Advertisement

Biochemical activity of soil contaminated with BPS, bioaugmented with a mould fungi consortium and a bacteria consortium

  • Magdalena Zaborowska
  • Jadwiga WyszkowskaEmail author
  • Jan Kucharski
Research Article

Abstract

This study analysed the scale of bisphenol S (BPS) toxicity to the soil biochemical activity and is part of a wider effort to find solutions to restore the global soil environment balance, including elimination of the effects of ecosystem pollution with BPA, of which BPS is a significant analogue. However, since there has been no research on the effect of BPS on soil health, the objective of the study was pursued based on increasing the levels of soil contamination with the bisphenol 0, 5, 50 and 500 mg BPS kg−1 DM of soil and by observing the response of seven soil enzymes: dehydrogenases, catalase, urease, acid phosphatase, alkaline phosphatase, arylsulphatase and β-glucosidase to the growing BPS pressure. The potential negative effect of bisphenol S was offset by bioaugmentation with a bacteria consortium—Pseudomonas umsongensis, Bacillus mycoides, Bacillus weihenstephanensis and Bacillus subtilis—and a fungi consortium Mucor circinelloides, Penicillium daleae, Penicillium chrysogenum and Aspergillus niger. BPS was found to be a significant inhibitor of the soil enzymatic activity and, in consequence, its fertility. Dehydrogenases and acid phosphatase proved to be the most susceptible to BPS pressure. Bioaugmentation with a bacteria consortium offset the negative effect of 500 mg BPS kg−1 DM of soil by inducing an increase in the activity of acid phosphatase and alkaline phosphatase, whereas the fungi consortium stimulated the activity of β-glucosidase and acid phosphatase. A spectacular dimension of bisphenol S inhibition corresponded with both the spring rape above-ground parts and root development disorders and the content of Ca and K in them. The BPS level in soil on day 5 of the experiment decreased by 61% and by another 19% on day 60.

Keywords

BPS  Soil enzymes Bioaugmentation Bacterial consortium Mould fungi consortium 

Notes

Funding information

The research was supported by the Ministry of Science and Higher Education funds for statutory activity and co-financed by the National Science Center (Project MINIATURA1). The project was financially supported by Minister of Science and Higher Education in the range of the programme entitled “Regional Initiative of Excellence” for the years 2019–2022, Project No. 010/RID/2018/19, amount of funding 12.000.000 PLN.”

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Alef K, Nannipieri P (1998) Methods in applied soil microbiology and biochemistry. Academic Press Harcourt Brace & Company, London, p 576Google Scholar
  2. Asimakopoulos AG, Xue De Carvalho B, Iyer A, Abualnaja KO, Yaghmoor SS, Kumosani TA, Kannan K (2016) Urinary biomarkers of exposure to 57 xenobiotics and its association with oxidative stress in a population in Jeddah, Saudi Arabia. Environ Res 150:573–581.  https://doi.org/10.1016/j.envres.2015.11.029 CrossRefGoogle Scholar
  3. Beale RPS, Liss JL, Dixon PD (2011) Quantification of oxygenated volatile organic compounds in seawater by membrane inlet-proton transfer reaction/mass spectrometry. Anal Chim Acta 706:128–134.  https://doi.org/10.1016/j.aca.2011.08.023 CrossRefGoogle Scholar
  4. Bisphenol S (2014) National toxicology programGoogle Scholar
