Bioadsorption of Rare Earth Elements through Cell Surface Display of Lanthanide Binding Tags

Environmental Science and Technology

Volumn 50, Issue 5, 2016, Pages 2735-2742

  Park, Dan M ^a   Reed, David W ^b   Yung, Mimi C ^a   Eslamimanesh, Ali ^c   Lencka, Malgorzata M ^c   Anderko, Andrzej ^c   Fujita, Yoshiko ^b   Riman, Richard E ^d   Navrotsky, Alexandra ^e   Jiao, Yongqin ^a  

^a LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

^b IDAHO NATIONAL LABORATORY   (United States)

^c OLI SYSTEMS INC   (United States)

^d Piscataway   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BINS; CELL MEMBRANES; RARE EARTH ELEMENTS; RARE EARTHS; STRAIN;

ADSORPTION CAPACITIES; ADSORPTION/DESORPTION; CELL SURFACE DISPLAYS; CLEAN ENERGY TECHNOLOGY; ENHANCED ADSORPTIONS; LANTHANIDE BINDING TAG; RARE EARTH ELEMENTS (REES); THERMODYNAMIC SPECIATION;

ADSORPTION;

CITRIC ACID; LANTHANIDE; TERBIUM;

ADSORPTION; BACTERIUM; CELLS AND CELL COMPONENTS; GENETIC ENGINEERING; RARE EARTH ELEMENT; SPECIATION (CHEMISTRY); THERMODYNAMICS;

ADSORPTION; ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; BINDING AFFINITY; CAULOBACTER VIBRIOIDES; CELL SURFACE DISPLAY; CHEMICAL BINDING; COMPLEX FORMATION; CONTROLLED STUDY; DESORPTION; ELUTION; LEACHING; NONHUMAN; SPECIES DIFFERENTIATION; THERMODYNAMICS; CHEMISTRY; GENETIC ENGINEERING; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MINING; PROCEDURES;

BACTERIA (MICROORGANISMS); CAULOBACTER VIBRIOIDES;

ADSORPTION; CAULOBACTER CRESCENTUS; CITRIC ACID; GENETIC ENGINEERING; LANTHANOID SERIES ELEMENTS; METALS, RARE EARTH; MINING; TERBIUM;

EID: 84959515525     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/acs.est.5b06129     Document Type: Article

References (58)

