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Combined toxic effects of polystyrene nanoplastics and lead on Chlorella vulgaris growth, membrane lipid peroxidation, antioxidant capacity, and morphological alterations

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Abstract

In recent years, there has been a significant rise in the utilization of amino-functionalized polystyrene nanoplastics (PS-NH2). This surge in usage can be attributed to their exceptional characteristics, including a substantial specific surface area, high energy, and strong reactivity. These properties make them highly suitable for a wide range of industrial and medical applications. Nevertheless, there is a growing apprehension regarding their potential toxicity to aquatic organisms, particularly when considering the potential impact of heavy metals like lead (Pb) on the toxicity of PS-NH2. Herein, we examined the toxic effects of sole PS-NH2 (90 nm) at five concentrations (e.g., 0, 0.125, 0.25, 0.5, and 1 mg/L), as well as the simultaneous exposure of PS-NH2 and Pb2+ (using two environmental concentrations, e.g., 20 μg/L for Pb low (PbL) and 80 μg/L for Pb higher (PbH)) to the microalga Chlorella vulgaris. After a 96-h exposure, significant differences in chlorophyll a content and algal growth (biomass) were observed between the control group and other treatments (ANOVA, p < 0.05). The algae exposed to PS-NH2, PS-NH2 + PbL, and PS-NH2 + PbH treatment groups exhibited dose-dependent toxicity responses to chlorophyll a content and biomass. According to the Abbott toxicity model, the combined toxicity of treatment groups of PS-NH2 and PbL,H showed synergistic effects. The largest morphological changes such as C. vulgaris’ size reduction and cellular aggregation were evident in the medium treated with elevated concentrations of both PS-NH2 and Pb2+. The toxicity of the treatment groups followed the sequence PS-NH2 < PS-NH2 + PbL < PS-NH2 + PbH. These results contribute novel insights into co-exposure toxicity to PS-NH2 and Pb2+ in algae communities.

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The datasets utilized in the study can be obtained from the first author upon a reasonable request.

References 

  • Abbott WS (1987) Abbotts formula—a method of computing the effectiveness of an insecticide. J Am Mosquito Contr 3:302–303

    CAS  Google Scholar 

  • Agustina S, Aidha NN, Oktarina E (2021) The extraction of antioxidants from Chlorella vulgaris for cosmetics. Mater Sci Eng 1011:012057. https://doi.org/10.1088/1757-899X/1011/1/012057

    Article  CAS  Google Scholar 

  • Ashton K, Holmes L, Turner A (2010) Association of metals with plastic production pellets in the marine environment. Mar Pollut Bull 60:2050–2055

    Article  CAS  Google Scholar 

  • Banerjee A, Qi J, Gogoi R, Wong J, Mitragotri S (2016) Role of nanoparticle size, shape and surface chemistry in oral drug delivery. J Control Release 238:76–185

    Article  Google Scholar 

  • Bellingeri A, Bergami E, Grassi G, Faleri C, Redondo-Hasselerharm P, Koelmans AA, Corsi I (2019) Combined effects of nanoplastics and copper on the freshwater alga Raphidocelis subcapitata. Aquat Toxicol 210:179–187

    Article  CAS  Google Scholar 

  • Besseling E, Wang B, Lürling M, Koelmans AA (2014) Nanoplastic affects growth of S. obliquus and reproduction of D. magna. Environ Sci Technol 48:12336–12343

    Article  CAS  Google Scholar 

  • Bhattacharya P, Lin S, Turner JP, Ke PC (2010) Physical adsorption of charged plastic nanoparticles affects algal photosynthesis. J Phys Chem C 114:16556–16561

    Article  CAS  Google Scholar 

  • Brandts I, Teles M, Gonçalves AP, Barreto A, Franco-Martinez L, Tvarijonaviciute A, Martins MA, Soares AMVM, Tort L, Oliveira M (2018) Effects of nanoplastics on Mytilus galloprovincialis after individual and combined exposure with carbamazepine. Sci Total Environ 643:775–784

    Article  CAS  Google Scholar 

  • Canesi L, Ciacci C, Fabbri R, Balbi T, Salis A, Damonte G, Cortese K, Caratto V, Monopoli MP, Dawson K (2016) Interactions of cationic polystyrene nanoparticles with marine bivalve hemocytes in a physiological environment: role of soluble hemolymph proteins. Environ Res 150:73–81

