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Bacteria of the Genus Shewanella from Radionuclide-Contaminated Groundwater

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Abstract

Decommissioned surface repositories of liquid radioactive waste remain a potential source of groundwater pollution. Establishment of biogeochemical barriers results in decreased migration of both radioactive and toxic macro-components of the waste. The article presents the results of studying the composition of the microbial community of groundwater sampled in the area of a surface repository for liquid radioactive waste. High-throughput sequencing of the 16S rRNA genes revealed the dominant and minor components of the community, among which were found bacteria of the genus Shewanella. Isolated pure cultures of Shewanella putrefaciens J1-6-2-2 and A-4-3 and Shewanella xiamenensis DCB2-1 were capable of reducing nitrate ions to dinitrogen, which resulted in a decrease in the redox potential of the medium and contributed to reduction and deposition of pertechnetate, uranyl, and chromate ions. In the presence of organic substrates the strains formed biofilms on a number of natural materials (vermiculite, pearlite, schungite, etc.) with high sorption characteristics for cesium, strontium, uranium, and technetium. Analysis of the genome of strain DCB2-1 revealed a cluster of genes homologous to those determining biofilm formation in the well-known strain Shewanella oneidensis MR-1. The isolated strains may be used for introduction into subsurface horizons and enrichment of the natural microbial community in order to create a biogeochemical barrier for purification of groundwater from nitrate ions and immobilization of radioactive waste components.

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REFERENCES

  1. Al-Kayssi, M., Magee, R.J., and Wilson, C.L., Spectrophotometric studies on technetium and rhenium, Talanta, 1962, vol. 9, pp. 125–132.

    Article  CAS  Google Scholar 

  2. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J., Gapped BLAST and PSI-BLAST: a new generation of protein database search programs, Nucl. Acids Res., 1997, vol. 25, pp. 3389–3402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Bolger, A.M., Lohse, M., and Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, 2014, vol. 30, pp. 2114–2120. https://doi.org/10.1093/bioinformatics/btu170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Peña, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., et al., QIIME allows analysis of high-throughput community sequencing data, Nat. Methods, 2010, vol. 7, pp. 335–336.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Chang, L.C., Chu, H.J., and Hsiao, C.T., Optimal planning of a dynamic pump-treat-inject groundwater remediation system, J. Hydrol., 2007, vol. 342, pp. 295–304.

    Article  Google Scholar 

  6. Fadrosh, D.W., Ma, B., Gajer, P., Sengamalay, N., Ott, S., Brotman, R.M., and Ravel, J., An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform, Microbiome, 2014, vol. 2, p. 6. https://doi.org/10.1186/2049-2618-2-6

    Article  PubMed  PubMed Central  Google Scholar 

  7. Gibert, O., Pomierny, S., Rowe, I., and Kalin, R.M., Selection of organic substrates as potential reactive materials for use in a denitrification permeable reactive barrier (PRB), Bioresour. Technol., 2008, vol. 99, pp. 7587–7596.

    Article  CAS  PubMed  Google Scholar 

  8. Grouzdev, D.S., Safonov, A.V., Babich, T.L., Tourova, T.P., Krutkina, M.S., and Nazina, T.N., Draft genome sequence of a dissimilatory U(VI)-reducing bacterium, Shewanella xiamenensis strain DCB2-1, isolated from nitrate- and radionuclide-contaminated groundwater in Russia, Genome Announc., 2018, vol. 6. Article e00555-18.https://doi.org/10.1128/genomeA.00555-18

    Article  PubMed  PubMed Central  Google Scholar 

  9. Huang, J., Sun, B., and Zhang, X., Shewanella xiamenensis sp. nov., isolated from coastal sea sediment, Int. J. Syst. Evol. Microbiol., 2010, vol. 60, pp. 1585‒1589.

    Article  CAS  PubMed  Google Scholar 

  10. Lovley, D.R. and Phillips, E.J.P., Novel mode of microbial energy metabolism: organic carbon oxidation coupled to dissimilatory reduction of iron or manganese, Appl. Environ. Microbiol., 1988, vol. 54, pp. 1472–1480.

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Maniatis, T., Frich, E., and Sambruk, G., Methods in Genetic Engineering: Molecular Cloning, Moscow: Mir, 1984.

