2024 Ecosystem Transformation 7 (4), 3-20

Nonylphenol biodegradation by Pseudomonas umsongensis bacterial strain in aquatic medium and soil microcosm

Zaytseva T.B. , Medvedeva N.G.

Environmental pollution with nonylphenols (NPs) is a serious environmental problem due to their persistence, toxicity and ability to have a negative impact on the endocrine system of humans and animals. Biodegradation of NPs is the most environmentally safe and effective way to reduce their content in water and soil ecosystems. A novel bacterial strain, Pseudomonas umsongensis 16, capable of degrading NP in aquatic media and soil microcosm, was isolated from soddy-podzolic soil contaminated with NP. The strain 16 exhibits the ability to degrade NP in a wide range of temperatures (from +5 to +35°C), pH (5–9), and xenobiotic concentrations up to 500 mg/l. Bioaugmentation of nonylphenol contaminated soil by cells of P. umsongensis 16 leads to an increase in the efficiency of NP destruction in the soil microcosm. The degree of pollutant degradation increases by 1.9 times with a 6.4-fold reduction in the time of its half-removal as compared with the soil microcosm without the introduction of the destructor strain cells. It has been established that as a result of bioaugmentation in soil contaminated with NP, the activity of the soil enzyme urease is restored to the level of uncontaminated soil. The results obtained can be used in the development of biotechnology for the purification of environmental objects contaminated with nonylphenols.

T. B. Zaytseva
St. Petersburg Federal Research Center of the Russian Academy of Sciences (SPC RAS), Scientific Research Centre for Ecological Safety of the Russian Academy of Sciences
18 Korpusnaya st., St. Petersburg, 197110 Russia

zaytseva.62@list.ru

N. G. Medvedeva
St. Petersburg Federal Research Center of the Russian Academy of Sciences (SPC RAS), Scientific Research Centre for Ecological Safety of the Russian Academy of Sciences
ul. Korpusnaya 18, St. Petersburg, 197110 Russia

