Abstract
The ubiquitous presence of TiO2 nanoparticles (nTiO2) and microplastics (MPs) in marine ecosystems has raised serious concerns about their combined impact on marine biota. This study investigated the combined toxic effect of nTiO2 (1 mg/L) and NH2 and COOH surface functionalized polystyrene MPs (PSMPs) (2.5 and 10 mg/L) on Chlorella sp. All the experiments were carried out under both visible light and UV-A radiation conditions to elucidate the impact of light on the combined toxicity of these pollutants. Growth inhibition results indicated that pristine nTiO2 exhibited a more toxic effect (38%) under UV-A radiation when compared to visible light conditions (27%). However, no significant change in the growth inhibitory effects of pristine PSMPs was observed between visible light and UVA radiation conditions. The combined pollutants (nTiO2 + 10 mg/L PSMPs) under UV-A radiation exhibited more growth inhibition (nTiO2 + NH2 PSMPs 66%; nTiO2 + COOH PSMPs 50%) than under visible light conditions (nTiO2 + NH2 PSMPs 55%; TiO2 + COOH PSMPs 44%). Independent action modeling indicated that the mixture of nTiO2 with PSMPs (10 mg/L) exhibited an additive effect on the algal growth inhibition under both the light conditions. The photoactive nTiO2 promoted increased production of reactive oxygen species under UV-A exposure, resulting in cellular damage, lipid peroxidation, and impaired photosynthesis. The effects were more pronounced in case of the mixtures where PSMPs added to the oxidative stress. The toxic effects of the binary mixtures of nTiO2 and PSMPs were further confirmed through the field emission electron microscopy, revealing specific morphological abnormalities. This study provides valuable insights into the potential risks associated with the combination of nTiO2 and MPs in marine environments, considering the influence of environmentally relevant light conditions and the test medium.
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References
Abdulrahman A-A, Zhang L, Yang J 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
Adochite C, Andronic L (2020) Aquatic toxicity of photocatalyst nanoparticles to green microalgae Chlorella vulgaris. Water (Basel) 13:77
Ali I, Tan X, Li J et al (2022) Interaction of microplastics and nanoplastics with natural organic matter (NOM) and the impact of NOM on the sorption behavior of anthropogenic contaminants—a critical review. J Clean Prod 376:134314. https://doi.org/10.1016/j.jclepro.2022.134314
Arrojo MÁ, Regaldo L, Calvo Orquín J et al (2022) Potential of the microalgae Chlorella fusca (Trebouxiophyceae, Chlorophyta) for biomass production and urban wastewater phycoremediation. AMB Express 12:43
Awashra M, Młynarz P (2023) The toxicity of nanoparticles and their interaction with cells: an in vitro metabolomic perspective. Nanoscale Adv 5:2674–2723
Bai F, Jia Y, Yang C et al (2019) Multiple physiological response analyses aid the understanding of sensitivity variation between Microcystis aeruginosa and Chlorella sp. under paraquat exposures. Environ Sci Eur 31:1–17
Bais AF, Lucas RM, Bornman JF et al (2018) Environmental effects of ozone depletion, UV radiation and interactions with climate change: UNEP Environmental Effects Assessment Panel, update 2017. Photochem Photobiol Sci 17:127–179
Bergmann M, Almroth BC, Brander SM et al (2022) A global plastic treaty must cap production. Science 376:469–470
Carmona-Valdivieso DE, Valdivieso T, Carmona-Galindo VD (2023) Detection of secondary microplastics in an aquatic mesocosm by means of object-based image analysis. Microplastics 2:268–277
