Advertisement

Environmental Science and Pollution Research

, Volume 25, Issue 32, pp 31895–31905 | Cite as

Combined treatment of contaminated soil with a bacterial Stenotrophomonas strain DXZ9 and ryegrass (Lolium perenne) enhances DDT and DDE remediation

  • Hui XieEmail author
  • Lusheng ZhuEmail author
  • Jun Wang
13th IHPA Forum and selected studies on POPs

Abstract

Bioremediation of contaminated soils by a combinational approach using specific bacterial species together with ryegrass is a promising strategy, resulting in potentially highly efficient degradation of organic contaminants. The present study tested the combination of strain DXZ9 of Stenotrophomonas sp. with ryegrass to remove DDT and DDE contaminants from soil under natural conditions in a pot experiment. The strain DXZ9 was successfully colonized in the natural soil, resulting in removal rates of approximately 77% for DDT, 52% for DDE, and 65% for the two pollutants combined after 210 days. Treatment with ryegrass alone resulted in slightly lower removal rates (72 and 48%, respectively, 61% for both combined), while the combination of strain DXZ9 and ryegrass significantly (p < 0.05) improved the removal rates to 81% for DDT and 55% for DDE (69% for both). The half-life of the contaminants was significantly shorter in combined treatment with DXZ9 and ryegrass compared to the control. The remediation was mostly due to degradation of the contaminants, as the net uptake of DDT and DDE by the ryegrass accounted for less than 3% of the total amount in the soil. DDT is reductively dechlorinated to DDD and dehydrochlorinated to DDE in the soil; the metabolites of DDE and DDD were multiple undefined substances. The toxicity of the soil was significantly reduced as a result of the treatment. The present study demonstrates that the bioremediation of soil contaminated with DDT and DDE by means of specific bacteria combined with ryegrass is feasible.

Keywords

Bioremediation DDT and DDE contaminated soil Stenotrophomonas sp. Ryegrass Soil detoxification 

Notes

Funding information

This study was supported by grants from the National Natural Science Foundation of China (No. 41671321) and National Key Research and Development Project of China (2016YFD0800304).

Compliance with ethical standards

Conflict of interests

The authors declare that they have no conflict of interest.

