Characteristics of Metabolic Changes and Antioxidative Response in a Potential Zinc Tolerant Fungal Strain, Aspergillus terreus

Research Article
First Online:
Received:
Revised:
Accepted:
  • 122 Downloads

Abstract

Heavy metal pollution is an alarming problem for the ecosystem. Zinc (Zn) is one of the most common heavy metal contaminant in the environment. In recent years different, abatement strategies are being implemented to control metal pollutants, amongst these, bioremediation has gained substantial focus. This paper detailed the Zn uptake and removal efficacies of a Zn tolerant fungal strain, Aspergillus terreus (minimum inhibitory concentration against Zn being 9100 ppm) which was capable of removing 75–35 % Zn from different Zn enriched media. However, the uptake and removal efficacies were found to be decreased with increasing Zn concentrations. FTIR spectra showed involvement of functional groups (present on outer surface of fungal cell wall) in Zn adsorption. Concurrently, Zn decreased the activities of two important metabolic enzymes, CMCase and α-amylase. Scanning electron micrographs clearly demonstrated the structural deformation of fungal hyphae due to Zn exposure. To combat the Zn stress A. terreus upregulated its antioxidative defense system, which is reflected through the significant upregulation of superoxide dismutase and catalase enzyme activities and metal responsive protein (metallothionein) with respect to control.

Keywords

Aspergillus terreus Antioxidative enzymes Metabolic enzymes Metallothionein Zinc 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

Authors are thankful to the UGC-DAE-CSR, Kolkata Centre for providing laboratory facilities and financial support; Dept. of Environmental Science for providing AAS facility; Govt. College of Engineering and Leather Technology, Kolkata (GCELT) for providing spectrophotometer, Dr. Srikanta Chakraborty, USIC, Burdwan University for using SEM and Dr.Prasun Mukherjee, CRNN, Calcutta University for using FTIR facility.

