The objective of this study was to investigate whether spent mushroom substrate (SMS) amendment was an appropriate way to reduce di(2-ehylhexyl) phthalate (DEHP) and di-n-butyl phthalate (DnBP) contents in soil and whether SMS could reduce DnBP accumulation in bok choy (Brassica rapa subsp. chinensis).
Materials and methods
Microcosm and pot experiments were carried out to study the influence of spent Agaricus bisporus substrate application on DnBP and DEHP dissipation in soils and plant uptake of DnBP. Variations in soil pH and enzyme activities were determined. The concentrations of phthalate esters (PAEs) in soils, bok choy, and atmosphere were examined with gas chromatography or gas chromatography–mass spectrometry.
Results and discussion
Adding sterilized or non-sterilized SMS can increase soil pH and urease activity, and non-sterilized SMS can promote soil laccase activity. The results show that the dissipation of DEHP is accelerated after incubation with SMS for 25 days; however, little effect can be found with continuing incubation due to low DEHP bioavailability. In this research, SMS amendment exhibits no effect on DnBP dissipation in soils and DnBP accumulation in bok choy. It was proposed that atmospheric deposition of DnBP might be the main source of DnBP in bok choy in the study, since equivalent amounts of DnBP were detected in the vegetables grown in soils with or without DnBP spiking.
This study indicates that the application of SMS as an organic fertilizer is less likely to affect the fate of PAEs in soils, and proper strategies should be conducted to reduce PAE levels in atmosphere to control PAE contamination in vegetables.
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Ahuactzin-Pérez M, Tlecuitl-Beristain S, García-Dávila J, González-Pérez M, Gutiérrez-Ruíz MC, Sánchez C (2016) Degradation of di (2-ethyl hexyl) phthalate by Fusarium culmorum: kinetics, enzymatic activities and biodegradation pathway based on quantum chemical modeling pathway based on quantum chemical modeling. Sci Total Environ 566:1186–1193. https://doi.org/10.1016/j.scitotenv.2016.05.169
Bourbonnais R, Paice MG (1990) Oxidation of non-phenolic substrates: an expanded role for laccase in lignin biodegradation. FEBS Lett 267:99–102
Cai QY, Mo CH, Zeng QY, QT W, Férard JF, Antizar-Ladislao B (2008) Potential of Ipomoea aquatica cultivars in phytoremediation of soils contaminated with di-n-butyl phthalate. Environ Exp Bot 62(3):205–211. https://doi.org/10.1016/j.envexpbot.2007.08.005
Cartwright CD, Thompson IP, Burns RG (2000) Degradation and impact of phthalate plasticizers on soil microbial communities. Environ Toxicol Chem 19(5):1253–1126. https://doi.org/10.1002/etc.5620190506
Chang BV, Yang CM, Cheng CH, Yuan SY (2004) Biodegradation of phthalate esters by two bacteria strains. Chemosphere 55(4):533–538. https://doi.org/10.1016/j.chemosphere.2003.11.057
Chatterjee S, Dutta TK (2008) Complete degradation of butyl benzyl phthalate by a defined bacterial consortium: role of individual isolates in the assimilation pathway. Chemosphere 70(5):933–941. https://doi.org/10.1016/j.chemosphere.2007.06.058
Chen H, Zhuang R, Yao J, Wang F, Qian Y (2013) A comparative study on the impact of phthalate esters on soil microbial activity. B Environ Contam Tox 91(2):217–223. https://doi.org/10.1007/s00128-013-1033-4
Chen N, Shuai W, Hao X, Zhang H, Zhou D, Gao J (2017) Contamination of phthalate esters in vegetable agriculture and human cumulative risk assessment. Pedosphere 27(3):439–451. https://doi.org/10.1016/S1002-0160(17)60340-0
Chiu SW, Gao T, Chan CSS, Ho CKM (2009) Removal of spilled petroleum in industrial soils by spent compost of mushroom Pleurotus pulmonarius. Chemosphere 75(6):837–842. https://doi.org/10.1016/j.chemosphere.2008.12.044
Dueck TA, Van Dijk CJ, David F, Scholz N, Vanwalleghem F (2003) Chronic effects of vapour phase di-n-butyl phthalate (DBP) on six plant species. Chemosphere 53(8):911–920. https://doi.org/10.1016/S0045-6535(03)00580-0
Engelhardt G, Wallnofer PR (1978) Metabolism of di-normal-butyl phthalate and mono-normal-butyl phthalate by soil bacteria. Appl Environ Microbiol 35(2):243–246
