Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Isolation of Dibutyl Phthalate-Degrading Bacteria and Its Coculture with Citrobacter freundii CD-9 to Degrade Fenvalerate

  • Wu, Min (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University) ;
  • Tang, Jie (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University) ;
  • Zhou, Xuerui (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University) ;
  • Lei, Dan (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University) ;
  • Zeng, Chaoyi (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University) ;
  • Ye, Hong (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University) ;
  • Cai, Ting (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University) ;
  • Zhang, Qing (Key Laboratory of Food Biotechnology, College of Food and Bioengineering, Xihua University)
  • Received : 2021.10.28
  • Accepted : 2022.01.12
  • Published : 2022.02.28
Download PDF
⟨ Previous Next ⟩

Abstract

Continued fenvalerate use has caused serious environmental pollution and requires large-scale remediation. Dibutyl phthalate (DBP) was discovered in fenvalerate metabolites degraded by Citrobacter freundii CD-9. Coculturing is an effective method for bioremediation, but few studies have analyzed the degradation pathways and potential mechanisms of cocultures. Here, a DBP-degrading strain (BDBP 071) was isolated from soil contaminated with pyrethroid pesticides (PPs) and identified as Stenotrophomonas acidaminiphila. The optimum conditions for DBP degradation were determined by response surface methodology (RSM) analysis to be 30.9 mg/l DBP concentration, pH 7.5, at a culture temperature of 37.2℃. Under the optimized conditions, approximately 88% of DBP was degraded within 48 h and five metabolites were detected. Coculturing C. freundii CD-9 and S. acidaminiphila BDBP 071 promoted fenvalerate degradation. When CD-9 was cultured for 16 h before adding BDBP 071, the strain inoculation ratio was 5:5 (v/v), fenvalerate concentration was 75.0 mg/l, fenvalerate was degraded to 84.37 ± 1.25%, and DBP level was reduced by 5.21 mg/l. In addition, 12 fenvalerate metabolites were identified and a pathway for fenvalerate degradation by the cocultured strains was proposed. These results provide theoretical data for further exploration of the mechanisms used by this coculture system to degrade fenvalerate and DBP, and also offer a promising method for effective bioremediation of PPs and their related metabolites in polluted environments.

Keywords

Acknowledgement

This study was funded by the National Natural Science Foundation of China (32102094), the Application Foundation Project of Sichuan Provincial Department of Science and Technology (2019YJ0389), the Science and Technology Support Project of Sichuan Province (No. 2019ZYZF0170), the Technological Innovation Project of Chengdu Science and Technology Bureau (2018-YF05-00522-SN), the Key Scientific Research Fund of Xihua University (Z1310525), and the Graduate Student Innovation Fund of Xihua University (ycjj2020130).

References

  1. Tang J, Liu B, Shi Y, Zeng CY, Chen TT, Zeng L, et al. 2018. Isolation, identification, and fenvalerate-degrading potential of Bacillus licheniformis CY-012. Biotechnol. Biotechnol. Equip. 32: 574-582. https://doi.org/10.1080/13102818.2018.1438210
  2. Cycon M, Piotrowska-Seget Z. 2016. Pyrethroid-degrading microorganisms and their potential for the bioremediation of contaminated soils: a review. Front. Microbiol. 7: 1463. https://doi.org/10.3389/fmicb.2016.01463
  3. Tripathi G, Verrna P. 2014. Fenvalerate-induced changes in a Catfish, Clariasbatrachus: metabolic enzymes, RNA and protein. Comp. Biochem. Physiol. PartC: Toxicol. Pharmacol. 138: 75-79. https://doi.org/10.1016/j.cca.2004.05.005
