Advertisement

Current Microbiology

, Volume 74, Issue 3, pp 309–319 | Cite as

Degradation of Di(2-Ethylhexyl) Phthalate by a Novel Gordonia alkanivorans Strain YC-RL2

  • Ruth Nahurira
  • Lei Ren
  • Jinlong Song
  • Yang Jia
  • Junhuan Wang
  • Shuanghu Fan
  • Haisheng Wang
  • Yanchun YanEmail author
Article

Abstract

One bacterial strain, YC-RL2, isolated from petroleum-contaminated soil, could utilize environmental hormone Di(2-Ethylhexyl) phthalate (DEHP) as a sole carbon source for growth. Strain YC-RL2 was identified as Gordonia alkanivorans by 16S rRNA gene analysis and Biolog tests. The effects of environmental factors which might affect the degrading process were optimized at 30 °C and pH 8.0. Strain YC-RL2 showed superior halotolerance and could tolerate up to 0–5% NaCl in trace element medium supplemented with DEHP, although the DEHP degradation rates slowed as NaCl concentration increased. It also showed an outstanding performance in a wide range of pH (6.0–11.0). Meanwhile, strain YC-RL2 was able to withstand high concentrations of DEHP (from 100 to 800 mg/L), and the degradation rates were all above 94%. The DEHP intermediates were detected by HPLC–MS, and the degradation pathway was deduced tentatively. DEHP was transformed into phthalic acid (PA) via mono (2-ethylhexyl) phthalate (MEHP), and PA was further utilized for growth via benzoic acid (BA). The enzyme expected to catalyze the hydrolysis of MEHP to PA was identified from strain YC-RL2. Further investigation found that the enzyme could catalyze the transformation of a wide range of monoalkyl phthalates to PA. This study is the first report about species G. alkanivorans which could degrade several kinds of phthalic acid esters (PAEs), and indicates its application potential for bioremediation of PAE-polluted sites.

Keywords

Phthalate DEHP Phthalic Acid Gordonia Butyl Benzyl Phthalate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We thank Lida Han (Biotechnology Research Institute of CAAS, China) for great help and good suggestions for HPLC and MS analyses. We also acknowledge the intellectual and material contributions by Organization of Women in Science in the Developing world (Fund Reservation No. 3240266458) and SIDA (Swedish International Development Cooperation Agency).This work was supported by the National Natural Science Foundation of China (NSFC, No. 31170119, No. 31540067 and No. 31300101) and Basic Research Fund of CAAS (No. 0042014006, No. 0042012003 and No. 0042011006).

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Statement of Human and Animal Rights

We declare that our study did not involve any animals or humans.

Supplementary material

284_2016_1159_MOESM1_ESM.docx (53 kb)
S1 (DOCX 52 kb)
284_2016_1159_MOESM2_ESM.docx (12 kb)
S2 (DOCX 12 kb)
284_2016_1159_MOESM3_ESM.docx (27 kb)
S3 (DOCX 26 kb)

