Skip to main content
Log in

Biofilm-Mediated Heavy Metal Removal from Aqueous System by Multi-Metal-Resistant Bacterial Strain Bacillus sp. GH-s29

  • Original Article
  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

Worldwide ever-augmenting urbanization, modernization, and industrialization have contributed to the release of pernicious compounds and a variety of pollutants into the environment. The pollutants discharged due to industrialization are of global concern. Industrial waste and effluent are comprised of hazardous organic and inorganic chemicals including heavy metals which pose a significant threat to the environment and may bring about numerous diseases or abnormalities in human beings. This brings on greater urgency for remediation of these polluted soil and water using sustainable approaches and mechanisms. In the present research, a multi-metal-resistant, gram-positive, non-virulent bacterial strain Bacillus sp. GH-s29 was isolated from contaminated groundwater of Bhojpur district, Bihar, India. The strain had the potential to develop a biofilm that was able to remediate different heavy metals [arsenic, cadmium, and chromium] from individual and multi-heavy metal solutions. Maximum removal for As (V), Cd (II), and Cr (VI) from individual-metal and the multi-metal solution was observed to be 73.65%, 57.37%, 61.62%, and 48.92%, 28.7%, and 35.46%, respectively. SEM-EDX analysis revealed the sequestration of multi-heavy metals by bacterial biofilm. Further characterization by FTIR analysis ensured that the presence of negatively charged functional groups on the biofilm-EPS such as hydroxyl, phosphate, sulfate, and carboxyl helps in binding to the positively charged metal ions. Thus, Bacillus sp. GH-s29 proved to be an effective and economical alternative for different heavy metal remediation from contaminated sites.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data Availability

All data generated or analyzed during this study are included in this research article (and also its supplementary informatory files).

References

  1. Bose, S., Maity, S., & Sarkar, A. (2022). Nano-materials as biosensor for heavy metal detection. In Food, Medical, and Environmental Applications of Nanomaterials (pp. 493–526). Elsevier. https://doi.org/10.1016/B978-0-12-822858-6.00018-2

    Chapter  Google Scholar 

  2. Bose, S., Maity, S., & Sarkar, A. (2021). Review of microbial biosensor for the detection of mercury in water. Environmental Quality Management. https://doi.org/10.1002/tqem.21742

  3. Maity, S., Biswas, R., & Sarkar, A. (2020a). Comparative valuation of groundwater quality parameters in Bhojpur, Bihar for arsenic risk assessment. Chemosphere, 259, 127398. https://doi.org/10.1016/j.chemosphere.2020.127398

    Article  CAS  PubMed  Google Scholar 

  4. Maity, S., Sinha, D., & Sarkar, A. (2020b). Wastewater and industrial effluent treatment by using nanotechnology. In Nanomaterials and Environmental Biotechnology (pp. 299–313). Springer.

    Chapter  Google Scholar 

  5. Banerjee, S., Mukherjee, S., LaminKa-Ot, A., Joshi, S. R., Mandal, T., & Halder, G. (2016). Biosorptive uptake of Fe2+, Cu2+ and As5+ by activated biochar derived from Colocasia esculenta: isotherm, kinetics, thermodynamics, and cost estimation. Journal of Advanced Research, 7(5), 597–610. https://doi.org/10.1016/j.jare.2016.06.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Maity, S., Biswas, R., Verma, S. K., & Sarkar, A. (2021a). Natural polysaccharides as potential biosorbents for heavy metal removal. In Food, Medical, and Environmental Applications of Polysaccharides (pp. 627–665). Elsevier. https://doi.org/10.1016/B978-0-12-819239-9.00012-9

    Chapter  Google Scholar 

  7. Maity, S., Nanda, S., & Sarkar, A. (2021b). Colocasia esculenta stem as novel biosorbent for potentially toxic metals removal from aqueous system. Environmental Science and Pollution Research, pp., 1–17. https://doi.org/10.1007/s11356-021-13026-1

