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Lead and cadmium-induced oxidative stress impacting mycelial growth of Oudemansiella radicata in liquid medium alleviated by microbial siderophores

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Abstract

In this study, the effects of siderophores produced by six bacteria on mycelium growth, Cd and Pb accumulation, lipid peroxidation, protein content and antioxidant enzyme in Oudemansiella radicata were investigated in Cd and Pb-containing liquid medium. The results showed that inoculation with siderophore-containing filtrates (SCF) partly enhanced the growth of O. radicata after 15 days, with 0.8–32.4% biomass increase for Cd and 0.7–20.8% for Pb compared to control(s), which lacked siderophore. The maximum enhancement for accumulation were found to be confined to Bacillus sp. FFQ2(s) (26.5%) for Cd and Pseudomonas sp. CY63(s) (158.9%) for Pb. A significant decrease in MDA content indicated that lipid peroxidation in O. radicata was alleviated by siderophores. Besides, antioxidant enzyme SOD and POD activities also displayed obviously decrease in SCF-treated mycelium compared to control(s) treatment, while CAT activity did not present significant change. Protein level in O. radicata treated by SCF increased from 0.3 to 138.0% for Cd and from 10.9 to 107.1% for Pb compared to control(s). Therefore, the present work suggests that microbial siderophores can reduce the toxicity of metals to mycelium and then alleviate heavy metals-inducing oxidative stress in O. radicata.

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References

  • Barzanti R, Ozino F, Bazzicalupo M, Gabbrielli R, Galardi F, Gonnelli C et al (2007) Isolation and characterization of endophytic bacteria from the nickel hyperaccumulator plant Alyssum bertolonii. Microb Ecol 53:306–316

    Article  CAS  Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  Google Scholar 

  • Beers RF Jr, Sizer IW (1952) A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140

    CAS  Google Scholar 

  • Bowler C, Montagu MV, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Biol 43:83–116

    Article  CAS  Google Scholar 

  • Braud A, Jézéquel K, Bazot S, Lebeau T (2009) Enhanced phytoextraction of an agricultural Cr- and Pb-contaminated soil by bioaugmentation with siderophore-producing bacteria. Chemosphere 74:280–286

    Article  Google Scholar 

  • Bric JM, Bostock RM, Silversone SE (1991) Rapid in situ assay for indoleacetic acid production by bacteria immobilized on a nitrocellulose membrane. Appl Environ Microb 57:535–538

    CAS  Google Scholar 

  • Byers HK, Stackebrandt E, Hayward C, Blackall LL (1998) Molecular investigation of a microbial mat associated with the great artesian basin. FEMS Microbiol Ecol 25:391–403

    Article  CAS  Google Scholar 

  • Collin-Hansen C, Andersen RA, Steinnes E (2005) Damage to DNA and lipids in Boletus edulis exposed to heavy metals. Mycol Res 109:1386–1396

    Article  CAS  Google Scholar 

  • Dazy M, Masfaraud J-F, Férard J-F (2009) Induction of oxidative stress biomarkers associated with heavy metal stress in Fontinalis antipyretica Hedw. Chemosphere 75:297–302

    Article  CAS  Google Scholar 

  • Demirbas A (2002) Metal ion uptake by mushrooms from natural and artificially enriched soils. Food Chem 78:89–93

    Article  CAS  Google Scholar 

  • Dimkpa CO, Svatos A, Dabrowska P, Schmidt A, Boland W, Kothe E (2008) Involvement of siderophores in the reduction of metal-induced inhibition of auxin synthesis in Streptomyces sp. Chemosphere 74:19–25

    Article  CAS  Google Scholar 

  • Dimkpa CO, Merten D, Svatos A, Büchel G, Kothe E (2009) Metal-induced oxidative stress impacting plant growth in contaminated soil is alleviated by microbial siderophores. Soil Biol Biochem 41:154–162

    Article  CAS  Google Scholar 

  • Fiske CH, Subbarow Y (1925) A colorimetric determination of phosphorus. J Biol Chem 66:375–400

    CAS  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    Article  CAS  Google Scholar 

  • Islam E, Liu D, Li T, Yang X, Jin X, Mahmood Q et al (2008) Effect of Pb toxicity on leaf growth, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 154:914–926

    Article  CAS  Google Scholar 

  • Jiang C-y, Sheng X-f, Qian M, Wang Q-y (2008) Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil. Chemosphere 72:157–164

    Article  CAS  Google Scholar 

  • Kalac P, Svoboda L (2000) A review of trace element concentrations in edible mushrooms. Food Chem 69:273–281

    Article  CAS  Google Scholar 

  • Kuffner M, Puschenreiter M, Wieshammer G, Gorfer M, Sessitsch A (2008) Rhizosphere bacteria affect growth and metal uptake of heavy metal accumulating willows. Plant Soil 304:35–44

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrought NJ, Farr AL, Randall RJ (1951) Protein measurement with folin-phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • Mallick S, Sinam G, Kumar Mishra R, Sinha S (2010) Interactive effects of Cr and Fe treatments on plants growth, nutrition and oxidative status in Zea mays L. Ecotoxicol Environ Saf 73:987–995

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Neubauer U, Furrer G, Kayser A, Schulin R (2000) Siderophores, NTA, and citrate: potential soil amendments to enhance heavy metal mobility in phytoremediation. Int J Phytoremediation 2:353–368

