Skip to main content

Microbial reduction of Cr(VI) in the presence of Ni, Cu and Zn by bacterial consortium enriched from an electroplating contaminated site

Abstract

The bioremediation of Cr(VI) has been intensively reported in recent years, while little information about Cr(VI)-reducing consortium enriched from in-situ contaminated soil has been revealed, specifically the functional genes involved. In this study, we verified a Cr(VI) reduction process by a consortium enriched from in-situ contaminated soil through enzymatic analysis. The chromate reductase gene ChrR has been successfully amplified and further analyzed, provided solid evidence to prove the Cr(VI) bio-reduction was an enzyme-mediated process. Meanwhile, the analysis of metabolic pathways demonstrates that the consortium could detoxicate and resist Cr(VI) and co-existing metals (Ni2+, Zn2+ and Cu2+) through membrane transport and DNA repair process. The co-existing heavy metals Zn and Cu had a relatively significant negative and positive effects on Cr(VI) reduction respectively, which may play important roles in the Cr(VI) contaminated soil bioremediation.

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 data presented in this study are available on request from the corresponding author.

References

  1. Ahemad M (2014) Bacterial mechanisms for Cr(VI) resistance and reduction: an overview and recent advances. Folia Microbiol 59(4):321–332

    CAS  Article  Google Scholar 

  2. An Q, Deng SM, Zhao B, Li Z, Xu J, Song JL (2021) Simultaneous denitrification and hexavalent chromium removal by a newly isolated Stenotrophomonas maltophilia strain W26 under aerobic conditions. Environ Chem 18(1):20–30

    CAS  Article  Google Scholar 

  3. Bhattacharya A, Gupta A (2013) Evaluation of Acinetobacter sp. B9 for Cr (VI) resistance and detoxification with potential application in bioremediation of heavy-metals-rich industrial wastewater. Environ Sci Pollut Res Int 20(9):6628–6637

    CAS  PubMed  Article  Google Scholar 

  4. Chai L, Ding C, Tang C, Yang W, Yang Z, Wang Y, Liao Q, Li J (2018) Discerning three novel chromate reduce and transport genes of highly efficient Pannonibacter phragmitetus BB: from genome to gene and protein. Ecotoxicol Environ Saf 162:139–146

    CAS  PubMed  Article  Google Scholar 

  5. Chaudhari AU, Tapase SR, Markad VL, Kodam KM (2013) Simultaneous decolorization of reactive Orange M2R dye and reduction of chromate by Lysinibacillus sp. KMK-a. J Hazard Mater 262:580–588

    CAS  PubMed  Article  Google Scholar 

  6. Chen R, Luo YH, Chen JX, Zhang Y, Wen LL, Shi LD, Tang Y, Rittmann BE, Zheng P, Zhao HP, Research P (2016) Evolution of the microbial community of the biofilm in a methane-based membrane biofilm reactor reducing multiple electron acceptors. Environ Sci Pollut Res 23(10):9540–9548

    CAS  Article  Google Scholar 

  7. De W, Fu B, Zhao W, Hu H, Wang Y (2008) Multifractal characteristics of soil particle size distribution under different land-use types on the Loess Plateau, China. CATENA 72(1):29–36

    Article  Google Scholar 

  8. Desai C, Jain K, Madamwar D (2008) Evaluation of in vitro Cr(VI) reduction potential in cytosolic extracts of three indigenous Bacillus sp. isolated from Cr(VI) polluted industrial landfill. Bioresour Technol 99(14):6059–6069

    CAS  PubMed  Article  Google Scholar 

  9. Elahi A, Ajaz M, Rehman A, Vuilleumier S, Khan Z, Hussain SZ (2019) Isolation, characterization, and multiple heavy metal-resistant and hexavalent chromium-reducing Microbacterium testaceum B-HS2 from tannery effluent. J King Saud Univ Sci 31(4):1437–1444

    Article  Google Scholar 

  10. Fajardo C, Costa G, Nande M, Botías P, García-Cantalejo J, Martín M (2019) Pb, Cd, and Zn soil contamination: monitoring functional and structural impacts on the microbiome. Appl Soil Ecol 135:56–64

    Article  Google Scholar 

  11. Ge S, Ge SC (2016) Simultaneous Cr(VI) reduction and Zn(II) biosorption by Stenotrophomonas sp. and constitutive expression of related genes. Biotechnol Lett 38(5):877–884