    Article  CAS  Google Scholar 

  • Chae Y, Kim D, Kim SW, An Y-J (2018) Trophic transfer and individual impact of nano-sized polystyrene in a four-species freshwater food chain. Sci Rep 8:284

    Article  Google Scholar 

  • Chen Y, Xu DQ (2010) Two patterns of leaf photosynthetic response to irradiance transition from saturating to limiting one in some plant species. New Phytol 169:789–798

    Article  Google Scholar 

  • Chen SG, Yang J, Zhang MS, Strasser RJ, Qiang S (2016) Classification and characteristics of heat tolerance in Ageratina adenophora populations using fast chlorophyll a fluorescence rise O-J-I-P. Environ Exp Bot 122:126–140

    Article  CAS  Google Scholar 

  • Chen Q, Yin D, Jia Y, Schiwy S, Legradi J, Yang S, Hollert H (2017) Enhanced uptake of BPA in the presence of nanoplastics can lead to neurotoxic effects in adult zebrafish. Sci Total Environ 609:1312–1321

    Article  CAS  Google Scholar 

  • Cole M, Lindeque P, Fileman E, Halsband C, Goodhead R, Moger J, Galloway TS (2013) Microplastic ingestion by zooplankton. Environ Sci Technol 47:6646–6655

    Article  CAS  Google Scholar 

  • Eriksen M, Mason S, Wilson S, Box C, Zellers A, Edwards W, Farley H, Amato S (2013) Microplastic pollution in the surface waters of the Laurentian Great Lakes. Mar Pollut Bull 77:177–182

    Article  CAS  Google Scholar 

  • Fadare OO, Wan B, Guo LH, Xin Y, Qin W, Yang Y (2019) Humic acid alleviates the toxicity of polystyrene nanoplastic particles to Daphnia magna. Environ Sci 6:1466–1477

    CAS  Google Scholar 

  • Fu D, Zhang Q, Fan Z, Qi H, Wang Z, Peng L (2019) Aged microplastics polyvinyl chloride interact with copper and cause oxidative stress towards microalgae Chlorella vulgaris. Aquat Toxicol 216:105319

    Article  CAS  Google Scholar 

  • Galloway TS, Cole M, Lewis C (2017) Interactions of microplastic debris throughout the marine ecosystem. Nat Ecol Evol 1:116

    Article  Google Scholar 

  • Gao Z, Wang S, Zhang Y, Liu F (2022) Single and combined toxicity of polystyrene nanoplastics and copper on Platymonas helgolandica var. tsingtaoensis: perspectives from growth inhibition, chlorophyll content and oxidative stress. Sci Total Environ 829:154571

    Article  CAS  Google Scholar 

  • Gonzalez-Fernandez C, Tallec K, Le NG, Lambert C, Soudant P, Huvet A, Suquet M, Berchel M, Paulpont I (2018) Cellular responses of Pacific oyster (Crassostrea gigas) gametes exposed in vitro to polystyrene nanoparticles. Chemosphere 208:764–772

    Article  CAS  Google Scholar 

  • Gonzalez-Fernandez C, Toullec J, Lambert C, Goïc NL, Seoane M, Moriceau B, Huvet A, Berchel M, Vincent D, Courcot L, Soudant P, Paul-Pont I (2019) Do transparent exopolymeric particles (TEP) affect the toxicity of nanoplastics on Chaetoceros Neogracile? Environ Pollut 250:873–882

    Article  CAS  Google Scholar 

  • Hazeem LJ, Yesilay G, Bououdina M, Perna S, Cetin D, Suludere Z, Barras A, Boukherroub R (2020) Investigation of the toxic effects of different polystyrene micro-and nanoplastics on microalgae Chlorella vulgaris by analysis of cell viability, pigment content, oxidative stress and ultrastructural changes. Mar Pollut Bull 156:111278

    Article  CAS  Google Scholar 

  • Hee CW, Shing WL, Chi CK (2021) Effect of Lead (Pb) exposure towards green microalgae (Chlorella vulgaris) on the changes of physicochemical parameters in water. S Afr J Chem Eng 37:252–255

    Google Scholar 

  • Hong Y, Hu H-Y, Li F-M (2008) Growth and physiological responses of freshwater green alga Selenastrum capricornutum to allelochemical ethyl 2-methyl acetoacetate (EMA) under different initial algal densities. Pestic Biochem Physiol 90:203–212