1. Zhuang, W. Q.; Fitts, J. P.; Ajo-Franklin, C. M.; Maes, S.; Alvarez-Cohen, L.; Hennebel, T. Recovery of critical metals using biometallurgy Curr. Opin. Biotechnol. 2015, 33, 327-335 10.1016/j.copbio.2015.03.019
2. Hennebel, T.; Boon, N.; Maes, S.; Lenz, M. Biotechnologies for critical raw material recovery from primary and secondary sources: R&D priorities and future perspectives New Biotechnol. 2015, 32 (1) 121-7 10.1016/j.nbt.2013.08.004
3. DOE, Critical Materials Strategy. http://www.energy.gov 2011.
4. Xie, F.; Zhang, T. A.; Dreisinger, D.; Doyle, F. A critical review on solvent extraction of rare earths from aqueous solutions Miner. Eng. 2014, 56, 10-28 10.1016/j.mineng.2013.10.021
5. Nash, K. L.; Jensen, M. P. Analytical-scale separations of the lanthanides: A review of techniques and fundamentals Sep. Sci. Technol. 2001, 36 (5-6) 1257-1282 10.1081/SS-100103649
6. Gadd, G. M. Metals, minerals and microbes: geomicrobiology and bioremediation Microbiology 2010, 156 (3) 609-43 10.1099/mic.0.037143-0
7. Blackwell, K. J.; Singleton, I.; Tobin, J. M. Metal cation uptake by yeast: a review Appl. Microbiol. Biotechnol. 1995, 43 (4) 579-84 10.1007/BF00164757
8. Moriwaki, H.; Yamamoto, H. Interactions of microorganisms with rare earth ions and their utilization for separation and environmental technology Appl. Microbiol. Biotechnol. 2013, 97 (1) 1-8 10.1007/s00253-012-4519-9
9. Texier, A. C.; Andres, Y.; Le Cloirec, P. Selective biosorption of lanthanide (La, Eu, Yb) ions by Pseudomonas aeruginosa Environ. Sci. Technol. 1999, 33 (3) 489-495 10.1021/es9807744
10. Tsuruta, T. Accumulation of rare earth elements in various microorganisms J. Rare Earths 2007, 25 (5) 526-532 10.1016/S1002-0721(07)60556-0
11. Ozaki, T.; Gillow, J. B.; Kimura, T.; Ohnuki, T.; Yoshida, Z.; Francis, A. J. Sorption behavior of europium(III) and curium(III) on the cell surfaces of microorganisms Radiochim. Acta 2004, 92 (9-11) 741-748 10.1524/ract.92.9.741.55006
12. Jiang, M. Y.; Ohnuki, T.; Tanaka, K.; Kozai, N.; Kamiishi, E.; Utsunomiya, S. Post-adsorption process of Yb phosphate nano-particle formation by Saccharomyces cerevisiae Geochim. Cosmochim. Acta 2012, 93, 30-46 10.1016/j.gca.2012.06.016
13. Fein, J. B.; Martin, A. M.; Wightman, P. G. Metal adsorption onto bacterial surfaces: Development of a predictive approach Geochim. Cosmochim. Acta 2001, 65 (23) 4267-4273 10.1016/S0016-7037(01)00721-9
14. Ginn, B. R.; Fein, J. B. The effect of species diversity on metal adsorption onto bacteria Geochim. Cosmochim. Acta 2008, 72 (16) 3939-3948 10.1016/j.gca.2008.05.063
15. Naeem, A.; Woertz, J. R.; Fein, J. B. Experimental measurement of proton, Cd, Pb, Sr, and Zn adsorption onto the fungal species Saccharomyces cerevisiae Environ. Sci. Technol. 2006, 40 (18) 5724-5729 10.1021/es0606935
16. Mejare, M.; Bulow, L. Metal-binding proteins and peptides in bioremediation and phytoremediation of heavy metals Trends Biotechnol. 2001, 19 (2) 67-73 10.1016/S0167-7799(00)01534-1
17. Kuroda, K.; Ueda, M. Engineering of microorganisms towards recovery of rare metal ions Appl. Microbiol. Biotechnol. 2010, 87 (1) 53-60 10.1007/s00253-010-2581-8
18. Kotrba, P.; Doleckova, L.; De Lorenzo, V.; Ruml, T. Enhanced bioaccumulation of heavy metal ions by bacterial cells due to surface display of short metal binding peptides Appl. Environ. Microbiol. 1999, 65 (3) 1092-1098
19. Wei, W.; Liu, X.; Sun, P.; Wang, X.; Zhu, H.; Hong, M.; Mao, Z. W.; Zhao, J. Simple Whole-Cell Biodetection and Bioremediation of Heavy Metals Based on an Engineered Lead-Specific Operon Environ. Sci. Technol. 2014, 48 (6) 3363-3371 10.1021/es4046567
20. Wei, W.; Zhu, T. Z.; Wang, Y.; Yang, H. L.; Hao, Z. Y.; Chen, P. R.; Zhao, J. Engineering a gold-specific regulon for cell-based visual detection and recovery of gold Chem. Sci. 2012, 3 (6) 1780-1784 10.1039/c2sc01119k
21. Nishitani, T.; Shimada, M.; Kuroda, K.; Ueda, M. Molecular design of yeast cell surface for adsorption and recovery of molybdenum, one of rare metals Appl. Microbiol. Biotechnol. 2010, 86 (2) 641-8 10.1007/s00253-009-2304-1
