A multiple analysis of the impact of the endocrine disruptor nonylphenol on the number of microorganisms, taxonomic structure of the microbial community, and phytotoxicity of a loamy soddy-podzolic soil (Eutric Albic Retisol (Abruptic, Loamic, Aric, Ochric)) was performed in model experiments for the first time. The upper horizons of a loamy soddy-podzolic soil from Leningrad oblast were analyzed. The number and group composition of the soil microbiota were determined by the inoculation of soil suspensions on standard nutrient media. The taxonomic composition of the microbial community was studied using the pyrosequencing method (Illumina MiSeq). The content of nonylphenol in soil samples was determined by high-performance liquid chromatography. The phytotoxicity of the soil samples was evaluated in relation to the test culture of soft wheat (Tríticum aestívum). It was found that nonylphenol induces dose- and time-dependent changes in the number of the main physiological groups of soil microorganisms. In the presence of nonylphenol, a significant increase in the number of heterotrophic and oligotrophic microorganisms, as well as of bacteria tolerant to nonylphenol was observed. Actinomycetes and spore-forming bacteria proved to be most sensitive to this chemical. Under the impact of nonylphenol, the species diversity of the soil microbial cenosis decreased. Proteobacteria became the dominant phylum (78%) in the taxonomic structure of the microbial community. In the soil polluted by nonylphenol, the intensity of microbiological mineralization of nitrogen-containing organic substances decreased, and nitrogen immobilization processes were inhibited. The phytotoxicity of the soil samples with a high dose of nonylphenol (300 mg/kg soil) manifested itself during a month-long incubation. The obtained results can be used in developing a scientifically grounded methodology for bioremediation of soils contaminated with endocrine disruptors. Changes in the phylogenetic structure of soil microbial cenoses can serve as a sensitive bioindicator of the ecological soil state.
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E. E. Andronov, E. P. Chizhevskaya, E. V. Korostik, G. A. Akhtemova, A. G. Pinaev, and S. N. Petrova, “Influence of introducing the genetically modified strain Sinorhizobium meliloti ACH-5 on the structure of the soil microbial community,” Microbiology (Moscow) 78, 474–482 (2009). https://doi.org/10.1134/S0026261709040110
E. V. Arinushkina, Manual on the Chemical Analyses of Soils (Moscow State Univ., Moscow, 1970) [in Russian].
R. P. Vorob’eva, A. S. Davydov, and Yu. S. Anan’eva, “Ecological assessment of sewage water sediments by their influence on soil biological activity,” Vestn. Altai. Gos. Univ., No. 4, 53–60 (2003).
A. V. Gorovtsov, “The structure of microbial cenoses of soils in Rostov-on-Don as a tool for monitoring anthropogenically-transformed soils,” Nauchn. Zh. Kuban. Gos. Agrar. Univ., No. 89 (5), 1–13 (2013).
V. A. Kasatikov, “Agroecological and technological aspects of using nontraditional organic fertilizers,” in All-Russian Scientific-Practical Conference “Improvement of Organization and Methodology of Agrochemical Studies in Geographical Experimental Network of Fertilizers” (Moscow, 2006) [in Russian].
A. S. Kondakova, A. P. Chernyaev, and L. I. Sokolova, “Determination of 4-nonylphenol in natural waters by high performance liquid chromatography,” Voda: Khim. Ekol., No. 12, 115–120 (2012).
N. G. Medvedeva, Yu. M. Polyak, S. V. Zinov’eva, and T. B. Zaitseva, “The influence of yperite and the products of its hydrolysis on soil microbiota,” Eurasian Soil Sci. 33, 894–898 (2000).
FR.1.39.2006.02264. Measurement Method of Seed Germination and Root Length of the Seedlings of Higher Plants to Determine Toxicity of Industrially Polluted Soils (St. Petersburg, 2009) [in Russian].
A. V. Panov, I. A. Kosheleva, A. M. Boronin, T. Z. Esikova, and S. L. Sokolov, “Influence of soil pollution on the composition of a microbial community,” Microbiology (Moscow) 82, 241–248. (2013). https://doi.org/10.1134/S0026261713010116
I. O. Plekhanova, “Self-purification of agrosoddy-podzolic sandy loamy soils fertilized with sewage sludge,” Eurasian Soil Sci. 50, 491–497 (2017). https://doi.org/10.1134/S1064229317040081
E. L. Chirak, E. V. Pershina, A. S. Dol’nik, O. V. Kutovaya, E. S. Vasilenko, B. M. Kogut, Ya. V. Merzlyakova, and E. E. Andronov, “Taxonomic structure of microbial association in different soils investigated by high-throughput sequencing of 16S-rRNA gene library,” S-kh. Biol., No. 3, 100–109 (2013). https://doi.org/10.15389/agrobiology.2013.3.100eng
J. G. Caporaso, J. Kuczynski, J. Stombaugh, et al., “QIIME allows analysis of high-throughput community sequencing data,” Nat. Methods 5 (7), 335–336 (2010).
