Correlative Cryogenic Spectromicroscopy to Investigate Selenium Bioreduction Products

Fakra, Sirine C.; Luef, Birgit; Castelle, Cindy J.; Mullin, Sean W.; Williams, Kenneth H.; Marcus, Matthew A.; Schichnes, Denise; Banfield, Jillian F.

doi:10.1021/acs.est.5b01409

Correlative Cryogenic Spectromicroscopy to Investigate Selenium Bioreduction Products

Journal Article · Thu Dec 28 23:00:00 EST 2017 · Environmental Science and Technology

DOI:https://doi.org/10.1021/acs.est.5b01409· OSTI ID:1512106

Fakra, Sirine C. ^[1]; Luef, Birgit ^[2]; Castelle, Cindy J. ^[2]; Mullin, Sean W. ^[2]; Williams, Kenneth H. ^[3]; Marcus, Matthew A. ^[4]; Schichnes, Denise ^[5]; Banfield, Jillian F. ^[6]

Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)
Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Earth Sciences Division
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS)
Univ. of California, Berkeley, CA (United States). Dept. of Plant & Microbial Biology
Univ. of California, Berkeley, CA (United States). Dept. of Earth and Planetary Science; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Earth Sciences Division

Accurate mapping of the composition and structure of minerals and associated biological materials is critical in geomicrobiology and environmental research. Here we developed an apparatus allowing correlation of cryogenic transmission electron microscopy (TEM) and synchrotron hard X-ray microprobe (SHXM) datasets to precisely determine the distribution, valence state and structure of selenium in biofilms sampled from a contaminated aquifer near Rifle, CO, USA. Results were replicated in the laboratory via anaerobic selenate-reducing enrichment cultures. 16S rRNA analyses of field-derived biofilm indicated the dominance of Beta proteobacteria from the Comamonadaceae family, and uncultivated members of the Simplicispira genus. The major product in field and culture-derived biofilms is ∼25-300nm red amorphous Se⁰ aggregates of colloidal nanoparticles. Correlative analyses of the cultures provided direct evidence for microbial dissimilatory reduction of Se(VI) to Se(IV) to Se⁰. Extended X-ray absorption fine structure spectroscopy showed red amorphous Se⁰ with a first shell Se-Se interatomic distance of 2.339 ± 0.003Å. Complementary scanning transmission X-ay microscopy revealed that these aggregates are strongly associated with a protein-rich biofilm matrix. These findings have important implications for predicting the stability and mobility of Se bioremediation products and understanding of Se biogeochemical cycling. The approach, involving correlation of cryo-SHXM and cryo-TEM datasets from the same specimen area, is broadly applicable to biological and environmental samples Published by American Chemical Society.

View Accepted Manuscript (DOE)

Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1512106

Alternate ID(s):: OSTI ID: 1530328

Journal Information:: Environmental Science and Technology, Journal Name: Environmental Science and Technology Journal Issue: 2 Vol. 52; ISSN 0013-936X

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (88)

