A<i>β</i>-Like Peptide Displayed on Bacteriophage T7 Catalyzes Chromate and Uranyl Reduction — Oak Academic Publishing
Research ArticleOpen AccessGoogle Scholar indexed
A<i>β</i>-Like Peptide Displayed on Bacteriophage T7 Catalyzes Chromate and Uranyl Reduction
1Fundamental & Computational Sciences Directorate, Pacific Northwest National Laboratory, Richland, USA; 2Department of Radi-ological Science, Washington University School of Medicine, St. Louis, USA
,
Fundamental & Computational Sciences Directorate, Pacific Northwest National Laboratory, Richland, USA
,
Fundamental & Computational Sciences Directorate, Pacific Northwest National Laboratory, Richland, USA
,
Fundamental & Computational Sciences Directorate, Pacific Northwest National Laboratory, Richland, USA
,
Xinhua Hospital Affiliated to Shanghai Jiaotong University, Shanghai, China
,
Xinhua Hospital Affiliated to Shanghai Jiaotong University, Shanghai, China
,
Xinhua Hospital Affiliated to Shanghai Jiaotong University, Shanghai, China
,
Fundamental & Computational Sciences Directorate, Pacific Northwest National Laboratory, Richland, USA
,
Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, USA
1 1Fundamental & Computational Sciences Directorate, Pacific Northwest National Laboratory, Richland, USA; 2Department of Radi-ological Science, Washington University School of Medicine, St. Louis, USA
2 Fundamental & Computational Sciences Directorate, Pacific Northwest National Laboratory, Richland, USA
3 Fundamental & Computational Sciences Directorate, Pacific Northwest National Laboratory, Richland, USA
4 Fundamental & Computational Sciences Directorate, Pacific Northwest National Laboratory, Richland, USA
5 Xinhua Hospital Affiliated to Shanghai Jiaotong University, Shanghai, China
6 Xinhua Hospital Affiliated to Shanghai Jiaotong University, Shanghai, China
7 Xinhua Hospital Affiliated to Shanghai Jiaotong University, Shanghai, China
8 Fundamental & Computational Sciences Directorate, Pacific Northwest National Laboratory, Richland, USA
9 Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, USA
In order to discover genes capable of catalyzing the reductive immobilization of toxic chromate and uranyl ions, we have created a T7 bacteriophage library containing cDNA from environmental microbes ( i.e. , Geobacter sulfurreducens and Shewanella oneidensis MR-1) that are known to mediate the reduction of chromate and uranyl ions. After three rounds of screening, ten bacteriophage mutants were found to mediate the NADH-dependent reduction of chromate and uranyl ions whose cDNA encodes polypeptide chains ranging 14 to 73 amino acids in length. All identified sequences contain disordered structural motifs similar to the β -amyloid peptide (A β ) known to promote aggregation and formation of high-affinity metal binding sites. Confirmation of this structural similarity involved phage display of the 42 amino-acid A β -peptides that have been found to catalyze the NADH-dependent reduction of both chromate and uranyl ions. Transmission electron microscopy (TEM) and X-ray absorption near edge structure (XANES) measurements confirm that reduced uranium is present on the surface of bacteriophage expressing the A β -peptide. The surface-displayed A β -like peptide on bacteriophage h as the potential to couple naturally occurring electron transfer shuttles present in soils to promote economically viable remediation of contaminated sites containing toxic chromate and uranyl ions .
