Influence of Uranium Concentration and pH on U-Phosphate Biomineralization by Caulobacter OR37

Morrison, Keith D.; Zavarin, Mavrik; Kersting, Annie B.; Begg, James D.; Mason, Harris E.; Balboni, Enrica; Jiao, Yongqin

doi:10.1021/acs.est.0c05437

Title: Influence of Uranium Concentration and pH on U-Phosphate Biomineralization by Caulobacter OR37

Journal Article · Wed Jan 20 00:00:00 EST 2021 · Environmental Science and Technology

DOI:https://doi.org/10.1021/acs.est.0c05437· OSTI ID:1787219

^[1];

^[2];

^[1]; Begg, James D. ^[3];

^[1];

^[1]

Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States). Glenn T. Seaborg Inst.
Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States); Amphos21, Barcelona (Spain)

Uranium contamination of soils and groundwater in the United States represents a significant health risk and will require multiple remediation approaches. Microbial phosphatase activity coupled to the addition of an organic P source has recently been studied as a remediation strategy that provides an extended release of inorganic P (Pi) into U-contaminated sites, resulting in the precipitation of meta-autunite minerals. Previous laboratory- and field-based biomineralization studies have investigated environments with relatively high U concentrations (>20 μM). However, most contaminated sites have much lower U concentrations (<2 μM). The Environmental Protection Agency (EPA) limit for U in drinking water is 0.126 μM. Reaching this regulatory limit becomes challenging as U concentrations approach autunite solubility. Furthermore, we studied the precipitation of U(VI)-phosphate minerals by an environmental isolate of Caulobacter sp. (strain OR37) from an Oak Ridge, Tennessee, U-contaminated site. Abiotic U(VI) solubility experiments reveal that U(VI)-phosphate minerals do not form in the presence of excess Pi (500 μM) when U(VI) concentrations are <1 μM and pH is <5. When OR37 cells are reacted under the same conditions with Pi or glycerol-2-phosphate, U(VI)-phosphate mineral formation was observed, along with the formation of intracellular polyphosphate granules. These results show that bacteria provide supersaturated microenvironments needed for U(VI)-phosphate mineralization while hydrolyzing organic P sources. This provides a pathway to lower U concentrations to below EPA limits for drinking water.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Lawrence Livermore National Lab. (LLNL), Livermore, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC52-07NA27344

OSTI ID:: 1787219

Report Number(s):: LLNL-JRNL-813614; 1021681; TRN: US2210425

Journal Information:: Environmental Science and Technology, Vol. 55, Issue 3; ISSN 0013-936X

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (64)

