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Cited by 31Environmental Toxicology and EcotoxicologyToxic Organic Pollutants ImpactEffects and risks of endocrine disrupting chemicals

Evaluating the Joint Toxicity of Two Benzophenone-Type UV Filters on the Green Alga Chlamydomonas reinhardtii with Response Surface Methodology

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Mao, Feijian, He, Yiliang, Gin, Karina·2018·Toxics
DOI 10.3390/toxics6010008PMC PMC5874781
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Abstract

The widespread occurrence of benzophenone-type ultraviolet (UV) filter has raised the public concerns over the ecotoxicological effects of these chemicals. The present study assessed the joint toxicity of two representative benzophenones, benzophenone-1 (BP-1) and benzophenone-3 (BP-3), on the green alga Chlamydomonas reinhardtii using response surface methodologies (RSM). Specific growth rate and photosynthetic pigments were used as endpoints to evaluate the toxic effects. Generally, exposure to the combined BP-1 and BP-3 negatively affected cell growth and pigments production, with higher inhibitions at higher exposure concentrations. The simultaneous reduction in growth rate and pigments contents indicated that BP-1 and BP-3 regulated the growth of the tested alga by affecting the photosynthesis process. Results also showed that second order polynomial regression models fitted well with experimental results for all endpoints. The obtained regression models further indicated that the effects of the combination stemmed significantly from the linear concentration of BP-1 and BP-3. The overall results demonstrated that RSM could be a useful tool in ecotoxicological studies.

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  • Benzophenone-1 and benzophenone-3 at 5 mg/L decrease photosynthetic pigments in C. reinhardtii, creating nutrient deficit.

    “Additionally, both benzophenones, at 5 mg/L, induced the decrease in photosynthetic pigments, and consequently create a deficit of nutrients essential for the growth and life of the marine algae C. reinhardtii [94].”

    From UV Filters: Challenges and Prospects (2022) · cites this paper as [94]

    The Results report that BP-1 and BP-3 reduced photosynthetic pigments in C. reinhardtii, with the greatest inhibition at 5 mg/L. The Discussion suggests that altered photosynthesis may affect growth, but it does not report a nutrient deficit or identify the tested alga as marine. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • Homosalate at 1 mg/L inhibits growth of Tetraselmis sp., and benzophenone-1 and benzophenone-3 at 5 mg/L inhibit growth of Chlamydomonas reinhardtii.

    “Growth inhibition was one of the negative effects that affects algae organisms, namely Tetraselmis sp. at concentrations of 1 mg/L for homosalate (8) [93] and green algae Chlamydomonas reinhardtii at 5 mg/L for benzophenone-1 and benzophenone-3 (10) [94].”

    From UV Filters: Challenges and Prospects (2022) · cites this paper as [94]

