Calcium-crosslinked alginate-encapsulated bacteria for remediating of cadmium-polluted water and production of CdS nanoparticles

Abstract

Pollution with the heavy metal cadmium (Cd2+) is a global problem. Cadmium adversely affects living organisms, highlighting the need to develop new methods for removal of this pollutant from the environment. In this study, we used a novel biomaterial based on calcium-crosslinked alginate-encapsulated bacteria to precipitate Cd2+ in polluted water. Our results show that calcium-crosslinked alginate-encapsulated bacteria effectively removed Cd2+ ions from cadmium-polluted water. Approximately 100% of Cd2+ ions were removed by 10 g (wet weight) of this biomaterial when the loading concentration of Cd2+ reached 1 mM in a volume of 50 ml water. During this process, a CdS nanoparticle, showing good crystallinity in the quantum range, was simultaneously produced. To validate the activity and stability of this biomaterial, we measured cysteine desulfhydrase activity in the stored biomaterial and whether this biomaterial could be recycled. The encapsulated bacteria maintained catalytic activity for at least 2 weeks. The capsules were easily regenerated and possessed good recyclability. Our results indicated that calcium-crosslinked alginate-encapsulated bacteria are suitable for depletion of Cd2+ in polluted water and for production of CdS nanoparticles. These calcium-crosslinked alginate-encapsulated bacteria are safe for biological manipulation and can be widely used to produce CdS nanoparticles during bioremediation of Cd2+-polluted water.

Key points

• Calcium-crosslinked alginate-encapsulated bacteria can effectively precipitate Cd 2+ in water coupled with production of CdS quantum dots.

• The encapsulated bacteria maintained catalytic activity for at least 2 weeks.

• The capsules were easily regenerated and possessed good recyclability.

This is a preview of subscription content, access via your institution.

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

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals--concepts and applications. Chemosphere. 91:869–881. https://doi.org/10.1016/j.chemosphere.2013.01.075

    CAS  Article  PubMed  Google Scholar 

  2. Bao H, Lu Z, Cui X, Qiao Y, Guo J, Anderson JM, Li CM (2010) Extracellular microbial synthesis of biocompatible CdTe quantum dots. Acta Biomater 6:3534–3541. https://doi.org/10.1016/j.actbio.2010.03.030

    CAS  Article  PubMed  Google Scholar 

  3. Chojnacka K (2010) Biosorption and bioaccumulation--the prospects for practical applications. Environ Int 36(3):299–307. https://doi.org/10.1016/j.envint.2009.12.001

    CAS  Article  PubMed  Google Scholar 

  4. Chu L, Ebersole JL, Kurzban GP, Holt SC (1997) Cystalysin, a 46-kilodalton cysteine desulfhydrase from Treponema denticola, with hemolytic and hemoxidative activities. Infect Immun 65(8):3231–3238. https://doi.org/10.1128/IAI.65.8.3231-3238.1997

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  5. Coradin T, Livage J (2007) Aqueous silicates in biological sol-gel applications: new perspectives for old precursors. Acc Chem Res 40(9):819–826. https://doi.org/10.1007/s002530100660

    CAS  Article  PubMed  Google Scholar 

  6. Cunningham DP, Lundie LL (1993) Precipitation of cadmium by Clostridium thermoaceticum. Appl Environ Microbiol 59(1):7–14. https://doi.org/10.1128/AEM.59.1.7-14.1993

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Gallardo C, Monrás JP, Plaza DO, Collao B, Saona LA, Durántoro V, Venegas FA, Soto C, Ulloa G, Vásquez CC (2014) Low-temperature biosynthesis of fluorescent semiconductor nanoparticles (CdS) by oxidative stress resistant Antarctic bacteria. J Biotechnol 187:108–115. https://doi.org/10.1016/j.jbiotec.2014.07.017

    CAS  Article  PubMed  Google Scholar 

  8. Hou Y, Cheng K, Li Z, Ma X, Wei Y, Zhang L, Wang Y (2015) Biosorption of cadmium and manganese using free cells of Klebsiella sp. isolated from waste water. PLoS One 10(10):e0140962. https://doi.org/10.1371/journal.pone.0140962