References

  1. Abhilash PC, Srivastava S, Singh N (2011) Comparative bioremediation potential of four rhizospheric microbial species against lindane. Chemosphere 82(1):56–63.  https://doi.org/10.1016/j.chemosphere.2010.10.009 CrossRefGoogle Scholar
  2. Ahmad F, Iqbal S, Anwar S, Afzal M, Islam E, Mustafa T, Khan QM (2012) Enhanced remediation of chlorpyrifos from soil using ryegrass (Lollium multiflorum) and chlorpyrifos-degrading bacterium Bacillus pumilus C2A1. J Hazard Mater 237-238:110–115.  https://doi.org/10.1016/j.jhazmat.2012.08.006 CrossRefGoogle Scholar
  3. Anderson TA, Guthrie EA, Walton BT (1993) Bioremediation in the rhizosphere. Environ Sci Technol 27(13):2630–2636.  https://doi.org/10.1021/es00049a001 CrossRefGoogle Scholar
  4. Arshad M, Hussain S, Saleem M (2008) Optimization of environmental parameters for biodegradation of alpha and beta endosulfan in soil slurry by Pseudomonas aeruginosa. J Appl Microbiol 104(2):364–370.  https://doi.org/10.1111/j.1365-2672.2007.03561.x CrossRefGoogle Scholar
  5. Bhalerao TS (2012) Bioremediation of endosulfan-contaminated soil by using bioaugmentation treatment of fungal inoculant Aspergillus niger. Turk J Biol 36:561–567Google Scholar
  6. Böltner D, Godoy P, Muñoz-Rojas J, Duque E, Moreno-Morillas S, Sánchez L, Ramos JL (2008) Rhizoremediation of lindane by root-colonizing Sphingomonas. Microb Biotechnol 1(1):87–93.  https://doi.org/10.1111/j.1751-7915.2007.00004.x CrossRefGoogle Scholar
  7. Cao X, Yang C, Liu R, Li Q, Zhang W, Liu J, Song C, Qiao C, Mulchandani A (2013) Simultaneous degradation of organophosphate and organochlorine pesticides by Sphingobium japonicum UT26 with surface-displayed organophosphorus hydrolase. Biodegradation 24(2):295–303.  https://doi.org/10.1007/s10532-012-9587-0 CrossRefGoogle Scholar
  8. Chattopadhyay S, Chattopadhyay D (2015) Remediation of DDT and its metabolites in contaminated sediment. Curr Pollut Rep 1(4):248–264.  https://doi.org/10.1007/s40726-015-0023-z CrossRefGoogle Scholar
  9. Comeau Y, Greer CW, Samson R (1993) Role of inoculum preparation and density on the bioremediation of 2,4-D contaminated soil by bioagumentation. Appl Microbiol Technol 38:681–6872Google Scholar
  10. Cycoń M, Piotrowska-Seget Z (2016) Pyrethroid-degrading microorganisms and their potential for the bioremediation of contaminated soils: a review. Front Microbiol 7:1463Google Scholar
  11. Cycoń M, Mrozik A, Piotrowska-Seget Z (2017) Bioaugmentation as a strategy for the remediation of pesticide-polluted soil: a review. Chemosphere 172:52–71.  https://doi.org/10.1016/j.chemosphere.2016.12.129 CrossRefGoogle Scholar
  12. Ding N, Xu JM, Schwab P (2013) Accumulation and transformation of PCBs in ryegrass (Lolium multiflorum L.). Functions of Natural Organic Matter in Changing Environment 637–640Google Scholar
  13. Duquenne P, Parekh NR, Gatroux G, Fournier JC (1996) Effect of inoculant density, formulation, dispersion and soil nutrient amendment on the removal of carbofuran residues from contaminated soils. Soil Biol Biochem 28:1805–1811CrossRefGoogle Scholar
  14. Fan B, Zhao YC, Mo GH, Ma WJ, Wu JQ (2013) Co-remediation of DDT-contaminated soil using white rot fungi and laccase extract from white rot fungi. J Soil Sediment 13(7):1232–1245.  https://doi.org/10.1007/s11368-013-0705-3 CrossRefGoogle Scholar
