Biodegradation of Benzo[a]pyrene by a White-Rot Fungus Phlebia acerina: Surfactant-Enhanced Degradation and Possible Genes Involved
Abstract
:1. Introduction
2. Materials and Methods
2.1. Fungus and Chemicals
2.2. BaP Degradation in Liquid Media by White-Rot Fungi
2.3. Cytochrome P450s Inhibition and Surfactant-Enhanced Degradation Experiments
2.4. Biomass and Enzyme Activity Estimation
2.5. RNA-Sequencing Analysis and Quantitative Real-Time PCR (qPCR)
3. Results
3.1. BaP Degradation by White-Rot Fungi and Surfactant-Enhanced BaP Degradation
3.2. Effect of Surfactant Brij 30 on Biomass and Enzyme Production
3.3. BaP Degradation Effects of Cytochrome P450s on BaP Degradation by P. acerina S-LWZ20190614-6
3.4. Transcriptome Analysis for BaP Degradation Mechanism by P. acerina S-LWZ20190614-6
3.5. qPCR Analysis
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Sahoo, B.M.; Ravi Kumar, B.V.V.; Banik, B.K.; Borah, P. Polyaromatic hydrocarbons (PAHs): Structures, synthesis and their biological profile. Curr. Org. Synth. 2020, 17, 625–640. [Google Scholar] [CrossRef] [PubMed]
- Reizer, E.; Viskolcz, B.; Fiser, B. Formation and growth mechanisms of polycyclic aromatic hydrocarbons: A mini-review. Chemosphere 2022, 291, 132793. [Google Scholar] [CrossRef]
- Dahlgren, J.; Takhar, H.; Schecter, A.; Schmidt, R.; Horsak, R.; Paepke, O.; Warshaw, R.; Lee, A.; Anderson-Mahoney, P. Residential and biological exposure assessment of chemicals from a wood treatment plant. Chemosphere 2007, 67, 279–285. [Google Scholar] [CrossRef] [PubMed]
- Kumar, M.; Bolan, N.S.; Hoang, S.A.; Sawarkar, A.D.; Jasemizad, T.; Gao, B.; Keerthanan, S.; Padhye, L.P.; Singh, L.; Kumar, S.; et al. Remediation of soils and sediments polluted with polycyclic aromatic hydrocarbons: To immobilize, mobilize, or degrade? J. Hazard. Mater. 2021, 420, 126534. [Google Scholar] [CrossRef] [PubMed]
- Xie, J.; Tao, L.; Wu, Q.; Lei, S.; Lin, T. Environmental profile, distributions and potential sources of halogenated polycyclic aromatic hydrocarbons. J. Hazard. Mater. 2021, 419, 126164. [Google Scholar] [CrossRef]
- Wang, Y.; Bao, M.; Zhang, Y.; Tan, F.; Zhao, H.; Zhang, Q.; Li, Q. Polycyclic aromatic hydrocarbons in the atmosphere and soils of Dalian, China: Source, urban-rural gradient, and air-soil exchange. Chemosphere 2020, 244, 125518. [Google Scholar] [CrossRef]
- Bai, Y.; Shi, K.; Yu, H.; Shang, N.; Hao, W.; Wang, C.; Huang, T.; Yang, H.; Huang, C. Source apportionment of polycyclic aromatic hydrocarbons (PAHs) in a sediment core from Lake Dagze Co, Tibetan Plateau, China: Comparison of three receptor models. J. Environ. Sci. 2022, 121, 224–233. [Google Scholar] [CrossRef]
- Chen, Y.; Wang, Y.; Yu, K.; Zhao, Z.; Lang, X. Occurrence characteristics and source appointment of polycyclic aromatic hydrocarbons and n-alkanes over the past 100 years in southwest China. Sci. Total Environ. 2022, 808, 151905. [Google Scholar] [CrossRef]
- Badger, G.M.; Novotny, J. Mode of Formation of 3,4-Benzopyrene at High Temperatures. Nature 1963, 198, 1086. [Google Scholar] [CrossRef]
- Keith, L.; Telliard, W. ES&T Special Report: Priority pollutants: I-a perspective view. Environ. Sci. Technol. 1979, 13, 416–423. [Google Scholar] [CrossRef]
- Cho, H.K.; Shin, H.S. Analysis of benzo[a]pyrene content from smoked food products in Korea. Food Sci. Biotechnol. 2012, 21, 1095–1100. [Google Scholar] [CrossRef]
