Environmental Science and Pollution Research

, Volume 25, Issue 32, pp 32549–32561 | Cite as

Effect of elevated benzophenone-4 (BP4) concentration on Chlorella vulgaris growth and cellular metabolisms

  • Yue Huang
  • Li Luo
  • Xiaoyan Y. Ma
  • Xiaochang C. WangEmail author
Research Article


Benzophenone-4 (BP4), as the raw material of common sunscreen products, usually shows strong eco-toxicity and endocrine-disrupting activity in aquatic animals. However, the potential adverse effect of BP4 on aquatic vegetation is still unclear. In order to evaluate the inhibitory effect of BP4 on phytoplankton, wild and acclimated Chlorella vulgaris was used as representative aquatic plant cells and experimental studies were conducted on the characteristics of its growth and cellular metabolisms upon exposure to elevated BP4 concentrations (1, 5, 10, 20, 50, and 100 mg L−1). C. vulgaris basically appeared low sensitivity to BP4 exposure because the 96-h EC50 was measured as 65.16 mg L−1 for its wild type. The 96-h EC50 of the acclimated type, which was pre-exposed to 10 mg L−1 of BP4 and transferred twice, was 140.76 mg L−1. By cellular response tests regarding non-enzymatic antioxidants carotenoid content, malondialdehyde (MDA), enzyme antioxidant superoxide dismutase (SOD) activity, and the photosynthetic efficiency, it was clarified that increasing exposure concentration elevated the hindrance to cellular metabolism. However, the rate of BP4 utilization as substrates for C. vulgaris growth showed a trend of decreasing with increasing BP4 concentration. The higher 96-h EC50 value of the acclimated C. vulgaris to BP4 inhibition than the wild C. vulgaris showed the enhanced tolerance capability; however, the continuous stress response of acclimated type should be taken into account when using microalgae species for toxicity assessment.


Chlorella vulgaris UV filters Benzophenone-4 Acclimation Stress action 


Funding information

This work was supported by the National Natural Science Foundation of China (No. 51508448, 51778522), the Science Foundation for Fostering Talents of Xi’an University of Architecture and Technology (RC1721), the National Program of Water Pollution Control (No. 2014ZX07323001), and the Program for Innovative Research Team in Shaanxi Province (No. 2013KCT-13).

Supplementary material

11356_2018_3171_MOESM1_ESM.docx (457 kb)
ESM 1 (DOCX 457 kb)


