Skip to main content

Advertisement

Log in

Combined effects of titanium dioxide nanoparticles and bisphenol-A on freshwater algae Scenedesmus obliquus, and the importance of humic acid in reducing toxicity

  • Original Paper
  • Published:
Nanotechnology for Environmental Engineering Aims and scope Submit manuscript

Abstract

The rising usage of titanium dioxide nanoparticles (nTiO2) in household products has led to their widespread occurrence in freshwater systems. Bisphenol-A (BPA), a secondary contaminant, can modify the toxic potential of nTiO2. This study aimed to investigate the effects of BPA on the poisonous effects of nTiO2 on algae. Four concentrations of nTiO2, 0.4, 0.8, 1.6, and 3.2 mg L−1, were mixed with 1 mg L−1 of BPA to perform the mixture toxicity tests with Scenedesmus obliquus, a freshwater alga. To understand the effects of natural organics on the combination toxicity of nTiO2 and BPA, humic acid (HA) was used as a model compound. The cell viability in the treatment groups containing both nTiO2 and BPA was significantly reduced compared to that with the single components. This was accompanied by increased oxidative stresses like ROS generation, LPO production, and resultant loss in the photosynthetic yield in the mixture-treated samples. The combination toxicity data was validated using Abbott’s independent action model. Furthermore, optical microscopic analysis was conducted to examine the morphological alterations in the algae. In another set of tests, 1 and 10 mg L−1 of HA were mixed with 3.2 mg L−1 of nTiO2 and 1 mg L−1 of BPA. Humic acid ameliorated the effects of the nTiO2 and BPA in the cells. This was evident from enhanced cell viability and decreased oxidative stress-enhanced photosynthetic activities in the cells. In addition, the fate of BPA in the presence of nTiO2 and HA was also studied during algal interaction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

Data will be provided on reasonable request.

References

  1. Liu J et al (2021) Occurrence, toxicity and ecological risk of bisphenol A analogues in the aquatic environment: a review. Ecotoxicol Environ Saf 208:111481

    Article  CAS  PubMed  Google Scholar 

  2. Huelsmann RD, Will C, Carasek E (2021) Determination of bisphenol A: old problem, recent creative solutions based on novel materials. J Sep Sci 44(6):1148–1173

    Article  CAS  PubMed  Google Scholar 

  3. Bouwmeester H, Hollman PC, Peters RJ (2015) Potential health impact of environmentally released micro-and nanoplastics in the human food production chain: experiences from nanotoxicology. Environ Sci Technol 49(15):8932–8947

    Article  CAS  PubMed  ADS  Google Scholar 

  4. Cera A, Cesarini G, Scalici M (2020) Microplastics in freshwater: What is the news from the world? Diversity 12(7):276

    Article  CAS  Google Scholar 

  5. Wang W et al (2017) Microplastics pollution in inland freshwaters of China: a case study in urban surface waters of Wuhan, China. Sci Total Environ 575:1369–1374

    Article  CAS  PubMed  ADS  Google Scholar 

  6. Rolsky C et al (2020) Municipal sewage sludge as a source of microplastics in the environment. Curr Opin Environ Sci Health 14:16–22

    Article  Google Scholar 

  7. de Jesus Piñon-Colin T et al (2020) Microplastics in stormwater runoff in a semiarid region, Tijuana, Mexico. Sci Total Environ 704:135411

    Article  ADS  Google Scholar 

  8. Gatidou G, Vassalou E, Thomaidis NS (2010) Bioconcentration of selected endocrine disrupting compounds in the Mediterranean mussel, Mytilus galloprovincialis. Mar Pollut Bullet 60(11):2111–2116

    Article  CAS  Google Scholar 

  9. Azizullah A et al (2022) The interplay between bisphenol A and algae: a review. J King Saud Univ Sci 34(5):102050

    Article  Google Scholar 

  10. Berhane TM et al (2017) Kinetic sorption of contaminants of emerging concern by a palygorskite-montmorillonite filter medium. Chemosphere 176:231–242

    Article  CAS  PubMed  ADS  Google Scholar 

  11. Frankowski R et al (2020) Removal of bisphenol A and its potential substitutes by biodegradation. Appl Biochem Biotechnol 191(3):1100–1110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Zhang C et al (2019) Phycoremediation of coastal waters contaminated with bisphenol A by green tidal algae Ulva prolifera. Sci Total Environ 661:55–62

    Article  CAS  PubMed  ADS  Google Scholar 

  13. Björnsdotter MK, de Boer J, Ballesteros-Gómez A (2017) Bisphenol A and replacements in thermal paper: a review. Chemosphere 182:691–706