References

  1. 1.
    Bonten LTC, Kroer JG, Groenendijk P, Grift BV (2012) Modeling diffusive Cd and Zn contaminant emissions from soils to surface waters. J Contam Hydrol 138:113–122CrossRefPubMedGoogle Scholar
  2. 2.
    Zenk MH (1996) Heavy metal detoxification in higher plant—a review. Gene 179:21–30CrossRefPubMedGoogle Scholar
  3. 3.
    Wang J, Chen C (2006) Biosorption of heavy metals by Saccharomyces cerevisiae: a review. Biotechnol Adv 24:427–451CrossRefPubMedGoogle Scholar
  4. 4.
    Kuyucak N, Volesky B (1988) Desorption of cobalt-laden algal biosorbent. Biotechnol Bioeng 33:815–822CrossRefGoogle Scholar
  5. 5.
    Gadd GM (1988) Heavy metal and radionuclide by fungi and yeasts. In: Norris PR, Kelly DP (eds) Biohydrometallurgy. A. Rowe, ChippenhamGoogle Scholar
  6. 6.
    Huang C, Huang C, Morehart AL (1990) The removal of copper from dilute aqueous solutions by Saccharomyces cerevisiae. Water Res 24:433–439CrossRefGoogle Scholar
  7. 7.
    Nourbakhsh MY, Sag D, Ozer Z, Aksu T, Caglar A (1994) A comparative study of various biosorbents for removal of chromium (VI) ions from industrial waste waters. Process Biochem 29:1–5CrossRefGoogle Scholar
  8. 8.
    Gadd GM (1993) Tansley review no. 47: interactions of fungi with toxic metals. New Phytol, 124:25 ± 60Google Scholar
  9. 9.
    Tuckwell D, Lavens SE, Birch M (2006) Two families of extracellular phospholipase C genes are present in aspergilla. Mycological Res 110:1140–1151CrossRefGoogle Scholar
  10. 10.
    Pérez J, Muñoz-Dorado J, De la Rubia T, Martínez J (2002) Biodegradation and biological treatments of cellulose, hemicellulose and lignin: an overview. Int Microbiol 5:53–63CrossRefPubMedGoogle Scholar
  11. 11.
    Baldrian P (2003) Interactions of heavy metals with white-rot fungi. Enzym Microb Technol 32:78–91CrossRefGoogle Scholar
  12. 12.
    Hatvani N, Mécs I (2003) Effects of certain heavy metals on the growth, dye decolorization, and enzyme activity of Lentinula edodes. Ecotoxicol Environ Saf 55(2):199–203CrossRefPubMedGoogle Scholar
  13. 13.
    Robles A, Lucas R, Martinez-Cañamero M, Omar NB, Pérez R, Gálvez A (2002) Characterization of lacase activity produced by the Hyphomycete Chalara (Syn. Thie-laviopsis) paradoxa CH32. Enzym Microb Technol 31(4):516–522CrossRefGoogle Scholar
  14. 14.
    Lanfranco L, Bolchi A, Cesale Ros E, Ottonello S, Bonfante P (2002) Differential expression of a metallothionein gene during the presymbiotic versus the symbiotic phase of an arbuscular mycorrhizal fungus. J Plant Physiol 130:58–67CrossRefGoogle Scholar
  15. 15.
    Poli G, Leonarduzzi G, Biasi F, Chiarpotto E (2004) Oxidative stress and cell signalling. Curr Med Chem 11:1163–1182CrossRefPubMedGoogle Scholar
  16. 16.
    Ozmen I, Atamanalp M, Bayir A, Sirkecioğlu AN, Mehtap CM, Cengiz M (2007) The effects of different stressors on antioxidant enzyme actıvıties ın the erythrocyte of rainbow trout (Oncorhynchus mykiss W., 1792). Fresenius Environ Bull 16:922–927Google Scholar
  17. 17.
    Vallino M, Martino E, Boella F, Murat C, Chiapello M, Perotto S (2009) Cu, Zn superoxide dismutase and zinc stress in themetal-tolerant ericoidmycorrhizal fungus Oidio dendronmaius. FEMS Microbiol Lett 293:48–57CrossRefPubMedGoogle Scholar
  18. 18.
    Liu P, Luo L, Guo J, Liu H, Wang B, Deng B, Long CA, Cheng Y (2010) Farnesol induces apoptosis and oxidative stress in the fungal pathogen Penicillium expansum. Mycologia 102(2):311–318CrossRefPubMedGoogle Scholar
  19. 19.
    Thorn C, Raper KB (1945) A manual of the Aspergilli. Williams and Wilkins, BaltimoreGoogle Scholar
  20. 20.
    Srivastava S, Thakur I (2006) Biosorption potency of Aspergillus niger for removal of chromium (VI). Curr Microbiol 53:232–237CrossRefPubMedGoogle Scholar
  21. 21.
    Xu C, Ma F, Zhang X (2009) Lignin degradation and enzyme production by Irpex lacteus CD2 during solid state fermentation of corn stover. J Biosci Bioeng 5:372–375CrossRefGoogle Scholar
  22. 22.
    Denison DA, Koehn RD (1977) Assay of cellulases. Mycologia LXIX:152Google Scholar
  23. 23.
    Bernfield P (1955) In: Colowick S, Kaplan, N.O (eds) Methods of enzymology. Academic Press, New York, 1, 149Google Scholar
  24. 24.
    Kaminskyj SGW, Dahms TES (2008) High spatial resolution surface imaging and analysis of fungal cells using SEM and AFM. Micron 39:349–361CrossRefPubMedGoogle Scholar
  25. 25.
    Mishra A, Malik A (2012) Simultaneous bioaccumulation of multiple metals from electroplating effluent using Aspergillus lentulus. Water Res 46:4991–4998CrossRefPubMedGoogle Scholar
  26. 26.
    Paoletti F, Mpcali A (1990) Determination of superoxide dismutase activity by purely chemical system based on NAD(P)H oxidation. Methods Enzymol 186:209–220CrossRefPubMedGoogle Scholar
  27. 27.
