Concentration effects of the UV filter oxybenzone in Cyperus alternifolius: assessment of tolerance by stress-related response

Research Article

Abstract

Phytoremediation has been proposed to reduce the load of the sunscreen oxybenzone (OBZ) in the aquatic environment. Despite the proven removal efficiency of this compound, little is known about its influence, particularly oxidative stress on plants. In this study, a short-term incubation of macrophytic Cyperus alternifolius was performed to prove the plant’s ability to withstand the stress. Detached shoots were immersed in medium spiked with different concentrations of OBZ (50, 100, and 500 μM) for 2, 4, and 7 days, respectively. Increased formation of O2 and H2O2 in Cyperus treated with OBZ was characterized by intense colorization following histochemical staining. Alterations of enzyme activities involved in the antioxidative defense system indicate an adaptive response of C. alternifolius to this xenobiotic stress. Quantification of lipid peroxidation reveals that no significant membrane damage occurred during incubation with OBZ. Overall, 50 μM OBZ (tenfold higher than the amount frequently detected in the environment) exhibited low toxic effects. Accordingly, this pilot study provides information on the potential use of Cyperus to remove emerging sunscreen contaminants from water bodies.

Keywords

Oxybenzone ROS H2O2 Antioxidative enzymes MDA GST 

Notes

Acknowledgements

We thank Mr. Michael Obermeier for his expertise on the IDRISI software. And thanks to Mr. Nik Dorndorf for his technical assistance. The manuscript was influenced by discussions in COST Action ES1202 Conceiving Wastewater Treatment in 2020-Energetic, environmental and economic challenges (Water_2020).

Supplementary material

11356_2018_1839_MOESM1_ESM.doc (1.9 mb)
ESM 1 (DOC 1956 kb)

