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Effect of copper−induced oxidative stress on sclerotial differentiation, endogenous antioxidant contents, and antioxidative enzyme activities of Penicillium thomii PT95

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Abstract

Penicillium thomii PT95 strain is able to form abundant orange, sand-shaped sclerotia in which carotenoids accumulate. We have studied the effects of copper (Cu)-induced oxidative stress on sclerotial differentiation, biosynthesis of some endogenous antioxidants, and activities of a number of the antioxidative enzymes of strain PT95. The association between sclerotial biomass, carotenoid, ascorbate and glutathione contents, and the activities of superoxide dismutase (SOD), catalase (CAT), ascorbate peroxidase (APX), and glutathione reductases (GR) were also analyzed in this fungal strain. We found that the oxidative stress induced by Cu was directly dependent on the concentrations of CuSO4 in the media, with higher CuSO4 concentrations resulting in higher oxidative stress. Cu-induced oxidative stress in strain PT95 was characterized by the initiation of lipid peroxidation. Under Cu-induced oxidative stress growth conditions, the initiation of exudates and sclerotia in strain PT95, as well as sclerotial maturation, were advanced by 1−2 days. Cu-induced oxidative stress favored sclerotial differentiation and the biosynthesis of endogenous antioxidants, i.e., carotenoids, ascorbate, and glutathione. Comparison of SOD, CAT, and GR activities at 0 and 100 μg/ml Cu revealed a 1.1-, 1.8-, and 1.2-fold increase, respectively, at the higher Cu concentration; comparison of their activities at 100 and 300 μg/ml Cu revealed a 1.4-, 3.1-, and 2.2-fold decrease, respectively, at the higher Cu concentration. APX activity decreased linearly with increasing CuSO4 concentration. Our results suggest that the ability of the P. thomii PT95 strain to cope with metal stress is related to its ability to trigger an efficient defense against oxidative stress. These findings may contribute to a better understanding of the response mechanisms of sclerotia production in Penicillium strains to metal stress and to better insights into metal–fungi interactions in natural environments.

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References

  • Asada K (1992) Ascorbate peroxidase: a hydrogen peroxide-scavenging enzyme in plants. Physiol Plant 85:235–241

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bai Z, Harvey LM, McNeil B (2003) Oxidative stress in submerged cultures of fungi. Crit Rev Biotechnol 23:267–302

    Article  CAS  PubMed  Google Scholar 

  • Baldrian P (2003) Interactions of heavy metals with white–rot fungi. Enzyme Microb Technol 32:78–91

    Article  CAS  Google Scholar 

  • Blaudez D, Botton B, Chalot M (2000) Cadmium uptake and subcellular compartmentation in the ectomycorrhizal fungus Paxillus involutus. Microbiology 146:1109–1117

    CAS  PubMed  Google Scholar 

  • Borkow G, Gabbay J (2005) Copper as a biocidal tool. Curr Med Chem 12(18):2163–2175

    Article  CAS  PubMed  Google Scholar 

  • Boscolo PRS, Menossi M, Jorge RA (2003) Aluminum induced oxidative stress in maize. Phytochemistry 62:181–189

    Article  CAS  PubMed  Google Scholar 

  • Brady D, Glaum D, Duncan JR (1994) Copper tolerance in Saccharomyces cerevisiae. Lett Appl Microbiol 18:245–250

    Article  CAS  Google Scholar 

  • Burton WG, Ingold UK (1984) β-carotene: an unusual type of lipid antioxidant. Science 224(4649):569–573

    Article  CAS  PubMed  Google Scholar 

  • Chillappagari S, Seubert A, Trip H, Kuipers OP, Marahiel MA, Miethke M (2010) Copper stress affects iron homeostasis by destabilizing iron–sulfur cluster formation in Bacillus subtilis. J Bacteriol 192(10):2512–2524

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dávila Costa JS, Albarracín VH, Abate CM (2011) Responses of environmental Amycolatopsis strains to copper stress. Ecotoxicol Environ Saf 74(7):2020–2028

    Article  PubMed  Google Scholar 

  • Dupont CL, Grass G, Rensing C (2011) Copper toxicity and the origin of bacterial resistance—new insights and applications. Metallomics 3(11):1109–1118