KeywordsChromateUranylBioremediationBacteriophage
C. Liu, J. M. Zachara, L. Zhong, S. M. Heald, Z. Wang, B.-H. Jeon and J. K. Fredrickson, “Microbial Reduction of Intragrain U(VI) in Contaminated Sediment,” Environmental Science & Technology, Vol. 43, No. 13, 2009, pp. 4928-4933. doi:10.1021/es8029208
A. L. N’Guessan, H. A. Vrionis, C. T. Resch, P. E. Long and D. R. Lovley, “Sustained Removal of Uranium From Contaminated Groundwater Following Stimulation of Dissimilatory Metal Reduction,” Environmental Science & Technology, Vol. 42, No. 8, 2008, pp. 2999-3004. doi:10.1021/es071960p
J. K. Fredrickson and J. M. Zachara, “Electron Transfer at the Microbe-Mineral Interface: A Grand Challenge in Biogeochemistry,” Geobiology, Vol. 6, No. 3, 2008, pp. 245-253. doi:10.1111/j.1472-4669.2008.00146.x
E. S. Shelobolina, M. V. Coppi, A. A. Korenevsky, L. N. DiDonato, S. A. Sullivan, H. Konishi, H. Xu, C. Leang, J. E. Butler, B. C. Kim and D. R. Lovley, “Importance of c-Type Cytochromes for U(VI) Reduction by Geobacter Sulfurreducens,” BMC Microbiology, Vol. 7, 2007, p. 16. doi:10.1186/1471-2180-7-16
J. D. Wall and L. R. Krumholz, “Uranium Reduction,” Annual Review of Microbiology, Vol. 60, 2006, pp. 149-166. doi:10.1146/annurev.micro.59.030804.121357
R. B. Payne, D. M. Gentry, B. J. Rapp-Giles, L. Casalot and J. D. Wall, “Uranium Reduction by Desulfovibrio desulfuricans Strain G20 and a Cytochrome c3 Mutant,” Applied and Environmental Microbiology, Vol. 68, No. 6, 2002, pp. 3129-3132. doi:10.1128/AEM.68.6.3129-3132.2002
D. R. Lovley and E. J. P. Phillips, “Bioremediation of Uranium Contamination with Enzymatic Uranium Reduction,” Environmental Science & Technology, Vol. 26, No. 11, 2002, pp. 2228-2234. doi:10.1021/es00035a023
M. J. Wilkins, N. C. Verberkmoes, K. H. Williams, S. J. Callister, P. J. Mouser, H. Elifantz, L. N’Guessan A, B. C. Thomas, C. D. Nicora, M. B. Shah, P. Abraham, M. S. Lipton, D. R. Lovley, R. L. Hettich, P. E. Long and J. F. Banfield, “Proteogenomic Monitoring of Geobacter Physiology during Stimulated Uranium Bioremediation,” Applied and Environmental Microbiology, Vol. 75, No. 20, 2009, pp. 6591-6599. doi:10.1128/AEM.01064-09
Y. Xiong, B. Chen, L. Shi, J. K. Fredrickson, D. J. Bigelow and T. C. Squier, “Targeted Protein Degradation of Outer Membrane Decaheme Cytochrome MtrC Metal Reductase in Shewanella oneidensis MR-1 Measured Using Biarsenical Probe CrAsH-EDT(2),” Biochemistry, Vol. 50, No. 45, 2011, pp. 9738-9751. doi:10.1021/bi200602f
L. Shi, S. M. Belchik, A. E. Plymale, S. Heald, A. C. Dohnalkova, K. Sybirna, H. Bottin, T. C. Squier, J. M. Zachara and J. K. Fredrickson, “Purification and Characterization of the [NiFe]-Hydrogenase of Shewanella oneidensis MR-1,” Applied and Environmental Microbiology, Vol. 77, No. 16, 2011, pp. 5584-5590. doi:10.1128/AEM.00260-11
Y. Barak, S. H. Thorne, D. F. Ackerley, S. V. Lynch, C. H. Contag and A. Matin, “New Enzyme for Reductive Cancer Chemotherapy, YieF, and Its Improvement by Directed Evolution,” Molecular Cancer Therapeutics, Vol. 5, No. 1, 2006, pp. 97-103. doi:10.1158/1535-7163.MCT-05-0365
Y. Barak, D. F. Ackerley, C. J. Dodge, L. Banwari, C. Alex, A. J. Francis and A. Matin, “Analysis of Novel Soluble Chromate and Uranyl Reductases and Generation of an Improved Enzyme by Directed Evolution,” Applied and Environmental Microbiology, Vol. 72, No. 11, 2006, pp. 7074-7082. doi:10.1128/AEM.01334-06
