Abstract
The effects of pristine polystyrene microplastics (pMPs) without any pretreatment at different concentrations (0, 10, 20, 50, and 100 mg/L) on Phaeodactylum tricornutum Bohlin at two initial algae densities (105 and 106 cells mL) were assessed in this study. Hormesis-like effects were found when microalgae grew with pMPs. The results showed that pMPs inhibited microalgae growth under a high concentration of microplastics tolerated by individual algal cell (low initial algae density) (up to −80.18±9.71%) but promoted growth when the situation was opposite (up to 15.27±3.66%). The contents of photosynthetic pigments including chlorophyll a, chlorophyll c and carotenoids showed resistance to pMPs stress under a low initial algae density and increased with time, but the opposite was true under a high initial algae density. Compared with the low initial algae density group, Qp received less inhibition, and NPQ (heat dissipation) also decreased under the high initial algae density. Under the low initial algae density, OJIP parameters such as Sm, N, Area, Pi Abs, Ψo, φEo, TRo/RC and ETo/RC were more perturbed initially and returned to the levels of the control group (without pMPs) over time, but they remained stable throughout the experiment at high initial algae density. These results show that microplastics in the marine environment may have different toxic effects on P. tricornutum at different growth stages, which is of great significance for understanding the impact of microplastics on marine microalgae and aquatic ecosystems.
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References
Andrady A L (2011). Microplastics in the marine environment. Marine Pollution Bulletin, 62(8): 1596–1605
Arnon D I (1949). Copper enzymes in isolated chloroplasts polyphenoloxidase in beta vulgaris. Plant Physiology, 24(1): 1–15
Avio C G, Gorbi S, Milan M, Benedetti M, Fattorini D, D’errico G, Pauletto M, Bargelloni L, Regoli F (2015). Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environmental Pollution, 198: 211–222
Baker N R (2008). Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annual Review of Plant Biology, 59(1): 89–113
Besseling E, Wang B, Lurling M, Koelmans A A (2014). Nanoplastic affects growth of S. obliquus and reproduction of D. magna. Environmental Science & Technology, 48(20): 12336–12343
Bilger W, Björkman O (1990). Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynthesis Research, 25(3): 173–185
Butler T, Kapoore R V, Vaidyanathan S (2020). Phaeodactylum tricornutum: A diatom cell factory. Trends in Biotechnology, 38(6): 606–622
Cai Z, Duan S, Wei W (2009). Darkness and UV radiation provoked compensatory growth in marine phytoplankton Phaeodactylum tricornutum (Bacillariophyceae). Aquaculture Research, 40(13): 1559–1562
Canniff P M, Hoang T C (2018). Microplastic ingestion by Daphnia magna and its enhancement on algal growth. Science of the Total Environment, 633: 500–507
Chen Z Y, Hong Y, Hao L C, Li L H (2020). Effects of aging microplastics on the growth and photosynthetic physiology of Phaeodactylum tricornutum bohlin. Environmental Science & Technology, 43(3): 30–37 (in Chinese)
Cunha C, Lopes J, Paulo J, Faria M, Kaufmann M, Nogueira N, Ferreira A, Cordeiro N (2020). The effect of microplastics pollution in microalgal biomass production: A biochemical study. Water Research, 186: 116370
Derraik J G B (2002). The pollution of the marine environment by plastic debris: A review. Marine Pollution Bulletin, 44(9): 842–852
Faseela P, Sinisha A K, Brestic M, Puthur J T (2020). Special issue in honour of Prof. Reto J. Strasser—Chlorophyll a fluorescence parameters as indicators of a particular abiotic stress in rice. Photosynthetica, 58(SI): 293–300
Genty B, Briantais J M, Baker N R (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta (BBA) — General Subjects, 990(1):87–92
Geyer R, Jambeck J R, Law K L (2017). Production, use, and fate of all plastics ever made. Science Advances, 3(7): e1700782
Goiris K, Van Colen W, Wilches I, León-Tamariz F, De Cooman L, Muylaert K (2015). Impact of nutrient stress on antioxidant production in three species of microalgae. Algal Research, 7: 51–57
