Abstract
There has been increasing concern over the toxic effects of microplastics (MP), nanoplastics (NP), and copper (Cu) on microalgae. However, the combined toxicity of the metal in the presence of polystyrene (PS) MP/NP on microalgae has not been well studied, particularly after long-term exposure (i.e., longer than 4 days). The primary aim of the present study was to investigate the effect of PS MP and NP on Cu toxicity on two freshwater microalgae, namely Chlorella sp. TJ6-5 and Pseudokirchneriella subcapitata NIES-35 after acute exposure for 4 days and up to 16 days. The results showed that both microalgae were sensitive to Cu, but tolerant to MP/NP. However, MP/NP increased the toxicity of Cu at EC50 in both microalgae, which was only noticeable in chronic exposure. Single and combined treatment of MP/NP and Cu induced higher oxidative stress and caused morphological and ultrastructural changes in both microalgae. The adsorption of Cu to MP and NP was low (0.23–14.9%), with most of the Cu present in free ionic form (81.6–105.8%). The findings on different sensitivity of microalgae to Cu in the presence of MP/NP may have significant implication as microalgae are likely to be exposed to a mixture of both MP/NP and Cu in the environment. For example, in air-blasting technology, MP and NP are used as abrasive medium to remove Cu-containing antifouling paints on hulls of ship and submerged surfaces. Wastewater treatment plants receive household wastes containing MP and NP, as well as stormwater runoffs and industrial wastes contaminated with heavy metals.
Similar content being viewed by others
References
Ahad RIA, Syiem MB (2018) Copper-induced morphological, physiological and biochemical responses in the cyanobacterium Nostoc muscorum Meg 1. Nature Environment & Pollution Technology 17(4)
Auta H, Emenike C, Fauziah S (2017) Distribution and importance of microplastics in the marine environment: a review of the sources, fate, effects, and potential solutions. Environ Int 102:165–176
Barba AA, Bochicchio S, Dalmoro A, Caccavo D, Cascone S, Lamberti G (2019) Polymeric and lipid-based systems for controlled drug release: an engineering point of view. Nanomaterials for Drug Delivery and Therapy (pp. 267-304) Elsevier
Bellingeri A, Bergami E, Grassi G, Faleri C, Redondo-Hasselerharm P, Koelmans A, Corsi I (2019) Combined effects of nanoplastics and copper on the freshwater alga Raphidocelis subcapitata. Aquat Toxicol. 210:179–187
Besseling E, Wang B, Lürling M, Koelmans AA (2014) Nanoplastic affects growth of S. obliquus and reproduction of D. magna. Environ Sci Technol 48(20):12336–12343
Bhattacharya P, Lin S, Turner JP, Ke PC (2010) Physical adsorption of charged plastic nanoparticles affects algal photosynthesis. J Phys Chem C 114(39):16556–16561
Borza C, Muntean D, Dehelean C, Săvoiu G, Şerban C, Simu G, Andoni M, Butur M, Drăgan S (2013) Oxidative stress and lipid peroxidation—a lipid metabolism dysfunction. Lipid Metabolism
Brennecke D, Duarte B, Paiva F, Caçador I, Canning-Clode J (2016) Microplastics as vector for heavy metal contamination from the marine environment. Estuar Coast Shelf Sci 178:189–195
Brown JN, Peake BM (2006) Sources of heavy metals and polycyclic aromatic hydrocarbons in urban stormwater runoff. Sci Total Environ 359(1-3):145–155
Canniff PM, Hoang TC (2018) Microplastic ingestion by Daphnia magna and its enhancement on algal growth. Sci Total Environ 633:500–507
Chae Y, Kim D, An Y (2019) Effects of micro-sized polyethylene spheres on the marine microalga Dunaliella salina: focusing on the algal cell to plastic particle size ratio. Aquat Toxicol 105296