A portable cryo-plunger for on-site intact cryogenic microscopy sample preparation in natural environments Comolli, Luis R.; Duarte, Robert; Baum, Dennis Microscopy Research and Technique, Vol. 75, Issue 6 https://doi.org/10.1002/jemt.22001	journal	December 2011
The Genus Zoogloea Dugan, Patrick R.; Stoner, Daphne L.; Pickrum, Harvey M. The Prokaryotes https://doi.org/10.1007/0-387-30747-8_42	book	January 2006
Transformation of selenate and selenite to elemental selenium byDesulfovibrio desulfuricans Tomei, Francisco A.; Barton, Larry L.; Lemanski, Cheryl L. Journal of Industrial Microbiology, Vol. 14, Issue 3-4 https://doi.org/10.1007/BF01569947	journal	March 1995
Ferribacterium limneticum , gen. nov., sp. nov., an Fe(III)-reducing microorganism isolated from mining-impacted freshwater lake sediments Cummings, David E.; Caccavo Jr., Frank; Spring, Stefan Archives of Microbiology, Vol. 171, Issue 3 https://doi.org/10.1007/s002030050697	journal	February 1999
Community structure and function in a H2-based membrane biofilm reactor capable of bioreduction of selenate and chromate Chung, Jinwook; Ryu, Hodon; Abbaszadegan, Morteza Applied Microbiology and Biotechnology, Vol. 72, Issue 6 https://doi.org/10.1007/s00253-006-0439-x	journal	May 2006
Reduction of Selenite to Elemental Red Selenium by Pseudomonas sp. Strain CA5 Hunter, William J.; Manter, Daniel K. Current Microbiology, Vol. 58, Issue 5 https://doi.org/10.1007/s00284-009-9358-2	journal	February 2009
Determination of chemical-structural changes in vitrinite accompanying luminescence alteration using C-NEXAFS analysis Cody, G. D.; Ade, H.; Wirick, S. Organic Geochemistry, Vol. 28, Issue 7-8 https://doi.org/10.1016/S0146-6380(98)00010-2	journal	May 1998
The biofilm matrix – an immobilized but dynamic microbial environment Sutherland, I. Trends in Microbiology, Vol. 9, Issue 5 https://doi.org/10.1016/S0966-842X(01)02012-1	journal	May 2001
Geochemical, mineralogical and microbiological characteristics of sediment from a naturally reduced zone in a uranium-contaminated aquifer Campbell, K. M.; Kukkadapu, R. K.; Qafoku, N. P. Applied Geochemistry, Vol. 27, Issue 8 https://doi.org/10.1016/j.apgeochem.2012.04.013	journal	August 2012
Characterization of a novel selenium methyltransferase from freshwater bacteria showing strong similarities with the calicheamicin methyltransferase Ranjard, Lionel; Prigent-Combaret, Claire; Favre-Bonté, Sabine Biochimica et Biophysica Acta (BBA) - Gene Structure and Expression, Vol. 1679, Issue 1 https://doi.org/10.1016/j.bbaexp.2004.05.001	journal	July 2004
Soft X-ray induced chemical modification of polysaccharides in vascular plant cell walls Cody, George D.; Brandes, Jay; Jacobsen, Chris Journal of Electron Spectroscopy and Related Phenomena, Vol. 170, Issue 1-3 https://doi.org/10.1016/j.elspec.2008.09.007	journal	March 2009
Some practical considerations about the effects of radiation damage on hydrated cells imaged by X-ray fluorescence microscopy Fayard, B.; Salomé, M.; Takemoto, K. Journal of Electron Spectroscopy and Related Phenomena, Vol. 170, Issue 1-3 https://doi.org/10.1016/j.elspec.2008.11.003	journal	March 2009
Introduction: Special issue on radiation damage Howells, Malcolm R.; Hitchcock, Adam P.; Jacobsen, Chris J. Journal of Electron Spectroscopy and Related Phenomena, Vol. 170, Issue 1-3 https://doi.org/10.1016/j.elspec.2009.01.004	journal	March 2009
Dose tolerance at helium and nitrogen temperatures for whole cell electron tomography Comolli, Luis R.; Downing, Kenneth H. Journal of Structural Biology, Vol. 152, Issue 3 https://doi.org/10.1016/j.jsb.2005.08.004	journal	December 2005
Biosynthesis and structural characterization of selenium nanoparticles mediated by Zooglea ramigera Srivastava, Nishant; Mukhopadhyay, Mausumi Powder Technology, Vol. 244 https://doi.org/10.1016/j.powtec.2013.03.050	journal	August 2013
