Skip to main content
Log in

Bacterial diversity and composition of an alkaline uranium mine tailings-water interface

  • Microbial Ecology and Environmental Microbiology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

The microbial diversity and biogeochemical potential associated with a northern Saskatchewan uranium mine water-tailings interface was examined using culture-dependent and -independent techniques. Morphologically-distinct colonies from uranium mine water-tailings and a reference lake (MC) obtained using selective and non-selective media were selected for 16S rRNA gene sequencing and identification, revealing that culturable organisms from the uranium tailings interface were dominated by Firmicutes and Betaproteobacteria; whereas, MC organisms mainly consisted of Bacteroidetes and Gammaproteobacteria. Ion Torrent (IT) 16S rRNA metagenomic analysis carried out on extracted DNA from tailings and MC interfaces demonstrated the dominance of Firmicutes in both of the systems. Overall, the tailings-water interface environment harbored a distinct bacterial community relative to the MC, reflective of the ambient conditions (i.e., total dissolved solids, pH, salinity, conductivity, heavy metals) dominating the uranium tailings system. Significant correlations among the physicochemical data and the major bacterial groups present in the tailings and MC were also observed. Presence of sulfate reducing bacteria demonstrated by culture-dependent analyses and the dominance of Desulfosporosinus spp. indicated by Ion Torrent analyses within the tailings-water interface suggests the existence of anaerobic microenvironments along with the potential for reductive metabolic processes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Akob, D.M., Mills, H.J., and Kostka, J.E. 2007. Metabolically active microbial communities in uranium-contaminated subsurface sediments. FEMS Microbiol. Ecol. 59, 95–107.

    Article  PubMed  CAS  Google Scholar 

  • Benedetto, J.S., de Almeida, S.K., Gomes, H.A., Vazoller, R.F., and Ladeira, A.C.Q. 2005. Monitoring of sulfate-reducing bacteria in acid water from uranium mines. Miner. Eng. 18, 1341–1343.

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bowers, K.J., Mesbah, N.M., and Wiegel, J. 2009. Biodiversity of poly-extremophilic Bacteria: Does combining the extremes of high salt, alkaline pH and elevated temperature approach a physic-chemical boundary for life? Saline Syst. 5, 9.

    Article  PubMed  Google Scholar 

  • Burkhardt, E.M., Akob, D.M., Bischoff, S., Sitte, S., Kostka, J.O., Banerjee, D., Scheinost, A.C., and Kusel, 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  PubMed  CAS  Google Scholar 

  • Dib, J.R., Annika, W., Neumann, A., Ordoñez, O., Estévez, M.C., and Farías, M.E. 2009. Isolation of bacteria from remote high altitude Andean Lakes able to grow in the presence of antibiotics. Recent Patents Anti-Infective Drug Discov. 4, 66–76.

    Article  CAS  Google Scholar 

  • Duckworth, A.W., Grant, W.D., Jones, B.E., and van Steenbergen, R. 1996. Phylogenetic diversity of soda lake alkaliphiles. FEMS Microbiol. Ecol. 19, 181–191.

    Article  CAS  Google Scholar 

  • Ellis, R.J.M., Morgan, P., Weightman, A.J., and Fry, J.C. 2003. Cultivation-dependent and -independent approaches for determining bacterial diversity in heavy-metal-contaminated soil. Appl. Environ. Microbiol. 69, 3223–3230.

    Article  PubMed  CAS  Google Scholar 

  • Herlihy, A.T. and Mills, A.L. 1985. Sulfate reduction in freshwater sediments receiving acid mine drainage. Appl. Environ. Microbiol. 49, 179–186.

    PubMed  CAS  Google Scholar 

  • Hirkala, D.L.M. and Germida, J.J. 2004. Field and soil microcosm studies on the survival and conjugation of a Pseudomonas putida strain bearing a recombination plasmid, pADPTel. Can. J. Microbiol. 50, 595–604.

    Article  PubMed  CAS  Google Scholar 

  • Islam, E., Dhal, P.K., Kazy, S.K., and Sar, P. 2011. Molecular analysis of bacterial communities in uranium ores and surrounding soils from Banduhurang open cast uranium mine, India: A comparative study. J. Environ. Sci. Heal. A. 46, 271–280.

    Article  CAS  Google Scholar 

  • Islam, E. and Sar, P. 2011. Culture-dependent and -independent molecular analysis of the bacterial community within uranium ore. J. Basic Microbiol. 51, 372–384.