  8. Maity, S., Patil, P. B., SenSharma, S., & Sarkar, A. (2022). Bioremediation of heavy metals from the aqueous environment using Artocarpus heterophyllus (jackfruit) seed as a novel biosorbent. Chemosphere, 307, 136115. https://doi.org/10.1016/j.chemosphere.2022.136115

    Article  CAS  PubMed  Google Scholar 

  9. Nakkeeran, E., Saranya, N., Giri Nandagopal, M. S., Santhiagu, A., & Selvaraju, N. (2016). Hexavalent chromium removal from aqueous solutions by a novel powder prepared from Colocasia esculenta leaves. International journal of phytoremediation, 18(8), 812–821. https://doi.org/10.1080/15226514.2016.1146229

    Article  CAS  PubMed  Google Scholar 

  10. Rangabhashiyam, S., Nandagopal, M. G., Nakkeeran, E., & Selvaraju, N. (2016). Adsorption of hexavalent chromium from synthetic and electroplating effluent on chemically modified Swietenia mahagoni shell in a packed bed column. Environmental monitoring and assessment, 188(7), 1–13. https://doi.org/10.1007/s10661-016-5415-z

    Article  CAS  Google Scholar 

  11. Rahimzadeh, M. R., Rahimzadeh, M. R., Kazemi, S., & Moghadamnia, A. A. (2017). Cadmium toxicity and treatment: An update. Caspian journal of internal medicine, 8(3), 135. https://doi.org/10.22088/cjim.8.3.135

    Article  Google Scholar 

  12. Rani, A., Kumar, A., Lal, A., & Pant, M. (2014). Cellular mechanisms of cadmium-induced toxicity: a review. International journal of environmental health research, 24(4), 378–399. https://doi.org/10.1080/09603123.2013.835032

    Article  CAS  PubMed  Google Scholar 

  13. Barakat, M. A. (2011). New trends in removing heavy metals from industrial wastewater. Arabian journal of chemistry, 4(4), 361–377. https://doi.org/10.1016/j.arabjc.2010.07.019

    Article  CAS  Google Scholar 

  14. Das, S., & Dash, H. R. (2014). Microbial bioremediation: A potential tool for restoration of contaminated areas. In Microbial biodegradation and bioremediation (pp. 1–21). Elsevier. https://doi.org/10.1016/B978-0-12-800021-2.00001-7

    Chapter  Google Scholar 

  15. Dash, H. R., Mangwani, N., Chakraborty, J., Kumari, S., & Das, S. (2013). Marine bacteria: Potential candidates for enhanced bioremediation. Applied microbiology and biotechnology, 97(2), 561–571. https://doi.org/10.1007/s00253-012-4584-0

    Article  CAS  PubMed  Google Scholar 

  16. Kurniawan, A., & Yamamoto, T. (2013). Biofilm polymer for biosorption of pollutant ions. Procedia Environmental Sciences, 17, 179–187. https://doi.org/10.1016/j.proenv.2013.02.027

    Article  CAS  Google Scholar 

  17. Dash, H. R., Basu, S., & Das, S. (2017). Evidence of mercury trapping in biofilm-EPS and mer operon-based volatilization of inorganic mercury in a marine bacterium Bacillus cereus BW-201B. Archives of microbiology, 199(3), 445–455. https://doi.org/10.1007/s00203-016-1317-2

    Article  CAS  PubMed  Google Scholar 

  18. Sheng, G. P., Yu, H. Q., & Yue, Z. B. (2005). Production of extracellular polymeric substances from Rhodopseudomonas acidophila in the presence of toxic substances. Applied microbiology and biotechnology, 69(2), 216–222. https://doi.org/10.1007/s00253-005-1990-6

