Skip to main content
Log in

Enhanced cadmium removal by growing Bacillus cereus RC-1 immobilized on different magnetic biochars through simultaneous adsorption and bioaccumulation

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Biosorption of cadmium by growing bacteria immobilized on the three magnetic biochars derived from rice straw (MRSB-pellet), sewage sludge (MSSB-pellet), and chicken manure (MCMB-pellet) was investigated, respectively. Total biosorption capacity of the pellets was tested under varying range of pH, culture time, and initial Cd2+ concentration. The maximum biosorption capacity of 93.02 mg/g was obtained with MRSB-pellet, followed by MSSB-pellet (68.02 mg/g) and MCMB-pellet (63.95 mg/g). The biosorption by these immobilized bacterial pellets was more effective than free bacteria; this enhancement could be the result of simultaneous adsorption and bioaccumulation, mainly resulting from magnetic biochar carrier and active bacteria, respectively. The biosorption process by immobilized pellets was primarily driven by ion exchange and complexation, which jointly contributed 73.56% (MRSB-pellet) to 78.62% (MSSB-pellet) of the total adsorption, while the mechanisms of chemical precipitation and physical adsorption could averagely contribute 6.91% (MSSB-pellet) and 11.24% (MRSB-pellet), respectively. Intracellular accumulation was comparably tiny among these mechanisms accounting for 4.30–5.92% of total biosorption; in turn, it would keep intracellular Cd2+ concentration below a toxic threshold to maintain cell activity. These suggested that magnetic biochar immobilized bacteria, particularly MRSB-pellet, could be used as an effective biosorbent to remove the Cd2+ from the growth medium. This study further deepened our understanding of biosorption process by microorganism immobilized onto magnetic biochar for the metal removal.

Graphical abstract

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
Fig. 8

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article.

References

  • Andrès Y, Thouand G, Boualam M, Mergeay M (2000) Factors influencing the biosorption of gadolinium by micro-organisms and its mobilization from stand. Appl Microbiol Biotechnol 54:262–267

    Google Scholar 

  • Barquilha CER, Cossich ES, Tavares CRG, Silva EA (2017) Biosorption of nickel(II) and copper(II) ions in batch and fixed-bed columns by free and immobilized marine algae Sargassum sp. J Clean Prod 150:58–64

    CAS  Google Scholar 

  • Chojnacka K (2010) Biosorpiton and bioaccumulation—the prospects for practical applications. Environ Int 36:299–307

    CAS  Google Scholar 

  • Cui X, Fang S, Yao Y, Li T, Ni Q, Yang X, He Z (2016) Potential mechanisms of cadmium removal from aqueous solution by Canna indica derived biochar. Sci Total Environ 562:517–525

    CAS  Google Scholar 

  • Demirbas A (2004) Effect of temperature and particle size on bio-char yield from pyrolysis of agricultural residues. J Anal Appl Pyrol 72:243–248

    CAS  Google Scholar 

  • EI-Helow ER, Sabry SA, Amer RM (2000) Cadmium biosorption by a cadmium resistant strain of Bacillus thuringiensis: regulation and optimization cell surface affinity for metal cations. Biometals 13:273–280

    Google Scholar 

  • Gao LY, Deng JH, Huang GF, Li K, Cai KZ, Liu Y, Huang F (2019) Relative distribution of Cd2+ adsorption mechanisms on biochars derived from rice straw and sewage sludge. Bioresour Technol 272:114–122

    CAS  Google Scholar 

  • Godt J, Scheidig F, Grosse-Siestrup C, Esche V, Brandenburg P, Reich A, Groneberg DA (2006) The toxicity of cadmium and resulting hazards for human health. J Occup Med Toxicol 1:22

    Google Scholar 

  • Huang F, Dang Z, Guo CL, Lu GN, Gu RR, Liu HJ, Zhang H (2013) Biosorption of Cd(II) by live and dead cells of Bacillus cereus RC-1 isolated from cadmium-contaminated soil. Colloids Surf B 107:11–18

