Skip to main content
SpringerLink
Log in

Effect of Nonylphenols on the Abundance and Taxonomic Structure of the Soil Microbial Community

  • SOIL BIOLOGY
  • Published:
Eurasian Soil Science Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.

Similar content being viewed by others

REFERENCES

  1. 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

    Article  Google Scholar 

  2. E. V. Arinushkina, Manual on the Chemical Analyses of Soils (Moscow State Univ., Moscow, 1970) [in Russian].

    Google Scholar 

  3. 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).

  4. 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).

  5. 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].

  6. 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).

  7. 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).

    Google Scholar 

  8. 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].

  9. 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

    Article  Google Scholar 

  10. 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

    Article  Google Scholar 

  11. 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

  12. 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).

    Article  Google Scholar 

  13. 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

    Article  Google Scholar 

  14. 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

    Article  Google Scholar 

  15. 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

    Google Scholar 

  16. 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

    Article  Google Scholar 

  17. 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

    Article  Google Scholar 

  18. 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

    Article  Google Scholar 

  19. 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

    Article  Google Scholar 

  20. 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

    Article  Google Scholar 

  21. 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

    Article  Google Scholar 

  22. 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

    Article  Google Scholar 

  23. 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

    Article  Google Scholar 

  24. 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.

  25. 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

    Article  Google Scholar 

  26. 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).

    Article  Google Scholar 

  27. 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

    Article  Google Scholar 

  28. 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

    Article  Google Scholar 

  29. 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

    Article  Google Scholar 

  30. 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

    Article  Google Scholar 

  31. 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

    Article  Google Scholar 

  32. 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).

    Article  Google Scholar 

  33. 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).

  34. 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

    Article  Google Scholar 

  35. 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

    Article  Google Scholar 

  36. 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

    Article  Google Scholar 

  37. 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

    Article  Google Scholar 

  38. 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

    Article  Google Scholar 

  39. 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

    Article  Google Scholar 

Download references

FUNDING

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.

Author information

Authors and Affiliations

  1. Saint Petersburg Research Center for Ecological Safety, Russian Academy of Sciences, 197110, St. Petersburg, Russia

    I. L. Kuzikova, T. B. Zaytseva, S. V. Zinoveva, A. D. Russu, N. V. Mayachkina & N. G. Medvedeva

  2. All-Russia Research Institute for Agricultural Microbiology, Russian Academy of Sciences, Pushkin-8, 196608, St. Petersburg, Russia

    A. A. Kichko

Authors
  1. I. L. Kuzikova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. B. Zaytseva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. A. Kichko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. V. Zinoveva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. A. D. Russu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. N. V. Mayachkina
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. N. G. Medvedeva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to I. L. Kuzikova.

Additional information

Translated by L. Kholopova

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1064229319060073

Keywords:

Search

Navigation