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Jacob JM, Lens PN, Balakrishnan RM (2016) Microbial synthesis of chalcogenide semiconductor nanoparticles: a review. Microb Biotechnol 9(1):11–21. https://doi.org/10.1111/1751-7915.12297

    CAS  Article  PubMed  Google Scholar 

  10. Kamalian N, Mirhosseini H, Mustafa S, Manap MY (2014) Effect of alginate and chitosan on viability and release behavior of Bifidobacterium pseudocatenulatum G4 in simulated gastrointestinal fluid. Carbohydr Polym 13(111):700–706. https://doi.org/10.1016/j.carbpol.2014.05.014

    CAS  Article  Google Scholar 

  11. Li Y, Cui R, Zhang P, Chen BB, Tian ZQ, Li L, Hu B, Pang DW, Xie ZX (2013) Mechanism-oriented controllability of intracellular quantum dots formation: the role of glutathione metabolic pathway. ACS Nano 7(3):2240–2221. https://doi.org/10.1111/1751-7915.12297

    CAS  Article  PubMed  Google Scholar 

  12. Luo S, Li X, Chen L, Chen J, Wan Y, Liu C (2014) Layer-by-layer strategy for adsorption capacity fattening of endophytic bacterial biomass for highly effective removal of heavy metals. Chem En J 239(1):312–321. https://doi.org/10.1016/j.cej.2013.11.029

    CAS  Article  Google Scholar 

  13. Martelli A, Rousselet E, Dycke C, Bouron A, Moulis JM (2006) Cadmium toxicity in animal cells by interference with essential metals. Biochimie. 88(11):1807–1814. https://doi.org/10.1016/j.biochi.2006.05.013

    CAS  Article  PubMed  Google Scholar 

  14. Masoudzadeh N, Zakeri F, Tb L, Sharafi H, Masoomi F, Zahiri HS, Ahmadian G, Noghabi KA (2011) Biosorption of cadmium by Brevundimonas sp. ZF12 strain, a novel biosorbent isolated from hot-spring waters in high background radiation areas. J Hazard Mater 197(6):190–198. https://doi.org/10.1016/j.jhazmat.2011.09.075

    CAS  Article  PubMed  Google Scholar 

  15. Mosa KA, Saadoun I, Kumar K, Helmy M, Dhankher OP (2016) Potential biotechnological strategies for the clean up of heavy metals and metalloids. Front Plant Sci 7(1035). https://doi.org/10.3389/fpls.2016.00303

  16. Murua A, Portero A, Orive G, Hernández RM, De CM, Pedraz JL (2008) Cell microencapsulation technology: towards clinical application. J Control Release 132(2):76–83. https://doi.org/10.1016/j.jconrel.2008.08.010

    CAS  Article  PubMed  Google Scholar 

  17. Perullini M, Jobbágy M, Mouso N, Forchiassin F, Bilmes SA (2010) Silica-alginate-fungi biocomposites for remediation of polluted water. J Mater Chem 20(31):6479–6483. https://doi.org/10.1039/c0jm01144d

    CAS  Article  Google Scholar 

  18. Perullini M, Amoura M, Jobbágy M, Roux C, Livage J, Coradin T, Bilmes SA (2011) Improving bacteria viability in metal oxide hosts via an alginate-based hybrid approach. J Mater Chem 21(22):8026–8031. https://doi.org/10.1039/c1jm10684h

    CAS  Article  Google Scholar 

  19. Sakimoto KK, Wong AB, Yang P (2016) Self-photosensitization of nonphotosynthetic bacteria for solar-to-chemical production. Science. 351(6268):74–77. https://doi.org/10.1126/science.aad3317

    CAS  Article  PubMed  Google Scholar 

  20. Sanghi R, Verma P (2009) A facile green extracellular biosynthesis of CdS nanoparticles by immobilized fungus. Chem Eng J 155(3):886–891. https://doi.org/10.1016/j.cej.2009.08.006

    CAS  Article  Google Scholar 

  21. Siegel LM (1965) A direct microdetermination for sulfide. Anal Biochem 11(1):126–132. https://doi.org/10.1016/0003-2697(65)90051-5