    Article  PubMed  ADS  Google Scholar 

  14. Oehlmann J et al (2006) Bisphenol A induces superfeminization in the ramshorn snail (Gastropoda: Prosobranchia) at environmentally relevant concentrations. Environ Health Perspect 114(Suppl 1):127–133

    Article  PubMed  Google Scholar 

  15. Li D et al (2017) The acute toxicity of bisphenol A and lignin-derived bisphenol in algae, daphnids, and Japanese medaka. Environ Sci Pollut Res 24(30):23872–23879

    Article  CAS  Google Scholar 

  16. Tišler T et al (2016) Hazard identification and risk characterization of bisphenols A, F and AF to aquatic organisms. Environ Pollut 212:472–479

    Article  PubMed  Google Scholar 

  17. Tahira S et al (2019) Bio-assessment and remediation of arsenic (arsenite As-III) in water by Euglena gracilis. J Appl Phycol 31(1):423–433

    Article  MathSciNet  CAS  Google Scholar 

  18. Norvill ZN, Shilton A, Guieysse B (2016) Emerging contaminant degradation and removal in algal wastewater treatment ponds: identifying the research gaps. J Hazard Mater 313:291–309

    Article  CAS  PubMed  Google Scholar 

  19. El-Sheekh M, Ghareib M, Abou-EL-Souod G (2012) Biodegradation of phenolic and polycyclic aromatic compounds by some algae and cyanobacteria. J Bioremediation Biodegradation 3(1):1000133

    Article  Google Scholar 

  20. Ouada SB et al (2018) Effect of bisphenol A on the extremophilic microalgal strain Picocystis sp. (Chlorophyta) and its high BPA removal ability. Ecotoxicol Environ Saf 158:1–8

    Article  PubMed  Google Scholar 

  21. Ji M-K et al (2014) Biodegradation of bisphenol A by the freshwater microalgae Chlamydomonas mexicana and Chlorella vulgaris. Ecol Eng 73:260–269

    Article  Google Scholar 

  22. Staniszewska M, Nehring I, Zgrundo A (2015) The role of phytoplankton composition, biomass and cell volume in accumulation and transfer of endocrine disrupting compounds in the Southern Baltic Sea (The Gulf of Gdansk). Environ Pollut 207:319–328

    Article  CAS  PubMed  Google Scholar 

  23. Wang S et al (2016) Fate and metabolism of the brominated flame retardant tetrabromobisphenol A (TBBPA) in rice cell suspension culture. Environ Pollut 214:299–306

    Article  CAS  PubMed  Google Scholar 

  24. Eio EJ et al (2015) Biodegradation of bisphenol A by an algal-bacterial system. Environ Sci Pollut Res 22:15145–15153

    Article  CAS  Google Scholar 

  25. Endo Y et al (2007) Adsorption of bisphenol A by lactic acid bacteria, Lactococcus, strains. Appl Microbiol Biotechnol 74:202–207

    Article  CAS  PubMed  Google Scholar 

  26. Ben Ouada S et al (2018) Effect and removal of bisphenol A by two extremophilic microalgal strains (Chlorophyta). J Appl Phycol 30:1765–1776

    Article  CAS  Google Scholar 

  27. Abbas Q et al (2020) Transformation pathways and fate of engineered nanoparticles (ENPs) in distinct interactive environmental compartments: a review. Environ Int 138:105646

    Article  CAS  PubMed  Google Scholar 

  28. Abdulrahman A-A et al (2021) Toxicity assessment of synthesized titanium dioxide nanoparticles in fresh water algae Chlorella pyrenoidosa and a zebrafish liver cell line. Ecotoxicol Environ Saf 211:111948

    Article  Google Scholar 

  29. Al-Ammari A et al (2021) Toxicity assessment of synthesized titanium dioxide nanoparticles in fresh water algae Chlorella pyrenoidosa and a zebrafish liver cell line. Ecotoxicol Environ Saf 211:111948

    Article  CAS  PubMed  Google Scholar 

  30. Sadiq IM et al (2011) Ecotoxicity study of titania (TiO(2)) NPs on two microalgae species: Scenedesmus sp. and Chlorella sp. Ecotoxicol Environ Saf 74(5):1180–1187

    Article  CAS  PubMed  Google Scholar 

  31. Chen L et al (2018) Dysbiosis of gut microbiota by chronic coexposure to titanium dioxide nanoparticles and bisphenol A: implications for host health in zebrafish. Environ Pollut 234:307–317

