Skip to main content
SpringerLink
Log in

Combined bioremediation of soil co-contaminated with cadmium and endosulfan by Pleurotus eryngii and Coprinus comatus

  • Reclamation and Management of Polluted Soils: Options and Case Studies
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

The subjects of this study were to investigate the remediating potential of the co-cultivation of Pleurotus eryngii and Coprinus comatus on soil that is co-contaminated with heavy metal (cadmium (Cd)) and organic pollutant (endosulfan), and the effects of the co-cultivated mushrooms on soil biochemical indicators, such as laccase enzyme activity and bacterial counts.

Materials and methods

A pot experiment was conducted to investigate the combined bioremediation effects on co-contaminated soil. After the mature fruiting bodies were harvested from each pot, the biomass of mushrooms was recorded. In addition, bacterial counts and laccase enzyme activity in soil were determined. The content of Cd in mushrooms and soil was detected by the flame atomic absorption spectrometry (FAAS), and the variations of Cd fractions in soil were determined following the modified BCR sequential extraction procedure. Besides, the residual endosulfan in soil was detected by gas chromatography-mass spectrometry (GC-MS).

Results and discussion

The results indicated that co-cultivation of P. eryngii and C. comatus exerted the best remediation effect on the co-contaminated soil. The biomass of mushroom in the co-cultivated group (T group) was 1.57–13.20 and 19.75–56.64% higher than the group individually cultivated with P. eryngii (P group) or C. comatus (C group), respectively. The concentrations of Cd in the fruiting bodies of mushrooms were 1.83–3.06, 1.04–2.28, and 0.67–2.60 mg/kg in T, P, and C groups, respectively. Besides, the removal rates of endosulfan in all treatments exceeded 87%. The best bioremediation effect in T group might be caused by the mutual promotion of these two kinds of mushrooms.

Conclusions

The biomass of mushroom, laccase activity, bacterial counts, and Cd content in mushrooms were significantly enhanced, and the dissipation effect of endosulfan was slightly higher in the co-cultivated group than in the individually cultivated groups. In this study, the effect of co-cultivated macro fungi P. eryngii and C. comatus on the remediation of Cd and endosulfan co-contaminated soil was firstly reported, and the results are important for a better understanding of the co-remediation for co-contaminated soil.

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

  • Akpinar M, Urek RO (2014) Extracellular ligninolytic enzymes production by Pleurotus eryngii on agroindustrial wastes. Prep Biochem Biotechol 44:772–781

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Baldrian P (2008) Wood-inhabiting ligninolytic basidiomycetes in soils: ecology and constraints for applicability in bioremediation. Fungal Ecol 1:4–12

    Article  Google Scholar 

  • Baldrian P, Wiesche CID (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

    Article  CAS  Google Scholar 

  • Batty LC, Anslow M (2008) Effect of a polycyclic aromatic hydrocarbon on the phytoremediation of zinc by two plant species (Brassica juncea and Festuca arundinacea). Int J Phytoremediation 10:236–251

    Article  CAS  Google Scholar 

  • Cen F, Chen L, Hu Y, Xu H (2011) Chelator-induced bioextraction of heavy metals from artificially contaminated soil by mushroom (Coprinus comatus). Chem Ecol 28:1–14

    Google Scholar 

  • Cen F, Hu Y, Xu H (2012) Responses of antioxidant defenses in Coprinus comatus exposed to cadmium and mercury toxicity. Asian J Chem 24:4679–4685

    CAS  Google Scholar 

  • Chaiyama V, Petcharat V, Kritsaneepaiboon P (2007) Some morphological and physiological aspects and cultivation of Coprinus comatus (O. F. Mull.) Gray Songklanakarin. J Sci Technol 29:261–274

    Google Scholar 

  • Chavez E, He ZL, Stoffella PJ, Mylavarapu R, Li Y, Baligar VC (2016) Evaluation of soil amendments as a remediation alternative for cadmium-contaminated soils under cacao plantations. Environ Sci Pollut Res 23:1–10