  15. Fang H, Dong B, Yan H, Tang FF, Yu YL (2010) Characterization of a bacterial strain capable of degrading DDT congeners and its use in bioremediation of contaminated soil. J Hazard Mater 184(1-3):281–289.  https://doi.org/10.1016/j.jhazmat.2010.08.034 CrossRefGoogle Scholar
  16. Fu DQ, Teng Y, Shen YY, Sun MM, Tu C, Luo YM, Li ZG, Christie P (2011) Dissipation of polycyclic aromatic hydrocarbons and microbial activity in a field soil planted with perennial ryegrass. Front Env Sci Eng 6(3):330–335CrossRefGoogle Scholar
  17. Fuentes MS, Sáez JM, Benimeli CS, Amoroso MJ (2011) Lindane biodegradation by defined consortia of indigenous Streptomyces strains. Water Air Soil Pollut 222(1-4):217–231.  https://doi.org/10.1007/s11270-011-0818-5 CrossRefGoogle Scholar
  18. Gandolfi I, Sicolo M, Franzetti A, Fontanarosa E, Santagostino A, Bestetti G (2010) Influence of compost amendment on microbial community and ecotoxicity of hydrocarbon-contaminated soils. Bioresour Technol 101(2):568–575.  https://doi.org/10.1016/j.biortech.2009.08.095 CrossRefGoogle Scholar
  19. Gang Ji WD, Xia ZL (1985) Pesticide of soil and water. Science Press, Beijing, p 156Google Scholar
  20. Gao C, Jin X, Ren J, Fang H, Yu Y (2015) Bioaugmentation of DDT-contaminated soil by dissemination of the catabolic plasmid pDOD. J Environ Sci 27:42–50.  https://doi.org/10.1016/j.jes.2014.05.045 CrossRefGoogle Scholar
  21. Hong Q, Zhang Z, Hong Y, Li S (2007) A microcosm study on bioremediation of fenitrothion-contaminated soil using Burkholderia sp. FDS-1. Int Biodeterior Biodegr 59(1):55–61.  https://doi.org/10.1016/j.ibiod.2006.07.013 CrossRefGoogle Scholar
  22. Huang XD, El-Alawi Y, Penrose DM, Glick BR, Greenberg BM (2004) Responses of three grass species to creosote during phytoremediation. Environ Pollut 130(3):453–463.  https://doi.org/10.1016/j.envpol.2003.12.018 CrossRefGoogle Scholar
  23. Huang H, Yu N, Wang L, Gupta D, He Z, 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(23):11034–11038.  https://doi.org/10.1016/j.biortech.2011.09.067 CrossRefGoogle Scholar
  24. Karpouzas DG, Walker A (2000) Factors influencing the ability of Pseudomonas putida epI to degrade ethoprophos in soil. Soil Biol Biochem 32(11-12):1753–1762.  https://doi.org/10.1016/S0038-0717(00)00093-6 CrossRefGoogle Scholar
  25. Kataoka R, Takagi K, Sakakibara F (2011) Biodegradation of endosulfan by Mortieralla sp. strain W8 in soil: influence of different substrates on biodegradation. Chemosphere 85(3):548–552.  https://doi.org/10.1016/j.chemosphere.2011.08.021 CrossRefGoogle Scholar
  26. Khan MI, Cheema SA, Tang XJ, Shen CF, Sahi ST, Jabbar A, Park J, Chen YX (2012) Biotoxicity assessment of pyrene in soil using a battery of biological assays. Arch Environ Contam Toxicol 63(4):503–512.  https://doi.org/10.1007/s00244-012-9793-0 CrossRefGoogle Scholar
  27. Kong LF (2013)Isolation of endosulfan degrading bacteria and its detoxification of endosulfan contaminated soil, Shandong Agricultural University, M.S. Thesis 51–56 (In Chinese) Google Scholar
  28. Kong LF, Zhu SY, Zhu LS, Wei K, Yan TX, Wang J, Wang JH, Wang FH, Sun FX (2014) Colonization of Alcaligenes faecalis strain JBW4 in natural soils and its detoxification of endosulfan. Appl Microbiol Biotechnol 98(3):1407–1416.  https://doi.org/10.1007/s00253-013-5033-4 CrossRefGoogle Scholar
  29. Li WM, Wang DS, Hu F, Li HX, Ma LL, Xu L (2016) Exogenous IAA treatment enhances phytoremediation of soil contaminated with phenanthrene by promoting soil enzyme activity and increasing microbial biomass. Environ Sci Pollut Res 11(23):10656–10664CrossRefGoogle Scholar
