Skip to main content
SpringerLink
Log in

Mechanism of Cr(VI) reduction by Aspergillus niger: enzymatic characteristic, oxidative stress response, and reduction product

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

Abstract

Bioremediation of hexavalent chromium by Aspergillus niger was attributed to the reduction product (trivalent chromium) that could be removed in precipitation and immobilized inside the fungal cells and on the surface of mycelium. The site location of reduction was conducted with assays of the permeabilized cells, cell-free extracts, and cell debris, which confirmed that the chromate reductase was mainly located in the soluble fraction of cells. The oxidation–reduction process was accompanied by the increase of reactive oxygen species and antioxidant levels after hexavalent chromium treatment. Michaelis–Menten constant (K m) and maximum reaction rate (V max), obtained from the Lineweaver–Burk plot were 14.68 μM and 434 μM min−1 mg−1 of protein, respectively. Scanning electron microscopy and Raman spectra analyses manifested that both Cr(VI) and Cr(III) species were present on the mycelium. Fourier transform-infrared spectroscopy analysis suggested that carboxyl, hydroxide, amine, amide, cyano-group, and phosphate groups from the fungal cell wall were involved in chromium binding by the complexation with the Cr(III) and Cr(VI) species. A Cr(VI) removal mechanism of Cr(VI) reduction followed by the surface immobilization and intracellular accumulation of Cr(III) in living A. niger was present.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

Reference

  • Ackerley DF, Gonzalez CF, Keyhan M, Blake R 2nd, Matin A (2004) Mechanism of chromate reduction by the Escherichia coli protein, NfsA, and the role of different chromate reductases in minimizing oxidative stress during chromate reduction. Environ Microbiol 6:851–860

    Article  CAS  Google Scholar 

  • Aravind P, Prasad M (2005) Cadmium-induced toxicity reversal by zinc in Ceratophyllum demersum L. (a free floating aquatic macrophyte) together with exogenous supplements of amino- and organic acids. Chemosphere 61:1720–1733

    Article  CAS  Google Scholar 

  • Bai RS, Abraham TE (2002) Studies on enhancement of Cr(VI) biosorption by chemically modified biomass of Rhizopus nigricans. Water Res 36:1224–1236

    Article  CAS  Google Scholar 

  • Baptista P, Ferreira S, Soares E, Coelho V, Bastos ML (2009) Tolerance and stress response of Macrolepiota procera to nickel. J Agric Food Chem 57:7145–7152

    Article  CAS  Google Scholar 

  • Camargo F, Okeke B, Bento F, Frankenberger W (2003) In vitro reduction of hexavalent chromium by a cell-free extract of Bacillus sp. ES 29 stimulated by Cu2+. Appl Microbiol Biotechnol 62:569–573

    Article  CAS  Google Scholar 

  • Cheng Y, Yan F, Huang F, Chu W, Pan D, Chen Z, Zheng J, Yu M, Lin Z, Wu Z (2010) Bioremediation of Cr (VI) and immobilization as Cr (III) by Ochrobactrum anthropi. Environ Sci Technol 44:6357–6363

    Article  CAS  Google Scholar 

  • Contreras E, Ferro Orozco A, Zaritzky N (2011) Biological Cr (VI) removal coupled with biomass growth, biomass decay, and multiple substrate limitation. Water Res 45:3034–3046

    Article  CAS  Google Scholar 

  • Dhal B, Thatoi H, Das N, Pandey B (2013) Chemical and microbial remediation of hexavalent chromium from contaminated soil and mining/metallurgical solid waste: a review. J Hazard Mater 250:272–291

    Article  Google Scholar 

  • Dhir B, Sharmila P, Saradhi PP (2004) Hydrophytes lack potential to exhibit cadmium stress induced enhancement in lipid peroxidation and accumulation of proline. Aquat Toxicol 66:141–147

    Article  CAS  Google Scholar 

  • Dong X, Ma LQ, Li Y (2011) Characteristics and mechanisms of hexavalent chromium removal by biochar from sugar beet tailing. J Hazard Mater 190:909–915

