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Research Perspective of an Extremophilic Bacterium, Deinococcus radiodurans on Bioremediation of Radioactive Wastes

방사성 폐기물의 생물정화를 위한 극한세균 데이노코쿠스 라디오두란스의 연구적 고찰

  • Jeong, Sun-Wook (School of Environmental Engineering, University of Seoul) ;
  • Choi, Yong Jun (School of Environmental Engineering, University of Seoul)
  • 정선욱 (서울시립대학교 환경공학부) ;
  • 최용준 (서울시립대학교 환경공학부)
  • Received : 2017.01.10
  • Accepted : 2017.01.31
  • Published : 2017.04.10

Abstract

Increasing concerns on radioactive wastes have drawn much attention on the development of remediation technologies. Massive amounts of radioactive wastes generated from hospital and nuclear power plants were exposed to our environment. Although physicochemical removal methods were developed, an eco-friendly remediation method has not yet been demonstrated. Recently, an extremophilic bacterium has received much attention due to their extraordinary characteristics. Among them, Deinococcus radiodurans (D. radiodurans) strain was regarded as the best host organism for the removal of radioactive heavy metals and radionuclides, because of their superb characteristics like tolerance against the high level of radioactivity. In this article, we briefly introduced the extraordinary nature of D. radiodurans and also discussed the potential use of D. radiodurans strain for the removal of radioactive wastes.

방사성 폐기물에 대한 우려가 증대됨에 따라 생물정화 기술에 대한 관심이 고조되고 있다. 병원과 원자력발전 등에서 발생되는 많은 양의 방사성 폐기물이 환경에 직접 노출됨에 따라, 이를 정화하기 위한 다양한 물리화학적 기술이 보고되고 있다. 하지만, 이러한 방법은 고비용 및 고위험성 과정이 수반되기 때문에 미생물을 이용한 친환경적 생물정화 기술이 요구되고 있다. 최근, 고방사선 노출 등과 같은 극한환경에서 서식할 수 있는 방사선저항성 미생물에 대한 연구가 많이 보고되고 있으며, 이를 이용한 방사성 폐기물 정화에 대한 연구적 관심이 높아지고 있다. 데이노코쿠스 라디오두란스는 대표적인 방사선저항성 미생물로써 높은 방사선에 저항성을 갖는 특성으로 인해 방사성 폐기물 등의 유해물질 정화에 이용될 수 있다. 본 총설에서는 데이노코쿠스 라디오두란스의 방사선내성과 관련한 일반적 기작에 대해 소개하고, 방사성 폐기물의 생물정화 활용 가능성에 대해 논의한다.

Keywords

References

  1. N. Yoshida and J. Kanda, Tracking the Fukushima radionuclides, Science, 336, 1115-1116 (2012). https://doi.org/10.1126/science.1219493
  2. K. O. Buesseler, S. R. Jayne, N. S. Fisher, I. I. Rypina, H. Baumann, Z. Baumann, C. F. Breier, E. M. Douglass, J. George, A. M. Macdonald, H. Miyamoto, J. Nishikawa, S. M. Pike, and S. Yoshida, Fukushima-derived radionuclides in the ocean and biota off Japan, Proc. Natl. Acad. Sci., U. S. A., 109, 5984-5988 (2012). https://doi.org/10.1073/pnas.1120794109
  3. F. F. Evans, S. Rosado, G. V. Sebastian, R. Casella, PLOA Machado, C. Holmstrom, S. Kjelleberg, J. D. Van Elsas, and L. Seldin, Impact of oil contamination and biostimulation on the diversity of indigenous bacterial communities in soil microcosms, FEMS Microbiol. Ecol., 49, 295-305 (2004). https://doi.org/10.1016/j.femsec.2004.04.007
  4. S. K. Brar, M. Verma, R. Y. Surampalli, K. Misra, R. D. Tyagi, N. Meunier, and J. F. Blais, Bioremediation of hazardous wastes: A review, Pract. Period. Hazard. Toxic Radioact. Waste Manag., 10, 59-72 (2006). https://doi.org/10.1061/(ASCE)1090-025X(2006)10:2(59)
  5. D. Prakash, P. Gabani, A. K. Chandel, Z. Ronen, and O. V. Singh, Bioremediation: a genuine technology to remediate radionuclides from the environment, Microb. Biotechnol., 6, 349-360 (2013). https://doi.org/10.1111/1751-7915.12059
  6. G. M. Gadd, Bioremedial potential of microbial mechanisms of metal mobilization and immobilization, Curr. Opin. Biotechnol., 11, 271-279 (2000). https://doi.org/10.1016/S0958-1669(00)00095-1
  7. J. R. Lloyd, J. Ridley, T. Khizniak, N. N. Lyalikova, and L. E. Macaskie, Reduction of technetium by Desulfovibrio desulfuricans: biocatalyst characterization and use in a flow-through bioreactor, Appl. Environ. Microbiol., 65, 2691-2696 (1999).