H. Jin, T. C. Squier and P. E. Long, “Dying for Good: Virus-Bacterium Biofilm Co-Evolution Enhances Environmental Fitness,” Biochemistry Insights, Vol. 5, 2012, pp. 1-9. doi:10.4137/BCI.S9553
Z. Guo and D. Eisenberg, “The Structure of a Fibril-Forming Sequence, NNQQNY, in the Context of a Globular Fold,” Protein Science, Vol. 17, No. 9, 2008, pp. 1617-1623. doi:10.1110/ps.036368.108
L. R. Krumpe, K. M. Schumacher, J. B. McMahon, L. Makowski and T. Mori, “Trinucleotide Cassettes Increase Diversity of T7 Phage-Displayed Peptide Library,” BMC Biotechnology, Vol. 7, 2007, p. 65. doi:10.1186/1472-6750-7-65
P. Rekha, D. S. Suman Raj, C. Aparna, V. Hima Bindu and Y. Anjaneyulu, “Bioremediation of Contaminated Lake Sediments and Evaluation of Maturity Indicies as Indicators of Compost Stability,” International Journal of Environmental Research and Public Health, Vol. 2, No. 2, 2005, pp. 251-262. doi:10.3390/ijerph2005020008
J. B. McKinlay and J. G. Zeikus, “Extracellular Iron Reduction Is Mediated in Part by Neutral Red and Hydrogenase in Escherichia coli,” Applied and Environmental Microbiology, Vol. 70, No. 6, 2004, pp. 3467-3474. doi:10.1128/AEM.70.6.3467-3474.2004
J. Dec, K. Haider and J. M. Bollag, “Release of Substituents from Phenolic Compounds during Oxidative Coupling Reactions,” Chemosphere, Vol. 52, No. 3, 2003, pp. 549-556. doi:10.1016/S0045-6535(03)00236-4
J. S. Kim, J. W. Park, S. E. Lee and J. E. Kim, “Formation of Bound Residues of 8-Hydroxybentazon by Oxidoreductive Catalysts in Soil,” Journal of Agricultural and Food Chemistry, Vol. 50, No. 12, 2002, pp. 3507-3511. doi:10.1021/jf011504z
H. Jin, G. L. Hayes, N. S. Darbha, E. Meyer and P. J. LiWang, “Investigation of CC and CXC Chemokine Quaternary State Mutants,” Biochemical and Biophysical Research Communications, Vol. 338, No. 2, 2005, pp. 987-999. doi:10.1016/j.bbrc.2005.10.062
G. J. Puzon, J. N. Petersen, A. G. Roberts, D. M. Kramer and L. Xun, “A Bacterial Flavin Reductase System Reduces Chromate to a Soluble Chromium(III)-NAD(+) Complex,” Biochemical and Biophysical Research Communications, Vol. 294, No. 1, 2002, pp. 76-81. doi:10.1016/S0006-291X(02)00438-2
Y. H. Kwak, D. S. Lee and H. B. Kim, “Vibrio harveyi Nitroreductase Is Also a Chromate Reductase,” Applied and Environmental Microbiology, Vol. 69, No. 8, 2003, pp. 4390-4395. doi:10.1128/AEM.69.8.4390-4395.2003
F. C. Bancroft and D. Freifelder, “Molecular Weights of Coliphages and Coliphage DNA. I. Measurement of the Molecular Weight of Bacteriophage T7 by High-Speed Equilibrium Centrifugation,” Journal of Molecular Biology, Vol. 54, No. 3, 1970, pp. 537-546. doi:10.1016/0022-2836(70)90124-5
A. Kumar, R. K. Singhal, S. Rout, U. Narayanan, R. Karpe and P. M. Ravi, “Adsorption and Kinetic Behavior of Uranium and Thorium in Seawater-Sediment System,” Journal of Radioanalytical and Nuclear Chemistry, Vol. 295, No. 1, 2013, pp. 649-656. doi:10.1007/s10967-012-1825-8
V. M. Chauthaiwale, A. Therwath and V. V. Deshpande, “Bacteriophage Lambda as a Cloning Vector,” Microbiology and Molecular Biology Reviews, Vol. 56, No. 4, 1992, pp. 577-591.