Chen L, Zhou L, Liu Y, Deng S, Wu H, Wang G (2012) Toxicological effects of nanometer titanium dioxide (nano-TiO2) on Chlamydomonas reinhardtii. Ecotoxicol Environ Saf 84:155–162
Cole M, Lindeque P, Halsband C, Galloway TS (2011) Microplastics as contaminants in the marine environment: a review. Mar Pollut Bullet 62(12):2588–2597
Crawford C, Quinn B (2017) 5-microplastics, standardisation and spatial distribution. Microplastic Pollutants; Elsevier: Kidlington, UK, 101-130
Davarpanah E, Guilhermino L (2015) Single and combined effects of microplastics and copper on the population growth of the marine microalgae Tetraselmis chuii. Estuar. Coast. Shelf Sci 167:269–275
Davidson TM (2012) Boring crustaceans damage polystyrene floats under docks polluting marine waters with microplastic. Mar Pollut Bull 64(9):1821–1828
Driedger AG, Dürr HH, Mitchell K, Van Cappellen P (2015) Plastic debris in the Laurentian Great Lakes: a review. J Great Lakes Res 41(1):9–19
Eerkes-Medrano D, Thompson RC, Aldridge DC (2015) Microplastics in freshwater systems: a review of the emerging threats, identification of knowledge gaps and prioritisation of research needs. Water Res 75:63–82
Europe Plastic (2018) The facts-2017. An analysis of European plastics production, demand and waste. Retrieved March 25, 2020, from https://www.plasticseurope.org/application/files/5715/1717/4180/Plastics_the_facts_2017_FINAL_for_website_one_page.pdf
Expósito N, Kumar V, Sierra J, Schuhmacher M, Papiol GG (2017) Performance of Raphidocelis subcapitata exposed to heavy metal mixtures. Sci Total Environ 601:865–873
Filimonova V, Nys C, De Schamphelaere KA, Gonçalves F, Marques JC, Gonçalves AM, De Troch M (2018) Ecotoxicological and biochemical mixture effects of an herbicide and a metal at the marine primary producer diatom Thalassiosira weissflogii and the primary consumer copepod Acartia tonsa. Environ Sci Pollut Res 1-16
Forsythe C (2017) The quantification of microplastics in intertidal sediments in the Bay of Fundy, Canada
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 105319
Gambardella C, Morgana S, Bramini M, Rotini A, Manfra L, Migliore L, Faimali M (2018) Ecotoxicological effects of polystyrene microbeads in a battery of marine organisms belonging to different trophic levels. Mar Environ Res. 141:313–321
Gerber IB, Dubery IA (2004) Fluorescence microplate assay for the detection of oxidative burst products in tobacco cell suspensions using 2′, 7′-dichlorofluorescein. Methods in Cell Science 25(3-4):115–122
Giorgetti L, Spanò C, Muccifora S, Bottega S, Barbieri F, Bellani L (2020) Exploring the interaction between polystyrene nanoplastics and Allium cepa during germination: internalization in root cells, induction of toxicity and oxidative stress. Plant Physiol Biochem 149:170–177
Godoy V, Blázquez G, Calero M, Quesada L, Martín-Lara M (2019) The potential of microplastics as carriers of metals. Environ Pollut 255:113363
Gouin T, Avalos J, Brunning I, Brzuska K, De Graaf J, Kaumanns J, Schlatter H (2015) Use of micro-plastic beads in cosmetic products in Europe and their estimated emissions to the North Sea environment. Sofw J 141(4):40–46
Hamed SM, Selim S, Klöck G, AbdElgawad H (2017) Sensitivity of two green microalgae to copper stress: growth, oxidative and antioxidants analyses. Ecotoxicol Environ Saf 144:19–25
Henderson R, Parsons SA, Jefferson B (2008) The impact of algal properties and pre-oxidation on solid–liquid separation of algae. Water Res 42(8-9):1827–1845
Hindarti D, Larasati A (2019) Copper (Cu) and cadmium (Cd) toxicity on growth, chlorophyll-a and carotenoid content of phytoplankton Nitzschia sp. Paper presented at the IOP Conference Series: Earth and Environmental Science 236(1):012053
