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Metals other than uranium affected microbial community composition in a historical uranium-mining site

  • Alteration and element mobility at the microbe-mineral interface
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Abstract

To understand the links between the long-term impact of uranium and other metals on microbial community composition, ground- and surface water-influenced soils varying greatly in uranium and metal concentrations were investigated at the former uranium-mining district in Ronneburg, Germany. A soil-based 16S PhyloChip approach revealed 2358 bacterial and 35 archaeal operational taxonomic units (OTU) within diverse phylogenetic groups with higher OTU numbers than at other uranium-contaminated sites, e.g., at Oak Ridge. Iron- and sulfate-reducing bacteria (FeRB and SRB), which have the potential to attenuate uranium and other metals by the enzymatic and/or abiotic reduction of metal ions, were found at all sites. Although soil concentrations of solid-phase uranium were high, ranging from 5 to 1569 μg·g (dry weight) soil−1, redundancy analysis (RDA) and forward selection indicated that neither total nor bio-available uranium concentrations contributed significantly to the observed OTU distribution. Instead, microbial community composition appeared to be influenced more by redox potential. Bacterial communities were also influenced by bio-available manganese and total cobalt and cadmium concentrations. Bio-available cadmium impacted FeRB distribution while bio-available manganese and copper as well as solid-phase zinc concentrations in the soil affected SRB composition. Archaeal communities were influenced by the bio-available lead as well as total zinc and cobalt concentrations. These results suggest that (i) microbial richness was not impacted by heavy metals and radionuclides and that (ii) redox potential and secondary metal contaminants had the strongest effect on microbial community composition, as opposed to uranium, the primary source of contamination.

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References

  • Abou-Shanab RAI, van Berkum P, Angle JS (2007) Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere 68:360–367

    Article  CAS  Google Scholar 

  • Acosta-Martınez V, Dowd S, Sun Y, Allen V (2008) Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol Biochem 40:2762–2770

    Article  Google Scholar 

  • Akob DM, Mills HJ, Kostka JE (2007) Metabolically active microbial communities in uranium-contaminated subsurface sediments. FEMS Microbiol Ecol 59:95–107

    Article  CAS  Google Scholar 

  • Amoozegar MA, Hamedi J, Dadashipour M, Shariatpanahi S (2005) Effect of salinity on the tolerance to toxic metals and oxyanions in native moderately halophilic spore-forming bacilli. World J Microbiol Biotechnol 21:1237–1243

    Article  CAS  Google Scholar 

  • Bååth E (1989) Effects of heavy metals in soil on microbial processes and populations. Water Air Soil Pollut 47:335–379

    Article  Google Scholar 

  • Bondici V, Lawrence J, Khan N, Hill J, Yergeau E, Wolfaardt G, Warner J, Korber D (2013) Microbial communities in low permeability, high pH uranium mine tailings: characterization and potential effects. J Appl Microbiol 114:1671–1686

    Article  CAS  Google Scholar 

  • Brodie E, Desantis T, Joyner D, Baek S, Larsen J, Andersen G, Hazen T, Richardson P, Herman D, Tokunaga T, Wan J, Firestone M (2006) Application of a high-density oligonucleotide microarray approach to study bacterial population dynamics during uranium reduction and reoxidation. Appl Environ Microbiol 72:6288–6298

    Article  CAS  Google Scholar 

  • Brooks SC (2001) Waste characteristics of the former S-3 ponds and outline of uranium chemistry relevant to NABIR Field Research Center studies. NABIR Field Research Center Oak Ridge, Tennessee

    Book  Google Scholar 

  • Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45:198–207

    Article  CAS  Google Scholar 

  • Burkhardt EM, Meißner S, Merten D, Büchel G, Küsel K (2009) Heavy metal retention and microbial activities in geochemical barriers formed in glacial sediments subjacent to a former uranium mining leaching heap. Chem Erde Geochem 69:21–34

    Article  CAS  Google Scholar 

  • Burkhardt EM, Akob DM, Bischoff S, Sitte J, Kostka JE, Banerjee D, Scheinost AC, Küsel K (2010) Impact of biostimulated redox processes on metal dynamics in an iron-rich creek soil of a former uranium mining area. Environ Sci Technol 44:177–183

    Article  CAS  Google Scholar 

  • Burkhardt EM, Bischoff S, Akob DM, Büchel G, Küsel K (2011a) Heavy metal tolerance of Fe(III)-reducing microbial communities in contaminated creek bank soils. Appl Environ Microbiol 77:3132–3136