  1. Almeida AC, Gomes T, Langford K, Thomas KV, Tollefsen KE (2017) Oxidative stress in the algae Chlamydomonas reinhardtii exposed to biocides. Aquat Toxicol 189:50–59. CrossRefGoogle Scholar
  2. Borecka M, Bialk-Bielinska A, Halinski LP, Pazdro K, Stepnowski P, Stolte S (2016) The influence of salinity on the toxicity of selected sulfonamides and trimethoprim towards the green algae Chlorella vulgaris. J Hazard Mater 308:179–86CrossRefGoogle Scholar
  3. Carrera-Martinez D, Mateos-Sanz A, Lopez-Rodas V, Costas E (2011) Adaptation of microalgae to a gradient of continuous petroleum contamination. Aquat Toxicol 101:342–350. CrossRefGoogle Scholar
  4. Chae Y, Kim D, An YJ (2016) Effect of fluoride on the cell viability, cell organelle potential, and photosynthetic capacity of freshwater and soil algae. Environ Pollut 219:359–367. CrossRefGoogle Scholar
  5. Cho K, Lee CH, Ko K, Lee YJ, Kim KN, Kim MK, Chung YH, Kim D, Yeo IK, Oda T (2016) Use of phenol-induced oxidative stress acclimation to stimulate cell growth and biodiesel production by the oceanic microalga Dunaliella salina. Algal Res 17:61–66. CrossRefGoogle Scholar
  6. Dao LH, Beardall J (2016) Effects of lead on growth, photosynthetic characteristics and production of reactive oxygen species of two freshwater green algae. Chemosphere 147:420–429. CrossRefGoogle Scholar
  7. Diebold L, Chandel NS (2016) Mitochondrial ROS regulation of proliferating cells. Free Radic Biol Med 100:86–93. CrossRefGoogle Scholar
  8. Ding T, Lin K, Yang B, Yang M, Li J, Li W, Gan J (2017) Biodegradation of naproxen by freshwater algae Cymbella sp. and Scenedesmus quadricauda and the comparative toxicity. Bioresour Technol 238:164–173. CrossRefGoogle Scholar
  9. Du Y, Wang WQ, Pei ZT, Ahmad F, Rou-Rou X, Zhang Y-M, Sun L-W (2017) Acute toxicity and ecological risk assessment of benzophenone-3 (BP-3) and benzophenone-4 (BP-4) in ultraviolet (UV)-filters. Int J Environ Res Public Health 14(11):1414. CrossRefGoogle Scholar
  10. Fuhrs H, Behrens C, Gallien S, Heintz D, Van Dorsselaer A, Braun HP, Horst WJ (2010) Physiological and proteomic characterization of manganese sensitivity and tolerance in rice (Oryza sativa) in comparison with barley (Hordeum vulgare). Ann Bot 105:1129–1140. CrossRefGoogle Scholar
  11. Gago-Ferrero P, Badia-Fabregat M, Olivares A, Piña B, Blánquez P, Vicent T, Caminal G, Díaz-Cruz MS, Barceló D (2012) Evaluation of fungal- and photo-degradation as potential treatments for the removal of sunscreens BP3 and BP1. Sci Total Environ 427–428:355–363. CrossRefGoogle Scholar
  12. Gilroy EA, Balakrishnan VK, Solomon KR, Sverko E, Sibley PK (2012) Behaviour of pharmaceuticals in spiked lake sediments-effects and interactions with benthic invertebrates. Chemosphere 86:578–584. CrossRefGoogle Scholar
  13. González-Pleiter M, Gonzalo S, Rodea-Palomares I, Leganés F, Rosal R, Boltes K, Marco E, Fernández-Piñas F (2013) Toxicity of five antibiotics and their mixtures towards photosynthetic aquatic organisms: implications for environmental risk assessment. Water Res 47:2050–2064. CrossRefGoogle Scholar
  14. Higo S, Maung Saw Htoo T, Yamatogi T, Ishida N, Hirae S, Koike K (2017) Application of a pulse-amplitude-modulation (PAM) fluorometer reveals its usefulness and robustness in the prediction of Karenia mikimotoi blooms: a case study in Sasebo Bay, Nagasaki, Japan. Harmful Algae 61:63–70. CrossRefGoogle Scholar
  15. Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193. CrossRefGoogle Scholar
  16. Jiao Y, Ouyang H-L, Jiang Y-J, Kong X-Z, He W, Liu W-X, Yang B, Xu F-L (2017) Effects of phosphorus stress on the photosynthetic and physiological characteristics of Chlorella vulgaris based on chlorophyll fluorescence and flow cytometric analysis. Ecol Indic 78:131–141. CrossRefGoogle Scholar
  17. Khona DK, Shirolikar SM, Gawde KK, Hom E, Deodhar MA, D’Souza JS (2016) Characterization of salt stress-induced palmelloids in the green alga, Chlamydomonas reinhardtii. Algal Res 16:434–448. CrossRefGoogle Scholar
  18. Kleywegt S, Smyth SA, Parrott J, Schaefer K, Lagace E, Payne M, Topp E, Beck A, McLaughlin A, Ostapyk K (2007) Pharmaceuticals and personal care products in the Canadian environment: research and policy directions. NWRI Scientific Assessment Report Series 8:53–57Google Scholar