Holmes LA, Turner A, Thompson RC (2012) Adsorption of trace metals to plastic resin pellets in the marine environment. Environ Pollut 160:42–48
Joseph E, Singhvi G (2019) Multifunctional nanocrystals for cancer therapy: a potential nanocarrier. Nanomaterials for drug delivery and therapy (pp. 91-116) Elsevier
Karbalaei S, Hanachi P, Walker TR, Cole M (2018) Occurrence, sources, human health impacts and mitigation of microplastic pollution. Environ Sci Pollut Res, 1-18
Koelmans AA, Besseling E, Shim WJ (2015) Nanoplastics in the aquatic environment. critical review. Marine anthropogenic litter. Springer, Cham, pp 325–340
Levy JL, Stauber JL, Jolley DF (2007) Sensitivity of marine microalgae to copper: the effect of biotic factors on copper adsorption and toxicity. Sci Total Environ 387(1-3):141–154
Li S, Wang P, Zhang C, Zhou X, Yin Z, Hu T (2020) Influence of polystyrene microplastics on the growth, photosynthetic efficiency and aggregation of freshwater microalgae Chlamydomonas reinhardtii. Sci Total Environ 714:136767
Lichtenthaler HK (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Current protocols in food analytical chemistry (pp. F4.3.1-F4.3.8)
Lin W, Su F, Lin M, Jin M, Li Y, Ding K (2020) Effect of microplastics PAN polymer and/or Cu2+ pollution on the growth of Chlorella pyrenoidosa. Environ Pollut 265:114985
Long M, Paul-Pont I, Hégaret 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
Machado MD, Soares EV (2019) Impact of erythromycin on a non-target organism: cellular effects on the freshwater microalga Pseudokirchneriella subcapitata. Aquat Toxicol 208:179–186
Malvern Panalytical (2006) Zeta potential - An introduction in 30 minutes. Retrieved from https://www.malvernpanalytical.com/en/learn/knowledge-center/technical-notes/TN101104ZetaPotentialIntroduction.html
Mao Y, Ai H, Chen Y, Zhang Z, Zeng P, Kang L, Li H (2018) Phytoplankton response to polystyrene microplastics: perspective from an entire growth period. Chemosphere. 208:59–68
Masojídek J, Torzillo G (2014) Mass cultivation of freshwater microalgae
Mattsson K, Jocic S, Doverbratt I, Hansson L (2018) Nanoplastics in the aquatic environment. Microplastic contamination in aquatic environments (pp. 379-399) Elsevier
Nishikawa K, Yamakoshi Y, Uemura I, Tominaga N (2003) Ultrastructural changes in Chlamydomonas acidophila (Chlorophyta) induced by heavy metals and polyphosphate metabolism. FEMS Microbiology Ecology 44(2):253–259
Nolte TM, Hartmann NB, Kleijn JM, Garnæs J, van de Meent D, Hendriks AJ, Baun A (2017) The toxicity of plastic nanoparticles to green algae as influenced by surface modification, medium hardness and cellular adsorption. Aquat Toxicol 183:11–20
Norberg-King TJ (1993) A linear interpolation method for sublethal toxicity: the inhibition concentration (ICp) approach. version 2.0 (No. 03-93)
Nugroho AP (2020) Integrated assessment of biomarker responses in algae Chlorella sorokiniana exposed to copper and cadmium. Biodiversitas Journal of Biological Diversity 21(8)
OECD (Organization for Economic Co-operation and Development) (2011) Test no. 201: Freshwater alga and cyanobacteria, growth inhibition test, section 2. OECD guidelines for the testing of chemicals. OECD Publishing, Paris, p 25
Ou H, Zeng EY (2018) Occurrence and fate of microplastics in wastewater treatment plants. Microplastic contamination in aquatic environments (pp. 317-338) Elsevier
Oukarroum A, Bras S, Perreault F, Popovic R (2012) Inhibitory effects of silver nanoparticles in two green algae, Chlorella vulgaris and Dunaliella tertiolecta. Ecotoxicol Environ Saf 78:80–85