References

  1. 1.
    Ahrens A, Braun A, von Gleich A, Heitmann K, Lißner L (2006) Hazardous chemicals in products and processes: substitution. Springer, Heidelberg. doi: 10.1007/3-7908-1643-4 CrossRefGoogle Scholar
  2. 2.
    Akita K, Naitou C, Maruyama K (2001) Purification and characterization of an esterase from Micrococcus sp. YGJ1 hydrolyzing phthalate esters. Biosci Biotechnol Biochem 65:1680–1683. doi: 10.1271/bbb.65.1680 CrossRefPubMedGoogle Scholar
  3. 3.
    Aranda J, Cerqueira NMFS, Fernandes PA, Roca M, Tuñon I, Ramos MJ (2014) The catalytic mechanism of carboxylesterases: a computational study. Biochemistry 53:5820–5829. doi: 10.1021/bi500934j CrossRefPubMedGoogle Scholar
  4. 4.
    Arenskötter M, Bröker D, Steinbüchel A (2004) Biology of the metabolically diverse genus Gordonia. Appl Environ Microbiol 70:3195–3204. doi: 10.1128/AEM.70.6.3195-3204.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Bachovchin DA, Ji T, Li W, Simon GM, Blankman JL, Adibekian A, Hoover H, Niessen S, Cravatt BF (2010) Superfamily-wide portrait of serine hydrolase inhibition achieved by library-versus-library screening. Proc Natl Acad Sci USA 107:20941–20946. doi: 10.1073/pnas.1011663107 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Bassin JP, Dezotti M, Sant’Anna GL (2011) Nitrification of industrial and domestic saline wastewaters in moving bed biofilm reactor and sequencing batch reactor. J Hazard Mater 185:242–248. doi: 10.1016/j.jhazmat.2010.09.024 CrossRefPubMedGoogle Scholar
  7. 7.
    Benjamin S, Pradeep S, Josh MS, Kumar S, Masai E, Sarath Josh M, Kumar S, Masai E (2015) A monograph on the remediation of hazardous phthalates. J Hazard Mater 298:58–72. doi: 10.1016/j.jhazmat.2015.05.004 CrossRefPubMedGoogle Scholar
  8. 8.
    Caldwell JC (2012) DEHP: genotoxicity and potential carcinogenic mechanisms—A review. Mutat Res 751:82–157. doi: 10.1016/j.mrrev.2012.03.001 CrossRefPubMedGoogle Scholar
  9. 9.
    Chang HK, Zylstra GJ (1998) Novel organization of the genes for phthalate degradation from Burkholderia cepacia DBO1. J Bacteriol 180:6529–6537PubMedPubMedCentralGoogle Scholar
  10. 10.
    Chatterjee S, Dutta TK (2003) Metabolism of butyl benzyl phthalate by Gordonia sp. strain MTCC 4818. Biochem Biophys Res Commun 309:36–43. doi: 10.1016/S0006-291X(03)01513-4 CrossRefPubMedGoogle Scholar
  11. 11.
    Chatterjee S, Dutta TK (2008) Metabolic cooperation of Gordonia sp. strain MTCC 481 8 and Arthrobacter sp. strain WY in the utilization of butyl benzyl phthalate: effect of a novel co-culture in the degradation of a mixture of phthalates. Microbiology 154:3338–3346. doi: 10.1099/mic.0.2008/021881-0 CrossRefPubMedGoogle Scholar
  12. 12.
    Chen J-AA, Li X, Li J, Cao J, Qiu Z, Zhao Q, Xu C, Shu W (2007) Degradation of environmental endocrine disruptor di-2-ethylhexyl phthalate by a newly discovered bacterium, Microbacterium sp. strain CQ0110Y. Appl Microbiol Biotechnol 74:676–682. doi: 10.1007/s00253-006-0700-3 CrossRefPubMedGoogle Scholar
  13. 13.
    Cortes-Lorenzo C, Cortés-Lorenzo C, Rodríguez-Díaz M, López-Lopez C, Sánchez-Peinado M, Rodelas B, González-López J (2012) Effect of salinity on enzymatic activities in a submerged fixed bed biofilm reactor for municipal sewage treatment. Bioresour Technol 121:312–319. doi: 10.1016/j.biortech.2012.06.083 CrossRefPubMedGoogle Scholar
  14. 14.
    Ding J, Wang C, Xie Z, Li J, Yang Y, Mu Y, Tang X, Xu B, Zhou J, Huang Z (2015) Properties of a newly identified esterase from Bacillus sp. K91 and its novel function in diisobutyl phthalate degradation. PLoS ONE 10:e0119216. doi: 10.1371/journal.pone.0119216 CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Fang HHP, Liang D, Zhang T (2007) Aerobic degradation of diethyl phthalate by Sphingomonas sp. Bioresour Technol 98:717–720. doi: 10.1016/j.biortech.2006.02.010 CrossRefPubMedGoogle Scholar