  5. Bjornsdotter MK, de Boer J, Ballesteros-Gomez A (2017) Bisphenol A and replacements in thermal paper: a review. Chemosphere 182:691–706.  https://doi.org/10.1016/j.chemosphere.2017.05.070 CrossRefGoogle Scholar
  6. Borowik A, Wyszkowska J, Wyszkowski M (2017) Resistance of aerobic microorganisms and soil enzyme response to soil contamination with Ekodiesel Ultra fuel. Environ Sci Pollut Res 24(31):24346–24363.  https://doi.org/10.1007/s11356-017-0076-1 CrossRefGoogle Scholar
  7. Buckley S, Allen D, Brackin R, Jämtgård S, Näsholm T, Schmidt S (2019) Microdialysis as an in situ technique for sampling soil enzymes. Soil Biol Biochem 135:20–27.  https://doi.org/10.1016/j.soilbio.2019.04.007 CrossRefGoogle Scholar
  8. Bunt JS, Rovira AD (1955) Microbiological studies of some subantarctic soil. J Soil Sci 6(1):119–128.  https://doi.org/10.1111/j.1365-2389.1955.tb00836.x CrossRefGoogle Scholar
  9. Calvet R (1989) Adsorption of organic chemicals in soils. Environ. Health Perspect 83:145–177CrossRefGoogle Scholar
  10. Carr DL, Morse AN, Zak JC, Anderson TA (2011) Microbially mediated degradation of common pharmaceuticals and personal care products in soil under aerobic and reduced oxygen conditions. Water Air Soil Pollut 216:633–642.  https://doi.org/10.1007/s11270-010-0558-y CrossRefGoogle Scholar
  11. Carvalho MB, Tavares S, Medeiros J, Núñez O, Gallart-Ayala H, Leitão MC, Galceran MT, Hursthouse A, Pereira CS (2011) Degradation pathway of pentachlorophenol by Mucor plumbeus involves phase II conjugation and oxidation–reduction reactions. J Hazard Mater 198:133–142.  https://doi.org/10.1016/j.jhazmat.2011.10.021 CrossRefGoogle Scholar
  12. Castro B, Sánchez P, Torres JM, Ortega E (2015) Bisphenol A, bisphenol F and bisphenol S affect differently 5α-reductase expression and dopamine–serotonin system in the prefrontal cortex of juvenile female rats. Environ Res 142:281–287.  https://doi.org/10.1016/j.envres.2015.07.001 CrossRefGoogle Scholar
  13. Chakraborty J, Das S (2016) Molecular perspectives and recent advances in microbial remediation of persistent organic pollutants. Environ Sci Pollut Res 23:16883–16903.  https://doi.org/10.1007/s11356-016-6887-7 CrossRefGoogle Scholar
  14. Chen D, Kannan K, Tan HL, Zheng ZG, Feng YL, Wu Y, Widelka M (2016) Bisphenol analogues other than BPA: environmental occurrence, human exposure, and toxicity-a review. Environ Sci Technol 50:5438–5453.  https://doi.org/10.1021/acs.est.5b05387 CrossRefGoogle Scholar
  15. Cheynier V, Comte G, Davies KM, Lattanzio V, Martens S (2013) Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol Biochem 72:1–20.  https://doi.org/10.1016/j.plaphy.2013.05.009 CrossRefGoogle Scholar
  16. Chintala R, Schumacher TE, Kumar S, Malo DD, Rice JA, Bleakley B, Chilom G, Clay DE, Julson JL, Papiernik SK, Gu ZR (2014) Molecular characterization of biochars and their influence on microbiological properties of soil. J Hazard Mater 279:244–256.  https://doi.org/10.1016/j.jhazmat.2014.06.074 CrossRefGoogle Scholar
  17. Choi YJ, Lee LS (2017) Aerobic soil biodegradation of bisphenol (BPA) alternatives bisphenol S and bisphenol AF compared to BPA. Environ Sci Technol 51(23):13698–13704.  https://doi.org/10.1021/acs.est.7b03889 CrossRefGoogle Scholar
  18. Chuanchuen R, Karkhoff-Schweizer RR, Schweizer HP (2003) High-level triclosan resistance in Pseudomonas aeruginosa is solely a result of efflux. Am J Infect Control 31:124–127.  https://doi.org/10.1067/mic.2003.11 CrossRefGoogle Scholar