A. I. Bush and R. E. Tanzi, “The Galvanization of Beta-Amyloid in Alzheimer’s Disease,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 99, No. 11, 2002, pp. 7317-7319. doi:10.1073/pnas.122249699
K. Suzuki, T. Miura and H. Takeuchi, “Inhibitory Effect of Copper(II) on Zinc(II)-Induced Aggregation of Amyloid Beta-Peptide,” Biochemical and Biophysical Research Communications, Vol. 285, No. 4, 2001, pp. 991-996. doi:10.1006/bbrc.2001.5263
T. Miura, K. Suzuki, N. Kohata and H. Takeuchi, “Metal Binding Modes of Alzheimer’s Amyloid Beta-Peptide in Insoluble Aggregates and Soluble Complexes,” Biochemistry, Vol. 39, No. 23, 2000, pp. 7024-7031. doi:10.1021/bi0002479
X. Huang, M. P. Cuajungco, C. S. Atwood, M. A. Hartshorn, J. D. Tyndall, G. R. Hanson, K. C. Stokes, M. Leopold, G. Multhaup, L. E. Goldstein, R. C. Scarpa, A. J. Saunders, J. Lim, R. D. Moir, C. Glabe, E. F. Bowden, C. L. Masters, D. P. Fairlie, R. E. Tanzi and A. I. Bush, “Cu(II) Potentiation of Alzheimer Abeta Neurotoxicity. Correlation with Cell-Free Hydrogen Peroxide Production and Metal Reduction,” The Journal of Biological Chemistry, Vol. 274, No. 52, 1999, pp. 37111-37116. doi:10.1074/jbc.274.52.37111
X. Huang, C. S. Atwood, M. A. Hartshorn, G. Multhaup, L. E. Goldstein, R. C. Scarpa, M. P. Cuajungco, D. N. Gray, J. Lim, R. D. Moir, R. E. Tanzi and A. I. Bush, “The A Beta Peptide of Alzheimer’s Disease Directly Produces Hydrogen Peroxide through Metal Ion Reduction,” Biochemistry, Vol. 38, No. 24, 1999, pp. 7609-7616. doi:10.1021/bi990438f
H. Zeng, A. Singh, S. Basak, K. U. Ulrich, M. Sahu, P. Biswas, J. G. Catalano and D. E. Giammar, “Nanoscale Size Effects on Uranium(VI) Adsorption to Hematite,” Environmental Science & Technology, Vol. 43, No. 5, 2009, pp. 1373-1378. doi:10.1021/es802334e
A. Schierz and H. Zanker, “Aqueous Suspensions of Carbon Nanotubes: Surface Oxidation, Colloidal Stability and Uranium Sorption,” Environmental Pollution, Vol. 157, No. 4, 2009, pp. 1088-1094. doi:10.1016/j.envpol.2008.09.045
T. Arnold, S. Utsunomiya, G. Geipel, R. C. Ewing, N. Baumann and V. Brendler, “Adsorbed U(VI) Surface Species on Muscovite Identified by Laser Fluorescence Spectroscopy and Transmission Electron Microscopy,” Environmental Science & Technology, Vol. 40, No. 15, 2006, pp. 4646-4652. doi:10.1021/es052507l
F. G. Gervais, D. Xu, G. S. Robertson, J. P. Vaillancourt, Y. Zhu, J. Huang, A. LeBlanc, D. Smith, M. Rigby, M. S. Shearman, E. E. Clarke, H. Zheng, L. H. Van Der Ploeg, S. C. Ruffolo, N. A. Thornberry, S. Xanthoudakis, R. J. Zamboni, S. Roy and D. W. Nicholson, “Involvement of Caspases in Proteolytic Cleavage of Alzheimer’s Amyloid-Beta Precursor Protein and Amyloidogenic A Beta Peptide Formation,” Cell, Vol. 97, No. 3, 1999, pp. 395-406. doi:10.1016/S0092-8674(00)80748-5