  16. 16.
    Feng Z, Kunyan C, Jiamo F, Guoying S, Huifang Y (2002) Biodegradability of di(2-ethylhexyl) phthalate by Pseudomonas fluorescens FS1. Water Air Soil Pollut 140:297–305. doi: 10.1023/A:1020108502776 CrossRefGoogle Scholar
  17. 17.
    Fu J, Pan F, Song S, Zhang LR, Luo Y, Chen W, Liang Y (2013) Biodegradation of phthalic acid esters in sewage sludge by composting with pig manure and rice straw. Environ Earth Sci 68:2289–2299. doi: 10.1007/s12665-012-1915-5 CrossRefGoogle Scholar
  18. 18.
    Gao DW, Wen ZD (2016) Phthalate esters in the environment: a critical review of their occurrence, biodegradation, and removal during wastewater treatment processes. Sci Total Environ 541:986–1001. doi: 10.1016/j.scitotenv.2015.09.148 CrossRefPubMedGoogle Scholar
  19. 19.
    Hara H, Stewart GR, Mohn WW (2010) Involvement of a novel ABC transporter and monoalkyl phthalate ester hydrolase in phthalate ester catabolism by Rhodococcus jostii RHA1. Appl Environ Microbiol 76:1516–1523. doi: 10.1128/AEM.02621-09 CrossRefPubMedGoogle Scholar
  20. 20.
    Hongjun Y, Wenjun X, Qing L, Jingtao L, Hongwen Y, Zhaohua L (2013) Distribution of phthalate esters in topsoil: a case study in the Yellow River Delta, China. Environ Monit Assess 185:8489–8500. doi: 10.1007/s10661-013-3190-7 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Ji Y, Wang F, Zhang L, Shan C, Bai Z, Sun Z, Liu L, Shen B (2014) A comprehensive assessment of human exposure to phthalates from environmental media and food in Tianjin, China. J Hazard Mater 279:133–140. doi: 10.1016/j.jhazmat.2014.06.055 CrossRefPubMedGoogle Scholar
  22. 22.
    Jianlong W, Xuan Z, Weizhong W (2004) Biodegradation of phthalic acid esters (PAEs) in soil bioaugmented with acclimated activated sludge. Process Biochem 39:1837–1841. doi: 10.1016/j.procbio.2003.08.005 CrossRefGoogle Scholar
  23. 23.
    Jin D, Bai Z, Chang D, Hoefel D, Jin B, Wang P, Wei D, Zhuang G (2012) Biodegradation of di-n-butyl phthalate by an isolated Gordonia sp. strain QH-11: genetic identification and degradation kinetics. J Hazard Mater 221–222:80–85. doi: 10.1016/j.jhazmat.2012.04.010 CrossRefPubMedGoogle Scholar
  24. 24.
    Jin D, Kong X, Cui B, Bai Z, Zhang H (2013) Biodegradation of di-n-butyl phthalate by a newly isolated halotolerant Sphingobium sp. Int J Mol Sci 14:24046–24054. doi: 10.3390/ijms141224046 CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Kartal B, Koleva M, Arsov R, van der Star W, Jetten MSM, Strous M (2006) Adaptation of a freshwater anammox population to high salinity wastewater. J Biotechnol 126:546–553. doi: 10.1016/j.jbiotec.2006.05.012 CrossRefPubMedGoogle Scholar
  26. 26.
    Li D, Yan J, Wang L, Zhang Y, Liu D, Geng H, Xiong L (2016) Characterization of the phthalate acid catabolic gene cluster in phthalate acid esters transforming bacterium-Gordonia sp. strain HS-NH1. Int Biodeterior Biodegrad 106:34–40. doi: 10.1016/j.ibiod.2015.09.019 CrossRefGoogle Scholar
  27. 27.
    Liu W, Niu L, Xu Y, Xu C, Yun L, Liu W (2014) Status of phthalate esters contamination in agricultural soils across China and associated health risks. Environ Pollut 195:16–23. doi: 10.1016/j.envpol.2014.08.014 CrossRefPubMedGoogle Scholar
  28. 28.
    Luo ZH, Pang KL, Wu YR, Gu JD, Chow RK, Vrijmoed LL (2012) Degradation of phthalate esters by Fusarium sp. DMT-5-3 and Trichosporon sp. DMI-5-1 isolated from mangrove sediments. Prog Mol Subcell Biol 53:299–328. doi: 10.1007/978-3-642-23342-5_15 CrossRefPubMedGoogle Scholar
  29. 29.
    Magdouli S, Daghrir R, Brar SK, Drogui P, Tyagi RD (2013) Di 2-ethylhexyl phthalate in the aquatic and terrestrial environment: a critical review. J Environ Manage 127:36–49. doi: 10.1016/j.jenvman.2013.04.013 CrossRefPubMedGoogle Scholar