Acir, I.-H., Guenther, K., 2018. Endocrine-disrupting metabolites of alkylphenol ethoxylates – A critical
review of analytical methods, environmental occurrences, toxicity, and regulation. Science of The
Total Environment 635, 1530–1546. http://doi.org/10.1016/j.scitotenv.2018.04.079
Bacosa, H.P., Ancla, S.M.B., Arcadio, C.G.L.A., Dalogdog, J.R.A., Ellos, D.M.C. et al., 2022. From
surface water to the deep sea: A review on factors affecting the biodegradation of spilled oil in
marine environment. Journal of Marine Science and Engineering 10, 426. https://doi.org/10.3390/
jmse10030426
Bai, N., Abuduaini, R., Wang, S., Zhang, M., Zhu, X., Zhao, Y., 2017. Nonylphenol biodegradation
characterizations and bacterial composition analysis of an effective consortium NP-M2. Environmental
Pollution 220, 95–104. https://doi.org/10.1016/j.envpol.2016.09.027
Bhandari, G., Bagheri, A.R., Bhatt, P., Bilal, M., 2021. Occurrence, potential ecological risks, and
degradation of endocrine disrupter, nonylphenol, from the aqueous environment. Chemosphere 275,
130013. https://doi.org/10.1016/j.chemosphere.2021.130013
Burlachenko, A.S., Salishcheva, O.V., Dyshlyuk, L.S., Prosekov, A.Y., 2021. Investigation of the
kinetic regularities of the process of biodegradation of betaine surfactant by bacteria of the genus
Pseudomonas. Applied Science 11 (19), 8939. https://doi.org/10.3390/app11198939
Careghini, A., Mastorgio, A.F., Saponaro, S., Sezenna, E., 2015. Bisphenol A, nonylphenols,
benzophenones, and benzotriazoles in soils, groundwater, surface water, sediments, and food: a review. Environmental Science and Pollution Research 22, 5711–5741. https://doi.org/10.1007/s11356-014-3974-5
De Bruin, W., Kritzinger, Q., Bornman, R., Korsten, L., 2019. Occurrence, fate and toxic effects of the
industrial endocrine disrupter, nonylphenol, on plants – A review. Ecotoxicology and Environmental
Safety 181, 419–427. https://doi.org/10.1016/j.ecoenv.2019.06.009
Diehl, J., Johnson, S.E., Xia, K., West, A., Tomanek, L., 2012. The distribution of 4-nonylphenol in
marine organisms of North American Pacific Coast estuaries. Chemosphere 87 (5), 490–497. https://
doi.org/10.1016/j.chemosphere.2011.12
Domene, X., Ramírez, W., Solà, L., Alcañiz, J.M., Andrés, P., 2009. Soil pollution by nonylphenol and
nonylphenol ethoxylates and their effects to plants and invertebrates. Journal of Soils and Sediments
9 (6), 555–567. https://doi.org/10.1007/s11368-009-0117-6
Forte, M., Di Lorenzo, M., Carrizzo, A., Valiante, S., Vecchione, C., Laforgia, V., De Falco, M., 2016.
Nonylphenol effects on human prostate non tumorigenic cells. Toxicology 357–358, 21–32. https://
doi.org/10.1016/j.tox.2016.05.024
Gautam, G.J., Chaube, R., Joy, K., 2015. Toxicity and tissue accumulation of 4-nonylphenol in the catfish
Heteropneustes fossilis with a note on prevalence of 4-NP in water samples. Endocrine Disruptors 3
(1), e981442. https://doi.org/10.4161/23273747.2014.981442
Huang, W., Yin, H., Yu, Y., Lu, G., Dang, Z., Chen, Z., 2020. Co-metabolic degradation of
tetrabromobisphenol A by Pseudomonas aeruginosa and its auto-poisoning effect caused during
degradation process. Ecotoxicology and Environmental Safety 202 (1), 110919. https://doi.org/10.1016/j.ecoenv.2020.110919
Ismanto, A., Hadibarata, T., Kristanti, R.A., Maslukah, L., Safinatunnajah, N., Kusumastuti, W., 2022.
Endocrine disrupting chemicals (EDCs) in environmental matrices: Occurrence, fate, health impact,
physio-chemical and bioremediation technology. Environmental Pollution 302, 119061. https://doi.org/10.1016/j.envpol.2022.119061
Ivey, C.D., Wang, N., Alvarez, D., Hammer, E.J., Bauer, C.R., 2018. Chronic toxicity of 4-nonylphenol to
two unionid mussels in water-only exposures. Bulletin of Environmental Contamination and Toxicology
101, 423–427. https://doi.org/10.1007/s00128-018-2422-5
Jiang, L., Yang, Y., Jia, L.X., Liu, Y., Pan, B., Lin, Y., 2018. Effects of earthworm casts on sorption
desorption, degradation, and bioavailability of nonylphenol in soil. Environmental Science and
Pollution Research 25, 7968–7977. https://doi.org/10.1007/s11356-017-1130-8
Jiang, L., Yang, Y., Zhang, Y., Liu, Y., Pan, B., Wang, B., Lin, Y., 2019. Accumulation and toxicological