    Article  CAS  Google Scholar 

  • Garavaglia L, Cerdeira SB, Vullo DL (2010) Chromium (VI) biotransformation by β-and γ-Proteobacteria from natural polluted environments: a combined biological and chemical treatment for industrial wastes. J Hazard Mater 175:104–110

    Article  CAS  Google Scholar 

  • 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 185:682–688

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Jin W, Zhang Z, Wu G, Tolba R, Chen A (2014) Integrated lignin-mediated adsorption-release process and electrochemical reduction for the removal of trace Cr(VI). RSC Adv 4:27843–27849

    Article  CAS  Google Scholar 

  • Joutey NT, Bahafid W, Sayel H, Ananou S, El Ghachtouli N (2014) Hexavalent chromium removal by a novel Serratia proteamaculans isolated from the bank of Sebou River (Morocco). Environ Sci Pollut R 21:3060–3072

    Article  Google Scholar 

  • Kamaludeen SP, Megharaj M, Juhasz AL, Sethunathan N, Naidu R (2003) Chromium-microorganism interactions in soils: remediation implications, reviews of environmental contamination and toxicology. Springer, pp. 93–164

  • Kapoor A, Viraraghavan T (1997) Heavy metal biosorption sites in Aspergillus niger. Bioresour Technol 61:221–227

    Article  CAS  Google Scholar 

  • Khambhaty Y, Mody K, Basha S, Jha B (2009) Biosorption of Cr (VI) onto marine Aspergillus niger: experimental studies and pseudo-second order kinetics. World J Microbiol Biotechnol 25:1413–1421

    Article  CAS  Google Scholar 

  • Kikuchi S, Kawauchi K, Kurosawa M, Honjho H, Yagishita T (2005) Non-destructive rapid analysis discriminating between chromium (VI) and chromium (III) oxides in electrical and electronic equipment using Raman spectroscopy. Anal Sci 21:197–198

    Article  CAS  Google Scholar 

  • Kılıç NK, Stensballe A, Otzen DE, Dönmez G (2010) Proteomic changes in response to chromium (VI) toxicity in Pseudomonas aeruginosa. Bioresour Technol 101:2134–2140

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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 47:0051–0054

    Article  CAS  Google Scholar 

  • Mohan D, Pittman CU Jr (2006) Activated carbons and low cost adsorbents for remediation of tri- and hexavalent chromium from water. J Hazard Mater 137:762–811

    Article  CAS  Google Scholar 

  • Myers C, Carstens B, Antholine W, Myers J (2000) Chromium (VI) reductase activity is associated with the cytoplasmic membrane of anaerobically grown Shewanella putrefaciens MR‐1. J Appl Microbiol 88:98–106

    Article  CAS  Google Scholar 

  • Park D, Yun YS, Hye Jo J, Park JM (2005a) Mechanism of hexavalent chromium removal by dead fungal biomass of Aspergillus niger. Water Res 39:533–540

    Article  CAS  Google Scholar 

  • Park D, Yun YS, Park JM (2005b) Use of dead fungal biomass for the detoxification of hexavalent chromium: screening and kinetics. Process Biochem 40:2559–2565

    Article  CAS  Google Scholar 

  • Rai V, Khatoon S, Bisht S, Mehrotra S (2005) Effect of cadmium on growth, ultramorphology of leaf and secondary metabolites of Phyllanthus amarus Schum. and Thonn. Chemosphere 61:1644–1650

    Article  CAS  Google Scholar 

  • Ravindranath SP, Henne KL, Thompson DK, Irudayaraj J (2011) Surface-enhanced Raman imaging of intracellular bioreduction of chromate in Shewanella oneidensis. PLoS ONE 6:e16634

    Article  CAS  Google Scholar 

  • Saradhi PP, Mohanty P (1993) Proline in relation to free radical production in seedlings of Brassica juncea raised under sodium chloride stress. Plant Soil 155:497–500

    Google Scholar 

  • Shen Y, Wang S, Tzou Y, Yan Y, Kuan W (2012) Removal of hexavalent Cr by coconut coir and derived chars—the effect of surface functionality. Bioresour Technol 104:165–172