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References 49 · Cited by 31

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  1. [1]Jeon H.-K. Chung Y. Ryu J.-C. Simultaneous determination of benzophenone-type UV filters in water and soil by gas chromatography–mass spectrometry J. Chromatogr. A 2006 1131 192 202 10.1016/j.chroma.2006.07.036 16890944 · DOI
  2. [2]Zhang Z. Ren N. Li Y.-F. Kunisue T. Gao D. Kannan K. Determination of benzotriazole and benzophenone UV filters in sediment and sewage sludge Environ. Sci. Technol. 2011 45 3909 3916 10.1021/es2004057 21480589 · DOI
  3. [3]Kim S. Choi K. Occurrences, toxicities, and ecological risks of benzophenone-3, a common component of organic sunscreen products: A mini-review Environ. Int. 2014 70 143 157 10.1016/j.envint.2014.05.015 24934855 · DOI
  4. [5]Sánchez-Quiles D. Tovar-Sánchez A. Are sunscreens a new environmental risk associated with coastal tourism? Environ. Int. 2015 83 158 170 10.1016/j.envint.2015.06.007 26142925 · DOI
  5. [7]Liao C. Kannan K. Widespread occurrence of benzophenone-type UV light filters in personal care products from China and the United States: An assessment of human exposure Environ. Sci. Technol. 2014 48 4103 4109 10.1021/es405450n 24588714 · DOI
  6. [10]Tsui M.M.P. Leung H.W. Wai T.-C. Yamashita N. Taniyasu S. Liu W. Lam P.K.S. Murphy M.B. Occurrence, distribution and ecological risk assessment of multiple classes of UV filters in surface waters from different countries Water Res. 2014 67 55 65 10.1016/j.watres.2014.09.013 25261628 · DOI
  7. [11]Ye L. Liu J. Yang X. Peng Y. Xu L. Orthogonal array design for the optimization of ionic liquid-based dispersive liquid-liquid microextraction of benzophenone-type UV filters J. Sep. Sci. 2011 34 700 706 10.1002/jssc.201000552 21290603 · DOI
  8. [12]Downs C.A. Kramarsky-Winter E. Segal R. Fauth J. Knutson S. Bronstein O. Ciner F. Jeger R. Lichtenfeld Y. Woodley C. 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. 2016 70 265 288 10.1007/s00244-015-0227-7 26487337 · DOI
  9. [13]Kasprzyk-Hordern B. Dinsdale R.M. Guwy A.J. The removal of pharmaceuticals, personal care products, endocrine disruptors and illicit drugs during wastewater treatment and its impact on the quality of receiving waters Water Res. 2009 43 363 380 10.1016/j.watres.2008.10.047 19022470 · DOI
  10. [14]Gago-Ferrero P. Mastroianni N. Díaz-Cruz M.S. Barceló D. Fully automated determination of nine ultraviolet filters and transformation products in natural waters and wastewaters by on-line solid phase extraction–liquid chromatography–tandem mass spectrometry J. Chromatogr. A 2013 1294 106 116 10.1016/j.chroma.2013.04.037 23659979 · DOI
  11. [15]Nie X.-P. Liu B.-Y. Yu H.-J. Liu W.-Q. Yang Y.-F. Toxic effects of erythromycin, ciprofloxacin and sulfamethoxazole exposure to the antioxidant system in Pseudokirchneriella subcapitata Environ. Pollut. 2013 172 23 32 10.1016/j.envpol.2012.08.013 22982550 · DOI
  12. [16]Rosi-Marshall E.J. Snow D. Bartelt-Hunt S.L. Paspalof A. Tank J.L. A review of ecological effects and environmental fate of illicit drugs in aquatic ecosystems J. Hazard. Mater. 2015 282 18 25 10.1016/j.jhazmat.2014.06.062 25062553 · DOI
  13. [17]Wilson B.A. Smith V.H. deNoyelles F. Larive C.K. Effects of three pharmaceutical and personal care products on natural freshwater algal assemblages Environ. Sci. Technol. 2003 37 1713 1719 10.1021/es0259741 12775039 · DOI
  14. [19]Petersen K. Heiaas H.H. Tollefsen K.E. Combined effects of pharmaceuticals, personal care products, biocides and organic contaminants on the growth of Skeletonema pseudocostatum Aquat. Toxicol. 2014 150 45 54 10.1016/j.aquatox.2014.02.013 24632557 · DOI
  15. [20]Sieratowicz A. Kaiser D. Behr M. Oetken M. Oehlmann J. Acute and chronic toxicity of four frequently used UV filter substances for Desmodesmus subspicatus and Daphnia magna J. Environ. Sci. Health Part A 2011 46 1311 1319 10.1080/10934529.2011.602936 21929467 · DOI