  19. Kurade MB, Kim JR, Govindwar SP, Jeon B-H (2016) Insights into microalgae mediated biodegradation of diazinon by Chlorella vulgaris : microalgal tolerance to xenobiotic pollutants and metabolism. Algal Res 20:126–134. CrossRefGoogle Scholar
  20. Li J, Peng J, Zhang Y, Ji Y, Shi H, Mao L, Gao S (2016) Removal of triclosan via peroxidases-mediated reactions in water: reaction kinetics, products and detoxification. J Hazard Mater 310:152–160. CrossRefGoogle Scholar
  21. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic membranes. Methods Enzymol 148:349–382Google Scholar
  22. Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Current Protocols in Food Analytical Chemistry 1:F4.3.1–F4.3.8CrossRefGoogle Scholar
  23. Liu X, Wang Y, Chen H, Zhang J, Wang C, Li X, Pang S (2018) Acute toxicity and associated mechanisms of four strobilurins in algae. Environ Toxicol Pharmacol 60:12–16. CrossRefGoogle Scholar
  24. Liu Y, Wang F, Chen X, Zhang J, Gao B (2015) Cellular responses and biodegradation of amoxicillin in Microcystis aeruginosa at different nitrogen levels. Ecotoxicol Environ Saf 111:138–145. CrossRefGoogle Scholar
  25. Maes M, Mihaylova I, Leunis JC (2006) Chronic fatigue syndrome is accompanied by an IgM-related immune response directed against neopitopes formed by oxidative or nitrosative damage to lipids and proteins. Neuro Endocrinol Lett 27:615–621Google Scholar
  26. Mao F, He Y, Kushmaro A, Gin KY (2017) Effects of benzophenone-3 on the green alga Chlamydomonas reinhardtii and the cyanobacterium Microcystis aeruginosa. Aquat Toxicol 193:1–8. CrossRefGoogle Scholar
  27. Molins-Delgado D, Diaz-Cruz MS, Barcelo D (2016a) Ecological risk assessment associated to the removal of endocrine-disrupting parabens and benzophenone-4 in wastewater treatment. J Hazard Mater 310:143–151. CrossRefGoogle Scholar
  28. Molins-Delgado D, Gago-Ferrero P, Diaz-Cruz MS, Barcelo D (2016b) Single and joint ecotoxicity data estimation of organic UV filters and nanomaterials toward selected aquatic organisms. Urban groundwater risk assessment. Environ Res 145:126–134. CrossRefGoogle Scholar
  29. Morais de P, Stoichev T, Basto MCP, Ramos V, Vasconcelos VM, Vasconcelos MTSD, (2014) Cyanobacterium Microcystis aeruginosa response to pentachlorophenol and comparison with that of the microalga Chlorella vulgaris. Water Res 52:63–72Google Scholar
  30. Muller R, Schreiber U, Escher BI, Quayle P, Bengtson Nash SM, Mueller JF (2008) Rapid exposure assessment of PSII herbicides in surface water using a novel chlorophyll a fluorescence imaging assay. Sci Total Environ 401:51–59. CrossRefGoogle Scholar
  31. Nie X, Wang X, Chen J, Vladimir Z, An T (2008) Response of the freshwater alga C. vulgaris to trichloroisocyanuric acid and ciprofloxacin. Environ Toxicol Chem 27:168–173. CrossRefGoogle Scholar
  32. Osundeko O, Dean AP, Davies H, Pittman JK (2014) Acclimation of microalgae to wastewater environments involves increased oxidative stress tolerance activity. Plant Cell Physiol 55:1848–1857. CrossRefGoogle Scholar
  33. Pan X, Zhang D, Chen X, Mu G, Li L, Bao A (2009) Effects of levofloxacin hydrochloride on photosystem II activity and heterogeneity of Synechocystis sp. Chemosphere 77:413–418. CrossRefGoogle Scholar
  34. Pancha I, Chokshi K, Maurya R, Trivedi K, Patidar SK, Ghosh A, Mishra S (2015) Salinity induced oxidative stress enhanced biofuel production potential of microalgae Scenedesmus sp. CCNM 1077. Bioresour Technol 189:341–348. CrossRefGoogle Scholar
  35. Pedersen JA, Soliman M, Suffet IH (2005) Human pharmaceuticals, hormones, and personal care product ingredients in runoff from agricultural fields irrigated with treated wastewater. Agriculture and Food Chemistry 53:1625–1632. CrossRefGoogle Scholar
  36. Perales-Vela HV, Garcia RV, Gomez-Juarez EA, Salcedo-Alvarez MO, Canizares-Villanueva RO (2016) Streptomycin affects the growth and photochemical activity of the alga Chlorella vulgaris. Ecotoxicol Environ Saf 132:311–317. CrossRefGoogle Scholar
  37. Qian H, Chen W, Sheng GD, Xu X, Liu W, Fu Z (2008) Effects of glufosinate on antioxidant enzymes, subcellular structure, and gene expression in the unicellular green alga Chlorella vulgaris. Aquat Toxicol 88:301–307. CrossRefGoogle Scholar