Modulation of Medium pH by Caulobacter crescentus Facilitates Recovery from Uranium-Induced Growth Arrest Park, Dan M.; Jiao, Yongqin Applied and Environmental Microbiology, Vol. 80, Issue 18 https://doi.org/10.1128/AEM.01294-14	journal	July 2014
Effects of Phosphate on Uranium(VI) Adsorption to Goethite-Coated Sand Cheng, Tao; Barnett, Mark O.; Roden, Eric E. Environmental Science & Technology, Vol. 38, Issue 22 https://doi.org/10.1021/es040388o	journal	November 2004
Draft Genome Sequence for Caulobacter sp. Strain OR37, a Bacterium Tolerant to Heavy Metals Utturkar, S. M.; Bollmann, A.; Brzoska, R. M. Genome Announcements, Vol. 1, Issue 3 https://doi.org/10.1128/genomeA.00322-13	journal	May 2013
Metal binding by bacteria from uranium mining waste piles and its technological applications Pollmann, K.; Raff, J.; Merroun, M. Biotechnology Advances, Vol. 24, Issue 1 https://doi.org/10.1016/j.biotechadv.2005.06.002	journal	January 2006
Solid-State NMR Study of the Role of H and Na in AB-Type Carbonate Hydroxylapatite Mason, Harris E.; Kozlowski, Andrew; Phillips, Brian L. Chemistry of Materials, Vol. 20, Issue 1 https://doi.org/10.1021/cm0716598	journal	December 2007
Dynamic interplay between uranyl phosphate precipitation, sorption, and phase evolution Munasinghe, P. Sumudu; Elwood Madden, Megan E.; Brooks, Scott C. Applied Geochemistry, Vol. 58 https://doi.org/10.1016/j.apgeochem.2015.04.008	journal	July 2015
The biogeochemistry and bioremediation of uranium and other priority radionuclides Newsome, Laura; Morris, Katherine; Lloyd, Jonathan R. Chemical Geology, Vol. 363 https://doi.org/10.1016/j.chemgeo.2013.10.034	journal	January 2014
Control of Heterogeneous Fe(III) (Hydr)oxide Nucleation and Growth by Interfacial Energies and Local Saturations Hu, Yandi; Neil, Chelsea; Lee, Byeongdu Environmental Science & Technology, Vol. 47, Issue 16 https://doi.org/10.1021/es401160g	journal	August 2013
Impact of phosphate on U(VI) immobilization in the presence of goethite Singh, Abhas; Ulrich, Kai-Uwe; Giammar, Daniel E. Geochimica et Cosmochimica Acta, Vol. 74, Issue 22 https://doi.org/10.1016/j.gca.2010.08.031	journal	November 2010
Groundwater contamination: pump-and-treat remediation Mackay, Douglas M.; Cherry, John A. Environmental Science & Technology, Vol. 23, Issue 6 https://doi.org/10.1021/es00064a001	journal	June 1989
The crystal structure of synthetic autunite, Ca[(UO ₂ )(PO ₄ )] ₂ (H ₂ O) ₁₁ Locock, Andrew J.; Burns, Peter C. American Mineralogist, Vol. 88, Issue 1 https://doi.org/10.2138/am-2003-0128	journal	January 2003
Effect of co-solutes on the products and solubility of uranium(VI) precipitated with phosphate Mehta, Vrajesh S.; Maillot, Fabien; Wang, Zheming Chemical Geology, Vol. 364 https://doi.org/10.1016/j.chemgeo.2013.12.002	journal	January 2014
Molecular-Scale Structure of Uranium(VI) Immobilized with Goethite and Phosphate Singh, Abhas; Catalano, Jeffrey G.; Ulrich, Kai-Uwe Environmental Science & Technology, Vol. 46, Issue 12 https://doi.org/10.1021/es300494x	journal	May 2012
Uranium Redox Cycling in Sediment and Biomineral Systems Law, Gareth T. W.; Geissler, Andrea; Burke, Ian T. Geomicrobiology Journal, Vol. 28, Issue 5-6 https://doi.org/10.1080/01490451.2010.512033	journal	June 2011
Microbial reduction of uranium Lovley, Derek R.; Phillips, Elizabeth J. P.; Gorby, Yuri A. Nature, Vol. 350, Issue 6317 https://doi.org/10.1038/350413a0	journal	April 1991