    Article  CAS  PubMed  Google Scholar 

  • Elleuch A, Chaâbene Z, Grubb Douglas C, Drira N, Mejdoub H, Khemakhem B (2013) Morphological and biochemical behavior of fenugreek (Trigonella foenumgraecum) under copper stress. Ecotoxicol Environ Saf 98:46–53

    Article  CAS  PubMed  Google Scholar 

  • Esterbauer H, Schaur JR, Zollner H (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonadehyde and related aldehydes. Free Radic Biol Med 11(1):81–128

    Article  CAS  PubMed  Google Scholar 

  • Fatima RA, Ahmad M (2005) Certain antioxidant enzymes of Allium cepa as biomarkers for the detection of toxic heavy metals in waste water. Sci Total Environ 346:256–273

    Article  CAS  PubMed  Google Scholar 

  • Fujs S, Gazdag Z, Poljšak B, Stibilj V, Milačič R, Pesti M (2005) The oxidative stress response of the yeast Candida intermedia to copper, zinc, and selenium exposure. J Basic Microbiol 45:125–135

  • Gadd GM (1993) Interactions of fungi with toxic metals. New Phytol 124:25–60

    Article  CAS  Google Scholar 

  • Georgiou CD (1997) Lipid peroxidation in Sclerotium rolfsii: a new look into the mechanism of sclerotial biogenesis in fungi. Mycol Res 101(4):460–464

    Article  CAS  Google Scholar 

  • Georgiou CD, Petropoulou KP (2001a) Role of erythroascorbate and ascorbate in sclerotial differentiation in Sclerotinia sclerotiorum. Mycol Res 105(11):1364–1370

    Article  CAS  Google Scholar 

  • Georgiou CD, Petropoulou KP (2001b) The role of ascorbic acid in the differentiation of sclerotia in Sclerotinia minor. Mycopathologia 154(2):71–77

    Article  Google Scholar 

  • Georgiou CD, Petropoulou KP (2001c) Effect of the antioxidant ascorbic acid on sclerotial differentiation in Rhizoctonia solani. Plant Pathol 50(5):594–600

    Article  CAS  Google Scholar 

  • Georgiou CD, Tairis N, Polycratis A (2001a) Production of β-carotene by Sclerotinia sclerotiorum and its role in sclerotium differentiation. Mycol Res 105(9):1110–1115

    Article  CAS  Google Scholar 

  • Georgiou CD, Zervoudakis G, Tairis N, Kornaros M (2001b) β-Carotene production and its role in sclerotial differentiation of Sclerotium rolfsii. Fungal Genet Biol 34(1):11–20

    Article  CAS  PubMed  Google Scholar 

  • Georgiou CD, Zervoudakis G, Petropoulou PK (2003) Ascorbic acid might play a role in sclerotial differentiation of Sclerotium rolfsii. Mycologia 95(2):308–316

    Article  CAS  PubMed  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. occurrence in higher plants. Plant Physiol 59(2):309–314

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gokhale NH, Cowan JA (2005) Inactivation of human angiotensin converting enzyme by copper peptide complexes containing ATCUN motifs. Chem Commun (Camb) 47(47):5916–5918

    Article  Google Scholar 

  • Gratão PL, Polle A, Lea PJ, Azevedo RA (2005) Making the life of heavy metal- stressed plants a little easier. Funct Plant Biol 32:481–494

    Article  Google Scholar 

  • Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106:207–212

    Article  CAS  PubMed  Google Scholar 

  • Guillén Y, Machuca Á (2008) The effect of copper on the growth of wood–rotting fungi and a blue–stain fungus. World J Microbiol Biotechnol 24(1):31–37

    Article  Google Scholar 

  • Han JR (1998) Sclerotia growth and carotenoid production of Penicillium sp. PT95 during solid-state fermentation of corn meal. Biotechnol Lett 20(11):1063–1065

    Article  CAS  Google Scholar 

  • Han JR, Wang XJ, Yuan XE (1998) Studies on the production of carotenoids in sclerotia of PT95 strain of Penicillium. Microbiology 25(6):319–321 (In Chinese)

