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Biodegradation of Phthalic Acid Esters by the White-Rot Fungus Peniophora lycii

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Abstract—

The ability of the white-rot fungus Peniophora lycii LE-BIN 2142 to degrade such phthalic acid esters (PAEs) as diethyl phthalate (DEP), dibutyl phthalate (DBP), di(2-ethylhexyl) phthalate (DEHP), diisobutyl phthalate (DiBP), and n-butylbenzyl phthalate (BBP) was studied. It was shown that DEHP was most efficiently biodegraded by the fungus (over 98% on day 6 of cultivation). The residual content of DBP and DiBP in the culture liquid of the fungus at the end of cultivation (10 days) was ~17–18%. BBP turned out to be the most difficult-to-degrade compound: its residual content on day 10 of P. lycii cultivation was ~40%. DEP was resistant to fungal biodegradation and exhibited a toxic effect at 1.5 g/L: the rate of radial growth of the fungus on agar decreased threefold compared to the control, and the amount of fungal biomass during liquid-phase submerged cultivation decreased by about 1.5 times. During the cultivation of P. lycii on media with PAEs, an increase in esterase activity by about 2 times and a significant decrease (by 2–4 times) in oxidase activity was shown compared to the control medium without phthalates.

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REFERENCES

  1. Ahmadi, E., Yousefzadeh, S., Ansari, M., Ghaffari, H.R., Azari, A., Miri, M., Nabizadeh, A.M.R., Kakavandi, B., Ahmadi, P., Badi, M.Y., Gholami ,M., Sharafi, K., Karimaei, M., Ghoochani, M., Brahmand, M.B., et al., Performance, kinetic, and biodegradation pathway evaluation of anaerobic fixed film fixed bed reactor in removing phthalic acid esters from wastewater, Sci. Rep., 2017, vol. 7, p. 41020. https://doi.org/10.1038/srep41020

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Ahuactzin-Perez, M., Tlecuitl-Beristain, S., García-Davila, J., Santacruz-Juárez, E., González-Pérez, M., Gutiérrez-Ruíz, M.C., and Sánchez, C., Mineralization of high concentrations of the endocrine disruptor dibutyl phthalate by Fusarium culmorum, 3 Biotech., 2018, vol. 8, no. 42, pp. 1–10. https://doi.org/10.1007/s13205-017-1065-2

  3. Akerman-Sanchez, G. and Rojas-Jimenez, K. Fungi for the bioremediation of pharmaceutical-derived pollutants: a bioengineering approach to water treatment, Environ. Adv., 2021, vol. 4. 100071. https://doi.org/10.1016/j.envadv.2021.100071

    Article  CAS  Google Scholar 

  4. Boll, M., Geiger, R., Junghare, M., and Schink, B., Microbial degradation of phthalates: biochemistry and environmental implications, Environ. Microbiol. Rep., 2020, vol. 12, pp. 3–15. https://doi.org/10.1111/1758-2229.12787

    Article  CAS  PubMed  Google Scholar 

  5. Brenelli, L.B., Persinoti, G.F., Franco Cairo, J.P.L., Liberato, M.V., Gonçalves, T.A., Otero, I.V.R., Mainardi, P.H., Felby, C., Sette, L.D., and Squina, F.M., Novel redox-active enzymes for ligninolytic applications revealed from multiomics analyses of Peniophora sp. CBMAI 1063, a laccase hyper-producer strain, Sci. Rep., 2019, vol. 9, p. 17564. https://doi.org/10.1038/s41598-019-53608-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Carstens, L., Cowan, A.R., Seiwert, B., and Schlosser, D., Biotransformation of phthalate plasticizers and bisphenol A by marine-derived, freshwater, and terrestrial fungi, Front. Microbiol., 2020, vol. 11, p. 317. https://doi.org/10.3389/fmicb.2020.00317

    Article  PubMed  PubMed Central  Google Scholar 

  7. Chang, B.V., Yang, C.P., and Yang, C.W., Application of fungus enzymes in spent mushroom composts from edible mushroom cultivation for phthalate removal, Microorganisms, 2021, vol. 9, p. 1989. https://doi.org/10.3390/microorganisms9091989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Das, M.T., Kumar, S.S., Ghosh, P., Shah, G., Malyan, S.K., Bajar, S., Thakur, I.S., and Singh, L., Remediation strategies for mitigation of phthalate pollution: challenges and future perspectives, J. Hazard. Mater., 2021, vol. 409, p. 124496. https://doi.org/10.1016/j.jhazmat.2020.124496