    Article  CAS  Google Scholar 

  • Burkhardt EM, Bischoff S, Akob DM, Büchel G, Küsel K (2011b) Heavy metal tolerance of Fe(III)-reducing microbial communities in contaminated creek bank soil. Appl Environ Microbiol 77:3132–3136

    Article  CAS  Google Scholar 

  • Carlsson E, Büchel G (2005) Screening of residual contamination at a former uranium heap leaching site, Thuringia, Germany. Chem Erde Geochem 65:75–95

    Article  CAS  Google Scholar 

  • Chang YJ, Long PE, Geyer R, Peacock AD, Resch CT, Sublette K, Pfiffner S, Smithgall A, Anderson RT, Vrionis HA, Stephen JR, Dayvault R, Ortiz-Bernad I, Lovley DR, White DC (2005) Microbial incorporation of C-13-labeled acetate at the field scale: detection of microbes responsible for reduction of U(VI). Environ Sci Technol 39:9039–9048

    Article  CAS  Google Scholar 

  • Cho K, Zholi A, Frabutt D, Flood M, Floyd D, Tiquia S (2012) Linking bacterial diversity and geochemistry of uranium-contaminated groundwater. Environ Technol 33:1629–1640

    Article  CAS  Google Scholar 

  • Cooper DC, Picardal FF, Coby AJ (2006) Interactions between microbial iron reduction and metal geochemistry: effect of redox cycling on transition metal speciation in iron bearing sediments. Environ Sci Technol 40:1884–1891

    Article  CAS  Google Scholar 

  • Cornell RM, Schwertmann U (2003) The iron oxides. WILEY-VCH, Weinheim

    Book  Google Scholar 

  • Craft ES, Abu-Qare AW, Flaherty MM, Garofolo MC, Rincavage HL, Abou-Donia MB (2004) Depleted and natural uranium: chemistry and toxicological effects. J Toxicol Environ Health Part B 7:297–317

    Article  CAS  Google Scholar 

  • Culhane AC, Thiolouse J, Perriere G, Higgins DG (2005) MADE4: an R package for multivariate analysis of gene expression data. Bioinformatics 21:2789–2790

    Article  CAS  Google Scholar 

  • DeAngelis KM, Brodie EL, DeSantis TZ, Andersen GL, Lindow SE, Firestone MK (2009) Selective progressive response of soil microbial community to wild oat roots. ISME J 3:168–178

    Article  CAS  Google Scholar 

  • Denkhaus E, Salnikow K (2002) Nickel essentiality, toxicity, and carcinogenicity. Crit Rev Oncol Hematol 42:35–56

    Article  CAS  Google Scholar 

  • DeSantis TZ, Brodie EL, Moberg JP, Zubieta IX, Piceno YM, Andersen GL (2007) High-density universal 16S rRNA microarray analysis reveals broader diversity than typical clone library when sampling the environment. Microb Ecol 53:371–383

    Article  CAS  Google Scholar 

  • Dray S (2007) Packfor: forward selection with permutation, R package version 0.0–7. http://pbil.univ-lyon1.fr/members/dray/software.php

  • Eden P, Schmidt TM, Blakemore R, Pace N (1991) Phylogenetic analysis of Aquaspirillum magnetotacticum using polymerase chain reaction-amplified 16S rRNA-specific DNA. Int J Syst Bacteriol 41:324–325

    Article  CAS  Google Scholar 

  • Emerson D, Moyer C (1997) Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH. Appl Environ Microbiol 63:4784–4792

    CAS  Google Scholar 

  • Forster JC (1995) Soil sampling, handling, storage and analysis. In: Alef K, Nannipieri P (eds) Methods in applied soil microbiology and biochemistry. Academic Press Ltd, San Diego, pp 49–121

    Chapter  Google Scholar 

  • Frostegård Å, Tunlid A, Bååth E (1993) Phospholipid fatty acid composition, biomass, and activity of microbial communities from two soil types experimentally exposed to different heavy metals. Appl Environ Microbiol 59:3605–3617

    Google Scholar 

  • Fude L, Harris B, Urrutia MM, Beveridge TJ (1994) Reduction of Cr(VI) by a consortium of sulfate-reducing bacteria (SRB III). Appl Environ Microbiol 60:1525–1531

    CAS  Google Scholar 

  • Gadd GM (2000) Bioremedial potential of microbial mechanisms of metal mobilization and immobilization. Curr Opin Biotechnol 11:271–279