    CAS  Google Scholar 

  • Han JR, Zhao WJ, Gao YY, Yuan JM (2005) Effect of oxidative stress and exogenous β-carotene on sclerotial differentiation and carotenoid yield of Penicillium sp. PT95. Lett Appl Microbiol 40(6):412–417

    Article  CAS  PubMed  Google Scholar 

  • Hayashi Y, Mutoh N (1994a) Cadystin (phytochelatin) in fungi. In: Winkelmann G, Winge DR (eds) Metal ions in fungi. Marcel Dekker, New York, pp 339–359

    Google Scholar 

  • Hayashi Y, Mutoh N (1994b) Cadystin (phytochelatin) in fungi. In: Winkelmann G, Winge DR (eds) Metal ions in fungi. Marcel Dekker, New York, pp 311–337

    Google Scholar 

  • Hodges MD, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207(4):604–611

    Article  CAS  Google Scholar 

  • Jamieson DJ (1998) Oxidative stress responses of the yeast Saccharomyces cerevisiae. Yeast 14:1511–1527

    Article  CAS  PubMed  Google Scholar 

  • Joho M, Inouhe M, Tohoyama H, Murayama T (1995) Nickel resistance mechanisms in yeasts and other fungi. J Ind Microbiol 14:164–168

    Article  CAS  PubMed  Google Scholar 

  • Krumova EZ, Pashova SB, Dolashka–Angelova PA, Stefanova T, Angelova MB (2009) Biomarkers of oxidative stress in the fungal strain Humicola lutea under copper exposure. Process Biochem 44(3):288–295

    Article  CAS  Google Scholar 

  • Krumova ET, Stoitsova SR, Paunova-Krasteva TS, Pashova SB, Angelova MB (2012) Copper stress and filamentous fungus Humicola lutea 103—ultrastructural changes and activities of key metabolic enzymes. Can J Microbio 58(12):1335–1343

    Article  CAS  Google Scholar 

  • Li LJ, Liu XM, Guo YP, Ma EB (2005) Activity of the enzymes of the antioxidative system in cadmium–treated Oxya chinensis (Orthoptera Acridoidae). Environ Toxicol Pharmacol 20(3):412–416

    Article  CAS  Google Scholar 

  • Li XL, Cui XH, Han JR (2006) Sclerotial biomass and carotenoid yield of Penicillium sp. PT95 under oxidative growth conditions and in the presence of antioxidant ascorbic acid. J Appl Microbiol 101(3):725–731

    Article  CAS  PubMed  Google Scholar 

  • Martino E, Franco B, Piccoli G, Stocchi V, Perotto S (2002) Influence of zinc ions on protein secretion in a heavy metal tolerant strain of the ericoid mycorrhizal fungus Oidiodendron maius. Mol Cell Biochem 231:179–185

    Article  CAS  PubMed  Google Scholar 

  • McKersie BD, Leshem YY (1994) Oxidative stress. In: McKersie BD, Leshem YY (eds) Stress and stress coping in cultivated plants. Kluwer, Dordrecht, pp 15–54

    Chapter  Google Scholar 

  • Merian E (1991) Metals and their compounds in the environment. VCH Verlag, Weinheim

    Google Scholar 

  • Mohr H, Schopfer P (1995) Plant physiology. Springer, Berlin

    Google Scholar 

  • Mukherjee A, Das D, Mondal SK, Biswas R, Das TK, Boujedaini N, Khuda–Bukhsh AR (2010) Tolerance of arsenate–induced stress in Aspergillus niger, a possible candidate for bioremediation. Ecotoxicol Environ Saf 73:172–182

    Article  CAS  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880

    CAS  Google Scholar 

  • Navari–Izzo F, Meneguzzo S, Loggini B, Vazzana C, Sgherri CLM (1997) The role of the glutathione system during dehydration of Boea hygroscopica. Physiol Plant 99:23–30

    Article  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49:249–279

    Article  CAS  Google Scholar 

  • Peña MMO, Lee J, Thiele DJ (1999) A delicate balance: homeostatic control of copper uptake and distribution. J Nutr 129(7):1251–1260

    PubMed  Google Scholar 

  • Pitt JI (2000) A laboratory guide to common Penicillium species, 3rd edn. CSIRO Division of Food Processing, North Ryde

