Degradation of phthalic acid esters by the microbial consortium isolated from a contaminated soil

Document Type : Original Article

Authors

1 P.h.D in soil biology and biotechnology, University of Tehran, Karaj, Iran

2 Department of Soil Science Engineering, University of Tehran, Karaj, Iran

3 Professor, Department of Food Science, Engineering, and Technology, University of Tehran, Karaj, Iran.

Abstract

Phthalic acid esters are synthetic compounds used as emollients in polymer and plastic compounds. The entry of these compounds into the environment and the human food cycle and the development of a variety of cancers has raised global concerns. The purpose of this research was to investigate the concentration of phthalic acid esters (PAEs) in the soil exposed to the leachate (landfill) and finding a microbial consortium capable of the degradation of these pollutants. The concentration of phthalic acid esters in the soil was measured by the ultrasonic method and GC-MS. The results showed that the concentration of diethyl hexyl phthalate (DEHP) in soil (4.52 mg/Kg) was 6 times that of its international standard (0.7 mg/Kg). Microbial enrichment was performed in a mineral salt medium containing phthalic acid esters (30 o C and 120 rpm) and a microbial consortium capable of degrading phthalic acid esters was isolated. To investigate the biodegradation of phthalic acid esters by consortium, the residual phthalate concentration was extracted with ethyl acetate and measured by GC-MS. The results showed that the this consortium was able to degrade more than 96% of low molecular weight phthalates of dimethyl phthalate, diethyl phthalate and dibutyl phthalate (medium molecular weight phthalate) (30 o C and 120 rpm). In the case of DEHP (the world's most widely used plasticizer), the consortium was able to degrade it by 55% at 400 mg/L. Besides, phthalic acid esters separately were degraded almost completely by this consortium (5 days incubation, 30 oC, 120 rpm). Our results demonstrate the biodegradation of phthalic acid esters by this consortium and recommend its use for bioremediation of phthalates in contaminated soils.