  8. R. AP. Thomas, A. J. Beswick, G. Basnakova, R. Moller, and L. E. Macaskie, Growth of naturally occurring microbial isolates in metal-citrate medium and bioremediation of metal-citrate wastes, J. Chem. Technol. Biotechnol., 75, 187-195 (2000). https://doi.org/10.1002/(SICI)1097-4660(200003)75:3<187::AID-JCTB206>3.0.CO;2-I
  9. G. Raghu, V. Balaji, G. Venkateswaran, A. Rodrigue, and P. M. Mohan, Bioremediation of trace cobalt from simulated spent decontamination solutions of nuclear power reactors using E. coli expressing NiCoT genes, Appl. Microbiol. Biotechnol., 81, 571-578 (2008). https://doi.org/10.1007/s00253-008-1741-6
  10. M. Daly, Engineering radiation-resistant bacteria for environmental biotechnology, Curr. Opin. Biotechnol., 11, 280-285 (2000). https://doi.org/10.1016/S0958-1669(00)00096-3
  11. H. Brim, A. Venkateswaran, H. M. Kostandarithes, J. K. Fredrickson, and M. J. Daly, Engineering Deinococcus geothermalis for bioremediation of high-temperature radioactive waste environments, Appl. Environ. Microbiol., 69, 4575-4582 (2003). https://doi.org/10.1128/AEM.69.8.4575-4582.2003
  12. E. Gerber, R. Bernard, S. Castang, N. Chabot, F. Coze, A. Dreux-Zigha, E. Hauser, P. Hivin, P. Joseph, C. Lazarelli, G. Letellier, J. Olive, and J.-P. Leonetti, Deinococcus as new chassis for industrial biotechnology: biology, physiology and tools, J. Appl. Microbiol., 119, 1-10 (2015). https://doi.org/10.1111/jam.12808
  13. D. M. Sweet and B. E. Moseley, The resistance of Micrococcus radiodurans to killing and mutation by agents which damage DNA, Mutat. Res., 34, 175-186 (1976). https://doi.org/10.1016/0027-5107(76)90122-6
  14. J. R. Battista, Against all odds: the survival strategies of Deinococcus radiodurans, Annu. Rev. Microbiol., 51, 203-224 (1997). https://doi.org/10.1146/annurev.micro.51.1.203
  15. M. M. Cox and J. R. Battista, Deinococcus radiodurans-the consummate survivor, Nat. Rev. Microbiol., 3, 882-892 (2005). https://doi.org/10.1038/nrmicro1264
  16. D. Slade and M. Radman, Oxidative stress resistance in Deinococcus radiodurans, Microbiol. Mol. Biol. Rev., 75, 133-191 (2011). https://doi.org/10.1128/MMBR.00015-10
  17. C. C. Lange, L. P. Wackett, K. W. Minton, and M. J. Daly, Engineering a recombinant Deinococcus radiodurans for organopollutant degradation in radioactive mixed waste environments, Nat. Biotechnol., 16, 929-933 (1998). https://doi.org/10.1038/nbt1098-929
  18. B. W. Brooks and R. G. E. Murray, Nomenclature for Micrococcus radiodurans and other radiation resistant cocci: Deinococcaceae fam. nov. and Deinococcus gen. nov., including five species, Int. J. Syst. Bacteriol., 31, 353-360 (1981). https://doi.org/10.1099/00207713-31-3-353
  19. S. H. Yoo, H. Y. Weon, S. J. Kim, Y. S. Kim, B. Y. Kim, and S. W. Kwon, Deinococcus aerolatus sp. nov. and Deinococcus aerophilus sp. nov., isolated from air samples, Int. J. Syst. Evol. Microbiol., 60, 1191-1195 (2010). https://doi.org/10.1099/ijs.0.016030-0
  20. W. T. Im, H. M. Jung, L. N. Ten, M. K. Kim, N. Bora M. Goodfellow, S. Y. Lim, J. W. Jung, and S. T. Lee, Deinococcus aquaticus sp. nov., isolated from fresh water, and Deinococcus caeni sp. nov., isolated from activated sludge, Int. J. Syst. Evol. Microbiol., 58, 2348-2353 (2008). https://doi.org/10.1099/ijs.0.64082-0