    CAS  PubMed  Article  Google Scholar 

  12. Gong WJ, Niu ZF, Wang XR, Zhao HP (2021) How the soil microbial communities and activities respond to long-term heavy metal contamination in electroplating contaminated site. Microorganisms 9(2):362–373

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. Han H, Ling Z, Zhou T, Xu R, He Y, Liu P, Li X (2017) Copper (II) binding of NAD(P)H- flavin oxidoreductase (NfoR) enhances its Cr (VI)-reducing ability. Sci Rep 7(1):15481–15492

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  14. Hantke K (2005) Bacterial zinc uptake and regulators. Curr Opin Microbiol 8(2):196–202

    CAS  PubMed  Article  Google Scholar 

  15. He Z, Gao F, Sha T, Hu Y, He C (2009) Isolation and characterization of a Cr(VI)-reduction Ochrobactrum sp. strain CSCr-3 from chromium landfill. J Hazard Mater 163(2–3):869–873

    CAS  PubMed  Article  Google Scholar 

  16. He M, Li X, Liu H, Miller SJ, Wang G, Rensing C (2011) Characterization and genomic analysis of a highly chromate resistant and reducing bacterial strain Lysinibacillus fusiformis ZC1. J Hazard Mater 185(2–3):682–688

    CAS  PubMed  Article  Google Scholar 

  17. Heidari P, Mazloomi F, Sanaeizade S (2020) Optimization study of nickel and copper bioremediation by microbacterium oxydans strain CM3 and CM7. Soil Sedim Contam 29(4):438–451

    CAS  Article  Google Scholar 

  18. Henson MW, Santo Domingo JW, Kourtev PS, Jensen RV, Dunn JA, Learman DR (2015) Metabolic and genomic analysis elucidates strain-level variation in Microbacterium spp. isolated from chromate contaminated sediment. PeerJ 3:1395–1411

    Article  CAS  Google Scholar 

  19. Hou D, Wang K, Liu T, Wang H, Lin Z, Qian J, Lu L, Tian S (2017) Unique rhizosphere micro-characteristics facilitate phytoextraction of multiple metals in soil by the hyperaccumulating plant Sedum alfredii. Environ Sci Technol 51(10):5675–5684

    CAS  PubMed  Article  Google Scholar 

  20. Hu P, Brodie EL, Suzuki Y, McAdams HH, Andersen GL (2005) Whole-genome transcriptional analysis of heavy metal stresses in Caulobacter crescentus. J Bacteriol 187(24):8437–8449

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  21. Ibrahim AS, El-Tayeb MA, Elbadawi YB, Al-Salamah AA, Antranikian G (2012) Hexavalent chromate reduction by alkaliphilic Amphibacillus sp. KSUCr3 is mediated by copper-dependent membrane-associated Cr(VI) reductase. Extremophiles 16(4):659–668

    CAS  PubMed  Article  Google Scholar 

  22. Jordao CP, Pereira Mde G, Einloft R, Santana MB, Bellato CR, de Mello JW (2002) Removal of Cu, Cr, Ni, Zn, and Cd from electroplating wastes and synthetic solutions by vermicompost of cattle manure. J Environ Sci Health A 37(5):875–892

    Article  Google Scholar 

  23. Kavita B, Keharia H (2012) Reduction of hexavalent chromium by Ochrobactrum intermedium BCR400 isolated from a chromium-contaminated soil. Biotech 2(1):79–87

    CAS  Google Scholar 

  24. Krishna KR, Philip L (2005) Bioremediation of Cr(VI) in contaminated soils. J Hazard Mater 121(1–3):109–117

    CAS  PubMed  Article  Google Scholar 

  25. Kwak YH, Lee DS, Kim HB (2003) Vibrio harveyi nitroreductase is also a chromate reductase. Appl Environ Microbiol 69(8):4390–4395

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  26. Lai CY, Dong QY, Rittmann BE, Zhao HP (2018) Bioreduction of antimonate by anaerobic methane oxidation in a membrane biofilm batch reactor. Environ Sci Technol 52(15):8693–8700

    CAS  PubMed  Article  Google Scholar 

  27. Lepš J, Šmilauer P (2003) Multivariate analysis of ecological data using CANOCO. Cambridge University Press, Cambridge