effects of nonylphenol in tomato (Solanum lycopersicum L.) plants. Scientific Reports 9 (1), 7022.
https://doi.org/10.1038/s41598-019-43550-7
Jayaraman, J., 2011. Laboratory manual in Biochemistry. New Age International Publisher Ltd., New
Age International Publishers, New Dehli, India, 176 p.
Kanwal, M., Ullah, H., Gulzar, A., Sadiq, T., Ullah, M. et al., 2022. Biodegradation of petroleum
hydrocarbons and the factors effecting rate of biodegradation. American Journal of Biomedical Science
& Reseach 16 (1), 6–15. AJBSR.MS.ID.002182. https://doi.org/10.34297/AJBSR.2022.16.002182
Kebede, G., Tafese, T., Abda, E.M., Kamaraj, M., Assefa, F., 2021 Factors influencing the bacterial bioremediation of hydrocarbon contaminants in the soil: mechanisms and impacts. Hindawi Journal
of Chemistry 2021, 9823362. https://doi.org/10.1155/2021/9823362
Korshunova, T.Y., Kuzina, E.V., Rafikova, G.F., Loginov, O.N., 2020. Using Pseudomonas for cleaning
the environment from oil contamination. EcoBiotech 3, 18–32. https://doi.org/10.31163/2618964x-2020-3-1-18-32 (In Russian).
Krige, N.R, Padgett, P.J., 2011. Phenotypic and physiological characterization methods. In: Rainey, F.,
Oren, A. (eds.), Methods in Microbiology. Vol. 38. Academic Press, New York, USA, 15–60. https://doi.org/10.1016/B978-0-12-387730-7.00003-6
Kuzikova, I.L., Zaytseva, T.B., Kichko, A.A., Zinoveva, S.V., Russu, A.D., Mayachkina, N.V., Medvedeva,
N.G., 2019. Effect of nonylphenols on the abundance and taxonomic structure of the soil microbial
community. Eurasian Soil Science 52, (6), 671–681. https://doi.org/10.1134/S1064229319060073
Kuzikova, I., Rybalchenko, O., Kurashov, E., Krylova, Y., Safronova, V., Medvedeva, N., 2020. Defense
responses of the marine-derived fungus Аspergillus tubingensis to alkylphenols stress. Water, Air, &
Soil Pollution 231 (6), 271. https://doi.org/10.1007/s11270-020-04639-2
Kuzikova, I., Andronov, E., Zaytseva, T., Metelkova, L., Zhakovskaya, Z., Medvedeva, N., 2022. A
microcosm approach for evaluating the microbial nonylphenol and butyltin biodegradation and
bacterial community shifts in co-contaminated bottom sediments from the Gulf of Finland, the Baltic
Sea. Environmental Science and Pollution Research 29 (46), 69849–69860. https://doi.org/10.1007/
s11356-022-20751-8
Laht, M., Volkov, E., 2011. Identification of sources and estimation of inputs/impacts on the Baltic
Sea. Cohiba Project “Control of Hazardous Substances in the Baltic Sea Region”. Summary Report,
Estonia, Tallinn, 446 p.
Lotfi, M., Hasanpour, A.H, Moghadamnia, A.A, Kazemi, S., 2021. The investigation into neurotoxicity
mechanisms of nonylphenol: A narrative review. Current Neuropharmacology 19, 1345–1353. https://doi.org/10.2174/1570159X18666201119160347
Ma, J., Chen, F., Tang, Y., Wang, X., 2018. Research on degradation characteristics of nonylphenol in
water by highly effective complex microorganisms. E3S Web of Conferences 53, 04016. https://doi.org/10.1051/e3sconf/20185304016
Medvedeva, N., Zaytseva, T., Kuzikova, I., 2017. Cellular responses and bioremoval of nonylphenol
by the bloom-forming cyanobacterium Planktothrix agardhii 1113. Journal of Marine Systems 171,
120–128. http://dx.doi.org/10.1016/j.jmarsys.2017.01.009
Merkova, M., Zalesak, M., Ringlova, E., Julinova, M., Ruzicka, J., 2018. Degradation of the surfactant
Cocamidopropyl betaine by two bacterial strains isolated from activated sludge. International
Biodeterioration & Biodegradation 127, 236–240. https://doi.org/10.1016/j.ibiod.2017.12.006
Noorimotlagh, Z., Mirzaee, S.A., Martinez, S.S., Rachoń, D., Hoseinzadeh, M., Jaafarzadeh, N.,
2020. Environmental exposure to nonylphenol and cancer progression Risk – A systematic review.
Environmental Research 184, 109263. https://doi.org/10.1016/j.envres.2020.109263
Paolella, G., Romanelli, A.M., Martucciello, S., Sposito, S., Lepretti, M. et al., 2021. The mechanism
of cytotoxicity of 4-nonylphenol in a human hepatic cell line involves ER-stress, apoptosis, and
mitochondrial dysfunction. Journal of Biochemical and Molecular Toxicology 35 (7), e22780. https://
doi.org/10.1002/jbt.22780
Pischedda, A., Tosin, M., Degli-Innocenti, F., 2019. Biodegradation of plastics in soil: The effect