References

  1. Balmer ME, Buser HR, Müller MD, Poiger T (2005) Occurrence of some organic UV filters in wastewater, in surface waters, and in fish from Swiss lakes. Environ Sci Technol 39:953–962.  https://doi.org/10.1021/es040055r CrossRefGoogle Scholar
  2. Bartha B, Huber C, Harpaintner R, Schröder P (2010) Effects of acetaminophen in Brassica juncea L. Czern.: investigation of uptake, translocation, detoxification, and the induced defense pathways. Environ Sci Pollut Res 17:1553–1562.  https://doi.org/10.1007/s11356-010-0342-y CrossRefGoogle Scholar
  3. Blüthgen N, Zucchi S, Fent K (2012) Effects of the UV filter benzophenone-3 (oxybenzone) at low concentrations in zebrafish (Danio rerio). Toxicol Appl Pharmacol 263:184–194.  https://doi.org/10.1016/j.taap.2012.06.008 CrossRefGoogle Scholar
  4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254.  https://doi.org/10.1016/0003-2697(76)90527-3 CrossRefGoogle Scholar
  5. Brandes RP, Janiszewski M (2005) Direct detection of reactive oxygen species ex vivo. Kidney Int 67:1662–1664.  https://doi.org/10.1111/j.1523-1755.2005.00258.x CrossRefGoogle Scholar
  6. Calafat AM, Wong L-Y, Ye X, Reidy JA, Needham LL (2008) Concentrations of the sunscreen agent benzophenone-3 in residents of the United States: national health and nutrition examination survey 2003–2004. Environ Health Perspect 116(7):893–897.  https://doi.org/10.1289/ehp.11269 CrossRefGoogle Scholar
  7. Chang IH, Cheng KT, Huang PC, Lin YY, Cheng LJ, Cheng TS (2012) Oxidative stress in greater duckweed (Spirodela polyrhiza) caused by long-term NaCl exposure. Acta Physiol Plant 34:1165–1176.  https://doi.org/10.1007/s11738-011-0913-7 CrossRefGoogle Scholar
  8. Chen F, Huber C, May R, Schröder P (2016) Metabolism of oxybenzone in a hairy root culture: perspectives for phytoremediation of a widely used sunscreen agent. J Hazard Mater 306:230–236.  https://doi.org/10.1016/j.jhazmat.2015.12.022 CrossRefGoogle Scholar
  9. Cheng TS (2012) The toxic effects of diethyl phthalate on the activity of glutamine synthetase in greater duckweed (Spirodela polyrhiza L.) Aquat Toxicol 124:171–178.  https://doi.org/10.1016/j.aquatox.2012.08.014 CrossRefGoogle Scholar
  10. Christou A, Antoniou C, Christodoulou C, Hapeshi E, Stavrou I, Michael C, Fatta-Kassinos D, Fotopoulos V (2016) Stress-related phenomena and detoxification mechanisms induced by common pharmaceuticals in alfalfa (Medicago sativa L.) plants. Sci Total Environ 557-558:652–664.  https://doi.org/10.1016/j.scitotenv.2016.03.054 CrossRefGoogle Scholar
  11. Deponte M (2013) Glutathione catalysis and the reaction mechanisms of glutathione-dependent enzymes. Biochim Biophys Acta Gen Subj 1830:3217–3266.  https://doi.org/10.1016/j.bbagen.2012.09.018 CrossRefGoogle Scholar
  12. Diekmann F, Nepovim A, Schröder P (2004) Influence of Serratia liquefaciens and a xenobiotic glutathione conjugate on the detoxification enzymes in a hairy root culture of horseradish (Armoracia rusticana). J Appl Bot 78:64–67Google Scholar
  13. Dordio AV, Belo M, Martins Teixeira D, Palace Carvalho AJ, Dias CMB, Picó Y, Pinto AP (2011) Evaluation of carbamazepine uptake and metabolization by Typha spp., a plant with potential use in phytotreatment. Bioresour Technol 102:7827–7834.  https://doi.org/10.1016/j.biortech.2011.06.050 CrossRefGoogle Scholar
  14. Downs CA, Kramarsky-Winter E, Segal R, Fauth J, Knutson S, Bronstein O, Ciner FR, Jeger R, Lichtenfeld Y, Woodley CM, Pennington P, Cadenas K, Kushmaro A, Loya Y (2016) Toxicopathological effects of the sunscreen UV filter, oxybenzone (Benzophenone-3), on coral planulae and cultured primary cells and its environmental contamination in Hawaii and the U.S. Virgin Islands. Arch Environ Contam Toxicol 70:265–288.  https://doi.org/10.1007/s00244-015-0227-7 CrossRefGoogle Scholar