    Article  Google Scholar 

  • Chen GQ, Yun C, Zeng GM, Zhang JC, Chen YN, Liang W, Zhang WJ (2010) Speciation of cadmium and changes in bacterial communities in red soil following application of cadmium-polluted compost. Environ Eng Sci 27:2169–2192

    Google Scholar 

  • Chigbo C, Batty L, Bartlett R (2013) Interactions of copper and pyrene on phytoremediation potential of Brassica juncea in copper–pyrene co-contaminated soil. Chemosphere 90:2542–2548

    Article  CAS  Google Scholar 

  • Forootanfar H, Movahednia MM, Yaghmaei S, Tabatabaei-Sameni M, Rastegar H, Sadighi A, Faramarzi MA (2012) Removal of chlorophenolic derivatives by soil isolated ascomycete of Paraconiothyrium variabile and studying the role of its extracellular laccase. J Hazard Mater 209-210:199–203

    Article  CAS  Google Scholar 

  • Gadd GM (1994) Interactions of fungi with toxic metals. Springer, US

    Book  Google Scholar 

  • Gogolev A, Wilke BM (1997) Combination effects of heavy metals and fluoranthene on soil bacteria. Biol Fertil Soils 25:274–278

    Article  CAS  Google Scholar 

  • Hadibarata T, Kristanti RA, Hamdzah M (2014) Biosorption and biotransformation of fluoranthene by the white-rot fungus Pleurotus eryngii F032. Biotechnol Appl Biochem 61:377–388

    Article  Google Scholar 

  • Huang H et al (2011) The phytoremediation potential of bioenergy crop Ricinus communis for DDTs and cadmium co-contaminated soil. Bioresour Technol 102:11034–11038

    Article  CAS  Google Scholar 

  • Hussain S, Arshad M, Saleem M, Khalid A (2008) Biodegradation of alpha- and beta-endosulfan by soil bacteria. Biodegradation 18:731–740

    Article  Google Scholar 

  • Jiang J, Liu H, Qiao L, Ni G, Yuan Y, Xu H (2015a) Combined remediation of Cd–phenanthrene co-contaminated soil by Pleurotus cornucopiae and Bacillus thuringiensis FQ1 and the antioxidant responses in Pleurotus cornucopiae. Ecotoxicol Environ Saf 120:386–393

    Article  CAS  Google Scholar 

  • Jiang J, Qin C, Shu X, Rong C, Song H, Qiao L, Xu H (2015b) Effects of copper on induction of thiol-compounds and antioxidant enzymes by the fruiting body of Oudemansiella radicata. Ecotoxicol Environ Saf 111:60–65

    Article  CAS  Google Scholar 

  • Kamei I, Takagi K, Kondo R (2011) Degradation of endosulfan and endosulfan sulfate by white-rot fungus Trametes hirsuta. J Wood Sci 57:317–322

    Article  CAS  Google Scholar 

  • Kang MS et al (2000) Studies on mycelial growth and artificial cultivation of Pleurotus eryngii. Korean J Mycol 28

  • Kathpal TS, Singh A, Dhankhar JS, Singh G (1997) Fate of endosulfan in cotton soil under sub-tropical conditions of northern India. Pestic Sci 50:21–27

    Article  CAS  Google Scholar 

  • Krastanov A (2000) Removal of phenols from mixtures by co-immobilized laccase/tyrosinase and polyclar adsorption. J Ind Microbiol Biotechnol 24:383–388

    Article  CAS  Google Scholar 

  • Krishnamurti GSR, Naidu R (2000) Speciation and phytoavailability of cadmium in selected surface soils of South Australia. Soil Res 38:991–1004

    Article  CAS  Google Scholar 

  • Li YJ, Hu PJ, Zhao J, Dong CX (2015) Remediation of cadmium- and lead-contaminated agricultural soil by composite washing with chlorides and citric acid. Environ Sci Pollut Res 22:5563–5571

    Article  CAS  Google Scholar 

  • Liu H, Guo S, Kai J, Hou J, Han X, Xu H (2015) Bioremediation of soils co-contaminated with heavy metals and 2,4,5-trichlorophenol by fruiting body of Clitocybe maxima. J Hazard Mater 294:121–127