Supplementing Bacillus sp. RS1 with Dechloromonas sp. HZ for enhancing selenate reduction in agricultural drainage water Zhang, Y.; Frankenbergerjr, W. Science of The Total Environment, Vol. 372, Issue 2-3 https://doi.org/10.1016/j.scitotenv.2006.10.027	journal	January 2007
Quantitative Speciation of Selenium in Soils Using X-ray Absorption Spectroscopy Pickering, Ingrid J.; Brown, Gordon E.; Tokunaga, Tetsu K. Environmental Science & Technology, Vol. 29, Issue 9 https://doi.org/10.1021/es00009a043	journal	September 1995
Microscopically Focused Synchrotron X-ray Investigation of Selenium Speciation in Soils Developing on Reclaimed Mine Lands Ryser, Amy L.; Strawn, Daniel G.; Marcus, Matthew A. Environmental Science & Technology, Vol. 40, Issue 2 https://doi.org/10.1021/es051674i	journal	January 2006
Combined Speciation Analysis by X-ray Absorption Near-Edge Structure Spectroscopy, Ion Chromatography, and Solid-Phase Microextraction Gas Chromatography−Mass Spectrometry To Evaluate Biotreatment of Concentrated Selenium Wastewaters Lenz, Markus; van Hullebusch, Eric D.; Farges, François Environmental Science & Technology, Vol. 45, Issue 3 https://doi.org/10.1021/es1022619	journal	February 2011
Colloidal Properties of Nanoparticular Biogenic Selenium Govern Environmental Fate and Bioremediation Effectiveness Buchs, Benjamin; Evangelou, Michael W. H.; Winkel, Lenny H. E. Environmental Science & Technology, Vol. 47, Issue 5 https://doi.org/10.1021/es304940s	journal	February 2013
Vanadate and Acetate Biostimulation of Contaminated Sediments Decreases Diversity, Selects for Specific Taxa, and Decreases Aqueous V ⁵⁺ Concentration Yelton, Alexis P.; Williams, Kenneth H.; Fournelle, John Environmental Science & Technology, Vol. 47, Issue 12 https://doi.org/10.1021/es4006674	journal	May 2013
Nitrate Shaped the Selenate-Reducing Microbial Community in a Hydrogen-Based Biofilm Reactor Lai, Chun-Yu; Yang, Xiaoe; Tang, Youneng Environmental Science & Technology, Vol. 48, Issue 6 https://doi.org/10.1021/es4053939	journal	March 2014
Uranium Bioreduction Rates across Scales: Biogeochemical Hot Moments and Hot Spots during a Biostimulation Experiment at Rifle, Colorado Bao, Chen; Wu, Hongfei; Li, Li Environmental Science & Technology, Vol. 48, Issue 17 https://doi.org/10.1021/es501060d	journal	August 2014
Influence of Heterogeneous Ammonium Availability on Bacterial Community Structure and the Expression of Nitrogen Fixation and Ammonium Transporter Genes during in Situ Bioremediation of Uranium-Contaminated Groundwater Mouser, Paula J.; N’Guessan, A. Lucie; Elifantz, Hila Environmental Science & Technology, Vol. 43, Issue 12 https://doi.org/10.1021/es8031055	journal	June 2009
Microbial Oxidation of Elemental Selenium in Soil Slurries and Bacterial Cultures Dowdle, Philip R.; Oremland, Ronald S. Environmental Science & Technology, Vol. 32, Issue 23 https://doi.org/10.1021/es970940s	journal	December 1998
La ₂ U ₂ Se ₉ : An Ordered Lanthanide/Actinide Chalcogenide with a Novel Structure Type Bugaris, Daniel E.; Copping, Roy; Tyliszczak, Tolek Inorganic Chemistry, Vol. 49, Issue 5 https://doi.org/10.1021/ic902503n	journal	March 2010
Biomineralization of Fine Selenium Crystalline Rods and Amorphous Spheres Kaur, Gurinder; Iqbal, Mohammad; Bakshi, Mandeep Singh The Journal of Physical Chemistry C, Vol. 113, Issue 31 https://doi.org/10.1021/jp903685g	journal	July 2009
A Selenium Cycle in Nature? Shrift, A. Nature, Vol. 201, Issue 4926 https://doi.org/10.1038/2011304a0	journal	March 1964
Anaerobic benzene oxidation coupled to nitrate reduction in pure culture by two strains of Dechloromonas Coates, John D.; Chakraborty, Romy; Lack, Joseph G. Nature, Vol. 411, Issue 6841 https://doi.org/10.1038/35082545	journal	June 2001