Keywords

References

Amir S., Hafidi M., Merlina G., Hamdi H., Jouraiphy A., and El Gharous, M. 2005. Fate of phthalic acid esters during composting of both lagooning and activated sludges. Process Biochem, 40 (6): 2183–2190.
Benjamin S., Predeep S., Josh M. S., Kumar S. and Masai, E. 2015. A monograph on the remediation of hazardous phthalates. J Hazard Mater, 298: 58–72.
Boll M., Geiger R., Junghare M., and Schink, B. 2020. Microbial degradation of phthalates: biochemistry and environmental implications. Environ Microbiol Rep, 12(1):3-15.
Boonyaroj V., Chiemchaisri C., Chiemchaisri W., Theepharaksapan S., and Yamamoto, K., 2012. Toxic organic micro-pollutants removal mechanisms in long-term operated membrane bioreactor treating municipal solid waste leachate. Bioresour Technol, 113: 174–180.
Carter M. R., and Gregorich, E. G. 2008. Soil Sampling and Methods of Analysis. 2nd (Ed.) Canadian Society of Soil Science. 1224.
Chai C., Cheng H., Ge W., Ma D., and Shi, Y. 2014. Phthalic acid esters in soils from vegetable greenhouses in Shandong Peninsula, East China. PLoS One, 18:9 (4):e95701.
Chaler R., Cantón L., Vaquero M., and Grimalt, J.O. 2004. Identification and quantification of n-octyl esters of alkanoic and hexanedioic acids and phthalates as urban wastewater markers in biota and sediments from estuarine areas. J Chromatogr A, 1046 (1–2): 203-10.
Chen Q., Sun H.W., Wang B., and Hu G.C. 2004. Effects of di (2-ethylhexyl) phthalate (DEHP) on microorganisms and animals in soil. J AgroEnviron Sci, 23(6):1156–1159.
Chen H.L., Yao J., and Wang, F. 2013. Soil microbial and enzyme properties as affected by long-term exposure to phthalate esters. Adv Mater Res, 726: 3653–3656.
Clara M., Windhofer G., Hartl,W., Braun K., Simon M., and Gans O. 2010. Occurrence of phthalates in surface runoff, untreated and treated wastewater and fate during wastewater treatment. Chemosphere, 78 (9):1078-84.
Daiem M.M.A., Rivera-Utrilla J., Ocampo-Perez R., Mendez-Diaz J.D., and Sanchez-Polo M. 2012. Environmental impact of phthalic acid esters and their removal from water and sediments by different technologies — a review. J Environ Manage, 109: 164–178.
Deblonde T., Cossu-Leguille C., and Hartemann P. 2011. Emerging pollutants in wastewater: A review of the literature. Int J Hyg Environ Health, 214 (6): 442-448.
European Commission. 1999. Ban of phthalates in childcare articles and toys, press release IP/99/829 10 November.
Fu J., Pan F., Song S., Zhang L.R., Luo Y., Chen W., et al. 2013. Biodegradation of phthalic
acid esters in sewage sludge by composting with pig manure and rice straw. Environ Earth Sci, 68 (8): 2289–2299
Gao D.W. and Wen D.Z. 2016. Phthalate esters in the environment: A critical reviewof their occurrence, biodegradation, and removal during wastewater treatment processes. Sci Total Environ, 541:986–1001.
Giuliani, A., Zuccarini, M., Cichelli, A., Khan, H. and Reale, M. 2020. Critical review on the presence of phthalates in food and evidence of their biological impact. Int J Environ Res Public Health, 17 (5655): 1-45.
Guo Y., Han R., Du W.T., Wu J.Y., Liu W. and Cai X.D. 2010. Effects of combined phthalate acid ester contamination on soil micro-ecology. Res Environ Sci, 23(11): 1410–1414.
He L., Gielen G., Bolan N., Zhang X., Qin H., Huang H., and Wang H. 2015. Contamination and remediation of phthalic acid esters in agricultural soils in china: a review. Agron Sustain Dev, 35:519-534.
He Z., Xiao H., Lu T., Min H., and Lu, Z. 2013. Biodegradation of di-n-butyl phthalate by a stable bacterial consortium, HD-1, enriched from activated sludge. Bioresour Technol,  128: 526-532.
Heudorf U., Mersch-Sundermann V., and Angerer J. 2007 Phthalates: Toxicology and exposure. Int J Hyg Environ Health, 210 (5): 623.