    Book  Google Scholar 

  28. Li C, Zhou K, Qin W, Tian C, Qi M, Yan X, Han W (2019a) A review on heavy metals contamination in soil: effects, sources, and remediation techniques. Soil Sedim Contam 28(4):380–394

    Article  CAS  Google Scholar 

  29. Li T, Liu Y, Lin S, Liu Y, Xie Y (2019b) Soil pollution management in china: a brief introduction. Sustainability 11(3):556–570

    Article  Google Scholar 

  30. Liu J, Zhang XH, Tran H, Wang DQ, Zhu YN (2011) Heavy metal contamination and risk assessment in water, paddy soil, and rice around an electroplating plant. Environ Sci Pollut Res Int 18(9):1623–1632

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  31. Lv PL, Shi LD, Wang Z, Rittmann B, Zhao HP (2019) Methane oxidation coupled to perchlorate reduction in a membrane biofilm batch reactor. Sci Total Environ 667:9–15

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  32. Ma L, Xu J, Chen N, Li M, Feng C (2019) Microbial reduction fate of chromium (Cr) in aqueous solution by mixed bacterial consortium. Ecotoxicol Environ Saf 170:763–770

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  33. Megharaj M, Avudainayagam S, Naidu R (2003) Toxicity of hexavalent chromium and its reduction by bacteria isolated from soil contaminated with tannery waste. Curr Microbiol 47(1):51–54

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  34. Mishra S, Chen S, Saratale GD, Saratale RG, Romanholo Ferreira LF, Bilal M, Bharagava RN (2020) Reduction of hexavalent chromium by Microbacterium paraoxydans isolated from tannery wastewater and characterization of its reduced products. J Water Process Eng 39:101748–101758

    Article  Google Scholar 

  35. 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 Res 55:21–29

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  36. Parks DH, Tyson GW, Hugenholtz P, Beiko RG (2014) STAMP: statistical analysis of taxonomic and functional profiles. Bioinformatics 30(21):3123–3124

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  37. Patra RC, Malik S, Beer M, Megharaj M, Naidu R (2010) Molecular characterization of chromium (VI) reducing potential in Gram positive bacteria isolated from contaminated sites. Soil Biol Biochem 42(10):1857–1863

    CAS  Article  Google Scholar 

  38. Qi F, Zhang R, Liu X, Niu Y, Zhang H, Li H, Li J, Wang B, Zhang G (2018) Soil particle size distribution characteristics of different land-use types in the Funiu mountainous region. Soil Tillage Res 184:45–51

    Article  Google Scholar 

  39. Rahman Z, Singh VP (2014) Cr(VI) reduction by Enterobacter sp. DU17 isolated from the tannery waste dump site and characterization of the bacterium and the Cr(VI) reductase. Int Biodeterior Biodegrad 91:97–103

    CAS  Article  Google Scholar 

  40. Ramirez-Diaz MI, Diaz-Perez C, Vargas E, Riveros-Rosas H, Campos-Garcia J, Cervantes C (2008) Mechanisms of bacterial resistance to chromium compounds. Biometals 21(3):321–332

    CAS  PubMed  Article  Google Scholar 

  41. Salamanca D, Strunk N, Engesser KH (2013) Chromate reduction in anaerobic systems by bacterial strain Pseudomonas aeruginosa CRM100. Chem Ing Tech 85(10):1575–1580

    CAS  Google Scholar 

  42. Sangeetha S, Silviya S, Gurunathan J (2012) Hexavalent chromium reduction by metal resistant and halotolerant Planococcus maritimus VITP21. Afr J Microbiol Res 6(47):7339–7349

    Article  CAS  Google Scholar 

  43. Song J, Shen Q, Wang L, Qiu G, Shi J, Xu J, Brookes PC, Liu X (2018) Effects of Cd, Cu, Zn and their combined action on microbial biomass and bacterial community structure. Environ Pollut 243(Pt A):510–518

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  44. Su CQ, Li LQ, Yang ZH, Chai LY, Qi LIAO, Yan SH, Li JW (2019) Cr(VI) reduction in chromium-contaminated soil by indigenous microorganisms under aerobic condition. T Nonferr Met Soc 29(6):1304–1311

    CAS  Article  Google Scholar 

  45. Tan H, Wang C, Zeng G, Luo Y, Li H, Xu H (2020) Bioreduction and biosorption of Cr(VI) by a novel Bacillus sp. CRB-B1 strain. J Hazard Mater 386:121628–121637