- Francesco, B.A.; Chapman, R.S.; Silverman, D.T.; He, X.Z.; Hu, W.; Vermeulen, R.; Ning, B.F.; Fraumeni, J.F.; Rothman, N.; Lan, Q. Risk of lung cancer associated with domestic use of coal in Xuanwei, China: Retrospective cohort study. BMJ 2012, 345, e5414. [Google Scholar] [CrossRef]
- Wu, G.; Qin, R.; Luo, W. Polycyclic aromatic hydrocarbons (PAHs) in the Bohai Sea: A review of their distribution, sources, and risks. Integr. Environ. Assess. Manag. 2022, 18, 1705–1721. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Z.; He, W.; Wu, R.; Xu, F. Distribution and Relationships of Polycyclic Aromatic Hydrocarbons (PAHs) in Soils and Plants near Major Lakes in Eastern China. Toxics 2022, 10, 577. [Google Scholar] [CrossRef] [PubMed]
- Lee, B.D.; Hosomi, M.; Murakami, A. Fenton oxidation with ethanol to degrade anthracene into biodegradable 9,10-anthraquinon: A pretreatment method for anthracene-contaminated soil. Water Sci. Technol. 1998, 38, 91–97. [Google Scholar] [CrossRef]
- Yu, D.; Kazanietz, M.; Harvey, R.; Penning, T. Polycyclic aromatic hydrocarbon o-quinones inhibit the activity of the catalytic fragment of protein kinase C. Biochemistry 2002, 41, 11888–11894. [Google Scholar] [CrossRef]
- Kim, J.; Choi, H. Modeling in situ ozonation for the remediation of nonvolatile PAH-contaminated unsaturated soils. J. Contam. Hydrol. 2002, 55, 261–285. [Google Scholar] [CrossRef]
- Salihoglu, N.K.; Karaca, G.; Salihoglu, G.; Tasdemir, Y. Removal of polycyclic aromatic hydrocarbons from municipal sludge using UV light Removal of polycyclic aromatic hydrocarbons from municipal sludge using UV light. Desalin. Water Treat. 2012, 44, 324–333. [Google Scholar] [CrossRef]
- Chaillan, F.; Flèche, A.L.; Bury, E.; Phantavong, Y.; Grimont, P.; Saliot, A.; Oudot, J. Identification and biodegradation potential of tropical aerobic hydrocarbon-degrading microorganisms. Res. Microbiol. 2004, 155, 587–595. [Google Scholar] [CrossRef]
- Hara, A.; Syutsubo, K.; Harayama, S. Alcanivorax which prevails in oil-contaminated seawater exhibits broad substrate specificity for alkane degradation. Environ. Microbiol. 2003, 5, 746–753. [Google Scholar] [CrossRef]
- Bao, M.T.; Wang, L.N.; Sun, P.Y.; Cao, L.X.; Zou, J.; Li, Y.M. Biodegradation of crude oil using an efficient microbial consortium in a simulated marine environment. Mar. Pollut. Bull. 2012, 64, 1177–1185. [Google Scholar] [CrossRef] [PubMed]
- Brakstad, O.G.; Daling, P.S.; Faksness, L.G.; Almås, I.K.; Vang, S.H.; Syslak, L.; Leirvik, F. Depletion and biodegradation of hydrocarbons in dispersions and emulsions of the Macondo 252 oil generated in an oil-on-seawater mesocosm flume basin. Mar. Pollut. Bull. 2014, 84, 125–134. [Google Scholar] [CrossRef] [PubMed]
- Agrawal, N.; Verma, P.; Shahi, S.K. Degradation of polycyclic aromatic hydrocarbons (phenanthrene and pyrene) by the ligninolytic fungi Ganoderma lucidum isolated from the hardwood stump. Bioresour. Bioprocess. 2018, 5, 11. [Google Scholar] [CrossRef]
- Torres-Farradá, G.; Manzano-León, A.M.; Rineau, F.; Leal, M.R.; Thijs, S.; Jambon, I.; Put, J.; Czech, J.; Rivera, G.G.; Carleer, R.; et al. Biodegradation of polycyclic aromatic hydrocarbons by native Ganoderma sp. strains: Identification of metabolites and proposed degradation pathways. Appl. Microbiol. Biotechnol. 2019, 103, 7203–7215. [Google Scholar] [CrossRef]