  16. [21]Mao F. He Y. Kushmaro A. Gin K.Y.-H. Effects of benzophenone-3 on the green alga Chlamydomonas reinhardtii and the cyanobacterium Microcystis aeruginosa Aquat. Toxicol. 2017 193 1 8 10.1016/j.aquatox.2017.09.029 28992446 · DOI
  17. [22]Molins-Delgado D. Gago-Ferrero P. Díaz-Cruz M.S. Barceló D. Single and joint ecotoxicity data estimation of organic UV filters and nanomaterials toward selected aquatic organisms. Urban groundwater risk assessment Environ. Res. 2016 145 126 134 10.1016/j.envres.2015.11.026 26674115 · DOI
  18. [23]Jurado A. Gago-Ferrero P. Vàzquez-Suñé E. Carrera J. Pujades E. Díaz-Cruz M.S. Barceló D. Urban groundwater contamination by residues of UV filters J. Hazard. Mater. 2014 271 141 149 10.1016/j.jhazmat.2014.01.036 24632366 · DOI
  19. [24]Jiménez-Díaz I. Iribarne-Durán L.M. Ocón O. Salamanca E. Fernández M.F. Olea N. Barranco E. Determination of personal care products–benzophenones and parabens–in human menstrual blood J. Chromatogr. B 2016 1035 57 66 10.1016/j.jchromb.2016.09.035 27693803 · DOI
  20. [25]Guo R. Xie W. Chen J. Assessing the combined effects from two kinds of cephalosporins on green alga (Chlorella pyrenoidosa) based on response surface methodology Food Chem. Toxicol. 2015 78 116 121 10.1016/j.fct.2015.02.007 25684417 · DOI
  21. [26]González-Pleiter M. Gonzalo S. Rodea-Palomares I. Leganés F. Rosal R. Boltes K. Marco E. Fernández-Piñas F. Toxicity of five antibiotics and their mixtures towards photosynthetic aquatic organisms: Implications for environmental risk assessment Water Res. 2013 47 2050 2064 10.1016/j.watres.2013.01.020 23399078 · DOI
  22. [27]Giloni-Lima P.C. Delello D. Cremonez M.L.M. Éler M.N. Lima V.A. Espíndola E.L.G. A study of the effects of chromium exposure on the growth of Pseudokirchneriella subcapitata (Korshikov) hindak evaluated by central composite design and response surface methodology Ecotoxicology 2010 19 1095 1101 10.1007/s10646-010-0491-2 20364368 · DOI
  23. [28]Khuri A.I. Mukhopadhyay S. Response surface methodology Wiley Interdiscip. Rev. Comput. Stat. 2010 2 128 149 10.1002/wics.73 · DOI
  24. [29]Guo R. Ren X. Ren H. A new method for analysis of the toxicity of organophosphorus pesticide, dimethoate on rotifer based on response surface methodology J. Hazard. Mater. 2012 237 270 276 10.1016/j.jhazmat.2012.08.041 22959264 · DOI
  25. [30]Gholami-Seyedkolaei S.J. Mirvaghefi A. Farahmand H. Kosari A.A. Gholami-Seyedkolaei S.J. Gholami-Seyedkolaei S.J. Optimization of recovery patterns in common carp exposed to Roundup using response surface methodology: Evaluation of neurotoxicity and genotoxicity effects and biochemical parameters Ecotoxicol. Environ. Saf. 2013 98 152 161 10.1016/j.ecoenv.2013.09.009 24094415 · DOI
  26. [32]Bolch C.J.S. Blackburn S.I. Isolation and purification of Australian isolates of the toxic cyanobacterium Microcystis aeruginosa Kütz J. Appl. Phycol. 1996 8 5 13 10.1007/BF02186215 · DOI
  27. [33]Hanrahan G. Lu K. Application of factorial and response surface methodology in modern experimental design and optimization Crit. Rev. Anal. Chem. 2006 36 141 151 10.1080/10408340600969478 · DOI
  28. [34]Fent K. Kunz P.Y. Zenker A. Rapp M. A tentative environmental risk assessment of the UV-filters 3-(4-methylbenzylidene-camphor), 2-ethyl-hexyl-4-trimethoxycinnamate, benzophenone-3, benzophenone-4 and 3-benzylidene camphor Mar. Environ. Res. 2010 69 S4 S6 10.1016/j.marenvres.2009.10.010 19910045 · DOI
  29. [35]Pancha I. Chokshi K. Maurya R. Trivedi K. Patidar S.K. Ghosh A. Mishra S. Salinity induced oxidative stress enhanced biofuel production potential of microalgae Scenedesmus sp. CCNM 1077 Bioresour. Technol. 2015 189 341 348 10.1016/j.biortech.2015.04.017 25911594 · DOI
  30. [36]Kunz P.Y. Fent K. Estrogenic activity of ternary UV filter mixtures in fish (Pimephales promelas)—An analysis with nonlinear isobolograms Toxicol. Appl. Pharmacol. 2009 234 77 88 10.1016/j.taap.2008.09.032 18992764 · DOI
