Long-Chain Alkylphenols Biodegradation Potential of the Soil Ascomycota

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Abstract

A total of 11 strains ascomycetes-destructors of technical nonylphenol (NP) and 4-tert-octylphenol (4-t-OP) were isolated from nonylphenol-contaminated soddy-podzolic loamy soil (Leningrad Region, Russia). Fungal isolates are able to degrade NP and 4-t-OP at a high load (300 mg/L). The most effective Fusarium solani 8F strain has the ability to degrade alkylphenols (AP) both under cometabolic conditions and without additional carbon and energy sources. The decrease in AP is due to the processes of biodegradation and/or biotransformation by the studied strain and, to a small extent, due to sorption by fungal cells. The NP and 4-t-OP half-life under cometabolic conditions is 3.5 and 6.4 hours, respectively, and without additional carbon and energy sources, 9 and 19.7 hours, respectively. The amount of the lipid peroxidation product, malondialdehyde, as well as the reduced glutathione content in the process of NP and 4-t-OP biodegradation under cometabolic conditions increases by 1.7 and 2 times, respectively, compared with the control. The high level of reduced glutathione in F. solani 8F cells may indicate the participation of this metabolite both in the processes of AP biodegradation and in providing strain resistance to oxidative stress. To our knowledge, this is the first report on the degradation of NP and 4-t-OP by ascomycetous fungus F. solani both under cometabolic conditions and without additional carbon and energy sources. The revealed high potential of soil ascomycetes to degrade alkylphenols can be the basis for new environmentally safe bioremediation technologies for the purification of endocrine-disruptors conta-minated soils, natural and waste waters.

