Advertisement

Environmental Science and Pollution Research

, Volume 23, Issue 16, pp 16609–16619 | Cite as

Biodegradation of phthalic acid esters by a newly isolated Mycobacterium sp. YC-RL4 and the bioprocess with environmental samples

  • Lei Ren
  • Yang Jia
  • Nahurira Ruth
  • Cheng Qiao
  • Junhuan Wang
  • Baisuo Zhao
  • Yanchun YanEmail author
Research Article

Abstract

Bacterial strain YC-RL4, capable of utilizing phthalic acid esters (PAEs) as the sole carbon source for growth, was isolated from petroleum-contaminated soil. Strain YC-RL4 was identified as Mycobacterium sp. by 16S rRNA gene analysis and Biolog tests. Mycobacterium sp. YC-RL4 could rapidly degrade dibutyl phthalate (DBP), diethyl phthalate (DEP), dimethyl phthalate (DMP), dicyclohexyl phthalate (DCHP), and di-(2-ethylhexyl) phthalate (DEHP) under both individual and mixed conditions, and all the degradation rates were above 85.0 % within 5 days. The effects of environmental factors which might affect the degrading process were optimized as 30 °C and pH 8.0. The DEHP metabolites 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) degradation pathway. Cell surface hydrophobicity (CSH) assays illuminated that the strain YC-RL4 was of higher hydrophobicity while grown on DEHP and CSH increased with the higher DEHP concentration. The degradation rates of DEHP by strain YC-RL4 in different environmental samples was around 62.0 to 83.3 % and strain YC-RL4 survived well in the soil sample. These results suggested that the strain YC-RL4 could be used as a potential and efficient PAE degrader for the bioremediation of contaminated sites.

Keywords

Phthalic acid esters Mycobacterium sp. Metabolic mechanism Cell surface hydrophobicity Bioremediation 

Notes

Acknowledgments

We thank Nahurira Ruth (Graduate School of Chinese Academy of Agricultural Sciences) for the revision of the manuscript, Jing Zhou (Agricultural Resources and Regional Planning Institute of CAAS, China) for providing the soil, Lida Han (Biotechnology Research Institute of CAAS, China) for great help and good suggestions for HPLC and MS analyses, and we also thank Gérald Thouand for his kind suggestions on the manuscript (Université de Nantes, France). We also acknowledge the intellectual and material contributions of Organization of Women in Science in the Developing World (OWSD) andSwedish International Development Cooperation Agency (SIDA). This work was supported by the National Natural Science Foundation of China (NSFC, 31170119 and 31540067) and the Basic Research Fund of CAAS (0042014006, 0042012003, and 0042011006).

Supplementary material

11356_2016_6829_MOESM1_ESM.docx (1.9 mb)
Supplementary file 1 (DOCX 1986 kb)