  4. Antwi FB, Reddy GVP. 2015. Toxicological effects of pyrethroids on non-target aquatic insects. Environ. Toxicol. Pharmacol. 40: 915-923. https://doi.org/10.1016/j.etap.2015.09.023
  5. Desneux N, Decourtye A, Delpuech JM. 2007. The sublethal effects of pesticides on beneficial arthropods. Ann. Rev. Entomol. 52: 81-106. https://doi.org/10.1146/annurev.ento.52.110405.091440
  6. Decourtye A, Devillers J, Genecque E, Menach KL, Budzinski H, Cluzeau S, et al. 2005. Comparative sublethaltoxicity of nine pesticides on olfactory learning performances of the Honeybee Apis mellifera. Arch. Environ. Contam. Toxicol. 48: 242-250. https://doi.org/10.1007/s00244-003-0262-7
  7. Das R, Das SJ, Das AC. 2016. Effect of synthetic pyrethroid insecticides on N-2-fixation and its mineralization in tea soil. Eur. J. Soil. Biol. 74: 9-15. https://doi.org/10.1016/j.ejsobi.2016.02.005
  8. Laffin B, Chavez M, Pine M. 2010. The pyrethroid metabolites 3-phenoxy benzoic acid and 3-phenoxy benzyl alcohol do not exhibit estrogenic activity in the MCF-7 human breast carcinoma cell line or Sprague-Dawley rats. Toxicology 267: 39-44. https://doi.org/10.1016/j.tox.2009.10.003
  9. Perry MJ, Venners SA, Barr DB, Xu X. 2007. Environmental pyrethroid and organophosphorus insecticide exposures and sperm concentration. Reprod. Toxicol. 23: 113-118. https://doi.org/10.1016/j.reprotox.2006.08.005
  10. Kolaczinski JH, Curtis CF. 2001. Chronic illness as a result of low-level exposure to synthetic pyrethroid insecticides: a review of the debate. Food Chem. Toxicol. 42: 697-706. https://doi.org/10.1016/j.fct.2003.12.008
  11. Wang BZ, Guo P, Hang BJ, Li L, He J, Li SP. 2009. Cloning of a novel pyrethroid-hydrolyzing carboxylesterase gene from Sphingobium sp. strain JZ-1 and characterization of the gene product. Appl. Environ. Microbiol. 75: 5496-5500. https://doi.org/10.1128/AEM.01298-09
  12. Chen SH, Hu MY, Liu JJ, Zhong G, Liu Y, Rizwan M, et al. 2011. Biodegradation of beta-cypermethrin and 3-phenoxybenzoic acid by a novel Ochrobactrumlupini DG-S-01. J. Hazard. Mater. 187: 433-440. https://doi.org/10.1016/j.jhazmat.2011.01.049
  13. Zhan H, Wang HS, Liao LS, Feng YM, Fan XH, Zhang LH, et al. 2018. Kinetics and novel degradation pathway of permethrin in Acinetobacter baumannii ZH-14. Front. Microbiol. 9: 98. https://doi.org/10.3389/fmicb.2018.00098
  14. Tang J, Hu Q, Liu B, Lei D, Chen TT, Sun Q, et al. 2019. Efficient biodegradation of 3-phenoxybenzoic acid and pyrethroid pesticides by a novel strain Klebsiella pneumoniae BPBA052. Can. J. Microbiol. 65: 795-804. https://doi.org/10.1139/cjm-2019-0183
  15. Chen SH, Hu QB, Hu MY, Luo J, Weng Q, Lai K. 2011. Isolation and characterization of a fungus able to degrade pyrethroids and 3-phenoxybenzaldehyde. Bioresour. Technol. 102: 8110-8116. https://doi.org/10.1016/j.biortech.2011.06.055
  16. Zhao T, Hu K, Li J, Zhu Y, Liu S. 2021. Current insights into the microbial degradation for pyrethroids: strain safety, biochemical pathway, and genetic engineering. Chemosphere 279: 130542. https://doi.org/10.1016/j.chemosphere.2021.130542
  17. Deng WQ, Lin DR, Yao K, Yuan HY, Wang ZL, Li JL, et al. 2015. Characterization of a novel β-cypermethrin-degrading Aspergillus niger YAT strain and the biochemical degradation pathway of β-cypermethrin. Appl. Microbiol. Biotechnol. 99: 8187-8198. https://doi.org/10.1007/s00253-015-6690-2
  18. Huang YC, Xiao LJ, Li FY, Xiao MS, Lin DR, Long XM, et al. 2018. Microbial degradation of pesticide residues and an emphasis on the degradation of cypermethrin and 3-phenoxybenzoic acid: a review. Molecules 23: 2313. https://doi.org/10.3390/molecules23092313
