Skip to main content
SpringerLink
Log in

Heavy metal-induced glutathione accumulation and its role in heavy metal detoxification in Phanerochaete chrysosporium

  • Applied microbial and cell physiology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Phanerochaete chrysosporium are known to be vital hyperaccumulation species for heavy metal removal with admirable intracellular bioaccumulation capacity. This study analyzes the heavy metal-induced glutathione (GSH) accumulation and the regulation at the intracellular heavy metal level in P. chrysosporium. P. chrysosporium accumulated high levels of GSH, accompanied with high intracellular concentrations of Pb and Cd. Pb bioaccumulation lead to a narrow range of fluctuation in GSH accumulation (0.72–0.84 μmol), while GSH plummeted under Cd exposure at the maximum value of 0.37 μmol. Good correlations between time-course GSH depletion and Cd bioaccumulation were determined (R 2 > 0.87), while no significant correlations have been found between GSH variation and Pb bioaccumulation (R 2 < 0.38). Significantly, concentration-dependent molar ratios of Pb/GSH ranging from 0.10 to 0.18 were observed, while molar ratios of Cd/GSH were at the scope of 1.53–3.32, confirming the dominant role of GSH in Cd chelation. The study also demonstrated that P. chrysosporium showed considerable hypertolerance to Pb ions, accompanied with demand-driven stimulation in GSH synthesis and unconspicuous generation of reactive oxygen stress. GSH plummeted dramatically response to Cd exposure, due to the strong affinity of GSH to Cd and the involvement of GSH in Cd detoxification mechanism mainly as Cd chelators. Investigations into GSH metabolism and its role in ameliorating metal toxicity can offer important information on the application of the microorganism for wastewater treatment.

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
Fig. 7

Similar content being viewed by others

References

  • Baldrian P, Gabriel J (1997) Effect of heavy metals on the growth of selected wood-rotting basidiomycetes. Folia Microbiol 42(5):521–523

    Article  CAS  Google Scholar 

  • Bertin G, Averbeck D (2006) Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). Biochimie 88(11):1549–1559

    Article  CAS  PubMed  Google Scholar 

  • Brey R, Rosen B, Sorensen E (1980) Cation/proton antiport systems in Escherichia coli. Properties of the potassium/proton antiporter. J Biol Chem 255(1):39–44

    CAS  PubMed  Google Scholar 

  • Bridges CC, Zalups RK (2005) Molecular and ionic mimicry and the transport of toxic metals. Toxicol Appl Pharm 204:274–308

    Article  CAS  Google Scholar 

  • Broda P, Sims PFG, Mason JC (1989) Lignin biodegradation: a molecular biological approach. Essays Biochem 24:82–114

    CAS  PubMed  Google Scholar 

  • Bussche JV, Soares EV (2011) Lead induces oxidative stress and phenotypic markers of apoptosis in Saccharomyces cerevisiae. Appl Microbiol Biotechnol 90(2):679–687

    Article  PubMed  Google Scholar 

  • Casalino E, Sblano C, Calzaretti G, Landriscina C (2006) Acute cadmium intoxication induces alpha-class glutathione S-transferase protein synthesis and enzyme activity in rat liver. Toxicology 217(2–3):240–5

    Article  CAS  PubMed  Google Scholar 

  • Clemens S (2001) Molecular mechanisms of plant metal tolerance and homeostasis. Planta 212(4):475–486

    Article  CAS  PubMed  Google Scholar 

  • Cobbett CS (2000) Phytochelatins and their roles in heavy metal detoxification. Plant Physiol 123(3):825–832

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cohen SP, Hooper D, Wolfson J, Souza K, McMurry L, Levy S (1988) Endogenous active efflux of norfloxacin in susceptible Escherichia coli. Antimicrob Agents Chemother 32(8):1187–1191

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Corticeiro SC, Lima AIG, Figueira EMAP (2006) The importance of glutathione in oxidative status of Rhizobium leguminosarum biovar viciae under Cd exposure. Enzyme Microb Technol 40(1):132–137

    Article  CAS  Google Scholar 

  • Dameron CT, Smith BR, Winge D (1989) Glutathione-coated cadmium-sulfide crystallites in Candida glabrata. J Biol Chem 264(29):17355–17360