  21. A. D. Groot, V. Chapon, P. Servant, R. Christen, M. F. Saux, S. Sommer, and T. Heulin, Deinococcus deserti sp. nov., a gamma-radiation-tolerant bacterium isolated from the Sahara Desert, Int. J. Syst. Evol. Microbiol., 55, 2441-2446 (2005). https://doi.org/10.1099/ijs.0.63717-0
  22. F. A. Rainey, K. Ray, M. Ferreira, B. Z. Gatz, M. F. Nobre, D. Bagaley, B. A. Rash, M. J. Park, A. M. Earl, N. C. Shank, A. M. Small, M. C. Henk, J. R. Battista, P. Kampfer, and M. S. da Costa, Extensive diversity of ionizing-radiation-resistant bacteria recovered from Sonoran Desert soil and description of nine new species of the genus Deinococcus obtained from a single soil sample, Appl. Environ. Microbiol., 71, 5225-5235 (2005). https://doi.org/10.1128/AEM.71.9.5225-5235.2005
  23. K. Suresh, G. S. Reddy, S. Sengupta, and S. Shivaji, Deinococcus indicus sp. nov., an arsenic resistant bacterium from aquifer in West Bengal, India, Int. J. Syst. Evol. Microbiol., 54, 457-461 (2004). https://doi.org/10.1099/ijs.0.02758-0
  24. A. C. Ferreira, M. F. Nobre, F. A. Rainey, M. T. Silva, R. Wait, J. Burghardt, A. P. Chung, and M. S. da Costa, Deinococcus geothermalis sp. nov. and Deinococcus murrayi sp. nov., two extremely radiation-resistant and slightly thermophilic species from hot springs, Int. J. Syst. Bacteriol., 47, 939-947 (1997). https://doi.org/10.1099/00207713-47-4-939
  25. P. Hirsch, C. A. Gallikowski, J. Siebert, K. Peissl, R. Kroppenstedt, P. Schumann, E. Stackebrandt, and R. Anderson, Deinococcus frigens sp. nov., Deinococcus saxicola sp. nov., and Deinococcus marmoris sp. nov., low temperature and draught-tolerating, UV resistant bacteria from continental Antarctica, Syst. Appl. Microbiol., 27, 636-645 (2004). https://doi.org/10.1078/0723202042370008
  26. M. Kolari, U. Schmidt, E. Kuismanen, and M. S. Salkinoja-Salonen, Firm but slippery attachment of Deinococcus geothermalis, J. Bacteriol., 184, 2473-2480 (2002). https://doi.org/10.1128/JB.184.9.2473-2480.2002
  27. O. White, J. A. Eisen, J. F. Heidelberg, E. K. Hickey, J. D. Peterson, R. J. Dodson, D. H. Haft, M. L. Gwinn et al., Genome sequence of the radioresistant bacterium Deinococcus radiodurans R1, Science, 286, 1571-1577 (1999). https://doi.org/10.1126/science.286.5444.1571
  28. X. Hua and Y. Hua, Improved complete genome sequence of the extremely radioresistant bacterium Deinococcus radiodurans R1 obtained using PacBio single-molecule sequencing, Genome Announc., 4, e00886-16 (2016).
  29. K. S. Makarova, M. V. Omelchenko, E. K. Gaidamakova, V. Y. Matrosova, A. Vasilenko, M. Zhai, A. Lapidus, A. Copeland, E. Kim, M. Land, K. Mavromatis, S. Pitluck, P. M. Richardson, and M. J. Daly, Deinococcus geothermalis: The pool of extreme radiation resistance genes shrinks, PLoS One, 2, e955 (2007). https://doi.org/10.1371/journal.pone.0000955
  30. A. de Groot, R. Dulermo, P. Ortet, L. Blanchard, P. Guerin, B. Fernandez, B. Vacherie, and C. Dossat, E. Jolivet, P. Siguire, M. Chandler, M. Barakat, A. Dedieu, and J. Armengaud, Alliance of proteomics and genomics to unravel the specificities of Sahara bacterium Deinococcus deserti, PLoS Genet., 5, e1000434 (2009). https://doi.org/10.1371/journal.pgen.1000434
