Skip to main content

Advertisement

SpringerLink
Log in

Engineered Deinococcus radiodurans R1 with NiCoT genes for bioremoval of trace cobalt from spent decontamination solutions of nuclear power reactors

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

The aim of the present work was to engineer bacteria for the removal of Co in contaminated effluents. Radioactive cobalt (60Co) is known as a major contributor for person-sievert budgetary because of its long half-life and high γ-energy values. Some bacterial Ni/Co transporter (NiCoT) genes were described to have preferential uptake for cobalt. In this study, the NiCoT genes nxiA and nvoA from Rhodopseudomonas palustris CGA009 (RP) and Novosphingobium aromaticivorans F-199 (NA), respectively, were cloned under the control of the groESL promoter. These genes were expressed in Deinococcus radiodurans in reason of its high resistance to radiation as compared to other bacterial strains. Using qualitative real time-PCR, we showed that the expression of NiCoT-RP and NiCoT-NA is induced by cobalt and nickel. The functional expression of these genes in bioengineered D. radiodurans R1 strains resulted in >60 % removal of 60Co (≥5.1 nM) within 90 min from simulated spent decontamination solution containing 8.5 nM of Co, even in the presence of >10 mM of Fe, Cr, and Ni. D. radiodurans R1 (DR-RP and DR-NA) showed superior survival to recombinant E. coli (ARY023) expressing NiCoT-RP and NA and efficiency in Co remediation up to 6.4 kGy. Thus, the present study reports a remarkable reduction in biomass requirements (2 kg) compared to previous studies using wild-type bacteria (50 kg) or ion-exchanger resins (8000 kg) for treatment of ~105-l spent decontamination solutions (SDS).

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

References

  • Akthar N, Sastry KS, Mohan PM (1996) Mechanism of metal biosorption by fungal biomass. Bimetals 9:21–28

    CAS  Google Scholar 

  • Amachi S, Minami K, Miyasaka I, Fukunaga S (2010) Ability of anaerobic microorganisms to associate with iodine: 125I tracer experiments using laboratory strains and enriched microbial communities from subsurface formation water. Chemosphere 79:349–354

    Article  CAS  PubMed  Google Scholar 

  • Appukuttan D, Rao AS, Apte SK (2006) Engineering of Deinococcus radiodurans R1 for Bioprecipitation of Uranium from Dilute Nuclear Waste. Appl Environ Microbiol 72:7873–7878

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ayres JA (1970) Decontamination of Nuclear reactors and equipments, Ronald Press Company NY. Libr Cong Cat Card Number 76:110543

  • Battista JR (1997) Against all odds: the survival strategies of Deinococcus radiodurans. Annu Rev Microbiol 51:203–224

    Article  CAS  PubMed  Google Scholar 

  • Bradbury D, Smee TL, Williams MR (1986) Recent reactor decontamination experience with LOMI/CANDECON and related processes. In: Proceedings of international conference on water chemistry of nuclear reactor systems (4), British Nuclear Energy Society (BNES) London, 257

  • Brim H, McFarlan SC, Fredrickson JK, Minton KW, Zhai M, Wackett LP, Daly MJ (2000) Engineering Deinococcus radiodurans for metal remediation in radioactive mixed waste environments. Nat Biotechnol 18:85–90

    Article  CAS  PubMed  Google Scholar 

  • Brim H, Venkateshwaran A, Kostandarithes HM, Fredrickson JK, Daly MJ (2003) Engineering Deinococcus geothermalis for bioremediation of high-temperature radioactive waste environments. Appl Environ Microbiol 69:4575–4582

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Carroll JD, Daly MJ, Minton KW (1996) Expression of recA in Deinococcus radiodurans. J Bacteriol 178:130–135

    PubMed Central  CAS  PubMed  Google Scholar 

  • Charlesworth DH (1971) Water reactor plant contamination and decontamination requirements - a survey. Proc Am Power Conf 33:749–756

    Google Scholar 

  • Cohen A (1980) Water coolant technology of power reactors. American Nuclear Society, La Grange Park