- Medić, A.; Lješević, M.; Inui, H.; Beškoski, V.; Kojić, I.; Stojanović, K.; Karadžić, I. Efficient biodegradation of petroleum n-alkanes and polycyclic aromatic hydrocarbons by polyextremophilic Pseudomonas aeruginosa san ai with multidegradative capacity. RSC Adv. 2020, 10, 14060–14070. [Google Scholar] [CrossRef]
- ul Arifeen, M.Z.; Ma, Y.; Wu, T.; Chu, C.; Liu, X.; Jiang, J.; Li, D.; Xue, Y.R.; Liu, C.H. Anaerobic biodegradation of polycyclic aromatic hydrocarbons (PAHs) by fungi isolated from anaerobic coal-associated sediments at 2.5 km below the seafloor. Chemosphere 2022, 303, 135062. [Google Scholar] [CrossRef]
- Bumpus, J.A.; Tien, M.; Wright, D.; Aust, S.D. Oxidation of persistent environmental pollutants by a white rot fungus. Science 1985, 228, 1434–1436. [Google Scholar] [CrossRef]
- Bamforth, S.M.; Singleton, I. Bioremediation of polycyclic aromatic hydrocarbons: Current knowledge and future directions. J. Chem. Technol. Biotechnol. 2005, 80, 723–736. [Google Scholar] [CrossRef]
- Johannes, C.; Majcherczyk, A. Laccase activity tests and laccase inhibitors. J. Biotechnol. 2000, 78, 193–199. [Google Scholar] [CrossRef]
- Majcherczyk, A.; Johannes, C.; Hüttermann, A. Oxidation of polycyclic aromatic hydrocarbons (PAH)by laccase of Trametes versicolor. Enzyme Microb. Technol. 1998, 22, 335–341. [Google Scholar] [CrossRef]
- Cho, S.J.; Park, S.J.; Lim, J.S.; Rhee, Y.H.; Shin, K.S. Oxidation of polycyclic aromatic hydrocarbons by laccase of Coriolus hirsutus. Biotechnol. Lett. 2002, 24, 1337–1340. [Google Scholar] [CrossRef]
- Masaphy, S.; Levanon, D.; Henis, Y.; Venkateswarlu, K.; Kelly, S.L. Evidence for cytochrome P-450 and P-450-mediated benzo(a)pyrene hydroxylation in the white rot fungus Phanerochaete chrysosporium. FEMS Microbiol. Lett. 1996, 135, 51–55. [Google Scholar] [CrossRef] [PubMed]
- Syed, K.; Doddapaneni, H.; Subramanian, V.; Lam, Y.W.; Yadav, J.S. Genome-to-function characterization of novel fungal P450 monooxygenases oxidizing polycyclic aromatic hydrocarbons (PAHs). Biochem. Biophys. Res. Commun. 2010, 399, 492–497. [Google Scholar] [CrossRef] [PubMed]
- Li, Q.Y.; Wang, J.Q.; Wang, Z.Y.; Zhang, W.Q.; Zhan, H.J.; Xiao, T.F.; Yu, X.L.; Zheng, Y. Surfactants double the biodegradation rate of persistent polycyclic aromatic hydrocarbons (PAHs) by a white-rot fungus Phanerochaete sordida. Environ. Earth Sci. 2023, 82, 285. [Google Scholar] [CrossRef]
- Lee, A.H.; Lee, H.; Heo, Y.M.; Lim, Y.W.; Kim, C.M.; Kim, G.H.; Chang, W.; Kim, J.J. A proposed stepwise screening framework for the selection of polycyclic aromatic hydrocarbon (PAH)-degrading white rot fungi. Bioprocess Biosyst. Eng. 2020, 43, 767–783. [Google Scholar] [CrossRef]
- Tien, M.; Kirk, T.K. Lignin Peroxidase of Phanerochaete chrysosporium. Meth. Enzymol. 1988, 161, 238–249. [Google Scholar] [CrossRef]
- Wang, J.Q.; Yin, R.; Zhang, X.; Wang, N.N.; Xiao, P.F.; Hirai, H.; Xiao, T.F. Transcriptomic analysis reveals ligninolytic enzymes of white-rot fungus Phanerochaete sordida YK-624 participating in bisphenol F biodegradation under ligninolytic conditions. Environ. Sci. Pollut. Res. 2021, 28, 62390–62397. [Google Scholar] [CrossRef]
- Cabana, H.; Alexandre, C.; Agathos, S.N.; Jones, J.P. Immobilization of laccase from the white rot fungus Coriolopsis polyzona and use of the immobilized biocatalyst for the continuous elimination of endocrine disrupting chemicals. Bioresour. Technol. 2009, 100, 3447–3458. [Google Scholar] [CrossRef]
