Biosorption of lead phosphates by lead-tolerant bacteria as a mechanism for lead immobilization

Abstract

The study of metal-tolerant bacteria is important for bioremediation of contaminated environments and development of green technologies for material synthesis due to their potential to transform toxic metal ions into less toxic compounds by mechanisms such as reduction, oxidation and/or sequestration. In this study, we report the isolation of seven lead-tolerant bacteria from a metal-contaminated site at Zacatecas, México. The bacteria were identified as members of the Staphylococcus and Bacillus genera by microscopic, biochemical and 16S rDNA analyses. Minimal inhibitory concentration of these isolates was established between 4.5 and 7.0 mM of Pb(NO3)2 in solid and 1.0–4.0 mM of Pb(NO3)2 in liquid media. A quantitative analysis of the lead associated to bacterial biomass in growing cultures, revealed that the percentage of lead associated to biomass was between 1 and 37% in the PbT isolates. A mechanism of complexation/biosorption of lead ions as inorganic phosphates (lead hydroxyapatite and pyromorphite) in bacterial biomass, was determined by Fourier transform infrared spectroscopy and X-ray diffraction analyses. Thus, the ability of the lead-tolerant isolates to transform lead ions into stable and highly insoluble lead minerals make them potentially useful for immobilization of lead in mining waste.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Akpor OB, Muchie M (2010) Remediation of heavy metals in drinking water and wastewater treatment systems: processes and applications. Int J Phys Sci 5(12):1807–1817

    CAS  Google Scholar 

  2. Bai J, Yang X, Du R, Chen Y, Wang S, Qiu R (2014) Biosorption mechanisms involved in immobilization of soil Pb by Bacillus subtilis DBM in a multi-metal-contaminated soil. J Environ Sci 26(10):2056–2064

    Article  Google Scholar 

  3. Batta N, Subudhi S, Lal B, Devi A (2013) Isolation of a lead tolerant novel bacterial species, Achromobacter sp. TL-3: assessment of bioflocculant activity. Indian J Exp Biol 51:1004–1011

    CAS  Google Scholar 

  4. Borremans B, Hobman JL, Provoost A, Brown NL, van Der Lelie D (2001) Cloning and functional analysis of the pbr lead resistance determinant of Ralstonia metallidurans CH34. J Bacteriol 183(19):5651–5658

    CAS  Article  Google Scholar 

  5. Chen B, Liu JN, Wang Z, Dong L, Fan JH, Qu JJ (2011) Remediation of Pb-resistant bacteria to Pb polluted soil. J Environ Prot 2(2):130–141

    CAS  Article  Google Scholar 

  6. Cutting SM, Vander Horn PB (1990) Genetic analysis. In: Harwood CR, Cutting SM (eds) Molecular biological methods for Bacillus. Wiley, Sussex, pp 27–74

    Google Scholar 

  7. Das SK, Guha AK (2007) Biosorption of chromium by Termitomyces clypeatus. Colloids Surf B 60(1):46–54

    CAS  Article  Google Scholar 

  8. Doshi H, Ray A, Kothari IL (2007) Biosorption of cadmium by live and dead Spirulina: IR spectroscopic, kinetics, and SEM studies. Curr Microbiol 54(3):213–218

    CAS  Article  Google Scholar 

  9. Drancourt M, Bollet C, Carlioz A, Martelin R, Gayral JP, Raoult D (2000) 16S ribosomal DNA sequence analysis of a large collection of environmental and clinical unidentifiable bacterial isolates. J Clin Microbiol 38(10):3623–3630

    CAS  Google Scholar 

  10. El-Shanshoury AERR, Elsilk SE, Ateya PS (2013) Uptake of some heavy metals by metal resistant Enterobacter sp. isolate from Egypt. Afr J Microbiol Res 7(23):2875–2884

    CAS  Article  Google Scholar 

  11. Elsilk SE, El-Shanshoury AERR, Ateya PS (2014) Accumulation of some heavy metals by metal resistant avirulent Bacillus anthracis PS2010 isolated from Egypt. Afr J Microbiol Res 8(12):1266–1276

    CAS  Article  Google Scholar 

  12. Gong J, Zhang Z, Bai H, Yang G (2007) Microbiological synthesis of nanophase PbS by Desulfotomaculum sp. Sci China Ser E 50(3):302–307