  19. Dong X, Zhang Z, Meng S, Pan C, Yang M, Wu X, Yang L, Xu H (2018) Parental exposure to bisphenol A and its analogs influences zebrafish offspring immunity. Sci Total Environ 610–611:291–297.  https://doi.org/10.1016/j.scitotenv.2017.08.057 CrossRefGoogle Scholar
  20. ECHA (2015) Bisphenol S Registration Data. 2015. European Chemicals AgencyGoogle Scholar
  21. Egner H, Riehm H, Domingo WR (1960) Untersuchun-gen über die chemische Bodenanalyse als Grundlage für die Beurteilung des Nährstoffzustandes der Böden. II. Chemische Extractionsmethoden zur Phospor- und Kaliumbestimmung. Ann R Agric Coll Sweden 26:199–215Google Scholar
  22. EUBIA Sweden 26:199-215EUBIA (2019) European Biomass Industry Association. [WWW Document]. URL. http://www.eubia.org/cms/wiki-biomass/biofuels/biodiesel/, Accessed date: 28 June 2019
  23. Feng Y, Jiao Z, Shi J, Li M, Guo Q, Shao B (2016) Effects of bisphenol analogues on steroidogenic gene expression and hormone synthesis in H295R cells. Chemosphere 147:9–19.  https://doi.org/10.1016/j.chemosphere.2015.12.081 CrossRefGoogle Scholar
  24. Ferlian O, Wirth C, Eisenhauer N (2017) Leaf and root C-to-N ratios are poor predictors of soil microbial biomass C and respiration across 32 tree species. Pedobiologia 65:16–23.  https://doi.org/10.1016/j.pedobi.2017.06.005 CrossRefGoogle Scholar
  25. Figueroa RA, MacKay AA (2005) Sorption of oxytetracycline to iron oxides and ironoxide-rich soils. Environ Sci Technol 39:6664–6671.  https://doi.org/10.1021/es048044l CrossRefGoogle Scholar
  26. Glausiusz J (2014) Toxicology: The plastics puzzle. Nature 508:306–308CrossRefGoogle Scholar
  27. Gomaa OM (2012) Ethanol induced response in Phanerochaete chrysosporium and its role in the decolorization of triarylmethane dye. Ann Microbiol 62:1403–1409.  https://doi.org/10.1007/s13213-011-0390-7 CrossRefGoogle Scholar
  28. Halliwell B, Clement MV, Long LH (2000) Hydrogen peroxide in the human body. FEBS Lett 486:10–13CrossRefGoogle Scholar
  29. Haritash AK, Kaushik CP (2009) Biodegradation aspects of polycyclic aromatic hydrocarbons (PAHs): a review. J Hazard Mater 169:1–5.  https://doi.org/10.1016/j.jhazmat.2009.03.137 CrossRefGoogle Scholar
  30. Herrero Ó, Aquilino M, Sánchez-Argüello P, Planelló R (2018) The BPA-substitute bisphenol S alters the transcription of genes related to endocrine, stress response and biotransformation pathways in the aquatic midge Chironomus riparius (Diptera, Chironomidae). PLoS One 13(2):e0193387.  https://doi.org/10.1371/journal.pone.0193387 CrossRefGoogle Scholar
  31. Horta LP, Mota YCC, Barbosa GM, Braga T, Marriel IE, Fátima A, Modolo LV (2016) Urease inhibitors of agricultural interest inspired by structures of plant phenolic aldehydes. J Braz Chem Soc 27(8):1512–1519.  https://doi.org/10.21577/0103-5053.20160208 CrossRefGoogle Scholar
  32. Huang Y, Wong C, Zheng J, Bouwman H, Barra R, Wahlström B, Neretin L, Wong M (2012) Bisphenol A (BPA) in China: a review of sources, Environmental levels, and potential human health impacts. Environ Int 42:91–99.  https://doi.org/10.1016/j.envint.2011.04.010 CrossRefGoogle Scholar
  33. ISO 10390 (2005) Soil quality-determination of pHGoogle Scholar
  34. ISO 11260 (2018). Soil Quality - Determination of E_ective Cation Exchange Capacity and Base Saturation Level Using Barium Chloride Solution; International Organization for Standardization: Geneva, Switzerland.Google Scholar