About the authors

I. L. Kuzikova

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

Author for correspondence.
Email: ilkuzikova@ya.ru
Russia, St. Petersburg

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

Author for correspondence.
Email: ngmedvedeva@gmail.com
Russia, St. Petersburg

References

  1. Barber L.B., Loyo-Rosales J.E., Rice C.P. et al. Endocrine disrupting alkylphenolic chemicals and other contaminants in wastewater treatment plant effluents, urban streams, and fish in the Great Lakes and Upper Mississippi River Regions. Science of the Total Environment. 2015. V. 517. P. 195–206. https://doi.org/10.1016/j.scitotenv.2015.02.035
  2. Beyer W.F., Fridovich I. Assaying for superoxide dismutase activity: some large consequences of minor changes in conditions. Anal. Biochem. 1987. V. 161 (2). P. 559–566. https://doi.org/10.1016/0003-2697(87)90489-1
  3. Bhandari G., Bagheri A.R., Bhatt P. et al. Occurrence, potential ecological risks, and degradation of endocrine disrupter, nonylphenol, from the aqueous environment. Chemosphere. 2021. V. 275. 130013. https://doi.org/10.1016/j.chemosphere.2021.130013
  4. Cahyanurani A.B., Chiu K.H., Wu T.M. Glutathione biosynthesis plays an important role against 4-tert-octylphenol-induced oxidative stress in Ceratophyllum demersum. Chemosphere. 2017. V. 183. P. 56–573. https://doi.org/10.1016/j.chemosphere.2017.05.150
  5. Cajthaml T. Biodegradation of endocrine-disrupting compounds by ligninolytic fungi: mechanisms involved in the degradation. Envir. Microbiol. 2015. V. 17. P. 4822–4834. https://doi.org/10.1111/1462-2920.12460
  6. Catapane M., Nicolucci C., Menale C. et al. Enzymatic removal of estrogenic activity of nonylphenol and octylphenol aqueous solutions by immobilized laccase from Trametes versicolor. J. Hazardous Materials. 2013. V. 248–249. P. 337–346. https://doi.org/10.1016/j.jhazmat.2013.01.031
  7. Chen B.S., Hsiao Y.L., Yen J.H. Effect of octylphenol on physiologic features during growth in Arabidopsis thaliana. Chemosphere. 2013. V. 93. P. 2264–2268. https://doi.org/10.1016/j.chemosphere.2013.08.002
  8. Dhindsa R.S., Plumb-Dhindsa P., Thorpe T.A. Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase. J. Experim. Bot. 1981. V. 32 (1). P. 93–101. https://doi.org/10.1093/jxb/32.1.93
  9. Domsch K., Gams W. Compendium of soil fungi. Academic Press, London, 1980.
  10. Esterhuizen-Londt M., Hertel S., Pflugmacher S. Uptake and biotransformation of pure commercial microcystin-LR versus microcystin-LR from a natural cyanobacterial bloom extract in the aquatic fungus Mucor hiemalis. Biotechnol. Lett. 2017. V. 39. P. 1537–1545. https://doi.org/10.1007/s10529-017-2378-2
  11. FAO Water Reports 38, Coping with water scarcity: an action framework for agriculture and food security. Rome, 2012.
  12. Gao Q.T., Tam N.F.Y. Growth, photosynthesis and antioxidant responses of two microalgal species, Chlorella vulgaris and Selenastrum capricornutum, to nonylphenol stress. Chemosphere. 2011. V. 82 (3). P. 346–354. https://doi.org/10.1016/j.chemosphere.2010.10.010
  13. Gingrich J., Ticiani E., Veiga-Lopez A. Placenta disrupted: endocrine disrupting chemicals and pregnancy. Trends Endocrinol. Metabol. 2020. V. 31 (7). P. 508–524. https://doi.org/10.1016/j.tem.2020.03.003
  14. Graca B., Staniszewska M., Zakrzewska D. et al. Reconstruction of the pollution history of alkylphenols (4-tert-octylphenol, 4-nonylphenol) in the Baltic Sea. Environ. Sci. Pollut. Res. 2016. V. 23. P. 11598–11610. https://doi.org/10.1007/s11356-016-6262-8
  15. Gu Y.L., Xu W.H., Liu Y.G. et al. Mechanism of Cr(VI) reduction by Aspergillus niger: enzymatic characteristic, oxidative stress response, and reduction product. Environ. Sci. Pollut. Res. 2015. V. 22. P. 6271–6279. https://doi.org/10.1007/s11356-014-3856-x