Frutos I, García-Delgado C, Cala V, Gárate A, Eymar E (2017) The use of spent mushroom compost to enhance the ability of Atriplex halimus to phytoremediate contaminated mine soils. Environ Technol 38(9):1075–1084. https://doi.org/10.1080/09593330.2016.1217938
Gao W, Liang J, Pizzul L, Feng XM, Zhang K, del Pilar Castillo M (2015) Evaluation of spent mushroom substrate as substitute of peat in Chinese biobeds. Int Biodeterior Biodegrad 98:107–112
García-Delgado C, D’Annibale A, Pesciaroli L, Yunta F, Crognale S, Petruccioli M, Eymar M (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. https://doi.org/10.1016/j.scitotenv.2014.11.046
Gómez-Hens A, Aguilar-Caballos MP (2003) Social and economic interest in the control of phthalic acid esters. TrAC Trends Anal Chem 22(11):847–857. https://doi.org/10.1016/S0165-9936(03)01201-9
Guo M, Chorover J (2006) Leachate migration from spent mushroom substrate through intact and repacked subsurface soil columns. Waste Manag 26(2):133–140. https://doi.org/10.1016/j.wasman.2004.12.024
Guo D, Wu Y (2011) Determination of phthalic acid esters of soil in south of Xinjiang cotton fields. Arid Environ Monit 25:76–79
He L, Gielen G, Bolan NS, Zhang X, Qin H, Huang H, Wang H (2015) Contamination and remediation of phthalic acid esters in agricultural soils in China: a review. Agron Sustain Dev 35:519–534
He L, Fan S, Müller K, Hu G, Huang H, Zhang X, Li X, Che L, Wang H (2016) Biochar reduces the bioavailability of di-(2-ethylhexyl) phthalate in soil. Chemosphere 142:24–27
Hwang SS, Kim HY, Ka JO, Ka HG (2012) Changes in the activities of enzymes involved in the degradation of butylbenzyl phthalate by Pleurotus ostreatus. J Microbiol Biotechnol 22(2):239–243. https://doi.org/10.4014/jmb.1107.07050
Jia Z, Deng J, Chen N, Shi W, Tang X, Xu H (2017) 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 Sediment 17:315–325
de Jonge H, de Jonge LW, Blicherb BW, Moldrup P (2002) Transport of di(2-ethylhexyl)phthalate (DEHP) applied with sewage sludge to undisturbed and repacked soil columns. J Environ Qual 31(6):1963–1971. https://doi.org/10.2134/jeq2002.1963
Jordan SN, Holland LB, Linnane SU (2012) Spent mushroom compost management and options for use. Environmental Protection Agency STRIVE Report Series No 74 http://wwwepaie/pubs/reports/research/waste/strivereport74html. Assessed 18 July 2015
Kandeler E, Gerber H (1988) Short-term assay of soil urease activity using colorimetric determination of ammonium. Biol Fertil Soils 6:68–72
Kästner M, Miltner A (2016) Application of compost for effective bioremediation of organic contaminants and pollutants in soil. Appl Microbiol Biotechnol 100(8):3433–3449. https://doi.org/10.1007/s00253-016-7378-y
Kim Y, Yeo S, Song HG, Choi HT (2008) Enhanced expression of laccase during the degradation of endocrine disrupting chemicals in Trametes versicolor. Microbiology 46:402–407
Li X, Wu Y, Lin X, Zhang J, Zeng J (2012) Dissipation of polycyclic aromatic hydrocarbons (PAHs) in soil microcosms amended with mushroom cultivation substrate. Soil Biol Biochem 47:191–197. https://doi.org/10.1016/j.soilbio.2012.01.001
Li C, Chen J, Wang J, Han P, Luan Y, Ma X, Lu A (2016) Phthalate esters in soil, plastic film, and vegetable from greenhouse vegetable production bases in Beijing, China: concentrations, sources, and risk assessment. Sci Total Environ 568:1037–1043. https://doi.org/10.1016/j.scitotenv.2016.06.077
Ling W, Ren L, Gao Y, Zhu X, Sun B (2009) Impact of low-molecular-weight organic acids on the availability of phenanthrene and pyrene in soil. Soil Biol Biochem 41(10):2187–2195. https://doi.org/10.1016/j.soilbio.2009.08.003
Liu H, Liang H, Liang Y, Zhang D, Wang C, Cai H, Shvartsev SL (2010) Distribution of phthalate esters in alluvial sediment: a case study at JiangHan Plain, Central China. Chemosphere 78(4):382–388. https://doi.org/10.1016/j.chemosphere.2009.11.009
Marín-Benito JM, Andrades MS, Sánchez-Martín MJ, Rodríguez-Cruz MS (2012) Dissipation of fungicides in a vineyard soil amended with different spent mushroom substrates. J Agric Food Chem 60(28):6936–6945. https://doi.org/10.1021/jf301322h
