Skip to main content
Log in

Bioremediation of cadmium-dichlorophen co-contaminated soil by spent Lentinus edodes substrate and its effects on microbial activity and biochemical properties of soil

  • Soils, Sec 1 • Soil Organic Matter Dynamics and Nutrient Cycling • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Soil contamination resulting from industrial and agricultural activities has caused high concerns in recent years. Compared with single pollutant, co-contaminants of heavy metal and organic pollutant in soil are quite complicated. The overall objective of this study was to evaluate the potential of spent Lentinus edodes substrate (SLS) as an organic amendment for bioremediation of cadmium (Cd) and dichlorophen (DCP) co-contaminated soil.

Materials and methods

Pot experiments were conducted to investigate the effect of SLS on the distribution of Cd and dissipation of DCP. The microbial counts and soil respiration rate were determined. The ligninolytic enzymes (manganese peroxidase and laccase) and soil enzymes (dehydrogenase, urease, and acid phosphatase) were analyzed. Variations of Cd fractions in soil were determined following the modified BCR sequential extraction procedure. DCP in soil was detected on a gas chromatography–mass spectrometry (Agilent 6890N GC–MS).

Results and discussion

Results showed that the addition of SLS or sterilized SLS (SSLS) could facilitate soil biological properties including microbial counts, respiration intensity, and soil enzyme activities compared to control soil. The HOAc extractable Cd decreased by 10.94–17.09 and 9.63–12.02 % in SLS and SSLS amended soil, respectively. As for the dissipation of DCP, the SSLS amended soil recorded 82.4–92.8 % while the SLS amended soil recorded 85.0–96.9 % compared to the non-amended soil (68.3–84.1 %). The presence of available residual nutrients in the substrate could promote the growth of indigenous microbes, which could contribute to the dissipation of DCP.

Conclusions

This study investigated the potential of SLS on the bioremediation of sites co-contaminated with Cd and DCP. The SLS-facilitated removal of soil DCP was due to SLS-promoted soil biological properties including the microbial numbers and soil respiration as well as the ligninolytic enzymes. The addition of SSLS and SLS resulted in a decrease of Cd extractability in soil, and significantly facilitated the activities of dehydrogenase, urease, and acid phosphatase. The results demonstrated the potential of SLS in ex situ bioremediation of soil co-contaminated with Cd and DCP, providing an attractive reusing option of this organic waste.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abou-Shanab RAI, Angle JS, Chaney RL (2006) Bacterial inoculants affecting nickel uptake by Alyssum murale from low, moderate and high Ni soils. Soil Biol Biochem 38:2882–2889

    Article  CAS  Google Scholar 

  • Aravindhan R, Madhan B, Rao JR, Nair BU, Ramasami T (2004) Bioaccumulation of chromium from tannery wastewater: an approach for chrome recovery and reuse. Environ Sci Technol 38:300–306

    Article  CAS  Google Scholar 

  • Bello D, Trasar-Cepeda C, Leiros MC, Gil-Sotres F (2013) Modification of enzymatic activity in soils of contrasting pH contaminated with 2,4-dichlorophenol and 2,4,5-trichlorophenol. Soil Biol Biochem 56:80–86

    Article  CAS  Google Scholar 

  • Castillo MD, Torstensson L (2007) Effect of biobed composition, moisture, and temperature on the degradation of pesticides. J Agric Food Chem 55:5725–5733

    Article  CAS  Google Scholar 

  • Cea M, Seaman JC, Jara AA, Fuentes B, Mora ML, Diez MC (2007) Adsorption behavior of 2,4-dichlorophenol and pentachlorophenol in an allophanic soil. Chemosphere 67:1354–1360

    Article  CAS  Google Scholar 

  • Chen YX, Lin Q, He YF, Tian GM (2004) Behavior of Cu and Zn under combined pollution of 2,4-dichlorophenol in the planted soil. Plant Soil 261:127–134

    Article  CAS  Google Scholar 

  • Chen BL, Wang YS, Hu DF (2010) Biosorption and biodegradation of polycyclic aromatic hydrocarbons in aqueous solutions by a consortium of white-rot fungi. J Hazard Mater 179:845–851

    Article  CAS  Google Scholar 

  • Chen M, Xu P, Zeng GM, Yang CP, Huang DL, Zhang JC (2015a) Bioremediation of soils contaminated with polycyclic aromatic hydrocarbons, petroleum, pesticides, chlorophenols and heavy metals by composting: applications, microbes and future research needs. Biotechnol Adv 33:745–755