Davarpanah E, Guilhermino L (2019) Are gold nanoparticles and microplastics mixtures more toxic to the marine microalgae Tetraselmis chuii than the substances individually? Ecotoxicol Environ Saf 181:60–68
Diffey BL (2002) Sources and measurement of ultraviolet radiation. Methods 28:4–13. https://doi.org/10.1016/S1046-2023(02)00204-9
Dong F, Lin Q, Li C et al (2021) Impacts of pre-oxidation on the formation of disinfection byproducts from algal organic matter in subsequent chlor(am)ination: a review. Sci Total Environ 754:141955. https://doi.org/10.1016/j.scitotenv.2020.141955
Filová A, Fargašová A, Molnárová M (2021) Cu, Ni, and Zn effects on basic physiological and stress parameters of Raphidocelis subcapitata algae. Environ Sci Pollut Res 28:58426–58441. https://doi.org/10.1007/s11356-021-14778-6
Fu L, Hamzeh M, Dodard S et al (2015) Effects of TiO2 nanoparticles on ROS production and growth inhibition using freshwater green algae pre-exposed to UV irradiation. Environ Toxicol Pharmacol 39:1074–1080. https://doi.org/10.1016/j.etap.2015.03.015
Gao G, Zhao X, Jin P et al (2021) Current understanding and challenges for aquatic primary producers in a world with rising micro-and nano-plastic levels. J Hazard Mater 406:124685
Giri S, Christudoss AC, Chandrasekaran N et al (2023) The role of algal EPS in reducing the combined toxicity of BPA and polystyrene nanoparticles to the freshwater algae Scenedesmus obliquus. Plant Physiol Biochem 197:107664
Gottschalk F, Debray B, Klaessig F et al (2023) Predicting accidental release of engineered nanomaterials to the environment. Nat Nanotechnol 18:412–418
Gunasekaran D, Chandrasekaran N, Jenkins D, Mukherjee A (2020a) Plain polystyrene microplastics reduce the toxic effects of ZnO particles on marine microalgae Dunaliella salina. J Environ Chem Eng 8:104250. https://doi.org/10.1016/j.jece.2020.104250
Guzzetti E, Sureda A, Tejada S, Faggio C (2018) Microplastic in marine organism: environmental and toxicological effects. Environ Toxicol Pharmacol 64:164–171. https://doi.org/10.1016/j.etap.2018.10.009
Hazeem LJ, Kuku G, Dewailly E et al (2019) Toxicity effect of silver nanoparticles on photosynthetic pigment content, growth, ROS production and ultrastructural changes of microalgae Chlorella vulgaris. Nanomaterials 9:914
Huang X, Huang Y, Wang D et al (2021) Cellular response of freshwater algae to halloysite nanotubes: alteration of oxidative stress and membrane function. Environ Sci Nano 8:3262–3272
Jung MR, Horgen FD, Orski SV et al (2018) Validation of ATR FT-IR to identify polymers of plastic marine debris, including those ingested by marine organisms. Mar Pollut Bull 127:704–716. https://doi.org/10.1016/j.marpolbul.2017.12.061
Khalifeh F, Salari H, Zamani H (2022) Mechanism of MnO2 nanorods toxicity in marine microalgae Chlorella sorokiniana during long-term exposure. Mar Environ Res 179:105669. https://doi.org/10.1016/j.marenvres.2022.105669
Kim J, Lee S, Kim C et al (2014) Non-monotonic concentration–response relationship of TiO2 nanoparticles in freshwater cladocerans under environmentally relevant UV-A light. Ecotoxicol Environ Saf 101:240–247
Koski M, Søndergaard J, Christensen AM, Nielsen TG (2021) Effect of environmentally relevant concentrations of potentially toxic microplastic on coastal copepods. Aquatic Toxicology 230:105713
Kumar A, Mishra S, Pandey R, Yu ZG, Kumar M, Khoo KS, Thakur TK, Show PL (2023) Microplastics in terrestrial ecosystems: Un-ignorable impacts on soil characterises, nutrient storage and its cycling. Trends Anal Chem 158. https://doi.org/10.1016/j.trac.2022.116869