Grobe C W, Murphy T M (1998). Solar ultraviolet-B radiation effects on growth and pigment composition of the intertidal alga Ulva expansa (Setch.) S. & G. (Chlorophyta). Journal of Experimental Marine Biology and Ecology, 225(1): 39–51
Harrison P J, Waters R E, Taylor F J R (1980). Abroad spectrum articial seawater medium for coastal and open ocean phytoplankton. Journal of Phycology, 16(1): 28–35
Hernandez O, Dukelow W R (1998). Aroclor-1254 (R) effects on the in vitro development of 8-cell mouse embryos. Bulletin of Environmental Contamination and Toxicology, 60(5): 773–780
Hong Y, Huang J J, Hu H Y (2009). Effects of a novel allelochemical ethyl 2-methyl acetoacetate (EMA) on the ultrastructure and pigment composition of cyanobacterium Microcystis aeruginosa. Bulletin of Environmental Contamination and Toxicology, 83(4): 502–508
Horton A A, Walton A, Spurgeon D J, Lahive E, Svendsen C (2017). Microplastics in freshwater and terrestrial environments: Evaluating the current understanding to identify the knowledge gaps and future research priorities. Science of the Total Environment, 586: 127–141
Jalal A, Oliveira Junior J C, Ribeiro J S, Fernandes G C, Mariano G G, Trindade V D R, Reis A R (2021). Hormesis in plants: Physiological and biochemical responses. Ecotoxicology and Environmental Safety, 207: 111225
Kaiser M J, Attrill M J, Jennings S, Thomas D N, Barnes D K A, Brierley A S, Hiddink J G, Kaartokalli H, Polunin N VC, Rafaelli D G (2011). Marine ecology: Processes, systems, and impacts. Marine Ecology, 28(2): 339
Kitajima M, Butler W L (1975). Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone. Biochimica et Biophysica Acta, 376(1): 105–115
Knuckey R M, Brown M R, Robert R, Frampton D M F (2006). Production of microalgal concentrates by flocculation and their assessment as aquaculture feeds. Aquacultural Engineering, 35(3): 300–313
Lee K W, Shim W J, Kwon O Y, Kang J H (2013). Size-dependent effects of micro polystyrene particles in the marine copepod Tigriopus japonicus. Environmental Science & Technology, 47(19): 11278–11283
Li L H, Li X Y, Hong Y, Jiang M R, Lu S L (2020). Use of microalgae for the treatment of black and odorous water: Purification effects and optimization of treatment conditions. Algal Research, 47: 101851
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. Environmental Pollution, 228: 454–463
Lusher A L, Mchugh M, Thompson R C (2013). Occurrence of microplastics in the gastrointestinal tract of pelagic and demersal fish from the English Channel. Marine Pollution Bulletin, 67(1–2): 94–99
Mao Y, Ai H, Chen Y, Zhang Z, Zeng P, Kang L, Li W, Gu W, He Q, Li H (2018). Phytoplankton response to polystyrene microplastics: Perspective from an entire growth period. Chemosphere, 208: 59–68
Nishida N, Farmer J D, Kodavanti P R S, Tilson H A, Macphail R C (1997). Effects of acute and repeated exposures to aroclor 1254 in adult rats: Motor activity and flavor aversion conditioning. Fundamental and Applied Toxicology, 40(1): 68–74
Qu Y, Zhou H L, Su W, Wu H F, Xue Q Z (2010). Oxidative stress and growth behavior responses of marine diatoms Phaeodactylum tricornutum and Skeletonema costatum to three typical persistent organic pollutants. In: Multimedia Technology (ICMT), 2010 International Conference on IEEE, pp. 1–6
Shimakawa G, Matsuda Y, Nakajima K, Tamoi M, Shigeoka S, Miyake C (2017). Diverse strategies of O2 usage for preventing photo-oxidative damage under CO2 limitation during algal photosynthesis. Scientific Reports, 7(1): 41022
Sjollema S B, Redondo-Hasselerharm P, Leslie H A, Kraak M H S, Vethaak A D (2016). Do plastic particles affect microalgal photosynthesis and growth? Aquatic Toxicology (Amsterdam, Netherlands), 170: 259–261
Song C, Liu Z, Wang C, Li S, Kitamura Y (2020). Different interaction performance between microplastics and microalgae: The bioelimination potential of Chlorella sp. L38 and Phaeodactylum tricornutum MASCC-0025. Science of the Total Environment, 723: 138146
Strasser B J, Strasser R J (1995) Measuring fast fluorescence transients to address environmental questions: The JIP test. Photosynthesis: From Light to Biosphere,4869–4872
Su L, Xue Y, Li L, Yang D, Kolandhasamy P, Li D, Shi H (2016). Microplastics in Taihu lake, China. Environmental Pollution, 216: 711–719