    Article  CAS  PubMed  Google Scholar 

  19. Deschatre, M., Ghillebaert, F., Guezennec, J., & Colin, C. S. (2013). Sorption of copper (II) and silver (I) by four bacterial exopolysaccharides. Applied biochemistry and biotechnology, 171(6), 1313–1327. https://doi.org/10.1007/s12010-013-0343-7

    Article  CAS  PubMed  Google Scholar 

  20. Sarkar, D., Poddar, K., Verma, N., Biswas, S., & Sarkar, A. (2020). Bacterial quorum sensing in environmental biotechnology: A new approach for the detection and remediation of emerging pollutants. In Emerging Technologies in Environmental Bioremediation (pp. 151–164). Elsevier. https://doi.org/10.1016/B978-0-12-819860-5.00006-7

    Chapter  Google Scholar 

  21. Mangwani, N., Kumari, S., & Das, S. (2016). Bacterial biofilms and quorum sensing: Fidelity in bioremediation technology. Biotechnology and Genetic Engineering Reviews, 32(1-2), 43–73. https://doi.org/10.1080/02648725.2016.1196554

    Article  CAS  PubMed  Google Scholar 

  22. Völkel, S., Fröls, S., & Pfeifer, F. (2018). Heavy metal ion stress on Halobacterium salinarum R1 planktonic cells and biofilms. Frontiers in microbiology, 9, 3157. https://doi.org/10.3389/fmicb.2018.03157

    Article  PubMed  PubMed Central  Google Scholar 

  23. Gupta, P., & Diwan, B. (2017). Bacterial exopolysaccharide mediated heavy metal removal: A review on biosynthesis, mechanism and remediation strategies. Biotechnology Reports, 13, 58–71. https://doi.org/10.1016/j.btre.2016.12.006

    Article  PubMed  Google Scholar 

  24. Priyadarshanee, M., & Das, S. (2021a). Bioremediation potential of biofilm forming multi-metal resistant marine bacterium Pseudomonas chengduensis PPSS-4 isolated from contaminated site of Paradip Port, Odisha. Journal of Earth System Science, 130(3), 1–17. https://doi.org/10.1007/s12040-021-01627-w

    Article  CAS  Google Scholar 

  25. Sarkar, A., Kazy, S. K., & Sar, P. (2013). Characterization of arsenic resistant bacteria from arsenic rich groundwater of West Bengal, India. Ecotoxicology, 22(2), 363–376. https://doi.org/10.1007/s10646-012-1031-z

    Article  CAS  PubMed  Google Scholar 

  26. Ejiofor, O. S., Ajunwa, O. M., Ezeudu, C. E., Emechebe, G. O., Okeke, K. N., Ifezulike, C. C., Ekejindu, I. M., Okoyeh, J. N., Osuala, E. O., & Oli, A. N. (2018). The bacteriology and its virulence factors in neonatal infections: threats to child survival strategies. Journal of pathogens, 2018. https://doi.org/10.1155/2018/4801247

  27. Preda, M., Mihai, M. M., Popa, L. I., Dițu, L. M., Holban, A. M., Manolescu, L. S. C., Popa, G. L., Muntean, A. A., Gheorghe, I., Chifiriuc, C. M., & Popa, M. I. (2021). Phenotypic and genotypic virulence features of staphylococcal strains isolated from difficult-to-treat skin and soft tissue infections. PLoS One, 16(2), e0246478. https://doi.org/10.1371/journal.pone.0246478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Alessandrello, M. J., Parellada, E. A., Tomás, M. S. J., Neske, A., Vullo, D. L., & Ferrero, M. A. (2017). Polycyclic aromatic hydrocarbons removal by immobilized bacterial cells using annonaceous acetogenins for biofilm formation stimulation on polyurethane foam. Journal of environmental chemical engineering, 5(1), 189–195. https://doi.org/10.1016/j.jece.2016.11.037