Lagarde F, Olivier O, Zanella M et al (2016) Microplastic interactions with freshwater microalgae: hetero-aggregation and changes in plastic density appear strongly dependent on polymer type. Environ Pollut 215:331–339
Li D, Tang X, Xu X, Zhao Y, Li L, Zhang B, Zhao Y (2023) UV-B radiation alleviated detrimental effects of polymethyl methacrylate microplastics on marine diatom Thalassiosira pseudonana. Sci Total Envi 892. https://doi.org/10.1016/j.scitotenv.2023.164388
Li J, Mao S, Ye Y et al (2021a) Micro-polyethylene particles reduce the toxicity of nano zinc oxide in marine microalgae by adsorption. Environ Pollut 290:118042
Li S, Wang P, Zhang C et al (2020a) Influence of polystyrene microplastics on the growth, photosynthetic efficiency and aggregation of freshwater microalgae Chlamydomonas reinhardtii. Sci Total Environ 714:136767. https://doi.org/10.1016/j.scitotenv.2020.136767
Li X, Qiu H, Zhang P et al (2023b) Role of heteroaggregation and internalization in the toxicity of differently sized and charged plastic nanoparticles to freshwater microalgae. Environ Pollut 316:120517
Li Z, Hu M, Song H et al (2021b) Toxic effects of nano-TiO2 in bivalves—a synthesis of meta-analysis and bibliometric analysis. J Environ Sci 104:188–203
Li Zhou, Juneau Philippe, Lian Yingli, Zhang Wei, Wang Shanquan, Wang Cheng, Shu Longfei, Yan Qingyun, He Zhili, Kui Xu (2020) Effects of Titanium Dioxide Nanoparticles on Photosynthetic and Antioxidative Processes of Scenedesmus obliquus. Plants 9(12):1748. https://doi.org/10.3390/plants9121748
Li Z, Yi X, Zhou H et al (2020c) Combined effect of polystyrene microplastics and dibutyl phthalate on the microalgae Chlorella pyrenoidosa. Environ Pollut 257:113604. https://doi.org/10.1016/j.envpol.2019.113604
Liu F, Gao Z, Chu W, Wang S (2022) Polystyrene nanoplastics alleviate the toxicity of CuO nanoparticles to the marine algae Platymonas helgolandica var. tsingtaoensis. Front Mar Sci 9:1089282
Liu Y, Wang S, Wang Z et al (2018) TiO2, SiO2 and ZrO2 nanoparticles synergistically provoke cellular oxidative damage in freshwater microalgae. Nanomaterials 8:95
Maltsev Y, Maltseva K, Kulikovskiy M, Maltseva S (2021) Influence of light conditions on microalgae growth and content of lipids, carotenoids, and fatty acid composition. Biology (Basel) 10:1060
Mao Y, Ai H, Chen Y et al (2018) Phytoplankton response to polystyrene microplastics: perspective from an entire growth period. Chemosphere 208:59–68
Middepogu A, Hou J, Gao X, Lin D (2018) Effect and mechanism of TiO2 nanoparticles on the photosynthesis of Chlorella pyrenoidosa. Ecotoxicol Environ Saf 161:497–506
Mo L, Yang Y, Zhao D et al (2022) Time-dependent toxicity and health effects mechanism of cadmium to three green algae. Int J Environ Res Public Health 19:10974
Moma J, Baloyi J (2019) Modified titanium dioxide for photocatalytic applications. Photocatalysts-Appl Attributes 18:10–5772
Natarajan L, Jenifer MA, Chandrasekaran N et al (2022) Polystyrene nanoplastics diminish the toxic effects of Nano-TiO2 in marine algae Chlorella sp. Environ Res 204:112400
Nava V, Leoni B (2021) A critical review of interactions between microplastics, microalgae and aquatic ecosystem function. Water Res 188:116476
Negi S, Perrine Z, Friedland N et al (2020) Light regulation of light-harvesting antenna size substantially enhances photosynthetic efficiency and biomass yield in green algae. Plant J 103:584–603
Nolte TM, Hartmann NB, Kleijn JM et al (2017) The toxicity of plastic nanoparticles to green algae as influenced by surface modification, medium hardness and cellular adsorption. Aquat Toxicol 183:11–20