Molecular analysis of phosphate limitation in Geobacteraceae during the bioremediation of a uranium-contaminated aquifer N'Guessan, A. Lucie; Elifantz, Hila; Nevin, Kelly P. The ISME Journal, Vol. 4, Issue 2 https://doi.org/10.1038/ismej.2009.115	journal	December 2009
Iron-reducing bacteria accumulate ferric oxyhydroxide nanoparticle aggregates that may support planktonic growth Luef, Birgit; Fakra, Sirine C.; Csencsits, Roseann The ISME Journal, Vol. 7, Issue 2 https://doi.org/10.1038/ismej.2012.103	journal	October 2012
Biostimulation induces syntrophic interactions that impact C, S and N cycling in a sediment microbial community Handley, Kim M.; VerBerkmoes, Nathan C.; Steefel, Carl I. The ISME Journal, Vol. 7, Issue 4 https://doi.org/10.1038/ismej.2012.148	journal	November 2012
Metabolic interdependencies between phylogenetically novel fermenters and respiratory organisms in an unconfined aquifer Wrighton, Kelly C.; Castelle, Cindy J.; Wilkins, Michael J. The ISME Journal, Vol. 8, Issue 7 https://doi.org/10.1038/ismej.2013.249	journal	March 2014
The biological role of death and lysis in biofilm development Bayles, Kenneth W. Nature Reviews Microbiology, Vol. 5, Issue 9 https://doi.org/10.1038/nrmicro1743	journal	September 2007
Multimetal resistance and tolerance in microbial biofilms Harrison, Joe J.; Ceri, Howard; Turner, Raymond J. Nature Reviews Microbiology, Vol. 5, Issue 12 https://doi.org/10.1038/nrmicro1774	journal	December 2007
Cryo-electron tomography of bacteria: progress, challenges and future prospects Milne, Jacqueline L. S.; Subramaniam, Sriram Nature Reviews Microbiology, Vol. 7, Issue 9 https://doi.org/10.1038/nrmicro2183	journal	August 2009
The biofilm matrix Flemming, Hans-Curt; Wingender, Jost Nature Reviews Microbiology, Vol. 8, Issue 9 https://doi.org/10.1038/nrmicro2415	journal	August 2010
Biotransformation of selenium and arsenic in multi-species biofilm Yang, Soo In; Lawrence, John R.; Swerhone, George D. W. Environmental Chemistry, Vol. 8, Issue 6 https://doi.org/10.1071/EN11062	journal	January 2011
A bacterial process for selenium nanosphere assembly Debieux, C. M.; Dridge, E. J.; Mueller, C. M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 33 https://doi.org/10.1073/pnas.1105959108	journal	August 2011
Local Sequence Dependence of Polyhydroxyalkanoic Acid Degradation in Hydrogenophaga pseudoflava Yoon, Sung Chul; Choi, Mun Hwan Journal of Biological Chemistry, Vol. 274, Issue 53 https://doi.org/10.1074/jbc.274.53.37800	journal	December 1999
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
Investigating different mechanisms for biogenic selenite transformations: Geobacter sulfurreducens , Shewanella oneidensis and Veillonella atypica Pearce, Carolyn I.; Pattrick, Richard A. D.; Law, Nicholas Environmental Technology, Vol. 30, Issue 12 https://doi.org/10.1080/09593330902984751	journal	November 2009
Reduction of Elemental Selenium to Selenide: Experiments with Anoxic Sediments and Bacteria that Respire Se-Oxyanions Herbel, Mitchell J.; Blum, Jodi Switzer; Oremland, Ronald S. Geomicrobiology Journal, Vol. 20, Issue 6 https://doi.org/10.1080/713851163	journal	November 2003
Role of proteins in controlling selenium nanoparticle size Dobias, J.; Suvorova, E. I.; Bernier-Latmani, R. Nanotechnology, Vol. 22, Issue 19 https://doi.org/10.1088/0957-4484/22/19/195605	journal	March 2011
Hydrogenophaga, a New Genus of Hydrogen-Oxidizing Bacteria That Includes Hydrogenophaga flava comb. nov. (Formerly Pseudomonas flava), Hydrogenophaga palleronii (Formerly Pseudomonas palleronii), Hydrogenophaga pseudoflava (Formerly Pseudomonas pseudoflava and "Pseudomonas carboxydoflava"), and Hydrogenophaga taeniospiralis (Formerly Pseudomonas taeniospiralis) Willems, A.; Busse, J.; Goor, M. International Journal of Systematic Bacteriology, Vol. 39, Issue 3 https://doi.org/10.1099/00207713-39-3-319	journal	July 1989