    Article  CAS  PubMed  Google Scholar 

  32. Guo Y et al (2019) Parental co-exposure to bisphenol A and nano-TiO2 causes thyroid endocrine disruption and developmental neurotoxicity in zebrafish offspring. Sci Total Environ 650:557–565

    Article  CAS  PubMed  ADS  Google Scholar 

  33. Jiang J, Oberdörster G, Biswas P (2009) Characterization of size, surface charge, and agglomeration state of nanoparticle dispersions for toxicological studies. J Nanopart Res 11(1):77–89

    Article  CAS  Google Scholar 

  34. Chen L et al (2019) TiO2 nanoparticles and BPA are combined to impair the development of offspring zebrafish after parental coexposure. Chemosphere 217:732–741

    Article  CAS  PubMed  ADS  Google Scholar 

  35. Chiang K et al (2004) Photocatalytic degradation and mineralization of bisphenol A by TiO2 and platinized TiO2. Appl Catal A 261(2):225–237

    Article  CAS  Google Scholar 

  36. Hunge Y et al (2021) Photocatalytic degradation of bisphenol A using titanium dioxide@ nanodiamond composites under UV light illumination. J Colloid Interface Sci 582:1058–1066

    Article  CAS  PubMed  ADS  Google Scholar 

  37. Zheng D et al (2012) Effects of the interaction of TiO2 nanoparticles with bisphenol A on their physicochemical properties and in vitro toxicity. J Hazard Mater 199:426–432

    Article  PubMed  Google Scholar 

  38. Sharma A, Anthal R (2016) Humic substances in aquatic ecosystems: a review. Int J Innov Res Sci Eng Technol 5:18462–18470

    Google Scholar 

  39. Glover CN, Pane EF, Wood CM (2005) Humic substances influence sodium metabolism in the freshwater crustacean Daphnia magna. Physiol Biochem Zool 78(3):405–416

    Article  CAS  PubMed  Google Scholar 

  40. Xiong J et al (2021) Quantitative characterization of the site density and the charged state of functional groups on biochar. ACS Sustain Chem Eng 9(6):2600–2608

    Article  CAS  Google Scholar 

  41. Aiken GR, Hsu-Kim H, Ryan JN (2011) Influence of dissolved organic matter on the environmental fate of metals, nanoparticles, and colloids. ACS Publications

    Book  Google Scholar 

  42. Saleh NB, Pfefferle LD, Elimelech M (2010) Influence of biomacromolecules and humic acid on the aggregation kinetics of single-walled carbon nanotubes. Environ Sci Technol 44(7):2412–2418

    Article  CAS  PubMed  ADS  Google Scholar 

  43. Phenrat T et al (2010) Estimating attachment of nano-and submicrometer-particles coated with organic macromolecules in porous media: development of an empirical model. Environ Sci Technol 44(12):4531–4538

    Article  CAS  PubMed  ADS  Google Scholar 

  44. Liu J-F, Zhao Z-S, Jiang G-B (2008) Coating Fe3O4 magnetic nanoparticles with humic acid for high efficient removal of heavy metals in water. Environ Sci Technol 42(18):6949–6954

    Article  CAS  PubMed  ADS  Google Scholar 

  45. Zhao J et al (2019) Humic acid mitigated toxicity of graphene-family materials to algae through reducing oxidative stress and heteroaggregation. Environ Sci Nano 6(6):1909–1920

    Article  CAS  Google Scholar 

  46. Cerrillo C et al (2016) Towards the standardization of nanoecotoxicity testing: natural organic matter ‘camouflages’ the adverse effects of TiO2 and CeO2 nanoparticles on green microalgae. Sci Total Environ 543:95–104

    Article  CAS  PubMed  ADS  Google Scholar 

  47. Liu G et al (2019) Microplastic impacts on microalgae growth: effects of size and humic acid. Environ Sci Technol 54(3):1782–1789

    Article  ADS  Google Scholar 

  48. Lin D et al (2012) The influence of dissolved and surface-bound humic acid on the toxicity of TiO2 nanoparticles to Chlorella sp. Water Res 46(14):4477–4487

    Article  CAS  PubMed  ADS  Google Scholar 

  49. Roy B et al (2021) Antibiotic tetracycline enhanced the toxic potential of photo catalytically active P25 titanium dioxide nanoparticles towards freshwater algae Scenedesmus obliquus. Chemosphere 267:128923

    Article  CAS  PubMed  Google Scholar 

  50. Parsai T, Kumar A (2021) Effect of seawater acidification and plasticizer (Bisphenol-A) on aggregation of nanoparticles. Environ Res 201:111498