Soil Property and Class Maps of the Conterminous United States at 100‐Meter Spatial Resolution Ramcharan, Amanda; Hengl, Tomislav; Nauman, Travis Soil Science Society of America Journal, Vol. 82, Issue 1 https://doi.org/10.2136/sssaj2017.04.0122	journal	January 2018
Microbe Encapsulation for Selective Rare-Earth Recovery from Electronic Waste Leachates Brewer, Aaron; Dohnalkova, Alice; Shutthanandan, Vaithiyalingam Environmental Science & Technology, Vol. 53, Issue 23 https://doi.org/10.1021/acs.est.9b04608	journal	November 2019
Dissolution kinetics of synthetic and natural meta-autunite minerals, X _{3− n} ^{( n )} ⁺ [(UO ₂ )(PO ₄ )] ₂ · xH ₂ O, under acidic conditions : META-AUTUNITE MINERALS Wellman, D. M.; Gunderson, K. M.; Icenhower, J. P. Geochemistry, Geophysics, Geosystems, Vol. 8, Issue 11 https://doi.org/10.1029/2007GC001695	journal	November 2007
The BAM complex subunit BamE (SmpA) is required for membrane integrity, stalk growth and normal levels of outer membrane -barrel proteins in Caulobacter crescentus Ryan, K. R.; Taylor, J. A.; Bowers, L. M. Microbiology, Vol. 156, Issue 3 https://doi.org/10.1099/mic.0.035055-0	journal	December 2009
Biomineralization of Uranium by PhoY Phosphatase Activity Aids Cell Survival in Caulobacter crescentus Yung, Mimi C.; Jiao, Yongqin Applied and Environmental Microbiology, Vol. 80, Issue 16 https://doi.org/10.1128/AEM.01050-14	journal	May 2014
Introduction of a plasmid-encoded phoA gene for constitutive overproduction of alkaline phosphatase in three subsurface Pseudomonas isolates Powers, Leigh G.; Mills, Heath J.; Palumbo, Anthony V. FEMS Microbiology Ecology, Vol. 41, Issue 2 https://doi.org/10.1111/j.1574-6941.2002.tb00972.x	journal	August 2002
Uranium Adsorption on Ferrihydrite - Effects of Phosphate and Humic Acid Payne, Τ. E.; Davis, J. A.; Waite, T. D. Radiochimica Acta, Vol. 74, Issue s1 https://doi.org/10.1524/ract.1996.74.special-issue.239	journal	January 1996
Biomineralization of U(VI) phosphate promoted by microbially-mediated phytate hydrolysis in contaminated soils Salome, Kathleen R.; Beazley, Melanie J.; Webb, Samuel M. Geochimica et Cosmochimica Acta, Vol. 197 https://doi.org/10.1016/j.gca.2016.10.008	journal	January 2017
Bioreduction Behavior of U(VI) Sorbed to Sediments Begg, James D. C.; Burke, Ian T.; Lloyd, Jonathan R. Geomicrobiology Journal, Vol. 28, Issue 2 https://doi.org/10.1080/01490451003761137	journal	February 2011
Interaction of Uranium with Bacterial Cell Surfaces: Inferences from Phosphatase-Mediated Uranium Precipitation Kulkarni, Sayali; Misra, Chitra Seetharam; Gupta, Alka Applied and Environmental Microbiology, Vol. 82, Issue 16 https://doi.org/10.1128/AEM.00728-16	journal	June 2016
Uranium Reduction Wall, Judy D.; Krumholz, Lee R. Annual Review of Microbiology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.micro.59.030804.121357	journal	October 2006
The role of pe, pH, and carbonate on the solubility of UO2 and uraninite under nominally reducing conditions Casas, Ignasi; de Pablo, Joan; Giménez, Javier Geochimica et Cosmochimica Acta, Vol. 62, Issue 13 https://doi.org/10.1016/S0016-7037(98)00140-9	journal	July 1998
Aerobic uranium (VI) bioprecipitation by metal-resistant bacteria isolated from radionuclide- and metal-contaminated subsurface soils Martinez, Robert J.; Beazley, Melanie J.; Taillefert, Martial Environmental Microbiology, Vol. 9, Issue 12 https://doi.org/10.1111/j.1462-2920.2007.01422.x	journal	December 2007