22. Xu, Z.; Lei, Y.; Patel, J. Bioremediation of soluble heavy metals with recombinant Caulobacter crescentus Bioeng Bugs 2010, 1 (3) 207-12 10.4161/bbug.1.3.11246
23. Zhou, L.; Bosscher, M.; Zhang, C.; Ozcubukcu, S.; Zhang, L.; Zhang, W.; Li, C. J.; Liu, J.; Jensen, M. P.; Lai, L.; He, C. A protein engineered to bind uranyl selectively and with femtomolar affinity Nat. Chem. 2014, 6 (3) 236-41 10.1038/nchem.1856
24. Valls, M.; de Lorenzo, V.; Gonzalez-Duarte, R.; Atrian, S. Engineering outer-membrane proteins in Pseudomonas putida for enhanced heavy-metal bioadsorption J. Inorg. Biochem. 2000, 79 (1-4) 219-223 10.1016/S0162-0134(99)00170-1
25. Mauro, J. M.; Pazirandeh, M. Construction and expression of functional multi-domain polypeptides in Escherichia coli: expression of the Neurospora crassa metallothionein gene Lett. Appl. Microbiol. 2000, 30 (2) 161-6 10.1046/j.1472-765x.2000.00697.x
26. Pazirandeh, M.; Wells, B. M.; Ryan, R. L. Development of bacterium-based heavy metal biosorbents: enhanced uptake of cadmium and mercury by Escherichia coli expressing a metal binding motif Appl. Environ. Microbiol. 1998, 64 (10) 4068-72
27. Martin, L. J.; Hahnke, M. J.; Nitz, M.; Wohnert, J.; Silvaggi, N. R.; Allen, K. N.; Schwalbe, H.; Imperiali, B. Double-lanthanide-binding tags: Design, photophysical properties, and NMR applications J. Am. Chem. Soc. 2007, 129 (22) 7106-7113 10.1021/ja070480v
28. Nitz, M.; Franz, K. J.; Maglathlin, R. L.; Imperiali, B. A powerful combinatorial screen to identify high-affinity terbium(III)-binding peptides ChemBioChem 2003, 4 (4) 272-6 10.1002/cbic.200390047
29. Liang, H. H.; Deng, X.; Bosscher, M.; Ji, Q. J.; Jensen, M. P.; He, C. Engineering Bacterial Two-Component System PmrA/PmrB to Sense Lanthanide Ions J. Am. Chem. Soc. 2013, 135 (6) 2037-2039 10.1021/ja312032c
30. Allen, K. N.; Imperiali, B. Lanthanide-tagged proteins - an illuminating partnership Curr. Opin. Chem. Biol. 2010, 14 (2) 247-54 10.1016/j.cbpa.2010.01.004
31. Franz, K. J.; Nitz, M.; Imperiali, B. Lanthanide-binding tags as versatile protein coexpression probes ChemBioChem 2003, 4 (4) 265-271 10.1002/cbic.200390046
32. Silvaggi, N. R.; Martin, L. J.; Schwalbe, H.; Imperiali, B.; Allen, K. N. Double-lanthanide-binding tags for macromolecular crystallographic structure determination J. Am. Chem. Soc. 2007, 129 (22) 7114-7120 10.1021/ja070481n
33. Amat, F.; Comolli, L. R.; Nomellini, J. F.; Moussavi, F.; Downing, K. H.; Smit, J.; Horowitz, M. Analysis of the Intact Surface Layer of Caulobacter crescentus by Cryo-Electron Tomography J. Bacteriol. 2010, 192 (22) 5855-5865 10.1128/JB.00747-10
34. Nomellini, J. F.; Li, C.; Lavallee, D.; Shanina, I.; Cavacini, L. A.; Horwitz, M. S.; Smit, J. Development of an HIV-1 specific microbicide using Caulobacter crescentus S-layer mediated display of CD4 and MIP1alpha PLoS One 2010, 5 (4) e10366 10.1371/journal.pone.0010366
35. Ford, M. J.; Nomellini, J. F.; Smit, J. S-layer anchoring and localization of an S-layer-associated protease in Caulobacter crescentus J. Bacteriol. 2007, 189 (6) 2226-37 10.1128/JB.01690-06
36. Bingle, W. H.; Nomellini, J. F.; Smit, J. Linker mutagenesis of the Caulobacter crescentus S-layer protein: Toward a definition of an N-terminal anchoring region and a C-terminal secretion signal and the potential for heterologous protein secretion J. Bacteriol. 1997, 179 (3) 601-611
37. Farr, C.; Nomellini, J. F.; Ailon, E.; Shanina, I.; Sangsari, S.; Cavacini, L. A.; Smit, J.; Horwitz, M. S. Development of an HIV-1 Microbicide Based on Caulobacter crescentus: Blocking Infection by High-Density Display of Virus Entry Inhibitors PLoS One 2013, 8 (6) e65965 10.1371/journal.pone.0065965
38. Duval, M.; Lewis, C. J.; Nomellini, J. F.; Horwitz, M. S.; Smit, J.; Cavacini, L. A. Enhanced neutralization of HIV by antibodies displayed on the S-layer of Caulobacter crescentus Antimicrob. Agents Chemother. 2011, 55 (12) 5547-52 10.1128/AAC.00509-11
