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Molecular Mechanisms of the Response to 4-tert-Octylphenol-Induced Stress in a Cyanobacterium Planktothrix agardhii

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Abstract

The molecular mechanisms of stress response of Planktothrix agardhii, one of the dominant cya-nobacteria in the basins of the Northwestern Russia and other regions during “blooming,” on the effect of 4-tert-octylphenol (OP), a hormone-like xenobiotic of anthropogenic origin, were studied. In the presence of OP, an increase in the permeability of P. agardhii cell membranes occurred, one of the reasons for which was the oxidation of membrane lipids under conditions of oxidative stress caused by generation of reactive oxygen species. A dose-dependent increase of the activities of enzymatic and non-enzymatic antioxidants in P. agardhii was registered in response to octylphenol-induced oxidative stress, indicating OP action as an activator of expression of stress regulons genes. Due to the structural similarity of 4-tert-octylphenol and alkylresorcinols (AR), the natural microbial regulators controlling development of microbial populations, OP released into the environment may imitate the functions of AR, interfering with the communication process of microbial cells in the population, which may adversely affect the succession and stability of functioning of microbial communities.

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REFERENCES

  1. Acir, I.-H. and Guenther, K., Endocrine-disrupting metabolites of alkylphenol ethoxylates —a critical review of analytical methods, environmental occurrences, toxicity, and regulation (Review), Sci. Total Environ., 2018, vol. 635, pp. 1530–1546.

    Article  CAS  PubMed  Google Scholar 

  2. Aeby, H., Catalase in vitro, Methods Enzymol., 1984, vol. 105, pp. 121–126.

    Article  Google Scholar 

  3. Bates, L.S., Walderen, R.D., and Teare, I.D., Rapid determination of free proline for water stress studies, Plant Soil, 1973, vol. 39, pp. 205–207.

    Article  CAS  Google Scholar 

  4. Booth, I.R., Jones, M.A., McLaggan, D., Nikolaev, Y., Ness, L.S., Wood, C.M., Miller, S., Totemeyer, S., and Ferguson, G.P., Bacterial ion channels, in Handbook of Biological Physics, Konings, W.N., Kaback, H.R., and Lolkema, J.S., Eds., Amsterdam: Elsevier, 1996, pp. 693–729.

    Google Scholar 

  5. Bukharin, O.V., Gintsburg, A.L., Romanova, Yu.M., and El’-Registan, G.I., Mekhanizmy vyzhivaniya bacterii (Mechanisms of Bacterial Survival), Moscow: Meditsina, 2005.

  6. Domonkos, I., Kis, M., Gombos, Z., and Ughy, B., Carotenoids, versatile components of oxygenic photosynthesis, Prog. Lipid. Res., 2013, vol. 52, pp. 539–561.

    Article  CAS  PubMed  Google Scholar 

  7. El-Sheekh, M.M., Khairy, H.M., and El-Shenody, R., Algal production of extra and intra-cellular polysaccharides as an adaptive response to the toxin crude extract of Microcystis aeruginosa, Iranian J. Environ. Health. Sci. Eng., 2012, vol. 9, no. 1, p. 10. El’-Registan, G.I., Muliukin, A.L., Nikolaev, Yu.A., Suzina, N.E., Gal’chenko, V.F., and Duda, V.I., Adaptogenic functions of extracellular autoregulators of microorganisms, Microbiology (Moscow), 2006, vol. 75, pp. 380–389.

    Article  CAS  Google Scholar 

  8. Environmental Risk Evalution Report: 4-tert-Octylphenol, Brooke, D., Johnson, I., Mitchell, R.J., and Watts, C., Eds., Wales: Env. Agency, 2005.

    Google Scholar 

  9. Fenderson, B.A., Eddy, E.M., and Hakomori, S., Glycoconjugate expression during embryogenesis and its biological significance, Bioassays, 1990, vol. 12, pp. 173–179.

    Article  CAS  Google Scholar 

  10. Gao, Q.T. and Tam, N.F.Y., Growth, photosynthesis and antioxidant responses of two microalgal species, Chlorella vulgaris and Selenastrum capricornutum, to nonylphenol stress, Chemosphere, 2011, vol. 82, pp. 346–354.