    Article  CAS  Google Scholar 

  29. Poddar, K., Sarkar, D., & Sarkar, A. (2019). Construction of potential bacterial consortia for efficient hydrocarbon degradation. International Biodeterioration & Biodegradation, 144, 104770. https://doi.org/10.1016/j.ibiod.2019.104770

    Article  CAS  Google Scholar 

  30. Padhan, B., Poddar, K., Sarkar, D., & Sarkar, A. (2021). Production, purification, and process optimization of intracellular pigment from novel psychrotolerant Paenibacillus sp. BPW19. Biotechnology Reports, 29, p.e00592. https://doi.org/10.1016/j.btre.2021.e00592

  31. Sarkar, D., Gupta, K., Poddar, K., Biswas, R., & Sarkar, A. (2019). Direct conversion of fruit waste to ethanol using marine bacterial strain Citrobacter sp. E4. Process Safety and Environmental Protection, 128, 203–210. https://doi.org/10.1016/j.psep.2019.05.051

    Article  CAS  Google Scholar 

  32. Poddar, K., Padhan, B., Sarkar, D., & Sarkar, A. (2021). Purification and optimization of pink pigment produced by newly isolated bacterial strain Enterobacter sp. PWN1. SN Applied Sciences, 3(1), 1–11. https://doi.org/10.1007/s42452-021-04146-x

    Article  CAS  Google Scholar 

  33. Sarkar, D., Nanda, S., Poddar, K., & Sarkar, A. (2021). Isolation and characterization of an antibacterial compound producing Stenotrophomonas strain from sewage water, production optimization, and its antibiotic potential evaluation. Environmental Quality Management. https://doi.org/10.1002/tqem.21764

  34. Priyadarshanee, M., & Das, S. (2021b). Biosorption and removal of toxic heavy metals by metal tolerating bacteria for bioremediation of metal contamination: A comprehensive review. Journal of Environmental Chemical Engineering, 9(1), 104686. https://doi.org/10.1016/j.jece.2020.104686

    Article  CAS  Google Scholar 

  35. Pakshirajan, K., & Swaminathan, T. (2009). Biosorption of lead, copper, and cadmium by Phanerochaete chrysosporium in ternary metal mixtures: Statistical analysis of individual and interaction effects. Applied biochemistry and biotechnology, 158(2), 457–469. https://doi.org/10.1007/s12010-008-8374-1

    Article  CAS  PubMed  Google Scholar 

  36. Ghosh, D., Bhadury, P., & Routh, J. (2014). Diversity of arsenite oxidizing bacterial communities in arsenic-rich deltaic aquifers in West Bengal, India. Frontiers in microbiology, 5, 602. https://doi.org/10.3389/fmicb.2014.00602

    Article  PubMed  PubMed Central  Google Scholar 

  37. Oremland, R. S., & Stolz, J. F. (2005). Arsenic, microbes and contaminated aquifers. Trends in microbiology, 13(2), 45–49. https://doi.org/10.1016/j.tim.2004.12.002

    Article  CAS  PubMed  Google Scholar 

  38. Fu, H., Chen, F., Liu, W., Kong, W., Wang, C., Fang, X., & Ye, J. (2020). Adding nutrients to the biocontrol strain JK-SH007 promotes biofilm formation and improves resistance to stress. AMB Express, 10(1), 1–13. https://doi.org/10.1186/s13568-019-0929-8

    Article  CAS  Google Scholar 

  39. García, C. F., Kretschmer, M., Lozano-Andrade, C. N., Schönleitner, M., Dragoŝ, A., Kovács, Á. T., & Lieleg, O. (2020). Metal ions weaken the hydrophobicity and antibiotic resistance of Bacillus subtilis NCIB 3610 biofilms. NPJ biofilms and microbiomes, 6(1), 1–11. https://doi.org/10.1038/s41522-019-0111-8