    CAS  PubMed  Google Scholar 

  • Das M, Saudagar P, Sundar S, Dubey VK (2013) Miltefosine–unresponsive Leishmania donovani has a greater ability than miltefosine–responsive L. donovani to resist reactive oxygen species. FEBS J 280(19):4807–4815

    Article  CAS  PubMed  Google Scholar 

  • De Vos CR, Vonk MJ, Vooijs R, Schat H (1992) Glutathione depletion due to copper-induced phytochelatin synthesis causes oxidative stress in Silene cucubalus. Plant Physiol 98(3):853–858

    Article  PubMed Central  PubMed  Google Scholar 

  • Dhawale SS, Lane AC, Dhawale SW (1996) Effects of mercury on the white rot fungus Phanerochaete chrysosporium. Bull Environ Contam Toxicol 56:825–832

    Article  CAS  PubMed  Google Scholar 

  • Drążkiewicz M, Skórzyńska-Polit E, Krupa Z (2003) Response of the ascorbate–glutathione cycle to excess copper in Arabidopsis thaliana (L.). Plant Sci 164(2):195–202

    Article  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82:70–77

    Article  CAS  PubMed  Google Scholar 

  • Estrella-Gómez NE, Sauri-Duch E, Zapata-Pérez O, Santamaría JM (2012) Glutathione plays a role in protecting leaves of Salvinia minima from Pb2+ damage associated with changes in the expression of SmGS genes and increased activity of GS. Environ Exp Bot 75:188–194

    Article  Google Scholar 

  • Falih AM (1997) Influence of heavy-metals toxicity on the growth in Phanerochaete chrysosporium. Bioresour Technol 60(1):87–90

    Article  CAS  Google Scholar 

  • Flora S, Mittal M, Mehta A (2008) Heavy metal induced oxidative stress & its possible reversal by chelation therapy. Indian J Med Res 128(4):501

    CAS  PubMed  Google Scholar 

  • Fourest E, Roux JC (1992) Heavy metal biosorption by fungal mycelial by-products: mechanisms and influence of pH. Appl Microbiol Biotechnol 37(3):399–403

    Article  CAS  Google Scholar 

  • Gadd GM (1990) Heavy metal accumulation by bacteria and other microorganisms. Experientia 46(8):834–840

    Article  CAS  Google Scholar 

  • Gutiérrez-Alcalá G, Gotor C, Meyer AJ, Fricker M, Vega JM, Romero LC (2000) Glutathione biosynthesis in Arabidopsis trichome cells. Pro Natl Acad Sci 97(20):11108–11113

    Article  Google Scholar 

  • Herbette S, Taconnat L, Hugouvieux V, Piette L, Magniette M, Cuine S, Auroy P, Richaud P, Forestier C, Bourguignon J (2006) Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 88(11):1751–1765

    Article  CAS  PubMed  Google Scholar 

  • Howlett NG, Avery SV (1997) Induction of lipid peroxidation during heavy metal stress in Saccharomyces cerevisiae and influence of plasma membrane fatty acid unsaturation. Appl Environ Microbiol 63(8):2971–2976

    CAS  PubMed Central  PubMed  Google Scholar 

  • Huang DL, Zeng GM, Feng CL, Hu S, Jiang XY, Tang L, Su FF, Zhang Y, Zeng W, Liu HL (2008) Degradation of lead-contaminated lignocellulosic waste by Phanerochaete chrysosporium and the reduction of lead toxicity. Environ Sci Technol 42(13):4946–4951

    Article  CAS  PubMed  Google Scholar 

  • Huang HW, Cao LX, Wan YX, Zhang RD, Wang WF (2012) Biosorption behavior and mechanism of heavy metals by the fruiting body of jelly fungus (Auricularia polytricha) from aqueous solutions. Appl Microbiol Biotechnol 96(3):829–840

    Article  CAS  PubMed  Google Scholar 

  • Kamei I, Sonoki S, Haraguchi K, Kondo R (2006) Fungal bioconversion of toxic polychlorinated biphenyls by white-rot fungus, Phlebia brevispora. Appl Microbiol Biotechnol 73(4'):932–940