Phosphatase-mediated heavy metal accumulation by a Citrobacter sp. and related enterobacteria Macaskie, L. E.; Bonthrone, K. M.; Rouch, D. A. FEMS Microbiology Letters, Vol. 121, Issue 2 https://doi.org/10.1111/j.1574-6968.1994.tb07090.x	journal	August 1994
The use of Escherichia coli bearing a phoN gene for the removal of uranium and nickel from aqueous flows Basnakova, G.; Stephens, E. R.; Thaller, M. C. Applied Microbiology and Biotechnology, Vol. 50, Issue 2 https://doi.org/10.1007/s002530051288	journal	August 1998
Enzymically mediated bioprecipitation of uranium by a Citrobacter sp.: a concerted role for exocellular lipopolysaccharide and associated phosphatase in biomineral formation Macaskie, Lynne E.; Bonthrone, Karen M.; Yong, Ping Microbiology, Vol. 146, Issue 8 https://doi.org/10.1099/00221287-146-8-1855	journal	August 2000
Geochemical and geophysical responses during the infiltration of fresh water into the contaminated saprolite of the Oak Ridge Integrated Field Research Challenge site, Tennessee: GEOCHEMICAL AND GEOPHYSICAL MONITORING Revil, A.; Wu, Y.; Karaoulis, M. Water Resources Research, Vol. 49, Issue 8 https://doi.org/10.1002/wrcr.20380	journal	August 2013
Effect of Reaction Pathway on the Extent and Mechanism of Uranium(VI) Immobilization with Calcium and Phosphate Mehta, Vrajesh S.; Maillot, Fabien; Wang, Zheming Environmental Science & Technology, Vol. 50, Issue 6 https://doi.org/10.1021/acs.est.5b06212	journal	February 2016
Bacterial interactions with uranium: An environmental perspective Merroun, Mohamed L.; Selenska-Pobell, Sonja Journal of Contaminant Hydrology, Vol. 102, Issue 3-4 https://doi.org/10.1016/j.jconhyd.2008.09.019	journal	December 2008
(Un)suitability of the use of pH buffers in biological, biochemical and environmental studies and their interaction with metal ions – a review Ferreira, Carlos M. H.; Pinto, Isabel S. S.; Soares, Eduardo V. RSC Advances, Vol. 5, Issue 39 https://doi.org/10.1039/C4RA15453C	journal	January 2015
The effect of pH and natural microbial phosphatase activity on the speciation of uranium in subsurface soils Beazley, Melanie J.; Martinez, Robert J.; Webb, Samuel M. Geochimica et Cosmochimica Acta, Vol. 75, Issue 19 https://doi.org/10.1016/j.gca.2011.07.006	journal	October 2011
Comparative Analysis of Soluble Phosphate Amendments for the Remediation of Heavy Metal Contaminants: Effect on Sediment Hydraulic Conductivity Wellman, Dawn M.; Icenhower, Jonathan P.; Owen, Antoinette T. Environmental Chemistry, Vol. 3, Issue 3 https://doi.org/10.1071/EN05023	journal	January 2006
Change in Bacterial Community Structure during In Situ Biostimulation of Subsurface Sediment Cocontaminated with Uranium and Nitrate North, N. N.; Dollhopf, S. L.; Petrie, L. Applied and Environmental Microbiology, Vol. 70, Issue 8 https://doi.org/10.1128/AEM.70.8.4911-4920.2004	journal	August 2004
Role of Cellular Design in Bacterial Metal Accumulation and Mineralization Beveridge, T. J. Annual Review of Microbiology, Vol. 43, Issue 1 https://doi.org/10.1146/annurev.mi.43.100189.001051	journal	October 1989
Uranium Biomineralization as a Result of Bacterial Phosphatase Activity: Insights from Bacterial Isolates from a Contaminated Subsurface Beazley, Melanie J.; Martinez, Robert J.; Sobecky, Patricia A. Environmental Science & Technology, Vol. 41, Issue 16 https://doi.org/10.1021/es070567g	journal	August 2007