  38. Ramos S, Homem V, Alves A, Santos L (2016) A review of organic UV-filters in wastewater treatment plants. Environ Int 86:24–44. CrossRefGoogle Scholar
  39. Rodil R, Quintana JB, López-Mahía P, Muniategui-Lorenzo S, Prada-Rodríguez D (2008) Multiclass determination of sunscreen chemicals in water samples by liquid chromatography–tandem mass spectrometry. Anal Chem 80:1307–1315. CrossRefGoogle Scholar
  40. Safi C, Zebib B, Merah O, Pontalier P-Y, Vaca-Garcia C (2014) Morphology, composition, production, processing and applications of Chlorella vulgaris: a review. Renew Sust Energ Rev 35:265–278. CrossRefGoogle Scholar
  41. Sieratowicz A, Kaiser D, Behr M, Oetken M, Oehlmann J (2011) Acute and chronic toxicity of four frequently used UV filter substances for Desmodesmus subspicatus and Daphnia magna. J Environ Sci Health Part A 46:1311–1319. CrossRefGoogle Scholar
  42. Spellman FR (2013) Current issues in water and wastewater treatment operations, handbook of water and wastewater treatment plant operations, third edn. CRC PressGoogle Scholar
  43. Suggett DJ, Prášil O, Borowitzka MA (2011) Chlorophyll a fluorescence in aquatic sciences: methods and applications. In: Suggett DJ (ed) Chlorophyll fluorescence applications in microalgal mass cultures. Springer, Netherlands, pp 277–292Google Scholar
  44. Sun HQ, Du Y, Zhang ZY, Jiang WJ, Guo YM, Lu XW, Zhang YM, Sun LW (2016) Acute toxicity and ecological risk assessment of benzophenone and N,N-diethyl-3 methylbenzamide in personal care products. Int J Environ Res Public Health 13:925. CrossRefGoogle Scholar
  45. Valle-Sistac J, Molins-Delgado D, Diaz M, Ibanez L, Barcelo D, Silvia Diaz-Cruz M (2016) Determination of parabens and benzophenone-type UV filters in human placenta. First description of the existence of benzyl paraben and benzophenone-4. Environ Int 88:243–249. CrossRefGoogle Scholar
  46. White E, Lowe SW (2009) Eating to exit: autophagy-enabled senescence revealed. Genes Dev 23:784–787. CrossRefGoogle Scholar
  47. Xiong JQ, Kurade MB, Abou-Shanab RA, Ji MK, Choi J, Kim JO, Jeon BH (2016) Biodegradation of carbamazepine using freshwater microalgae Chlamydomonas mexicana and Scenedesmus obliquus and the determination of its metabolic fate. Bioresour Technol 205:183–190. CrossRefGoogle Scholar
  48. Xiong JQ, Kurade MB, Jeon B-H (2017a) Biodegradation of levofloxacin by an acclimated freshwater microalga, Chlorella vulgaris. Chem Eng J 313:1251–1257. CrossRefGoogle Scholar
  49. Xiong JQ, Kurade MB, Kim JR, Roh HS, Jeon BH (2017b) Ciprofloxacin toxicity and its co-metabolic removal by a freshwater microalga Chlamydomonas mexicana. J Hazard Mater 323:212–219. CrossRefGoogle Scholar
  50. Yin Y, Li S, Liao W, Lu Q, Wen X, Lu C (2010) Photosystem II photochemistry, photoinhibition, and the xanthophyll cycle in heat-stressed rice leaves. J Plant Physiol 167:959–966. CrossRefGoogle Scholar
  51. Zhang W, Zhang M, Lin KF, Sun WF, Xiong B, Guo MJ, Cui XH, Fu RB (2012) Eco-toxicological effect of carbamazepine on Scenedesmus obliquus and Chlorella pyrenoidosa. Environ Toxicol Pharmacol 33:344–352CrossRefGoogle Scholar
  52. Zhang P, Li Z, Lu L, Xiao Y, Liu J, Guo J, Fang F (2017) Effects of stepwise nitrogen depletion on carotenoid content, fluorescence parameters and the cellular stoichiometry of Chlorella vulgaris. Spectrochim Acta A Mol Biomol Spectrosc 181:30–38. CrossRefGoogle Scholar
  53. Zhao F, Xiang Q, Zhou Y, Xu X, Qiu X, Yu Y, Ahmad F (2017) Evaluation of the toxicity of herbicide topramezone to Chlorella vulgaris: oxidative stress, cell morphology and photosynthetic activity. Ecotoxicol Environ Saf 143:129–135. CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.International Science and Technology Cooperation Center for Urban Alternative Water Resources DevelopmentXi’an University of Architecture and TechnologyXi’anChina
  2. 2.Key Lab of Northwest Water Resource, Environment and Ecology, MOEXi’an University of Architecture and TechnologyXi’anChina
  3. 3.Engineering Research Center for Wastewater Treatment and Reuse, Shaanxi ProvinceXi’an University of Architecture and TechnologyXi’anChina
  4. 4.Key Lab of Environmental Engineering, Shaanxi ProvinceXi’an University of Architecture and TechnologyXi’anChina

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