    Article  CAS  Google Scholar 

  • Chen M, Zeng GM, Lai C, Li J, Xu P, Wu HP (2015b) Molecular basis of laccase bound to lignin: insight from comparative studies on the interaction of Trametes versicolor laccase with various lignin model compounds. RSC Adv 5:52307–52313

    Article  CAS  Google Scholar 

  • Chen M, Qin XS, Zeng GM, Li J (2016) Impacts of human activity modes and climate on heavy metal “spread” in groundwater are biased. Chemosphere 152:439–445

    Article  CAS  Google Scholar 

  • De Amarante OP Jr, Brito NM, Dos Santos TC, Nunes GS, Ribeiro ML (2003) Determination of 2,4-dichlorophenoxyacetic acid and its major transformation product in soil samples by liquid chromatographic analysis. Talanta 60:115–121

    Article  Google Scholar 

  • Escalada JP, Pajares A, Gianotti J, Biasutti A, Criado S, Molina P, Massad W, Amat-Guerri F, Garcia NA (2011) Photosensitized degradation in water of the phenolic pesticides bromoxynil and dichlorophen in the presence of riboflavin, as a model of their natural photodecomposition in the environment. J Hazard Mater 186:466–472

    Article  CAS  Google Scholar 

  • Escalada JP, Arce VB, Porcal GV, Biasutti MA, Criado S, Garcia NA, Martire DO (2014) The effect of dichlorophen binding to silica nanoparticles on its photosensitized degradation in water. Water Res 50:229–236

    Article  CAS  Google Scholar 

  • Formentini TA, Mallmann FJK, Pinheiro A, Fernandes CVS, Bender MA, da Veiga M, dos Santos DR, Doelsch E (2015) Copper and zinc accumulation and fractionation in a clayey Hapludox soil subject to long-term pig slurry application. Sci Total Environ 536:831–839

    Article  CAS  Google Scholar 

  • Gao WX, Liang JF, Pizzul L, Feng XM, Zhang KQ, Castillo MD (2015) Evaluation of spent mushroom substrate as substitute of peat in Chinese biobeds. Int Biodeter Biodegr 98:107–112

    Article  Google Scholar 

  • Garcia-Delgado C, Jimenez-Ayuso N, Frutos I, Garate A, Eymar E (2013) Cadmium and lead bioavailability and their effects on polycyclic aromatic hydrocarbons biodegradation by spent mushroom substrate. Environ Sci Pollut Res 20:8690–8699

    Article  CAS  Google Scholar 

  • García-Delgado C, D’Annibale A, Pesciaroli L, Yunta F, Crognale S, Petruccioli M, Eymar E (2015) Implications of polluted soil biostimulation and bioaugmentation with spent mushroom substrate (Agaricus bisporus) on the microbial community and polycyclic aromatic hydrocarbons biodegradation. Sci Total Environ 508:20–28

    Article  Google Scholar 

  • Gomes HI, Dias-Ferreira C, Ribeiro AB (2013) Overview of in situ and ex situ remediation technologies for PCB-contaminated soils and sediments and obstacles for full-scale application. Sci Total Environ 445:237–260

    Article  Google Scholar 

  • Grujić M, Dojnov B, Potočnik I, Duduk B, Vujčić Z (2015) Spent mushroom compost as substrate for the production of industrially important hydrolytic enzymes by fungi Trichoderma spp. and Aspergillus niger in solid state fermentation. Int Biodeter Biodegr 104:290–298

    Article  Google Scholar 

  • Hackett R (2015) Spent mushroom compost as a nitrogen source for spring barley. Nutr Cycl Agroecosyst 102:253–263

    Article  Google Scholar 

  • Hatvani N, Mécs I (2002) Effect of the nutrient composition on dye decolorisation and extracellular enzyme production by Lentinus edodes on solid medium. Enzyme Microb Technol 30:381–386

    Article  CAS  Google Scholar 

  • He Y, Xu JM, Tang CX, Wu YP (2005) Facilitation of pentachlorophenol degradation in the rhizosphere of ryegrass (Lolium perenne L.). Soil Biol Biochem 37:2017–2024

    Article  CAS  Google Scholar 

  • Hechmi N, Aissa NB, Abdenaceur H, Jedidi N (2014) Evaluating the phytoremediation potential of Phragmites australis grown in pentachlorophenol and cadmium co-contaminated soils. Environ Sci Pollut Res Int 21:1304–1313

    Article  CAS  Google Scholar 

  • Herrero-Hernandez E, Andrades MS, Rodriguez-Cruz MS, Sanchez-Martin MJ (2011) Effect of spent mushroom substrate applied to vineyard soil on the behaviour of copper-based fungicide residues. J Environ Manag 92:1849–1857