Transposon Mutagenesis Paired with Deep Sequencing of Caulobacter crescentus under Uranium Stress Reveals Genes Essential for Detoxification and Stress Tolerance Yung, Mimi C.; Park, Dan M.; Overton, K. Wesley Journal of Bacteriology, Vol. 197, Issue 19 https://doi.org/10.1128/JB.00382-15	journal	July 2015
The cell surface associated phosphatase activity of Mycobacterium bovis BCG is not regulated by environmental inorganic phosphate Braibant, Martine; Content, Jean FEMS Microbiology Letters, Vol. 195, Issue 2 https://doi.org/10.1111/j.1574-6968.2001.tb10508.x	journal	February 2001
Uranium phosphate biomineralization by fungi: Uranium biomineralization by fungi Liang, Xinjin; Hillier, Stephen; Pendlowski, Helen Environmental Microbiology, Vol. 17, Issue 6 https://doi.org/10.1111/1462-2920.12771	journal	March 2015
Modeling of radionuclide and heavy metal sorption around low- and high-pH waste disposal sites at Oak Ridge, Tennessee Saunders, James A.; Toran, Laura E. Applied Geochemistry, Vol. 10, Issue 6 https://doi.org/10.1016/0883-2927(95)00036-4	journal	November 1995
Uranium solution-mineral equilibria at low temperatures with applications to sedimentary ore deposits Langmuir, Donald Geochimica et Cosmochimica Acta, Vol. 42, Issue 6 https://doi.org/10.1016/0016-7037(78)90001-7	journal	June 1978
Enhanced Uranium Immobilization by Phosphate Amendment under Variable Geochemical and Flow Conditions: Insights from Reactive Transport Modeling Wen, Hang; Pan, Zezhen; Giammar, Daniel Environmental Science & Technology, Vol. 52, Issue 10 https://doi.org/10.1021/acs.est.7b05662	journal	April 2018
Sources of anthropogenic radionuclides in the environment: a review Hu, Qin-Hong; Weng, Jian-Qing; Wang, Jin-Sheng Journal of Environmental Radioactivity, Vol. 101, Issue 6 https://doi.org/10.1016/j.jenvrad.2008.08.004	journal	June 2010
Nitrate-Reducing Bacteria at the Nitrate and Radionuclide Contaminated Oak Ridge Integrated Field Research Challenge Site: A Review Spain, Anne M.; Krumholz, Lee R. Geomicrobiology Journal, Vol. 28, Issue 5-6 https://doi.org/10.1080/01490451.2010.507642	journal	June 2011
Isolation and Physiology of Bacteria from Contaminated Subsurface Sediments Bollmann, A.; Palumbo, A. V.; Lewis, K. Applied and Environmental Microbiology, Vol. 76, Issue 22 https://doi.org/10.1128/AEM.00376-10	journal	September 2010
Synthesis and characterization of sodium meta-autunite, Na[UO2PO4]·3H2O Wellman, D. M.; Catalano, J. G.; Icenhower, J. P. Radiochimica Acta, Vol. 93, Issue 7 https://doi.org/10.1524/ract.2005.93.7.393	journal	January 2005
In - Situ Evidence for Uranium Immobilization and Remobilization Senko, John M.; Istok, Jonathan D.; Suflita, Joseph M. Environmental Science & Technology, Vol. 36, Issue 7 https://doi.org/10.1021/es011240x	journal	April 2002
Review of uranyl mineral solubility measurements Gorman-Lewis, Drew; Burns, Peter C.; Fein, Jeremy B. The Journal of Chemical Thermodynamics, Vol. 40, Issue 3 https://doi.org/10.1016/j.jct.2007.12.004	journal	March 2008
Actinide speciation in the environment Choppin, G. R. Journal of Radioanalytical and Nuclear Chemistry, Vol. 273, Issue 3 https://doi.org/10.1007/s10967-007-0933-3	journal	June 2007
Characterizing phosphorus in environmental and agricultural samples by 31P nuclear magnetic resonance spectroscopy Cademenun, B. Talanta, Vol. 66, Issue 2 https://doi.org/10.1016/j.talanta.2004.12.024	journal	April 2005