  30. Lu M, Zhang ZZ (2014) Phytoremediation of soil co-contaminated with heavy metals and deca-BDE by co-planting of Sedum alfredii with tall fescue associated with Bacillus cereus JP12. Plant Soil 382(1-2):89–102.  https://doi.org/10.1007/s11104-014-2147-0 CrossRefGoogle Scholar
  31. Ma J, Pan LB, Yang XY, Liu XL, Tao SY, Zhao L, Qin XP, Sun ZJ, Hou H, Zhou YZ (2016) DDT, DDD, and DDE in soil of Xiangfen County, China: residues, sources, spatial distribution, and health risks. Chemosphere 163:578–583.  https://doi.org/10.1016/j.chemosphere.2016.08.050 CrossRefGoogle Scholar
  32. Meng L, Qiao M, Arp HPH (2011) Phytoremediation efficiency of a PAH-contaminated industrial soil using ryegrass, white clover, and celery as mono- and mixed cultures. J Soils Sediments 11(3):482–490.  https://doi.org/10.1007/s11368-010-0319-y CrossRefGoogle Scholar
  33. Mitton FM, Gonzalez M, Pena A, Miglioranza Karina SB (2012) Effects of amendments on soil availability and phytoremediation potential of aged p,p′-DDT, p,p′-DDE and p,p′-DDD residues by willow plants (Salix sp.) J Hazard Mater 203-204:62–68.  https://doi.org/10.1016/j.jhazmat.2011.11.080 CrossRefGoogle Scholar
  34. Miyazaki R, Sato Y, Ito M, Ohtsubo Y, Nagata Y, Tsuda M (2006) Complete nucleotide sequence of an exogenously isolated plasmid pLB1, involved in gamma-hexachlorocyclohexane degradation. Appl Environ Microbiol 72(11):6923–6933.  https://doi.org/10.1128/AEM.01531-06 CrossRefGoogle Scholar
  35. Moubashera HA, Hegazya AK, Mohamedc NH, Moustafac YM, Kabiela HF, Hamada AA (2015) Phytoremediation of soils polluted with crude petroleum oil using Bassia scoparia and its associated rhizosphere microorganisms. Int Biodeterior Biodegrad 98:113–120.  https://doi.org/10.1016/j.ibiod.2014.11.019 CrossRefGoogle Scholar
  36. Odukkathil G, Vasudevan N (2016) Residues of endosulfan in surface and subsurface agricultural soil and its bioremediation. J Environ Manag 65:72–80CrossRefGoogle Scholar
  37. Purnomo AS, Mori T, Takagi K, Kondo R (2011) Bioremediation of DDT contaminated soil using brown-rot fungi. Int Biodeterior Biodegrad 65(5):691–695.  https://doi.org/10.1016/j.ibiod.2011.04.004 CrossRefGoogle Scholar
  38. Qiu XH, Zhu T, Li PHS, Li QL, Miao GF, Gong JC (2004) Organochlorine pesticides in the air around Taihu Lake, china. Environ Sci Technol 38(5):1368–1374.  https://doi.org/10.1021/es035052d CrossRefGoogle Scholar
  39. Qiu XH, Zhu T, Yao B (2005) Contribution of Dicofol to the current DDT pollution in China. Environ Sci Technol 39(12):4385–4390.  https://doi.org/10.1021/es050342a CrossRefGoogle Scholar
  40. Quensen Iii JF, Mueller SA, Jain MK, Tiedje JM (1998) Reductive dechlorination of DDE to DDMU in marine sediment microcosms. Science 280(5364):722–724.  https://doi.org/10.1126/science.280.5364.722 CrossRefGoogle Scholar
  41. Quensen Iii JF, Tiedje JM, Jain MK, Mueller SA (2001) Factors controlling the proportion of DDE dechlorination to DDMU in Palos Verdes margin sediments under anaerobic conditions. Environ Sci Technol 35(2):286–291.  https://doi.org/10.1021/es0012873 CrossRefGoogle Scholar
  42. Queyrel W, Habets F, Blanchoud H, Ripoche D, Launay M (2016) Pesticide fate modeling in soils with the crop model STICS: feasibility for assessment of agricultural practices. Sci Total Environ 542(Pt A):787–802.  https://doi.org/10.1016/j.scitotenv.2015.10.066 CrossRefGoogle Scholar
