Rev Miner Geochem 38:393–432

    CAS  Google Scholar 

  38. Jroundi F, Merroun ML, Arias JM, Rossberg A, Selenska-Pobell S, González-Muñoz MT (2007) Spectroscopic and microscopic characterization of uranium biomineralization in Myxococcusxanthus. Geomicrobiol J 24:441–449

    Article  CAS  Google Scholar 

  39. Liu F, Teng S, Song R, Wang S (2010) Adsorption of methylene blue on anaerobic granular sludge: effect of functional groups. Desalination 263:11–17

    Article  CAS  Google Scholar 

  40. MüllerK BV, Foerstendorf H (2008) Aqueous uranium(VI) hydrolysis species characterized by attenuated total reflection Fourier-transform infrared spectroscopy. Inorg Chem 47:10127–10134

    Article  Google Scholar 

  41. Kazy SK, D’Souza SF, Sar P (2009) Uranium and thorium sequestration by a Pseudomonas sp.: mechanism and chemical characterization. J Hazard Mater 163(1):65–72

    Article  CAS  Google Scholar 

Download references

Funding

This study was funded by the National Natural Science Foundation of China (21571163, 21407133, 41402248 and 51608498), the key research and development projects of Sichuan science and technology department (No: 2018SZ0298), the science and technology planning projects of Panzhihua science and technology bureau (No. 2017CY-N-8), the Longshan academic research talent support program of Southwest University of Science and Technology (Nos. 17LZX308, 17LZX613, 18LZX638 and 18LZXT03) and the Scientific research project of Sichuan education department (No. 16ZB0150), Nuclear Facility Decommissioning and radioactive waste treatment research project of the State Administration of science, technology and industry of national defense (No. 1521 [2018] of the second division of science and Technology), Southwest University of Science and Technology Natural Science Foundation (No.18zx7125).

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F-CY, SF and H-X Huang designed experiments, and F-YH and H-LZ directed experiments and wrote the manuscript. Y-PW and M-XC performed experiments. J-C, W-JY and JZ helped with the experimentation. All authors read and approved the final manuscript.

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Correspondence to Fa-Cheng Yi, Su Feng or He-Xiang Huang.

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Huang, FY., Zhang, HL., Wang, YP. et al. Uranium speciation and distribution in Shewanella putrefaciens and anaerobic granular sludge in the uranium immobilization process. J Radioanal Nucl Chem 326, 393–405 (2020). https://doi.org/10.1007/s10967-020-07279-2

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