    Google Scholar 

  • Pócsi I, Prade RA, Penninckx J (2004) Glutathione altruistic metabolite in fungi. Adv Microbial Physiol 49:1–76

    Article  Google Scholar 

  • Radic S, Babic M, Skobic D, Roje V, Pevalek–Kozlina B (2010) Ecotoxicological effects of aluminum and zinc on growth and antioxidants in Lemna minor L. Ecotoxicol Environ Saf 73:336–342

    Article  CAS  PubMed  Google Scholar 

  • Ray AA (1985) SAS users guide: statistics. SAS Institute, Cary

    Google Scholar 

  • Rizzo DM, Blanchette RA, Palmer MA (1992) Biosorption of metal ions by Armillaria rhizomorphs. Can J Bot 70:1515–1520

    Article  CAS  Google Scholar 

  • Romero–Isart N, Vašák M (2002) Advances in the structure and chemistry of metallothioneins. J Inorg Biochem 88:388–396

    Article  PubMed  Google Scholar 

  • Schraudner M, Langebartels J, Sandermann H (1997) Changes in the biochemical status of plant cell induced by the environmental pollutant ozone. Physiol Plant 100(2):274–280

    Article  CAS  Google Scholar 

  • Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14(1):43–50

    Article  CAS  PubMed  Google Scholar 

  • Simic GM (1992) Carotenoid free radicals. In: Packer L (ed) Methods in enzymology. Academic, New York, pp 444–453

    Google Scholar 

  • Stratton PS, Liebler DC (1997) Determination of singlet oxygen-specific versus radical-mediated lipid peroxidation in photosensitized oxidation of lipid bilayers: Effect of β-carotene and α-tocopherol. Biochemistry 36(42):12911–12920

    Article  CAS  PubMed  Google Scholar 

  • Sun HS, Wang HN, Wang YY (2007) Study on activities of glutathione reductase in the haemolymph of Chlamys farreri. Mar Sci Bull 26:108–112

    Google Scholar 

  • Suresh K, Subramanyam C (1996) Isolation and characterization of a copper containing protein from blue cell walls of Neurospora crassa. Indian J Exp Biol 34:671–677

    CAS  PubMed  Google Scholar 

  • Thounaojam TC, Panda P, Mazumdar P, Kumar D, Sharma GD, Sahoo L (2012) Excess copper induced oxidative stress and response of antioxidants in rice. Plant Physiol Biochem 53:33–39

    Article  CAS  PubMed  Google Scholar 

  • Uauy R, Olivares M, Gonzalez M (1998) Essentiality of copper in humans. Am J Clin Nutr 67[Suppl]:952S–959S

    CAS  PubMed  Google Scholar 

  • Wang S, Teng S, Fan M (2010) Interaction between heavy metals and aerobic granular sludge. In: Santosh Kumar Sarkar (ed) Environmental management. Sciyo, Croatia, pp 173–188

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inzé D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C-3 plants. EMBO J 16:4806–4816

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamamoto Y, Kobayashi Y, Devi SR, Rikiishi S, Matsumoto H (2002) Aluminum toxicity is associated with mitochondrial dysfunction and the production of reactive oxygen species in plant cells. Plant Physiol 128:63–72

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yazdanpanah M, Luo XP, Lau R, Greenberg M, Fisher LJ, Lehotay DC (1997) Cytotoxic aldehydes as possible markers for childhood cancer. Free Radic Biol Med 23(6):870–878

    Article  CAS  PubMed  Google Scholar 

  • Zervoudakis G, Tairis N, Salahas G, Georgiou CD (2003) β-Carotene production and sclerotial differentiation in Sclerotinia minor. Mycol Res 107(5):624–631

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Support for this research by the Chinese National Natural Science Fund (grant no. 31070048) is gratefully acknowledged.

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Correspondence to Wenjing Zhao.

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Zhao, W., Han, J. & Long, D. Effect of copper−induced oxidative stress on sclerotial differentiation, endogenous antioxidant contents, and antioxidative enzyme activities of Penicillium thomii PT95. Ann Microbiol 65, 1505–1514 (2015). https://doi.org/10.1007/s13213-014-0989-6

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