    Google Scholar 

  • Daly MJ, Minton KW (1995) Resistance to radiation. Science 270:1318

    Article  CAS  PubMed  Google Scholar 

  • Daly MJ, Minton KW (1996) An alternative pathway of recombination of chromosomal fragments precedes recA-dependent recombination in the radioresistant bacterium Deinococcus radiodurans. J Bacteriol 178:4461–4471

    PubMed Central  CAS  PubMed  Google Scholar 

  • Daly MJ (2000) Engineering radiation-resistant bacteria for environmental biotechnology. Curr Opin Biotechnol 11:280–285

    Article  CAS  PubMed  Google Scholar 

  • Deng X, Jinmei H, Ning H (2013) Comparative study on Ni2+-affinity transport of nickel/cobalt permeases (NiCoTs) and the potential of recombinant Escherichia coli for Ni2+ bioaccumulation. Bioresour Technol 130:69–74

    Article  CAS  PubMed  Google Scholar 

  • Duprey A, Viviane C, Franck F, Clémence G, Yoann L, Philippe L, Fanny S, Valérie D, Agnès R, Corinne D (2014) “NiCo Buster”: engineering E. coli for fast and efficient capture of cobalt and nickel. J Biol Eng 8:19

    Article  PubMed Central  PubMed  Google Scholar 

  • Frišták V, Martin P, Michaela V, Juraj L, Marián R (2014a) Monitoring 60Co activity for the characterization of the sorption process of Co2+ ions in municipal activated sludge. J Radioanal Nucl Chem 299:1607–1614

    Article  PubMed Central  PubMed  Google Scholar 

  • Frišták V, Michaela V, Martin P, Juraj L (2014b) The Influence of chemical modification on the Co 2+ ion sorption process by anaerobic sludge. Pol J Environ Stud 23:705–712

  • Gadd GM, White C (1989) Heavy metal and radionuclide accumulation and toxicity in fungi and yeast. In: Poole RK, Gadd GM (eds) Metal-microbe interactions. IRI, Oxford, pp 19–38

    Google Scholar 

  • Green SJ, Prakash O, Jasrotia P, Overholt WA, Cardenas E, Hubbard D, Tiedje JM, Watson DB, Schadt CW, Brooks SC, Kostka JE (2012) Denitrifying bacteria from the genus Rhodanobacter dominate bacterial communities in the highly contaminated subsurface of a nuclear legacy waste site. Appl Environ Microbiol 78:1039–1047

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gunjan P, Paul D, Jain RK (2005) Conceptualizing “suicidal genetically bioengineered microorganisms” for bioremediation applications. Biochem Biophys Res Commun 327:637–639

    Article  Google Scholar 

  • Hebbeln P, Eitinger T (2004) Heterologous production and characterization of bacterial nickel/cobalt permeases. FEMS Microbiol Lett 230:129–135

    Article  CAS  PubMed  Google Scholar 

  • Komeda H, Kobayashi M, Shimizu S (1997) A novel transporter involved in cobalt uptake. Proc Natl Acad Sci 94:36–41

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kulkarni S, Anand B, Shree KA (2013) Bioprecipitation of uranium from alkaline waste solutions using recombinant Deinococcus radiodurans. J Hazard Mater 262:853–861

    Article  CAS  PubMed  Google Scholar 

  • Kumar R, Singh S, Singh OV (2007) Bioremediation of radionuclides: emerging technologies. OMICS 11:295–304

    Article  CAS  PubMed  Google Scholar 

  • Prakash D, Prashant G, Anuj K, Chandel ZR, Om VS (2013) Bioremediation: a genuine technology to remediate radionuclides from the environment. Microb Biotechnol 6:349–360

    Article  PubMed Central  PubMed  Google Scholar 

  • Kurnaz A, Kucukomeroglu B, Keser R, Okumusoglu NT, Korkmaz F, Karahan G, Cevik U (2007) Determination of radioactivity levels and hazards of soil and sediment samples in Firtina Valley (Rize, Turkey). Appl Radiat Isot 65:1281–1289

    Article  CAS  PubMed  Google Scholar 

  • Lange CC, Wackett LP, Minton KW, Daly MJ (1998) Engineering a recombinant Deinococcus radiodurans for organopollutant degradation in radioactive mixed waste environments. Nat Biotechnol 16:929–933