    Article  CAS  PubMed  Google Scholar 

  9. de Souza Machado, A.A., Lau, C.W., Kloas, W., Bergmann, J., Bachelier, B.J., Faltin, E., Becker, R., Görlich, A.S., and Rillig, M.C., Microplastics can change soil properties and affect plant performance, Environ. Sci. Technol., 2019, vol. 53, pp. 6044−6052. https://doi.org/10.1021/acs.est.9b01339

    Article  CAS  PubMed  Google Scholar 

  10. Dutta, S., Haggerty, D.K., Rappolee, D.A., and Ruden, D.M., Phthalate exposure and long-term epigenomic consequences: a review, Front. Genet., 2020, vol. 11, p. 405. https://doi.org/10.3389/fgene.2020.00405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Gao, D. and Wen, Z., Phthalate esters in the environment: a critical review of their occurrence, biodegradation, and removal during wastewater treatment processes, Sci. Total Environ., 2016, vol. 541, pp. 986–1001.

    Article  CAS  PubMed  Google Scholar 

  12. González-Márquez, A., Ahuactzin-Pérez, M., and Sánchez, C., Lentinula edodes grown on di(2-ethylhexyl)phthalate-containing media: mycelial growth and enzyme activities, BioResources, 2015, vol. 10, pp. 7898–7906. https://doi.org/10.15376/biores.10.4.7898-7906

    Article  CAS  Google Scholar 

  13. Hofmann, U. and Schlosser, D., Biochemical and physicochemical processes contributing to the removal of endocrine-disrupting chemicals and pharmaceuticals by the aquatic ascomycete Phoma sp. UHH 5-1-03, Appl. Microbiol. Biotechnol., 2016, vol. 100, pp. 2381–2399. https://doi.org/10.1007/s00253-015-7113-0

    Article  CAS  PubMed  Google Scholar 

  14. Hwang, S., Choi, H.T., and Song, H., Biodegradation of endocrine-disrupting phthalates by Pleurotus ostreatus, J. Microbiol. Biotechnol., 2008, vol. 18, pp. 767–772.

    CAS  PubMed  Google Scholar 

  15. Li, H., Dai, Q., Yang, M., Li, F., Liu, X., Zhou, M., and Qian, X., Unraveling consequences of soil micro- and nano-plastic pollution on soil-plant system: implications for nitrogen (N) cycling and soil microbial activity, Chemosphere, 2020, vol. 260, p. 127578. https://doi.org/10.1016/j.chemosphere.2020.127578

    Article  CAS  Google Scholar 

  16. Ma, J., Yue, H., Li, H., Zhang, J., Zhang, Y., Wang, X., Gong, S., and Liu, G., Selective delignification of poplar wood with a newly isolated white‑rot basidiomycete Peniophora incarnata T‑7 by submerged fermentation to enhance saccharification, Biotechnol. Biofuels, 2021, vol. 14, p. 135. https://doi.org/10.1186/s13068-021-01986-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Moiseenko, K.V., Glazunova, O.A., Shakhova, N.V., Savinova, O.S., Vasina, D.V., Tyazhelova, T.V., Psurtseva, N.V., and Fedorova, T.V., Fungal adaptation to the advanced stages of wood decomposition: insights from the Steccherinum ochraceum, Microorganisms, 2019, vol. 7, p. 527. https://doi.org/10.3390/microorganisms7110527

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Naveen, K.V., Saravanakumar, K., Zhang, X., Anbazhagan, K., and Wang, M., Impact of environmental phthalate on human health and their bioremediation strategies using fungal cell factory—a review, Environ. Res., 2022, vol. 214, p. 113781. https://doi.org/10.1016/j.envres.2022.113781

    Article  CAS  PubMed  Google Scholar 

  19. Savinova, O.S., Shabaev, A.V., Glazunova, O.A., Eremin, S.A., and Fedorova, T.V., Biodestruction of phthalic acid esters by white rot fungi, Appl. Biochem. Microbiol., 2022a, vol. 58, pp. 598–612. https://doi.org/10.31857/S0555109922050142