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  46. Viti C, Marchi E, Decorosi F, Giovannetti L (2014) Molecular mechanisms of Cr(VI) resistance in bacteria and fungi. FEMS Microbiol Rev 38(4):633–659

    CAS  PubMed  Article  Google Scholar 

  47. Wang Y, Peng B, Yang Z, Chai L, Liao Q, Zhang Z, Li C (2015) Bacterial community dynamics during bioremediation of Cr(VI)-contaminated soil. Appl Soil Ecol 85:50–55

    Article  Google Scholar 

  48. Wang N, Zhang S, He M (2018) Bacterial community profile of contaminated soils in a typical antimony mining site. Environ Sci Pollut Res Int 25(1):141–152

    CAS  PubMed  Article  Google Scholar 

  49. Xiao L, Guan D, Chen Y, Dai J, Ding W, Peart MR, Zhang C (2019) Distribution and availability of heavy metals in soils near electroplating factories. Environ Sci Pollut Res 26(22):22596–22610

    CAS  Article  Google Scholar 

  50. Yan C, Wang F, Geng H, Liu H, Pu S, Tian Z, Chen H, Zhou B, Yuan R, Yao J (2020) Integrating high-throughput sequencing and metagenome analysis to reveal the characteristic and resistance mechanism of microbial community in metal contaminated sediments. Sci Total Environ 707:136116–136117

    CAS  PubMed  Article  Google Scholar 

  51. Yang Y, Wang L, Wendroth O, Liu B, Cheng C, Huang T, Shi Y (2019) Is the laser diffraction method reliable for soil particle size distribution analysis? Soil Sci Soc Am J 83(2):276–287

    CAS  Article  Google Scholar 

  52. Zhang JK, Wang ZH, Ye Y (2016) Heavy metal resistances and chromium removal of a novel Cr(VI)-reducing pseudomonad strain isolated from circulating cooling water of iron and steel plant. Appl Biochem Biotechnol 180(7):1328–1344

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the “National Key Technology R&D Program (2018YFC1802203)”, the “Key Technology R&D Program of Zhejiang Province (2020C03011, 2021C03171)”, and the “National Natural Science Foundation of China (Grant No. 32061133002)” for their financial support.

Funding

National Key Technology R&D Program: 2018YFC1802203. National Natural Science Foundation of China: 51878596, 21577123.

Author information

Affiliations

Authors

Contributions

Conceptualization, HPZ; formal analysis, WJG, XW; investigation, WJG; methodology, WJG; project administration, HPZ; resources, XW; writing—review and editing, HPZ.

Corresponding author

Correspondence to He-Ping Zhao.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

10532_2021_9962_MOESM1_ESM.docx

Supplementary file1 (DOCX 1050 kb). Supplementary Materials: The following are available online at www.mdpi.com/xxx/s1, Figure S1: The reduction of Cr(VI) with different initial Cr(VI) concentrations; Figure S2: PCR carried out with DNA extracted from consortiums with different concentration of Cr(VI) (0, 30, 50, 100, 150, 200, 300) and specific primers. 1-7: amplification with primer ChR; 8: marker; 9-15: amplification with primer NfsA; 16-22: amplification with primer NfsB; Figure S3: PCR carried out with primer ChrR and DNA extracted from consortium without Cr(VI). M: marker, 14: DNA extracted from consortium without Cr(VI). 5: Control group without DNA; Figure S4: The microbial community composition at genus-level of the original consortium under different concentrations of co-existing metals (A), and microbial function annotation by PICRUSt (B, C, D: Microbial function annotation under Cu, Ni and Zn stress); Figure S5: The effect of LB culture and the consortium on the concentration of Ni, Cu and Zn; Figure S6: The abundances of the ChrR gene of the consortium having different concentrations of Ni, Cu and Zn and 50mg/L Cr(VI); Table S1: The particle composition (%) of tested soil sample; Table S2: The DNA fragment amplified by NfsA; Supplement table: The result of genome-wide annotation.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gong, WJ., Wang, XR. & Zhao, HP. Microbial reduction of Cr(VI) in the presence of Ni, Cu and Zn by bacterial consortium enriched from an electroplating contaminated site. Biodegradation 32, 711–722 (2021). https://doi.org/10.1007/s10532-021-09962-x

Download citation

Keywords

  • Cr(VI) contamination
  • Cr(VI) reduction
  • Bacteria consortium
  • Co-existing metals