  19. Huang Y, Lin Z, Zhang WP, Pang SM, Bhatt P, Rene ER, et al. 2020. New insights into the microbial degradation of D-cyphenothrin in contaminated water/soil environments. Microorganisms 8: 473. https://doi.org/10.3390/microorganisms8040473
  20. Tang J, Hu Q, Lei D, Wu M, Zeng CY, Zhang Q. 2020. Characterization of deltamethrin degradation and metabolic pathway by co-culture of Acinetobacter junii LH-1-1 and Klebsiella pneumoniae BPBA052. AMB Express 10: 106. https://doi.org/10.1186/s13568-020-01043-1
  21. Yang JJ, Feng YM, Zhan H, Liu J, Yang F, Zhang KY, et al. 2018. Characterization of a pyrethroid-degrading Pseudomonas fulva strain P31 and biochemical degradation pathway of D-phenothrin. Front. Microbiol. 9: 1003. https://doi.org/10.3389/fmicb.2018.01003
  22. Tang J, Lei D, Wu M, Hu Q, Zhang Q. 2020. Biodegradation and metabolic pathway of fenvalerate by Citrobacter freundii CD-9. AMB Express 10: 194. https://doi.org/10.1186/s13568-020-01128-x
  23. Sun RX, Wang L, Jiao YQ, Zhang Y, Zhang X, Wu P, et al. 2019. Metabolic process of di-n-butyl phthalate (DBP) by Enterobacter sp. DNB-S2, isolated from Mollisol region in China. Environ. Pollut. 255: 113344. https://doi.org/10.1016/j.envpol.2019.113344
  24. Liu TF, Li J, Qiu LQ, Zhang FM, Linhardt RJ, Zhong WH. 2020. Combined genomic and transcriptomic analysis of dibutyl phthalate metabolic pathway in Arthrobacter sp. ZJUTW. Biotechnol. Bioeng. 117: 3712-3726. https://doi.org/10.1002/bit.27524
  25. Wang IJ, Lin CC, Lin YJ, Hsieh WS, Chen PC. 2014. Early life phthalate exposure and atopic disorders in children: a prospective birth cohort study. Environ. Int. 62: 48-54. https://doi.org/10.1016/j.envint.2013.09.002
  26. Cho SC, Bhang SY, Hong YC, Shin MS, Kim BN, Kim JW, et al. 2010. Relationship between environmental phthalate exposure and the intelligence of school-age children. Environ. Health Perspect. 118: 1027-1032. https://doi.org/10.1289/ehp.0901376
  27. Tellez-Rojo MM, Cantoral A, Cantonwine DE, Schnaas L, Peterson K, Hu H, et al. 2013. Prenatal urinary phthalate metabolites levels and neurodevelopment in children at two and three years of age. Sci. Total Environ. 461: 386-390. https://doi.org/10.1016/j.scitotenv.2013.05.021
  28. Hatch EE, Nelson JW, Qureshi MM, Weinberg J, Moore LL, Singer M, et al. 2008. Association of urinary phthalate metabolite concentrations with body mass index and waist circumference: a cross-sectional study of NHANES data, 1999-2002. Environ. Health 7: 1-15. https://doi.org/10.1186/1476-069X-7-1
  29. Stahlhut RW, Van Wijngaarden E, Dye TD, Stephen C, Shanna HS. 2007. Concentrations of urinary phthalate metabolites are associated with increased waist circumference and insulin resistance in adult U.S. males. Environ. Health Perspect. 115: 876-882. https://doi.org/10.1289/ehp.9882
  30. Svensson K, Hernandez-Ramirez RU, Burguete-Garcia A, Cebrian ME, Carrillo LL. 2011. Phthalate exposure associated with self-reported diabetes among Mexican women. Environ. Res. 111: 792-796. https://doi.org/10.1016/j.envres.2011.05.015
  31. Zhang JF, Zhang CN, Zhu YP, Li JL, Li XT. 2018. Biodegradation of seven phthalate esters by Bacillus mojavensis B1811. Int Biodeter. Biodegrad. 132: 200-207. https://doi.org/10.1016/j.ibiod.2018.04.006
  32. Yuan SY, Huang IC, Chang BV. 2010. Biodegradation of dibutyl phthalate and di-(2-ethylhexyl) phthalate and microbial community changes in mangrove sediment. J. Hazard Mater. 184: 826-831. https://doi.org/10.1016/j.jhazmat.2010.08.116
  33. Lu Y, Tang F, Wang Y, Zhao J, Zeng X, Luo Q, et al. 2009. Biodegradation of dimethyl phthalate, diethyl phthalate and di-n-butyl phthalate by Rhodococcus sp. L4 isolated from activated sludge. J. Hazard Mater. 168: 938-943. https://doi.org/10.1016/j.jhazmat.2009.02.126