    Article  CAS  PubMed  Google Scholar 

  • Lejon J, Hermansson A, Bertholdt HO (1994) A full system decontamination of Oskarshamn 1 BWR. Proc Int Conf Water Chem Nucl Reactor Syst 1:203–210

    CAS  Google Scholar 

  • Lin J, Qi R, Aston C, Jing J, Anantharaman TS, Mishra B, White O, Daly MJ, Minton KW, Venter JC, Schwartz DC (1999) Whole-genome shotgun optical mapping of Deinococcus radiodurans. Science 285:1558–1562

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Duu-Jong L (2014) Biosorption studies on bioremediation and biorecovery. J Taiwan Inst Chem Eng 45(2):1863–1864

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔ CT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lloyd JR, Renshaw JC (2005) Bioremediation of radioactive waste: radionuclide-microbe interactions in laboratory and field-scale studies. Curr Opin Biotechnol 16:254–60

    Article  CAS  PubMed  Google Scholar 

  • Meima R, Lidstrom ME (2000) Characterization of the minimal replicon of a cryptic Deinococcus radiodurans SARK plasmid and development of versatile Escherichia coli-D. radiodurans shuttle vectors. Appl Environ Microbiol 66:3856–3867

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Misra CS, Rita M, Shree KA (2014) Harnessing a radiation inducible promoter of Deinococcus radiodurans for enhanced precipitation of uranium. J Biotechnol 189:88–93

    Article  CAS  PubMed  Google Scholar 

  • Maruthi Mohan P, Kiranmayi P, Haritha A, Premsagar K, Tiwari A, Raghu G (2007) Bioremediation of toxic metal ions: a focused view of metal transportomes. In: Chopra VL, Sharma RP, Bhat SR, Prasanna BM (eds) Search for new genes, 1st edn 14. Academic Foundation in association with the National Academy of Agricultural Science (NAAS), New Delhi, pp 231-243

  • Naveena Lavanya Latha J, Rashmi K, Maruthi Mohan P (2005) Cell wall bound metal ions are taken up in Neurospora crassa. Can J Microbiol 51:1021–1026

    Article  PubMed  Google Scholar 

  • Raghu G, Balaji V, Venkateswaran G, Rodrigue A, Maruthi Mohan P (2008) 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

    Article  CAS  PubMed  Google Scholar 

  • Rama Rao K, Sajani LS, Maruthi Mohan P (1996) Bioaccumulation and biosorption of cobalt ions by Neurospora crassa. Biotechnol Lett 18:1205–1208

    Article  Google Scholar 

  • Rashmi K, Naga Sowjanya T, Maruthi Mohan P, Balaji V, Venkateswaran G (2004) Bioremediation of 60Co from simulated spent decontamination solutions. Sci Total Environ 328:1–14

    Article  CAS  PubMed  Google Scholar 

  • Rashmi K, Haritha A, Balaji V, Tripathi VS, Venkateswaran G, Maruthi Mohan P (2007) Bioremediation of 60-Co from simulated spent decontamination solutions of nuclear power reactors by bacteria. Curr Sci 92(10):1407–1409

    CAS  Google Scholar 

  • Rodrigue A, Effantin G, Mandrand BM (2005) Identification of rcnA (yohM), a nickel and cobalt resistance gene in Escherichia coli. J Bacteriol 187(8):2912–2916

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132(3):365–386

    CAS  PubMed  Google Scholar 

  • Satinder KB, Verma M, Surampalli RY, Misra K, Tyagi RD, Meunier N, Blais JF (2006) Bioremediation of hazardous wastes -a review. Pract Periodical Hazard Toxic Radioactive Waste Manage 10 (2): 59-72 doi: 10.1061/(ASCE)1090-025X 10:2(59)

  • Shih TY, Shen-Long T (2014) Simultaneous silver recovery and bactericidal bionanocomposite formation via engineered biomolecules. R Soc Chem Adv 4:40994–40998

    CAS  Google Scholar 

  • Taylor NK (1976) Review of available data on the release, transport and deposition of corrosion products in PWR, BWR and SGHWR Systems. United Kingdom Atomic Energy Authority Report, AERE-R8164