    Article  CAS  Google Scholar 

  • Gans J, Wolinsky M, Dunbar J (2005) Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science 309:1387–1390

    Article  CAS  Google Scholar 

  • Geletneky JW, Fengler HJ (2004) Quartäre Talentwicklung des oberen Gessentales im ehemaligen Ronneburger Uranbergbaugebiet, Ostthüringen. Beitr. Geologie Thüringen 11:35–67

    Google Scholar 

  • Gihring T, Zhang G, Brandt C, Brooks S, Campbell J, Carroll S, Criddle C, Green S, Jardine P, Kostka J, Lowe K, Mehlhorn T, Overholt W, Watson D, Yang Z, Wu W, Schadt C (2011) A limited microbial consortium is responsible for extended bioreduction of uranium in a contaminated aquifer. Appl Environ Microbiol 77:5955–5965

    Article  CAS  Google Scholar 

  • Girvan MS, Campbell CD, Kilham K, Prosser JI, Glover LA (2005) Bacterial diversity promotes community stability and functional resilience after perturbation. Environ Microbiol 7:301–313

    Article  CAS  Google Scholar 

  • Grawunder A, Lonschinski M, Merten D, Büchel G (2009) Distribution and bonding of residual contamination in glacial sediments at the former uranium mining leaching heap of Gessen/Thuringia, Germany. Chem Erde Geochem 69S2:5–19

    Article  Google Scholar 

  • Griffiths BS, Diaz-Raviña M, Ritz K, McNicol JW, Ebblewhite N, Bååth E (1997) Community DNA hybridisation and %G + C profiles of microbial communities from heavy metal polluted soils. FEMS Microbiol Ecol 24:103–112

    Article  CAS  Google Scholar 

  • Handley K, Wrighton K, Piceno YM, Andersen GL, DeSantis TZ, Williams KH, Wilkins M, N'Guessan A, Peacock A, Bargar J, Long PE, Banfield JF (2012) High-density PhyloChip profiling of stimulated aquifer microbial communities reveals a complex response to acetate amendment. FEMS Microbiol Ecol 81:188–204

    Article  CAS  Google Scholar 

  • Hershberger KL, Barns S, Reysenbach AL, Dawson SC, Pace N (1996) Wide diversity of Crenarchaeota. Nature 384:420

    Article  CAS  Google Scholar 

  • Huber G, Stetter KO (1991) Sulfolobus metallicus, sp. nov., a novel strictly chemolithoautotrophic thermophilic archaeal species of metal-mobilizers. Syst Appl Microbiol 14:372–378

    Article  CAS  Google Scholar 

  • Jakubick A, Gatzweile R, Mager D, Mac A, Robertson G (1997) The Wismut waste rock pile remediation programme of the Ronneburg district, Germany, Abstr. 4th International Conference on Acid Rock Drainage, Vancouver B.C. 1285–1301

  • Johnson D, Knoepp J, Swank W, Shan J, Morris L, Van_Lear D, Kapeluck R (2001) Effects of forest management on soil carbon: results of some long-term resampling studies. Environ Pollut 116:S201–S208

    Article  Google Scholar 

  • Jørgensen BB (2006) Bacteria and marine biogeochemistry. In: Schulz HD, Zabel M (eds) Marine geochemistry. Springer, Berlin Heidelberg

    Google Scholar 

  • Kaplan DI, Yeager C, Denham ME, Zhang S, Xu C, Schwehr KA, Li H, Brinkmeyer R, Santschi PH (2012) Biogeochemical considerations related to the remediation of 129I plumes. U.S. Department of Energy 59

  • Kelly JJ, Häggblom MM, Tate RT (2003) Effects of heavy metal contamination and remediation on soil microbial communities in the vicinity of a zinc smelter as indicated by analysis of microbial community phospholipid fatty acid profiles. Biol Fertil Soils 38:65–71

    Article  CAS  Google Scholar 

  • Kimiran-Erdem A, Arslan EO, Yurudu NOS, Zeybek Z, Dogruoz N, Cotuk A (2007) Isolation and identification of enterococci from seawater samples: assessment of their resistance to antibiotics and heavy metals. Environ Monit Assess 125:219–228

    Article  CAS  Google Scholar 

  • Kostka J, Green S (2011) Microorganisms and processes linked to uranium reduction and immobilization. In: Stolz J, Oremland R (eds) Microbial metal and metalloid metabolism. ASM Press, Washington, pp 117–138