OECD (2011) OECD guidelines for the testing of chemicals. Organ Econ Coop Dev, Freshwater alga and cyanobacteria, Growth inhibition test. https://doi.org/10.1787/9789264203785-en
Okoye CO, Addey CI, Oderinde O, Okoro JO, Uwamungu JY, Ikechukwu CK, Okeke ES, Ejeromedoghene O, Odii EC (2022) Toxic Chemicals and Persistent Organic Pollutants Associated with Micro-and Nanoplastics Pollution. Chem Eng J Advances 11:100310. https://doi.org/10.1016/j.ceja.2022.100310
Oladipupo P, Raman A, Pekny JF (2023) Minimum production scale for economic feasibility of a titanium dioxide plant. J Adv Manuf Proc 5(4). https://doi.org/10.1002/amp2.10167
Pattanaik P, Sahoo MK (2014) TiO2 photocatalysis: progress from fundamentals to modification technology. Desalination Water Treat 52:6567–6590
Pencik O, Durdakova M, Molnarova K et al (2023) Microplastics and nanoplastics toxicity assays: a revision towards to environmental-relevance in water environment. J Hazard Mater 454:131476. https://doi.org/10.1016/j.jhazmat.2023.131476
Pikula K, Johari SA, Santos-Oliveira R, Golokhvast K (2022) Individual and binary mixture toxicity of five nanoparticles in marine microalga Heterosigma akashiwo. Int J Mol Sci 23:990
Pirsaheb M, Hossini H, Makhdoumi P (2020) Review of microplastic occurrence and toxicological effects in marine environment: experimental evidence of inflammation. Process Saf Environ Protect 142:1–14
Pourebrahimi S, Pirooz M (2023) Microplastic pollution in the marine environment: a review. J Hazard Mater Adv 10:100327. https://doi.org/10.1016/j.hazadv.2023.100327
Prata JC, Lavorante BR, Maria da Conceição BSM, Guilhermino L (2018) Influence of microplastics on the toxicity of the pharmaceuticals procainamide and doxycycline on the marine microalgae Tetraselmis chuii. Aquat Toxicol 197:143–152. https://doi.org/10.1016/j.aquatox.2018.02.015
Qi N, Wang P, Wang C, Ao Y (2018) Effect of a typical antibiotic (tetracycline) on the aggregation of TiO2 nanoparticles in an aquatic environment. J Hazard Mater 341:187–197. https://doi.org/10.1016/j.jhazmat.2017.07.046
Qian W, Chen CC, Zhou S et al (2020) TiO2 nanoparticles in the marine environment: enhancing bioconcentration, while limiting biotransformation of arsenic in the mussel Perna viridis. Environ Sci Technol 54:12254–12261. https://doi.org/10.1021/acs.est.0c01620
Rezayian M, Niknam V, Ebrahimzadeh H (2019) Oxidative damage and antioxidative system in algae. Toxicol Rep 6:1309–1313
Roy B, Chandrasekaran H, Suresh PK et al (2018a) UVΑ pre-irradiation to P25 titanium dioxide nanoparticles enhanced its toxicity towards freshwater algae Scenedesmus obliquus. Environ Sci Pollut Res 25:16729–16742. https://doi.org/10.1007/s11356-018-1860-2
Roy B, Suresh PK, Chandrasekaran N, Mukherjee A (2020) UVB pre-irradiation of titanium dioxide nanoparticles is more detrimental to freshwater algae than UVA pre-irradiation. J Environ Chem Eng 8:104076. https://doi.org/10.1016/j.jece.2020.104076
Sachdev S, Ansari SA, Ansari MI (2023) Photosynthetic apparatus: major site of oxidative damage. In: Reactive Oxygen Species in Plants: The Right Balance. Springer, pp 75–92
Sendra M, Moreno-Garrido I, Yeste MP et al (2017a) Toxicity of TiO2, in nanoparticle or bulk form to freshwater and marine microalgae under visible light and UV-A radiation. Environ Pollut 227:39–48. https://doi.org/10.1016/j.envpol.2017.04.053
Sendra M, Yeste MP, Gatica JM et al (2017c) Homoagglomeration and heteroagglomeration of TiO2, in nanoparticle and bulk form, onto freshwater and marine microalgae. Sci Total Environ 592:403–411. https://doi.org/10.1016/j.scitotenv.2017.03.127