  16. Janicki T., Krupinski M., Dlugonski J. Degradation and toxicity reduction of the endocrine disruptors nonylphenol, 4-tert-octylphenol and 4-cumylphenol by the non-ligninolytic fungus Umbelopsis isabellina. Bioresource Technol. 2016. V. 200. P. 223–229. https://doi.org/10.1016/j.biortech.2015.10.034
  17. Jiang L., Yang Y., Zhang Y. et al. Accumulation and toxicological effects of nonylphenol in tomato (Solanum lycopersicum L.) plants. Scientific Reports. 2019. V. 9 (1). https://doi.org/10.1038/s41598-019-43550-7
  18. Kolvenbach B.A., Corvini P.F.X. The degradation of alkylphenols by Sphingomonas sp. TTNP3 – a review on seven years of research. New Biotechnology. 2012. V. 30 (1). P. 88–95. https://doi.org/10.1016/j.nbt.2012.07.008
  19. Krupinski M., Janicki T., Palecz B. et al. Biodegradation and utilization of 4-n-nonylphenol by Aspergillus versicolor as a sole carbon and energy source. J. Hazardous Materials. 2014. V. 280. P. 678–684. https://doi.org/10.1016/j.jhazmat.2014.08.060
  20. Krupinski M., Szewczyk R., Dlugonski J. Detoxification of xenoestrogen nonylphenol by the filamentous fungus Aspergillus versicolor. Int. Biodeterior. Biodegrad. 2013. V. 82. P. 59–66. https://doi.org/10.1016/j.ibiod.2013.03.011
  21. Kuzikova I., Rybalchenko O., Kurashov E. et al. Defense responses of the marine-derived fungus Aspergillus tubingensis to alkylphenols stress. Water, Air, and Soil Pollution. 2020. P. 231. https://doi.org/10.1007/s11270-020-04639-2
  22. Kuzikova I., Safronova V., Zaytseva T. et al. Fate and effects of nonylphenol in the filamentous fungus Penicillium expansum isolated from the bottom sediments of the Gulf of Finland. J. Marine Systems. 2017. V. 171. P. 111–119. https://doi.org/10.1016/j.jmarsys.2016.06.003
  23. Kuzikova I.L., Russu A.D., Medvedeva N.G. Biodegradation of nonylphenol and 4-tert-octylphenol by fungi of genera Penicillium derived from bottom sediments of Gulf of Finland. Mikologiya i fitopatologiya. 2018. V. 52 (2). P. 134–143 (in Russ.).
  24. 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 Science. 2019. V. 52 (6). P. 671–681. https://doi.org/10.1134/S1064229319060073
  25. Liu J., Shan J., Jiang B. et al. Degradation and bound-residue formation of nonylphenol in red soil and effects of ammonium. Envir. Pollution. 2014. V. 186. P. 83–89. https://doi.org/10.1016/j.envpol.2013.11.017
  26. Ma J., Chen F., Tang Y. et al. Research on degradation characteristics of nonylphenol in water by highly effective complex microorganisms. E3S Web of Conferences. 2018. V. 53. P. 1–7. https://doi.org/10.1051/e3sconf/20185304016
  27. Moon D.S., Song H.G. Degradation of alkylphenols by white rot fungus Irpex lacteus and its manganese peroxidase. Appl. Biochem. Biotechnol. 2012. V. 168 (3). P. 542–549. https://doi.org/10.1007/s12010-012-9795-4
  28. Mtibaà R., Ezzanad A., Aranda E. et al. Biodegradation and toxicity reduction of nonylphenol, 4-tert-octylphenol and 2,4-dichlorophenol by the ascomycetous fungus Thielavia sp. HJ22: Identification of fungal metabolites and proposal of a putative pathway. Science of the Total Environment. 2020. V. 708. P. 135129. https://doi.org/10.1016/j.scitotenv.2019.135129
  29. Priac A., Morin-Crini N., Druart C. et al. Alkylphenol and alkylphenol polyethoxylates in water and wastewater: A review of options for their elimination. Arabian J. Chemistry. 2017. V. 10. P. 3749–3773. https://doi.org/10.1016/j.arabjc.2014.05.011
  30. Rajendran R.K., Huang S.L., Lin C.C. et al. Aerobic degradation of estrogenic alkylphenols by yeasts isolated from a sewage treatment plant. RSC Adv. 2016. V. 6. P. 82862–82871. https://doi.org/10.1039/C6RA08839B
  31. Rajendran R.K., Huang S.L., Lin C.C. et al. Biodegradation of the endocrine disrupter 4-tert-octylphenol by the yeast strain Candida rugopelliculosa RRKY5 via phenolic ring hydroxylation and alkyl chain oxidation pathways. Bioresource Technol. 2017a. V. 226. P. 55–64. https://doi.org/10.1016/j.biortech.2016.11.129