  35. IUSS Working Group WRB (2014) World Reference Base for Soil Resources: International Soil Classification System for Naming Soils and Creating Legends for Soil Maps. Rome, FAO.Google Scholar
  36. Jin J, Wang M, Lua W, Zhang L, Jiang Q, Yeqing J, Lu K, Sun S, Cao Q, Wang Y, Xiao M (2019) Effect of plants and their root exudate on bacterial activities during rhizobacterium–plant remediation of phenol from water. Environ Int 127:114–124.  https://doi.org/10.1016/j.envint.2019.03.015 CrossRefGoogle Scholar
  37. Journal of Laws No. 1, item 1395 (2016) Regulation of the Minister of the Environment of September 1, 2016 on the way of assessing the pollution of the earth’s surfaceGoogle Scholar
  38. Kalyani DC, Telke AA, Surwase SN, Jadhav SB, Lee JK, Jadhav JP (2012) Effectual decolorization and detoxification of triphenylmethane dye Malachite Green (MG) by Pseudomonas aeruginosa NCIM 2074 and its enzyme system. Clean Techn Environ Policy 14:989–1001.  https://doi.org/10.1007/s10098-012-0473-6 CrossRefGoogle Scholar
  39. Karigar CS, Rao SS (2011) Role of microbial enzymes in the bioremediation of pollutants: a review. Enzyme Res 7:805187.  https://doi.org/10.4061/2011/805187 CrossRefGoogle Scholar
  40. Karimi A, Aghbolaghy M, Khataee A, Bargh SS (2012) Use of enzymatic bio-Fenton as a new approach in decolorization of Malachite Green. Sci World J 691569:1–5.  https://doi.org/10.1100/2012/691569 CrossRefGoogle Scholar
  41. Khadem A, Raiesi F (2019) Response of soil alkaline phosphatase to biochar amendments: Changes in kinetic and thermodynamic Characteristics. Geoderma 337:44–54.  https://doi.org/10.1016/j.geoderma.2018.09.001 CrossRefGoogle Scholar
  42. Klute A (1996) Methods of soil analysis, vol 9. American Society of Agronomy Agronomy Monograph, MadisonGoogle Scholar
  43. Kolla S, Morcos M, Martin B, Vandenberg LN (2018) Low dose bisphenol S or ethinyl estradiol exposures during the perinatal period alter female mouse mammary gland development. Reprod Toxicol 78:50–59.  https://doi.org/10.1016/j.reprotox.2018.03.003 CrossRefGoogle Scholar
  44. Kucharski J, Tomkiel M, Baćmaga M, Borowik A, Wyszkowska J (2016) Enzyme activity and microorganisms diversity in soil contaminated with the Boreal 58 WG. J Environ Sci Health B 51(7):446–454.  https://doi.org/10.1080/03601234.2016.1159456 CrossRefGoogle Scholar
  45. Kumar M, Rawat P, Khan MF, Tamarkar AK, Srivastava AK, Arya KR, Maurya R (2010) Phenolic glycosides from Dodecadenia grandiflora and their glucose-6-phosphatase inhibitory activity. Fitoterapia 81(6):475–479.  https://doi.org/10.1016/j.fitote.2010.01.011 CrossRefGoogle Scholar
  46. Liao C, Kannan K (2013) A survey of alkylphenols, bisphenols, and triclosan in personal care products from China and the United States. Arch Environ Contam Toxicol 67(1):50–59.  https://doi.org/10.1007/s00244-014-0016-8 CrossRefGoogle Scholar
  47. Liu Z, Zeng Z, Zeng G, Li J, Zhong H, Yuan X, Liu Y, Zhang J, Chen M, Liu Y, Xie G (2012) Influence of rhamnolipids and Triton X-100 on adsorption of phenol by Penicillium simplicissimum. Bioresour Technol 110:468–473.  https://doi.org/10.1016/j.biortech.2012.01.092 CrossRefGoogle Scholar
  48. Lu L, Yang Y, Zhang J, Shao B (2014) Determination of seven bisphenol analogues in reed and Callitrichaceae by ultraperformance liquid chromatography-tandem mass spectrometry. J Chromatogr B 953-954:80–85.  https://doi.org/10.1016/j.jchromb.2014.02.003 CrossRefGoogle Scholar