    Chapter  Google Scholar 

  • Leigh MB, Wu W, Cardenas E, Uhlik O, Carroll S, Gentry T, Marsh TL, Zhou J, Jardine P, Criddle CS, Tiedje JM (2014) Microbial communities biostimulated by ethanol during uranium (VI) bioremediation in contaminated sediment as shown by stable isotope probing. Frontiers of Environmental Science & Engineering: 5

  • Liang Y, Van Nostrand J, N'guessan L, Peacock A, Deng Y, Long P, Resch C, Wu L, He Z, Li G, Hazen T, Lovley D, Zhou J (2012) Microbial functional gene diversity with a shift of subsurface redox conditions during in situ uranium reduction. Appl Environ Microbiol 78:2966–2972

    Article  CAS  Google Scholar 

  • Liger E, Charlet L, Van Cappellen P (1999) Surface catalysis of uranium(VI) reduction by iron(II). Geochim Cosmochim Acta 63:2939–2955

    Article  CAS  Google Scholar 

  • Lin X, Kennedy D, Peacock A, Mckinley J, Resch C, Fredrickson J, Konopka A (2012) Distribution of microbial biomass and potential for anaerobic respiration in Hanford site 300 area subsurface sediment. Appl Environ Microbiol 78:759–767

    Article  CAS  Google Scholar 

  • Lloyd J (2003) Microbial reduction of metals and radionuclides. FEMS Microbiol Rev 27:411–425

    Article  CAS  Google Scholar 

  • Macdonald CA, Campbell CD, Bacon JR, Singh BK (2008) Multiple profiling of soil microbial communities identifies potential genetic markers of metal-enriched sewage sludge. FEMS Microbiol Ecol 65:555–564

    Article  CAS  Google Scholar 

  • Michalsen MM, Goodman BA, Kelly SD, Kemner KM, McKinley JP, Stucki JW, Istok JD (2006) Uranium and technetium bio-immobilization in intermediate-scale physical models of an in situ bio-barrier. Environ Sci Technol 40:7048–7053

    Article  CAS  Google Scholar 

  • Miller AC, McClain D (2007) A review of depleted uranium biological effects: in vitro and in vivo studies. Rev Environ Health 22:75–89

    Article  CAS  Google Scholar 

  • Mori K, Yamamoto H, Kamagata Y, Hatsu M, Takamizawa K (2000) Methanocalculus pumilus sp. nov., a heavy-metal-tolerant methanogen isolated from a waste-disposal site. Int J Syst Evol Microbiol 50:1723–1729

    Article  CAS  Google Scholar 

  • Morse JW, Arakaki T (1993) Adsorption and coprecipitation of divalent metals with mackinawite (FeS). Geochim Cosmochim Acta 57:3635–3640

    Article  CAS  Google Scholar 

  • Muyzer G, Stams AJ (2008) The ecology and biotechnology of sulphate-reducing bacteria. Nat Rev Microbiol 6:441–454

    CAS  Google Scholar 

  • Oksanen J, Kindt R, Legendre P, O'Hara B, Simpson GL, Solymos P, Stevens MHH, Wagner H (2008) Vegan: community ecology package. R package version 1.15-1. http://cran.r-project.org/, http://vegan.r-forge.r-project.org/

  • Oren A (2006) The order Halobacteriales. Prokaryotes 3:113–164

    Article  Google Scholar 

  • Özverdi A, Erdem M (2006) Cu2+, Cd2+ and Pb2+ adsorption from aqueous solutions by pyrite and synthetic iron sulphide. J Hazard Mater B137:626–632

    Article  Google Scholar 

  • R Development Core Team (2005) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. www.R-project.org

  • Rastogi G, Osman S, Vaishampayan P, Andersen GL, Stetler L, Sani RK (2010) Microbial diversity in uranium mining-impacted soils as revealed by high-density 16S microarray and clone library. Microb Ecol 59:94–108

    Article  CAS  Google Scholar 

  • Roesch LFW, Fulthorpe RR, Riva A, Casella G, Hadwin AKM, Kent AD, Daroub SH, Camargo FAO, Farmerie WG, Triplett EW (2007) Pyrosequencing enumerates and contrasts soil microbial diversity. ISME J 1:283–290

    CAS  Google Scholar 

  • Sandaa R, Enger O, Torsvik V (1999) Abundance and diversity of archaea in heavy-metal-contaminated soils. Appl Environ Microbiol 65:3293–3297