    CAS  Google Scholar 

  • Huang F, Guo CL, Lu GN, Yi XY, Zhu DL, Dang Z (2014) Bioaccumulation characterization of cadmium by growing Bacillus cereus RC-1 and its mechanism. Chemosphere 109:134–142

    CAS  Google Scholar 

  • Huang F, Gao LL, Wu RR, Wang H, Xiao RB (2020) Qualitative and quantitative characterization of adsorption mechanisms for Cd2+ by silicon-rich biochar. Sci Total Environ 731:139163

    CAS  Google Scholar 

  • Huang F, Li K, Wu RR, Yan YJ, Xiao RB (2020) Insight into the Cd2+ biosorption by viable Bacillus cereus RC-1 immobilized on different biochars: roles of bacterial cell and biochar matrix. J Clean. Prod 272:122743

    CAS  Google Scholar 

  • Huang F, Zhang SM, Wu RR, Zhang L, Wang P, Xiao RB (2021) Magnetic biochars have lower adsorption but higher separation effectiveness for Cd2+ from aqueous solution compared to nonmagnetic biochars. Environ Pollut 275:116485

    CAS  Google Scholar 

  • Hou D, Shen X, Luo Q, He Y, Wang Q, Liu Q (2013) Enhancement of the diesel oil degradation ability of a marine bacterial strain by immobilization on a novel compound carrier material. Marin Pollut Bullet 67:146–151

    CAS  Google Scholar 

  • Khan Z, Rehman A, Hussain SZ (2016) Resistance and uptake of cadmium by yeast, Pichia hampshirensis 4Aer, isolated from industrial effluent and its potential use in decontamination of wastewater. Chemosphere 159:32–43

    CAS  Google Scholar 

  • Letnik I, Avrahami R, Port R, Greiner A, Zussman E, Stefan Rokem J, Greenblatt C (2017) Biosorption of copper from aqueous environments by Micrococcus luteus in cell suspension and when encapsulated. Int Biodeterior Biodegrad 116:64–72

    CAS  Google Scholar 

  • Li X, Dai L, Zhang C, Zeng G, Liu Y, Zhou C, Xu W, Wu Y, Tang X, Lan S (2017) Enhanced biological stabilization of heavy metals in sediment using immobilized sulfate reducing bacteria beads with inner cohesive nutrient. J Hazard Mater 324:340–347

    CAS  Google Scholar 

  • Liu SH, Zeng ZT, Niu QY, Xiao R, Zeng GM, Liu Y, Tao JJ (2019) Influence of immobilization on phenanthrene degradation by Bacillus sp. P1 in the presence of Cd(II). Sci Total Environ 665:1279–1287

    Google Scholar 

  • Luo S, Xia X, Xi Q, Wan Y, Chen L, Zeng G, Liu C, Guo H, Chen J (2011) Enhancement of cadmium bioremediation by endophytic bacterium Bacillus sp. L14 using industrially used metabolic inhibitors (DCC or DNP). J Hazard Mater 190:1079–1082

    CAS  Google Scholar 

  • Ma X, Cui W, Yang L, Yang Y, Chen H, Wang K (2015) Efficient biosorption of lead(II) and cadmium(II) ions from aqueous solutions by functionalized cell with intracellular CaCO3 mineral scaffolds. Bioresour Technol 185:70–78

    CAS  Google Scholar 

  • Mahmoud ME, Abdou AEH, Mohamed SMS, Osman MM (2016) Engineered Staphylococcus aureus via immobilization on magnetic Fe3O4-phthalate nanoparticles for biosorption of divalent ions from aqueous solutions. J Environ Chem Engineer 4:3810–3824

    CAS  Google Scholar 

  • Markou D, Mitrogiannis D, Celekli A, Bozkurt H, Georgakakis D, Chrysikopoulos CV (2015) Biosorption of Cu2+ and Ni2+ by Arthrospira platensis with different biochemical compositions. Chem Eng J 259:806–813