    Article  CAS  PubMed  Google Scholar 

  • Karlovsky P (2011) Biological detoxification of the mycotoxin deoxynivalenol and its use in genetically engineered crops and feed additives. Appl Microbiol Biotechnol 91(3):491–504

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lima AIG, Corticeiro SC, de Almeida Paula Figueira EM (2006) Glutathione-mediated cadmium sequestration in Rhizobium leguminosarum. Enzyme Microb Technol 39(4):763–769

    Article  CAS  Google Scholar 

  • Meister A (1995) Glutathione metabolism. Methods Enzymol 251:3–7

    Article  CAS  PubMed  Google Scholar 

  • Mendoza-Cózatl D, Loza-Tavera H, Hernández-Navarro A, Moreno-Sánchez R (2005) Sulfur assimilation and glutathione metabolism under cadmium stress in yeast, protists and plants. FEMS Microbiol Rev 29(4):653–671

    Article  PubMed  Google Scholar 

  • Mendoza-Cózatl DG, Butko E, Springer F, Torpey JW, Komives EA, Kehr J, Schroeder JI (2008) Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role for thiol-peptides in the long-distance transport of cadmium and the effect of cadmium on iron translocation. Plant J 54(2):249–259

    Article  PubMed Central  PubMed  Google Scholar 

  • Milner MJ, Kochian LV (2008) Investigating heavy-metal hyperaccumulation using Thlaspi caerulescens as a model system. Ann Bot 102(1):3–13

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mishra S, Srivastava S, Tripathi R, Govindarajan R, Kuriakose S, Prasad M (2006) Phytochelatin synthesis and response of antioxidants during cadmium stress in Bacopa monnieri L. Plant Physiol Biochem 44(1):25–37

    Article  CAS  PubMed  Google Scholar 

  • Mutoh N, Hayashi Y (1988) Isolation of mutants of Schizosaccharomyces pombe unable to synthesize cadystin, small cadmium-binding peptides. Biochem Biophys Res Commun 151(1):32–39

    Article  CAS  PubMed  Google Scholar 

  • Pauling L (1988) General chemistry, 3rd edn. Dover, New York

    Google Scholar 

  • Perrin D, Watt AE (1971) Complex formation of zinc and cadmium with glutathione. BBA Gen Subj 230(1):96–104

    Article  CAS  Google Scholar 

  • Pointing S (2001) Feasibility of bioremediation by white-rot fungi. Appl Microbiol Biotechnol 57(1–2):20–33

    CAS  PubMed  Google Scholar 

  • Price N, Morel F (1990) Cadmium and cobalt substitution for zinc in a marine diatom. Nature 344(6267):658–660

    Article  CAS  Google Scholar 

  • Schützendübe A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    Article  Google Scholar 

  • Srivastava S, Mishra S, Tripathi RD, Dwivedi S, Gupta DK (2006) Copper-induced oxidative stress and responses of antioxidants and phytochelatins in Hydrilla verticillata (Lf) Royle. Aquat Toxicol 80(4):405–415

    Article  CAS  PubMed  Google Scholar 

  • Sun Q, Ye ZH, Wang XR, Wong MH (2007) Cadmium hyperaccumulation leads to an increase of glutathione rather than phytochelatins in the cadmium hyperaccumulator Sedum alfredii. J Plant Physiol 164(11):1489–1498

    Article  CAS  PubMed  Google Scholar 

  • Tsezos M, Volesky B (1982) The mechanism of uranium biosorption by Rhizopus arrhizus. Biotechnol Bioeng 24:385–401

    Article  CAS  PubMed  Google Scholar 

  • Vögeli-Lange R, Wagner GJ (1996) Relationship between cadmium, glutathione and cadmium-binding peptides (phytochelatins) in leaves of intact tobacco seedlings. Plant Sci 114(1):11–18

    Article  Google Scholar 

  • Vatamaniuk OK, Mari S, Lu YP, Rea PA (2000) Mechanism of heavy metal ion activation of phytochelatin (PC) synthase: blocked thiols are sufficient for PC synthase-catalyzed transpeptidation of glutathione and related thiol peptides. J Biol Chem 275:31451–31459