  31. R. Pukall, A. Zeytun, S. Lucas, A. Lapidus, N. Hammon, S. Deshpande, M. Nolan, J. F. Cheng, S. Pitluck, K. Liolios, L. Pagani, N. Mikhailova, N. Ivanova, K. Mavromatis, A. Pati, R. Tapia, C. Han, L. Goodwin, A. Chen, K. Palaniappan, M. Land, L. Hauser, Y. J. Chang, C. D. Jeffries, E. M. Brambilla, M. Rohde, M. Goker, J. C. Detter, T. Woyke, J. Bristow, J. A. Eisen, V. Markowitz, P. Hugenholtz, N. C. Kyrpides, and H. P. Klenk, Complete genome sequence of Deinococcus maricopensis type strain (LB-34T), Stand. Genomic Sci., 4, 163-172 (2011). https://doi.org/10.4056/sigs.1633949
  32. M. Yuan, M. Chen, W. Zhang, W. Lu, J. Wang, M. Yang, P. Zhao, R. Tang, X. Li, Y. Hao, Z. Zhou, Y. Zhan, H. Yu, and M. Lin, Genome sequence and transcriptome analysis of the radioresistant bacterium Deinococcus gobiensis: Insights into the extreme environmental adaptations, PLoS One, 7, e34458 (2012). https://doi.org/10.1371/journal.pone.0034458
  33. A. Copeland, A. Zeytun, M. Yassawong, M. Nolan, S. Lucas, N. Hammon, S. Deshpande, J. F. Cheng, C. Han, R. Tapia, L. A. Goodwin, S. Pitluck, K. Mavromatis, K. Liolios, I. Pagani, N. Ivanova, A. Pati, A. Chen, K. Palaniappan, M. Land, L. Hauser, C. D. Jeffries, E. M. Brambilla, M. Rohde, J. Sikorski, R. Pukall, M. Goker, J. C. Detter, T. Woyke, J. Bristow, J. A. Eisen, V. Markowitz, N. C. Kyrpides, H. P. Klenk, and A. Lapidus, Complete genome sequence of the orange-red pigmented, radioresistant Deinococcus proteolyticus type strain (MRPT), Stand. Genomic Sci., 6, 240-250 (2012). https://doi.org/10.4056/sigs.2756060
  34. X. Xu, L. Jiang, Z. Zhang, Y. Shi, and H. Huang, Genome sequence of a gamma- and UV-ray-resistant Strain, Deinococcus wulumuqiensis R12, Genome Announc., 1, e00206-13 (2013).
  35. Y. Hu, X. Xu, P. Song, L. Jiang, Z. Zhang, and H. Huang, Draft genome sequence of Deinococcus xibeiensis R13, a new carotenoid-producing strain, Genome Announc., 1, e00987-13 (2013).
  36. V. G. Stepanov, P. Vaishampayan, K. Venkateswaran, and G. E. Fox, Draft genome sequence of Deinococcus phoenicis, a novel strain isolated during the phoenix lander spacecraft assembly, Genome Announc., 2, e00301-14 (2014).
  37. K. Satoh, T. Onodera, K. Omoso, K. T. Yano, T. Katayama, Y. Oono, and I. Narumi, Draft genome sequence of the radioresistant bacterium Deinococcus grandis, isolated from freshwater fish in Japan, Genome Announc., 4, e01631-15 (2016).
  38. J. A. Imlay, Cellular defenses against superoxide and hydrogen peroxide, Annu. Rev. Biochem., 77, 755-776 (2008). https://doi.org/10.1146/annurev.biochem.77.061606.161055
  39. M. M. Cox, J. L. Keck, and J. R. Battista, Rising from the Ashes: DNA Repair in Deinococcus radiodurans, PLoS Genet., 6, e1000815 (2010). https://doi.org/10.1371/journal.pgen.1000815
  40. D. Ghosal, M. V. Omelchenko, E. K. Gaidamakova, V. Y. Matrosova, A. Vasilenko, A. Venkateswaran, M. Zhai, H. M. Kostandarithes, H. Brim, K. S. Makarova, L. P. Wackett, J. K. Fredrickson, and M. J. Daly, How radiation kills cells: survival of Deinococcus radiodurans and Shewanella oneidensis under oxidative stress, FEMS Microbiol. Rev., 29, 361-375 (2005).
  41. K. Zahradka, D. Slade, A. Bailone, S. Sommer, D. Averbeck, M. Petranovic, A. B. Lindner, and M. Radman, Reassembly of shattered chromosomes in Deinococcus radiodurans, Nature, 443, 569-573 (2006).
  42. E. Griffiths and R. S. Gupta, Identification of signature proteins that are distinctive of the Deinococcus-Thermus phylum, Int. Microbiol., 10, 201-208 (2007).