Malikia granosa gen. nov., sp. nov., a novel polyhydroxyalkanoate- and polyphosphate-accumulating bacterium isolated from activated sludge, and reclassification of Pseudomonas spinosa as Malikia spinosa comb. nov. Spring, Stefan; Wagner, Michael; Schumann, Peter International Journal of Systematic and Evolutionary Microbiology, Vol. 55, Issue 2 https://doi.org/10.1099/ijs.0.63356-0	journal	March 2005
Proposal of Giesbergeria voronezhensis gen. nov., sp. nov. and G. kuznetsovii sp. nov. and reclassification of [Aquaspirillum] anulus, [A.] sinuosum and [A.] giesbergeri as Giesbergeria anulus comb. nov., G. sinuosa comb. nov. and G. giesbergeri comb. nov., and [Aquaspirillum] metamorphum and [A.] psychrophilum as Simplicispira metamorpha gen. nov., comb. nov. and S. psychrophila comb. nov. Grabovich, Margarita; Gavrish, Ekaterina; Kuever, Jan International Journal of Systematic and Evolutionary Microbiology, Vol. 56, Issue 3 https://doi.org/10.1099/ijs.0.64027-0	journal	March 2006
Effect of pressure on the atom positions in Se and Te Keller, R.; Holzapfel, W. B.; Schulz, Heinz Physical Review B, Vol. 16, Issue 10 https://doi.org/10.1103/PhysRevB.16.4404	journal	November 1977
Structural study of amorphous selenium by in situ EXAFS: Observation of photoinduced bond alternation Kolobov, Alexander V.; Oyanagi, Hiroyuki; Tanaka, Kazunobu Physical Review B, Vol. 55, Issue 2 https://doi.org/10.1103/PhysRevB.55.726	journal	January 1997
XAFS study of interchain and intrachain order in Se 1 − x Te x glasses: Nearest neighbors Majid, M.; Bénazeth, S.; Souleau, C. Physical Review B, Vol. 58, Issue 10 https://doi.org/10.1103/PhysRevB.58.6104	journal	September 1998
Selenium Accumulation, Distribution, and Speciation in Spineless Prickly Pear Cactus: A Drought- and Salt-Tolerant, Selenium-Enriched Nutraceutical Fruit Crop for Biofortified Foods Bañuelos, Gary S.; Fakra, Sirine C.; Walse, Spencer S. Plant Physiology, Vol. 155, Issue 1 https://doi.org/10.1104/pp.110.162867	journal	November 2010
IFEFFIT : interactive XAFS analysis and FEFF fitting Newville, Matthew Journal of Synchrotron Radiation, Vol. 8, Issue 2 https://doi.org/10.1107/S0909049500016964	journal	March 2001
Beamline 10.3.2 at ALS: a hard X-ray microprobe for environmental and materials sciences Marcus, Matthew A.; MacDowell, Alastair A.; Celestre, Richard Journal of Synchrotron Radiation, Vol. 11, Issue 3 https://doi.org/10.1107/S0909049504005837	journal	April 2004
ATHENA , ARTEMIS , HEPHAESTUS : data analysis for X-ray absorption spectroscopy using IFEFFIT Ravel, B.; Newville, M. Journal of Synchrotron Radiation, Vol. 12, Issue 4 https://doi.org/10.1107/S0909049505012719	journal	June 2005
XANES measurements of the rate of radiation damage to selenomethionine side chains Holton, James M. Journal of Synchrotron Radiation, Vol. 14, Issue 1 https://doi.org/10.1107/S0909049506048898	journal	December 2006
Synchrotron-radiation-induced oxidation of selenite to selenate in coal-derived fly ash Huggins, Frank E.; Sanei, Hamed Journal of Synchrotron Radiation, Vol. 18, Issue 3 https://doi.org/10.1107/S0909049511002627	journal	March 2011
X-ray-induced photo-chemistry and X-ray absorption spectroscopy of biological samples George, Graham N.; Pickering, Ingrid J.; Pushie, M. Jake Journal of Synchrotron Radiation, Vol. 19, Issue 6 https://doi.org/10.1107/S090904951203943X	journal	October 2012
Field evidence of selenium bioreduction in a uranium-contaminated aquifer: Field evidence of selenium bioreduction Williams, Kenneth H.; Wilkins, Michael J.; N'Guessan, A. Lucie Environmental Microbiology Reports, Vol. 5, Issue 3 https://doi.org/10.1111/1758-2229.12032	journal	February 2013
