Skip to main content

Advertisement

SpringerLink
Log in

Cadmium and lead bioavailability and their effects on polycyclic aromatic hydrocarbons biodegradation by spent mushroom substrate

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

Abstract

Bioremediation of mixed metal–organic soil pollution constitutes a difficult task in different ecosystems all around the world. The aims of this work are to determine the capacity of two spent mushroom substrates (Agaricus bisporus and Pleurotus ostreatus) to immobilize Cd and Pb, to assess the effect of these metals on laccase activity, and to determine the potential of spent A. bisporus substrate to biodegrade four polycyclic aromatic hydrocarbons (PAH): fluorene, phenanthrene, anthracene, and pyrene, when those toxic heavy metals Cd and Pb are present. According to adsorption isotherms, spent P. ostreatus and A. bisporus substrates showed a high Pb and Cd adsorption capacity. Pb and Cd interactions with crude laccase enzyme extracts from spent P. ostreatus and A. bisporus substrates showed Cd and Pb enzyme inhibition; however, laccase activity of A. bisporus presented lower inhibition. Spent A. bisporus substrate polluted with PAH and Cd or Pb was able to biodegrade PAH, although both metals decrease the biodegradation rate. Spent A. bisporus substrate contained a microbiological consortium able to oxidize PAH with high ionization potential. Cd and Pb were immobilized during the bioremediation process by spent A. bisporus substrate. Consequently, spent A. bisporus substrate was adequate as a multi-polluted soil bioremediator.

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

Similar content being viewed by others

References

  • Aranda E, Ullrich R, Hofrichter M (2010) Conversion of polycyclic aromatic hydrocarbons, methyl naphthalenes and dibenzofuran by two fungal peroxigenases. Biodegradation 21:267–281. doi:10.1007/s10532-009-9299-2

    Article  CAS  Google Scholar 

  • Baldrian P, Wiesche C, Gabriel J, Nerud F, Zadrazil F (2000) Influence of cadmium and mercury on activities of ligninolytic enzymes and degradation of polycyclic aromatic hydrocarbons by Pleurotus ostreatus in soil. Appl Environ Microbiol 66:2471–2478. doi: 0099-2240/00/$04.00+0

  • Baldrian P, Gabriel J (2002) Copper and cadmium increase laccase activity in Pleurotus ostreatus. FEMS Microbiol Lett 206:69–74. doi:10.1016/S0378-1097(01)00519-5

    Article  CAS  Google Scholar 

  • Baldrian P (2003) Interactions of heavy metals with white-rot fungi. Enzyme Microb Technol 32:78–91. doi:10.1016/S0141-0229(02)00245-4

    Article  CAS  Google Scholar 

  • Baldrian P, Valášková V, Merhautová V, Gabriel J (2005) Degradation of lignocellulose by Pleurotus ostreatus in the presence of copper, manganese, lead and zinc. Res Microbiol 156:670–676. doi:10.1016/j.resmic.2005.03.007

    Article  CAS  Google Scholar 

  • Baldrian P (2006) Fungal laccases—occurrence and properties. FEMS Microbiol Rev 30:215–242. doi:10.1111/j.1574-4976.2005.00010.x

    Article  CAS  Google Scholar 

  • Beesley L, Moreno-Jiménez E, Gomez-Eyles JL (2010) Effects of biochar and greenwaste compost amendments on mobility, bioavailability and toxicity of inorganic and organic contaminants in a multi-element polluted soil. Environ Pollut 158:2282–2287. doi:10.1016/j.envpol.2010.02.003

    Article  CAS  Google Scholar 

  • Chen GQ, Zeng GM, Tu X, Huang GH, Chen YN (2005) A novel biosorbent: characterization of the spent mushroom compost and its application for removal of heavy metals. J Environ Sci 17:756–760

    CAS  Google Scholar 

  • Covino S, Svobodová K, Cvancarová M, Dannibale A, Petruccioli M, Federici F, Kresinova Z, Galli E, Cajthaml T (2010) An efficient PAH-degrading Lentinus (Panus) tigrinus strain: effect of inoculum formulation and pollutant bioavailability in solid matrices. J Hazard Mater 183:669–676. doi:10.1016/j.jhazmat.2010.07.078

    Article  CAS  Google Scholar 

  • Farnet AM, Gil G, Ruaudel F, Chevremont AC, Ferre E (2009) Polycyclic aromatic hydrocarbon transformation with laccases of a white-rot fungus isolated from a Mediterranean schlerophyllous litter. Geoderma 149:267–271. doi:10.1016/j.geoderma.2008.12.011