    Article  CAS  Google Scholar 

  • Jambeck JR, Geyer R, Wilcox C, Siegler TR, Perryman M, Andrady A, Narayan R, Law KL (2015) Plastic waste inputs from land into the ocean. Science 347:68–771

    Article  Google Scholar 

  • Jeong CB, Kang HM, Lee YH, Kim MS, Lee JS, Seo JS, Wang M, Lee JS (2018) Nanoplastic ingestion enhances toxicity of persistent organic pollutants (POPs) in the monogonont rotifer Brachionus koreanus via multi xenobiotic resistance (MXR) disruption. Environ Sci Technol 52:11411–11418

    Article  CAS  Google Scholar 

  • Kataba A, Botha TL, Nakayama SMM, Yohannes YB, Ikenaka Y, Wepener V, Ishizuka M (2022) Environmentally relevant lead (Pb) water concentration induce toxicity in zebrafish (Danio rerio) larvae. Comp Biochem Physiol Part c: Toxicol Pharmacol 252:09215

    Google Scholar 

  • Khoshnamvand M, Ashtiani S, Liu J (2020) Acute toxicity of gold nanoparticles synthesized from macroalga Saccharina japonica towards Daphnia magna. Environ Sci Pollut Res 27:22120–22126

    Article  CAS  Google Scholar 

  • Khoshnamvand M, Hao Z, Fadare OO, Hanachi P, Chen Y, Liu J (2020) Toxicity of biosynthesized silver nanoparticles to aquatic organisms of different trophic levels. Chemosphere 258:27346

    Article  Google Scholar 

  • Khoshnamvand M, Hanachi P, Ashtiani S, Walker TR (2021) Toxic effects of polystyrene nanoplastics on microalgae Chlorella vulgaris: changes in biomass, photosynthetic pigments and morphology. Chemosphere 280:130725

    Article  CAS  Google Scholar 

  • Kik K, Bukowska B, Sicinska P (2020) Polystyrene nanoparticles: sources, occurrence in the environment, distribution in tissues, accumulation and toxicity to various organisms. Environ Pollut 262:114297

    Article  CAS  Google Scholar 

  • Lambert S, Wagner M (2016) Characterization of nanoplastics during the degradation of polystyrene. Chemosphere 145:265–268

    Article  CAS  Google Scholar 

  • Lee KW, Shim WJ, Kwon OY, Kang JH (2013) Size-dependent effects of micro polystyrene particles in the marine copepod Tigriopus japonicas. Environ Sci Technol 47:11278–11283

    Article  CAS  Google Scholar 

  • Li H, Getzinger GJ, Ferguson PL, Orihuela B, Zhu M, Rittschof D (2016) Effects of toxic leachates from commercial plastics on larval survival and settlement of the barnacle Amphibalanus amphitrite. Environ Sci Technol 50:924–931

    Article  CAS  Google Scholar 

  • Li ZC, Yi XL, Zhou H, Chi TT, Li WT, Yang KM (2020) Combined effect of polystyrene nanoplastics and dibutyl phthalate on the microalgae Chlorella pyrenoidosa. Environ Pollut 257:113604

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    Article  CAS  Google Scholar 

  • Long M, Moriceau B, Gallinari M, Lambert C, Huvet A, Raffray J, Soudant P (2015) Interactions between microplastics and phytoplankton aggregates: impact on their respective fates. Mar Chem 175:39–46

    Article  CAS  Google Scholar 

  • Long M, Paul-Pont I, Hegaret H, Moriceau B, Lambert C, Huvet A, Soudant P (2017) Interactions between polystyrene microplastics and marine phytoplankton lead to species-specific hetero-aggregation. Environ Pollut 228:454–463

    Article  CAS  Google Scholar 

  • Manfra L, Rotini A, Bergami E, Grassi G, Faleri C, Corsi I (2017) Comparative ecotoxicity of polystyrene nanoparticles in natural seawater and reconstituted seawater using the rotifer Brachionus plicatilis. Ecotox Environ Safe 145:557–563

    Article  CAS  Google Scholar 

  • Miller DM, Buettner GR, Aust SD (1990) Transition metals as catalysts of autoxidation reactions. Free Radic Biol Med 8:95–108

    Article  CAS  Google Scholar 

  • Natarajan L, Omer S, Jetly N, Jenifer MA, Chandrasekaran N, Suraishkumar GK, Mukherjee A (2020) Eco-corona formation lessens the toxic effects of polystyrene nanoplastics towards marine microalgae Chlorella sp. Environ Res 188:109842