    Article  CAS  Google Scholar 

  • Lu M, Xu K, Chen J (2013) Effect of pyrene and cadmium on microbial activity and community structure in soil. Chemosphere 91:491–497

    Article  CAS  Google Scholar 

  • Lu M, Zhang ZZ, Wang JX, Zhang M, Xu YX, Wu XJ (2014) Interaction of heavy metals and pyrene on their fates in soil and tall fescue (Festuca arundinacea). Environ Sci Technol 48:1158–1165

    Article  CAS  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  Google Scholar 

  • Najafi S, Jalali M (2015) Effects of organic acids on cadmium and copper sorption and desorption by two calcareous soils. Environ Monit Assess 187:1–10

    Article  CAS  Google Scholar 

  • Narin I, Soylak M, Dogan M (1997) Traffic pollution in Nigde-Turkiye: investigation of trace element contents of soil samples. Fresenius Environ Bull 6:749–752

    CAS  Google Scholar 

  • Perronnet K, Schwartz C, Gérard E, Morel JL (2000) Availability of cadmium and zinc accumulated in the leaves of Thlaspi caerulescens incorporated into soil. Plant Soil 227:257–263

    Article  CAS  Google Scholar 

  • Qi L, Wang Z, Song M, Chen Y (2006) Evaluation of dissipation mechanisms by Lolium perenne L, and Raphanus sativus for pentachlorophenol (PCP) in copper co-contaminated soil. Sci Total Environ 368:814–822

    Article  Google Scholar 

  • Ribeiro B et al (2008) Comparative study of phytochemicals and antioxidant potential of wild edible mushroom caps and stipes. Food Chem 110:47–56

    Article  CAS  Google Scholar 

  • Rivero A, Niell S, Cesio V, Cerdeiras MP, Heinzen H (2012) Analytical methodology for the study of endosulfan bioremediation under controlled conditions with white rot fungi. J Chromatogr B 907:168–172

    Article  CAS  Google Scholar 

  • Roy P, Dhara K, Manassero M, Banerjee P (2000) Effects of long-term contamination of DDT on soil microflora with special reference to soil algae and algal transformation of DDT. Environ Pollut 109:35–42

    Article  Google Scholar 

  • Sikkema J, de Bont JA, Poolman B (1994) Interactions of cyclic hydrocarbons with biological membranes. J Biol Chem 269:8022–8028

    CAS  Google Scholar 

  • Sinsabaugh RL (2010) Phenol oxidase, peroxidase and organic matter dynamics of soil. Soil Biol Biochem 42:391–404

    Article  CAS  Google Scholar 

  • Souza SCRD, Andrade SALD, Souza LAD, Schiavinato MA (2012) Lead tolerance and phytoremediation potential of Brazilian leguminous tree species at the seedling stage. J Environ Manag 110:299–307

    Article  Google Scholar 

  • Soylak M, Türkoglu O (1999) Trace metal accumulation caused by traffic in an agricultural soil near a motorway in Kayseri, Turkey. J Trace Microprobe Tech 17:209–217

    CAS  Google Scholar 

  • Sun Y, Zhou Q, Xu Y, Wang L, Liang X (2011) Phytoremediation for co-contaminated soils of benzo[a]pyrene (B[a]P) and heavy metals using ornamental plant Tagetes patula. J Hazard Mater 186:2075–2082

    Article  CAS  Google Scholar 

  • Sungur A, Soylak M, Yilmaz E (2015) Characterization of heavy metal fractions in agricultural soils by sequential extraction procedure: the relationship between soil properties and heavy metal fractions. Soil Sediment Contam 24:1–15

    Article  CAS  Google Scholar 

  • Tang X, Dong S, Shi W, Gao N, Zuo L, Xu H (2016) Fates of nickel and fluoranthene during the bioremediation by Pleurotus eryngii in three different soils. J Basic Microbiol 56:1194–1202

    Article  CAS  Google Scholar 

  • Ulčnik A, Cigić IK, Pohleven F (2013) Degradation of lindane and endosulfan by fungi, fungal and bacterial laccases. World J Microbiol Biotechnol 29:2239–2247