  30. 30.
    Meng X, Niu G, Yang W, Cao X (2015) Di(2-ethylhexyl) phthalate biodegradation and denitrification by a Pseudoxanthomonas sp. strain. Bioresour Technol 180:356–359. doi: 10.1016/j.biortech.2014.12.071 CrossRefPubMedGoogle Scholar
  31. 31.
    Navacharoen A, Vangnai AS (2011) Biodegradation of diethyl phthalate by an organic-solvent-tolerant Bacillus subtilis strain 3C3 and effect of phthalate ester coexistence. Int Biodeterior Biodegrad 65:818–826. doi: 10.1016/j.ibiod.2011.05.005 CrossRefGoogle Scholar
  32. 32.
    Net S, Sempere R, Delmont A, Paluselli A, Ouddane B (2015) Occurrence, fate, behavior and ecotoxicological state of phthalates in different environmental matrices. Environ Sci Technol 49:4019–4035. doi: 10.1021/es505233b CrossRefPubMedGoogle Scholar
  33. 33.
    Nishioka T, Iwata M, Imaoka T, Mutoh M, Egashira Y, Nishiyama T, Shin T, Fujii T (2006) A mono-2-ethylhexyl phthalate hydrolase from a Gordonia sp. that is able to dissimilate di-2-ethylhexyl phthalate. Appl Environ Microbiol 72:2394–2399. doi: 10.1128/AEM.72.4.2394-2399.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Peijnenburg WJGM, Struijs J (2006) Occurrence of phthalate esters in the environment of the Netherlands. Ecotoxicol Environ Saf 63:204–215. doi: 10.1016/j.ecoenv.2005.07.023 CrossRefPubMedGoogle Scholar
  35. 35.
    Planelló R, Herrero O, Martínez-Guitarte JL, Morcillo G (2011) Comparative effects of butyl benzyl phthalate (BBP) and di(2-ethylhexyl) 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 105:62–70. doi: 10.1016/j.aquatox.2011.05.011 CrossRefPubMedGoogle Scholar
  36. 36.
    Pradeep S, Josh MKS, Binod P, Devi RS, Balachandran S, Anderson RC, Benjamin S (2015) Achromobacter denitrificans strain SP1 efficiently remediates Di(2-Ethylhexyl) phthalate. Ecotoxicol Environ Saf 112:114–121. doi: 10.1016/j.ecoenv.2014.10.035 CrossRefPubMedGoogle Scholar
  37. 37.
    Purich DL, Schramm VL (1979) Enzyme kinetics and mechanism. Academic Press, San DiegoGoogle Scholar
  38. 38.
    Quan CS, Liu Q, Tian WJ, Kikuchi J, Fan SD (2005) Biodegradation of an endocrine-disrupting chemical, di-2-ethylhexyl phthalate, by Bacillus subtilis No. 66. Appl Microbiol Biotechnol 66:702–710. doi: 10.1007/s00253-004-1683-6 CrossRefPubMedGoogle Scholar
  39. 39.
    Ren L, Jia Y, Ruth N, Qiao C, Wang J, Zhao B, 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 23:1–11. doi: 10.1007/s11356-016-6829-4 CrossRefGoogle Scholar
  40. 40.
    Ren L, Jia Y, Ruth N, Shi Y, Wang J, Qiao C, Yan Y (2016) Biotransformations of bisphenols mediated by a novel Arthrobacter sp. strain YC-RL1. Appl Microbiol Biotechnol 100:1967–1976. doi: 10.1007/s00253-015-7076-1 CrossRefPubMedGoogle Scholar
  41. 41.
    Rengarajan S, Parthasarathy C, Anitha M, Balasubramanian K (2007) Diethylhexyl phthalate impairs insulin binding and glucose oxidation in Chang liver cells. Toxicol Vitr. doi: 10.1016/j.tiv.2006.07.005 Google Scholar
  42. 42.
    Sarath Josh MK, Pradeep S, Adarsh VK, Vijayalekshmi Amma KS, Sudha Devi R, Balachandran S, Sreejith MN, Abdul Jaleel UC, Benjamin S (2013) In silico evidences for the binding of phthalates onto human estrogen receptor α, β subtypes and human estrogen-related receptor γ. Mol Simul 40:408–417. doi: 10.1080/08927022.2013.814131 CrossRefGoogle Scholar
  43. 43.
    Sarkar J, Chowdhury PP, Dutta TK (2013) Complete degradation of di-n-octyl phthalate by Gordonia sp. strain Dop5. Chemosphere 90:2571–2577. doi: 10.1016/j.chemosphere.2012.10.101 CrossRefPubMedGoogle Scholar
  44. 44.
    Schreiber A, Fu F, Yang O, Wan E, Gu L, Leblanc Y (2011) Increasing selectivity and confidence in detection when analyzing phthalates by LC-MS/MS. AB Sciex App Note 1–6Google Scholar