Hu XY., Wen B., Zhang S., and Shan X.Q. 2005. Bioavailability of phthalate congeners to earthworms (Eisenia Fetida) in artificially contaminated soils. Ecotox Environ Safe, 62:26–34.
Jin D.C., Bai Z.H., Chang D.D., Hoefel D., Jin B., Wang P., et al. 2012. Biodegradation of din-butyl phthalate by an isolated Gordonia sp. strain QH-11: genetic identification and degradation kinetics. J Hazard Mater, 221: 80–85.
Jin D., Kong X., Li Y., Bai Z., Zhuang G., Zhuang X., and Deng Y. 2015. Biodegradation of di-n-Butyl Phthalate by Achromobacter sp. Isolated from Rural Domestic Wastewater. Int J Environ Res Public Health, 12: 13510-13522.
Julinová, and Slavík, R. 2012. Removal of phthalates from aqueous solution by different adsorbents: a short review. J Environ Manage, 94 (1):13–24.
Karimpour‑Fard, M. 2019. Rehabilitation of Saravan dumpsite in Rasht, Iran: geotechnical characterization of municipal solid waste. Int J Environ Sci Technol, 16 (8):4419-4436.
Kastner J., Cooper D.G., Marić M., Dodd P., and Yargeau, V. 2012. Aqueous leaching of di-2-ethylhexyl phthalate and “green” plasticizers from polyvinyl chloride. Sci Total Environ, 432: 357-64.
Li F., Liu Y., Wang D., Zhang C., Yang Z., Lu S., et al. 2018. Biodegradation of di-(2-ethylhexyl) phthalate by a halotolerant consortium LF. PLoS ONE, 13 (10): e0204324.
Liu W.L., Shen C.F., Zhang Z., Zhang C.B. 2009. Distribution of phthalate esters in soil of E-waste recycling sites from Taizhou city in China. Bull Environ Contam Toxicol, 82 (6): 665–667.
Ma T.T., Wu H. L., Chen L., Zhang H. B., Teng Y., and Luo, Y. M. 2015. Phthalate esters contamination in soils and vegetables of plastic film greenhouses of suburb Nanjing, China and the potential human health risk. Environ Sci Pollut Res, 22:12018–12028.
Net S., Delmont A., Sempéré R., Paluselli A., and Baghdad, O. 2015a. Occurrence, fate, behavior and ecotoxicological state of phthalates in different environmental matrices. Environ Sci and Technol, 49 (7): 4019-4035.
Net S., Delmont A., Sempéré R., Paluselli A., and Baghdad, O. 2015b. Reliable quantification of phthalates in environmental matrices (air, water, sludge, sediment and soil): A review. Sci Total Environ, 515-516:162-180.
Net S., Rabodonirina S., Sghaier R.B., Dumoulin D., Chbib C., Tlili I., and Ouddane B. 2015c. Distribution of phthalates, pesticides and drug residues in the dissolved, particulate and sedimentary phases from transboundary rivers (France–Belgium). Sci Total Environ, 521–522: 152–159.
Park M.A., Hwang K.A., Lee H.R., Yi B.R., Jeung E.B., and Choi K.C. 2012. Cell growth of BG-1 ovarian cancer cells is promoted by di-n-butyl phthalate and hexabromocyclododecane via upregulation of the cyclin D and cyclin-dependent kinase-4 genes. Mol Med Rep, 5(3): 761–766.
Planello R., Herrero O., Martinez-Guitarte J.L., and Morcillo G. 2011. Comparative effects of butyl benzyl phthalate (BBP) and di (2ethylhexyl) phthalate (DEHP) on the aquatic larvae of Chironomus riparius based on gene expression assays related to the endocrine system, the stress response and ribosomes. Aquat Toxicol, 105(1–2):62–70.
Pradeep S., Sarath M.K., Josh P., Binod R., Devi S., Balachandran S., Robin C.A. and Benjamin S. 2015. Achromobacter denitrificans strain SP1 efficiently remediates di (2-ethylhexyl) phthalate. Ecotoxicol Environ Safe, 112: 114–121.
Ren L., Jia Y., Ruth N., Qiao C., Wang J., Zhao B., and Yan Y. 2016. Biodegradation of phthalic acid esters by a newly isolated Mycobacterium sp. YC-RL4 and the bioprocess with environmental samples. Environ Sci Pollut Res, 23:16609–16619.
Shariatmadari N.  Askari Lasaki B., Eshghinezhad H., Alidoust P.  2018. Effects of landfill leachate on mechanical behaviour of adjacent soil: a case study of Saravan Landfill, Rasht, Iran. Int J Civi Eng, 16:1503–1513.