References

  1. Akita K, Naitou C, Maruyama K (2001) Purification and characterization of an esterase from Micrococcus sp. YGJ1 hydrolyzing phthalate esters. Biosci Biotech Bioch 65:1680–1683CrossRefGoogle Scholar
  2. Al-Tahhan RA, Sandrin TR, Bodour AA, Maier RM (2000) Rhamnolipid-induced removal of lipopolysaccharide from Pseudomonas aeruginosa: effect on cell surface properties and interaction with hydrophobic substrates. Appl Environ Microbiol 66:3262–3268CrossRefGoogle Scholar
  3. Blom A, Ekman E, Johannisson A, Norrgren L, Pesonen M (1998) Effects of xenoestrogenic environmental pollutants on the proliferation of a human breast cancer cell line (MCF-7). Arch Environ Contam Toxicol 34:306–310CrossRefGoogle Scholar
  4. Caldwell JC (2012) DEHP: genotoxicity and potential carcinogenic mechanisms—a review. Mutat Res Rev Mutat 751:82–157CrossRefGoogle Scholar
  5. Ceresana (2013) Market study: plasticizers (3rd edition). Data available from: http://www.ceresana.com/en/market-studies/additives/plasticizers/ceresana-market-study-plasticizers.html
  6. Chen X, Xu S, Tan T et al (2014) Toxicity and estrogenic endocrine disrupting activity of phthalates and their mixtures. Int J Environ Res Public Health 11:3156–3168CrossRefGoogle Scholar
  7. Chen X, Zhang X, Yang Y, Yue D, Xiao L, Yang L (2015) Biodegradation of an endocrine-disrupting chemical di-n-butyl phthalate by newly isolated Camelimonas sp. and enzymatic properties of its hydrolase. Biodegradation 26:171–182CrossRefGoogle Scholar
  8. Cheung JKH, Lam RKW, Shi MY, Gu JD (2007) Environmental fate of endocrine-disrupting dimethyl phthalate esters (DMPE) under sulfate-reducing condition. Sci Total Environ 381:126–133CrossRefGoogle Scholar
  9. Ding J, Wang C, Xie Z et al (2015) Properties of a newly identified esterase from Bacillus sp. K91 and its novel function in diisobutyl phthalate degradation. PLoS One 10:e119216Google Scholar
  10. Federici E, Leonardi V, Giubilei M et al (2007) Addition of allochthonous fungi to a historically contaminated soil affects both remediation efficiency and bacterial diversity. Appl Microbiol Biotechnol 77:203–211CrossRefGoogle Scholar
  11. Hindson BJ, Ness KD, Masquelier DA et al (2011) High-throughput droplet digital PCR system for absolute quantitation of DNA copy number. Anal Che 83(22):8604–8610CrossRefGoogle Scholar
  12. Hsu P, Kuo Y, Guo Y, Chen J, Tsai S, Chao H, Teng Y, Pan M (2014) The adverse effects of low-dose exposure to di(2-ethylhexyl) phthalate during adolescence on sperm function in adult rats. Environ Toxicol. doi: 10.1002/tox.22083 Google Scholar
  13. Jiang W, Joens JA, Dionysiou DD et al (2013) Optimization of photocatalytic performance of TiO2 coated glass microspheres using response surface methodology and the application for degradation of dimethyl phthalate. J Photoch Photobio A 262:7–13CrossRefGoogle Scholar
  14. Jiao Y, Chen X, Wang X et al (2013) Identification and characterization of a cold-active phthalate esters hydrolase by screening a metagenomic library derived from biofilms of a wastewater treatment plant. PLoS ONE 8:e75977CrossRefGoogle Scholar
  15. Jin D, Kong X, Li Y, Bai Z, Zhuang G, Zhuang X, Deng Y (2015) Biodegradation of di-n-butyl phthalate by Achromobacter sp. isolated from rural domestic wastewater. Int J Env Res Pub He 12:13510–13522CrossRefGoogle Scholar
  16. Jobling S, Reynolds T, White R, Parker MG, Sumpter JP (1995) A variety of environmentally persistent chemicals, including some phthalate plasticizers, are weakly estrogenic. Environ Health Perspect 103:582–587CrossRefGoogle Scholar
  17. Kaczorek E, Chrzanowski Ł, Pijanowska A, Olszanowski A (2008) Yeast and bacteria cell hydrophobicity and hydrocarbon biodegradation in the presence of natural surfactants: rhamnolipides and saponins. Bioresour Technol 99:4285–4291CrossRefGoogle Scholar
  18. Karandikar R, Badri A, Phale PS (2015) Biochemical characterization of inducible ‘reductase’ component of benzoate dioxygenase and phthalate isomer dioxygenases from Pseudomonas aeruginosa strain PP4. Appl Biochem Biotech 177:318–333CrossRefGoogle Scholar
  19. Kelley K, Cosman A, Belgrader P et al (2013) Detection of methicillin-resistant Staphylococcus aureus by a duplex droplet digital PCR assay. J Clin Microbiol 51:2033–2039CrossRefGoogle Scholar
  20. Lin L, Wang S, Chang Y, Huang P, Cheng J, Su P, Liao P (2011) Associations between maternal phthalate exposure and cord sex hormones in human infants. Chemosphere 83:1192–1199CrossRefGoogle Scholar
  21. Lowell Center for Sustainable Production (2011) Phthalates and their alternatives: health and environmental concerns. Available from: http://www.sustainableproduction.org/downloads
  22. Lu Y, Tang F, Wang Y, Zhao J, Zeng X, Luo Q, Wang L (2009) Biodegradation of dimethyl phthalate, diethyl phthalate and di-n-butyl phthalate by Rhodococcus sp. L4 isolated from activated sludge. J Hazard Mater 168:938–943CrossRefGoogle Scholar