  32. Rajendran R.K., Lin C.C., Huang S.L. et al. Enrichment, isolation, and biodegradation potential of long-branched chain alkylphenol degrading non-ligninolytic fungi from wastewater. Marine Pollut. Bull. 2017b. V. 125 (1–2). P. 416–425. https://doi.org/10.1016/j.marpolbul.2017.09.04
  33. Rajendran R.K., Lee Y.W., Chou P.H. et al. Biodegradation of the endocrine disrupter 4-t-octylphenol by the non-ligninolytic fungus Fusarium falciforme RRK20: Process optimization, estrogenicity assessment, metabolite identification and proposed pathways. Chemosphere. 2020. V. 240. 124876. https://doi.org/10.1016/j.chemosphere.2019.124876
  34. Rozalska S., Sobon A., Pawlowska J. et al. Biodegradation of nonylphenol by a novel entomopathogenic Metarhizium robertsii strain. Bioresource Technol. 2015. V. 191. P. 166–172. https://doi.org/10.1016/j.biortech.2015.05.011
  35. Samson R.A., Reenen-Hoekstra E.S. Introduction to food-borne fungi. 3rd ed. Baarn, 1988.
  36. Smirnov L.P., Suhovskaya I.V. The role of glutathione in the functioning of antioxidant defense systems and biotransformation (Review). Uchenye zapiski Petrozavodskogo gosudarstvennogo universiteta. 2014. V. 6. P. 34–40 (in Russ.).
  37. Szewczyk R., Sobon A., Rozalska S. et al. Intracellular proteome expression during 4-n-nonylphenol biodegradation by the filamentous fungus Metarhizium robertsii. Int. Biodeterior. Biodegrad. 2014. V. 93. P. 44–53. https://doi.org/10.1016/J.IBIOD.2014.04.026
  38. Tabassum H., Ashafaq M., Parvez S. et al. Role of melatonin in mitigating nonylphenol-induced toxicity in frontal cortex and hippocampus of rat brain. Neurochem. Int. 2017. V. 104. P. 11–26. https://doi.org/10.1016/j.neuint.2016.12.010
  39. Vallini G., Frassinetti S., Andrea F. et al. Biodegradation of 4-(1-nonyl) phenol by axenic cultures of the yeast Candida aquaetextoris: identification of microbial breakdown products and proposal of a possible metabolic pathway. Int. Biodeterior. Biodegrad. 2001. V. 47. P. 133–140. https://doi.org/10.1016/S0964-8305(01)00040-3
  40. Wang J., Majima N., Hirai H. et al. Effective removal of endocrine disrupting compounds by lignin peroxidase from the white-rot fungus Phanerochaete sordida YK-624. Current Microbiol. 2012. V. 64. P. 300–303. https://doi.org/10.1007/s00284-011-0067-2
  41. Wang S., Liu F., Wu W. et al. Migration and health risks of nonylphenol and bisphenol a in soil-winter wheat systems with long-term reclaimed water irrigation. Ecotoxicology and Environmental Safety. 2018. V. 158. P. 28–36. https://doi.org/10.1016/j.ecoenv.2018.03.082
  42. Wang Z., Yang Y., Sun W. et al. Nonylphenol biodegradation in river sediment and associated shifts in community structures of bacteria and ammonia-oxidizing microorganisms. Ecotoxicol. Environ. Saf. 2014. V. 106. P. 1–5. https://doi.org/10.1016/j.ecoenv.2014.04.019
  43. Watanabe W., Hori Y., Nishimura S., Takagi A., Kikuchi M., Sawai J. Bacterial degradation and reduction in the estrogen activity of 4-nonylphenol. Biocontrol Sci. 2012. V. 17 (3). P. 143–147. https://doi.org/10.4265/bio.17.143
  44. Zaytseva T.B., Zinoveva S.V., Kuzikova I.L. et al. Impact of nonylphenols on biological activity of loamy soddy-podzolic soil. Eurasian Soil Science. 2020. V. 53. P. 661–667. https://doi.org/10.1134/S1064229320050178
  45. Кузикова И.Л., Руссу А.Д., Медведева Н.Г. (Kuzikova et al.) Биодеградация нонилфенола и 4-трет-октилфенола грибами родов Penicillium, выделенными из донных осадков Финского залива // Микология и фитопатология. 2018. Т. 52. № 2. С. 134–143.
  46. Смирнов Л.П., Суховская И.В. (Smirnov, Sukhovskaya) Роль глутатиона в функционировании систем антиоксидантной защиты и биотрансформации (обзор) // Ученые записки Петрозаводского государственного университета. 2014. Т. 6. С. 34–40.

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