    CAS  Article  PubMed  Google Scholar 

  22. Vena MP, Jobbágy M, Bilmes SA (2016) Microorganism mediated biosynthesis of metal chalcogenides; a powerful tool to transform toxic effluents into functional nanomaterials. Sci Total Environ 565:804–810. https://doi.org/10.1016/j.scitotenv.2016.04.019

    CAS  Article  PubMed  Google Scholar 

  23. Vinodini NA, Chatterjee PK, Chatterjee P, Chakraborti S, Nayanatara AK, Bhat RM, Rashmi KS, Suman VB, Shetty SB, Pai SR (2015) Protective role of aqueous leaf extract of moringa oleiferaon blood parameters in cadmium exposed adult wistar albino rats. Inter J Curr Res Acad Rev 3:192–199 http://eprints.manipal.edu/id/eprint/141694

    CAS  Google Scholar 

  24. Wang CL, Maratukulam PD, Lum AM, Clark DS, Keasling JD (2000) Metabolic engineering of an aerobic sulfate reduction pathway and its application to precipitation of cadmium on the cell surface. Appl Environ Microbiol 66(10):4497–4502. https://doi.org/10.1128/aem.66.10.4497-4502

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Wang C, Lum A, Ozuna S, Clark D, Keasling J (2001) Aerobic sulfide production and cadmium precipitation by Escherichia coli expressing the Treponema denticola cysteine desulfhydrase gene. Appl Microbiol Biotechnol 56(3-4):425–430

    CAS  Article  Google Scholar 

  26. Xu SZ, Lu XS, Xing YH, Liu S, Huang QY, Chen WL (2019a) Complete genome sequence of Raoultella sp. strain X13, a promising cell factory for the synthesis of CdS quantum dots. 3 Biotech 9:120. https://doi.org/10.1007/s13205-019-1649-0

    Article  PubMed  PubMed Central  Google Scholar 

  27. Xu S, Xing Y, Liu S, Huang QY, Chen WL (2019b) Role of novel bacterial Raoultella sp. strain X13 in plant growth promotion and cadmium bioremediation in soil. Appl Microbiol Biotechnol 103:3887–3897. https://doi.org/10.1007/s00253-019-09700-7

    CAS  Article  PubMed  Google Scholar 

  28. Yang CF, Lee CM (2008) Pentachlorophenol contaminated groundwater bioremediation using immobilized Sphingomonas cells inoculation in the bioreactor system. J Hazard Mater 152:159–165. https://doi.org/10.1016/j.jhazmat.2007.06.102

    CAS  Article  PubMed  Google Scholar 

  29. Yang Z, Lu L, Berard VF, He Q, Kiely C, Berger BW, Mcintosh S (2015) Biomanufacturing of CdS quantum dots. Green Chem 17(7):3775–3782. https://doi.org/10.1039/C5GC00194C

    CAS  Article  Google Scholar 

  30. Yin J, Blanch HW (1989) A biomimetic cadmium adsorbent: design, synthesis, and characterization. Biotechnol Bioeng 34(2):180–188. https://doi.org/10.1002/bit.260340206

    CAS  Article  PubMed  Google Scholar 

Download references

Funding

The research was financially supported by The National Key Research and Development Program of China (2017YFA0605001 and 2016YFD0800206), and the Technical Innovation Major Projects of Hubei Province (2018ABA092).

Author information

Affiliations

Authors

Contributions

S.Z.X. and W.L.C. conceived and designed research. S.Z.X. conducted experiments and wrote the manuscript. S.Z.X. and X.S.L contributed to summarizing and analyzing the data. Q.Y.H. and W.L.C. contributed to editing and revising the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Qiaoyun Huang or Wenli Chen.

Ethics declarations

Ethics approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(PDF 379 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Xu, S., Luo, X., Huang, Q. et al. Calcium-crosslinked alginate-encapsulated bacteria for remediating of cadmium-polluted water and production of CdS nanoparticles. Appl Microbiol Biotechnol 105, 2171–2179 (2021). https://doi.org/10.1007/s00253-021-11155-8

Download citation

Keywords

  • Biomaterial
  • Cadmium
  • Biomineralization
  • CdS nanoparticles