of temperature. Polymer Degradation and Stability 170, 109017. https://doi.org/10.1016/j.polymdegradstab.2019.109017
Qhanya, L.B., Mthakathi, N.T., Boucher, C.E., Mashele, S.S., Theron, C.W., Syed, K., 2017. Isolation
and characterisation of endocrine disruptor nonylphenol using bacteria from South Africa. South
African Journal of Science 113 (5–6). http://dx.doi.org/10.17159/sajs.2017/20160287
Ravi, K., Javier, G-H., Nöbel, M., Grauslund, M-F., Lidén, G., 2018. Biological conversion of aromatic
monolignol compounds by a Pseudomonas isolate from sediments of the Baltic Sea. AMB Express 8
(1), 32. http://dx.doi.org/10.1186/s13568-018-0563-x
Ribeiro, A.R., Nunes, O.C., Pereira, M.F.R., Silva, A.M.T., 2015. An overview on the advanced oxidation
processes applied for the treatment of water pollutants defined in the recently launched Directive
2013/39/EU. Environment International 75, 33–51. http://dx.doi.org/10.1016/j.envint.2014.10.027
Sebiomo, A., Banjo, F.M., Ade-Ogunnowo, F.E., Fagbemi, F.T., 2017. Microbial population,
dehydrogenase and urease activities in soils polluted with spent engine and diesel oil. African Journal
of Science & Nature 4, 56–65. https://doi.org/10.46881/ajsn.v4i0.84
Shah, M.P., 2018. Microbial degradation of phenol by an application of Pseudomonas mendocina.
Austin Journal of Microbiology 4 (2), 1022.
Shirdel, I., Kalbassi, M.R., 2016. Effects of nonylphenol on key hormonal balances and histopathology of
the endangered Caspian brown trout (Salmo trutta caspius). Comparative Biochemistry and Physiology
Part C: Toxicology & Pharmacology 183–184, 28–35. https://doi.org/10.1016/j.cbpc.2016.01.003
Sole, M., Lopez de Alda, M.J., Castillo, M., Porte, C., Ladegaard-Pedersen, K., Barcelo, D., 2000.
Estrogenicity determination in sewage treatment plants and surface waters from Catalonian area
(NE Spain). Environmental Science & Technology 34 (24), 5076–5083. http:// dx.doi.org/10.1021/
es991335n
Spadoto, M., Sueitt, A.P.E., Galinaro, C.A., Pinto, T. da S., Pompei, C.M.E., Botta, C.M.R., Vieira,
E.M., 2017. Ecotoxicological effects of bisphenol A and nonylphenol on the freshwater cladocerans
Ceriodaphnia silvestrii and Daphnia similis. Drug and Chemical Toxicology 41 (4), 449–458. https://doi.org/10.1080/01480545.2017.1381109
Suen, J.-L., Hung, C.-H., Yu, H.-S., Huang, S.-K., 2012. Alkylphenols – potential modulators of the
allergic response. The Kaohsiung Journal of Medical Sciences 28 (7 Suppl), S43–S48. https://doi.org/10.1016/j.kjms.2012.05.009
Surkatti, R., El-Naas, M.H., 2017. Competitive interference during the biodegradation of cresols.
International Journal of Environmental Science and Technology 15 (2), 301–308. https://doi.org/10.1007/s13762-017-1383-2
Wang, Z., Yang, Y.Y., He, T., Xie, S.G., 2015. Change of microbial community structure and functional
gene abundance in nonylphenol-degrading sediment. Applied Microbiology and Biotechnology 99,
3259–3268. https://doi.org/10.1007/s00253-014-6222-5
Wang, L., Xiao, H., He, N., Sun, D., Duan, S., 2019. Biosorption and biodegradation of the environmental hormone nonylphenol by four marine microalgae. Scientific Reports 9, 5377. https://doi.org/10.1038/s41598-019-41808-8
Watanabe, W., Hori, Y., Nishimura, S., Takagi, A., Kikuchi, M., Sawai, J., 2012. Bacterial degradation
and reduction in the estrogen activity of 4-nonylphenol. Biocontrol Science 17 (3), 143–147. https://doi.org/10.4265/bio.17.143
Weisburg, W.G., Barns, S.M., Pelletier, D.A., Lane, D.J., 1991. 16S ribosomal DNA amplification for phylogenetic study. Journal of Bacteriology 173 (2), 697–703. https://doi.org/10.1128/jb.173.2.697
703.1991
Xie, Y., Pan, Y., Bai, B., Xu, Z., Ding, L. et al., 2015. Degradation performance and optimal parameters
of two bacteria in degrading nonylphenol. Journal of Computational and Theoretical Nanoscience 12
(9), 2657–2663. https://doi.org/10.1166/jctn.2015.4159
Zaytseva, T.B., Zinoveva, S.V., Kuzikova, I.L., Russu, A.D., Chugunova, M.V., Medvedeva, N.G., 2020.
Impact of nonylphenols on biological activity of loamy soddy-podzolic soil. Eurasian Soil Science 53
(5), 661–667. https://doi.org/10.1134/s1064229320050178