  34. Hara H, Stewart GR, Mohn WW. 2010. Involvement of a novel ABC transporter and monoalkyl phthalate ester hydrolase in phthalate ester catabolism by Rhodococcusjostii RHA1. Appl. Environ. Microbiol. 76: 1516-1523. https://doi.org/10.1128/AEM.02621-09
  35. Zeng P, Moy BYP, Song YH, Tay JH. 2008. Biodegradation of dimethyl phthalate by Sphingomonas sp. isolated from phthalic-acid-degrading aerobic granules. Appl. Microbiol Biotechnol. 80: 899-905. https://doi.org/10.1007/s00253-008-1632-x
  36. Xu YQ, Minhazul KAHM, Wang XC, Liu X, Li XT, Meng Q, et al. 2020. Biodegradation of phthalate esters by Paracoccus kondratievae BJQ0001 isolated from Jiuqu (Baijiu fermentation starter) and identification of the ester bond hydrolysis enzyme. Environ. Pollut. 263: 114506. https://doi.org/10.1016/j.envpol.2020.114506
  37. Yu H, Wang L, Lin YL, Liu WX, Tuyiringire D, Jiao YQ, et al. 2020. Complete metabolic study by dibutyl phthalate degrading Pseudomonas sp. DNB-S1. Ecotoxicol. Environ. Saf. 194: 110378. https://doi.org/10.1016/j.ecoenv.2020.110378
  38. Liu FF, Chi YL, Wu S, Jia DY, Yao K. 2014. Simultaneous degradation of cypermethrin and its metabolite, 3-phenoxybenzoic acid, by the cooperation of Bacillus licheniformis B-1 and Sphingomonas sp. SC-1. J. Agric. Food Chem. 62: 8256-8262. https://doi.org/10.1021/jf502835n
  39. Wang LL, Chen YY, Shang F, Liu W, Lan J, Gao P, et al. 2019. Structural insight into the carboxylesterase BioH from Klebsiella pneumoniae. Biochem. Biophys. Res. Comm. 520: 538-543. https://doi.org/10.1016/j.bbrc.2019.10.050
  40. Chen SH, Luo JJ, Hu MY, Lai KP, Geng P, Huang HS. 2012. Enhancement of cypermethrin degradation by a coculture of Bacillus cereus ZH-3 and Streptomyces aureus HP-S-01. Bioresour. Technol. 110: 97-104. https://doi.org/10.1016/j.biortech.2012.01.106
  41. Birolli WG, Arai MS, Nitschke M, Andre LMP. 2019. The pyrethroid (±)-lambda-cyhalothrinenantio selective biodegradation by a bacterial consortium. Pest Biochem. Physiol. 156: 129-137. https://doi.org/10.1016/j.pestbp.2019.02.014
  42. Zhao JY, Chi YL, Xu YC, Jia DY, Yao K. 2016. Co-Metabolic degradation of β-cypermethrin and 3-phenoxybenzoic acid by coculture of Bacillus licheniformis B-1 and Aspergillus oryzae M-4. PLoS One 11: e0166796. https://doi.org/10.1371/journal.pone.0166796
  43. Holt JG, Krieg NR, Sneath PH, Staley JT, Williams ST. 1994. Bergey's manual of determinative bacteriology, 9th ed; Willian and Wilkins: Baltimore, MD, USA.
  44. Tang WJ, Zhang LS, Fang Y, Zhou Y, Ye BC. 2016. Biodegradation of phthalate esters by newly isolated Rhizobium sp. LMB-1 and its biochemical pathway of di- n-butyl phthalate. J. Appl. Microbiol. 121: 177-186. https://doi.org/10.1111/jam.13123
  45. Mahajan R, Verma S, Kushwaha M, Dharam S, Yusuf A, Subhankar C. 2018. Biodegradation of di-n-butyl phthalate by psychrotolerant Sphingobium yanoikuyae strain P4 and protein structural analysis of carboxylesterase involved in the pathway. Int. J. Biol. Macromol. 122: 806-816. https://doi.org/10.1016/j.ijbiomac.2018.10.225
  46. Birolli WG, Dos SA, Pilau E, Pilau E, Rodrigues FE. 2021. New role for a commercially available bioinsecticide: Bacillus thuringiensis Berliner biodegrades the pyrethroid cypermethrin. Environ. Sci. Technol. 55: 4792-4803. https://doi.org/10.1021/acs.est.0c06907
  47. Zhao JY, Jia DY, Chi YL, Yao K. 2019. Co-metabolic enzymes and pathways of 3-phenoxybenzoic acid degradation by Aspergillusoryzae M-4. Ecotoxicol. Environ. Saf. 189: 109953. https://doi.org/10.1016/j.ecoenv.2019.109953
  48. Bhatt P, Huang YH, Zhan H, Chen SH. 2019. Insight into microbial applications for the biodegradation of pyrethroid insecticides. Front. Microbiol. 10: 1778. https://doi.org/10.3389/fmicb.2019.01778