    Article  CAS  Google Scholar 

  • Nogueira DJ, da Silva ACDO, da Silva MLN, Vicentini DS, Matias WG (2021) Individual and combined multigenerational effects induced by polystyrene nanoplastic and glyphosate in Daphnia magna (Strauss, 1820). Sci Total Environ 811:151360

  • OECD (2011) OECD Guidelines for the Testing of Chemicals, Section 2: Effects on Biotic Systems: Freshwater Alga and Cyanobacteria, Growth Inhibition Test. Test No. 201. Organisation for Economic Co-Operation and Development, Paris. https://doi.org/10.1787/9789264069923-en

  • Oukarroum A, Bras S, Perreault F et al (2012) Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Ecotoxicol Environ Saf 78:80–85

    Article  CAS  Google Scholar 

  • Qian H, Xu X, Chen W, Jiang H, Jin Y, Liu W, Fu Z (2009) Allelochemical stress causes oxidative damage and inhibition of photosynthesis in Chlorella vulgaris. Chemosphere 75:368–375

    Article  CAS  Google Scholar 

  • Rashkov GD, Dobrikova AG, Pouneva ID, Misra AN, Apostolova EL (2012) Sensitivity of Chlorella vulgaris to herbicides. Possibility of using it as a biological receptor in biosensors. Sens Actuators B Chem 161:151–155

    Article  CAS  Google Scholar 

  • Sendra M, Staffieri E, Yeste MP, Moreno-Garrido I, Gatica JM, Corsi I, Blasco J (2019) Are the primary characteristics of polystyrene nanoplastics responsible for toxicity and ad/absorption in the marine diatom Phaeodactylum tricornutum? Environ Pollut 249:610–619

    Article  CAS  Google Scholar 

  • Shen M, Zhang Y, Zhu Y, Song B, Zeng G, Hu D, Wen X, Ren X (2019) Recent advances in toxicological research of nanoplastics in the environment: a review. Environ Pollut 252:511–521

    Article  CAS  Google Scholar 

  • Stephens B, Azimi P, El Orch Z, Ramos T (2013) Ultrafine particle emissions from desktop 3D printers. Atmos Environ 79:334–339

    Article  CAS  Google Scholar 

  • Sun N, Shi H, Xiangxiang Li, Gao C, Liu R (2023) Combined toxicity of micro/nanoplastics loaded with environmental pollutants to organisms and cells: role, effects, and mechanism. Environ Int 171:107711

    Article  CAS  Google Scholar 

  • Tan BL, Norhaizan ME, Liew W, Rahman HS (2018) Antioxidant and oxidative stress: a mutual interplay in age-related diseases. Front Pharmacol 9:1162. https://doi.org/10.3389/fphar.2018.01162

    Article  Google Scholar 

  • Tunali M, Uzoefuna EN, Tunali MM, Yenigun O (2020) Effect of microplastics and microplastic-metal combinations on growth and chlorophyll a concentration of Chlorella vulgaris. Sci Total Environ 743:140479

    Article  CAS  Google Scholar 

  • Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotocicol Environ Saf 64:178–189

    Article  CAS  Google Scholar 

  • Vance ME, Kuiken T, Vejerano EP, McGinnis SP, Hochella MF Jr, Rejeski D, Hull MS (2015) Nanotechnology in the real world: redeveloping the nanomaterial consumer products inventory. Beilstein J Nanotechnol 6:1769

    Article  CAS  Google Scholar 

  • Vedolin MC, Teophilo CYS, Turra A, Figueira RCL (2018) Spatial variability in the concentrations of metals in beached microplastics. Mar Pollut Bull 129:487–493

    Article  CAS  Google Scholar 

  • Wagner M, Scherer C, Alvarez-Muneoz D, Brennholt N, Bourrain X, Buchinger S, Fries E, Grosbois C, Klasmeier J, Marti T, Rodriguez-Mozaz S, Urbatzka R, Vethaak AD, Winther-Nielsen M, Reifferscheid G (2014) Microplastics in freshwater ecosystems: what we know and what we need to know. Environ Sci Eur 26:12

    Article  Google Scholar 

  • Wan JK, Chu WL, Kok YY, Lee C-S (2021) Influence of polystyrene microplastic and nanoplastic on copper toxicity in two freshwater microalgae. Environ Sci Pollut Res 28:33649–33668