- Yin, R.; Zhang, X.; Wang, B.J.; Jia, J.B.; Wang, N.N.; Xie, C.Y.; Su, P.Y.; Xiao, P.F.; Wang, J.Q.; Xiao, T.F.; et al. Biotransformation of bisphenol F by white-rot fungus Phanerochaete sordida YK-624 under non-ligninolytic condition. Appl. Microbiol. Biotechnol. 2022, 106, 6277–6287. [Google Scholar] [CrossRef]
- Ghosh, I.; Mukherji, S. Diverse effect of surfactants on pyrene biodegradation by a Pseudomonas strain utilizing pyrene by cell surface hydrophobicity induction. Int. Biodeterior. Biodegrad. 2016, 108, 67–75. [Google Scholar] [CrossRef]
- Shome, A.; Roy, S.; Das, P.K. Nonionic Surfactants: A key to enhance the enzyme activity at cationic reverse micellar interface. Langmuir 2007, 23, 4130–4136. [Google Scholar] [CrossRef] [PubMed]
- Hadibarata, T.; Kristanti, R.A. Fluorene biodegradation and identification of transformation products by white-rot fungus Armillaria sp. F022. Biodegradation 2014, 25, 373–382. [Google Scholar] [CrossRef] [PubMed]
- Cao, H.; Wang, C.; Liu, H.; Jia, W.; Sun, H. Enzyme activities during Benzo[a]pyrene degradation by the fungus Lasiodiplodia theobromae isolated from a polluted soil. Sci. Rep. 2020, 10, 865. [Google Scholar] [CrossRef]
- Park, H.; Min, B.; Jang, Y.; Kim, J.; Lipzen, A.; Sharma, A.; Andreopoulos, B.; Johnson, J.; Riley, R.; Spatafora, J.W.; et al. Comprehensive genomic and transcriptomic analysis of polycyclic aromatic hydrocarbon degradation by a mycoremediation fungus, Dentipellis sp. KUC8613. Appl. Microbiol. Biotechnol. 2019, 103, 8145–8155. [Google Scholar] [CrossRef] [PubMed]
- Li, Q.W.; Liu, J.C.; Gadd, G.M. Fungal bioremediation of soil co-contaminated with petroleum hydrocarbons and toxic metals. Appl. Microbiol. Biotechnol. 2020, 104, 8999–9008. [Google Scholar] [CrossRef]
- Haritash, A.K.; Kaushik, C.P. Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): A review. J. Hazard. Mater. 2009, 169, 1–15. [Google Scholar] [CrossRef] [PubMed]
- Marco-Urrea, E.; Pérez-Trujillo, M.; Vicent, T.; Caminal, G. Ability of white-rot fungi to remove selected pharmaceuticals and identification of degradation products of ibuprofen by Trametes versicolor. Chemosphere 2009, 74, 765–772. [Google Scholar] [CrossRef]
- Xiao, P.; Kondo, R. Potency of Phlebia species of white rot fungi for the aerobic degradation, transformation and mineralization of lindane. J. Microbiol. 2020, 58, 395–404. [Google Scholar] [CrossRef]
- Lin, S.; Wei, J.; Yang, B.; Zhang, M.; Zhuo, R. Bioremediation of organic pollutants by white rot fungal cytochrome P450: The role and mechanism of CYP450 in biodegradation. Chemosphere 2022, 301, 134776. [Google Scholar] [CrossRef]
- Sant, D.G.; Tupe, S.G.; Ramana, C.V.; Deshpande, M.V. Fungal cell membrane-promising drug target for antifungal therapy. J. Appl. Microbiol. 2016, 121, 1498–1510. [Google Scholar] [CrossRef]
- Barnsley, E.A. The bacterial degradation of fluoranthene and benzo[a]pyrene. Can. J. Microbiol. 1975, 21, 1004–1008. [Google Scholar] [CrossRef] [PubMed]
- Hirari, H.; Kondo, R.; Sakai, K. Screening of lignin-degrading fungi and their ligninolytic enzyme activities during biological bleaching of kraft pulp. Mokuzai Gakkaishi. 1994, 40, 980–986. Available online: https://agriknowledge.affrc.go.jp/RN/201050270 (accessed on 5 March 2011).
