Spatial distribution of an uranium-respiring betaproteobacterium at the Rifle, CO field research site

Koribanics, Nicole M.; Tuorto, Steven J.; Lopez-Chiaffarelli, Nora; McGuinness, Lora R.; Häggblom, Max M.; Williams, Kenneth H.; Long, Philip E.; Kerkhof, Lee J.; Morais, Paula V

doi:10.1371/journal.pone.0123378

Title: Spatial distribution of an uranium-respiring betaproteobacterium at the Rifle, CO field research site

Journal Article · Mon Apr 13 00:00:00 EDT 2015 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0123378· OSTI ID:1185054

Koribanics, Nicole M. ^[1]; Tuorto, Steven J. ^[1]; Lopez-Chiaffarelli, Nora ^[1]; McGuinness, Lora R. ^[1]; Häggblom, Max M. ^[1]; Williams, Kenneth H. ^[2]; Long, Philip E. ^[2]; Kerkhof, Lee J. ^[1]; Morais, Paula V ^[3]

Rutgers Univ., New Brunswick, NJ (United States)
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Univ. of Coimbra (Portugal)

The Department of Energy’s Integrated Field-Scale Subsurface Research Challenge Site (IFRC) at Rifle, Colorado was created to address the gaps in knowledge on the mechanisms and rates of U(VI) bioreduction in alluvial sediments. Previous studies at the Rifle IFRC have linked microbial processes to uranium immobilization during acetate amendment. Several key bacteria believed to be involved in radionuclide containment have been described; however, most of the evidence implicating uranium reduction with specific microbiota has been indirect. Here, we report on the cultivation of a microorganism from the Rifle IFRC that reduces uranium and appears to utilize it as a terminal electron acceptor for respiration with acetate as electron donor. Furthermore, this bacterium constitutes a significant proportion of the subsurface sediment community prior to biostimulation based on TRFLP profiling of 16S rRNA genes. 16S rRNA gene sequence analysis indicates that the microorganism is a betaproteobacterium with a high similarity to Burkholderia fungorum. This is, to our knowledge, the first report of a betaproteobacterium capable of uranium respiration. Our results indicate that this microorganism occurs commonly in alluvial sediments located between 3-6 m below ground surface at Rifle and may play a role in the initial reduction of uranium at the site.

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Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC06-76RL01830

OSTI ID:: 1185054

Journal Information:: PLoS ONE, Vol. 10, Issue 4; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 15 works

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References (54)