  43. A. M. Earl, M. M. Mohundro, I. S. Mian, and J. R. Battista, The IrrE protein of Deinococcus radiodurans R1 is a novel regulator of recA expression, J. Bacteriol., 184, 6216-6224 (2002). https://doi.org/10.1128/JB.184.22.6216-6224.2002
  44. Y. Hua, I. Narumi, G. Gao, B. Tian, K. Satoh, S. Kitayama, and B. Shen, PprI: a general switch responsible for extreme radioresistance of Deinococcus radiodurans, Biochem. Biophys. Res. Commun., 306, 354-360 (2003). https://doi.org/10.1016/S0006-291X(03)00965-3
  45. H. Lu, G. Gao, G. Xu, L. Fan, L. Yin, B. Shen, and Y. Hua, Deinococcus radiodurans PprI switches on DNA damage-response and cellular survival networks after radiation damage, Mol. Cell. Proteom., 8, 481-494 (2009). https://doi.org/10.1074/mcp.M800123-MCP200
  46. Y. Wang, Q. Xu, H. Lu, L. Lin, L. Wang, H. Xu, X. Cui, H. Zhang, T. Li, and Y. Hua, Protease activity of PprI facilitates DNA damage response: $Mn^{(2+)}$-dependence and substrate sequence-specificity of the proteolytic reaction, PLoS One, 10, e0122071 (2015). https://doi.org/10.1371/journal.pone.0122071
  47. M. Ludanyi, L. Blanchard, R. Dulermo, G. Brandelet, L. Bellanger, D. Pignol, D. Lemaire, and A. de Groot, Radiation response in Deinococcus deserti: IrrE is a metalloprotease that cleaves repressor protein DdrO, Mol. Microbiol., 94, 434-449 (2014). https://doi.org/10.1111/mmi.12774
  48. A. Devigne, S. Ithurbide, T. C. Bouthier, F. Passot, M. Mathieu, S. Sommer, and P. Servant, DdrO is an essential protein that regulates the radiation desiccation response and the apoptotic-like cell death in the radioresistant Deinococcus radiodurans bacterium, Mol. Microbiol., 96, 1069-1084 (2015). https://doi.org/10.1111/mmi.12991
  49. L. Wang, X. Guangzhi, H. Chen,Y. Zhao, N. Xu, B. Tian, and Y. Hua, DrRRA: a novel response regulator essential for the extreme radioresistance of Deinococcus radiodurans, Mol. Microbiol., 67, 1211-1222 (2008). https://doi.org/10.1111/j.1365-2958.2008.06113.x
  50. S. S. Desai, Y. S. Rajpurohit, H. S. Misra, and D. N. Deobagkar, Characterization of the role of the RadS/RadR two-component system in the radiation resistance of Deinococcus radiodurans, Microbiology, 157, 2974-2982 (2011). https://doi.org/10.1099/mic.0.049361-0
  51. C. H. Tsai, R. Liao, B. Chou, and L. M. Contreras, Transcriptional analysis of Deinococcus radiodurans reveals novel small RNAs that are differentially expressed under ionizing radiation, Appl. Environ. Microbiol., 81, 1754-1764 (2015). https://doi.org/10.1128/AEM.03709-14
  52. A. Martinez and R. Kolter, Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps, J. Bacteriol., 179, 5188-5194 (1997). https://doi.org/10.1128/jb.179.16.5188-5194.1997
  53. J. K. Fredrickson, S. M. Li, E. K. Gaidamakova, V. Y. Matrosova, M. Zhai, H. M. Sulloway, J. C. Scholten, M. G. Brown, D. L. Balkwill, and M. J. Daly, Protein oxidation: key to bacterial desiccation resistance?, ISME J., 2, 393-403 (2008). https://doi.org/10.1038/ismej.2007.116
  54. M. J. Daly, E. K. Gaidamakova, V. Y. Matrosova, A. Vasilenko, M. Zhai, A. Venkateswaran, M. Hess, M. V. Omelchenko, H. M. Kostandarithes, K. S. Makarova, L. P. Wackett, J. K. Fredrickson, and D. Ghosal, Accumulation of Mn(II) in Deinococcus radiodurans facilitates gamma-radiation resistance, Science, 306, 1025-1028 (2004). https://doi.org/10.1126/science.1103185
  55. M. J. Daly, E. K. Gaidamakova, V. Y. Matrosova, J. G. Kiang, R. Fukumoto, D. Y. Lee, N. B. Wehr, G. A. Viteri, B. S. Berlett, and R. L. Levine, Small-molecule antioxidant proteome-shields in Deinococcus radiodurans, PLoS One, 5, e12570 (2010). https://doi.org/10.1371/journal.pone.0012570
  56. L. Lemee, E. Peuchant, M. Clerc, M. Brunner, and H. Pfander, Deinoxanthin: a new carotenoid isolated from Deinococcus radiodurans, Tetrahedron, 53, 919-926 (1997). https://doi.org/10.1016/S0040-4020(96)01036-8