High-density PhyloChip profiling of stimulated aquifer microbial communities reveals a complex response to acetate amendment Handley, Kim M.; Wrighton, Kelly C.; Piceno, Yvette M. FEMS Microbiology Ecology, Vol. 81, Issue 1 https://doi.org/10.1111/j.1574-6941.2012.01363.x	journal	April 2012
Intracellular degradation of poly(3-hydroxybutyrate) granules of Zoogloea ramigera I-16-M Saito, T.; Saegusa, H.; Miyata, Y. FEMS Microbiology Letters, Vol. 103, Issue 2-4 https://doi.org/10.1111/j.1574-6968.1992.tb05855.x	journal	December 1992
Extracellular Proteins Limit the Dispersal of Biogenic Nanoparticles Moreau, J. W.; Weber, P. K.; Martin, M. C. Science, Vol. 316, Issue 5831 https://doi.org/10.1126/science.1141064	journal	June 2007
Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla Wrighton, K. C.; Thomas, B. C.; Sharon, I. Science, Vol. 337, Issue 6102 https://doi.org/10.1126/science.1224041	journal	September 2012
Shedding Light on Selenium Biomineralization: Proteins Associated with Bionanominerals Lenz, Markus; Kolvenbach, Boris; Gygax, Benjamin Applied and Environmental Microbiology, Vol. 77, Issue 13 https://doi.org/10.1128/AEM.01713-10	journal	May 2011
Imaging Hydrated Microbial Extracellular Polymers: Comparative Analysis by Electron Microscopy Dohnalkova, Alice C.; Marshall, Matthew J.; Arey, Bruce W. Applied and Environmental Microbiology, Vol. 77, Issue 4 https://doi.org/10.1128/AEM.02001-10	journal	December 2010
Reduction of Selenate to Selenide by Sulfate-Respiring Bacteria: Experiments with Cell Suspensions and Estuarine Sediments Zehr, Jonathan P.; Oremland, Ronald S. Applied and Environmental Microbiology, Vol. 53, Issue 6 https://doi.org/10.1128/AEM.53.6.1365-1369.1987	journal	June 1987
Selenate Reduction to Elemental Selenium by Anaerobic Bacteria in Sediments and Culture: Biogeochemical Significance of a Novel, Sulfate-Independent Respiration Oremland, Ronald S.; Hollibaugh, James T.; Maest, Ann S. Applied and Environmental Microbiology, Vol. 55, Issue 9 https://doi.org/10.1128/AEM.55.9.2333-2343.1989	journal	September 1989
Dissimilatory Selenate Reduction Potentials in a Diversity of Sediment Types Steinberg, Nisan A.; Oremland, Ronald S. Applied and Environmental Microbiology, Vol. 56, Issue 11 https://doi.org/10.1128/AEM.56.11.3550-3557.1990	journal	November 1990
Nitrate Is a Preferred Electron Acceptor for Growth of Freshwater Selenate-Respiring Bacteria Steinberg, Nisan A.; Blum, Jodi Switzer; Hochstein, Lawrence Applied and Environmental Microbiology, Vol. 58, Issue 1 https://doi.org/10.1128/AEM.58.1.426-428.1992	journal	January 1992
Isolation of Geobacter species from diverse sedimentary environments. Coates, J. D.; Phillips, E. J.; Lonergan, D. J. Applied and environmental microbiology, Vol. 62, Issue 5 https://doi.org/10.1128/AEM.62.5.1531-1536.1996	journal	January 1996
Reduction of Selenium Oxyanions by Enterobacter cloacae SLD1a-1: Isolation and Growth of the Bacterium and Its Expulsion of Selenium Particles Losi, M. E.; Frankenberger, W. T. Applied and Environmental Microbiology, Vol. 63, Issue 8 https://doi.org/10.1128/AEM.63.8.3079-3084.1997	journal	August 1997
Simultaneous Reduction of Nitrate and Selenate by Cell Suspensions of Selenium-Respiring Bacteria Oremland, Ronald S.; Blum, Jodi Switzer; Bindi, Allana Burns Applied and Environmental Microbiology, Vol. 65, Issue 10 https://doi.org/10.1128/AEM.65.10.4385-4392.1999	journal	October 1999
Reduction of Selenite and Detoxification of Elemental Selenium by the Phototrophic Bacterium Rhodospirillum rubrum Kessi, J.; Ramuz, M.; Wehrli, E. Applied and Environmental Microbiology, Vol. 65, Issue 11 https://doi.org/10.1128/AEM.65.11.4734-4740.1999	journal	November 1999
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