Sirohi P, Verma H, Singh SK et al (2022) Microalgal carotenoids: therapeutic application and latest approaches to enhance the production. Curr Issues Mol Biol 44:6257–6279
Song X, Kong F, Liu B-F et al (2023) Thallium-mediated NO signaling induced lipid accumulation in microalgae and its role in heavy metal bioremediation. Water Res 239:120027
St Mary L (2020) Time-related formation of bioactive polycyclic aromatic hydrocarbon (PAH) photoproducts upon interaction with TiO2 nanoparticles in the aqueous phase (Doctoral dissertation, Heriot-Watt University)
Strokal M, Vriend P, Bak MP et al (2023) River export of macro-and microplastics to seas by sources worldwide. Nat Commun 14:4842
Su Y, Cheng Z, Hou Y et al (2022) Biodegradable and conventional microplastics posed similar toxicity to marine algae Chlorella vulgaris. Aquat Toxicol 244:106097
Thiagarajan V, Alex SA, Seenivasan R et al (2021) Toxicity evaluation of nano-TiO2 in the presence of functionalized microplastics at two trophic levels: algae and crustaceans. Sci Total Environ 784:147262
Thiagarajan V, Iswarya VPAJ, Seenivasan R, Chandrasekaran N, Mukherjee A (2019a) Influence of differently functionalized polystyrene microplastics on the toxic effects of P25 TiO2 NPs towards marine algae Chlorella sp. Aquat Toxicol 207:208–216. https://doi.org/10.1016/j.aquatox.2018.12.014
Thiagarajan V, Natarajan L, Seenivasan R et al (2019c) Tetracycline affects the toxicity of P25 n-TiO2 towards marine microalgae Chlorella sp. Environ Res 179:108808. https://doi.org/10.1016/j.envres.2019.108808
Wan J-K, Chu W-L, Kok Y-Y, Lee C-S (2021) Influence of polystyrene microplastic and nanoplastic on copper toxicity in two freshwater microalgae. Environ Sci Pollut Res 28:33649–33668
Wang H, Xia X, Wang Z et al (2021) Contribution of dietary uptake to pah bioaccumulation in a simplified pelagic food chain: Modeling the influences of continuous vs intermittent feeding in zooplankton and fish. Environ Sci Technol 55:1930–1940
Wang L, Zhang J, Huang W, He Y (2023) Laboratory simulated aging methods, mechanisms and characteristic changes of microplastics: A review. Chemosphere 315. https://doi.org/10.1016/j.chemosphere.2023.137744
Wang T, Huang X, Jiang X et al (2019) Differential in vivo hemocyte responses to nano titanium dioxide in mussels: effects of particle size. Aquat Toxicol 212:28–36. https://doi.org/10.1016/j.aquatox.2019.04.012
Worm B, Lotze HK, Jubinville I et al (2017) Plastic as a persistent marine pollutant. Annu Rev Environ Resour 42:1–26
Wu D, Yang S, Du W et al (2019) Effects of titanium dioxide nanoparticles on Microcystis aeruginosa and microcystins production and release. J Hazard Mater 377:1–7
Wu W, Shan G, Wang S et al (2016) Environmentally relevant impacts of nano-TiO2 on abiotic degradation of bisphenol A under sunlight irradiation. Environ Pollut 216:166–172
Xia B, Zhu L, Han Q et al (2017a) Effects of TiO2 nanoparticles at predicted environmental relevant concentration on the marine scallop Chlamys farreri: an integrated biomarker approach. Environ Toxicol Pharmacol 50:128–135
Xiao R, Zheng Y (2016) Overview of microalgal extracellular polymeric substances (EPS) and their applications. Biotechnol Adv 34:1225–1244. https://doi.org/10.1016/j.biotechadv.2016.08.004
Yang W, Gao P, Nie Y et al (2021) Comparison of the effects of continuous and accumulative exposure to nanoplastics on microalga Chlorella pyrenoidosa during chronic toxicity. Sci Total Environ 788:147934