    CAS  Article  Google Scholar 

  13. Govarthanan M, Lee KJ, Kim JS, Kamala-Kannnan S, Oh BT (2013) Significance of autochthonous Bacillus sp. KK1 on biomineralization of lead in mine tailings. Chemosphere 90(8):2267–2272

    CAS  Article  Google Scholar 

  14. Holt JG, Rieg NR, Sneath PHA, Staley JT, Williams ST (1994) Bergey’s manual of determinative bacteriology, 9th edn. Williams and Wilkins, Maryland

    Google Scholar 

  15. Hookoom M, Puchooa D (2013) Isolation and identification of heavy metals tolerant bacteria from industrial and agricultural areas in Mauritius. Curr Res Microbiol Biotechnol 1(3):119–123

    Google Scholar 

  16. Jarosławiecka A, Piotrowska-Seget Z (2014) Lead resistance in microorganisms. Microbiology 160(1):12–25

    Article  Google Scholar 

  17. Kamika I, Momba MNB (2013) Assesing the resistance and bioremediation ability of selected bacterial and protozoan species of heavy metals in metal-rich industrial wastewater. BMC Microbiol 13:28

    CAS  Article  Google Scholar 

  18. Kandeler E (2007) Physiological and biochemical methods for studying soil biota and their function. In: Paul EA (ed) Soil microbiology, ecology, and biochemistry, 3rd edn. Elsevier, Burlington, pp 53–83

    Google Scholar 

  19. Kim SU, Cheong YH, Seo DC, Hur JS, Heo JS, Cho JS (2007) Characterisation of heavy metal tolerance and biosorption capacity of bacterium strain CPB4 (Bacillus spp.). Water Sci Technol 55(1–2):105–111

    CAS  Article  Google Scholar 

  20. Kneipp J, Lasch P, Baldauf E, Beekes M, Naumann D (2000) Detection of pathological molecular alterations in scrapie-infected hamster brain by Fourier transform infrared (FT-IR) spectroscopy. Biochim Biophys Acta 1501(2):189–199

    CAS  Article  Google Scholar 

  21. Leedjärv A, Ivask A, Virta M (2008) Interplay of different transporters in the mediation of divalent heavy metal resistance in Pseudomonas putida KT2440. J Bacteriol 190(8):2680–2689

    Article  Google Scholar 

  22. Levinson HS, Mahler I (1998) Phosphatase activity and lead resistance in Citrobacter freundii and Staphylococcus aureus. FEMS Microbiol Lett 161(1):135–138

    CAS  Article  Google Scholar 

  23. Levinson HS, Mahler I, Blackwelder P, Hood T (1996) Lead resistance and sensitivity in Staphylococcus aureus. FEMS Microbiol Lett 145(3):421–425

    CAS  Article  Google Scholar 

  24. Loukidou MX, Zouboulis AI, Karapantsios TD, Matis KA (2004) Equilibrium and kinetic modeling of chromium (VI) biosorption by Aeromonas caviae. Colloid Surf A 242(1):93–104

    CAS  Article  Google Scholar 

  25. Mac Faddin JF (1984) Pruebas bioquímicas para la identificación de bacterias de importancia clínica, 2nd edn. Médica Panamericana SA (ed) Williams and Wilkins, Baltimore

    Google Scholar 

  26. Mire CE, Tourjee JA, O’Brien WF, Ramanujachary KV, Hecht GB (2004) Lead precipitation by Vibrio harveyi: evidence for novel quorum-sensing interactions. Appl Environ Microbiol 70(2):855–864

    CAS  Article  Google Scholar 

  27. Mohseni M (2014) Bioremediation activity of Pb(II) resistance Citrobacter sp. MKH2 isolated from heavy metal contaminated sites in Iran. J Sci I R Iran 25(2):105–111

    Google Scholar 

  28. Murthy S, Bali G, Sarangi SK (2014) Effect of lead on growth, protein and biosorption capacity of Bacillus cereus isolated from industrial effluent. J Environ Biol 35(2):407–411

    Google Scholar 

  29. Nichols PD, Henson JM, Guckert JB, Nivens DE, White DC (1985) Fourier transform-infrared spectroscopic methods for microbial ecology: analysis of bacteria, bacteri-polymer mixtures and biofilms. J Microbiol Methods 4(2):79–94