    Article  CAS  Google Scholar 

  • Huang HG, Yu N, Wang LJ, Gupta DK, He ZL, Wang K, Zhu ZQ, Yan XC, Li TQ, Yang XE (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 

  • Huang L, Gao X, Liu M, Du G, Guo JS, Ntakirutimana T (2012) Correlation among soil microorganisms, soil enzyme activities, and removal rates of pollutants in three constructed wetlands purifying micro-polluted river water. Ecol Eng 46:98–106

    Article  CAS  Google Scholar 

  • Jin HP, Choppala GK, Bolan NS, Chung JW, Chuasavathi T (2011) Biochar reduces the bioavailability and phytotoxicity of heavy metals. Plant Soil 348:439–451

    Article  Google Scholar 

  • Kadian N, Gupta A, Satya S, Mehta RK, Malik A (2008) Biodegradation of herbicide (atrazine) in contaminated soil using various bioprocessed materials. Bioresour Technol 99:4642–4647

    Article  CAS  Google Scholar 

  • Karanasios E, Tsiropoulos NG, Karpouzas DG, Menkissoglu-Spiroudi U (2010) Novel biomixtures based on local Mediterranean lignocellulosic materials: evaluation for use in biobed systems. Chemosphere 80:914–921

    Article  CAS  Google Scholar 

  • Khan FI, Husain T, Hejazi R (2004) An overview and analysis of site remediation technologies. J Environ Manag 71:95–122

    Article  Google Scholar 

  • Khan S, Cao Q, Zheng YM, Huang YZ, Zhu YG (2008) Health risk of heavy metals in contaminated soils and food crops irrigated with waste water in Beijing, China. Environ Pollut 152:686–692

    Article  CAS  Google Scholar 

  • Lebrun JD, Trinsoutrot‐Gattin I, Laval K, Mougin C (2010) Insights into the development of fungal biomarkers for metal ecotoxicity assessment: case of Trametes versicolor exposed to copper. Environ Toxicol Chem 29:902–908

    Article  CAS  Google Scholar 

  • Lebrun JD, Trinsoutrot-Gattin I, Vinceslas-Akpa M, Bailleul C, Brault A, Mougin C, Laval K (2012) Assessing impacts of copper on soil enzyme activities in regard to their natural spatiotemporal variation under long-term different land uses. Soil Biol Biochem 49:150–156

    Article  CAS  Google Scholar 

  • Li JR, Xu YM (2015) Immobilization of Cd in a paddy soil using moisture management and amendment. Chemosphere 122:131–136

    Article  CAS  Google Scholar 

  • Li XJ, Li PJ, Lin X, Zhang CG, Li Q, Gong ZQ (2008) Biodegradation of aged polycyclic aromatic hydrocarbons (PAHs) by microbial consortia in soil and slurry phases. J Hazard Mater 150:21–26

    Article  CAS  Google Scholar 

  • Lin Q, Wang ZW, Ma S, Chen YX (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  CAS  Google Scholar 

  • Lin Q, Zhao HM, Chen YX (2007) Effects of 2,4-dichlorophenol, pentachlorophenol and vegetation on microbial characteristics in a heavy metal polluted soil. J Environ Sci Health B 42:551–557

    Article  CAS  Google Scholar 

  • Liu H, Guo S, Jiao K, Hou J, Xie H, 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 

  • Macleod I, Savage AL, Pahl O, Baird J (2008) Decline in microbial activity does not necessarily indicate an end to biodegradation in MSW-biowaste: a case study. Bioresour Technol 99:8626–8630

    Article  CAS  Google Scholar 

  • Maliszewska-Kordybach B, Smreczak B (2003) Habitat function of agricultural soils as affected by heavy metals and polycyclic aromatic hydrocarbons contamination. Environ Int 28:719–728

    Article  CAS  Google Scholar 

  • Maslin P, Maier RM (2010) Rhamnolipid-enhanced mineralization of phenanthrene in organic-metal co-contaminated soils. Bioremediat J 4:295–308

    Article  Google Scholar 

  • Medina E, Paredes C, Perez-Murcia MD, Bustamante MA, Moral R (2009) Spent mushroom substrates as component of growing media for germination and growth of horticultural plants. Bioresour Technol 100:4227–4232

    Article  CAS  Google Scholar 

  • Padmavathiamma PK, Li LY (2010) Phytoavailability and fractionation of lead and manganese in a contaminated soil after application of three amendments. Bioresour Technol 101:5667–5676

    Article  CAS  Google Scholar 

  • Pan J, Yu L (2011) Effects of Cd or/and Pb on soil enzyme activities and microbial community structure. Ecol Eng 37:1889–1894