  43. Ramadan MA, EL-Tayeb OM, Alexander M (1990) Inoculum size as a factor limiting success of inoculation for biodegradation. Appl Environ Microbiol 56:1392–1396Google Scholar
  44. Raina V, Suar M, Singh A, Prakash O, Dadhwal M, Gupta SK, Dogra C, Lawlor K, Lal S, van der Meer JR, Hollinger C, Lal R (2008) Enhanced biodegradation of hexachlorocyclohexane (HCH) in contaminated soils via inoculation with Sphingobium indicum B90A. Biodegradation 19(1):27–40.  https://doi.org/10.1007/s10532-007-9112-z CrossRefGoogle Scholar
  45. Rostamia S, Azhdarpoorb A, Rostamic M, Samaei MR (2016) The effects of simultaneous application of plant growth regulators and bioaugmentation on improvement of phytoremediation of pyrene contaminated soils. Chemosphere 161:219–223.  https://doi.org/10.1016/j.chemosphere.2016.07.026 CrossRefGoogle Scholar
  46. Sáez JM, Benimelli CS, Amorosso MJ (2012) Lindane removal by pure and mixed cultures of immobilized actinobacteria. Chemosphere 89(8):982–987.  https://doi.org/10.1016/j.chemosphere.2012.06.057 CrossRefGoogle Scholar
  47. Sayles GD, You G, Wang M, Kupferle MJ (1997) DDT, DDD, and DDE dechlorination by zero-valent iron. Environ Sci Technol 31(12):3448–3454.  https://doi.org/10.1021/es9701669 CrossRefGoogle Scholar
  48. Shen CF, Chen YX, Huang SB (2009) Dioxin-like compounds in agricultural soils near e-waste recycling sites from Taizhou area, China: chemical and bioanalytical characterization. Environ Int 35(1):50–55.  https://doi.org/10.1016/j.envint.2008.07.005 CrossRefGoogle Scholar
  49. Shi YJ, Zhang QB, Huang DQ, Zheng XQ, Shi YJ (2016) Survival, growth, detoxifying and antioxidative responses of earthworms (Eisenia fetida) exposed to soils with industrial DDT contamination. Pestic Biochem Physiol 128:22–29.  https://doi.org/10.1016/j.pestbp.2015.10.009 CrossRefGoogle Scholar
  50. Singh BK, Walker A, Wright DJ (2006) Bioremedial potential of fenamiphos and chlorpyrifos degrading isolates: influence of different environmental conditions. Soil Biol Biochem 38(9):2682–2693.  https://doi.org/10.1016/j.soilbio.2006.04.019 CrossRefGoogle Scholar
  51. Song Y, Zhu LS, Wang J, Wang JH, Liu W, Xie H (2009) DNA damage and effects on antioxidative enzymes in earthworm (Eisenia foetida) induced by atrazine. Soil Biol Biochem 41(5):905–909.  https://doi.org/10.1016/j.soilbio.2008.09.009 CrossRefGoogle Scholar
  52. Sudharshan S, Naidu R, Mallavarapu M, Bolan N (2012) DDT remediation in contaminated soils: a review of recent studies. Biodegradation 23(6):851–863.  https://doi.org/10.1007/s10532-012-9575-4 CrossRefGoogle Scholar
  53. Sun GD, Zhang X, Hu Q, Zhang HQ, Zhang DY, Li GH (2015) Biodegradation of dichlorodiphenyltrichloroethanes (DDTs) and hexachlorocyclohexanes (HCHs) with plant and nutrients and their effects on the microbial ecological kinetics. Microb Ecol 69(2):281–292.  https://doi.org/10.1007/s00248-014-0489-z CrossRefGoogle Scholar
  54. Tang JC, Wang RG, Niu XW, Zhou QX (2010) Enhancement of soil petroleum remediation by using a combination of ryegrass (Lolium perenne) and different microorganisms. Soil Till Res 110(1):87–93.  https://doi.org/10.1016/j.still.2010.06.010 CrossRefGoogle Scholar
  55. Tang HZ, Li J, Hu HY (2012) A newly isolated strain of Stenotrophomonas sp. hydrolyzes acetamiprid, a synthetic insecticide. Process Biochem 47(12):1820–1825.  https://doi.org/10.1016/j.procbio.2012.06.008 CrossRefGoogle Scholar