Stimulating the In Situ Activity of Geobacter Species To Remove Uranium from the Groundwater of a Uranium-Contaminated Aquifer Anderson, R. T.; Vrionis, H. A.; Ortiz-Bernad, I. Applied and Environmental Microbiology, Vol. 69, Issue 10 https://doi.org/10.1128/AEM.69.10.5884-5891.2003	journal	October 2003
Genetic Diversity of Endophytic Diazotrophs of the Wild Rice, Oryza alta and Identification of the New Diazotroph, Acinetobacter oryzae sp. nov. Chaudhary, Hassan Javed; Peng, Guixiang; Hu, Mei Microbial Ecology, Vol. 63, Issue 4 https://doi.org/10.1007/s00248-011-9978-5	journal	November 2011
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
Microbial Community Changes in Response to Ethanol or Methanol Amendments for U(VI) Reduction Vishnivetskaya, T. A.; Brandt, C. C.; Madden, A. S. Applied and Environmental Microbiology, Vol. 76, Issue 17 https://doi.org/10.1128/AEM.00308-10	journal	July 2010
Utilization of Microbial Biofilms as Monitors of Bioremediation Peacock, A. D.; Chang, Y. -J.; Istok, J. D. Microbial Ecology, Vol. 47, Issue 3 https://doi.org/10.1007/s00248-003-1024-9	journal	March 2004
Biodegradation of carbofuran in sequencing batch reactor augmented with immobilised Burkholderia cepacia PCL3 on corncob Plangklang, P.; Reungsang, A. Chemistry and Ecology, Vol. 29, Issue 1 https://doi.org/10.1080/02757540.2012.686609	journal	January 2013
Burkholderia fungorum DBT1: a promising bacterial strain for bioremediation of PAHs-contaminated soils: Burkholderia fungorum DBT1 for soil bioremediation Andreolli, Marco; Lampis, Silvia; Zenaro, Elena FEMS Microbiology Letters, Vol. 319, Issue 1 https://doi.org/10.1111/j.1574-6968.2011.02259.x	journal	March 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
Modeling Reduction of Uranium U(VI) under Variable Sulfate Concentrations by Sulfate-Reducing Bacteria Spear, J. R.; Figueroa, L. A.; Honeyman, B. D. Applied and Environmental Microbiology, Vol. 66, Issue 9 https://doi.org/10.1128/AEM.66.9.3711-3721.2000	journal	September 2000
Importance of c-Type cytochromes for U(VI) reduction by Geobacter sulfurreducens Shelobolina, Evgenya S.; Coppi, Maddalena V.; Korenevsky, Anton A. BMC Microbiology, Vol. 7, Issue 1 https://doi.org/10.1186/1471-2180-7-16	journal	January 2007
Bacterial communities in tetrachloroethene-polluted groundwaters: A case study Kotik, Michael; Davidová, Anna; Voříšková, Jana Science of The Total Environment, Vol. 454-455 https://doi.org/10.1016/j.scitotenv.2013.02.082	journal	June 2013
Microbial reduction of uranium under iron- and sulfate-reducing conditions: Effect of amended goethite on microbial community composition and dynamics Moon, H. S.; McGuinness, L.; Kukkadapu, R. K. Water Research, Vol. 44, Issue 14 https://doi.org/10.1016/j.watres.2010.05.003	journal	July 2010
Phase Preference by Active, Acetate-Utilizing Bacteria at the Rifle, CO Integrated Field Research Challenge Site Kerkhof, Lee J.; Williams, Ken H.; Long, Philip E. Environmental Science & Technology, Vol. 45, Issue 4 https://doi.org/10.1021/es102893r	journal	February 2011
Hexavalent uranium supports growth of Anaeromyxobacter dehalogenans and Geobacter spp. with lower than predicted biomass yields Sanford, Robert A.; Wu, Qingzhong; Sung, Youlboong Environmental Microbiology, Vol. 9, Issue 11 https://doi.org/10.1111/j.1462-2920.2007.01405.x	journal	November 2007
Enrichment of Members of the Family Geobacteraceae Associated with Stimulation of Dissimilatory Metal Reduction in Uranium-Contaminated Aquifer Sediments Holmes, D. E.; Finneran, K. T.; O'Neil, R. A. Applied and Environmental Microbiology, Vol. 68, Issue 5 https://doi.org/10.1128/AEM.68.5.2300-2306.2002	journal	May 2002
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
In Situ Bioreduction of Technetium and Uranium in a Nitrate-Contaminated Aquifer Istok, J. D.; Senko, J. M.; Krumholz, L. R. Environmental Science & Technology, Vol. 38, Issue 2 https://doi.org/10.1021/es034639p	journal	January 2004
Proteogenomic Monitoring of Geobacter Physiology during Stimulated Uranium Bioremediation Wilkins, M. J.; VerBerkmoes, N. C.; Williams, K. H. Applied and Environmental Microbiology, Vol. 75, Issue 20 https://doi.org/10.1128/AEM.01064-09	journal	August 2009
Microbial Incorporation of ¹³ C-Labeled Acetate at the Field Scale: Detection of Microbes Responsible for Reduction of U(VI) Chang, Yun-Juan; Long, Philip E.; Geyer, Roland Environmental Science & Technology, Vol. 39, Issue 23 https://doi.org/10.1021/es051218u	journal	December 2005
