Abstract
A promising bacterial strain for biodegrading dibutyl phthalate (DBP) was successfully isolated from activated sludge and characterized as a potential novel Microbacterium sp. USTB-Y based on 16S rRNA sequence analysis and whole genome average nucleotide identity (ANI). Initial DBP of 50 mg/L could be completely biodegraded by USTB-Y both in mineral salt medium and in DBP artificially contaminated soil within 12 h at the optimal culture conditions of pH 7.5 and 30 ℃, which indicates that USTB-Y has a strong ability in DBP biodegradation. Phthalic acid (PA) was identified as the end-product of DBP biodegraded by USTB-Y using GC/MS. The draft genome of USTB-Y was sequenced by Illumina NovaSeq and 29 and 188 genes encoding for putative esterase/carboxylesterase and hydrolase/alpha/beta hydrolase were annotated based on NR (non redundant protein sequence database) analysis, respectively. Gene3781 and gene3780 from strain USTB-Y showed 100% identity with dpeH and mpeH from Microbacterium sp. PAE-1. But no phthalate catabolic gene (pht) cluster was found in the genome of strain USTB-Y. The results in the present study are valuable for obtaining a more holistic understanding on diverse genetic mechanisms of PAEs biodegrading Microbacterium sp. strains.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adeogun AO, Ibor OR, Omogbemi ED, Chukwuka AV, Adegbola RA, Adewuyi GA, Arukwe A (2015) Environmental occurrence and biota concentration of phthalate esters in Epe and Lagos Lagoons, Nigeria. Mar Environ Res 108:24–32. https://doi.org/10.1016/j.marenvres.2015.04.002
Benjamin S, Pradeep S, Josh MS, Kumar S, Masai E (2015) A monograph on the remediation of hazardous phthalates. J Hazard Mater 298:58–72. https://doi.org/10.1016/j.jhazmat.2015.05.004
Cazals F, Huguenot D, Crampon M et al (2019) Production of biosurfactant using the endemic bacterial community of a PAHs contaminated soil, and its potential use for PAHs remobilization. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2019.136143
Chen JA, Li X, Li J, Cao J, Qiu ZQ, Zhao Q, Xu C, Shu WQ (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. https://doi.org/10.1007/s00253-006-0700-3
Chen X, Zhang XL, Yang Y, Yue DM, Xiao L, Yang LY (2015) Biodegradation of an endocrine-disrupting chemical di-n-butyl phthalate by newly isolated Camelimonas sp. and enzymatic properties of its hydrolase. Biodegradation 26:171–182. https://doi.org/10.1007/s10532-015-9725-6
Daiem MMA, Rivera-Utrilla J, Ocampo-Pérez R, Mendez-Diaz JD, 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. https://doi.org/10.1016/j.jenvman.2012.05.014
European Union (1993) Council Regulation (EEC), No 793/93 of 23 March 1993 on the evaluation and control of the risks of existing substances (OJ L84, 5 April 1993). European Union, Brussels
Feng L, Liu H, Cheng D, Mao XM, Wang Y, Wu Z, Wu Q (2018a) Characterization and genome analysis of a phthalate esters-degrading strain Sphingobium yanoikuyae SHJ. BioMed Res Int. https://doi.org/10.1155/2018/3917054
Feng NX, Yu J, Mo CH, Zhao HM, Li YW, Wu BX, Wong MH et al (2018b) Biodegradation of di-n-butyl phthalate (DBP) by a novel endophytic Bacillus megaterium strain YJB3. Sci Total Environ 616–617:117–127. https://doi.org/10.1016/j.scitotenv.2017.10.298
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. https://doi.org/10.1016/j.scitotenv.2015.09.148
He Z, Xiao H, Tang L, Min H, Lu Z (2013) Biodegradation of di-n-butyl phthalate by a stable bacterial consortium, HD-1, enriched from activated sludge. Biores Technol 128:526–532. https://doi.org/10.1016/j.biortech.2012.10.107
Heo J, Cho HY, Kim MA, Hamada M, Tamura T, Saitou S, Kim SJ, Kwon SW (2020) Microbacterium protaetiae sp. nov., isolated from gut of larva of Protaetia brevitarsis seulensis. Int J Syst Evol Microbiol 70:2226–2232. https://doi.org/10.1099/ijsem.0.003967
Huang YH, Huang XJ, Chen XH, Cai QY, Chen SH, Mo CH, Lü HX, Wong MH (2018) Biodegradation of di-butyl phthalate (DBP) by a novel endophytic bacterium Bacillus subtilis and its bioaugmentation for removing DBP from vegetation slurry. J Environ Manage 224:1–9. https://doi.org/10.1016/j.jenvman.2018.07.023
Iwata M, Imaoka T, Nishiyama T, Fujii T (2016) Re-characterization of mono-2-ethylhexyl phthalate hydrolase belonging to the serine hydrolase family. J Biosci Bioeng 122:140–145. https://doi.org/10.1016/j.jbiosc.2016.01.008
Jin DC, Kong X, Liu HJ, Wang XX, Deng Y, Jia MH, Yu XY (2016) Characterization and genomic analysis of a highly efficient dibutyl phthalate-degrading bacterium Gordonia sp. Strain QH-12. Int J Mol Sci 17:1012. https://doi.org/10.3390/ijms17071012