B. V. Chang, Z. J. Lu, and S. Y. Yuan, “Anaerobic degradation of nonylphenol in subtropical mangrove sediments,” J. Hazard. Mater. 165, 162–167 (2009). https://doi.org/10.1016/j.jhazmat.2008.09.085
K. C. Das and K. Xia, “Transformation of 4-nonylphenol isomers during biosolids composting,” Chemosphere 70, 761–768 (2008). https://doi.org/10.1016/j.chemosphere.2007.07.039
W. Doucette, B. R. Wheeler, J. K. Chard, B. Bugbee, C. G. Naylor, J. P. Carbone, and R. C. Sims, “Uptake of nonylphenol and nonylphenol ethoxylates by crested wheatgrass,” Environ. Sci. Technol. 24, 2965–2972 (2005). https://doi.org/10.1897/05-171R.1
R. Ekelund, A. Bergman, A. Granmo, and M. Berggren, “Bioaccumulation of 4-nonylphenol in marine animals: a re-evaluation,” Environ. Pollut. 64, 107–120 (1990). https://doi.org/10.1016/0269-7491(90)90108-O
K. Fujii, N. Urano, H. Ushio, M. Satomi, and S. Kimura, “Sphingomonas cloacae sp. nov., a nonylphenol-degrading bacterium isolated from wastewater of a sewage-treatment plant in Tokyo,” Int. J. Syst. Evol. Microbiol. 51, 603–610 (2001). https://doi.org/10.1099/00207713-51-2-603
C. Hansel, P. Fendorf, S. Jardine, and C. Francis, “Changes in bacterial and archaeal community structure and functional diversity along a geochemically variable soil profile,” Appl. Environ. Microbiol. 74, 1620–1633 (2008). https://doi.org/10.1128/AEM.01787-07
Z. Y. Hseu, “Response of microbial activities in two contrasting soils to 4-nonylphenol treated with biosolids,” Chemosphere 64, 1769–1776 (2006). https://doi.org/10.1016/j.chemosphere.2005.12.042
M. Jontofsohn, M. Stoffels, A. Hartman, G. Pfister, et al., “Influence of nonylphenol on the microbial community of lake sediments in microcosms,” Sci. Total Environ. 285, 3–10 (2002). https://doi.org/10.1007/BF02991042
Y. Kim, G. V. Korshin, and A. B. Velichenko, “Comparative study of electrochemical degradation and ozonation of nonylphenol,” Water Res. 39, 2527–2534 (2005). https://doi.org/10.1016/j.watres.2005.04.070
I. Kuzikova, V. Safronova, T. Zaytseva, and N. Medvedeva, “Fate and effects of nonylphenol in the filamentous fungus Penicillium expansum isolated from the bottom sediments of the Gulf of Finland,” J. Mar. Syst. 171, 111–119 (2017). https://doi.org/10.1016/j.jmarsys.2016.06.003
K. A. Langdon, M. J. St. Warne, R. J. Smernik, A. Shareef, and R. S. Kookana, “Degradation of 4-nonylphenol, 4-t-octylphenol, bisphenol A, and triclosan following biosolids addition to soil under laboratory conditions,” Chemosphere 84, 1556–1562 (2011). https://doi.org/10.1016/j.chemosphere.2011.05.053
R. Leschber, “Evaluation of the relevance of organic micro-pollutants in sewage sludge,” in Background Values in European Soils and Sewage Sludges: Results of a JRC-Coordinated Study on Background Values, Ed. by B. M. Gawlik and G. Bidoglio (Office for Official Publications of the European Communities, Luxemburg, 2006), Part 1.
J. Liu, J. Shan, B. Jiang, L. Wang, B. Yu, J. Chen, H. Guo, and R. Ji, “Degradation and bound-residue formation of nonylphenol in red soil and the effects of ammonium,” Environ. Pollut. 186, 83–89 (2014). https://doi.org/10.1016/j.envpol.2013.11.017
W. Ma, C. Nie, F. Su, X. Cheng, Y. Yan, B. Chen, and X. Lun, “Migration and biotransformation of three selected endocrine disrupting chemicals in different river-based aquifers media recharge with reclaimed water,” Int. Biodeterior. Biodegrad. 102, 298–307 (2015).