Sheikh I. A. and Beg M. A. 2019. Structural characterization of potential endocrine-disrupting activity of alternate plasticizers di-(2-ethylhexyl) adipate (DEHA), acetyl tributyl citrate (ATBC) and 2,2,4-trimethyl 1,3-pentanediol diisobutyrate (TPIB) with human sex hormone-binding globulin. Rep Toxicol, 83: 46–53.
Sparks D. L. 1996. Method of soil Analysis. Part3. Chemical Methods. American Society of Agronomy. 1390p.
Sun J.Q., Huang J., Zhang A.P., Liu W.P., and Cheng, W.W. 2013. Occurrence of phthalate esters in sediments in Qiantang River, China and inference with urbanization and river flow regime. J Hazard Mater, 248:142–149.
Tran T.M. and Kannan K. 2015. Occurrence of phthalate diesters in particulate and vapor phases in indoor air and implications for human exposure in Albany, New York, USA. Arch Environ Contam Toxicol, 68: 489–499.
Wang Y., Fan Y., and Gu J.D. 2004. Dimethyl phthalate ester degradation by two planktonic and immobilized bacterial consortia. Int Biodeterior Biodegrad, 53: 93–101.
Wang J., Lv S., Zhang M., Chen G., Zhu T., Zhang S., Teng Y., Christie P., and Luo Y. 2016 Effects of plastic film residues on occurrence of phthalates and microbial activity in soils. Chemosphere, 151:171-1777. 
Wang J., Jiang L.H., Zhou Y., and Ye B.C. 2017a. Enhanced biodegradation of di-n-butyl phthalate by Acinetobacter species strain LMB-5 coated with magnetic nanoparticles. Int Biodeter Biodegr, 116:184–190.
Wang Y., Li F., Ruan X., Song J., Lv L., Chai L., et al. 2017b. Biodegradation of di-n-butyl phthalate by bacterial consortium LV-1 enriched from river sludge. PLoS ONE, 12 (5): e0178213.
Wang H., Liang H., and Gao D. 2017c. Occurrence and distribution of phthalate esters (PAEs) in wetland sediments. J For Res, 28 (6):1241–1248.
Wen Z.D., Gao D.W., and Wu W.M. 2014. Biodegradation and kinetic analysis of phthalates by an Arthrobacter strain isolated from constructed wetland soil. Appl Microbiol Biotechnol, 98:4683–4690.
Wu X.L., Liang R.X., Dai Q.Y., Jin D.C., Wang Y.Y., and Chao W.L. 2010. Complete degradation of di-n-octyl phthalate by biochemical cooperation between Gordonia sp. strain JDC-2 and Arthrobacter sp. strain JDC-32 isolated from activated sludge. J Hazard Mater, 176 (1–3): 262–268.
Wu X.L., Wang Y.Y., Liang R.X., Dai Q.Y., Jin D.C. and Chao W.L. 2011. Biodegradation of an endocrine-disrupting chemical di-n-butyl phthalate by newly isolated Agrobacterium sp. and the biochemical pathway. Process Biochem, 46 (5):1090–1094.
Xu, W., You, Y., Wang, Z., Chen, W., Zeng, J, Zhao, X. and & Su, Y. 2018. Dibutyl phthalate alters the metabolic pathways of microbes in black soils. Sci Rep, 8 (2605): 1-13.
Zeng F., Wen J., Cui K., Wu L., Liu M., Li Y., et al. 2009. Seasonal distribution of phthalate esters in surface water of the urban lakes in the subtropical city, Guangzhou, China. J Hazard Mater, 169 (1-3): 719-725.
Zhao H.M., Du H., Lin J., Chen X.B., Li Y.W., Li H., Cai Q.Y., Mo C.H., Qin H.M., and Wong, M.H. 2016. Complete degradation of the endocrine disruptor di-(2-ethylhexyl) phthalate by a novel Agromyces sp. MT-O strain and its application to bioremediation of contaminated soil. Sci Total Environ, 562: 170–178.
Zhao H.M., Hu R.W., Chen X.X., Chen X.B., Lü H., Li Y.W., Li H., Mo C.H., Cai Q.Y. Wong M.H. 2018. Biodegradation pathway of di-(2-ethylhexyl) phthalate by a novel Rhodococcus pyridinivorans XB and its bioaugmentation for remediation of DEHP contaminated soil. Sci Total Environ, 640 (641):1121-1131.
Applied Soil Research
Volume 10, Issue 2 - Serial Number 2
September 2022
Pages 1-13

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History

  • Receive Date: 18 January 2021
  • Revise Date: 02 May 2021
  • Accept Date: 03 May 2021

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