Kim M, Oh HS, Park SC, Chun J (2014) Towards a taxonomic coherence between average nucleotide identity and 16SrRNA gene sequence similarity for species demarcation of prokaryotes. Int J Syst Evol Microbiol 64(2):346–351. https://doi.org/10.1099/ijs.0.059774-0
Latini G, Del Vecchio A, Massaro M, Verrotti A, De Felice C (2006) Phthalate exposure and male infertility. Toxicology 226(2–3):90–98. https://doi.org/10.1016/j.tox.2006.07.011
Lei J, Wei S, Ren L, Hu S, Chen P (2017) Hydrolysis mechanism of carbendazim hydrolase from the strain Microbacterium sp. djl-6F. J Environ Sci 54:171–177. https://doi.org/10.1016/j.jes.2016.05.027
Li J, Chen JA, Zhao Q, Li X, Shu W (2006) Bioremediation of environmental endocrine disruptor di-n-butyl phthalate ester by Rhodococcus ruber. Chemosphere 65(9):1627–1633. https://doi.org/10.1016/j.chemosphere.2006.03.005
Liang DW, Zhang T, Fang HHP, He JZ (2008) Phthalates biodegradation in the environment. Appl Microbiol Biotechnol 80:183–198. https://doi.org/10.1007/s00253-008-1548-5
Liu DD, Yan JL, Wang L, Zhang YZ, Liu DL, 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. https://doi.org/10.1016/j.ibiod.2015.09.019
Lü H, Mo CH, Zhao HM, Xiang L, Katsoyiannis A, Li YW, Cai QY, Wong MH (2018) Soil contamination and sources of phthalates and its health risk in China: a review. Environ Res 164:417–429. https://doi.org/10.1016/j.envres.2018.03.013
Lu MY, Jiang WK, Gao QQ, Zhang ML, Hong Q (2020) Degradation of dibutyl phthalate (DBP) by a bacterial consortium and characterization of two novel esterases capable of hydrolyzing PAEs sequentially. Ecotoxicol Environ Saf 195:110517. https://doi.org/10.1016/j.ecoenv.2020.110517
Mathieu-Denoncourt J, de Solla SR, Langlois VS (2015) Chronic exposures to monomethyl phthalate in western clawed frogs. Gen Comp Endocrinol 219:53–63. https://doi.org/10.1016/j.ygcen.2015.01.019
Nahurira R, Ren L, Song J, Jia Y, Wang J, Fan S, Wang H, Yan Y (2017) Degradation of di-(2-ethylhexyl) phthalate by a novel Gordonia alkanivorans strain YC-RL2. Curr Microbiol 74:1–11. https://doi.org/10.1007/s00284-016-1159-9
Philip JM, Aravind UK, Aravindakumar CT (2018) Emerging contaminants in Indian environmental matrices-a review. Chemosphere 190:307–326. https://doi.org/10.1016/j.chemosphere.2017.09.120
Qin W, Zhu Y, Fan F, Wang Y, Liu X, Ding A, Dou J (2017) Biodegradation of benzo (a) pyrene by Microbacterium sp. strain under denitrification: degradation pathway and effects of limiting electron acceptors or carbon source. Biochem Eng J 121:131–138. https://doi.org/10.1016/j.bej.2017.02.001
Ren L, Lin Z, Liu HM, Hu HQ (2018) Bacteria-mediated phthalic acid esters degradation and related molecular mechanisms. Appl Microbiol Biotechnol 102:1085–1096. https://doi.org/10.1007/s00253-017-8687-5
Ricken B, Fellmann O, Kohler HPE, Schaffer A, Corvini PFX, Kolvenbach BA (2015) Degradation of sulfonamide antibiotics by Microbacterium sp strain BR1- elucidating the downstream pathway. New Biotechnol 32(6):710–715. https://doi.org/10.1016/j.nbt.2015.03.005
Schippers A (2005) Microbacterium oleivorans sp. nov. and Microbacterium hydrocarbonoxydans sp. nov. novel crude-oil-degrading Gram-positive bacteria. Int J Syst Evol Microbiol 55(2):655–660. https://doi.org/10.1099/ijs.0.63305-0
Shen S, Wang XY, Wang HX, Ren H, Lü ZM (2019) Advances in biodegradation of phthalates esters (Article in Chinese). Sheng Wu Gong Gheng Xue Bao 35(11):2104–2120. https://doi.org/10.13345/j.cjb.190177
Stojanoska MM, Milosevic N, Milic N, Abenavoli L (2017) The influence of phthalates and bisphenol A on the obesity development and glucose metabolism disorders. Endocrine 55(3):666–681. https://doi.org/10.1007/s12020-016-1158-4
Suzuki K, Hamada M, Genus I, Orla-Jensen M. 179AL emend. Takeuchi and Hatano 1998b, 744VP. In: Goodfellow M, Kämpfer P, Busse HJ, Trujillo ME and Suzuki K (editors). Bergey’s Manual of Systematic Bacteriology. 2012. Athens, 1919: 814–852
Tichonovas M, Krugly E, Jankunaite D, Racys V, Martuzevicius D (2017) Ozone-UV-catalysis based advanced oxidation process for wastewater treatment. Environ Sci Pollut Res 24:17584–17597. https://doi.org/10.1007/s11356-017-9381-y
US EPA, 1992 and update. Code of federal regulations. 40 CFR, Part 136 Union E. 1993. Council Regulation (EEC), No 793/93 of 23 March 1993 on the evaluation and control of the risks of existing substances (OJ L84, 5 April 1993). European Union, Brussels.