    Article  CAS  Google Scholar 

  • Smutok O, Broda D, Smutok H, Dmytruk K, Gonchar M (2011) Chromate-reducing activity of Hansenula polymorpha recombinant cells over-producing flavocytochrome b 2. Chemosphere 83:449–454

    Article  CAS  Google Scholar 

  • Sultan S, Hasnain S (2007) Reduction of toxic hexavalent chromium by Ochrobactrum intermedium strain SDCr-5 stimulated by heavy metals. Bioresour Technol 98:340–344

    Article  CAS  Google Scholar 

  • Thacker U, Parikh R, Shouche Y, Madamwar D (2007) Reduction of chromate by cell-free extract of Brucella sp. isolated from Cr (VI) contaminated sites. Bioresour Technol 98:1541–1547

    Article  CAS  Google Scholar 

  • Theis T, Wedde M, Meyer V, Stahl U (2003) The antifungal protein from Aspergillus giganteus causes membrane permeabilization. Antimicrob Agents Ch 47:588–593

    Article  CAS  Google Scholar 

  • Vaskova H, Kolomaznik K (2013) Determination of trivalent and hexavalent chromium by Raman spectroscopy, Conference on Raman and Luminescence Spectroscopy in the Earth. Sciences, Austria

    Google Scholar 

  • Xu L, Yang L, Luo M, Liang X, Wei X, Zhao J, Liu H (2011) Reduction of hexavalent chromium by Pannonibacter phragmitetus LSSE-09 coated with polyethylenimine-functionalized magnetic nanoparticles under alkaline conditions. J Hazard Mater 189:787–793

    Article  CAS  Google Scholar 

  • Yee N, Benning LG, Phoenix VR, Ferris FG (2004) Characterization of metal-cyanobacteria sorption reactions: a combined macroscopic and infrared spectroscopic investigation. Environ Sci Technol 38:775–782

    Article  CAS  Google Scholar 

  • Zeng G, Chen A, Chen G, Hu X, Guan S, Shang C, Lu L, Zou Z (2012) Responses of Phanerochaete chrysosporium to toxic pollutants: physiological flux, oxidative stress, and detoxification. Environ Sci Technol 46:7818–7825

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank financial support from the National Natural Science Foundation of China (51108167), Research Fund for Doctoral Program of Higher Education of China (20100161120011), the Hunan Provincial Natural Science Foundation of China (11JJB003), and the Fundamental Research Funds for the Central Universities, Hunan University.

Author information

Authors and Affiliations

  1. College of Environmental Science and Engineering, Hunan University, Changsha, 410082, People’s Republic of China

    Yanling Gu, Weihua Xu, Yunguo Liu, Guangming Zeng, Jinhui Huang, Xiaofei Tan, Hao Jian, Xi Hu, Fei Li & Dafei Wang

  2. Key Laboratory of Environmental Biology and Pollution Control (Hunan University), Ministry of Education, Changsha, 410082, People’s Republic of China

    Yanling Gu, Weihua Xu, Yunguo Liu, Guangming Zeng, Jinhui Huang, Xiaofei Tan, Hao Jian, Xi Hu, Fei Li & Dafei Wang

Authors
  1. Yanling Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Weihua Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yunguo Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guangming Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jinhui Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaofei Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Hao Jian
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xi Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Fei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Dafei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Weihua Xu.

Additional information

Responsible editor: Philippe Garrigues

Highlights:

A systematic mechanism of removal of Cr(VI) by living fungi was presented.

The removal efficiency reached above 80 % for 100 mg L−1 Cr (VI) solutions.

Cr(VI)-induced oxidative stress in Aspergillus niger was concentration-dependent.

Key functional groups and their roles in biosorption were described.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gu, Y., Xu, W., Liu, Y. et al. Mechanism of Cr(VI) reduction by Aspergillus niger: enzymatic characteristic, oxidative stress response, and reduction product. Environ Sci Pollut Res 22, 6271–6279 (2015). https://doi.org/10.1007/s11356-014-3856-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3856-x

Keywords

Search

Navigation