  56. Tullo PD, Versini A, Bueno M, Hécho IL, Thiry Y, Biron P, Castrec-Rouelle M, Pannier F (2015) Stable isotope tracing: a powerful tool for selenium speciation and metabolic studies in non-hyperaccumulator plants (ryegrass Lolium perenne L.) Anal Bioanal Chem 407(30):9029–9042.  https://doi.org/10.1007/s00216-015-9069-4 CrossRefGoogle Scholar
  57. Wang CF, Wang XP, Gong P, Yao TD (2016) Residues, spatial distribution and risk assessment of DDTs and HCHs in agricultural soil and crops from the Tibetan Plateau. Chemosphere 149:358–365.  https://doi.org/10.1016/j.chemosphere.2016.01.120 CrossRefGoogle Scholar
  58. White JC (2001) Plant facilitated mobilization and translocation of weathered 2,2-bis (p-chlorophenyl)-1,1-dichloroethylene (p,p-DDE) from an agricultural soil. Environ Toxicol Chem 20(9):2047–2052Google Scholar
  59. White JC, Kottler BD (2002) Citrate-mediated increase in the uptake of weathered 2, 2-bis (p-chlorophenyl),1,1-dichloroethylene residues by plants. Environ Toxicol Chem 21(3):550–556.  https://doi.org/10.1002/etc.5620210312 CrossRefGoogle Scholar
  60. Xiao PF, Mori T, Kamei I, Kondo R (2011) A novel metabolic pathway for biodegradation of DDT by the white rot fungi, Phlebia lindtneri and Phlebia brevispora. Biodegradation 22(5):859–867.  https://doi.org/10.1007/s10532-010-9443-z CrossRefGoogle Scholar
  61. Xie H, Zhu LS, Xu QF, Wang J, Liu W, Jiang JH (2011) Isolation and degradation ability of the DDT-degrading bacterial strain KK. Environ Earth Sci 62(1):93–99.  https://doi.org/10.1007/s12665-010-0500-z CrossRefGoogle Scholar
  62. Yu XZ, Wu SC, Wu FY, Wong MH (2011) Enhanced dissipation of PAHs from soil using mycorrhizal ryegrass and PAH-degrading bacteria. J Hazard Mater 186(2-3):1206–1217.  https://doi.org/10.1016/j.jhazmat.2010.11.116 CrossRefGoogle Scholar
  63. Zhang H, Yang C, Zhao Q, Qiao CL (2009) Development of an autofluorescent organophosphates-degrading Stenotrophomonas sp. with dehalogenase activity for the biodegradation of hexachlorocyclohexane (HCH). Bioresour Technol 100(13):3199–3204.  https://doi.org/10.1016/j.biortech.2009.02.008 CrossRefGoogle Scholar
  64. Zhang MY, Teng Y, Zhu Y (2014a) Isolation and characterization of chlorothalonil-degrading bacterial strain H4 and its potential for remediation of contaminated soil. Pedosphere 24(6):799–807.  https://doi.org/10.1016/S1002-0160(14)60067-9 CrossRefGoogle Scholar
  65. Zhang QM, Zhu LS, Wang J, Xie H, Wang JH, Wang FH, Sun FX (2014b) Effects of fomesafen on soil enzyme activity, microbial population, and bacterial community composition. Environ Monit Assess 186(5):2801–2812.  https://doi.org/10.1007/s10661-013-3581-9 CrossRefGoogle Scholar
  66. Zhu ZQ, Yang XE, Wang K, Huang HG, Zhang XC, Fang H, Li TQ, Alva AK, He ZL (2012) Bioremediation of Cd-DDT co-contaminated soil using the Cd-hyperaccumulator Sedum alfredii and DDT-degrading microbes. J Hazard Mater 235-236:144–151.  https://doi.org/10.1016/j.jhazmat.2012.07.033 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Key Laboratory of Agricultural Environment in Universities of Shandong, College of Resources and EnvironmentShandong Agricultural UniversityTaianChina
  2. 2.National Engineering Laboratory for Efficient Utilization of Soil and Fertilizer ResourcesShandong Agricultural UniversityTaianChina

Personalised recommendations