    CAS  Google Scholar 

  • Sani RK, Peyton BM, Dohnalkova A (2006) Toxic effects of uranium on Desulfovibrio desulfuricans G20. Environ Toxicol Chem 25:1231–1238

    Article  CAS  Google Scholar 

  • Schmidt A, Haferburg G, Schmidt A, Lischke U, Merten D, Ghergel F, Büchel G, Kothe E (2009) Heavy metal resistance to the extreme: Streptomyces strains from a former uranium mining area. Chem Erde Geochem 69(S2):35–44

    Article  CAS  Google Scholar 

  • Sitte J, Akob DM, Kaufmann C, Finster K, Banerjee D, Burkhardt EM, Kostka JE, Scheinost AC, Büchel G, Küsel K (2010) Microbial links between sulfate reduction and metal retention in uranium- and heavy metal-contaminated soil. Appl Environ Microbiol 76:3143–3152

    Article  CAS  Google Scholar 

  • Sitte J, Pollok K, Langenhorst F, Küsel K (2013) Nanocrystalline nickel and cobalt sulfides formed by a heavy metal-tolerant, sulfate-reducing enrichment culture. Geomicrobiol J 30:36–47

    Article  CAS  Google Scholar 

  • Sponagel H, Grottenthaler W, Hartmann K-J, Hartwich R, Janetzko P, Joisten H, Kühn D, Sabel K-J, Traidl R (2005) Bodenkundliche Kartieranleitung. Bundesanstalt für Geowissenschaften und Rohstoffe. Schweizerbartsche Verlagsbuchhandlung, Stuttgart

    Google Scholar 

  • Tokunaga TK, Wan J, Kim Y, Daly RA, Brodie EL, Hazen TC, Herman D, Firestone MK (2008) Influences of organic carbon supply rate on uranium bioreduction in initially oxidizing, contaminated sediment. Environ Sci Technol 42:8901–8907

    Article  CAS  Google Scholar 

  • Tom-Petersen A, Leser TD, Marsh TL, Nybroe O (2003) Effects of copper amendment on the bacterial community in agricultural soil analyzed by the T-RFLP technique. FEMS Microbiol Ecol 46:53–62

    Article  CAS  Google Scholar 

  • U.S. Department of Energy (1999) Final site observational work plan for the UMTRA project Old Rifle site GJO-99-88-TAR. U.S. Department of Energy, Grand Junction

    Google Scholar 

  • Vanengelen MR, Szilagyi RK, Gerlach R, Lee BD, Apel WA, Peyton BM (2011) Uranium exerts acute toxicity by binding to pyrroloquinoline quinone cofactor. Environ Sci Technol 45:937–942

    Article  CAS  Google Scholar 

  • Vig K, Megharaj M, Sethunathan N, Naidu R (2003) Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: a review. Adv Environ Res 8:121–135

    Article  CAS  Google Scholar 

  • Wall JD, Krumholz LR (2006) Uranium reduction. Annu Rev Microbiol 60:149–166

    Article  CAS  Google Scholar 

  • Watson DB, Kostka JE, Fields MW, Jardine PM (2004) The Oak Ridge field research center conceptual model. NABIR Field Research Center Oak Ridge, Tennessee

    Google Scholar 

  • Weisburg W, Barns S, Pelletier D, Lane D (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    CAS  Google Scholar 

  • Zeien H, Brümmer GW (1989) Chemische Extraktionen zur Bestimmung von Schwermetallbindungsformen in Böden. Mitt Dt Bodenkundl Ges 59:505–510

    Google Scholar 

  • Zerling L, Hanisch C, Junge FW, Müller A (2003) Heavy metals in Saale sediments—changes in the contamination since 1991. Acta Hydrochim Hydrobiol 31:368–377

    Article  CAS  Google Scholar 

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Acknowledgments

The authors thank Dirk Merten and Denise M. Akob for the valuable discussion, Ingo Schöning for soil horizon nomenclature, Michael Rzanny for the helpful suggestions with the statistical analyses, Katy Hartwig and Sylvia Meißner for the technical assistance, and Peter Bouwma for proofreading the manuscript. This project was part of the graduate research school “Alteration and element mobility at the microbe-mineral interface” financially supported by the German Research Foundation (DFG 1257) and embedded in the Jena School of Microbial Communication (JSMC).

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Sitte, J., Löffler, S., Burkhardt, EM. et al. Metals other than uranium affected microbial community composition in a historical uranium-mining site. Environ Sci Pollut Res 22, 19326–19341 (2015). https://doi.org/10.1007/s11356-015-4791-1

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