  15. Eggen T, Asp TN, Grave K, Hormazabal V (2011) Uptake and translocation of metformin, ciprofloxacin and narasin in forage- and crop plants. Chemosphere 85:26–33.  https://doi.org/10.1016/j.chemosphere.2011.06.041 CrossRefGoogle Scholar
  16. Envrionmental Working Group (2015) The Trouble With Sunscreen Chemicals. EWG’s 2015 Guide to Sunscreens. http://www.ewg.org/sunscreen/report/ the-trouble-with-sunscreen-chemicals/. Accessed Nov 28 2016
  17. Faure M, San Miguel A, Ravanel P, Raveton M (2012) Concentration responses to organochlorines in Phragmites australis. Environ Pollut 164:188–194.  https://doi.org/10.1016/j.envpol.2012.01.040 CrossRefGoogle Scholar
  18. Fediuc E, Erdei L (2002) Physiological and biochemical aspects of cadmium toxicity and protective mechanisms induced in Phragmites australis and Typha latifolia. J Plant Physiol 159:265–271.  https://doi.org/10.1078/0176-1617-00639 CrossRefGoogle Scholar
  19. Fent K, Zenker A, Rapp M (2010) Widespread occurrence of estrogenic UV-filters in aquatic ecosystems in Switzerland. Environ Pollut 158:1817–1824.  https://doi.org/10.1016/j.envpol.2009.11.005 CrossRefGoogle Scholar
  20. Gough DR, Cotter TG (2011) Hydrogen peroxide: a Jekyll and Hyde signaling molecule. Cell Death Dis 2:e213.  https://doi.org/10.1038/cddis.2011.96 CrossRefGoogle Scholar
  21. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione S-transferases: the first enzymatic step in mercapturic acid formation. J Biol Chem 249:7130–7139Google Scholar
  22. Hadad HR, Maine MA, Bonetto CA (2006) Macrophyte growth in a pilot-scale constructed wetland for industrial wastewater treatment. Chemosphere 63:1744–1753.  https://doi.org/10.1016/j.chemosphere.2005.09.014 CrossRefGoogle Scholar
  23. Halliwell B, Chirico S (1993) Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr 57:715S–724S; discussion 724S–725SCrossRefGoogle Scholar
  24. Hanson KM, Gratton E, Bardeen CJ (2006) Sunscreen enhancement of UV-induced reactive oxygen species in the skin. Free Radic Biol Med 41:1205–1212.  https://doi.org/10.1016/j.freeradbiomed.2006.06.011 CrossRefGoogle Scholar
  25. Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198.  https://doi.org/10.1016/0003-9861(68)90654-1 CrossRefGoogle Scholar
  26. Hechmi N, Ben AN, Abdenaceur H, Jedidi N (2014) Evaluating the phytoremediation potential of Phragmites australis grown in pentachlorophenol and cadmium co-contaminated soils. Environ Sci Pollut Res 21:1304–1313.  https://doi.org/10.1007/s11356-013-1997-y CrossRefGoogle Scholar
  27. Iori V, Pietrini F, Zacchini M (2012) Assessment of ibuprofen tolerance and removal capability in Populus nigra L. by in vitro culture. J Hazard Mater 229-230:217–223.  https://doi.org/10.1016/j.jhazmat.2012.05.097 CrossRefGoogle Scholar
  28. Jiang Z, Ma B, Erinle KO et al (2015) Enzymatic antioxidant defense in resistant plant: Pennisetum americanum (L.) K. Schum during long-term atrazine exposure. Pestic Biochem Physiol.  https://doi.org/10.1016/j.pestbp.2016.03.003
  29. Lehotai N, Lyubenova L, Schröder P, Feigl G, Ördög A, Szilágyi K, Erdei L, Kolbert Z (2016) Nitro-oxidative stress contributes to selenite toxicity in pea (Pisum sativum L). Plant Soil 400:107–122.  https://doi.org/10.1007/s11104-015-2716-x CrossRefGoogle Scholar
  30. Liu YS, Ying GG, Shareef A, Kookana RS (2012) Occurrence and removal of benzotriazoles and ultraviolet filters in a municipal wastewater treatment plant. Environ Pollut 165:225–232.  https://doi.org/10.1016/j.envpol.2011.10.009 CrossRefGoogle Scholar