Pancha I, Chokshi K, Maurya R, Trivedi K, Patidar SK, Ghosh A (2015) Salinity induced oxidative stress enhanced biofuel production potential of microalgae Scenedesmus sp. CCNM 1077. Bioresour Technol 189:341–348
Pap E, Drummen G, Winter V, Kooij T, Rijken P, Wirtz K, Post J (1999) Ratio-fluorescence microscopy of lipid oxidation in living cells using C11-BODIPY581/591. FEBS Letters 453(3):278–282
Peng L, Fu D, Qi H, Lan CQ, Yu H, Ge C (2019a) Micro-and nano-plastics in marine environment: source, distribution and threats—a review. Sci Total Environ 698:134254
Peng S, Long M, Zheng L, Song L, Li J (2019b) Physiological sensitivity of Haematococcus pluvialis (Chlorophyta) to environmental pollutants: a comparison with Microcystis wesenbergii (Cyanobacteria) and Pseudokirchneriella subcapitata (Chlorophyta). J Appl Phycol 31(1):365–374
Prata JC, da Costa JP, Lopes I, Duarte AC, Rocha-Santos T (2019) Effects of microplastics on microalgae populations: a critical review. Sci Total Environ. 665:400–405
Rangsayatorn N, Upatham E, Kruatrachue M, Pokethitiyook P, Lanza G (2002) Phytoremediation potential of Spirulina (Arthrospira) platensis: biosorption and toxicity studies of cadmium. Environ Pollut 119(1):45–53
Rochman CM, Kross SM, Armstrong JB, Bogan MT, Darling ES, Green SJ, Veríssimo D (2015) Scientific Evidence Supports a Ban on Microbeads.
Rogers NJ, Franklin NM, Apte SC, Batley GE, Angel BM, Lead JR, Baalousha M (2010) Physico-chemical behaviour and algal toxicity of nanoparticulate CeO2 in freshwater. Environ Chem 7(1):50–60
Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012
Shim WJ, Hong SH, Eo S (2018) Marine microplastics: abundance, distribution, and composition. Microplastic contamination in aquatic environments (pp. 1-26) Elsevier
Shnoudeh AJ, Hamad I, Abdo RW, Qadumii L, Jaber AY, Surchi HS (2019) Synthesis, characterization, and applications of metal nanoparticles. Biomaterials and bionanotechnology (pp. 527-612) Elsevier
Silva JC, Echeveste P, Lombardi AT (2018) Higher biomolecules yield in phytoplankton under copper exposure. Ecotoxicol Environ Saf 161:57–63
Sousa CA, Soares HM, Soares EV (2019) Chronic exposure of the freshwater alga Pseudokirchneriella subcapitata to five oxide nanoparticles: hazard assessment and cytotoxicity mechanisms. Aquat Toxicol 214:105265
Srinivasan M, Swain GW (2007) Managing the use of copper-based antifouling paints. Environ Manage 39(3):423–441
Stein JR, Hellebust JA, Craigie J (1973) Handbook of phycological methods: culture methods and growth measurements. Cambridge University Press
Strejckova A, Dvorak M, Klejdus B, Krystofova O, Hedbavny J, Adam V, Huska D (2019) The strong reaction of simple phenolic acids during oxidative stress caused by nickel, cadmium and copper in the microalga Scenedesmus quadricauda. New Biotechnology 48:66–75
Syed S, Arasu A, Ponnuswamy I (2015) The uses of Chlorella vulgaris as antimicrobial agent and as a diet: the presence of bio-active compounds which caters the vitamins, minerals in general. International Journal of Bio-Science and Bio-Technology 7(1):185–190
Tsigie YA, Huynh LH, Ismadji S, Engida AM, Ju Y (2012) In situ biodiesel production from wet Chlorella vulgaris under subcritical condition. Chem Eng J 213:104–108
Turner A, Holmes LA (2015) Adsorption of trace metals by microplastic pellets in fresh water. Environ Chem 12(5):600–610
Ugya AY, Imam TS, Li A, Ma J, Hua X (2020) Antioxidant response mechanism of freshwater microalgae species to reactive oxygen species production: a mini review. Chem Ecol 36(2):174–193
Volland S, Bayer E, Baumgartner V, Andosch A, Lütz C, Sima E, Lütz-Meindl U (2014) Rescue of heavy metal effects on cell physiology of the algal model system Micrasterias by divalent ions. J Plant Physiol 171(2):154–163