    Article  CAS  Google Scholar 

  • Wang J, Peng J, Tan Z, Gao Y, Zhan Z, Chen Q, Cai L (2017) Microplastics in the surface sediments from the Beijing River littoral zone: composition, abundance, surface textures and interaction with heavy metals. Chemosphere 171:248–258

    Article  CAS  Google Scholar 

  • Wang S, Liu M, Wang J, Huang J, Wang J (2020) Polystyrene nanoplastics cause growth inhibition, morphological damage and physiological disturbance in the marine microalga Platymonas helgolandica. Mar Pollut Bull 158:111403

    Article  CAS  Google Scholar 

  • Wang L, Wu W-M, Bolan NS et al (2021) Environmental fate, toxicity and risk management strategies of nanoplastics in the environment: current status and future perspectives. J Hazard Mater 401:123415

    Article  CAS  Google Scholar 

  • Wright SL, Kelly FJ (2017) Plastic and human health: a micro issue? Environ Sci Technol 51:6634–6647

    Article  CAS  Google Scholar 

  • Yang W, Gao P, Nie Y, Huang J, Wu Y, Wan L, Ding H, Zhang W (2021) Comparison of the effects of continuous and accumulative exposure to nanoplastics on microalga Chlorella pyrenoidosa during chronic toxicity. Sci Total Environ 788:147934

    Article  CAS  Google Scholar 

  • Yonny ME, Garcia EM, Lopez A, Arroquy JI, Nazareno MA (2016) Measurement of malondialdehyde as oxidative stress biomarker in goat plasma by HPLC-DAD. Microchem J 129:281–285

    Article  CAS  Google Scholar 

  • Zhang WW, Duan XJ, Huang HL, Zhang Y, Wang BG (2007) Evaluation of 28 marine algae from the Qingdao coast for antioxidative capacity and determination of antioxidant efficiency and total phenolic content of fractions and subfractions derived from Symphyocladia latiuscula (Rhodomelaceae). J Appl Phycol 19:97–108

    Article  Google Scholar 

  • Zhang H, Kuo Y-Y, Gerecke AC, Wang J (2012) Co-release of hexabromocyclododecane (HBCD) and nano-and microparticles from thermal cutting of polystyrene foams. Environ Sci Technol 46:10990–10996

    Article  CAS  Google Scholar 

  • Zhang W, Xiong B, Chen L, Lin K, Cui X, Bi H, Guo M, Wang W (2013) Toxicity assessment of Chlorella vulgaris and Chlorella protothecoides following exposure to Pb(II). Environ Toxicol Pharmacol 36:51–57

    Article  Google Scholar 

  • 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 Safety 143:29–135

    Article  Google Scholar 

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Funding

This work was funded by Iran National Science Foundation (INSF) under project no. 97002416, High-Level Talents Project of Chongqing Medical University (No. R4014), and China-Sri Lanka Joint Research and Demonstration Center for Water Technology, and China-Sri Lanka Joint Center for Education and Research, Chinese Academy of Sciences, China.

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Mehdi Khoshnamvand: methodology, investigation, formal analysis, conceptualization, resources, and writing—original draft. Amir Hossein Hamidian: supervision, project administration, writing—review and editing, and funding acquisition. Saeed Ashtiani: methodology and review and editing. Jafar Ali: review and editing. De-Sheng Pei: supervision, project administration, review and editing, and funding acquisition.

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Correspondence to Amir Hossein Hamidian.

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Highlights

•The binary toxicities of PS-NH2 and PbL,H treatment groups to C. vulgaris are synergistic.

• PS-NH2, PS-NH2+PbL,, and PS-NH2+PbH treatment groups induce oxidative stress in C. vulgaris.

• PS-NH2+PbH treatment group causes the lowest antioxidant capacity in C. vulgaris.

• Largest C. vulgaris’ morphological changes are observed in the medium treated with high PS-NH2 and Pb.

• Toxicity levels of the treatment groups increased in the following order: PS-NH2 < PS-NH2+PbL < PS-NH2+PbH.

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Khoshnamvand, M., Hamidian, A.H., Ashtiani, S. et al. Combined toxic effects of polystyrene nanoplastics and lead on Chlorella vulgaris growth, membrane lipid peroxidation, antioxidant capacity, and morphological alterations. Environ Sci Pollut Res 31, 28620–28631 (2024). https://doi.org/10.1007/s11356-024-33084-5

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