Sun Y, Yuan J, Zhou T, Zhao Y, Yu F, Ma J (2020). Laboratory simulation of microplastics weathering and its adsorption behaviors in an aqueous environment: A systematic review. Environmental pollution, 265(Pt B): 114864
Tang Y, Liu Y, Chen Y, Zhang W, Zhao J, He S, Yang C, Zhang T, Tang C, Zhang C, Yang Z (2021). A review: Research progress on microplastic pollutants in aquatic environments. Science of the Total Environment, 766: 142572
Thompson R C, Olsen Y, Mitchell R P, Davis A, Rowland S J, John A W G, Mcgonigle D, Russell A E (2004). Lost at sea: Where is all the plastic? Science, 304(5672): 838
Von Moos N, Burkhardt-Holm P, Köhler A (2012). Uptake and effects of microplastics on cells and tissue of the blue mussel Mytilus edulis L. after an experimental exposure. Environmental Science & Technology, 46(20): 11327–11335
Wang C, Zhao J, Xing B (2021). Environmental source, fate, and toxicity of microplastics. Journal of Hazardous Materials, 407: 124357
Wang W, Ndungu A W, Li Z, Wang J (2017). Microplastics pollution in inland freshwaters of China: A case study in urban surface waters of Wuhan, China. Science of the Total Environment, 575: 1369–1374
Waring J, Klenell M, Bechtold U, Underwood G J C, Baker N R (2010). Light-induced responses of oxygen photoreduction, reactive oxygen species production and scavenging in two diatom species. Journal of Phycology, 46(6): 1206–1217
Wituszyńska W, Szechyńska-Hebda M, Sobczak M, Rusaczonek A, Kozłowska-Makulska A, Witoń D, Karpiński S (2015). Lesion simulating disease 1 and enhanced disease susceptibility 1 differentially regulate UV-C-induced photooxidative stress signalling and programmed cell death in Arabidopsis thaliana. Plant, Cell & Environment, 38(2): 315–330
Wu Y, Guo P, Zhang X, Zhang Y, Xie S, Deng J (2019). Effect of microplastics exposure on the photosynthesis system of freshwater algae. Journal of Hazardous Materials, 374: 219–227
Xiao Y, Jiang X, Liao Y, Zhao W, Zhao P, Li M (2020). Adverse physiological and molecular level effects of polystyrene microplastics on freshwater microalgae. Chemosphere, 255: 126914
Zhang C, Chen X, Wang J, Tan L (2017). Toxic effects ofmicroplastic on marine microalgae Skeletonema costatum: Interactions between microplastic and algae. Environmental Pollution, 220(Pt B): 1282–1288
Zhang K, Gong W, Lv J, Xiong X, Wu C (2015). Accumulation of floating microplastics behind the Three Gorges Dam. Environmental Pollution, 204: 117–123
Zhang Q, Zhan J J, Hong Y (2016). The effects of temperature on the growth, lipid accumulation and nutrient removal characteristics of Chlorella sp. HQ. Desalination and Water Treatment, 57(22): 10403–10408
Zhao T, Tan L, Huang W, Wang J (2019). The interactions between micro polyvinyl chloride (mPVC) and marine dinoflagellate Karenia mikimotoi: The inhibition of growth, chlorophyll and photosynthetic efficiency. Environmental Pollution, 247: 883–889
Zhu X G, Govindjee, Baker N R, deSturler E, Ort D R, Long S P (2005). Chlorophyll a fluorescence induction kinetics in leaves predicted from a model describing each discrete step of excitation energy and electron transfer associated with photosystem II. Planta, 223(1): 114–133
Acknowledgements
This study was supported by the National Natural Science Foundation of China (No. 52071030) and Science and Technology Program of Henan Province (No.132102310498).
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Highlights
• Polystyrene microplastic caused hormesis-like effects in Phaeodactylum tricornutum.
• Low concentration of microplastic promoted growth, otherwise the opposite was true.
• The change trends of pigment contents were opposite at two initial algae densities.
• The chlorophyll fluorescence parameters were more sensitive at low algae density.
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Hormesis-like growth and photosynthetic physiology of marine diatom Phaeodactylum tricornutum Bohlin exposed to polystyrene microplastics
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Chen, Z., Li, L., Hao, L. et al. Hormesis-like growth and photosynthetic physiology of marine diatom Phaeodactylum tricornutum Bohlin exposed to polystyrene microplastics. Front. Environ. Sci. Eng. 16, 2 (2022). https://doi.org/10.1007/s11783-021-1436-0
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DOI: https://doi.org/10.1007/s11783-021-1436-0