  12. Michalsen, M.M., Peacock, A.D., Smithgal, A.N., White, D.C., Spain, A.M., Sanchez-Rosario, Y., Krumholz, L.R., Kelly, Sh.D., Kemner, K.M., McKinley, J., Heald, S.M., Bogle, M.A., Watson, D.B., and Istok, J.D., Treatment of nitric acid-, U(VI)-, and Tc(VII)-contaminated groundwater in intermediate-scale physical models of an in situ biobarrier, Environ. Sci. Technol., 2009, vol. 43. P. 1952–1961.

    Article  CAS  PubMed  Google Scholar 

  13. Nazina, T.N., Luk’yanova, E.A., Zakharova, E.V., Konstantinova, L.I., Kalmykov, S.N., Poltaraus, A.B., and Zubkov, A.A., Microorganisms in a disposal site for liquid radioactive wastes and their influence on radionuclides, Geomicrobiol. J., 2010, vol. 27, pp. 473–486.

    Article  CAS  Google Scholar 

  14. Ning, Z., Ishiguro, M., Koopal, L.K., Sato, T., and Kashiwagi, J., Comparison of strontium retardation for kaolinite, illite, vermiculite and allophane, J. Radioanal. Nucl. Chem., 2018, vol. 317, pp. 409–419.

    Article  CAS  Google Scholar 

  15. Noubactep, C., Caré, S., and Crane, R., Nanoscale metallic iron for environmental remediation: prospects and limitations, Water Air Soil Pollution, 2012, vol. 223, pp. 1363–1382.

    Article  CAS  PubMed  Google Scholar 

  16. Ortiz-Bernad, I., Anderson, R.T., Vrionis, H.A., and Lovley, D.R., Resistance of solid-phase U(VI) to microbial reduction during in situ bioremediation of uranium-contaminated groundwater, Appl. Environ. Microbiol., 2004, vol. 70, pp. 7558–7560.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Onishi, H. and Sekine, K., Spectrophotometric determination of zirconium, uranium, thorium and rare earths with arsenazo III after extractions with thenoyltrifluoroacetone and tri-n-octylamine, Talanta, 1972, vol. 19, pp. 473–478.

    Article  CAS  PubMed  Google Scholar 

  18. Plakunov, V.K., Mart’yanov, S.V., Teteneva, N.A., and Zhurina, M.V., A universal method for quantitative characterization of growth and metabolic activity of microbial biofilms in static models, Microbiology (Moscow), 2016, vol. 85, pp. 509–513.

    Article  CAS  Google Scholar 

  19. Rybal’chenko, A.I., Pimenov, M.K., Kostin, P.P., Balukova, V.D., Nosukhin, A.V., Mikerin, E.I., Egorov, N.N., Kaimin, E.P., Kosareva, I.M., and Kurochkin, V.M., Deep Injection Disposal of Liquid Radioactive Waste in Russia, Foley, M.G. and Ballou, L.M.G., Eds., Columbus, Ohio: Battelle, 1998.

    Google Scholar 

  20. Safonov, A.V., Il’in, V.A., Tregubova, V.E., Zakharova, E.V., Ershov, B.G., Babich, T.L., and Nazina, T.N., Biological antimigration barriers in underground water-bearing horizons for conservation of LRW repositories, Vopr. Radiats. Bezopas., 2015, no. 3, pp. 99–105.

  21. Safonov, A.V., Babich, T.L., Sokolova, D.S, Grouzdev, D.S., Tourova, T.P., Poltaraus, A.B., Zakharova, E.V., Merkel, A.Y., Novikov, A.P., and Nazina, T.N., Microbial community and in situ bioremediation of groundwater by nitrate removal in the zone of a radioactive waste surface repository, Front. M-icrobiol., 2018, vol. 9, article 1985. https://doi.org/10.3389/fmicb.2018.01985

    Article  Google Scholar 

  22. Sellin, P. and Leupin, O.X., The use of clay as an engineered barrier in radioactive-waste management – a review, Clays Clay Minerals, 2013, vol. 61, pp. 477–498.

    Article  CAS  Google Scholar 

  23. Senko, J.M., Istok, J.D., Suflita, J.M., and Krumholz, L.R. In-situ evidence for uranium immobilization and remobilization, Environ. Sci. Technol., 2002, vol. 36, pp. 1491–1496.

    Article  CAS  PubMed  Google Scholar 

  24. Sheng, L. and Fein, J.B., Uranium reduction by Shewanella oneidensis MR-1 as a function of NaHCO3 concentration: surface complexation control of reduction kinetics, Environ. Sci. Technol., 2014, vol. 48, pp. 3768–3775.