    Article  CAS  Google Scholar 

  • García-Delgado C, Cala V, Eymar E (2012) Influence of chemical and mineralogical properties of organic amendments on the selection of an adequate analytical procedure for trace elements determination. Talanta 88:375–384. doi:10.1016/j.talanta.2011.11.003

    Article  Google Scholar 

  • García-Delgado C, Yunta F, Eymar E (2013) Methodology for polycyclic aromatic hydrocarbons extraction from either fresh or dry spent mushroom compost and quantification by HPLC-PDA. Comm Soil Sci Plant Anal 44:817–825. doi:10.1080/00103624.2013.749439

    Article  Google Scholar 

  • Guo MX, Chorover J, Fox RH (2001) Effects of spent mushroom substrate weathering on the chemistry of underlying soils. J Environ Qual 30:2127–2134. doi:10.2134/jeq2001.2127

    Article  CAS  Google Scholar 

  • Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–15. doi:10.1016/j.jhazmat.2009.03.137

    Article  CAS  Google Scholar 

  • Hwang HM, Zhao HXX (2007) Enhanced bioremediation of polycyclic aromatic hydrocarbons by environmentally friendly techniques. J Environ Sci Health C 25:313–352. doi:10.1080/10590500701704011

    Article  CAS  Google Scholar 

  • Jarosz-Wilkolazka A, Graz M, Braha B, Menge S, Schlosser D, Krauss GJ (2006) Species-specific Cd-stress response in the white rot basidiomycetes Abortiporus biennis and Cerrena unicolor. Biometals 19:39–49. doi:10.1007/s10534-005-4599-4

    Article  CAS  Google Scholar 

  • Leonardi V, Giubilei MA, Federici E, Spaccapelo R, Sasek V, Novotny C, Petruccioli M, Dannibale A (2008) Mobilizing agents enhance fungal degradation of polycyclic aromatic hydrocarbons and affect diversity of indigenous bacteria in soil. Biotechnol Bioeng 101:273–285. doi:10.1002/bit.21909

    Article  CAS  Google Scholar 

  • Li X, Lin X, Zhang J, Wu Y, Yin R, Feng Y, Wang Y (2010) Degradation of polycyclic aromatic hydrocarbons by crude extracts from spent mushroom substrate and its possible mechanisms. Curr Microbiol 60:336–342. doi:10.1007/s00284-009-9546-0

    Article  CAS  Google Scholar 

  • Majcherczyk A, Johannes C, Hüttermann A (1998) Oxidation of polycyclic aromatic hydrocarbons (PAH) by laccase of Trametes versicolor. Enzyme Microb Technol 22:335–341. doi:10.1016/S0141-0229(97)00199-3

    Article  CAS  Google Scholar 

  • Márquez-Rocha FJ, Hernández-Rodríguez VZ, Vázquez-Duahlt R (2000) Biodegradation of soil-adsorbed polycyclic aromatic hydrocarbons by the white rot fungus Pleurotus ostreatus. Biotechnol Lett 22:469–472. doi:10.1023/A:1005663419547

    Article  Google Scholar 

  • Mayolo-Deloisa K, Machin-Ramirez C, Rito-Palomares M, Trejo-Hernández MR (2011) Oxidation of polycyclic aromatic hydrocarbons using partially purified laccase from residual compost of Agaricus bisporus. Chem Eng Technol 34:1368–1372. doi:10.1002/ceat.201000205

    Article  CAS  Google Scholar 

  • Megharaj M, Ramakrishnan B, Venkateswarlu K, Sethunanthan N, Naidu R (2011) Bioremediation approaches for organic pollutants: a critical perspective. Environ Int 37:136–1375. doi:10.1016/j.envint.2011.06.003

    Article  Google Scholar 

  • Michael HW, Bultosa G, Pant LM (2011) Nutritional contents of three edible oyster mushrooms grown on two substrates at Haramaya, Ethiopia, and sensory properties of boiled mushroom and mushroom sauce. Int J Food Sci Tech 46:372–738. doi:10.1111/j.1365-2621.2010.02543.x

    Article  Google Scholar 

  • Pardo-Giménez A, Pardo-González JE (2008) Evaluation of casing materials made from spent mushroom substrate and coconut fibre pith for use in production of Agaricus bisporus (Lange) Imbach. Spanish J Agr Res 6:683–690. doi:10.5424/361

    Article  Google Scholar 

  • Peng RH, Xiong AS, Xue Y, Fu XY, Gao F, Zhao W, Tian YS, Yao QH (2008) Microbial biodegradation of polyaromatic hydrocarbons. FEMS Microbiol Rev 32:927–955. doi:10.1111/j.1574-6976.2008.00127.x