    Article  PubMed  CAS  Google Scholar 

  • Jain, D.K. 1995. Evaluation of semisolid Postgate’s B medium for enumerating sulfate-reducing bacteria. J. Microbiol. Methods 22, 27–38.

    Article  CAS  Google Scholar 

  • Jones, B.E., Grant, W.D., Duckworth, A.W., and Owenson, G.G. 1998. Microbial diversity of soda lakes. Extremophiles 2, 191–200.

    Article  PubMed  CAS  Google Scholar 

  • Kimura, M. 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16, 111–120.

    Article  PubMed  CAS  Google Scholar 

  • Landa, E.R., Phillips, E.J.P., and Lovley, D.R. 1991. Release of (super 226) Ra from uranium mill tailings by microbial Fe(III) reduction. Appl. Geochem. 6, 647–652.

    Article  CAS  Google Scholar 

  • Ley, R.E., Turnbaugh, P.J., Klein, S., and Gordon, J.T. 2006. Microbial ecology: Human gut microbes associated with obesity. Nature 444, 1022–1023.

    Article  PubMed  CAS  Google Scholar 

  • Lovley, D.R. and Phillips, E.J.P. 1992. Reduction of uranium by Desulfovibrio desulfuricans. Appl. Environ. Microbiol. 58, 850–856.

    PubMed  CAS  Google Scholar 

  • Lovley, D.R., Widman, P.K., Woodward, J.C., and Phillips, E.J. 1993. Reduction of uranium by cytochrome C3 of Desulfovibrio vulgaris. Appl. Environ. Microbiol. 59, 3572–3576.

    PubMed  CAS  Google Scholar 

  • Ma, Y., Xue, Y., Grant, W.D., Collins, N.C., Duckworth, A.W., van Steenbergen, R.P., and Jones, B.E. 2004. Alkalimonas amylolytica gen. nov., sp. nov., and Alkalimonas delamerensis gen. nov., sp. nov., novel alkaliphilic bacteria from soda lakes in China and East Africa. Extremophiles 8, 193–200.

    Article  PubMed  CAS  Google Scholar 

  • Miller, C.L., Landa, E.R., and Updegraff, D.M. 1987. Ecological aspects of microorganisms inhabiting uranium mill tailings. Microb. Ecol. 14, 141–155.

    Article  Google Scholar 

  • Mills, A.L., Bell, P.E., and Herlihy, A.T. 1989. Microbes, sediments, and acidified waters: the importance of biological buffering, pp. 1–19. In Rao, S.S. (ed.), Microbial interactions in acid stressed aquatic ecosystems. CRC Press, Inc., Boca Raton, FL, USA.

    Google Scholar 

  • Mitsui, H., Gorlach, K., Lee, H., Hattori, J.R., and Hattori, T. 1997. Incubation time and media requirements of culturable bacteria from different phylogenetic groups. J. Microbiol. Methods 30, 103–110.

    Article  CAS  Google Scholar 

  • Moldovan, B.J. and Hendry, M.J. 2005. Characterizing and quantifying controls on arsenic solubility over a pH range 1–11 in a uranium mill experiment. Environ. Sci. Technol. 39, 4913–4920.

    Article  PubMed  CAS  Google Scholar 

  • Moreels, D., Garry, C., Garafola, C., Monteleone, D., Taghavi, S., Fitts, J.P., and van der Lelie, D. 2008. Microbial community dynamics in uranium contaminated subsurface sediments under biostimulated conditions with high nitrate and nickel pressure. Environ. Sci. Pollut. Res. 15, 481–491.

    Article  CAS  Google Scholar 

  • Natural Resources Canada. 2006. Canada’s uranium production and nuclear power. Nuclear Issue Briefing, Paper No. 3. Ottawa, Ontario, Canada.

    Google Scholar 

  • Pyle, G.G., Swanson, S.M., and Lehmkuhl, D.M. 2002. Toxicity of uranium mine receiving waters to early life stage fathead minnows (Pimephales promelas) in the laboratory. Environ. Pollut. 116, 243–255.

    Article  PubMed  CAS  Google Scholar 

  • Radeva, G. and Selenska-Pobell, S. 2005. Bacterial diversity in water samples from uranium wastes as demonstrated by 16S rDNA and ribosomal intergenic spacer amplification retrievals. Can. J. Microbiol. 51, 910–923.

    Article  PubMed  CAS  Google Scholar 

  • Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4, 406–425.

    PubMed  CAS  Google Scholar 

  • Saskatchewan Mining Association. 2010. Saskatchewan Mining Association Fact Sheet. 2010. SMA, Regina, SK, Canada.