Uranium bioaccumulation by a Citrobacter sp. as a result of enzymically mediated growth of polycrystalline HUO2PO4 Macaskie, L.; Empson, R.; Cheetham, A. Science, Vol. 257, Issue 5071 https://doi.org/10.1126/science.1496397	journal	August 1992
U-phosphate biomineralization induced by Bacillus sp. dw-2 in the presence of organic acids Tu, Hong; Yuan, Guoyuan; Zhao, Changsong Nuclear Engineering and Technology, Vol. 51, Issue 5 https://doi.org/10.1016/j.net.2019.03.002	journal	August 2019
Phosphate Mineral Reactivity and Global Sustainability Oelkers, E. H.; Valsami-Jones, E. Elements, Vol. 4, Issue 2 https://doi.org/10.2113/GSELEMENTS.4.2.83	journal	April 2008
Sodium meta-autunite colloids: Synthesis, characterization, and stability Zheng, Zuoping; Wan, Jiamin; Song, Xiangyun Colloids and Surfaces A: Physicochemical and Engineering Aspects, Vol. 274, Issue 1-3 https://doi.org/10.1016/j.colsurfa.2005.08.032	journal	February 2006
Enhancement of uranium bioaccumulation by aCitrobacter sp. via enzymically-mediated growth of polycrystalline NH4UO2PO4 Yong, Ping; Macaskie, Lynne E. Journal of Chemical Technology AND Biotechnology, Vol. 63, Issue 2 https://doi.org/10.1002/jctb.280630202	journal	June 1995
Engineering of Deinococcus radiodurans R1 for Bioprecipitation of Uranium from Dilute Nuclear Waste Appukuttan, Deepti; Rao, Amara Sambasiva; Apte, Shree Kumar Applied and Environmental Microbiology, Vol. 72, Issue 12 https://doi.org/10.1128/AEM.01362-06	journal	October 2006
ENVIRONMENT: Avoiding Destructive Remediation at DOE Sites Whicker, F. W. Science, Vol. 303, Issue 5664 https://doi.org/10.1126/science.1093187	journal	March 2004
Uranium Biominerals Precipitated by an Environmental Isolate of Serratia under Anaerobic Conditions Newsome, Laura; Morris, Katherine; Lloyd, Jonathan. R. PLOS ONE, Vol. 10, Issue 7 https://doi.org/10.1371/journal.pone.0132392	journal	July 2015
Natural Uranium Contamination in Major U.S. Aquifers Linked to Nitrate Nolan, Jason; Weber, Karrie A. Environmental Science & Technology Letters, Vol. 2, Issue 8 https://doi.org/10.1021/acs.estlett.5b00174	journal	July 2015
Thermodynamic Properties of Autunite, Uranyl Hydrogen Phosphate, and Uranyl Orthophosphate from Solubility and Calorimetric Measurements Gorman-Lewis, Drew; Shvareva, Tatiana; Kubatko, Karrie-Ann Environmental Science & Technology, Vol. 43, Issue 19 https://doi.org/10.1021/es9012933	journal	October 2009

Similar Records

Biomineralization of Uranium by PhoY Phosphatase Activity Aids Cell Survival in Caulobacter crescentus

Journal Article · Tue Jul 22 00:00:00 EDT 2014 · Applied and Environmental Microbiology · OSTI ID:1787219

Yung, M C; Jiao, Y

Promoting Uranium Immobilization by the Activities of Microbial Phosphatases

Conference · Thu Apr 19 00:00:00 EDT 2007 · OSTI ID:1787219

Martinez, Robert J; Beazley, Melanie J; Webb, Samuel M; +2 more

300 Area Uranium Stabilization Through Polyphosphate Injection: Final Report

Technical Report · Tue Jun 30 00:00:00 EDT 2009 · OSTI ID:1787219

Vermeul, Vincent R; Bjornstad, Bruce N; Fritz, Brad G; +7 more

Related Subjects

38 RADIATION CHEMISTRY, RADIOCHEMISTRY, AND NUCLEAR CHEMISTRY
peptides and proteins
phosphates
solubility
minerals
precipitation

Title: Influence of Uranium Concentration and pH on U-Phosphate Biomineralization by Caulobacter OR37

Citation Formats

References (64)

Similar Records

Related Subjects