    Article  CAS  Google Scholar 

  40. Fernandez, M., Paulucci, N. S., Reynoso, E., Morales, G. M., Agostini, E., & González, P. S. (2020). Morphological and structural response of Bacillus sp. SFC 500-1E after Cr (VI) and phenol treatment. Journal of basic microbiology, 60(8), 679–690. https://doi.org/10.1002/jobm.202000076

    Article  CAS  PubMed  Google Scholar 

  41. Ayangbenro, A. S., & Babalola, O. O. (2020). Genomic analysis of Bacillus cereus NWUAB01 and its heavy metal removal from polluted soil. Scientific reports, 10(1), 1–12. https://doi.org/10.1038/s41598-020-75170-x

    Article  CAS  Google Scholar 

  42. Sharma, R., Jasrotia, T., Kumar, R., Kumar, R., Umar, A., Alharthi, F. A., Alghamdi, A. A., & Al-Zaqri, N. (2021). An insight into the mechanism of ‘symbiotic-bioremoval’of heavy metal ions from synthetic and industrial samples using bacterial consortium. Environmental Technology & Innovation, 21, 101302. https://doi.org/10.1016/j.eti.2020.101302

    Article  CAS  Google Scholar 

  43. Singh, N., Gupta, S., Marwa, N., Pandey, V., Verma, P. C., Rathaur, S., & Singh, N. (2016). Arsenic mediated modifications in Bacillus aryabhattai and their biotechnological applications for arsenic bioremediation. Chemosphere, 164, 524–534. https://doi.org/10.1016/j.chemosphere.2016.08.119

    Article  CAS  PubMed  Google Scholar 

  44. Ma, H., Wei, M., Wang, Z., Hou, S., Li, X., & Xu, H. (2020). Bioremediation of cadmium polluted soil using a novel cadmium immobilizing plant growth promotion strain Bacillus sp. TZ5 loaded on biochar. Journal of hazardous materials, 388, 122065. https://doi.org/10.1016/j.jhazmat.2020.122065

    Article  CAS  PubMed  Google Scholar 

  45. Li, L., Shang, X., Sun, X., Xiao, X., Xue, J., Gao, Y., & Gao, H. (2021). Bioremediation potential of hexavalent chromium by a novel bacterium Stenotrophomonas acidaminiphila 4-1. Environmental Technology & Innovation, 22, 101409. https://doi.org/10.1016/j.eti.2021.101409

    Article  CAS  Google Scholar 

  46. Chojnacka, K., Chojnacki, A., & Gorecka, H. (2005). Biosorption of Cr3+, Cd2+ and Cu2+ ions by blue–green algae Spirulina sp.: Kinetics, equilibrium and the mechanism of the process. Chemosphere, 59(1), 75–84. https://doi.org/10.1016/j.chemosphere.2004.10.005

    Article  CAS  PubMed  Google Scholar 

  47. Bueno, B. Y. M., Torem, M. L., Molina, F. A. L. M. S., & De Mesquita, L. M. S. (2008). Biosorption of lead (II), chromium (III) and copper (II) by R. opacus: Equilibrium and kinetic studies. Minerals engineering, 21(1), 65–75. https://doi.org/10.1016/j.mineng.2007.08.013

    Article  CAS  Google Scholar 

  48. Pandi, M., Shashirekha, V., & Swamy, M. (2009). Bioabsorption of chromium from retan chrome liquor by cyanobacteria. Microbiological Research, 164(4), 420–428. https://doi.org/10.1016/j.micres.2007.02.009

    Article  CAS  PubMed  Google Scholar 

  49. Saba, Rehman, Y., Ahmed, M. and Sabri, A.N., 2019. Potential role of bacterial extracellular polymeric substances as biosorbent material for arsenic bioremediation. Bioremediation Journal, 23(2), pp.72-81. https://doi.org/10.1080/10889868.2019.1602107

  50. Mohite, B. V., Koli, S. H., & Patil, S. V. (2018). Heavy metal stress and its consequences on exopolysaccharide (EPS)-producing Pantoea agglomerans. Applied biochemistry and biotechnology, 186(1), 199–216. https://doi.org/10.1007/s12010-018-2727-1