    Article  CAS  PubMed  Google Scholar 

  51. Zhao Y et al (2020) The effect of humic acid and bovine serum albumin on the adsorption and stability of ZnO nanoparticles on powdered activated carbon. J Clean Prod 251:119695

    Article  CAS  Google Scholar 

  52. Hanachi P et al (2022) Nano-sized polystyrene plastics toxicity to microalgae Chlorella vulgaris: toxicity mitigation using humic acid. Aquat Toxicol 245:106123

    Article  CAS  PubMed  Google Scholar 

  53. Das S et al (2022) Nanoplastics enhance the toxic effects of titanium dioxide nanoparticle in freshwater algae Scenedesmus obliquus. Comp Biochem Physiol Part C: Toxicol Pharmacol 256:109305

    CAS  Google Scholar 

  54. Zhang W et al (2014) Acute and chronic toxic effects of bisphenol a on Chlorella pyrenoidosa and Scenedesmus obliquus. Environ Toxicol 29(6):714–722

    Article  CAS  PubMed  ADS  Google Scholar 

  55. Li R et al (2008) Physiological responses of the alga Cyclotella caspia to bisphenol A exposure

  56. Naasz S, Altenburger R, Kühnel D (2018) Environmental mixtures of nanomaterials and chemicals: the Trojan-horse phenomenon and its relevance for ecotoxicity. Sci Total Environ 635:1170–1181

    Article  CAS  PubMed  ADS  Google Scholar 

  57. Ding Y et al (2019) Humic acid regulation of the environmental behavior and phytotoxicity of silver nanoparticles to Lemna minor. Environ Sci Nano 6(12):3712–3722

    Article  CAS  Google Scholar 

  58. Fathi P et al (2020) Effects of copper oxide nanoparticles on the Chlorella algae in the presence of humic acid. SN Appl Sci 2(2):1–11

    Article  Google Scholar 

  59. Roy B et al (2020) UVB pre-irradiation of titanium dioxide nanoparticles is more detrimental to freshwater algae than UVA pre-irradiation. J Environ Chem Eng 8(5):104076

    Article  CAS  Google Scholar 

  60. Tunali M et al (2020) Effect of microplastics and microplastic-metal combinations on growth and chlorophyll a concentration of Chlorella vulgaris. Sci Total Environ 743:140479

    Article  CAS  PubMed  ADS  Google Scholar 

  61. Fadare OO et al (2019) Humic acid alleviates the toxicity of polystyrene nanoplastic particles to Daphnia magna. Environ Sci Nano 6(5):1466–1477

    Article  CAS  Google Scholar 

  62. Tallec K et al (2019) Surface functionalization determines behavior of nanoplastic solutions in model aquatic environments. Chemosphere 225:639–646

    Article  CAS  PubMed  ADS  Google Scholar 

  63. Iswarya V et al (2015) Combined toxicity of two crystalline phases (anatase and rutile) of Titania nanoparticles towards freshwater microalgae: Chlorella sp. Aquat Toxicol 161:154–169

    Article  CAS  PubMed  Google Scholar 

  64. Borza C et al (2013) Oxidative stress and lipid peroxidation: a lipid metabolism dysfunction. Lipid Metab 2013(34):23–38

    Google Scholar 

  65. Zhang Y et al (2019) The effects of humic acid on the toxicity of graphene oxide to Scenedesmus obliquus and Daphnia magna. Sci Total Environ 649:163–171

    Article  CAS  PubMed  ADS  Google Scholar 

  66. Zhao Z et al (2021) Toxicity mechanism of silver nanoparticles to Chlamydomonas reinhardtii: photosynthesis, oxidative stress, membrane permeability, and ultrastructure analysis. Environ Sci Pollut Res 28(12):15032–15042

    Article  CAS  Google Scholar 

  67. Ohko Y et al (2001) Degradation of bisphenol A in water by TiO2 photocatalyst. Environ Sci Technol 35(11):2365–2368

    Article  CAS  PubMed  ADS  Google Scholar 

  68. Mills A, Lee S-K (2002) A web-based overview of semiconductor photochemistry-based current commercial applications. J Photochem Photobiol A 152(1–3):233–247

    Article  CAS  Google Scholar 

  69. Blake D. Bibliography of work on the heterogeneous photocatalytic removal of hazardous compounds from water and air--update number 4 to October 2001. 2001, National Renewable Energy Lab.(NREL), Golden, CO (United States)

  70. Nomiyama K et al (2007) Oxidative degradation of BPA using TiO2 in water, and transition of estrogenic activity in the degradation pathways. Arch Environ Contam Toxicol 52(1):8–15