  45. 45.
    Staples CA, Peterson DR, Parkerton TF, Adams WJ (1997) The environmental fate of phthalate esters: a literature review. Chemosphere 35:667–749. doi: 10.1016/S0045-6535(97)00195-1 CrossRefGoogle Scholar
  46. 46.
    Thomas Johnson B, Heitkamp MA, Jones JR (1984) Environmental and chemical factors influencing the biodegradation of phthalic acid esters in freshwater sediments. Environ Pollut Ser B, Chem Phys 8:101–118. doi: 10.1016/0143-148X(84)90021-1 CrossRefGoogle Scholar
  47. 47.
    Wang J, Zhang M-Y, Chen T, Zhu Y, Teng Y, Luo Y-M, Christie P, Jun W, Man-yun Z, Chen T, Zhu YE, Teng Y, Christie P (2015) Isolation and identification of a di- (2-ethylhexyl) phthalate-degrading bacterium and its role in the bioremediation of a contaminated soil. Pedosph An Int J 25:202–211. doi: 10.1016/S1002-0160(15)60005-4 Google Scholar
  48. 48.
    Wang W, Xu X, Fan CQ (2015) Health hazard assessment of occupationally di-(2-ethylhexyl)-phthalate-exposed workers in China. Chemosphere 120:37–44. doi: 10.1016/j.chemosphere.2014.05.053 CrossRefPubMedGoogle Scholar
  49. 49.
    Wu J, Liao X, Yu F, Wei Z, Yang L (2013) Cloning of a dibutyl phthalate hydrolase gene from Acinetobacter sp. strain M673 and functional analysis of its expression product in Escherichia coli. Appl Microbiol Biotechnol 97:2483–2491. doi: 10.1007/s00253-012-4232-8 CrossRefPubMedGoogle Scholar
  50. 50.
    Wu Q, Liu H, Ye LS, Li P, Wang YH (2013) Biodegradation of di-n-butyl phthalate esters by Bacillus sp. SASHJ under simulated shallow aquifer condition. Int Biodeterior Biodegrad 76:102–107. doi: 10.1016/j.ibiod.2012.06.013 CrossRefGoogle Scholar
  51. 51.
    Wu X, Liang R, Dai Q, Jin D, Wang Y, Chao W (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 176:262–268. doi: 10.1016/j.jhazmat.2009.11.022 CrossRefPubMedGoogle Scholar
  52. 52.
    Wu Y, Tam NFY, Wong MH (2008) Effects of salinity on treatment of municipal wastewater by constructed mangrove wetland microcosms. Mar Pollut Bull 57:727–734. doi: 10.1016/j.marpolbul.2008.02.026 CrossRefPubMedGoogle Scholar
  53. 53.
    Xu XR, Li HB, Gu JD (2005) Biodegradation of an endocrine-disrupting chemical di-n-butyl phthalate ester by Pseudomonas fluorescens B-1. Int Biodeterior Biodegrad 55:9–15. doi: 10.1016/j.ibiod.2004.05.005 CrossRefGoogle Scholar
  54. 54.
    Xue Y (2003) Gordonia paraffinivorans sp. nov., a hydrocarbon-degrading actinomycete isolated from an oil-producing well. Int J Syst Evol Microbiol 53:1643–1646. doi: 10.1099/ijs.0.02605-0 CrossRefPubMedGoogle Scholar
  55. 55.
    Young C-C, Lin T-C, Yeh M-S, Shen F-T, Chang J-S (2005) Identification and kinetic characteristics of an indigenous diesel-degrading Gordonia alkanivorans strain. World J Microbiol Biotechnol 21:1409–1414. doi: 10.1007/s11274-005-5742-7 CrossRefGoogle Scholar
  56. 56.
    Zeng F, Cui K, Li X, Fu J, Sheng G (2004) Biodegradation kinetics of phthalate esters by Pseudomonas fluoresences FS1. Process Biochem 39:1125–1129. doi: 10.1016/S0032-9592(03)00226-7 CrossRefGoogle Scholar
  57. 57.
    Zhang Y, Tao Y, Zhang H, Wang L, Sun G, Sun X, Erinle KO, Feng C, Song Q, Li M (2015) Effect of di-n-butyl phthalate on root physiology and rhizosphere microbial community of cucumber seedlings. J Hazard Mater 289:9–17. doi: 10.1016/j.jhazmat.2015.01.071 CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Ruth Nahurira
    • 1
  • Lei Ren
    • 1
  • Jinlong Song
    • 2
  • Yang Jia
    • 1
  • Junhuan Wang
    • 1
  • Shuanghu Fan
    • 1
  • Haisheng Wang
    • 1
  • Yanchun Yan
    • 1
    Email author
  1. 1.Graduate School of Chinese Academy of Agricultural SciencesBeijingChina
  2. 2.Chinese Academy of Fishery SciencesBeijingChina

Personalised recommendations