  31. Liu L, Liu Y, Liu C, Wang Z, Dong J, Zhu GF, Huang X (2013) Potential effect and accumulation of veterinary antibiotics in Phragmites australis under hydroponic conditions. Ecol Eng 53:138–143.  https://doi.org/10.1016/j.ecoleng.2012.12.033 CrossRefGoogle Scholar
  32. Lyubenova L, Schröder P (2011) Plants for waste water treatment—effects of heavy metals on the detoxification system of Typha latifolia. Bioresour Technol 102:996–1004.  https://doi.org/10.1016/j.biortech.2010.09.072 CrossRefGoogle Scholar
  33. Lyubenova L, Nehnevajova E, Herzig R, Schröder P (2009) Response of antioxidant enzymes in Nicotiana tabacum clones during phytoextraction of heavy metals. Environ Sci Pollut Res 16:573–581.  https://doi.org/10.1007/s11356-009-0175-8 CrossRefGoogle Scholar
  34. Lyubenova L, Bipuah H, Belford E, Michalke B, Winkler B, Schröder P (2015) Comparative study on the impact of copper sulphate and copper nitrate on the detoxification mechanisms in Typha latifolia. Environ Sci Pollut Res 22:657–666.  https://doi.org/10.1007/s11356-014-3402-x CrossRefGoogle Scholar
  35. Marnett LJ (1999) Lipid peroxidation—DNA damage by malondialdehyde. Mutat Res Mol Mech Mutagen 424:83–95.  https://doi.org/10.1016/S0027-5107(99)00010-X CrossRefGoogle Scholar
  36. Marrs KA, Walbot V (1997) Expression and RNA splicing of the maize glutathione S-transferase Bronze2 gene is regulated by cadmium and other stresses. Plant Physiol 113:93–102CrossRefGoogle Scholar
  37. Mendarte-Alquisira C, Gutiérrez-Rojas M, González-Márquez H, Volke-Sepúlveda T (2016) Improved growth and control of oxidative stress in plants of Festuca arundinacea exposed to hydrocarbons by the endophytic fungus Lewia sp. Plant Soil 411(1–12):347–358.  https://doi.org/10.1007/s11104-016-3035-6 Google Scholar
  38. Messner B, Schröder P (1999) Burst amplifying system in cell suspension cultures of spruce (Picea abies): modulation of elicitor-induced release of hydrogen peroxide (oxidative burst) by ionophores and salicylic acid. Appl Botany 73:6–10Google Scholar
  39. Mishra S, Tripathi A, Tripathi DK, Chauhan DK (2015) Role of sedges (Cyperaceae) in wetlands, environmental cleaning and as food material. In: Azooz MM, Ahmad P (eds) Plant-environment interaction: responses and approaches to mitigate stress. Wiley, Chichester, pp 327–338CrossRefGoogle Scholar
  40. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410CrossRefGoogle Scholar
  41. Nehnevajova E, Lyubenova L, Herzig R, Schröder P, Schwitzguébel JP, Schmülling T (2012) Metal accumulation and response of antioxidant enzymes in seedlings and adult sunflower mutants with improved metal removal traits on a metal-contaminated soil. Environ Exp Bot 76:39–48.  https://doi.org/10.1016/j.envexpbot.2011.10.005 CrossRefGoogle Scholar
  42. Obermeier M, Schröder CA, Helmreich B, Schröder P (2015) The enzymatic and antioxidative stress response of Lemna minor to copper and a chloroacetamide herbicide. Environ Sci Pollut Res 22:18495–18507.  https://doi.org/10.1007/s11356-015-5139-6 CrossRefGoogle Scholar
  43. Pettitt TR, Wainwright MF, Wakeham AJ, White JG (2011) A simple detached leaf assay provides rapid and inexpensive determination of pathogenicity of Pythium isolates to “all year round” (AYR) chrysanthemum roots. Plant Pathol 60:946–956.  https://doi.org/10.1111/j.1365-3059.2011.02451.x0 CrossRefGoogle Scholar
  44. Pilon-Smits E (2005) Phytoremediation. Annu Rev Plant Biol 56:15–39.  https://doi.org/10.1146/annurev.arplant.56.032604.144214 CrossRefGoogle Scholar