Wang YY, Fan YZ, Gu JD (2003) Aerobic degradation of phthalic acid by Comamonas acidovoran Fy-1 and dimethyl phthalate ester by two reconstituted consortia from sewage sludge at high concentrations. World J Microbiol Biotechnol 19:811–815. https://doi.org/10.1023/A:1026021424385
Wang YY, Li FF, Ruan XL, Song J, Lv L, Chai LY, Yang ZH, Luo L (2017) Biodegradation of di-n-butyl phthalate by bacterial consortium LV-1 enriched from river sludge. PLoS ONE 12(5):e0178213. https://doi.org/10.1371/journal.pone.0178213
Wu XL, Wang YY, Dai QY, Liang RX, Jin DC (2011) Isolation and characterization of four di-n-butyl phthalate (DBP)-degrading Gordonia sp. strains and cloning the 3, 4-phthalate dioxygenase gene. World J Microbiol Biotechnol 27:2611–2617. https://doi.org/10.1007/s11274-011-0734-2
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 97:2275–2275. https://doi.org/10.1007/s00253-012-4232-8
Xu X, Li H, Gu J (2005) Biodegradation of an endocrine-disrupting chemical dibutyl phthalate ester by Pseudomonas fluorescens B-1. Int Biodeterior Biodegrad 55(1):9–15. https://doi.org/10.1016/j.procbio.2011.01.031
Yang J, Guo CL, Liu SS, Liu WT, Wang H, Dang Z, Lu G (2018) Characterization of a di-n-butyl phthalate-degrading bacterial consortium and its application in contaminated soil. Environ Sci Pollut Res 25(18):17645–17653. https://doi.org/10.1007/s11356-018-1862-0
You S, Hu Y, Liu X, Wei C, Wei C (2018) Synergetic removal of Pb (II) and dibutyl phthalate mixed pollutants on Bi2O3–TiO2 composite photocatalyst under visible light. Appl Catal B - Environ 232:288–298. https://doi.org/10.1016/j.apcatb.2018.03.025
Yu YY, Yin H, Peng H, Lu GN, Dang Z (2019) Proteomic mechanism of decabromodiphenyl ether (BDE-209) biodegradation by Microbacterium Y2 and its potential in remediation of BDE-209 contaminated water-sediment system. J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2019.121708
Zhao HM, Du H, Feng NX, Xiang L, Li YW, Li H, Cai QY, Mo CH (2016) Biodegradation of di-n-butylphthalate and phthalic acid by a novel Providencia sp. 2D and its stimulation in a compost-amended soil. Biol Fertil Soils 52:65–76. https://doi.org/10.1007/s00374-015-1054-8
Zhao ZZ, Liu C, Xu Q, Liu Y, Yan H (2021) Pathway for biodegrading coumarin by a newly isolated Pseudomonas sp. USTB-Y. World J Microbiol Biotechnol 37(5):89. https://doi.org/10.1007/s11274-021-03055-w
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Grant No. 21677011) and the Fundamental Research Funds for the Central Universities (PRF-MP-20-39).
Author information
Authors and Affiliations
Contributions
ZZ and HY conceived and designed the experiments. ZZ performed the experiments. CL and SA were involved in sample preparation. QX, AA, HZ, YL and YP were involved in identification of biodegradation products and genome analysis. Data was statistically analyzed by ZZ. The paper was written by ZZ, reviewed and edited by HY.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhao, Z., Liu, C., Xu, Q. et al. Characterization and genomic analysis of an efficient dibutyl phthalate degrading bacterium Microbacterium sp. USTB-Y. World J Microbiol Biotechnol 37, 212 (2021). https://doi.org/10.1007/s11274-021-03181-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-021-03181-5