    Article  CAS  PubMed  Google Scholar 

  • Williams LE, Pittman JK, Hall J (2000) Emerging mechanisms for heavy metal transport in plants. BBA Biomembr 1465(1):104–126

    Article  CAS  Google Scholar 

  • Wu Y, Xiao X, Xu C, Cao D, Du D (2013) Decolorization and detoxification of a sulfonated triphenylmethane dye aniline blue by Shewanella oneidensis MR-1 under anaerobic conditions. Appl Microbiol Biotechnol 97(16):7439–7446

    Article  CAS  PubMed  Google Scholar 

  • Xiang CB, Oliver DJ (1998) Glutathione metabolic genes coordinately respond to heavy metals and jasmonic acid in Arabidopsis. Plant Cell 10(9):1539–1550

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Xu P, Zeng G, Huang D, Hu S, Feng C, Lai C, Zhao M, Huang C, Li N, Wei Z (2013) Synthesis of iron oxide nanoparticles and their application in Phanerochaete chrysosporium immobilization for Pb(II) removal. Colloids Surf A 419:147–155

    Article  CAS  Google Scholar 

  • Xu P, Zeng GM, Huang DL, Feng CL, Hu S, Zhao MH, Lai C, Wei Z, Huang C, Xie GX (2012a) Use of iron oxide nanomaterials in wastewater treatment: a review. Sci Total Environ 424:1–10

    Article  CAS  PubMed  Google Scholar 

  • Xu P, Zeng GM, Huang DL, Lai C, Zhao MH, Wei Z, Li NJ, Huang C, Xie GX (2012b) Adsorption of Pb(II) by iron oxide nanoparticles immobilized Phanerochaete chrysosporium: equilibrium, kinetic, thermodynamic and mechanisms analysis. Chem Eng J 203:423–431

    Article  CAS  Google Scholar 

  • Zeng GM, Chen M, Zeng ZT (2013) Risks of neonicotinoid pesticides. Science 340:1403

    Article  CAS  PubMed  Google Scholar 

  • Zeng GM, Huang DL, Huang GH, Hu TJ, Jiang XY, Feng CL, Chen Y, Tang L, Liu HL (2007) Composting of lead-contaminated solid waste with inocula of white-rot fungus. Bioresour Technol 98(2):320–326

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The study was financially supported by the National Natural Science Foundation of China (51378190, 51039001, 51278176), the Hunan Provincial Innovation Foundation For Postgraduate (CX2012B137, CX2013B152), the Program for New Century Excellent Talents in University (NCET-13-0186), Zhejiang Provincial Key Laboratory of solid Waste Treatment and Recycling open fun (SWTR-2012-07), Shanghai Tongji Gao Tingyao Environmental Science & Technology Development Foundation (STGEF), and the Young Teacher Growth Program of Hunan University and the New Century Excellent Talents in University (NCET − 08 − 0181).

Author information

Authors and Affiliations

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

    Piao Xu, Liang Liu, Guangming Zeng, Danlian Huang, Cui Lai, Meihua Zhao, Chao Huang, Ningjie Li, Zhen Wei, Haipeng Wu, Chen Zhang, Mingyong Lai & Yibin He

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

    Piao Xu, Liang Liu, Guangming Zeng, Danlian Huang, Cui Lai, Meihua Zhao, Chao Huang, Ningjie Li, Zhen Wei, Haipeng Wu, Chen Zhang, Mingyong Lai & Yibin He

Authors
  1. Piao Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Liang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Guangming Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Danlian Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Cui Lai
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Meihua Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Chao Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ningjie Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zhen Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Haipeng Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Chen Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Mingyong Lai
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Yibin He
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Guangming Zeng or Danlian Huang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xu, P., Liu, L., Zeng, G. et al. Heavy metal-induced glutathione accumulation and its role in heavy metal detoxification in Phanerochaete chrysosporium . Appl Microbiol Biotechnol 98, 6409–6418 (2014). https://doi.org/10.1007/s00253-014-5667-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-014-5667-x

Keywords

Search

Navigation