Structural and Spectral Features of Selenium Nanospheres Produced by Se-Respiring Bacteria Oremland, R. S.; Herbel, M. J.; Blum, J. S. Applied and Environmental Microbiology, Vol. 70, Issue 1 https://doi.org/10.1128/AEM.70.1.52-60.2004	journal	January 2004
Chemical Forms of Selenium in the Metal-Resistant Bacterium Ralstonia metallidurans CH34 Exposed to Selenite and Selenate Sarret, G.; Avoscan, L.; Carriere, M. Applied and Environmental Microbiology, Vol. 71, Issue 5 https://doi.org/10.1128/AEM.71.5.2331-2337.2005	journal	May 2005
Reduction of Selenate to Selenide by Sulfate-Respiring Bacteria: Experiments with Cell Suspensions and Estuarine Sediments Zehr, Jonathan P.; Oremland, Ronald S. Applied and Environmental Microbiology, Vol. 53, Issue 6 https://doi.org/10.1128/aem.53.6.1365-1369.1987	journal	June 1987
Selenate Reduction to Elemental Selenium by Anaerobic Bacteria in Sediments and Culture: Biogeochemical Significance of a Novel, Sulfate-Independent Respiration Oremland, Ronald S.; Hollibaugh, James T.; Maest, Ann S. Applied and Environmental Microbiology, Vol. 55, Issue 9 https://doi.org/10.1128/aem.55.9.2333-2343.1989	journal	September 1989
Dissimilatory Selenate Reduction Potentials in a Diversity of Sediment Types Steinberg, Nisan A.; Oremland, Ronald S. Applied and Environmental Microbiology, Vol. 56, Issue 11 https://doi.org/10.1128/aem.56.11.3550-3557.1990	journal	November 1990
Nitrate Is a Preferred Electron Acceptor for Growth of Freshwater Selenate-Respiring Bacteria Steinberg, Nisan A.; Blum, Jodi Switzer; Hochstein, Lawrence Applied and Environmental Microbiology, Vol. 58, Issue 1 https://doi.org/10.1128/aem.58.1.426-428.1992	journal	January 1992
Isolation of Geobacter species from diverse sedimentary environments. Coates, J. D.; Phillips, E. J.; Lonergan, D. J. Applied and environmental microbiology, Vol. 62, Issue 5 https://doi.org/10.1128/aem.62.5.1531-1536.1996	journal	January 1996
Reduction of Selenium Oxyanions by Enterobacter cloacae SLD1a-1: Isolation and Growth of the Bacterium and Its Expulsion of Selenium Particles Losi, M. E.; Frankenberger, W. T. Applied and Environmental Microbiology, Vol. 63, Issue 8 https://doi.org/10.1128/aem.63.8.3079-3084.1997	journal	August 1997
Organic chemical differentiation within fossil plant cell walls detected with X-ray spectromicroscopy Kevin Boyce, C.; Cody, George D.; Feser, Michael Geology, Vol. 30, Issue 11 https://doi.org/10.1130/0091-7613(2002)030<1039:OCDWFP>2.0.CO;2	journal	January 2002
Reduction of selenate and selenite to elemental selenium by Wolinella succinogenes Tomei, Francisco A.; Barton, Larry L.; Lemanski, Cheryl L. Canadian Journal of Microbiology, Vol. 38, Issue 12 https://doi.org/10.1139/m92-219	journal	December 1992
Dissimilatory Metal Reduction Lovley, Derek R. Annual Review of Microbiology, Vol. 47, Issue 1 https://doi.org/10.1146/annurev.mi.47.100193.001403	journal	October 1993
Micro-spectroscopic investigation of selenium-bearing minerals from the Western US Phosphate Resource Area Ryser, Amy L.; Strawn, Daniel G.; Marcus, Matthew A. Geochemical Transactions, Vol. 6, Issue 1 https://doi.org/10.1186/1467-4866-6-1	journal	January 2005
Metabolic analysis of the soil microbe Dechloromonas aromatica str. RCB: indications of a surprisingly complex life-style and cryptic anaerobic pathways for aromatic degradation Salinero, Kennan; Keller, Keith; Feil, William S. BMC Genomics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2164-10-351	journal	January 2009
Selenite reduction by the obligate aerobic bacterium Comamonas testosteroni S44 isolated from a metal-contaminated soil Zheng, Shixue; Su, Jing; Wang, Liang BMC Microbiology, Vol. 14, Issue 1 https://doi.org/10.1186/s12866-014-0204-8	journal	August 2014
Inter-species interconnections in acid mine drainage microbial communities Comolli, Luis R.; Banfield, Jill F. Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00367	journal	July 2014