  57. L. Zhang, Q. Yang, X. Luo, C. Fang, Q. Zhang, and Y. Tang, Knockout of crtB or crtI gene blocks the carotenoid biosynthetic pathway in Deinococcus radiodurans R1 and influences its resistance to oxidative DNA-damaging agents due to change of free radicals scavenging ability, Arch. Microbiol., 188, 411-419 (2007). https://doi.org/10.1007/s00203-007-0262-5
  58. B. Tian, Z. Xu, Z. Sun, J. Lin, and Y. Hua, Evaluation of the antioxidant effects of carotenoids from Deinococcus radiodurans through targeted mutagenesis, chemiluminescence, and DNA damage analyses, Biochim. Biophys. Acta, 1770, 902-911 (2007). https://doi.org/10.1016/j.bbagen.2007.01.016
  59. D. Appukuttan, A. S. Rao, and S. K. Apte, Engineering of Deinococcus radiodurans R1 for bioprecipitation of uranium from dilute nuclear waste, Appl. Environ. Microbiol., 72, 7873-7878 (2006). https://doi.org/10.1128/AEM.01362-06
  60. H. Brim, S. C. McFarlan, J. K. Fredrickson, K. W. Minton, M. Zhai, L. P. Wackett, and M. J. Daly, Engineering Deinococcus radiodurans for metal remediation in radioactive mixed waste environments, Nat. Biotechnol., 18, 85-90 (2000). https://doi.org/10.1038/71986
  61. C. C. Lange, L. P. Wackett, K. W. Minton, and M. J. Daly, Engineering a recombinant Deinococcus radiodurans for organopollutant degradation in radioactive mixed waste environments, Nat. Biotechnol., 16, 929-933 (1998). https://doi.org/10.1038/nbt1098-929
  62. G. Raghu, S. S Singh, S. K. Lunavat, M. M. Pamarthi, A. Rodrigue, B. Vadivelu, P. B. Phanithi, V. Gopala, and S. K. Apte, Engineered Deinococcus radiodurans R1 with NiCoT genes for bioremoval of trace cobalt from spent decontamination solutions of nuclear power reactors, Appl. Microbiol. Biotechnol., 99, 9203-9213 (2015). https://doi.org/10.1007/s00253-015-6761-4
  63. L. Newsome, K. Morris, and J. R. Lloyd, The biogeochemistry and bioremediation of uranium and other priority radionuclides, Chem. Geol., 363, 164-184 (2014). https://doi.org/10.1016/j.chemgeo.2013.10.034
  64. L. Xiangqian, X. Huizhong, Z. S. Chen, and G. Chen, Biosynthesis of Nanoparticles by Microorganisms and Their Applications, J. Nanomater, 2011, 1-16 (2011).
  65. M. H. Choi, H. E. Shim, S. J. Yun, S. H. Park, D. S. Choi, B. S. Jang, Y. J. Choi, and J. J. Jeon, Gold-nanoparticle-immobilized Desalting columns for highly efficient and specific removal of radioactive iodine in aqueous media, ACS Appl. Mater. Interfaces, 8, 29227-29231 (2016). https://doi.org/10.1021/acsami.6b11136
  66. L. Du, H. Jiang, X. Liu, and E. Wang, Biosynthesis of gold nanoparticles assisted by Escherichia coli $DH5{\alpha}$ and its application on direct electrochemistry of hemoglobin. Electrochem. Commun., 9, 1165-1170 (2007). https://doi.org/10.1016/j.elecom.2007.01.007
  67. M. I. Husseiny, M. A. El-Aziz, Y. Badr, and M. A. Mahmoud, Biosynthesis of gold nanoparticles using Pseudomonas aeruginosa, Spectrochim. Acta A, 67, 1003-1006 (2007). https://doi.org/10.1016/j.saa.2006.09.028
  68. S. Bose, M. F. Hochella, Y. A. Gorby, D. W. Kennedy, D. E. McCready, A. S. Madden, and B. H. Lower, Bioreduction of hematite nanoparticles by the dissimilatory iron reducing bacterium Shewanella oneidensis MR-1, Geochim. Cosmochim. Acta, 73, 962-976 (2009). https://doi.org/10.1016/j.gca.2008.11.031
  69. M. M. G. Babu and P. Gunasekaran, Production and structural characterization of crystalline silver nanoparticles from Bacillus cereus isolate, Colloids Surf. B, 74, 191-195 (2009). https://doi.org/10.1016/j.colsurfb.2009.07.016
  70. S. He, Z. Guo, Y. Zhang, S. Zhang, J. Wang, and N. Gu, Biosynthesis of gold nanoparticles using the bacteria Rhodopseudomonas capsulate, Mater. Lett., 61, 3984-3987 (2007). https://doi.org/10.1016/j.matlet.2007.01.018
  71. R. R. Kulkarni, N. S. Shaiwale, D. N. Deobagkar, and D. D. Deobagkar, Synthesis and extracellular accumulation of silver nanoparticles by employing radiation-resistant Deinococcus radiodurans, their characterization, and determination of bioactivity, Int. J. Nanomed., 10, 963-974 (2015).