Yang W, Gao X, Wu Y et al (2020) The combined toxicity influence of microplastics and nonylphenol on microalgae Chlorella pyrenoidosa. Ecotoxicol Environ Saf 195:110484
Yao J, Wen J, Li H, Yang Y (2022) Surface functional groups determine adsorption of pharmaceuticals and personal care products on polypropylene microplastics. J Hazard Mater 423:127131. https://doi.org/10.1016/j.jhazmat.2021.127131
Yasir AM, Ma J, Ouyang X et al (2022) Effects of selected functional groups on nanoplastics transport in saturated media under diethylhexyl phthalate co-contamination conditions. Chemosphere 286:131965. https://doi.org/10.1016/j.chemosphere.2021.131965
Yu H, Yang B, Waigi MG et al (2020) The effects of functional groups on the sorption of naphthalene on microplastics. Chemosphere 261:127592. https://doi.org/10.1016/j.chemosphere.2020.127592
Zhang C, Chen X, Wang J, Tan L (2017) Toxic effects of microplastic on marine microalgae Skeletonema costatum: Interactions between microplastic and algae. Environ Pollut 220:1282–1288. https://doi.org/10.1016/j.envpol.2016.11.005
Zhang C, Lin X, Gao P, Zhao X, Ma C, Wang L, Sun H, Sun L, Liu C (2023) Combined effects of microplastics and excess boron on Microcystis aeruginosa. Sci Total Envi 891. https://doi.org/10.1016/j.scitotenv.2023.164298
Zhang F, Fan Y, Zhang D et al (2020a) Effect and mechanism of the algicidal bacterium Sulfitobacter porphyrae ZFX1 on the mitigation of harmful algal blooms caused by Prorocentrum donghaiense. Environ Pollut 263:114475
Zhang F, Wang Z, Song L et al (2020b) Aquatic toxicity of iron-oxide-doped microplastics to Chlorella pyrenoidosa and Daphnia magna. Environ Pollut 257:113451. https://doi.org/10.1016/j.envpol.2019.113451
Zhang J, Xie X, Li Q et al (2023b) Combined toxic effects of TiO2 nanoparticles and organochlorines on Chlorella pyrenoidosa in karst area natural waters. Aquat Toxicol 257:106442
Zhang X, Peng M, Zhang Q et al (2023c) UV-photoaging behavior of polystyrene microplastics enhanced by thermally-activated persulfate. J Environ Chem Eng 11:110508
Zheng X, Zhang L, Jiang C et al (2023) Acute effects of three surface-modified nanoplastics against Microcystis aeruginosa: growth, microcystin production, and mechanisms. Sci Total Environ 855:158906. https://doi.org/10.1016/j.scitotenv.2022.158906
Zhu L, Booth AM, Feng S et al (2022a) UV-B radiation enhances the toxicity of TiO 2 nanoparticles to the marine microalga Chlorella pyrenoidosa by disrupting the protection function of extracellular polymeric substances. Environ Sci Nano 9:1591–1604
Zhu X, Zhao W, Chen X et al (2020a) Growth inhibition of the microalgae Skeletonema costatum under copper nanoparticles with microplastic exposure. Mar Environ Res 158:105005
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We acknowledge Vellore Institute of Technology, Vellore, India, for field emission scanning electron microscopy (FE-SEM) facility used in this study.
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Camil Rex M: investigation, methodology, visualization, formal analysis, and writing—original draft. Amitava Mukherjee: conceptualization, methodology, supervision, project administration, and writing—review and editing.
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Rex M, C., Mukherjee, A. The comparative effects of visible light and UV-A radiation on the combined toxicity of P25 TiO2 nanoparticles and polystyrene microplastics on Chlorella sp.. Environ Sci Pollut Res 30, 122700–122716 (2023). https://doi.org/10.1007/s11356-023-30910-0
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DOI: https://doi.org/10.1007/s11356-023-30910-0