  • Tišáková L, Pipíška M, Godány A, Horník M, Vidová B, Augustín J (2013) Bioaccumulation of 137Cs and 60Co by bacteria isolated from spent nuclear fuel pools. J Radioanal Nucl Chem 295:737–748

    Article  Google Scholar 

  • Urch SD (2013) Radiochemistry. Annual Reports Section “A”(Inorg Chem) 109: 468-483

  • Venkateswaran G, Dey GR, Kerkar AS, Gokhale BK, Gokhale AS, Balaji V, Kumbhar AG, Nema MK, Anantharaman K, Kumar J, Ananthan P, Kumar S, Sathe SM, Sah DN, Sanyal DN, Nath R, Sahu RK, Ramu A, Kansara HN, Muraisharan K, Save CB, Patil DP, Padmanabhan SA, Shinde RP, Pisharody NN, Upadyaya TC, Sharma BL, Katiyar SC, Wagh PM (2003) Chemical decontamination of cleanup system of unit-2 Tarapur Atomic Power Station Phase 2 Task. BARC Report No. BARC/ 2003/ 012

  • Won SW, Pratap K, Wei W, Areum L, Yeoung-Sang Y (2014) Biosorbents for recovery of precious metals. Bioresour Technol 160:203–212

    Article  CAS  PubMed  Google Scholar 

  • Ybarra GR, Webb R (1999) Effects of divalent metal cations, resistance mechanisms of the cyanobacterium Synechococcus sp. strain 7942. J Hazard Subst Res 2:1–9

    Google Scholar 

Download references

Acknowledgments

The authors dedicate this manuscript to late Prof P. Maruthi Mohan. The authors thank Dr. Thomas Eitinger, Humboldt University, Germany, for providing the plasmids (pCH675-RP and pCH675-NA), K. W. Minton and M. J. Daly, Uniformed Services University of the Health Sciences, Bethesda, MD, for providing the D. radiodurans R1 strain, and M. E. Lidstrom, Departments of Chemical Engineering and Microbiology, University of Washington, Seattle, for providing the E. coli-Deinococcus shuttle vector pRAD1. We thank Deepti Appukuttan, who provided technical information related to Deinococcus transformation. We thank Dr. Venkata Prasuja Nakka, Department of Biotechnology and Bioinformatics, University of Hyderabad, Dr. Abdul Qadeer Mohammed, Department of Biochemistry, Osmania University, Hyderabad for their helpful suggestions and critical evaluation of the manuscript. The research work was supported by grants from the Department of Atomic Energy (No: 2004/37/17/BRNS), IFCPAR (3709-1), UGC-SAP (DRS-II), and INSPIRE Faculty Award (DST) IFA12-LSPA-11 to Raghu Gogada.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Department of Biotechnology and Bioinformatics, School of Life Sciences, University of Hyderabad, Hyderabad, 500046, India

    Raghu Gogada & Prakash-Babu Phanithi

  2. Department of Biochemistry, Osmania University, Hyderabad, 500 007, India

    Raghu Gogada, Surya Satyanarayana Singh, Shanti Kumari Lunavat & Maruthi Mohan Pamarthi

  3. Molecular Biology Division, Bhabha Atomic Research Center, Mumbai, 400 085, India

    Shree Kumar Apte

  4. Water Steam Chemistry Division, Bhabha Atomic Research Center, Mumbai, 400 085, India

    Balaji Vadivelu

  5. Analytical Chemistry Division, Bhabha Atomic Research Center, Mumbai, 400 085, India

    Venkateswaran Gopala

  6. Université Lyon 1, INSA de Lyon, CNRS, UMR5240, Microbiologie, Adaptation et Pathogénie, Université de Lyon, 69621, Villeurbanne, France

    Agnes Rodrigue

Authors
  1. Raghu Gogada
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Surya Satyanarayana Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shanti Kumari Lunavat
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maruthi Mohan Pamarthi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Agnes Rodrigue
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Balaji Vadivelu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Prakash-Babu Phanithi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Venkateswaran Gopala
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Shree Kumar Apte
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Raghu Gogada or Shree Kumar Apte.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gogada, R., Singh, S.S., Lunavat, S.K. et al. 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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-015-6761-4

Keywords

Search

Navigation