Wan JK, Chu WL, Kok YY, Cheong KW (2017) Assessing the toxicity of copper oxide nanoparticles and copper sulfate in a tropical Chlorella. J Appl Phycol, 1-13
Wan JK, Chu WL, Kok YY, Lee CS (2018) Distribution of microplastics and nanoplastics in aquatic ecosystems and their impacts on aquatic organisms, with emphasis on microalgae. Rev Environ Contam Toxicol 246:133–158 Springer
Wang H, Sathasivam R, Ki J (2017a) Physiological effects of copper on the freshwater alga Closterium ehrenbergii Meneghini (Conjugatophyceae) and its potential use in toxicity assessments. Algae 32(2):131–137
Wang J, Peng J, Tan Z, Gao Y, Zhan Z, Chen Q, Cai L (2017b) Microplastics in the surface sediments from the Beijiang River littoral zone: composition, abundance, surface textures and interaction with heavy metals. Chemosphere 171:248–258
Wu C, He C (2019) Interaction effects of oxytetracycline and copper at different ratios on marine microalgae Isochrysis galbana. Chemosphere 225:775–784
Yi X, Chi T, Li Z, Wang J, Yu M, Wu M, Zhou H (2019) Combined effect of polystyrene plastics and triphenyltin chloride on the green algae Chlorella pyrenoidosa. Environ Sci Pollut Res, 1-8.
Yokota K, Waterfield H, Hastings C, Davidson E, Kwietniewski E, Wells B (2017) Finding the missing piece of the aquatic plastic pollution puzzle: interaction between primary producers and microplastics. Limnology and Oceanography Letters 2(4):91–104
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
Zhang Q, Qu Q, Lu T, Ke M, Zhu Y, Zhang M, Sun L (2018) The combined toxicity effect of nanoplastics and glyphosate on Microcystis aeruginosa growth. Environ Pollut 243:1106–1112
Acknowledgments
We would like to dedicate this paper to Professor Chu Wan Loy. We also would like to acknowledge International Medical University for providing the funding and research facility to support this project.
Availability of data and materials
The authors declare that all data supporting the findings of this study are available within the article and its supplementary information files.
Funding
This project was financially supported by Internal Grant IMU 377/2017 from International Medical University.
Author information
Authors and Affiliations
Author notes
†Deceased on 15 June 2020
- Wan-Loy Chu
Contributions
All authors contributed to the study conception and design. Material preparation, and data collection and analysis were performed by J.K. The first draft of the article was written by JK and all authors commented on previous versions of the manuscript. All authors (J.K., Y.Y., and C.S.) read and approved the final manuscript. Written consent was obtained from the widow of the late W.L. to include his name in the final manuscript. The authors (J.K., Y.Y., and C.S.) were agreeable to the inclusion of W.L.’s name in final authorship list as he was instrumental in critically reviewing the early versions of the manuscript.
Corresponding author
Ethics declarations
Ethics approval
This project was approved by the International Medical University Joint Committee on Research and Ethics (IMU-JC) (Project ID number IMU 377/2017).
Competing interests
The authors declare that they have no competing interests.
Additional information
Responsible editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Wan, JK., Chu, WL., Kok, YY. et al. Influence of polystyrene microplastic and nanoplastic on copper toxicity in two freshwater microalgae. Environ Sci Pollut Res 28, 33649–33668 (2021). https://doi.org/10.1007/s11356-021-12983-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-12983-x