Removal of Ni2+ and Cd2+ by Surface Display of Polyhistidine on Bacillus subtilis Spore Using CotE Anchor Protein

Abstract

In this paper, we report removing heavy metal using Bacillus subtilis spore surface display system. We used CotE protein as an anchoring motif because of its high abundance and location in the outer coat layer. And we inserted His12 (double histidine 6 tag) at the C-terminal end of anchoring motif. The proper expression of CotE-His12 fusion protein (22.8 kDa) was confirmed by western blot. We confirmed the surface expression of the CotE-His12 fusion protein using flow cytometry. We tried Ni2+ and Cd2+ adsorption with recombinant spore DB104 (pCotE-His12) and DB104 spore. The amount of adsorbed Ni2+ was 18.2 nmol/mg for DB104 spore and 82.4 nmol/mg for DB104 (pCotE-His12) spore. In the case of Cd2+, the adsorbed amount was 32.6 nmol/mg for DB104 spore and 79.1 nmol/mg for DB104 (pCotE-His12) spore. This means that our spore displayed His12 system can be generally applied for the removal of various kind of heavy metals in the field.

References

  1. 1.

    Hinc, K., S. Ghandili, G. Karbalaee, A. Shali, K. A. Noghabi, E. Ricca, and G. Ahmadian (2010) Efficient binding of nickel ions to recombinant Bacillus subtilis spores. Res. Microbiol. 161: 757–764.

    Article  CAS  PubMed  Google Scholar 

  2. 2.

    He, Z. L., X. E. Yang, and P. J. Stoffella (2005) Trace elements in agroecosystems and impacts on the environment. J. Trace Elem. Med. Biol. 19: 125–140.

    Article  CAS  PubMed  Google Scholar 

  3. 3.

    Ahalya, N., T. Ramachandra, and R. Kanamadi (2003) Biosorption of heavy metals. Res. J. Chem. Environ. 7: 71–79.

    CAS  Google Scholar 

  4. 4.

    Fourest, E. and J. C. Roux (1992) Heavy metal biosorption by fungal mycelial by-products: mechanisms and influence of pH. Appl. Microbiol. Biotechnol. 37: 399–403.

    Article  CAS  Google Scholar 

  5. 5.

    Kratochvil, D. and B. Volesky (1998) Advances in the biosorption of heavy metals. Trends Biotechnol. 16: 291–300.

    Article  CAS  Google Scholar 

  6. 6.

    Kratochvil, D. and B. Volesky (1998) Biosorption of Cu from ferruginous wastewater by algal biomass. Water Res. 32: 2760–2768.

    Article  CAS  Google Scholar 

  7. 7.

    Francisco, J. A., C. F. Earhart, and G. Georgiou (1992) Transport and anchoring of beta-lactamase to the external surface of Escherichia coli. Proc. Natl. Acad. Sci. USA 89: 2713–7.

    Article  CAS  PubMed  Google Scholar 

  8. 8.

    Ueda M. (2016) Establishment of cell surface engineering and its development. Biosci. Biotechnol. Biochem. 80: 1243–53.

    Article  CAS  PubMed  Google Scholar 

  9. 9.

    Boder, E. T. and K. D. Wittrup (1997) Yeast surface display for screening combinatorial polypeptide libraries. Nat. Biotechnol. 15: 553–557.

    Article  CAS  PubMed  Google Scholar 

  10. 10.

    Jung, H. C., J. M. Lebeault, and J.-G. Pan (1998) Surface display of Zymomonas mobilis levansucrase by using the ice-nucleation protein of Pseudomonas syringae. Nat. Biotechnol. 16: 576.

    Article  CAS  PubMed  Google Scholar 

  11. 11.

    Richins, R. D., I. Kaneva, A. Mulchandani, and W. Chen (1997) Biodegradation of organophosphorus pesticides by surface-expressed organophosphorus hydrolase. Nat. Biotechnol. 15: 984.

    Article  CAS  PubMed  Google Scholar 

  12. 12.

    Sousa, C., A. Cebolla, and V. De Lorenzo (1996) Enhanced metalloadsorption of bacterial cells displaying poly-His peptides. Nat. Biotechnol. 14: 1017–20.

    Article  CAS  PubMed  Google Scholar 

  13. 13.

    Georgiou, G., C. Stathopoulos, P. S. Daugherty, A. R. Nayak, B. L. Iverson, and R. Curtiss, 3rd (1997) Display of heterologous proteins on the surface of microorganisms: from the screening of combinatorial libraries to live recombinant vaccines. Nat. Biotechnol. 15: 29–34.

    Article  CAS  PubMed  Google Scholar 

  14. 14.

    Kim, J. H., C. S. Lee, and B. G. Kim (2005) Spore-displayed streptavidin: a live diagnostic tool in biotechnology. Biochem. Biophys. Res. Commun. 331: 210–214.

    Article  CAS  PubMed  Google Scholar 

  15. 15.

    Kim, J. H., C. Roh, C. W. Lee, D. Kyung, S. K. Choi, H. C. Jung, J. G. Pan, and B. G. Kim (2007) Bacterial surface display of GFP (uv) on bacillus subtilis spores. J. Microbiol. Biotechnol. 17: 677–680.

    CAS  PubMed  Google Scholar 

  16. 16.

    Kim, J. H., B. G. Kim, S. K. Choi, H. C. Jung, and J. G. Pan (2009) Method for expression of proteins on spore surface. Journal (Issue).

  17. 17.

    Kim, J. and W. Schumann (2009) Display of proteins on Bacillus subtilis endospores. Cell Mol. Life Sci. 66: 3127–3136.