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Selenium Accumulation, Speciation and Localization in Brazil Nuts (Bertholletia excelsa H.B.K.) Lima, Leonardo W.; Stonehouse, Gavin C.; Walters, Christina Plants, Vol. 8, Issue 8 https://doi.org/10.3390/plants8080289	journal	August 2019
Microbial communities across a hillslope‐riparian transect shaped by proximity to the stream, groundwater table, and weathered bedrock Lavy, Adi; McGrath, David Geller; Matheus Carnevali, Paula B. Ecology and Evolution, Vol. 9, Issue 12 https://doi.org/10.1002/ece3.5254	journal	May 2019
Analysis of uranium removal capacity of anaerobic granular sludge bacterial communities under different initial pH conditions Zeng, Taotao; Li, Licheng; Mo, Guanhai Environmental Science and Pollution Research, Vol. 26, Issue 6 https://doi.org/10.1007/s11356-018-4017-4	journal	January 2019
Identification and physiological comparison of plant species that show positive or negative co-occurrence with selenium hyperaccumulators Reynolds, R. Jason B.; Jones, Rachel R.; Stonehouse, Gavin C. Metallomics, Vol. 12, Issue 1 https://doi.org/10.1039/c9mt00217k	journal	January 2020
Distribution and chemical form of selenium in Neptunia amplexicaulis from Central Queensland, Australia Harvey, Maggie-Anne; Erskine, Peter D.; Harris, Hugh H. Metallomics, Vol. 12, Issue 4 https://doi.org/10.1039/c9mt00244h	journal	January 2020