  72. J. Li, Q. Li, X. Ma, B. Tian, T. Li, J. Yu, S. Dai, Y. Weng, and Y. Hua, Biosynthesis of gold nanoparticles by the extreme bacterium Deinococcus radiodurans and an evaluation of their antibacterial properties, Int. J. Nanomed., 11, 5931-5944 (2016). https://doi.org/10.2147/IJN.S119618
  73. C. S. Misra, D. Appukuttan, V. S. Kantamreddi, A. S. Rao, and S. K. Apte, Recombinant D. radiodurans cells for bioremediation of heavy metals from acidic/neutral aqueous wastes, Bioeng. Bugs, 3, 44-48 (2012).
  74. J. K. Fredrickson, H. M. Kostandarithes, S. W. Li, A. E. Plymale, and M. J. Daly, Reduction of Fe(III), Cr(VI), U(VI), and Tc(VII) by Deinococcus radiodurans R1, Appl. Environ. Microbiol., 66, 2006-2011 (2000). https://doi.org/10.1128/AEM.66.5.2006-2011.2000
  75. R. B. Payne, D. M. Gentry, B. J. Rapp-Giles, L. Casalot, and J. D. Wall, Uranium reduction by Desulfovibrio desulfuricans strain G20 and a cytochrome c3 mutant, Appl. Environ. Microbiol., 68, 3129-3132 (2002) https://doi.org/10.1128/AEM.68.6.3129-3132.2002
  76. D. R. Lovley and E. J. Phillips, Reduction of uraniumby Desulfovibrio desulfuricans, Appl. Environ. Microbiol., 58, 850-856 (1992).
  77. K. S. Nilgiriwala, A. Alahari, A. S. Rao, and S. K. Apte, Cloning and overexpression of alkaline phosphatase PhoK from Sphingomonas sp. strain BSAR-1 for bioprecipitation of uranium from alkaline solutions, Appl. Environ. Microbiol., 74, 5516-5523 (2008). https://doi.org/10.1128/AEM.00107-08
  78. A. S. Madden, A. I. Swindle, M. J. Beazley, J. W. Moon, B. Ravel, and T. J. Phelps, Longterm solid-phase fate of co-precipitated U(VI)-Fe(III) following biological iron reduction by Thermoanaerobacter, Am. Mineral., 97, 1641-1652 (2012). https://doi.org/10.2138/am.2012.4122
  79. T. V. Khijniak, A. I. Slobodkin, V. Coker, J. C. Renshaw, F. R. Livens, E. A. Bonch-Osmolovskaya, N. K. Birkeland, N. N. Medvedeva-Lyalikova, and J. R. Lloyd, Reduction of uranium(VI) phosphate during growth of the thermophilic bacterium Thermoterrabacterium ferrireducens, Appl. Environ. Microbiol., 71, 6423-6426 (2005). https://doi.org/10.1128/AEM.71.10.6423-6426.2005
  80. L. E. Macaskie, R. M. Empson, A. K. Cheetham, C. P. Grey, and A. J. Skarnulis, Uranium bioaccumulation by a Citrobacter sp. as a result of enzymically mediated growth of polycrystalline $HUO_2PO_4$, Science, 257, 782-784 (1992). https://doi.org/10.1126/science.1496397
  81. J. R. Lloyd, C. Leang, C., A. L. Hodges Myerson, M. V. Coppi, S. Cuifo, B. Methe, S. J. Sandler, and D. R. Lovely, Biochemical and genetic characterization of PpcA, a periplasmic c-type cytochrome in Geobacter sulfurreducens, Biochem. J., 369, 153-161 (2003). https://doi.org/10.1042/bj20020597
  82. J. R. Lloyd, P. Yong, and L. E. Macaskie, Biological reduction and removal of Np(V) by two microorganisms, Environ. Sci. Technol., 34, 1297-1301 (2000). https://doi.org/10.1021/es990394y
  83. J. R. Lloyd, J. Ridley, T. Khizniak, N. N. Lyalikova, and L. E. Macaskie, Reduction of technetium by Desulfovibrio desulfuricans: biocatalyst characterization and use in a flowthrough bioreactor, Appl. Environ. Microbiol., 65, 2691-2696 (1999).
  84. N. N. Lyalikova and T. V. Khizhnyak, Reduction of heptavalent technetium by acidophilic bacteria of the genus Thiobacillus, Microbiology, 65, 468-473 (1996).