    Article  Google Scholar 

  • Vig K, Megharaj M, Sethunathan N, Naidu R (2003) Bioavailability and toxicity of cadmium to microorganisms and their activities in soil: a review. Adv Environ Res 8:121–135

    Article  CAS  Google Scholar 

  • Wang C, Yu D, Shi W, Jiao K, Wu B, Xu H (2016) Application of spent mushroom (Lentinula edodes) substrate and acclimated sewage sludge on the bioremediation of polycyclic aromatic hydrocarbon polluted soil. RSC Adv 6:37274–37285

    Article  CAS  Google Scholar 

  • Wang K, Zhu Z, Huang H, Li T, He Z, Yang X, Alva A (2012) Interactive effects of Cd and PAHs on contaminants removal from co-contaminated soil planted with hyperaccumulator plant Sedum alfredii. J Soils Sediments 12:556–564

    Article  CAS  Google Scholar 

  • Wang S, Mulligan CN (2004) Rhamnolipid foam enhanced remediation of cadmium and nickel contaminated soil. Water Air and Soil Pollut 157:315–330

    Article  CAS  Google Scholar 

  • Wu B (2015) Mycoremediation potential of Coprinus comatus in soil co-contaminated with copper and naphthalene. RSC Adv 5:67524–67531

    Article  CAS  Google Scholar 

  • Xiang L, Ding S (2010) Effect of Cu 2+, Mn 2+ and aromatic compounds on the production of laccase isoforms by Coprinus comatus. Mycoscience 51:68–74

    Article  Google Scholar 

  • Xu SY, Chen YX, Wu WX, Wang KX, Lin Q, Liang XQ (2006) Enhanced dissipation of phenanthrene and pyrene in spiked soils by combined plants cultivation. Sci Total Environ 363:206–215

    Article  CAS  Google Scholar 

  • Ying L, Feng Z, Jie C, Gan H, Guo Y (2007) Chemical fractionation of heavy metals in urban soils of Guangzhou. China Environ Monit Asses 134:429–439

    Article  Google Scholar 

  • Yoshida H, Sugahara T, Hayashi J (1986) Studies on free sugars, free sugaralcohols and organic acids of wild mushrooms. J Jpn Soc Food Sci 33:426–433

    Article  CAS  Google Scholar 

  • Zhang GQ, Wang YF, Zhang XQ, Ng TB, Wang HX (2010) Purification and characterization of a novel laccase from the edible mushroom Clitocybe maxima. Process Biochem 45:627–633

    Article  CAS  Google Scholar 

  • Zhang RF, Cui ZL, Jian HE, Huang TT, Shun-Peng LI (2004) Ecological effects of long-term methylparathion contamination on soil microflora. Rural Eco-environ 20:48–50

    CAS  Google Scholar 

  • Zhu MJ, Du F, Zhang GQ, Wang HX, Ng TB (2013) Purification a laccase exhibiting dye decolorizing ability from an edible mushroom Russula virescens. Int Biodeterior Biodegrad 82:33–39

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was financially supported by the NSFC (No. 41171253, No. J1103518) and the National High Technology Research and Development Program of China (No. 2013AA06A210). The authors wish to thank Professor Guanglei Cheng and Dong Yu from Sichuan University for their technical assistance.

Author information

Authors and Affiliations

  1. Key Laboratory of Bio-Resources and Eco-Environment (Ministry of Education), College of Life Sciences, Sichuan University, Chengdu, Sichuan, 610064, China

    Ying Wang, BoWen Zhang, NanJun Chen, Can Wang, Su Feng & Heng Xu

Authors
  1. Ying Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. BoWen Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. NanJun Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Can Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Su Feng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Heng Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Su Feng or Heng Xu.

Additional information

Responsible editor: Jaume Bech

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Y., Zhang, B., Chen, N. et al. Combined bioremediation of soil co-contaminated with cadmium and endosulfan by Pleurotus eryngii and Coprinus comatus . J Soils Sediments 18, 2136–2147 (2018). https://doi.org/10.1007/s11368-017-1762-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-017-1762-9

Keywords

Search

Navigation