    Article  CAS  PubMed  Google Scholar 

  11. Gerken, H.G., Donohoe, B., and Knoshaug, E.P., Enzymatic cell wall degradation of Chlorella vulgaris and other microalgae for biofuels production, Planta, 2013, vol. 237, pp. 239–253.

    Article  CAS  PubMed  Google Scholar 

  12. Giannopolitis, C.N. and Ries, S.K., Superoxide dismutase I. Occurrence in higher plants, Plant Physiol., 1977, vol. 59, pp. 309–314.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Golod, N.A., Loiko, N.G., Lobanov, K.V., Mironov, A.S., Voieikova, T.A., Gal’chenko, V.F., Nikolaev, Yu.A., and El’-Registan, G.I., Involvement of alkylhydroxybenzenes, microbial autoregulators, in controlling the expression of stress regulons, Microbiology (Moscow), 2009, vol. 78, pp. 678–688.

    Article  CAS  Google Scholar 

  14. Herbert, D., Phipps, P.J., and Stange, R.E., Chapter III.Chemical analysis of microbial cells, Methods Microbiol., 1971, vol. 5 (Part B), pp. 209–344.

    Google Scholar 

  15. Hernando, M., Minaglia, M.C.C., Malanga, G., Houghton, C., Andrinolo, D., Sedan, D., Rosso, L., and Giannuzzi, L., Physiological responses and toxin production of Microcystis aeruginosa in short-term exposure to solar UV radiation, Photochem. Photobiol. Sci., 2018, vol. 17, pp. 69–80.

    Article  CAS  PubMed  Google Scholar 

  16. Konanykhina, I.A., Shanenko, E.F., Loiko, N.G., Nikolaev, Yu.A., and El’-Registan, G.I., Regulatory effect of microbial alkyloxybenzenes of different structure on the stress response of yeast, Appl. Biochem. Microbiol., 2008, vol. 44, pp. 518–522.

    Article  CAS  Google Scholar 

  17. Liu, Y., Dai, X., and Wei, J., Toxicity of the xenoestrogen nonylphenol and its biodegradation by the alga Cyclotella caspia, J. Environ. Sci., 2013, vol. 25, pp. 1662–1671.

    Article  CAS  Google Scholar 

  18. Medvedeva, N., Zaytseva, T., and Kuzikova, I., Cellular responses and bioremoval of nonylphenol by the bloom-forming cyanobacterium Planktothrix agardhii 1113, J. Mar. Syst., 2017, vol. 171, pp. 120–128.

    Article  Google Scholar 

  19. Mil’ko, E.S., Khabibullin, S.S., Nikolaev, Yu.A., Kozlova, A.N., and El’-Registan, G.I., Dynamics of the growth and population composition of mixed cultures of R-, S-, and M- dissociants of Pseudomonas aeruginosa, Microbiology (Moscow), 2005, vol. 74, pp. 408–414.

    Article  CAS  Google Scholar 

  20. Nikolaev, Yu.A., Extracellular factors of bacterial adaptation to unfavorable environmental conditions, Appl. Biochem. Microbiol., 2004, vol. 40, pp. 327–336.

    Article  CAS  Google Scholar 

  21. Nikolaev, Yu.A., Loiko, N.G., Stepanenko, I.Yu., Shanenko, E.F., Martirosova, E.I., Plakunov, V.K., Kozlova, A.N., Borzenkov, I.A., Korotina, O.A., Rodin, D.S., Krupyanskii, Yu.F., and El’-Registan, G.I., Changes in physicochemical properties of proteins, caused by modification with alkylhydroxybenzenes, Appl. Biochem. Microbiol., 2008, vol. 44, pp. 143–150.

    Article  CAS  Google Scholar 

  22. Oktyabrskii, O.N. and Smirnova, G.V., Redox potencial changes in bacterial cultures under stress conditions, Microbiology (Moscow), 2012, vol. 81, pp. 131–142.