Net S, Sempéré R, Delmont A, Paluselli A, Ouddane B (2015) Occurrence, fate, behavior and ecotoxicological state of phthalates in different environmental matrices. Environ Sci Technol 49(7):4019–4035. https://doi.org/10.1021/es505233b
Richards DJ, Shieh WK (1986) Biological fate of organic priority pollutants in the aquatic environment. Water Res 20(9):1077–1090. https://doi.org/10.1016/0043-1354(86)90054-0
Rousk J, Brookes PC, Bååth E (2009) Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization. Appl Environ Microbiol 75(6):1589–1596. https://doi.org/10.1128/AEM.02775-08
Scotti R, Bonanomi G, Scelza R, Zoina A, Rao MA (2015) Organic amendments as sustainable tool to recovery fertility in intensive agricultural systems. J Soil Sci Plant Nutr 15:333–352
Sharma M, Maloo S (2005) Assessment of ambient air PM10 and PM2.5 and characterization of PM10 in the city of Kanpur, India. Atmos Environ 39(33):6015–6026. https://doi.org/10.1016/j.atmosenv.2005.04.041
Swan SH (2008) Environmental phthalate exposure in relation to reproductive outcomes and other health endpoints in humans. Environ Res 108(2):177–184. https://doi.org/10.1016/j.envres.2008.08.007
Walsh G, Grogan H, Kellegher T, Plunkett M, Lalor S (2013) Spent mushroom compost–nutrient content for application to agricultural crops. Teagasc Technol Updates Project No 6355. http://www.teagasc.ie/publications/. Accessed 18 July 2015
Wang JL, Chen LJ, Shi HC, Qian Y (2000) Microbial degradation of phthalic acid esters under anaerobic digestion of sludge. Chemosphere 41:1245–1248
Wang JW, QZ D, Song YQ (2010) Concentration and risk assessment of DEHP in vegetables around plastic industrial area. Chin J Environ Sci 31:2450–2455
Wang L, Xu X, Lu X (2015) Phthalic acid esters (PAEs) in vegetable soil from the suburbs of Xianyang city, Northwest China. Environ Earth Sci 74(2):1487–1496. https://doi.org/10.1007/s12665-015-4141-0
Wang Z, Liu S, Xu W, Hu Y, Hu Y, Zhang Y (2016) The microbiome and functions of black soils are altered by dibutyl phthalate contamination. Appl Soil Ecol 99:51–61. https://doi.org/10.1016/j.apsoil.2015.11.024
Wittassek M, Koch HM, Angerer J, Brüning T (2011) Assessing exposure to phthalates—the human biomonitoring approach. Mol Nutr Food Res 55(1):7–31. https://doi.org/10.1002/mnfr.201000121
Xu G, Li F, Wang Q (2008) Occurrence and degradation characteristics of dibutyl phthalate (DBP) and di-(2-ethylhexyl) phthalate (DEHP) in typical agricultural soils of China. Sci Total Environ 393(2-3):333–340. https://doi.org/10.1016/j.scitotenv.2008.01.001
Yang F, Wang M, Wang Z (2013) Sorption behavior of 17 phthalic acid esters on three soils: effects of pH and dissolved organic matter, sorption coefficient measurement and QSPR study. Chemosphere 93:82–89
Zeng QY, Mo CH, Cai QY, QT W (2006) Possible pathways through which phthalic acid esters (PAEs) are accumulated in radish plants (Raphanus Sativus). Acta Scientiae Circumstantiae 26:10–16
Zhang X, Wang H, He L, Lu K, Sarmah A, Li J, Bolan NS, Pei J, Huang H (2013) Using biochar for remediation of soils contaminated with heavy metals and organic pollutants. Environ Sci Pollut Res 20(12):8472–8483. https://doi.org/10.1007/s11356-013-1659-0
Zhang T, Zhou CY, Chen SS, Zhou JX, Bai B (2017) Accumulation and metabolism of phthalates in Brassica campestris ssp. chinensis Makino. Acta Agricultureae Shanghai 33:86–90
Zhao HM, Du H, Feng NX, Xiang L, Li YW, Li H, Cai QY, Mo CH (2016) Biodegradation of di-n-butylphthalate and phthalic acid by a novel Providencia sp. 2D and its stimulation in a compost-amended soil. Biol Fertil Soils 52:65–76
This research was funded by the National Key Basic Research Program of China (No. 2014CB441105), the National Natural Science Foundation of China (No. 21377136), the Research Instrument Development Program of the Chinese Academy of Sciences (YZ201638), and the 135 Research Program of the Chinese Academy of Sciences.
Responsible editor: Kitae Baek
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Zhu, F., Zhu, C., Chen, N. et al. Will spent mushroom substrate application affect the dissipation and plant uptake of phthalate esters?. J Soils Sediments 18, 1579–1589 (2018). https://doi.org/10.1007/s11368-017-1876-0
- Phthalate ester
- Spent mushroom substrate