    Article  CAS  PubMed  Google Scholar 

  71. Wang L et al (2017) The growth behavior of Chlorella vulgaris in bisphenol a under different cultural conditions. J Environ Anal Toxicol 7(529):2161–0525

    Google Scholar 

  72. Imai S et al (2007) Removal of phenolic endocrine disruptors by Portulaca oleracea. J Biosci Bioeng 103(5):420–426

    Article  CAS  PubMed  Google Scholar 

  73. Morohoshi K et al (2003) Synthesis and estrogenic activity of bisphenol A mono-and di-β-D-glucopyranosides, plant metabolites of bisphenol A. Environ Toxicol Chem: Int J 22(10):2275–2279

    Article  CAS  Google Scholar 

  74. Nakajima N et al (2007) Glycosylation of bisphenol A by freshwater microalgae. Chemosphere 69(6):934–941

    Article  CAS  PubMed  ADS  Google Scholar 

  75. Wang R et al (2017) Identification of novel pathways for biodegradation of bisphenol A by the green alga Desmodesmus sp. WR1, combined with mechanistic analysis at the transcriptome level. Chem Eng J 321:424–431

    Article  CAS  ADS  Google Scholar 

  76. Wu F, Deng N (2006) Photodegradation of bisphenol A in simulated lake water containing algae, humic acid and ferric ions. Environ Pollut 144(3):840–846

    Article  PubMed  Google Scholar 

  77. Gattullo CE et al (2012) Removal of bisphenol A by the freshwater green alga Monoraphidium braunii and the role of natural organic matter. Sci Total Environ 416:501–506

    Article  CAS  PubMed  ADS  Google Scholar 

  78. Han P et al (2014) Transport and retention behaviors of titanium dioxide nanoparticles in iron oxide-coated quartz sand: effects of pH, ionic strength, and humic acid. Colloids Surf, A 454:119–127

    Article  CAS  Google Scholar 

  79. Sadiq IM et al (2011) Ecotoxicity study of titania (TiO2) NPs on two microalgae species: Scenedesmus sp. and Chlorella sp. Ecotoxicol Environ Saf 74(5):1180–1187

    Article  CAS  PubMed  Google Scholar 

  80. OECD O (2011) guideline for the testing of chemicals, Freshwater Alga and Cyanobacteria, Growth Inhibition Test (201). http://www.oecdbookshop.org/oecd/index.asp

  81. Giri S, Mukherjee A (2021) Ageing with algal EPS reduces the toxic effects of polystyrene nanoplastics in freshwater microalgae Scenedesmus obliquus. J Environ Chem Eng 9(5):105978

    Article  CAS  Google Scholar 

  82. Natarajan L et al (2022) Polystyrene nanoplastics diminish the toxic effects of Nano-TiO2 in marine algae Chlorella sp. Environ Res 204:112400

    Article  CAS  PubMed  Google Scholar 

  83. Natarajan L et al (2020) Eco-corona formation lessens the toxic effects of polystyrene nanoplastics towards marine microalgae Chlorella sp.. Environ Res 188:109842

    Article  CAS  PubMed  Google Scholar 

  84. Setsukinai K et al (2003) Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J Biol Chem 278(5):3170–3175

    Article  CAS  PubMed  Google Scholar 

  85. Thiagarajan V et al (2019) Influence of differently functionalized polystyrene microplastics on the toxic effects of P25 TiO2 NPs towards marine algae Chlorella sp.. Aquat Toxicol 207:208–216

    Article  CAS  PubMed  Google Scholar 

  86. Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18(2):265–267

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are thankful and would like to acknowledge Vellore Institute of Technology, Vellore and Indian Institute of Technology, Bombay, India for Transmission electron microscopy (TEM) and High resolution Orbitrap liquid chromatograph mass spectrometer (OHR-LCMS) facilities used in this study. This project did not receive any specific grant from funding agencies.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Amitava Mukherjee.

Ethics declarations

Conflict of interest

Soupam Das and Amitava Mukherjee declares that they have no conflicts of interest.

Ethical statement

This article contains no studies with human participants or animals performed by authors.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 4130 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Das, S., Mukherjee, A. Combined effects of titanium dioxide nanoparticles and bisphenol-A on freshwater algae Scenedesmus obliquus, and the importance of humic acid in reducing toxicity. Nanotechnol. Environ. Eng. 9, 85–98 (2024). https://doi.org/10.1007/s41204-023-00355-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s41204-023-00355-4

Keywords

Navigation