    Article  CAS  Google Scholar 

  23. Parsons, T.R. and Strickland, J.D.H., Discussion of spectrophotometric determination of marine-plant pigments with revised equations for ascertaining chlorophylls and carotenoids, J. Mar. Res., 1963, vol. 21, pp. 155–163.

    CAS  Google Scholar 

  24. Rippka, R., Deruelles, J., Waterbury, J.B., Herdman, M., and Stanier, R.Y., Genetic assignments, strain histories and properties of pure cultures of cyanobacteria, J. Gen. Microbiol., 1979, vol. 111, pp. 1–61.

    Google Scholar 

  25. Sheikh, I.F., Tayubi, I.A., Ahmad, E., Ganaie, M.A., Bajouh, O.S., AlBasri, S.F., Abdulkarim, I.M.J., and Beg, M.A., Computational insights into the molecular interactions of environmental xenoestrogens 4-tert-octylphenol, 4-nonylphenol, bisphenol A (BPA), and BPA metabolite, 4-methyl-2, 4-bis(4-hydroxyphenyl) pent-1-ene (MBP) with human sex hormone-binding globulin, Ecotoxicol. Environ. Saf., 2017, vol. 135, pp. 284–291.

    Article  CAS  PubMed  Google Scholar 

  26. Staniszewska, M., Nehring, I., and Mudrak-Cegiołka, S., Changes of concentrations and possibility of accumulation of bisphenol A and alkylphenols, depending on biomass and composition, in zooplankton of the Southern Baltic (Gulf of Gdansk), Environ. Pollut., 2016, vol. 213, pp. 489–501.

    Article  CAS  PubMed  Google Scholar 

  27. Trabelsi, L., Chaieb, O., Mnari, A., Abid-Essafi, S., and Aleya, L., Partial characterization and antioxidant and antiproliferative activities of the aqueous extracellular polysaccharides from the thermophilic microalgae Graesiella sp., BMC Complem. Altern. Med., 2016, vol. 16, pp. 210–219.

    Article  CAS  Google Scholar 

  28. Wan, J., Guo, P., Peng, X., and Wen, K., Effect of erythromycin exposure on the growth, antioxidant system and photosynthesis of Microcystis flos-aquae, J. Hazard. Mater., 2015, vol. 283, pp. 778–786.

    Article  CAS  PubMed  Google Scholar 

  29. Zaytseva, T.B., Medvedeva, N.G., and Mamontova, V.N., Peculiarities of the effect of octyl- and nonylphenols on the growth and development of microalgae, Inland Water Biol., 2015b, vol. 8, pp. 406–413.

    Article  Google Scholar 

  30. Zaytseva, T.B., Milman, B.L., Lugovkina, N.V., Chernova, E.N., Russkikh, I.V., Sataeva, S.M., and Medvedeva, N.G., Effect of octyl- and nonylphenols on the growth, photosynthetic activity and toxin production of cyanobacteria Planktothrix agardhii, Hydrobiol. J., 2015a, vol. 51, no. 6, pp. 36–47.

    Article  Google Scholar 

  31. Zhou, G.-J., Peng, F.u-Q., Yang, B., Ying, G.-G. Cellular responses and bioremoval of nonylphenol and octylphenol in the freshwater green microalgae Scenedesmus obliquus, Ecotoxicol. Environ. Saf., 2013, vol. 87, pp. 10–16.

    Article  CAS  PubMed  Google Scholar 

  32. Zutshi, S., Bano, F., Ningthoujam, M., Habib, K., and Fatma, T., Metabolic adaptation to arsenic-induced oxidative stress in Hapalosiphon fontinalis-339, Int. J. Innov. Res. Sci. Eng. Technol., 2014, vol. 3, pp. 9386–9394.

    Google Scholar 

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Correspondence to T. B. Zaytseva or N. G. Medvedeva.

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Translated by P. Sigalevich

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Zaytseva, T.B., Medvedeva, N.G. Molecular Mechanisms of the Response to 4-tert-Octylphenol-Induced Stress in a Cyanobacterium Planktothrix agardhii. Microbiology 88, 416–422 (2019). https://doi.org/10.1134/S0026261719040143

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  • DOI: https://doi.org/10.1134/S0026261719040143

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