    Google Scholar 

  • Selenska-Pobell, S. 2002. Diversity and activity of bacteria in uranium waste piles, pp. 225–254. In Keith-Roach, M.J. and Livens, F.R. (eds.), Interactions of microorganisms with radionuclides, Elsevier Sciences Ltd., Oxford, UK.

    Chapter  Google Scholar 

  • Selenska-Pobell, S., Kampf, G., Hemming, K., Radeva, G., and Satchanska, G. 2001. Bacterial diversity in soil samples from two uranium waste piles as determined by rep-APD, RISA and 16S rDNA retrieval. Antonie van Leeuwenheok 79, 149–161.

    Article  CAS  Google Scholar 

  • Shaw, S.A., Hendry, M.J., Esselfie-Dughan, J., Kotzer, T., and Wallschlager, D. 2011 Distribution, characterization, and geochemical controls of elements of concern in uranium mine tailings, Key Lake, Saskatchewan, Canada. Appl. Geochem. 26, 2044–2056.

    Article  CAS  Google Scholar 

  • Shelobolina, E.S., O’Neill, K., Finneran, K.T., Hayes, L.A., and Lovley, D.R. 2003. Potential for in situ bioremediation of a low-pH, high-nitrate uranium-contaminated groundwater. Soil Sediment Contam. 12, 865–884.

    Article  CAS  Google Scholar 

  • Singleton, R. Jr. 1993. The sulfate-reducing bacteria: an overview, pp. 1–20. In Odom, J.M. and Singleton, R. (eds.), The sulfate-reducing bacteria: contemporary perspectives. Springer Verlag, Inc., New York, N.Y., USA.

    Chapter  Google Scholar 

  • Sitte, J., Akob, M.D.M., Kaufmann, C., Finster, K., Banerjee, D., Burkhardt, E.M., Kostka, J.E., Scheinost, A.C., Büchel, G., and 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  PubMed  CAS  Google Scholar 

  • Sorokin, D.Y., Banciu, H., van Loosdrecht, M., and Kuenen, J.G. 2003. Growth physiology and competitive interaction of obligately chemolithoautotrophic, haloalkaliphilic, sulphur-oxidizing bacteria from soda lakes. Extremophiles 7, 195–203.

    PubMed  Google Scholar 

  • Stackebrandt, E., Schumann, P., Schüler, E., and Hippe, H. 2003. Reclassification of Desulfotomaculum auripigmentum as Desulfosporosinus auripigmenti corrig., comb. nov. Int. J. Syst. Evol. Microbiol. 53, 1439–1443.

    Article  PubMed  CAS  Google Scholar 

  • Suzuki, Y., Kelly, S.D., Kemner, K.M., and Banfield, J.F. 2002. Nanometre-sized products of uranium bioreduction. Nature 419, 134.

    Article  PubMed  CAS  Google Scholar 

  • Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. 2011. MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol. Biol. Evol. 28, 2731–2739.

    Article  PubMed  CAS  Google Scholar 

  • Vatsurina, A., Badrutdinova, D., Schumann, P., and Spring, S.M. 2008. Desulfosporosinus hippei sp. nov., a mesophilic sulfate-reducing bacterium isolated from permafrost. Int. J. Syst. Evol. Microbiol. 58, 1228–1232.

    Article  PubMed  CAS  Google Scholar 

  • Wagner, D. 2008. Microbial communities and processes in arctic permafrost environments, pp. 133–154. In Dion, P. and Chandra, S.N. (eds.), Microbiology of extreme soils. Soil Biology. vol. 13. Springer, Berlin, Germany.

    Chapter  Google Scholar 

  • Wolfaardt, G.M., Hendry, M.J., and Korber, D.R. 2008. Microbiology of saturated, high pH uranium-mine tailings, Saskatchewan, Canada. Can. J. Microbiol. 54, 932–940.

    Article  PubMed  CAS  Google Scholar 

  • Yergeau, E., Lawrence, J.R., Sanschagrin, S., Waiser, M.J., Korber, D.R., and Greer, C.W. 2012. Next-generation sequencing of microbial communities in the Athabasca River and its tributaries in relation to oil sands mining activities. Appl. Environ. Microbiol. 78, 7626–7637.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Darren R. Korber.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Khan, N.H., Bondici, V.F., Medihala, P.G. et al. Bacterial diversity and composition of an alkaline uranium mine tailings-water interface. J Microbiol. 51, 558–569 (2013). https://doi.org/10.1007/s12275-013-3075-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-013-3075-z

Keywords

Navigation