Algae (Raphidocelis subcapitata) mitigate combined toxicity of microplastic and lead on Ceriodaphnia dubia

Highlights

• Micro-plastics (MPs) significantly increase Pb toxicity.

• Algae reduce the combined toxicity of MP and Pb.

• The toxicity increase comes from high soluble Pb and MP-Pb uptake.

• The toxicity reduction might come from energy related pathway.

Abstract

Microplastics (MPs) have been recognized as a new class of emerging contaminants in recent years. They not only directly impact aquatic organisms, but also indirectly impact these organisms by interacting with background toxins in the environment. Moreover, under realistic environmental conditions, algae, a natural food for aquatic organisms, may alter the toxicity pattern related to MPs. In this research, we first examined the toxicity of MPs alone, and their effect on the toxicity of lead (Pb) on Ceriodaphnia dubia (C. dubia), a model aquatic organism for toxicity survey. Then, we investigated the effect of algae on the combined toxicity of MPs and Pb. We observed that, MPs significantly increased Pb toxicity, which was related to the increase in soluble Pb concentration and the intake of Pb-loaded MPs, both of which increased the accumulation of Pb in C. dubia. The presence of algae mitigated the combined toxicity of MPs and Pb, although algae alone increased Pb accumulation. Therefore, the toxicity mitigation through algae uptake came from mechanisms other than Pb accumulation, which will need further investigation.

Graphical abstract

Keywords

Microplastic / Lead / Toxicity / Algae / C. dubia

References

[1] Ab Latif Wani, Ara A, Usmani J A (2015). Lead toxicity: A review. Interdisciplinary Toxicology, 8(2): 55–64

[2] Braakhuis H M, Cassee F R, Fokkens P H, de La Fonteyne L J, Oomen A G, Krystek P, De Jong W H, Van Loveren H, Park M V (2016). Identification of the appropriate dose metric for pulmonary inflammation of silver nanoparticles in an inhalation toxicity study. Nanotoxicology, 10(1): 63–73

[3] Bray T M, Bettger W J (1990). The physiological role of zinc as an antioxidant. Free Radical Biology & Medicine, 8(3): 281–291

[4] Chen Q, Gundlach M, Yang S, Jiang J, Velki M, Yin D, Hollert H (2017). Quantitative investigation of the mechanisms of microplastics and nanoplastics toward zebrafish larvae locomotor activity. Science of the Total Environment, 584–585: 1022–1031

[5] Ebert D P (2005). Ecology, epidemiology, and evolution of parasitism in Daphnia. Bethesda, MD: National Library of Medicine (US), National Center for Biotechnology Information, [2005] ©2005

[6] Elmore S (2007). Apoptosis: A review of programmed cell death. Toxicologic Pathology, 35(4): 495–516

[7] EPA (2002). Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. Washington DC: U.S. Environmental Protection Agency

[8] Ercal N, Gurer-Orhan H, Aykin-Burns N (2001). Toxic metals and oxidative stress part I: Mechanisms involved in metal-induced oxidative damage. Current Topics in Medicinal Chemistry, 1(6): 529–539

[9] Erten-Unal M, Wixson B G, Gale N, Pitt J L (1998). Evaluation of toxicity, bioavailability and speciation of lead, zinc and cadmium in mine/mill wastewaters. Chemical Speciation and Bioavailability, 10(2): 37–46

[10] Escudero-García R, Espinoza-Estrada E, Tavera F (2013). Precipitation of lead species in a Pb–H₂O system. Research Journal of Recent Sciences, 9(4): 1–8

[11] Europe P (2018). Plastics-the facts 2018: An analysis of European latest plastics production, demand and waste data. Plastic Europe: 1–60

[12] Geller W, Müller H (1981). The filtration apparatus of Cladocera: Filter mesh-sizes and their implications on food selectivity. Oecologia, 49(3): 316–321

[13] Gillis P, Chow-Fraser P, Ranville J, Ross P, Wood C (2005).Daphnia need to be gut-cleared too: The effect of exposure to and ingestion of metal-contaminated sediment on the gut-clearance patterns of D. magna. Aquatic Toxicology (Amsterdam, Netherlands), 71(2): 143–154

[14] Haegerbaeumer A, Mueller M T, Fueser H, Traunspurger W (2019). Impacts of micro-and nano-sized plastic particles on benthic invertebrates: A literature review and gap analysis. Frontiers in Environmental Science, 7: e17