  31. [37]Heneweer M. Muusse M. van den Berg M. Sanderson J.T. Additive estrogenic effects of mixtures of frequently used UV filters on pS2-gene transcription in MCF-7 cells Toxicol. Appl. Pharmacol. 2005 208 170 177 10.1016/j.taap.2005.02.006 16183391 · DOI
  32. [38]Kunz P.Y. Fent K. Estrogenic activity of UV filter mixtures Toxicol. Appl. Pharmacol. 2006 217 86 99 10.1016/j.taap.2006.07.014 17027055 · DOI
  33. [39]Pillai S. Behra R. Nestler H. Suter M.J.-F. Sigg L. Schirmer K. Linking toxicity and adaptive responses across the transcriptome, proteome, and phenotype of Chlamydomonas reinhardtii exposed to silver Proc. Natl. Acad. Sci. USA 2014 111 3490 3495 10.1073/pnas.1319388111 24550482 PMC3948315 · DOI
  34. [40]Paredes E. Perez S. Rodil R. Quintana J.B. Beiras R. Ecotoxicological evaluation of four UV filters using marine organisms from different trophic levels Isochrysis galbana, Mytilus galloprovincialis, Paracentrotus lividus, and Siriella armata Chemosphere 2014 104 44 50 10.1016/j.chemosphere.2013.10.053 24359924 · DOI
  35. [41]Kunz P.Y. Galicia H.F. Fent K. Comparison of in vitro and in vivo estrogenic activity of UV filters in fish Toxicol. Sci. 2006 90 349 361 10.1093/toxsci/kfj082 16403853 · DOI
  36. [42]Li M.-H. Acute toxicity of benzophenone-type UV filters and paraben preservatives to freshwater planarian, Dugesia japonica Toxicol. Environ. Chem. 2012 94 566 573 10.1080/02772248.2012.655695 · DOI
  37. [43]Li R. Chen G.-Z. Tam N.F.Y. Luan T.-G. Shin P.K.S. Cheung S.G. Liu Y. Toxicity of bisphenol A and its bioaccumulation and removal by a marine microalga Stephanodiscus hantzschii Ecotoxicol. Environ. Saf. 2009 72 321 328 10.1016/j.ecoenv.2008.05.012 18639342 · DOI
  38. [44]Kabra A.N. Ji M.-K. Choi J. Kim J.R. Govindwar S.P. Jeon B.-H. Toxicity of atrazine and its bioaccumulation and biodegradation in a green microalga, Chlamydomonas mexicana Environ. Sci. Pollut. Res. 2014 21 12270 12278 10.1007/s11356-014-3157-4 24928381 · DOI
  39. [45]Zhang S. Qiu C.B. Zhou Y. Jin Z.P. Yang H. Bioaccumulation and degradation of pesticide fluroxypyr are associated with toxic tolerance in green alga Chlamydomonas reinhardtii Ecotoxicology 2011 20 337 347 10.1007/s10646-010-0583-z 21153053 · DOI
  40. [46]DeLorenzo M.E. Scott G.I. Ross P.E. Toxicity of pesticides to aquatic microorganisms: A review Environ. Toxicol. Chem. 2001 20 84 98 10.1002/etc.5620200108 11351418 · DOI
  41. [47]Alla M.M.N. Hassan N.M. Changes of antioxidants levels in two maize lines following atrazine treatments Plant Physiol. Biochem. 2006 44 202 210 10.1016/j.plaphy.2006.05.004 16777423 · DOI
  42. [48]Sztatelman O. Grzyb J. Gabryś H. Banaś A.K. The effect of UV-B on Arabidopsis leaves depends on light conditions after treatment BMC Plant Biol. 2015 15 281 10.1186/s12870-015-0667-2 26608826 PMC4660668 · DOI
  43. [49]Ding T. Lin K. Yang B. Yang M. Li J. Li W. Gan J. Biodegradation of naproxen by freshwater algae Cymbella sp. and Scenedesmus quadricauda and the comparative toxicity Bioresour. Technol. 2017 238 164 173 10.1016/j.biortech.2017.04.018 28433904 · DOI
  44. [50]Melegari S.P. Perreault F. Costa R.H.R. Popovic R. Matias W.G. Evaluation of toxicity and oxidative stress induced by copper oxide nanoparticles in the green alga Chlamydomonas reinhardtii Aquat. Toxicol. 2013 142 431 440 10.1016/j.aquatox.2013.09.015 24113166 · DOI
  45. [51]Zamani H. Moradshahi A. Jahromi H.D. Sheikhi M.H. Influence of PbS nanoparticle polymer coating on their aggregation behavior and toxicity to the green algae Dunaliella salina Aquat. Toxicol. 2014 154 176 183 10.1016/j.aquatox.2014.05.012 24907922 · DOI
  46. [52]Broderius S.J. Kahl M.D. Elonen G.E. Hammermeister D.E. Hoglund M.D. A comparison of the lethal and sublethal toxicity of organic chemical mixtures to the fathead minnow (Pimephales promelas) Environ. Toxicol. Chem. 2005 24 3117 3127 10.1897/05-094R.1 16445094 · DOI
  47. [53]Ozáez I. Morcillo G. Martínez-Guitarte J.-L. The effects of binary UV filter mixtures on the midge Chironomus riparius Sci. Total Environ. 2016 556 154 162 10.1016/j.scitotenv.2016.02.210 26971216 · DOI