Multiple influences of nitrate on uranium solubility during bioremediation of uranium-contaminated subsurface sediments Finneran, Kevin T.; Housewright, Meghan E.; Lovley, Derek R. Environmental Microbiology, Vol. 4, Issue 9 https://doi.org/10.1046/j.1462-2920.2002.00317.x	journal	September 2002
Reduction of Uranium(VI) Phosphate during Growth of the Thermophilic Bacterium Thermoterrabacterium ferrireducens Khijniak, T. V.; Slobodkin, A. I.; Coker, V. Applied and Environmental Microbiology, Vol. 71, Issue 10 https://doi.org/10.1128/AEM.71.10.6423-6426.2005	journal	October 2005
Microbial community dynamics in uranium contaminated subsurface sediments under biostimulated conditions with high nitrate and nickel pressure Moreels, David; Crosson, Garry; Garafola, Craig Environmental Science and Pollution Research, Vol. 15, Issue 6 https://doi.org/10.1007/s11356-008-0034-z	journal	August 2008
Acetate Availability and its Influence on Sustainable Bioremediation of Uranium-Contaminated Groundwater Williams, Kenneth H.; Long, Philip E.; Davis, James A. Geomicrobiology Journal, Vol. 28, Issue 5-6 https://doi.org/10.1080/01490451.2010.520074	journal	June 2011
Characterization of hydrocarbon-degrading bacterial strains isolated from oil-polluted soil Tanase, Ana-Maria; Ionescu, Robertina; Chiciudean, Iulia International Biodeterioration & Biodegradation, Vol. 84 https://doi.org/10.1016/j.ibiod.2012.05.022	journal	October 2013
Composition, stability, and measurement of reduced uranium phases for groundwater bioremediation at Old Rifle, CO Campbell, K. M.; Davis, J. A.; Bargar, J. Applied Geochemistry, Vol. 26 https://doi.org/10.1016/j.apgeochem.2011.03.094	journal	June 2011
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
Geobacter uraniireducens sp. nov., isolated from subsurface sediment undergoing uranium bioremediation Shelobolina, E. S.; Vrionis, H. A.; Findlay, R. H. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 58, Issue 5 https://doi.org/10.1099/ijs.0.65377-0	journal	May 2008
Burkholderia fungorum sp. nov. and Burkholderia caledonica sp. nov., two new species isolated from the environment, animals and human clinical samples Coenye, T.; Laevens, S.; Willems, A. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 51, Issue 3 https://doi.org/10.1099/00207713-51-3-1099	journal	May 2001
Trends between gene content and genome size in prokaryotic species with larger genomes Konstantinidis, K. T.; Tiedje, J. M. Proceedings of the National Academy of Sciences, Vol. 101, Issue 9 https://doi.org/10.1073/pnas.0308653100	journal	February 2004
Inhibition of Bacterial U(VI) Reduction by Calcium Brooks, Scott C.; Fredrickson, James K.; Carroll, Sue L. Environmental Science & Technology, Vol. 37, Issue 9 https://doi.org/10.1021/es0210042	journal	May 2003
Replicability of Bacterial Communities in Denitrifying Bioreactors as Measured by PCR/T-RFLP Analysis McGuinness, Lora M.; Salganik, Max; Vega, Leticia Environmental Science & Technology, Vol. 40, Issue 2 https://doi.org/10.1021/es050900l	journal	January 2006
Geobacter bemidjiensis sp. nov. and Geobacter psychrophilus sp. nov., two novel Fe(III)-reducing subsurface isolates Nevin, K. P. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 55, Issue 4 https://doi.org/10.1099/ijs.0.63417-0	journal	July 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
Sulfate-reducing bacterium grows with Cr(VI), U(VI), Mn(IV), and Fe(III) as electron acceptors Tebo, Bradley M.; Obraztsova, Anna Ya FEMS Microbiology Letters, Vol. 162, Issue 1 https://doi.org/10.1111/j.1574-6968.1998.tb12998.x	journal	May 1998
Geobacter daltonii sp. nov., an Fe(III)- and uranium(VI)-reducing bacterium isolated from a shallow subsurface exposed to mixed heavy metal and hydrocarbon contamination Prakash, O.; Gihring, T. M.; Dalton, D. D. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 60, Issue 3 https://doi.org/10.1099/ijs.0.010843-0	journal	August 2009
Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility Chain, P. S. G.; Denef, V. J.; Konstantinidis, K. T. Proceedings of the National Academy of Sciences, Vol. 103, Issue 42 https://doi.org/10.1073/pnas.0606924103	journal	October 2006
Adaptation and Antibiotic Tolerance of Anaerobic Burkholderia pseudomallei Hamad, Mohamad A.; Austin, Chad R.; Stewart, Amanda L. Antimicrobial Agents and Chemotherapy, Vol. 55, Issue 7 https://doi.org/10.1128/AAC.00953-10	journal	May 2011