    CAS  Google Scholar 

  • Mohan D, Kumar H, Sarswat A, Alexandrefranco M, Pittman CU (2014) Cadmium and lead remediation using magnetic oak wood and oak bark fast pyrolysis bio-chars. Chem Eng J 236:513–528

    CAS  Google Scholar 

  • Naskar A, Bera D (2018) Mechanistic exploration of Ni(II) removal by immobilized bacterial biomass and interactive influence of coexisting surfactants. Environ Prog Sustain Energy. https://doi.org/10.1002/ep.12685

    Article  Google Scholar 

  • Nasreen A, Muhammad I, Saeed Iqbal A, Javed I (2008) Biosorption characteristics of unicellular green alga Chlorella sorokiniana immobilized in loofa sponge for removal of Cr(III). J Environ Sci 20:231–239

    Google Scholar 

  • Neumann G, Veeranagouda Y, Karegoudar TB, Sahin Ö, Mäusezahl I, Kabelitz N, Kappelmeyer U, Heipieper HJ (2005) Cells of Pseudomonas putida and Enterobacter sp. adapt to toxic organic compounds by increasing the size. Extremophiles 9:163–168

    CAS  Google Scholar 

  • Nithya C, Gnanalakshmi B, Pandian SK (2011) Assessment and characterization of heavy metal resistance in Palk Bay sediment bacteria. Mar Environ Res 71:283–294

    CAS  Google Scholar 

  • Piccirillo C, Pereira SIA, Marques AP, Pullar RC, Tobaldi DN, Pintado ME, Castro PM (2013) Bacteria immobilisation on hydroxyapatite surface for heavy metals removal. J Environ Manage 121:87–95

    CAS  Google Scholar 

  • Robalds A, Naja GM, Klavins M (2016) Highlighting inconsistencies regarding metal biosorption. J Hazard Mater 304:553–556

    CAS  Google Scholar 

  • Sarma SJ, Pakshirajan K (2011) Surfactant aided biodegradation of pyrene using immobilized cells of Mycobacterium frederiksbergense. Int Biodeterior Biodegrad 65:73–77

    CAS  Google Scholar 

  • Shen Y, Li H, Zhu W, Ho SH, Yuan W, Chen J, Xie Y (2017) Microalgal-biochar immobilized complex: a novel efficient biosorbent for cadmium removal from aqueous solution. Bioresour Technol 244:1031–1038

    CAS  Google Scholar 

  • Shen Y, Zhu W, Li H, Ho SH, Chen J, Xie Y, Shi X (2018) Enhancing cadmium bioremediation by a complex of water-hyacinth derived pellets immobilized with Chlorella sp. Bioresour Technol 257:157–163

    CAS  Google Scholar 

  • Sohbatzadeh H, Keshtkar AR, Safdari J, Fatemi F (2017) Insights into the biosorption mechanisms of U(VI) by chitosan bead containing bacterial cells: a supplementary approach using desorption eluents, chemical pretreatment and PIXE-RBS analyses. Chem Eng J 323:492–501

    CAS  Google Scholar 

  • Tsekova K, Todorova D, Dencheva V, Ganeva S (2010) Biosorption of copper(II) and cadmium(II) from aqueous solutions by free and immobilized biomass of Aspergillus niger. Bioresour Technol 101:1727–1731

    CAS  Google Scholar 

  • Uchimiya M, lima IM, Klasson KT, Chang S, Wartelle LH, Rodgers JE (2010) Immobilization of heavy metals ions (CuII, CdII, NiII and PbII) by broiler litter-derived biochars in water and soil. J Agric Food Chem 58:5538–5544

    CAS  Google Scholar 

  • Uchimiya M (2014) Influence of pH, ionic strength, and multidentate ligand on the interaction of CdII with biochars. ACS Sustainable Chem Eng 2:2019–2027

    Google Scholar 

  • Wan S, Wu J, Zhou S, Wang R, Gao B, He F (2018) Enhanced lead and cadmium removal using biochar-supported hydrated manganese oxide (HMO) nanoparticles: behavior and mechanism. Sci Total Environ 616–617:1298–1306