- Wang, J.Q.; Ogata, M.; Hirai, H.; Kawagishi, H. Detoxification of aflatoxin B1 by manganese peroxidase from the white-rot fungus Phanerochaete sordida YK-624. FEMS Microbiol. Lett. 2011, 314, 164–169. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.Q.; Yamamoto, Y.; Hirai, H.; Kawagishi, H. Dimerization of bisphenol A by hyper lignin-degrading fungus Phanerochaete sordida YK-624 under ligninolytic condition. Curr. Microbiol. 2013, 66, 544–547. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.Q.; Yamamoto, R.; Yamamoto, Y.; Tokumoto, T.; Dong, J.; Thomas, P.; Hirai, H.; Kawagishi, H. Hydroxylation of bisphenol A by hyper lignin-degrading fungus Phanerochaete sordida YK-624 under non-ligninolytic condition. Chemosphere 2013, 93, 1419–1423. [Google Scholar] [CrossRef]
- Wang, J.Q.; Tanaka, Y.; Ohno, H.; Jia, J.B.; Mori, T.; Xiao, T.F.; Yan, B.; Kawagishi, H.; Hirai, H. Biotransformation and detoxification of the neonicotinoid insecticides nitenpyram and dinotefuran by Phanerochaete sordida YK-624. Environ. Pollut. 2019, 252, 856–862. [Google Scholar] [CrossRef]
- Masrat, R.; Maswal, M.; Dar, A. Competitive solubilization of naphthalene and pyrene in various micellar systems. J. Hazard. Mater. 2013, 244–245, 662–670. [Google Scholar] [CrossRef]
- Lamichhane, S.; Bal Krishna, K.C.; Sarukkalige, R. Surfactant-enhanced remediation of polycyclic aromatic hydrocarbons: A review. J. Environ. Manag. 2017, 199, 46–61. [Google Scholar] [CrossRef]
- Zeng, J.; Zhu, Q.; Wu, Y.; Shan, J.; Ji, R.; Lin, X. Oxidation of benzo[a]pyrene by laccase in soil enhances bound residue formation and reduces disturbance to soil bacterial community composition. Environ. Pollut. 2018, 242, 462–469. [Google Scholar] [CrossRef]
- Premnath, N.; Mohanrasu, K.; Guru Raj Rao, R.; Dinesh, G.H.; Prakash, G.S.; Ananthi, V.; Ponnuchamy, K.; Muthusamy, G.; Arun, A. A crucial review on polycyclic aromatic Hydrocarbons—Environmental occurrence and strategies for microbial degradation. Chemosphere 2021, 280, 130608. [Google Scholar] [CrossRef]
- Hadibarata, T.; Kristanti, R.A.; Bilal, M.; Al-Mohaimeed, A.M.; Chen, T.W.; Lam, M.K. Microbial degradation and transformation of benzo[a]pyrene by using a white-rot fungus Pleurotus eryngii F032. Chemosphere 2022, 307, 136014. [Google Scholar] [CrossRef] [PubMed]
- Korripally, P.; Hunt, C.G.; Houtman, C.J.; Jones, D.C.; Kitin, P.J.; Cullen, D.; Hammel, K.E. Regulation of gene expression during the onset of ligninolytic oxidation by Phanerochaete chrysosporium on spruce wood. Appl. Environ. Microbiol. 2015, 81, 7802–7812. [Google Scholar] [CrossRef] [PubMed]
- Ichinose, H.; Kitaoka, T. Insight into metabolic diversity of the brown-rot basidiomycete Postia placenta responsible for sesquiterpene biosynthesis: Semi-comprehensive screening of cytochrome P450 monooxygenase involved in protoilludene metabolism. Microb. Biotechnol. 2018, 11, 952–965. [Google Scholar] [CrossRef] [PubMed]
- Mori, T.; Dohra, H.; Kawagishi, H.; Hirai, H. The complete mitochondrial genome of the white-rot fungus Phanerochaete sordida YK-624. Mitochondrial DNA B 2022, 7, 1743–1745. [Google Scholar] [CrossRef]
- Wang, Y.; Zeng, X.; Liu, W. De novo transcriptomic analysis during Lentinula Edodes fruiting body growth. Gene 2018, 641, 326–334. [Google Scholar] [CrossRef]
- Chen, Z.; Yu, J.; Feng, Y.; Ma, M.; Wansong, Y.; Guo, X. Transcriptome different analysis of Tremella aurantialba at mycelium and fruiting body stages. Biotechnol. Bull. 2021, 376, 73–84. [Google Scholar] [CrossRef]