    Article  CAS  PubMed  Google Scholar 

  18. 18.

    Hwang, B. Y., B. G. Kim, and J. H. Kim (2011) Bacterial surface display of a co-factor containing enzyme, omega-transaminase from Vibrio fluvialis using the Bacillus subtilis spore display system. Biosci. Biotechnol. Biochem. 75: 1862–1865.

    Article  CAS  PubMed  Google Scholar 

  19. 19.

    Hwang, B. Y., J. G. Pan, B. G. Kim, and J. H. Kim (2013) Functional display of active tetrameric β-galactosidase using Bacillus subtilis spore display system. J. Nanosci. Nanotechnol. 13: 2313–2319.

    Article  CAS  PubMed  Google Scholar 

  20. 20.

    Richter, A., W. Kim, J. H. Kim, and W. Schumann (2015) Disulfide bonds of proteins displayed on spores of Bacillus subtilis can occur spontaneously. Curr. Microbiol. 71: 156–161.

    Article  CAS  PubMed  Google Scholar 

  21. 21.

    Hosseini Abari, A., B. G. Kim, S. H. Lee, G. Emtiazi, W. Kim, and J. H. Kim (2016) Surface display of bacterial tyrosinase on spores of Bacillus subtilis using CotE as an anchor protein. J. Basic Microbiol. 56: 1331–1337.

    Article  CAS  PubMed  Google Scholar 

  22. 22.

    Kim, J. (2017) Surface display of lipolytic enzyme, Lipase A and Lipase B of Bacillus subtilis on the Bacillus subtilis spore. Biotechnol. Bioprocess Eng. 22: 462–468.

    Article  CAS  Google Scholar 

  23. 23.

    Chen, H., J. Ullah, and J. Jia (2017) Progress in Bacillus subtilis spore surface display technology towards environment, vaccine development, and biocatalysis. J. Mol. Microbiol. Biotechnol. 27: 159–167.

    Article  CAS  PubMed  Google Scholar 

  24. 24.

    Mckenney, P. T., A. Driks, and P. Eichenberger (2013) The Bacillus subtilis endospore: assembly and functions of the multilayered coat. Nat. Rev. Microbiol. 11: 33–44.

    Article  CAS  PubMed  Google Scholar 

  25. 25.

    Monroe, A. and P. Setlow (2006) Localization of the transglutaminase cross-linking sites in the Bacillus subtilis spore coat protein GerQ. J. Bacteriol. 188: 7609–7616.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Das, K. K., R. C. Reddy, I. B. Bagoji, S. Das, S. Bagali, L. Mullur, J. P. Khodnapur, and M. S. Biradar (2018) Primary concept of nickel toxicity — an overview. J. Basic Clin. Physiol. Pharmacol.

  27. 27.

    Bertin, G. and D. Averbeck (2006) Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). Biochimie 88: 1549–1559.

    Article  CAS  PubMed  Google Scholar 

  28. 28.

    Bae, W., A. Mulchandani, and W. Chen (2002) Cell surface display of synthetic phytochelatins using ice nucleation protein for enhanced heavy metal bioaccumulation. J. Inorg. Biochem. 88: 223–227.

    Article  CAS  PubMed  Google Scholar 

  29. 29.

    Wei, Q., H. Zhang, D. Guo, and S. Ma (2016) Cell surface display of four types of Solanum nigrum metallothionein on Saccharomyces cerevisiae for biosorption of cadmium. J. Microbiol. Biotechnol. 28: 846–853.

    Article  CAS  Google Scholar 

  30. 30.

    Kuroda, K. and M. Ueda (2006) Effective display of metallothionein tandem repeats on the bioadsorption of cadmium ion. Appl. Microbiol. Biotechnol. 70: 458–463.

    Article  CAS  PubMed  Google Scholar 

  31. 31.

    Biondo, R., F. A. Da Silva, E. J. Vicente, J. E. Souza Sarkis, and A. C. Schenberg (2012) Synthetic phytochelatin surface display in Cupriavidus metallidurans CH34 for enhanced metals bioremediation. Environ. Sci. Technol. 46: 8325–8332.

    Article  CAS  PubMed  Google Scholar 

  32. 32.

    Saffar, B., B. Yakhchali, and M. Arbabi (2007) Development of a bacterial surface display of hexahistidine peptide using CS3 pili for bioaccumulation of heavy metals. Curr. Microbiol. 55: 273–277.

    Article  CAS  PubMed  Google Scholar 

  33. 33.

    Xu, Z. and S. Y. Lee (1999) Display of polyhistidine peptides on the Escherichia coli cell surface by using outer membrane protein C as an anchoring motif. Appl. Environ. Microbiol. 65: 5142–5147.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Zheng, L. B. and R. Losick (1990) Cascade regulation of spore coat gene expression in Bacillus subtilis. J. Mol. Biol. 212: 645–660.

    Article  CAS  PubMed  Google Scholar 

  35. 35.

    Driks, A., S. Roels, B. Beall, C. Moran, and R. Losick (1994) Subcellular localization of proteins involved in the assembly of the spore coat of Bacillus subtilis. Genes Dev. 8: 234–244.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgment

This work was supported by the Dong-A University research fund.

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Correspondence to Afrouzossadat Hosseini Abari or Junehyung Kim.

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Kim, W., Kim, D., Back, S. et al. Removal of Ni2+ and Cd2+ by Surface Display of Polyhistidine on Bacillus subtilis Spore Using CotE Anchor Protein. Biotechnol Bioproc E 24, 375–381 (2019). https://doi.org/10.1007/s12257-018-0467-2

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Keyword

  • Bacillus subtilis
  • spore surface display
  • CotE
  • metal adsorption