39. Nomellini, J. F.; Duncan, G.; Dorocicz, I. R.; Smit, J. S-layer-mediated display of the immunoglobulin G-binding domain of streptococcal protein G on the surface of Caulobacter crescentus: Development of an immunoactive reagent Appl. Environ. Microbiol. 2007, 73 (10) 3245-3253 10.1128/AEM.02900-06
40. Park, D. M.; Jiao, Y. Modulation of medium pH by Caulobacter crescentus facilitates recovery from uranium-induced growth arrest Appl. Environ. Microbiol. 2014, 80 (18) 5680-8 10.1128/AEM.01294-14
41. Hutner, S. H.; Provasoli, L.; Shatz, A.; Haskins, C. P. Some approaches to the study of the role of metals in the metabolism of microorganisms Proc. Am. Philos. Soc. 1950, 94, 152-170
42. Nitz, M.; Sherawat, M.; Franz, K. J.; Peisach, E.; Allen, K. N.; Imperiali, B. Structural origin of the high affinity of a chemically evolved lanthanide-binding peptide Angew. Chem., Int. Ed. 2004, 43 (28) 3682-3685 10.1002/anie.200460028
43. Ritz, C.; Streibig, J. C. Bioassay analysis using R J. Stat Softw 2005, 12 (5) 1-22 10.18637/jss.v012.i05
44. Cheng, Y.; Prusoff, W. H. Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50% inhibition (I50) of an enzymatic reaction Biochem. Pharmacol. 1973, 22 (23) 3099-3108 10.1016/0006-2952(73)90196-2
45. Wang, P.; Anderko, A.; Springer, R. D.; Young, R. D. Modeling Phase Equilibria and Speciation in Mixed-Solvent Electrolyte Systems: II. Liquid-Liquid Equilibria and Properties of Associating Electrolyte Solutions J. Mol. Liq. 2006, 125 (1) 37-44 10.1016/j.molliq.2005.11.030
46. Wang, P.; Anderko, A.; Young, R. D. A Speciation-Based Model for Mixed-Solvent Electrolyte Systems Fluid Phase Equilib. 2002, 203 (1-2) 141-176 10.1016/S0378-3812(02)00178-4
47. Walker, S. G.; Smith, S. H.; Smit, J. Isolation and comparison of the paracrystalline surface layer proteins of freshwater caulobacters J. Bacteriol. 1992, 174 (6) 1783-92
48. Smit, J.; Engelhardt, H.; Volker, S.; Smith, S. H.; Baumeister, W. The S-layer of Caulobacter crescentus: three-dimensional image reconstruction and structure analysis by electron microscopy J. Bacteriol. 1992, 174 (20) 6527-6538
49. Nomellini, J. F.; Kupcu, S.; Sleytr, U. B.; Smit, J. Factors controlling in vitro recrystallization of the Caulobacter crescentus paracrystalline S-layer J. Bacteriol. 1997, 179 (20) 6349-6354
50. Lo, Y. C.; Cheng, C. L.; Han, Y. L.; Chen, B. Y.; Chang, J. S. Recovery of high-value metals from geothermal sites by biosorption and bioaccumulation Bioresour. Technol. 2014, 160, 182-190 10.1016/j.biortech.2014.02.008
51. Bunzli, J. C. Benefiting from the unique properties of lanthanide ions Acc. Chem. Res. 2006, 39 (1) 53-61 10.1021/ar0400894
52. Bayer, M. E.; Bayer, M. H. Lanthanide accumulation in the periplasmic space of Escherichia coli B J. Bacteriol. 1991, 173 (1) 141-149
53. Jones, A. P.; Wall, F.; Williams, C. T. Rare Earth Minerals: Chemistry Origin and Ore Deposits. Chapman & Hall: London, 1996.
54. Binnemans, K.; Jones, P. T.; Blanpain, B.; Van Gerven, T.; Yang, Y. X.; Walton, A.; Buchert, M. Recycling of rare earths: a critical review J. Cleaner Prod. 2013, 51, 1-22 10.1016/j.jclepro.2012.12.037
55. Rahimi, Y.; Goulding, A.; Shrestha, S.; Mirpuri, S.; Deo, S. K. Mechanism of copper induced fluorescence quenching of red fluorescent protein, DsRed Biochem. Biophys. Res. Commun. 2008, 370 (1) 57-61 10.1016/j.bbrc.2008.03.034
56. Goyne, K. W.; Brantley, S. L.; Chorover, J. Rare earth element release from phosphate minerals in the presence of organic acids Chem. Geol. 2010, 278 (1-2) 1-14 10.1016/j.chemgeo.2010.03.011
57. Firsching, F. H.; Brune, S. N. Solubility Products of the Trivalent Rare-Earth Phosphates J. Chem. Eng. Data 1991, 36 (1) 93-95 10.1021/je00001a028
58. Fujita, Y.; Barnes, J.; Eslamimanesh, A.; Lencka, M. M.; Anderko, A.; Riman, R. E.; Navrotsky, A. Effects of Simulated Rare Earth Recycling Wastewaters on Biological Nitrification Environ. Sci. Technol. 2015, 49 (16) 9460-8 10.1021/acs.est.5b01753