  23. Luo QS, Wang H, Zhang XH, Qian Y (2005) Effect of direct electric current on the cell surface properties of phenol-degrading bacteria. Appl Environ Microb 71:423–427CrossRefGoogle Scholar
  24. Luo Z, Wu Y, Chow RKK, Luo J, Gu J, Vrijmoed LLP (2012) Purification and characterization of an intracellular esterase from a Fusarium species capable of degrading dimethyl terephthalate. Process Biochem 47:687–693CrossRefGoogle Scholar
  25. Maruyama K (2005) Purification and characterization of an esterase hydrolyzing monoalkyl phthalates from Micrococcus sp. YGJ1. J Biochem 137:27–32CrossRefGoogle Scholar
  26. Nishioka T, Iwata M, Imaoka T et al (2006) A mono-2-ethylhexyl phthalate hydrolase from a Gordonia sp that is able to dissimilate di-2-ethylhexyl phthalate. Appl Environ Microb 72:2394–2399CrossRefGoogle Scholar
  27. Plaza GA, Ulfig K, Brigmon RL (2005) Surface active properties of bacterial strains isolated from petroleum hydrocarbon-bioremediated soil. Pol J Microbiol 54:161–167Google Scholar
  28. 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 100:1967–1976CrossRefGoogle Scholar
  29. Roberts C, Last A, Molina-Gonzalez S et al (2013) Development and evaluation of a next-generation digital PCR diagnostic assay for ocular Chlamydia trachomatis infections. J Clin Microbiol 51:2195–2203CrossRefGoogle Scholar
  30. Rosenberg M (2006) Microbial adhesion to hydrocarbons: twenty-five years of doing MATH. FEMS Microbiol Lett 262:129–134CrossRefGoogle Scholar
  31. Rosenberg M, Gutnick D, Rosenberg E (1980) Adherence of bacteria tohydrocarbons: a simple method for measuring cell surface hydrophobicity. FEMS Microbiol Lett 9:22–33CrossRefGoogle Scholar
  32. Shakirova L, Auzina L, Grube M, Zikmanis P (2008) Relationship between the cell surface hydrophobicity and survival of bacteria Zymomonas mobilis after exposures to ethanol, freezing or freeze-drying. J Ind Microbiol Biotechnol 35:1175–1180CrossRefGoogle Scholar
  33. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  34. Tucker B, Radtke C, Kwon S, Andersson A (1995) Suppression of bioremediation by Phanerochaete chrysosporium by soil factors. J Hazard Mater 41:251–265CrossRefGoogle Scholar
  35. US EPA (1992 and update) Code of federal regulations. 40 CFR, Part 136Google Scholar
  36. Wang J, Liu P, Qian Y (1995) Microbial degradation of di-n-butyl phthalate. Chemosphere 31:4051–4056CrossRefGoogle Scholar
  37. Wang J, Luo Y, Teng Y, Ma W, Christie P, Li Z (2013) Soil contamination by phthalate esters in Chinese intensive vegetable production systems with different modes of use of plastic film. Environ Pollut 180:265–273CrossRefGoogle Scholar
  38. Wang J, Zhang M, Chen T, Zhu Y, Teng Y, Luo Y, Christie P (2015a) Isolation and identification of a di-(2-ethylhexyl) phthalate-degrading bacterium and its role in the bioremediation of a contaminated soil. Pedosphere 25:202–211CrossRefGoogle Scholar
  39. Wang W, Wu Q, Wang C, He T, Hu H (2015b) Health risk assessment of phthalate esters (PAEs) in drinking water sources of China. Environ Sci Pollut Res 22:3620–3630CrossRefGoogle Scholar
  40. 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 176:262–268CrossRefGoogle Scholar
  41. 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 97:2483–2491CrossRefGoogle Scholar
  42. Xia X, Yang L, Bu Q, Liu R (2011) Levels, distribution, and health risk of phthalate esters in urban soils of Beijing, China. J Environ Qual 40:1643–1651CrossRefGoogle Scholar
  43. Xie Z, Ebinghaus R, Temme C, Lohmann R, Caba A, Ruck W (2007) Occurrence and air–sea exchange of phthalates in the Arctic. Environ Sci Technol 41:4555–4560CrossRefGoogle Scholar
  44. Yang X, Zhang C, He Z et al (2013) Isolation and characterization of two n-butyl benzyl phthalate degrading bacteria. Int Biodeter Biodegr 76:8–11CrossRefGoogle Scholar
  45. Zeng P, Moy BY, Song Y, Tay J (2008) Biodegradation of dimethyl phthalate by Sphingomonas sp. isolated from phthalic-acid-degrading aerobic granules. Appl Microbiol Biotechnol 80:899–905CrossRefGoogle Scholar
  46. Zhang J, Sun Z, Li Y, Peng X, Li W, Yan Y (2009) Biodegradation of p-nitrophenol by Rhodococcus sp. CN6 with high cell surface hydrophobicity. J Hazard Mater 163:723–728CrossRefGoogle Scholar
  47. Zhang C, Jia L, Wang S et al (2010) Biodegradation of beta-cypermethrin by two Serratia spp. with different cell surface hydrophobicity. Bioresour Technol 101:3423–3429CrossRefGoogle Scholar
  48. Zhang Y, Tao Y, Zhang H et al (2015) Effect of di-n-butyl phthalate on root physiology and rhizosphere microbial community of cucumber seedlings. J Hazard Mater 289:9–17CrossRefGoogle Scholar
  49. Zheng D, Bao J, Lu J, Gao C (2015) Isolation and characterization of a furfural-degrading bacterium Bacillus cereus sp. strain DS1. Curr Microbiol 70:199–205CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Lei Ren
    • 1
  • Yang Jia
    • 1
  • Nahurira Ruth
    • 1
  • Cheng Qiao
    • 1
  • Junhuan Wang
    • 1
  • Baisuo Zhao
    • 1
  • Yanchun Yan
    • 1
    Email author
  1. 1.Graduate School of Chinese Academy of Agricultural SciencesBeijingChina

Personalised recommendations