    Article  CAS  PubMed  Google Scholar 

  25. Takahashi, S., Tomita, J., Nishioka, K., Hisada, T., and Nishijima, M., Development of a prokaryotic universal primer for simultaneous analysis of Bacteria and Archaea using next-generation sequencing, PLoS One, 2014, vol. 9. Article e105592.

    Article  PubMed  PubMed Central  Google Scholar 

  26. Verma, P.K., Romanchuk, A.Yu., Vlasova, I.E., Krupskaya, V.V., and Kalmykov, S.N., Np(V) uptake by bentonite clay: Effect of accessory Fe oxides/hydroxides on sorption and speciation, Appl. Geochem., 2017, vol. 78, pp. 74–82.

    Article  CAS  Google Scholar 

  27. Wall, J.D. and Krumholz, L.R., Uranium reduction, Annu. Rev. Microbiol., 2006, vol. 60, pp. 149–166.

    Article  CAS  PubMed  Google Scholar 

  28. Wang, H., Cheng, H., Wang, F., Wei, D., and Wang, X., An improved 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl tetrazolium bromide (MTT) reduction assay for evaluating the viability of Escherichia coli cells, J. Microbiol. Methods, 2010, vol. 82, pp. 330–333.

    Article  CAS  PubMed  Google Scholar 

  29. Wildung, R.E., Gorby, Y.A., Krupka, K.M., Hess, N.J., Li, S.W., Plymale, A.E., McKinley, J.P., and Fredrickson, J.K., Effect of electron donor and solution chemistry on products of dissimilatory reduction of technetium by Shewanella putrefaciens, Appl. Environ. Microbiol., 2000, vol. 66, pp. 2451–2460.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Wu, W.-M., Carley, J., Green, S.J., Luo, J., Kelly, S.D., Nostrand, J., Lowe, K., Mehlhorn, T., Carroll, S., Boonchayanant, B., Löfller, F.E., Watson, D., Kemner, K.M., Zhou, J., Kitanidis, P.K., et al., Effects of nitrate on the stability of uranium in a bioreduced region of the subsurface, Environ. Sci. Technol., 2010, vol. 44, pp. 5104–5111.

    Article  CAS  PubMed  Google Scholar 

  31. Xu, M., Wu, W.M., Wu, L., He, Z., Van Nostrand, J.D., Deng, Y., Luo, J., Carley, J., Ginder-Vogel, M., Gentry, T.J., Gu, B., Watson, D., Jardine, Ph.M., Marsh, T.L., Tiedje, J.M., et al., Responses of microbial community functional structures to pilot-scale uranium in situ bioremediation, ISME J., 2010, vol. 4, pp. 1060–1070.

    Article  PubMed  Google Scholar 

  32. Yildiz, B., Erten, H.N., and Kis, M., The sorption behavior of Cs+ ion on clay minerals and zeolite in radioactive waste management: sorption kinetics and thermodynamics, J. Radioanal. Nucl. Chem., 2011, vol. 288, pp. 475–483.

    Article  CAS  Google Scholar 

  33. Zhou, G., Yuan, J., and Gao, H., Regulation of biofilm formation by BpfA, BpfD, and BpfG in Shewanella oneidensis, Front. Microbiol., 2015, vol. 6. Article 790. https://doi.org/10.3389/fmicb.2015.00790

    Article  PubMed  PubMed Central  Google Scholar 

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ACKNOWLEDGMENTS

Analytical measurements were carried out using the equipment available at the Frumkin Institute of Physical Chemistry and Electrochemistry, Russian Academy of Sciences and the Research Center of Biotechnology, Russian Academy of Sciences.

Funding

This work was supported by the Russian Science Foundation, project no. 17-17-01212; biofilm research was supported by the Russian Foundation for Basic Research, project no. 16-03-00153); bioinformatic analysis of the genome, experiments on radionuclide reduction, maintenance of the culture collection, and phenotype research were supported by the Ministry of Science and Higher Education of the Russian Federation.

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Correspondence to T. N. Nazina.

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The authors declare that they have no conflict of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

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Translated by P. Sigalevich

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Babich, T.L., Safonov, A.V., Grouzdev, D.S. et al. Bacteria of the Genus Shewanella from Radionuclide-Contaminated Groundwater. Microbiology 88, 613–623 (2019). https://doi.org/10.1134/S0026261719040039

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