    Article  CAS  Google Scholar 

  • Omran RG (1980) Peroxide levels and the activities of catalase, peroxidase, and indoleacetic acid oxidase during and after chilling cucumber seedlings. Plant Physiol 65:407–408

    Article  CAS  Google Scholar 

  • Pérez-Miranda S, Cabirol N, George-Téllez R, Zamudio-Rivera LS, Fernández FJ (2007) O-CAS, a fast and universal method for siderophore detection. J Microbiol Methods 70:127–131

    Article  Google Scholar 

  • Rajkumar M, Freitas H (2008a) Effects of inoculation of plant-growth promoting bacteria on Ni uptake by Indian mustard. Bioresour Technol 99:3491–3498

    Article  CAS  Google Scholar 

  • Rajkumar M, Freitas H (2008b) Influence of metal resistant-plant growth-promoting bacteria on the growth of Ricinus communis in soil contaminated with heavy metals. Chemosphere 71:834–842

    Article  CAS  Google Scholar 

  • Rajkumar M, Ae N, Prasad MNV, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149

    Article  CAS  Google Scholar 

  • Ranieri A, Castagna A, Scebba F, Careri M, Zagnoni I, Predieri G et al (2005) Oxidative stress and phytochelatin characterisation in bread wheat exposed to cadmium excess. Plant Physiol Biochem 43:45–54

    Article  CAS  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  CAS  Google Scholar 

  • Serafín Muñoz AH, Wrobel K, Gutierrez Corona JF, Wrobel K (2007) The protective effect of selenium inorganic forms against cadmium and silver toxicity in mycelia of Pleurotus ostreatus. Mycol Res 111:626–632

    Article  Google Scholar 

  • Sheng X-F, Xia J–J, Jiang C-Y, He L-Y, Qian M (2008) Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environ Pollut 156:1164–1170

    Article  CAS  Google Scholar 

  • Singh R, Tripathi RD, Dwivedi S, Kumar A, Trivedi PK, Chakrabarty D (2010) Lead bioaccumulation potential of an aquatic macrophyte Najas indica are related to antioxidant system. Bioresour Technol 101:3025–3032

    Article  CAS  Google Scholar 

  • Sinha S, Mukherjee S (2008) Cadmium-induced siderophore production by a high Cd-resistant bacterial strain relieved cd toxicity in plants through root colonization. Curr Microbiol 56:55–60

    Article  CAS  Google Scholar 

  • Somashekaraiah BV, Padmaja K, Prasad ARK (1992) Phytotoxicity of cadmium ions on germinating seedlings of mung bean (Phaseolus vulgaris): Involvement of lipid peroxides in chlorphyll degradation. Physiol Plant 85:85–89

    Article  CAS  Google Scholar 

  • Sundara-Rao WVB, Sinha MK (1963) Phosphate dissolving microorganisms in the soil and rhizosphere. Indian J Agric Sci 33:272–278

    Google Scholar 

  • Tripathi M, Munot HP, Shouche Y, Meyer JM, Goel R (2005) Isolation and functional characterization of siderophore-producing lead- and cadmium-resistant Pseudomonas putida KNP9. Curr Microbiol 50:233–237

    Article  CAS  Google Scholar 

  • Xu H, Song P, Gu W, Yang Z (2011) Effects of heavy metals on production of thiol compounds and antioxidant enzymes in Agaricus bisporus. Ecotoxicol Environ Saf 74:1685–1692

    Google Scholar 

  • Yannarelli GG, Fernández-Alvarez AJ, Santa-Cruz DM, Tomaro ML (2007) Glutathione reductase activity and isoforms in leaves and roots of wheat plants subjected to cadmium stress. Phytochemistry 68:505–512

    Article  CAS  Google Scholar 

  • Zhang F-Q, Wang Y-S, Lou Z-P, Dong J-D (2007) Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza). Chemosphere 67:44–50

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was financially supported by the NSFC (No.41171253), the National 863 High Technology Research and Development Program of China (No. 2006AA06Z361), and Science and Technology Development Projiect of Longquanyi District Aro-technical Extension Centre, Chengdu. The authors wish to thank Professor Guanglei Cheng and Dong Yu from Sichuan University for their technical assistance.

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Authors and Affiliations

  1. Key Laboratory for Bio-resources and Eco-environment of Education Ministry, College of Life Science, Sichuan University, Chengdu, 610064, China

    Yan-ru Cao, Qi-qi Zhao & Heng Xu

  2. College of Chemistry and Life Science, Leshan Normal University, Leshan, 614000, China

    Xi-yu Zhang

  3. Longquanyi Aro-technical Extension Centre, Chengdu, 610100, China

    Jia-yu Deng

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  1. Yan-ru Cao
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  2. Xi-yu Zhang
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  5. Heng Xu
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Correspondence to Heng Xu.

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Cao, Yr., Zhang, Xy., Deng, Jy. et al. Lead and cadmium-induced oxidative stress impacting mycelial growth of Oudemansiella radicata in liquid medium alleviated by microbial siderophores. World J Microbiol Biotechnol 28, 1727–1737 (2012). https://doi.org/10.1007/s11274-011-0983-0

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  • DOI: https://doi.org/10.1007/s11274-011-0983-0

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