N. Medvedeva, T. Zaytseva, and I. Kuzikova, “Cellular responses and bioremoval of nonylphenol by the bloom-forming cyanobacterium Planktothrix agardhii 1113,” J. Mar. Syst. 171, 120–128 (2017). https://doi.org/10.1016/j.jmarsys.2017.01.009
R. K. Rajendran, S. Huang, C. Lin, and R. Kirschner, “Aerobic degradation of estrogenic alkylphenols by yeasts isolated from a sewage treatment plant,” RSC Adv. 6, 82862–82871 (2016). https://doi.org/10.1039/c6ra08839b
A. Soares, B. Guieysse, and B. Mattiasson, “Aerobic biodegradation of nonylphenol by cold-adapted bacteria,” Biotechnol. Lett. 25, 731–738 (2003). https://doi.org/10.1023/A:1023466916678
N. N. Tuan, H. C. Hsieh, Y. W. Lin, and S. L. Huang, “Analysis of bacterial degradation pathways for long-chain alkylphenols involving phenol hydroxylase, alkylphenol monooxygenase and catechol dioxygenase genes,” Bioresour. Technol. 102, 4232–4240 (2011). https://doi.org/10.1016/j.biortech.2010.12.067
N. N. Tuan, Y. W. Lin, and S. L. Huang, “Catabolism of 4-alkylphenols by Acinetobacter sp. OP5: Genetic organization of the oph gene cluster and characterization of alkylcatechol 2,3-dioxygenase,” Bioresour. Technol. 131, 420–428 (2013). https://doi.org/10.1016/j.biortech.2012.1
R. Vazquez-Duhalt, F. Marquez-Rocha, E. Ponce, A. F. Licea, and M. T. Viana, “Nonylphenol, an integrated vision of a pollutant. Scientific review,” Appl. Ecol. Environ. Res. 4 (1), 1–25 (2005).
J. Vikelsoe, M. Thomsen, E. Johansen, and L. Carlsen, Phthalates and Nonylphenols in Soil: NERI Technical Report No. 268 (Ministry of Environment and Energy National Environmental Research Institute, Copenhagen, 1999).
Z. Wang, Y. Yang, Y. Dai, and S. Xi, “Anaerobic biodegradation of nonylphenol in river under nitrate- or sulfate-reducing conditions and associated bacterial community,” J. Hazard. Mater. 286, 306–314 (2015). https://doi.org/10.1016/j.jhazmat.2014.12.057
Z. Wang, Y. Yang, W. Sun, S. Xie, and Y. Liu, “Nonylphenol biodegradation in river sediment and associated shifts in community structures of bacteria and ammonia-oxidizing microorganisms,” Ecotoxicol. Environ. Saf. 106, 1–5 (2014). https://doi.org/10.1016/j.ecoenv.2014.04.019
T. N. Widarto, M. Holmstrup, and V. E. Forbes, “The influence of nonylphenol on life-history of the earthworm Dendrobaena octaedra Savigny: linking effects from the individual-to the population-level,” Ecotoxicol. Environ. Saf. 58, 147–159 (2004). https://doi.org/10.1016/j.ecoenv.2004.03.006
C. W. Yang, S. L. Tang, L. Y. Chen, and B. V. Chang, “Removal of nonylphenol by eartworms and bacterial community change,” Int. Biodeterior. Biodegrad. 96, 9–17 (2014). https://doi.org/10.1016/j.ibiod.2014.09.010
G. G. Ying, R. S. Kookana, and P. Dillon, “Sorption and degradation of selected five endocrine disrupting chemicals in aquifer material,” Water Res. 37, 3785–3791 (2003). https://doi.org/10.1016/S0043-1354(03)00261-6
Y. Zhang, Y. Liu, H. Dong, X. Li, and D. Zhang, “The nonylphenol biodegradation study by estuary sediment-derived fungus Penicillium simplicissimum,” Environ. Sci. Pollut. Res. 23 (15), 15122–15132 (2016). https://doi.org/10.1007/s11356-016-6656-7
This work was performed within the framework of the Program for Basic Scientific Research of State Academies of Sciences for 2013–2020, project no. 01201360068 “The Impact of Anthropogenic Endocrine Disrupting Pollutants on Soil and Aquatic Microbial Cenoses in the North-west of the Russian Federation”, project no. 01201360068.
Translated by L. Kholopova
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Kuzikova, I.L., Zaytseva, T.B., Kichko, A.A. et al. Effect of Nonylphenols on the Abundance and Taxonomic Structure of the Soil Microbial Community. Eurasian Soil Sc. 52, 671–681 (2019). https://doi.org/10.1134/S1064229319060073
- loamy soddy-podzolic soil Eutric Albic Retisol (Abruptic
- microbial community