  49. Makoś P, Przyjazny A, Boczkaj G (2019) Methods of assaying volatile oxygenated organic compounds in effluent samples by gas chromatography - a review. J Chromatogr A 1592:143–160.  https://doi.org/10.1016/j.chroma.2019.01.045 CrossRefGoogle Scholar
  50. Martin J (1950) Use of acid rose bengal and streptpmycin in the plate method for estimating soil fungi. Soil Sci 69:215–233CrossRefGoogle Scholar
  51. Naikoo MI, Dar MI, Hassan F, Raghib J, Bilal A, Aamir R, Khan FA, Naushin F (2019) Chapter 9 - role and regulation of plants phenolics in abiotic stress tolerance: an overview, plant signaling molecules role and regulation under stressful environments:157–168.  https://doi.org/10.1016/B978-0-12-816451-8.00009-5
  52. Nakamura S, Wongkaew A, Nakaid Y, Raib H, Ohkama-Ohtsue N (2019) Foliar-applied glutathione activates zinc transport from roots to shoots in oilseed rape. Plant Sci 283:424–434.  https://doi.org/10.1016/j.plantsci.2018.10.018 CrossRefGoogle Scholar
  53. Nelson DW, Sommers LE (1996) Total carbon, organic carbon, and organicmatter. In: Sparks DL (ed) Method of soil analysis: chemical methods, American Society of Agronomy, Madison, pp 1201–1229Google Scholar
  54. Nicholls P, Fita I, Loewen PC (2001) Enzymology and structure of catalases. Adv Inorg Chem 51: 51–106.  https://doi.org/10.1016/S0898-8838(00)51001-0
  55. Noszczyńska M, Piotrowska-Seget Z (2018) Bisphenols: application, occurrence, safety, and biodegradation mediated by bacterial communities in wastewater treatment plants and rivers. Chemosphere 201:214–223.  https://doi.org/10.1016/j.chemosphere.2018.02.179 CrossRefGoogle Scholar
  56. Ogata Y, Goda S, Toyama T, Sei K, Ike M (2013) The 4-tert-butylphenol-utilizing bacterium Sphingobium fuliginis OMI can degrade bisphenols via phenolic ring hydroxylation and meta-cleavage pathway. Environ Sci Technol 47:1017–1023.  https://doi.org/10.1021/es303726h CrossRefGoogle Scholar
  57. Öhlinger R (1996) Dehydrogenases activity with the substrate TTC. In: Schinner F, Öhlinger R, Kandele E, Margesin R (eds) Methods in soil biology. Springer Verlag, Berlin, p 241Google Scholar
  58. Orwin KH, Wardle DA (2004) New indices for quantifying the resistance and resilience of soil biota to exogenous disturbances. Soil Biol Biochem 36:1907–1912.  https://doi.org/10.1016/j.soilbio.2004.04.036 CrossRefGoogle Scholar
  59. Peyre L, Rouimi P, de Sousa G, Héliès-Toussaint C, Carré B, Barcellini S, Chagnon MC, Rahmani R (2014) Comparative study of bisphenol A and its analogue bisphenol S on human hepatic cells: a focus on their potential involvement in nonalcoholic fatty liver disease. Food Chem Toxicol 70:9–18.  https://doi.org/10.1016/j.fct.2014.04.011 CrossRefGoogle Scholar
  60. Pivnenko K, Pederse GA, Eriksson E, Astrup TF (2015) Bisphenol A and its structural analogues in household waste paper. Waste Manag 44:39–47.  https://doi.org/10.1016/j.wasman.2015.07.017 CrossRefGoogle Scholar
  61. Qiu W, Zhan H, Hu J, Zhang T, Xu H, Wong M, Xu B, Zheng C (2019) The occurrence, potential toxicity, and toxicity mechanism of bisphenol S, a substitute of bisphenol A: a critical review of recent progres. Ecotoxicol Environ Saf 173:192–202.  https://doi.org/10.1016/j.ecoenv.2019.01.114 CrossRefGoogle Scholar