  49. Deng SY, Chen Y, Wang DS, Shi TZ, Wu XW, Ma X, et al. 2015. Rapid biodegradation of organophosphorus pesticides by Stenotrophomonas sp. G1. J. Hazard Mater. 297: 17-24. https://doi.org/10.1016/j.jhazmat.2015.04.052
  50. Zhang QM, Liu HY, Saleem M, Wang CX. 2019. Biotransformation of chlorothalonil by strain Stenotrophomonas acidaminiphila BJ1 isolated from farmland soil. Royal Soc. Open Sci. 6: 190562. https://doi.org/10.1098/rsos.190562
  51. Dwivedi S, Singh BR, Al-Khedhairy AA, Alarifi S, Musarrat J. 2010. Isolation and characterization of butachlor-catabolizing bacterial strain Stenotrophomonas acidaminiphila JS-1 from soil and assessment of its biodegradation potential. Lett. Appl. Microbiol. 51: 54-60. https://doi.org/10.1111/j.1472-765X.2010.02854.x
  52. Cai MY, Qian YY, Chen N, Ling TJ, Wang JJ, Jiang H, et al. 2020. Detoxification of aflatoxin B1 by Stenotrophomonas sp. CW117 and characterization the thermophilic degradation process. Environ. Pollut. 261: 114178. https://doi.org/10.1016/j.envpol.2020.114178
  53. Guo P, Wang BZ, Hang BJ, Li L, Shinawar WA, He J, et al. 2009. Pyrethroid-degrading Sphingobium sp. JZ-2 and the purification and characterization of a novel pyrethroid hydrolase. Int. Biodeter. Biodegrad. 63: 1107-1112. https://doi.org/10.1016/j.ibiod.2009.09.008
  54. Tang AX, Wang BW, Liu YY, Li QY, Tong ZF, Wei YJ. 2015. Biodegradation and extracellular enzymatic activities of Pseudomonas aeruginosa strain GF31 on β-cypermethrin. Environ. Sci. Pollut. Res. 22: 13049-13057. https://doi.org/10.1007/s11356-015-4545-0
  55. Zhao HM, Du H, Feng NX, Xiang L, Li YW, Li H, et al. 2016. Biodegradation of di-n-butyl phthalate and phthalic acid by a novel Providencia sp. 2D and its stimulation in a compost-amended soil. Biol. Fert Soils 52: 65-76. https://doi.org/10.1007/s00374-015-1054-8
  56. Yuan L, Cheng J, Chu Q, Ji X, Yuan JJ, Feng FY, et al. 2019. Di-n-butyl phthalate degrading endophytic bacterium Bacillus amyloliquefaciens subsp. strain JR20 isolated from garlic chive and its colonization in a leafy vegetable. J. Environ. Sci. Health-Part B. 54: 1-9. https://doi.org/10.1080/03601234.2018.1501143
  57. Feng L, Lu H, Cheng D, Mao X, Wu Q. 2018. Characterization and genome analysis of a phthalate esters-degrading strain Sphingobium yanoikuyae SHJ. BioMed. Res. Int. 2018: 3917054.
  58. Zhang Q, Zhang W. 2017. Microbial flora analysis for the degradation of beta-cypermethrin. Environ. Sci. Pollut. Res. 24: 6554-6562. https://doi.org/10.1007/s11356-017-8370-5
  59. Nzila A. 2013. Update on the cometabolism of organic pollutants by bacteria. Environ. Pollut. 178: 474-482. https://doi.org/10.1016/j.envpol.2013.03.042
  60. Tran NH, Urase T, Ngo HH, Hu JY,Ong SL. 2013. Insight into metabolic and cometabolic activities of autotrophic and heterotrophic microorganisms in the biodegradation of emerging trace organic contaminants. Bioresour. Technol.146: 721-731. https://doi.org/10.1016/j.biortech.2013.07.083
  61. Zhao H, Geng Y, Chen L, Tao K, Hou T. 2013. Biodegradation of cypermethrin by a novel Catellibacterium sp. strain CC-5 isolated from contaminated soil. Can. J. Microbiol. 59: 311-317. https://doi.org/10.1139/cjm-2012-0580
  62. Larisa CT, Salles JF, Dirk V. 2017. Bacterial synergism in lignocellulose biomass degradation-complementary roles of degraders as influenced by complexity of the carbon source. Front. Microbiol. 8: 1628. https://doi.org/10.3389/fmicb.2017.01628
  63. Chen C, Wang ZY, Zhao M, Yuan BH, Yao JC, Chen J, et al. 2021. A fungus-bacterium co-culture synergistically promoted nitrogen removal by enhancing enzyme activity and electron transfer. Sci. Total Environ. 754: 142109. https://doi.org/10.1016/j.scitotenv.2020.142109