  85. M. J. Marshall, A. C. Dohnalkova, D. W. Kennedy, A. E. Plymale, S. H. Thomas, F. E. Loffler, R. A. Sanford, J. M. Zachara, J. K. Fredrickson, and A. S. Beliaev, Electron donordependent radionuclide reduction and nanoparticle formation by Anaeromyxobacter dehalogenans strain 2CP-C, Environ. Microbiol., 11, 534-543 (2009). https://doi.org/10.1111/j.1462-2920.2008.01795.x
  86. H. Boukhalfa, G. A. Icopini, S. D. Reilly, and M. P. Neu, Plutonium (IV) reduction by the metal-reducing bacteria Geobacter metallireducens GS15 and Shewanella oneidensis MR1, Appl. Environ. Microbiol., 73, 5897-5903 (2007). https://doi.org/10.1128/AEM.00747-07
  87. B. Luksiene, R. Druteikiene, D. Peciulyte, D. Baltrunas, V. Remeikis, and A. Paskevicius, Effect of microorganisms on the plutonium oxidation states, Appl. Radiat. Isot., 70, 442-449 (2012). https://doi.org/10.1016/j.apradiso.2011.11.016
  88. L. E. Macaskie, B. C. Jeong, and M. R. Tolley, Enzymically accelerated biomineralization of heavy metals: Application to the removal of americium and plutonium from aqueous flows, FEMS Microbiol. Rev., 14, 351-367 (1994). https://doi.org/10.1111/j.1574-6976.1994.tb00109.x
  89. T. Councell, E. Landa, and D. Lovley, Microbial reduction of iodate, Water Air Soil Pollut., 100, 99-106 (1997). https://doi.org/10.1023/A:1018370423790
  90. S. Anderson and V. D. Appanna, Microbial formation of crystalline strontium carbonate, FEMS Microbiol. Lett., 116, 43-48 (1994). https://doi.org/10.1111/j.1574-6968.1994.tb06673.x
  91. V. Achal, X. Pan, and D. Zhang, Bioremediation of strontium (Sr) contaminated aquifer quartz sand based on carbonate precipitation induced by Sr resistant Halomonas sp, Chemosphere, 89, 764-768 (2012). https://doi.org/10.1016/j.chemosphere.2012.06.064
  92. F. G. Ferris, C. M. Fratton, J. P. Gerits, S. Schultze-Lam, and B. S. Lollar, Microbial precipitation of a strontium calcite phase at a groundwater discharge zone near Rock Creek, British Columbia, Canada, Geomicrobiol. J., 13, 57-67 (1995). https://doi.org/10.1080/01490459509378004
  93. D. L. Vullo, H. M. Ceretti, E. A. Hughes, S. Ramyrez, and A. Zalts, Cadmium, zinc and copper biosorption mediated by Pseudomonas veronii 2E, Bioresour. Technol., 99, 5574-5581 (2008). https://doi.org/10.1016/j.biortech.2007.10.060
  94. H. Guo, S. Luo, L. Chen, X. Xiao, Q. Xi, W. Wei, G. Zeng, C. Liu, Y. Wan, J. Chen, and Y. He, Bioremediation of heavy metals by growing hyperaccumulator endophytic bacterium Bacillus sp. L14, Bioresour. Technol., 101, 8599-8605 (2010). https://doi.org/10.1016/j.biortech.2010.06.085
  95. V. Achal, X. Pan, and D. Zhang, Remediation of copper-contaminated soil by Kocuria flava CR1, based on microbially induced calcite precipitation, Ecol. Eng., 37, 1601-1605 (2011). https://doi.org/10.1016/j.ecoleng.2011.06.008
  96. K. Hrynkiewicz, G. Dabrowska, C. Baum, K. Niedojadlo, and P. Leinweber, Interactive and single effects of ectomycorrhiza formation and Bacillus cereus on metallothionein MT1 expression and phytoextraction of Cd and Zn by Willows, Water Air Soil Pollut., 223, 957-968 (2012). https://doi.org/10.1007/s11270-011-0915-5
  97. V. Achal, X. Pan, Q. Fu, and D. Zhang, Biomineralization based remediation of As (III) contaminated soil by Sporosarcina ginsengisoli. J. Hazard. Mater., 201-202, 178-184 (2012). https://doi.org/10.1016/j.jhazmat.2011.11.067
  98. P. Kanmani, J. Aravind, and D. Preston, Remediation of chromium contaminants using bacteria, Int. J. Environ. Sci. Technol., 9, 183-193 (2012). https://doi.org/10.1007/s13762-011-0013-7