  62. Quintella CM, Mata AMT, Lima LCP (2019) Overview of bioremediation with technology assessment and emphasis on fungal bioremediation of oil contaminated soils. J Environ Manag 241:156–166.  https://doi.org/10.1016/j.jenvman.2019.04.019 CrossRefGoogle Scholar
  63. Roh H, Subramanya N, Zhao F, Yu CP, Sandt J, Chu KH (2009) Biodegradation potential of wastewater micropollutants by ammonia-oxidizing bacteria. Chemosphere 77(8):1084–1089.  https://doi.org/10.1016/j.chemosphere.2009.08.049 CrossRefGoogle Scholar
  64. Samuilov VD, Kiselevsky DB, Oleskin AV (2019) Mitochondria-targeted quinones suppress the generation of reactive oxygen species, programmed cell death and senescence in plants. Mitochondrion 46:164–171.  https://doi.org/10.1016/j.mito.2018.04.008 CrossRefGoogle Scholar
  65. Shah MB, Liu J, Zhang Q, Stout CD, Halpert JR (2017) Halogen−π interactions in the cytochrome P450 active site: structural insights into human CYP2B6 substrate selectivity. ACS Chem Biol 12(5):1204–1210.  https://doi.org/10.1021/acschembio.7b00056 CrossRefGoogle Scholar
  66. Shedbalkar U, Dhanve R, Jadhav J (2008) Biodegradation of triphenylmethane dye cotton blue by Penicillium ochrochloron MTCC 517. J Hazard Mater 157:472–479.  https://doi.org/10.1016/j.jhazmat.2008.01.023 CrossRefGoogle Scholar
  67. Sivitskaya V, Wyszkowski M (2013) Changes in the content of some macroelements in maize (Zea mays L.) under effect of fuel oil after application of different substances to soil. J Elem 8:705–714Google Scholar
  68. Statsoft Inc (2018) Data Analysis Software System. Version 12.0. Available at: http://www.statsoft.com
  69. Stolz A, Schönfelder G, Schneider MR (2018) Endocrine disruptors: adverse health effects mediated by EGFR? Trends Endocrinol Metab 29(2):69–71.  https://doi.org/10.1016/j.tem.2017.12.003 CrossRefGoogle Scholar
  70. Takeda K, Umezawa K, Va’ rnai A, VGH E, Igarashi K, Yoshida M, Nakamura N (2019) Fungal PQQ-dependent dehydrogenases and their potential in biocatalysis. Curr Opin Chem Biol 49:113–112.  https://doi.org/10.1016/j.cbpa.2018.12.001 CrossRefGoogle Scholar
  71. Takishima K, Suga T, Mamiya G (1988) The structure of jack bean urease. The complete amino acid sequence, limited proteolysis and reactive cysteine residues. Eur J Biochem 175(1):151–165.  https://doi.org/10.1111/j.1432-1033.1988.tb14177.x CrossRefGoogle Scholar
  72. Tang Z, Chen H, He H, Ma C (2019) Assays for alkaline phosphatase activity: progress and prospects. TrAC Trends Anal Chem 113:32–43.  https://doi.org/10.1016/j.trac.2019.01.019 CrossRefGoogle Scholar
  73. USEPA (1999) Biosolids Generation, Use, and Disposal in the United States. U.S. Environmental Protection Agency Municipal and Industrial Solid Waste Division. Office of Solid Waste 1-77.Google Scholar
  74. Wang Y, Xiao M, Geng X, Liu J, Chen J (2007) Horizontal transfer of genetic determinants for degradation of phenol between the bacteria living in plant and its rhizosphere. Appl Microbiol Biotechnol 77:733–739.  https://doi.org/10.1007/s00253-007-1187-2 CrossRefGoogle Scholar
  75. Wang CJ, Li Z, Jiang WT, Jean JS, Liu CC (2010) Cation exchange interaction between antibiotic ciprofloxacin and montmorillonite. J Hazard Mater 183:309–314.  https://doi.org/10.1016/j.jhazmat.2010.07.025 CrossRefGoogle Scholar
  76. Wilson B, Zhu J, Cantwell M, Olsen CR (2008) Short-term dynamics and retention of triclosan in the lower Hudson river estuary. Mar Pollut Bull 56:1230–1233.  https://doi.org/10.1016/j.marpolbul.2008.03.017 CrossRefGoogle Scholar