    Article  Google Scholar 

  • Perez-Esteban J, Escolastico C, Masaguer A, Vargas C, Moliner A (2014) Soluble organic carbon and pH of organic amendments affect metal mobility and chemical speciation in mine soils. Chemosphere 103:164–171

    Article  CAS  Google Scholar 

  • Rauret G, Lopez-Sanchez JF, Sahuquillo A, Rubio R, Davidson C, Ure A, Quevauviller P (1999) Improvement of the BCR three step sequential extraction procedure prior to the certification of new sediment and soil reference materials. J Environ Monit 1:57–61

    Article  CAS  Google Scholar 

  • Ribas LCC, de Mendonca MM, Camelini CM, Soares CHL (2009) Use of spent mushroom substrates from Agaricus subrufescens (syn. A. blazei, A. brasiliensis) and Lentinula edodes productions in the enrichment of a soil-based potting media for lettuce (Lactuca sativa) cultivation: growth promotion and soil bioremediation. Bioresour Technol 100:4750–4757

    Article  CAS  Google Scholar 

  • Rijkenberg MJA, Depree CV (2010) Heavy metal stabilization in contaminated road-derived sediments. Sci Total Environ 408:1212–1220

    Article  CAS  Google Scholar 

  • Sun YB, Zhou QX, Xu YM, Wang L, Liang XF (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 

  • Tam NV, Wang CH (2015) Use of spent mushroom substrate and manure compost for honeydew melon seedlings. J Plant Growth Regul 34:417–424

    Article  Google Scholar 

  • Tapia Y, Cala V, Eymar E, Frutos I, Garate A, Masaguer A (2010) Chemical characterization and evaluation of composts as organic amendments for immobilizing cadmium. Bioresour Technol 101:5437–5443

    Article  CAS  Google Scholar 

  • Tuomela M, Oivanen P, Hatakka A (2002) Degradation of synthetic 14C-lignin by various white-rot fungi in soil. Soil Biol Biochem 34:1613–1620

    Article  CAS  Google Scholar 

  • van Gestel CAM (2008) Physico-chemical and biological parameters determine metal bioavailability in soils. Sci Total Environ 406:385–395

    Article  Google Scholar 

  • Wang YP, Li QB, Shi JY, Lin Q, Chen XC, Wu WX, Chen YX (2008) Assessment of microbial activity and bacterial community composition in the rhizosphere of a copper accumulator and a non-accumulator. Soil Biol Biochem 40:1167–1177

    Article  CAS  Google Scholar 

  • Wang L, Cui XF, Cheng HG, Chen F, Wang JT, Zhao XY, Lin CY, Pu X (2015) A review of soil cadmium contamination in China including a health risk assessment. Environ Sci Pollut Res 22:16441–16452

    Article  CAS  Google Scholar 

  • Wariishi H, Valli K, Gold MH (1992) Manganese(II) oxidation by manganese peroxidase from the basidiomycete Phanerochaete chrysosporium. Kinetic mechanism and role of chelators. J Biol Chem 267:23688–23695

    CAS  Google Scholar 

  • Wolfenden BS, Willson RL (1982) Radical cations as reference chromogens in studies of one-electron transfer reactions: pulse radio analysis studies of 2,2-Azinobis-(3-ethylbenzthiazoline-β-sulfonate). J Chem Soc Perkin Trans 2:805–812

    Article  Google Scholar 

  • Yao XH, Min H, Lu ZH, Yuan HP (2006) Influence of acetamiprid on soil enzymatic activities and respiration. Eur J Soil Biol 42:120–126

    Article  CAS  Google Scholar 

  • Zhang L, Sun XY (2014) Changes in physical, chemical, and microbiological properties during the two-stage co-composting of green waste with spent mushroom compost and biochar. Bioresour Technol 171:274–284

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was financially supported by the Science and Technology Support Program of Sichuan Province (2016NZ0050), Science and Technology Program for Public Wellbeing of Chengdu (2014-HM01-00163-SF), the Science and Technology Innovation Seedling Project of Sichuan Province (2015RZ0019), the National Science and Technology Supporting Program (2015BAD05B01-5), and the NSFC (No. J1103518). The authors also wish to thank Professor Guanglei Cheng and Dong Yu from Sichuan University for their technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Heng Xu.

Additional information

Responsible editor: Gabriele E. Schaumann

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jia, Z., Deng, J., Chen, N. et al. Bioremediation of cadmium-dichlorophen co-contaminated soil by spent Lentinus edodes substrate and its effects on microbial activity and biochemical properties of soil. J Soils Sediments 17, 315–325 (2017). https://doi.org/10.1007/s11368-016-1562-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-016-1562-7

Keywords

Navigation