    Aebi H (1984) Catalase in vitro. In: Packer L (ed) Methods in enzymology. Oxygen radicals in biological systems, vol 105. Academic Press, Orlando, pp 121–126Google Scholar
  28. 28.
    Viarengo A, Ponzano E, Dondero F, Fabbri R (1997) A simple spectrometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic Molluscs. Marine Environ Res 44:69–84CrossRefGoogle Scholar
  29. 29.
    Pal SK, Konar SS, Mukherjee A, Das TK (2008) Removal of cadmium ion by cadmium resistant mutant of Aspergillus niger from cadmium contaminated Aqua – environment. Can J Pure Appl Sci 2(2):317–321Google Scholar
  30. 30.
    Pal TK, Bhattacharya S, Basumajumdar A (2010) Cellular distribution of bioaccumulated toxic heavy metals in Aspergillus niger and Rhizopus arrhizus. Int J Pharma Biosci VI(2):1–6Google Scholar
  31. 31.
    Akthar MN, Mohan PM (1995) Bioremediation of toxic metal ions from polluted lake waters and industrial effluents by fungal biosorbent. Curr Sci 69:1028–1030Google Scholar
  32. 32.
    Price MS, Classen JJ, Payne GA (2001) Aspergillus niger absorbs copper and zinc from swine wastewater. Biores Technol 77:41–49CrossRefGoogle Scholar
  33. 33.
    Ozsoy HD (2010) Biosorptive removal of Hg(II) ions by Rhizopus oligosporus produced from corn processing wastewater. Afr J Biotechnol 9(51):8783–8790Google Scholar
  34. 34.
    Rao PR, Bhargavi C (2013) Studies on biosorption of heavy metals using pretreated biomass of fungal species. Int J Chem Chem Eng 3(3):171–180Google Scholar
  35. 35.
    Damodaran D, Balakrishnan RM, Shetty VK (2013) The uptake mechanism of Cd(II), Cr(VI), Cu(II), Pb(II), and Zn(II) by mycelia and fruiting bodies of Galerina vittiformis. Bio Med Res Int 2013:1–11Google Scholar
  36. 36.
    Baldrian P, Valaškova V, Merhautova V, Gabriel J (2005) Degradation of lignocellulose by Pleurotus ostreatus in the presence of copper, manganese, lead and zinc. Res Microbiol 156:670–676CrossRefPubMedGoogle Scholar
  37. 37.
    Baldrian T, Gabriel J (2003) Lignocellulose degradation by Pleurotus ostreatus in the presence of cadmium. FEMS Microbiol Lett 220(2):235–240CrossRefPubMedGoogle Scholar
  38. 38.
    Huang DL, Zeng GM, Jiang XY, Feng CL, Yu HY, Liu HL (2006) Bioremediation of Pb-contaminated soil by incubating with Phanerochaete chrysosporium and straw. J Hazard Mater B134:268–276CrossRefGoogle Scholar
  39. 39.
    Yoo HY, Chang MS, Rho HM (1999) Heavy metal-mediated activation of the rat Cu/Zn superoxide dismutase gene via a metal-responsive element. Mol Genom Genet 262:310–317CrossRefGoogle Scholar
  40. 40.
    Frealle E, Noel C, Viscogliosi E, Camus D, Dei-Cas E, Delhaes L (2005) Manganese superoxide dismutase in pathogenic fungi: an issue with pathophysiological and phylogenetic involvements. FEMS Immunol Med Microbiol 45:411–422CrossRefPubMedGoogle Scholar
  41. 41.
    Azevedo MM, Carvalho A, Pascoal C, Rodrigues F, Cassio F (2007) Responses of antioxidant defenses to Cu and Zn stress in two aquatic fungi. Sci Total Environ 377:233–243CrossRefPubMedGoogle Scholar
  42. 42.
    Abrashev R, Dolashka P, Christova R, Stefanova L, Angelova M (2005) Role of antioxidant enzymes in survival of Aspergillus niger 26 under conditions of temperature stress. J Appl Microbiol 99:902–909CrossRefPubMedGoogle Scholar
  43. 43.
    Cobbett C, Goldsbrough P (2002) Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis. Annu Rev Plant Biol 53:159–182CrossRefPubMedGoogle Scholar
  44. 44.
    Kameo S, Iwahashi H, Kojima Y, Satoh H (2000) Induction of metallothioneins in the heavy metal resistant fungus Beauveria bassiana exposed to copper or cadmium. Analusis 28:382–385CrossRefGoogle Scholar
  45. 45.
    Gonzalez-Guerrero M, Cano C, Azcon-Aguilar C, Ferrol N (2007) GintMT1 encodes a functional metallothionein in Glomus intraradices that responds to oxidative stress. Mycorrhiza 17:327–335CrossRefPubMedGoogle Scholar
  46. 46.
    Tucker SL, Thornton CR, Tasker K, Jacob C, Giles G, Egan M, Talbot NJ (2004) A fungal metallothionein is required for pathogenicity of Magnaporthe grisea. Plant Cell 16:1575–1588CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Jacob C, Courbot M, Brun A, Steinman HM, Jacquot JP, Botton B, Chalot M (2001) Molecular cloning, characterization and regulation by cadmium of a superoxide dismutase from the ectomycorrhizal fungus Paxillus involutus. Eur J Biochem 268:3223–3232CrossRefPubMedGoogle Scholar
  48. 48.
    Ott T, Fritz E, Polle A, Schu A, Schutzendubel A (2002) Characterisation of antioxidative systems in the ectomycorrhiza-building basidiomycete Paxillus involutus (Bartsch) Fr. and its reaction to cadmium. FEMS Microbiol Ecol 42:359–366CrossRefPubMedGoogle Scholar

Copyright information

© The National Academy of Sciences, India 2015

Authors and Affiliations

  1. 1.Department of Environmental ScienceUniversity of KalyaniKalyaniIndia
  2. 2.UGC-DAE, Consortium for Scientific ResearchKolkataIndia

Personalised recommendations