    Article  CAS  Google Scholar 

  • Reid BJ, Fermor TR, Semple KT (2002) Induction of PAH-catabolism in mushroom compost and its use in the biodegradation of soil-associated phenanthrene. Environ Pollut 118:65–73. doi:10.1016/S0269-7491(01)00239-1

    Article  CAS  Google Scholar 

  • Royse JR (2010) Effects of fragmentation, supplementation and the addition of phase II compost to 2nd break compost on mushroom (Agaricus bisporus) yield. Biores Technol 101:188–192. doi:10.1016/j.biortech.2009.07.073

    Article  CAS  Google Scholar 

  • Smith MJ, Flowers TH, Duncan HJ, Saito H (2011) Study of PAH dissipation and phytoremediation in soils: comparing freshly spiked with weathered soil from a former works. J Hazard Mater 192:1219–1225. doi:10.1021/es903415t

    Article  CAS  Google Scholar 

  • Tanaka H, Itakura S, Enoki A (1999) Hydroxyl radical generation by an extracellular low-molecular-weight substance and phenol oxidase activity during wood degradation by the white-rot basidiomycete Trametes versicolor. J Biotechnol 75:57–70. doi:10.1016/S0168-1656(99)00138-8

    Article  CAS  Google Scholar 

  • Tandy S, Healey JR, Nasona MA, Williamson JC, Jones DL (2009) Heavy metal fractionation during the co-composting of biosolids, deinking paper fibre and green waste. Biores Technol 100:4220–4226. doi:10.1016/j.envpol.2008.08.006

    Article  CAS  Google Scholar 

  • Tapia Y, Cala V, Eymar E, Frutos I, Gárate A, Masaguer A (2010) Chemical characterization and evaluation of composts as organic amendments for immobilizing cadmium. Biores Technol 101:5437–5443. doi:10.1016/j.biortech.2010.02.034

    Article  CAS  Google Scholar 

  • Thavamani P, Megharaj M, Krishnamurti GSR, McFarland R, Naidu R (2011) Finger printing of mixed contaminants from former manufactured gas plant (MGP) site soils: implications to bioremediation. Environ Int 37:184–189. doi:10.1016/j.envint.2010.08.017

    Article  CAS  Google Scholar 

  • Trejo-Hernández MR, López-Munguia A, Quintero Ramirez R (2001) Residual compost of Agaricus bisporus as a source of crude laccase for enzymic oxidation of phenolic compounds. Process Biochem 36:635–639. doi:10.1016/S0032-9592(00)00257-0

    Article  Google Scholar 

  • Wariishi H, Vallis K, Gold MH (1992) Manganese(II) oxidation by manganese peroxidase from the basidiomycete Phanerochate chrysosporium. Kinetic mechanisms and role of chelators. J Biol Chem 267:23689–23695

    Google Scholar 

  • Wong DWS (2009) Structure and action mechanism of ligninolytic enzymes. Appl Biochem Biotechnol 157:174–209. doi:10.1007/s12010-008-8279-z

    Article  CAS  Google Scholar 

  • Zhang S, Lu A, Shan XQ, Wang Z, Wang S (2002) Microwave extraction of heavy metals from wet rhizosphere soils and its applications to evaluation of bioavailability. Anal Bioanal Chem 374:942–947. doi:10.1016/j.envpol.2005.08.031

    Article  CAS  Google Scholar 

  • Zhou D, Zhang L, Guo S (2005) Mechanisms of lead biosorption on cellulose/chitin beads. Water Res 39:3755–3762. doi:10.1016/j.watres.2005.06.033

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Ministry of Education and Science and the Ministry of Science and Innovation of Spain (project 2005-06258-C02-02/TECNO CTM and project 2009-13140-C02-02/TECNO CTM, respectively). C. García-Delgado was on a “FPI” pre-doctoral grant from the Autonomous University of Madrid. The authors wish to thank Recomsa for providing spent mushroom substrates.

Author information

Authors and Affiliations

  1. Department of Agricultural Chemistry, Autonomous University of Madrid, Madrid, 28049, Spain

    C. García-Delgado, N. Jiménez-Ayuso, I. Frutos, A. Gárate & E. Eymar

Authors
  1. C. García-Delgado
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. Jiménez-Ayuso
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. Frutos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Gárate
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. E. Eymar
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Eymar.

Additional information

Responsible editor: Céline Guéguen

Rights and permissions

Reprints and permissions

About this article

Cite this article

García-Delgado, C., Jiménez-Ayuso, N., Frutos, I. et al. Cadmium and lead bioavailability and their effects on polycyclic aromatic hydrocarbons biodegradation by spent mushroom substrate. Environ Sci Pollut Res 20, 8690–8699 (2013). https://doi.org/10.1007/s11356-013-1829-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-013-1829-0

Keywords

Search

Navigation