  77. Wong KH, Durrani TS (2017) Exposures to endocrine disrupting chemicals in consumer products—a guide for pediatricians. Curr Prob Pediatr Adolesc Health Care 47(5):107–118.  https://doi.org/10.1016/j.cppeds.2017.04.002 CrossRefGoogle Scholar
  78. Wright SL, Kelly FJ (2017) Plastic and human health: a micro issue? Environ Sci Technol 51(12): 6634–6647. ACS Chem Biol 12:1204–1210.  https://doi.org/10.1021/acs.est.7b00423 CrossRefGoogle Scholar
  79. Wu LH, Zhang XM, Wang F, Gao CJ, Chen D, Palumbo JR, Guo Y, Zeng EY (2018) Occurrence of bisphenol S in the environment and implications for human exposure: a short review. Sci Total Environ 615:87–98.  https://doi.org/10.1016/j.scitotenv.2017.09.194 CrossRefGoogle Scholar
  80. Wyszkowska J, Borowik A, Kucharski M, Kucharski J (2013) Applicability of biochemical indices to quality assessment of soil pulluted with heavy metal. J Elem 18(4):723–732.  https://doi.org/10.5601/jelem.2013.18.4.504 CrossRefGoogle Scholar
  81. Wyszkowska J, Boros-Lajszner E, Lajszner W, Kucharski J (2017) Reaction of soil enzymes and spring barley to copper chloride and copper sulphate. Environ Earth Sci 76:403–414.  https://doi.org/10.1007/s12665-017-6742-2 CrossRefGoogle Scholar
  82. Xue J, Wan Y, Kannan K (2016) Occurrence of bisphenols, bisphenol A diglycidyl ethers (BADGEs), and novolac glycidyl ethers (NOGEs) in indoor air from Albany, New York, USA, and its implications for inhalation exposure. Chemosphere 151:1–8.  https://doi.org/10.1016/j.chemosphere.2016.02.038 CrossRefGoogle Scholar
  83. Yamazaki E, Yamashita N, Taniyasu S, Lam J, Lam PKS, Moon HB, Jeong Y, Kannan P, Achyuthan H, Munuswamy N, Kannan K (2015) Bisphenol A and other bisphenol analogues including BPS and BPF in surface water samples from Japan, China, Korea and India. Ecotoxicol Environ Saf 122:565–572.  https://doi.org/10.1016/j.ecoenv.2015.09.029 CrossRefGoogle Scholar
  84. Yang YJ, Guan J, Yin J, Shao B, Li H (2014) Urinary levels of bisphenol analogues in residents living near a manufacturing plant in south China. Chemosphere 112:481–486.  https://doi.org/10.1016/j.chemosphere.2014.05.004 CrossRefGoogle Scholar
  85. Yu X, Xue J, Yao H, Wu Q, Venkatesan AK, Halden RU, Kannan K (2015) Occurrence and estrogenic potency of eight bisphenol analogs in sewage sludge from the US EPA targeted national sewage sludge survey. J Hazard Mater 299:733–739.  https://doi.org/10.1016/j.jhazmat.2015.07.012 CrossRefGoogle Scholar
  86. Zaborowska M, Kucharski J, Wyszkowska J (2018) Biochemical and microbiological activity of soil contaminated with o-cresol and biostimulated with Perna canaliculus mussel meal. Environ Monit Assess 190:602.  https://doi.org/10.1007/s10661-018-6979-6 CrossRefGoogle Scholar
  87. Zeng J, Zhu QH, Wu YC, Lin XG (2016) Oxidation of polycyclic aromatic hydrocarbons using Bacillus subtilis CotA with high laccase activity and copper independence. Chemosphere 148:1–7.  https://doi.org/10.1016/j.chemosphere.2016.01.019 CrossRefGoogle Scholar
  88. Zhang R, Liu R, Zong W (2016) Bisphenol S interacts with catalase and induces oxidative stress in mouse liver and renal cells. J Agric Food Chem 64(34):6630–6640.  https://doi.org/10.1021/acs.jafc.6b02656 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of MicrobiologyUniversity of Warmia and Mazury in OlsztynOlsztynPoland

Personalised recommendations