  45. Polle A, Krings B, Rennenberg H (1989) Superoxide dismutase activity in needles of Norwegian spruce trees (Picea abies L.) Plant Physiol 90:1310–1315.  https://doi.org/10.1104/pp.90.4.1310 CrossRefGoogle Scholar
  46. Prasad SM, Kumar S, Parihar P, Singh R (2016) Interactive effects of herbicide and enhanced UV-B on growth, oxidative damage and the ascorbate-glutathione cycle in two Azolla species. Ecotoxicol Environ Saf 133:341–349.  https://doi.org/10.1016/j.ecoenv.2016.07.036 CrossRefGoogle Scholar
  47. Rao ASVC, Reddy AR (2008) Glutathione reductase: a putative redox regulatory system in plant cells. In: Sulfur assimilation and abiotic stress in plants. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 111–147CrossRefGoogle Scholar
  48. Schröder P (2001) The role of glutathione and glutathione S-transferases in plant reaction and adaptation to xenobiotics. pp 155–183Google Scholar
  49. Schröder P, Fischer C, Debus R, Wenzel A (2003) Reaction of detoxification mechanisms in suspension cultured spruce cells (Picea abies L. Karst.) to heavy metals in pure mixture and in soil eluates. Environ Sci Pollut Res 10:225–234.  https://doi.org/10.1007/BF02979658 CrossRefGoogle Scholar
  50. Schröder P, Grosse W, Gschlössl T (2005a) Phytoremediation-Möglichkeiten zur Entfernung von Mikroschadstoffen mit Verfahren der naturnahen Abwasserreinigung. In: Fränzle S, Markert B, Wünschmann S (eds) Technische Umweltchemie: Innovative Verfahren der Reinigung verschiedener Umweltkompartimente, Ecomed Biowissenschaften, Germany, pp.229–237. ISBN: 3-609-16331-3Google Scholar
  51. Schröder P, Maier H, Debus R (2005b) Detoxification of herbicides in Phragmites australis. Z Naturforsch C J Biosci 60:317–324Google Scholar
  52. Schröder P, Navarro-Aviñó J, Azaizeh H et al (2007) Using phytoremediation technologies to upgrade waste water treatment in Europe. Environ Sci Pollut Res Int 14:490–497.  https://doi.org/10.1065/espr2006.12.373 CrossRefGoogle Scholar
  53. Schröder P, Daubner D, Maier H, Neustifter J, Debus R (2008) Phytoremediation of organic xenobiotics—glutathione dependent detoxification in Phragmites plants from European treatment sites. Bioresour Technol 99:7183–7191.  https://doi.org/10.1016/j.biortech.2007.12.081 CrossRefGoogle Scholar
  54. Shenker M, Harush D, Ben-Ari J, Chefetz B (2011) Uptake of carbamazepine by cucumber plants—a case study related to irrigation with reclaimed wastewater. Chemosphere 82:905–910.  https://doi.org/10.1016/j.chemosphere.2010.10.052 CrossRefGoogle Scholar
  55. Tsui MMP, Leung HW, Lam PKS, Murphy MB (2014) Seasonal occurrence, removal efficiencies and preliminary risk assessment of multiple classes of organic UV filters in wastewater treatment plants. Water Res 53:58–67.  https://doi.org/10.1016/j.watres.2014.01.014 CrossRefGoogle Scholar
  56. Vanacker H, Carver TLW, Foyer CH (1998) Pathogen-induced changes in the antioxidant status of the apoplast in barley leaves. Plant Physiol 117:1103–1114.  https://doi.org/10.1104/pp.117.3.1103 CrossRefGoogle Scholar
  57. Verma S, Dubey RS (2003) Lead toxicity induces lipid peroxidation and alters the activities of antioxidant enzymes in growing rice plants. Plant Sci 164:645–655.  https://doi.org/10.1016/S0168-9452(03)00022-0 CrossRefGoogle Scholar
  58. Wolff MS, Engel SM, Berkowitz GS, Ye X, Silva MJ, Zhu C, Wetmur J, Calafat AM (2008) Prenatal phenol and phthalate exposures and birth outcomes. Environ Health Perspect 116:1092–1097.  https://doi.org/10.1289/ehp.11007 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Helmholtz Zentrum München, GmbH, German Research Center for Environmental Health, Research Unit Microbiome AnalysisNeuherbergGermany
  2. 2.Humboldt UniversityBerlinGermany

Personalised recommendations