    Article  CAS  Google Scholar 

  20. Savinova, O.S., Shabaev, A.V., Glazunova, O.A., Moiseenko, K.V., and Fedorova, T.V., Benzyl butyl phthalate and diisobutyl phthalate biodegradation by white-rot fungus Trametes hirsuta, Appl. Biochem. Microbiol., 2022b, vol. 58, suppl. 1, pp. S113‒S125. https://doi.org/10.1134/S0003683822100118

    Article  CAS  Google Scholar 

  21. Shabaev, A.V., Moiseenko, K.V., Glazunova, O.A., Savinova, O.S., and Fedorova, T.V., Comparative analysis of Peniophora lycii and Trametes hirsuta exoproteomes demonstrates “Shades of Gray” in the concept of white-rotting fungi, Int. J. Mol. Sci., 2022, vol. 23, p. 10322. https://doi.org/10.3390/ijms231810322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Shkaeva, I.E., Solntseva, S.A., Nikulia, O.S., Nikolaev, A.I., Dulov, S.A., and Zemlyanoi, A.V., Toxicity and danger of phthalates, Toksikol. Vestn., 2019, vol. 159, no. 6, pp. 3–9.

    Google Scholar 

  23. Sinitsyn, A.P, Gusakov, A.V., and Chernoglazov, V.M., Biokonversiya lignotsellyuloznykh materialov (Bioconversion of Lignocellulose Materials), Moscow: Mos. Gos. Univ., 1995.

  24. Suárez-Segundo, J.L., Vazquez-Lopez, D., Torres-Garcia, J.L., Ahuactzin-Perez, M., Montiel-Martínez, N., Tlecuitl-Beristain, S., and Sánchez, C., Growth of colonies and hyphal ultrastructure of filamentous fungi grown on dibutyl phthalate and di(2-ethylhexyl)phthalate, Revista Mexicana de Ingeniería Química, 2013, vol. 12, pp. 499–504.

    Google Scholar 

  25. Tang, Y., Zhang, Y., Jiang, L., Yang, C., and Rittmann, B.E., Enhanced dimethyl phthalate biodegradation by accelerating phthalic acid di-oxygenation, Biodegradation, 2017, vol. 28, pp. 413–421. https://doi.org/10.1007/s10532-017-9805-x

    Article  CAS  PubMed  Google Scholar 

  26. Tran, H.T., Lin, C., Bui, H.-T., Nguyen, M.K., Cao, N.D.T., Mukhtar, H., Hoang, H.G., Varjani, S., Ngo, H.H., and Nghiem, L.D., Phthalates in the environment: characteristics, fate and transport, and advanced wastewater treatment technologies, Bioresour. Technol., 2022, vol. 344, p. 126249. https://doi.org/10.1128/jcm.02479

    Article  Google Scholar 

  27. Weaver, J.A., Beverly, B.E.J., Keshava, N. Mudipalli, A., Arzuaga, X., Cai, C., Hotchkiss, A.K., Makris, S.L., and Yost, E.E., Hazards of diethyl phthalate (DEP) exposure: a systematic review of animal toxicology studies, Environ. Int., 2020, vol. 145, p. 105848. https://doi.org/10.1016/j.envint.2020.105848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Zhao, F., Wang, P., Lucardi, R.D., Su, Z., and Li, S., Natural sources and bioactivities of 2,4-di-tert-butylphenol and its analogs, Toxins, 2020, vol. 12, p. 35. https://doi.org/10.3390/toxins12010035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This research was funded by the Russian Science Foundation (grant no. 21-14-00306).

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Authors and Affiliations

  1. Bach Institute of Biochemistry, Research Center of Biotechnology, Russian Academy of Sciences, 119071, Moscow, Russia

    O. S. Savinova, A. V. Shabaev & T. V. Fedorova

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  1. O. S. Savinova
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  2. A. V. Shabaev
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  3. T. V. Fedorova
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Correspondence to T. V. Fedorova.

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Translated by E. Babchenko

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Savinova, O.S., Shabaev, A.V. & Fedorova, T.V. Biodegradation of Phthalic Acid Esters by the White-Rot Fungus Peniophora lycii. Microbiology 92, 427–433 (2023). https://doi.org/10.1134/S0026261723600222

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