    Article  CAS  PubMed  Google Scholar 

  51. Pereira, S., Micheletti, E., Zille, A., Santos, A., Moradas-Ferreira, P., Tamagnini, P., & De Philippis, R. (2011). Using extracellular polymeric substances (EPS)-producing cyanobacteria for the bioremediation of heavy metals: Do cations compete for the EPS functional groups and also accumulate inside the cell. Microbiology, 157(2), 451–458. https://doi.org/10.1099/mic.0.041038-0

    Article  CAS  PubMed  Google Scholar 

  52. Thapa, S., Bharti, A., & Prasanna, R. (2017). Algal biofilms and their biotechnological significance. In Algal green chemistry (pp. 285–303). Elsevier. https://doi.org/10.1016/B978-0-444-63784-0.00014-X

    Chapter  Google Scholar 

  53. Cui, J., Xie, Y., Sun, T., Chen, L., & Zhang, W. (2021). Deciphering and engineering photosynthetic cyanobacteria for heavy metal bioremediation. Science of The Total Environment, 761, 144111. https://doi.org/10.1016/j.scitotenv.2020.144111

    Article  CAS  PubMed  Google Scholar 

  54. Pan, X., Liu, Z., Chen, Z., Cheng, Y., Pan, D., Shao, J., Lin, Z., & Guan, X. (2014). Investigation of Cr (VI) reduction and Cr (III) immobilization mechanism by planktonic cells and biofilms of Bacillus subtilis ATCC-6633. Water research, 55, 21–29. https://doi.org/10.1016/j.watres.2014.01.066

    Article  CAS  PubMed  Google Scholar 

  55. Andreasen, R., Li, Y., Rehman, Y., Ahmed, M., Meyer, R. L., & Sabri, A. N. (2018). Prospective role of indigenous Exiguobacterium profundum PT 2 in arsenic biotransformation and biosorption by planktonic cultures and biofilms. Journal of applied microbiology, 124(2), 431–443. https://doi.org/10.1111/jam.13636

    Article  CAS  PubMed  Google Scholar 

  56. Patel, J., Wilson, G., McKay, R. M. L., Vincent, R., & Xu, Z. (2010). Self-immobilization of recombinant Caulobacter crescentus and its application in removal of cadmium from water. Applied biochemistry and biotechnology, 162(4), 1160–1173. https://doi.org/10.1007/s12010-009-8885-4

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Department of Science and Technology, Government of India for providing financial support to the research work (DST/TM/WTI/2K16/264). We would also like to express our appreciation to the National Institute of Technology Rourkela for providing the infrastructure and instrumental support to proceed with the work.

Funding

This study has been funded by Department of Science and Technology, Government of India (DST/TM/WTI/2K16/264).

Author information

Authors and Affiliations

Authors

Contributions

All authors have contributed to the construction of this manuscript. Sourav Maity: Conceptualization, Data curation, Investigation, Methodology, Writing–original draft. Debapriya Sarkar: Conceptualization, Investigation, Validation, Writing–original draft. Kasturi Poddar: Methodology, Writing–original draft. Pritam Patil: Writing–original draft. Angana Sarkar: Supervision, Project administration. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Angana Sarkar.

Ethics declarations

Ethical Approval

Not applicable.

Consent to Participate

Not applicable.

Consent to Publish

Not applicable.

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.

Additional file

Additional file 1

(DOCX 141 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Maity, S., Sarkar, D., Poddar, K. et al. Biofilm-Mediated Heavy Metal Removal from Aqueous System by Multi-Metal-Resistant Bacterial Strain Bacillus sp. GH-s29. Appl Biochem Biotechnol 195, 4832–4850 (2023). https://doi.org/10.1007/s12010-022-04288-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-022-04288-7

Keywords

Navigation