Y.-J. Chang, P. E. Long, R. Geyer, A. D. Peacock, C. T. Resch, K. Sublette, S. Pfiffner, A. Smithgall, R. T. Anderson, H. A. Vrionis, J. R. Stephen, R. Dayvault, I. Ortiz-Bernad, D. R. Lovley and D. C. White, “Microbial Incorporation of 13C-Labeled Acetate at the Field Scale: Detection of Microbes Responsible for Reduction of U(VI),” Environmental Science & Technology, Vol. 39, No. 23, 2005, pp. 9039-9048. doi:10.1021/es051218u
I. Bento, V. H. Teixeira, A. M. Baptista, C. M. Soares, P. M. Matias and M. A. Carrondo, “Redox-Bohr and Other Cooperativity Effects in the Nine-Heme Cytochrome C from Desulfovibrio desulfuricans ATCC 27774: Crystallographic and Modeling Studies,” The Journal of Biological Chemistry, Vol. 278, 2003, pp. 36455-36469. doi:10.1074/jbc.M301745200
C. Opazo, X. Huang, R. A. Cherny, R. D. Moir, A. E. Roher, A. R. White, R. Cappai, C. L. Masters, R. E. Tanzi, N. C. Inestrosa and A. I. Bush, “Metalloenzyme-Like Activity of Alzheimer’s Disease Beta-Amyloid. Cu-Dependent Catalytic Conversion of Dopamine, Cholesterol, and Biological Reducing Agents to Neurotoxic H2O2,” The Journal of Biological Chemistry, Vol. 277, 2002, pp. 40302-40308. doi:10.1074/jbc.M206428200
X. H. Zong, P. Zhou, Z. Z. Shao, S. M. Chen, X. Chen, B. W. Hu, F. Deng and W. H. Yao, “Effect of pH and Copper(II) on the Conformation Transitions of Silk Fibroin Based on EPR, NMR, and Raman Spectroscopy,” Biochemistry, Vol. 43, 2004, pp. 11932-11941. doi:10.1021/bi049455h
J. Dong, C. S. Atwood, V. E. Anderson, S. L. Siedlak, M. A. Smith, G. Perry and P. R. Carey, “Metal Binding and Oxidation of Amyloid-Beta within Isolated Senile Plaque Cores: Raman Microscopic Evidence,” Biochemistry, Vol. 42, No. 10, 2003, pp. 2768-2773. doi:10.1021/bi0272151
S. S. Sidhu, “Engineering M13 for Phage Display,” Biomolecular Engineering, Vol. 18, No. 2, 2001, pp. 57-63. doi:10.1016/S1389-0344(01)00087-9
S. B. Santos, A. M. Kropinski, P. J. Ceyssens, H. W. Ackermann, A. Villegas, R. Lavigne, V. N. Krylov, C. M. Carvalho, E. C. Ferreira and J. Azeredo, “Genomic and Proteomic Characterization of the Broad-Host-Range Salmonella Phage PVP-SE1: Creation of a New Phage Genus,” Journal of Virology, Vol. 85, No. 21, 2011, pp. 11265-11273. doi:10.1128/JVI.01769-10
M. Gourmelon, M. P. Caprais, R. Segura, C. Le Mennec, S. Lozach, J. Y. Piriou and A. Rince, “Evaluation of Two Library-Independent Microbial Source Tracking Methods to Identify Sources of Fecal Contamination in French Estuaries,” Applied and Environmental Microbiology, Vol. 73, No. 15, 2007, pp. 4857-4866. doi:10.1128/AEM.03003-06
D. I. Kurtboke, “Actinophages as Indicators of Actinomycete Taxa in Marine Environments,” Antonie Van Leeuwenhoek, Vol. 87, No. 1, 2005, pp. 19-28. doi:10.1007/s10482-004-6535-y
A. Trovato, F. Seno and S. C. Tosatto, “The PASTA Server for Protein Aggregation Prediction,” Protein Engineering, Design & Selection, Vol. 20, No. 10, 2007, pp. 521-523. doi:10.1093/protein/gzm042