- Bezalel, L.; Hadar, Y.; Fu, P.P.; Freeman, J.P.; Cerniglia, C.E. Metabolism of phenanthrene by the white rot fungus Pleurotus ostreatus. Appl. Environ. Microbiol. 1996, 62, 2547–2553. [Google Scholar] [CrossRef]
- Durairaj, P.; Hur, J.S.; Yun, H. Versatile biocatalysis of fungal cytochrome P450 monooxygenases. Microb. Cell Fact. 2016, 15, 125. [Google Scholar] [CrossRef]
- Bhattacharya, S.S.; Yadav, J.S. Microbial P450 enzymes in bioremediation and drug discovery: Emerging potentials and challenges. Curr. Protein Pept. Sci. 2018, 19, 75–86. [Google Scholar] [CrossRef]
- Peng, T.; Kan, J.; Hu, J.; Hu, Z. Genes and novel sRNAs involved in PAHs degradation in marine bacteria Rhodococcus sp. P14 revealed by the genome and transcriptome analysis. 3 Biotech 2020, 10, 140. [Google Scholar] [CrossRef]
- Peng, S.; Wu, W.; Chen, J. Removal of PAHs with surfactant-enhanced soil washing: Influencing factors and removal effectiveness. Chemosphere 2011, 82, 1173–1177. [Google Scholar] [CrossRef] [PubMed]
- Pan, T.; Deng, T.; Zeng, X.; Dong, W.; Yu, S. Extractive biodegradation and bioavailability assessment of phenanthrene in the cloud point system by Sphingomonas polyaromaticivorans. Appl. Microbiol. Biotechnol. 2016, 100, 431–437. [Google Scholar] [CrossRef] [PubMed]
- Varade, S.R.; Ghosh, P. Foaming in aqueous solutions of zwitterionic surfactant: Effects of oil and salts. J. Dispers. Sci. Technol. 2017, 38, 1174–1191. [Google Scholar] [CrossRef]
- Lombard, V.; Golaconda Ramulu, H.; Drula, E.; Coutinho, P.M.; Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 2014, 42, D490–D495. [Google Scholar] [CrossRef]
- Häkkinen, M.; Arvas, M.; Oja, M.; Aro, N.; Penttilä, M.; Saloheimo, M.; Pakula, T.M. Re-annotation of the CAZy genes of Trichoderma reesei and transcription in the presence of lignocellulosic substrates. Microb. Cell Factories 2012, 11, 134. [Google Scholar] [CrossRef]
- Hori, C.; Gaskell, J.; Igarashi, K.; Kersten, P.; Mozuch, M.; Samejima, M.; Cullen, D. Temporal alterations in the secretome of the selective ligninolytic fungus Ceriporiopsis subvermispora during growth on aspen wood reveal this organism’s strategy for degrading lignocellulose. Appl. Environ. Microbiol. 2014, 80, 2062–2070. [Google Scholar] [CrossRef]
- Jeong, C.B.; Kim, D.H.; Kang, H.M.; Lee, Y.H.; Kim, H.S.; Kim, I.C.; Lee, J.S. Genome-wide identification of ATP-binding cassette (ABC) transporters and their roles in response to polycyclic aromatic hydrocarbons (PAHs) in the copepod Paracyclopina nana. Aquat. Toxicol. 2017, 183, 144–155. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zhang, W.; Li, Q.; Wang, J.; Wang, Z.; Zhan, H.; Yu, X.; Zheng, Y.; Xiao, T.; Zhou, L.-W. Biodegradation of Benzo[a]pyrene by a White-Rot Fungus Phlebia acerina: Surfactant-Enhanced Degradation and Possible Genes Involved. J. Fungi 2023, 9, 978. https://doi.org/10.3390/jof9100978
Zhang W, Li Q, Wang J, Wang Z, Zhan H, Yu X, Zheng Y, Xiao T, Zhou L-W. Biodegradation of Benzo[a]pyrene by a White-Rot Fungus Phlebia acerina: Surfactant-Enhanced Degradation and Possible Genes Involved. Journal of Fungi. 2023; 9(10):978. https://doi.org/10.3390/jof9100978
Chicago/Turabian StyleZhang, Wenquan, Qiaoyu Li, Jianqiao Wang, Ziyu Wang, Hongjie Zhan, Xiaolong Yu, Yan Zheng, Tangfu Xiao, and Li-Wei Zhou. 2023. "Biodegradation of Benzo[a]pyrene by a White-Rot Fungus Phlebia acerina: Surfactant-Enhanced Degradation and Possible Genes Involved" Journal of Fungi 9, no. 10: 978. https://doi.org/10.3390/jof9100978