Authors
Mao, F., He, Y., & Gin, K.
Affiliations
  • National University of Singapore (SG)
  • Shanghai Jiao Tong University (CN)
Corresponding author
Gin, Karina
ORCID
Venue
Toxics
Publisher
MDPI AG
Published
2018-01-10
Volume
6
Issue
1
Pages
8
ISSN
2305-6304 (ISSN-L)
DOI
10.3390/toxics6010008
PMC
PMC5874781
OpenAlex
W2783816246
Cited by
31
References
49
Citations by year
2026: 1 · 2025: 5 · 2024: 3 · 2023: 3 · 2022: 3 · 2021: 6 · 2020: 4 · 2019: 4 · 2018: 2
FWCI
1.98
Type
journal article
Language
en
Open access
Licence
Locations
  • Toxics (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • National University of Singapore (submittedVersion)
Funders
  • National Research Foundation, Prime Minister’s Office, Singapore under its Campus for Research Excellence and Technological Enterprise (CREATE) programme
  • China Scholarship Council (CSC)
  • National University of Singapore (NUS)
Topics
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Environmental Toxicology and Ecotoxicology
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Toxic Organic Pollutants Impact
  • Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Effects and risks of endocrine disrupting chemicals
Keywords
benzophenone UV filters, benzophenone-1, benzophenone-3, combined toxicity, Chlamydomonas reinhardtii, green algae, ecotoxicology, photosynthetic pigments, algal growth inhibition, photosynthesis inhibition, response surface methodology, polynomial regression

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