    CAS  Article  Google Scholar 

  30. Pandey S, Saha P, Biswas S, Maiti TK (2011) Characterization of two metal resistant Bacillus strains isolated from slag disposal site at Burnpur, India. J Environ Biol 32:773–779

    CAS  Google Scholar 

  31. Pérez MPJA, García-Ribera R, Quesada T, Aguilera M, Ramos-Cormenzana A, Monteoliva-Sánchez M (2008) Biosorption of heavy metals by the exopolysaccharide produced by Paenibacillus jamilae. World J Microbiol Biotechnol 24:2699–2704

    Article  Google Scholar 

  32. Rensing C, Sun Y, Mitra B, Rosen BP (1998) Pb(II)-translocating P-type ATPases. J Biol Chem 273(49):32614–32617

    CAS  Article  Google Scholar 

  33. Richards JW, Krumholz GD, Chval MS, Tisa LS (2002) Heavy metal resistance patterns of Frankia strains. Appl Environ Microbiol 68(2):923–927

    CAS  Article  Google Scholar 

  34. Roane TM (1999) Lead resistance in two bacterial isolates from heavy metal-contaminated soils. Microbial Ecol 37(3):218–224

    CAS  Article  Google Scholar 

  35. Santos-Santos E, Yarto-Ramírez M, Gavilán-García I, Castro-Díaz J, Gavilán-García A, Rosiles R, Suárez S, López-Villegas T (2006) Analysis of arsenic, lead and mercury in farming areas with mining contaminated soils at Zacatecas, Mexico. J Mex Chem Soc 50(2):57–63

    CAS  Google Scholar 

  36. Singh SK, Tripathi VR, Jain RK, Vikram S, Garg SK (2010) An antibiotic, heavy metal resistant and halotolerant Bacillus cereus SIU1 and its thermoalkaline protease. Microbial Cell Fact 9:59

    Article  Google Scholar 

  37. Socrates G (2004) Infrared and Raman characteristic group frequencies: tables and charts, 3rd edn. Wiley, Chichester

    Google Scholar 

  38. Sparks DL (2005) Toxic metals in the environment: the role of surfaces. Elements 1(4):193–197

    CAS  Article  Google Scholar 

  39. Tchounwou PB, Yedjou CG, Patlolla AK, Sutton DJ (2012) Heavy metals toxicity and the environment. Mol Clin Environ Toxicol 101:133–164

    Article  Google Scholar 

  40. Varghese R, Krishna MP, Babu VA, Hatha AM (2012) Biological removal of lead by Bacillus sp. obtained from metal contaminated industrial area. J Microbiol Biotech Food Sci 2(2):756–770

    CAS  Google Scholar 

  41. Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S Ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2):697–703

    CAS  Article  Google Scholar 

  42. Yilmaz EI (2003) Metal tolerance and biosorption capacity of Bacillus circulans strain EB1. Res Microbiol 154(6):409–415

    CAS  Article  Google Scholar 

  43. Zanardini E, Andreoni V, Borin S, Cappitelli F, Daffonchio D, Talotta P, Cariati F (1997) Lead-resistant microorganisms from red stains of marble of the Certosa of Pavia, Italy and use of nucleic acid-based techniques for their detection. Int Biodeterior Biodegrad 40(2):171–182

    CAS  Article  Google Scholar 

Download references

Acknowledgements

We thanks and appreciate the technical support of the M.D. Beatriz A. Rivera Escoto from Laboratorio Nacional de Investigaciones en Nanociencias y Nanotecnología (LINAN-IPICYT). The authors would like to express their gratitude to Consejo Nacional de Ciencia y Tecnología (CONACyT) for the financial support and scholarship for V.R.S. (Grants LINAN-0271911 and FOMIX-ZAC-2013-C01-202597).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Luz Elena Vidales-Rodríguez.

Ethics declarations

Conflict of interest

All authors declare that they have no conflict of interests

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rodríguez-Sánchez, V., Guzmán-Moreno, J., Rodríguez-González, V. et al. Biosorption of lead phosphates by lead-tolerant bacteria as a mechanism for lead immobilization. World J Microbiol Biotechnol 33, 150 (2017). https://doi.org/10.1007/s11274-017-2314-6

Download citation

Keywords

  • Biosorption
  • Hydroxyapatite
  • Lead phosphates
  • Lead tolerance
  • Pyromorphite