    Google Scholar 

  • Wang RZ, Huang DL, Liu YG, Zhang C, Lai C, Zeng GM, Cheng M, Gong XM, Wan J, Luo H (2018) Investigating the adsorption behavior and the relative distribution of Cd2+ sorption mechanisms on biochars by different feedstock. Bioresour Technol 261:265–271

    CAS  Google Scholar 

  • Wang H, Huang F, Zhao ZL, Wu RR, Xu WX, Wang P, Xiao RB (2021) High-efficiency removal capacities and quantitative adsorption mechanisms of Cd2+ by thermally modified biochars derived from different feedstocks. Chemosphere 272:129594

    CAS  Google Scholar 

  • Wen X, Du C, Zeng G, Huang D, Zhang J, Yin L, Tan S, Huang L, Chen H, Yu G, Hu X, Lai C, Xu P, Wan J (2018) A novel biosorbent prepared by immobilized Bacillus licheniformis for lead removal from wastewater. Chemosphere 200:173–179

    CAS  Google Scholar 

  • Yilmaz EI, Ensari NY (2005) Cadmium biosorption by Bacillus sirculans strain EB1. World J Microbiol Biotechnol 21:777–779

    CAS  Google Scholar 

  • Yu W, Lian F, Gui G, Liu Z (2018) N-doping effectively enhances the adsorption capacity of biochar for heavy metal ions from aqueous solution. Chemosphere 193:8–16

    CAS  Google Scholar 

  • Yuan S, Hong M, Li H, Ye Z, Gong H, Zhang J, Huang Q, Tan Z (2020) Contributions and mechanisms of components in modified biochar to adsorb cadmium in aqueous solution. Sci Total Environ 733:139320

    CAS  Google Scholar 

  • Zamani H, Rakhshaee R, Garakoui SR (2018) Two contrary roles of Fe3O4 nanoparticles on kinetic and thermodynamic of paclitaxel degradation by Citrobacter amalonaticus Rashtia immobilized on sodium alginate gel beads. J Hazard Mater 344:566–575

    CAS  Google Scholar 

  • Zhang K, Liu Y, Luo H, Chen Q, Zhu Z, Chen J, Ji L, Mo Y (2017) Bacterial community dynamics and enhanced degradation of di-n-octyl phthalate (DOP) by corncob-sodium alginate immobilized bacteria. Geoderma 305:264–274

    CAS  Google Scholar 

  • Zhu X, Chen B, Zhu L, Xing B (2017) Effects and mechanisms of biochar-microbe interactions in soil improvement and pollution remediation: a review. Environ Pollut 227:98–115

    CAS  Google Scholar 

  • Zhu L, Tong L, Zhao N, Wang X, Yang X, Lv Y (2020) Key factors and microscopic mechanisms controlling adsorption of cadmium surface oxidized and aminated biochars. J Hazard Mater 382:121002

    CAS  Google Scholar 

Download references

Funding

This research was financially supported by the National Natural Science Foundation of China (No. 42007323), the Shenzhen Science & Technology Project (SZIITWDZC2021A01), the Basic and Applied Research Program of Guangdong Province (2019A1515012187), and the High-level Professionals and Innovative Teams (No. SZIIT2019KJ024; No. SZIIT2019KJ007).

Author information

Authors and Affiliations

Authors

Contributions

Dan Peng conceived and designed the ideas to develop in the article. Min Deng analyzed data and wrote the manuscript with the help of Kai Li providing the experimental sets. Yu-Jian Yan and Fei Huang conducted the SEM–EDS, FTIR, and XRD tests for the biochars studied in this study. All authors contributed to the final version of this manuscript.

Corresponding author

Correspondence to Dan Peng.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Zhihong Xu

Publisher's note

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

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Deng, M., Li, K., Yan, YJ. et al. Enhanced cadmium removal by growing Bacillus cereus RC-1 immobilized on different magnetic biochars through simultaneous adsorption and bioaccumulation. Environ Sci Pollut Res 29, 18495–18507 (2022). https://doi.org/10.1007/s11356-021-17125-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-17125-x

Keywords

Navigation