A Simple, Fast, and Accurate Algorithm to Estimate Large Phylogenies by Maximum Likelihood Guindon, Stéphane; Gascuel, Olivier Systematic Biology, Vol. 52, Issue 5 https://doi.org/10.1080/10635150390235520	journal	October 2003
Electrode-Based Approach for Monitoring In Situ Microbial Activity During Subsurface Bioremediation Williams, Kenneth H.; Nevin, Kelly P.; Franks, Ashley Environmental Science & Technology, Vol. 44, Issue 1 https://doi.org/10.1021/es9017464	journal	January 2010
Geochemical and mineralogical investigation of uranium in multi-element contaminated, organic-rich subsurface sediment Qafoku, Nikolla P.; Gartman, Brandy N.; Kukkadapu, Ravi K. Applied Geochemistry, Vol. 42 https://doi.org/10.1016/j.apgeochem.2013.12.001	journal	March 2014
Growth and cometabolic reduction kinetics of a uranium- and sulfate-reducingDesulfovibrio/Clostridia mixed culture: Temperature effects Boonchayaanant, Benjaporn; Kitanidis, Peter K.; Criddle, Craig S. Biotechnology and Bioengineering, Vol. 99, Issue 5 https://doi.org/10.1002/bit.21670	journal	January 2008
Degradation of Aromatic Compounds Coupled to Selenate Reduction Knight, Victoria K.; Nijenhuis, Ivonne; Kerkhof, Lee J. Geomicrobiology Journal, Vol. 19, Issue 1 https://doi.org/10.1080/014904502317246183	journal	January 2002
Uranium redox transition pathways in acetate-amended sediments Bargar, J. R.; Williams, K. H.; Campbell, K. M. Proceedings of the National Academy of Sciences, Vol. 110, Issue 12 https://doi.org/10.1073/pnas.1219198110	journal	March 2013
Nitrate-dependent anaerobic carbon monoxide oxidation by aerobic CO-oxidizing bacteria: Nitrate-dependent CO oxidation King, G. M. FEMS Microbiology Ecology, Vol. 56, Issue 1 https://doi.org/10.1111/j.1574-6941.2006.00065.x	journal	April 2006
Reduction of uranium by Desulfovibrio desulfuricans. Lovley, D. R.; Phillips, E. J. Applied and Environmental Microbiology, Vol. 58, Issue 3 https://doi.org/10.1128/AEM.58.3.850-856.1992	journal	January 1992
Studies revealing bioremediation potential of the strain Burkholderia sp. GB-01 for abamectin contaminated soils Ali, Shinawar Waseem; Yu, Fang-bo; Li, Lian-tai World Journal of Microbiology and Biotechnology, Vol. 28, Issue 1 https://doi.org/10.1007/s11274-011-0790-7	journal	May 2011
Bicarbonate impact on U(VI) bioreduction in a shallow alluvial aquifer Long, Philip E.; Williams, Kenneth H.; Davis, James A. Geochimica et Cosmochimica Acta, Vol. 150 https://doi.org/10.1016/j.gca.2014.11.013	journal	February 2015
Biodegradation of quinoline by gel immobilized Burkholderia sp. Jianlong, Wang; Liping, Han; Hanchang, Shi Chemosphere, Vol. 44, Issue 5 https://doi.org/10.1016/s0045-6535(00)00469-0	journal	August 2001
Fe(III) reduction activity and cytochrome content of Shewanella putrefaciens grown on ten compounds as sole terminal electron acceptor Blakeney, M. D.; Moulaei, T.; Dichristina, T. J. Microbiological Research, Vol. 155, Issue 2 https://doi.org/10.1016/s0944-5013(00)80042-7	journal	January 2000
Assessment of Changes in Microbial Community Structure during Operation of an Ammonia Biofilter with Molecular Tools Sakano, Y.; Kerkhof, L. Applied and Environmental Microbiology, Vol. 64, Issue 12 https://doi.org/10.1128/aem.64.12.4877-4882.1998	journal	December 1998
Detection and Characterization of a Dehalogenating Microorganism by Terminal Restriction Fragment Length Polymorphism Fingerprinting of 16S rRNA in a Sulfidogenic, 2-Bromophenol-Utilizing Enrichment Fennell, D. E.; Rhee, S. -K.; Ahn, Y. -B. Applied and Environmental Microbiology, Vol. 70, Issue 2 https://doi.org/10.1128/aem.70.2.1169-1175.2004	journal	February 2004
Biphenyl and Benzoate Metabolism in a Genomic Context: Outlining Genome-Wide Metabolic Networks in Burkholderia xenovorans LB400 Denef, V. J.; Park, J.; Tsoi, T. V. Applied and Environmental Microbiology, Vol. 70, Issue 8 https://doi.org/10.1128/aem.70.8.4961-4970.2004	journal	August 2004
Microbiological and Geochemical Heterogeneity in an In Situ Uranium Bioremediation Field Site Vrionis, H. A.; Anderson, R. T.; Ortiz-Bernad, I. Applied and Environmental Microbiology, Vol. 71, Issue 10 https://doi.org/10.1128/aem.71.10.6308-6318.2005	journal	October 2005
Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility Reyes, V. L.; Marx, C. J.; Spilker, T. National Academy of Sciences NAS https://doi.org/10.7892/boris.91420	text	January 2006

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