[15] Hu J, Wang D, Wang J, Wang J (2012). Toxicity of lead on Ceriodaphnia dubia in the presence of nano-CeO₂ and nano-TiO₂. Chemosphere, 89(5): 536–541

[16] Jaikumar G, Baas J, Brun N R, Vijver M G, Bosker T (2018). Acute sensitivity of three Cladoceran species to different types of microplastics in combination with thermal stress. Environmental Pollution, 239: 733–740

[17] Jaikumar G, Brun N R, Vijver M G, Bosker T (2019). Reproductive toxicity of primary and secondary microplastics to three Cladocerans during chronic exposure. Environmental Pollution, 249: 638–646

[18] Johansen M P, Prentice E, Cresswell T, Howell N (2018). Initial data on adsorption of Cs and Sr to the surfaces of microplastics with biofilm. Journal of Environmental Radioactivity, 190–191: 130–133

[19] Kazmiruk T, Kazmiruk V, Bendell L (2018). Abundance and distribution of microplastics within surface sediments of a key shellfish growing region of Canada. PLoS One, 13(5): e0196005

[20] Kim D, Chae Y, An Y J (2017). Mixture toxicity of nickel and microplastics with different functional groups on Daphnia magna. Environmental Science & Technology, 51(21): 12852–12858

[21] Korshin G V, Ferguson J F, Lancaster A N (2005). Influence of natural organic matter on the morphology of corroding lead surfaces and behavior of lead-containing particles. Water Research, 39(5): 811–818

[22] Lambert S, Sinclair C J, Bradley E L, Boxall A B A (2013). Effects of environmental conditions on latex degradation in aquatic systems. Science of the Total Environment, 447: 225–234

[23] Lee W S, Cho H J, Kim E, Huh Y H, Kim H J, Kim B, Kang T, Lee J S, Jeong J (2019). Bioaccumulation of polystyrene nanoplastics and their effect on the toxicity of Au ions in zebrafish embryos. Nanoscale, 11(7): 3173–3185

[24] Liu X, Wang J, Huang Y W, Kong T (2019). Algae (Raphidocelis) reduce combined toxicity of nano-TiO₂ and lead on C. dubia. Science of the Total Environment, 686: 246–253

[25] Luo Z, Wang Z, Yan Y, Li J, Yan C, Xing B (2018). Titanium dioxide nanoparticles enhance inorganic arsenic bioavailability and methylation in two freshwater algae species. Environmental Pollution, 238: 631–637

[26] Moltedo O, Verde C, Capasso A, Parisi E, Remondelli P, Bonatti S, Alvarez-Hernandez X, Glass J, Alvino C G, Leone A (2000). Zinc transport and metallothionein secretion in the intestinal human cell line Caco-2. Journal of Biological Chemistry, 275(41): 31819–31825

[27] NIST (2012). NIST X-ray Photoelectron Spectroscopy Database, Version 4.1. Gaithersburg: National Institute of Standards and Technology

[28] Poljsak B, Šuput D, Milisav I (2013). Achieving the balance between ROS and antioxidants: When to use the synthetic antioxidants. Oxidative Medicine and Cellular Longevity, 2013: e956792

[29] Porter K G (1977). The plant-animal interface in freshwater ecosystems: Microscopic grazers feed differentially on planktonic algae and can influence their community structure and succession in ways that are analogous to the effects of herbivores on terrestrial plant communities. American Scientist, 65(2): 159–170

[30] Romay C, Armesto J, Remirez D, Gonzalez R, Ledon N, Garcia I (1998). Antioxidant and anti-inflammatory properties of C-phycocyanin from blue-green algae. Inflammation Research, 47(1): 36–41

[31] Town R M, Van Leeuwen H P, Blust R (2018). Biochemodynamic features of metal ions bound by micro-and nanoplastics in aquatic media. Frontiers in Chemistry, 6: e627

[32] Turner A, Holmes L A (2015). Adsorption of trace metals by microplastic pellets in fresh water. Environmental Chemistry, 12(5): 600–610

[33] Wang J, Li Y, Lu L, Zheng M, Zhang X, Tian H, Wang W, Ru S (2019). Polystyrene microplastics cause tissue damages, sex-specific reproductive disruption and transgenerational effects in marine medaka (Oryzias melastigma). Environmental Pollution, 254: 113024

[34] Yu F, Yang C, Zhu Z, Bai X, Ma J (2019). Adsorption behavior of organic pollutants and metals on micro/nanoplastics in the aquatic environment. Science of the Total Environment, 694: 133643

[35] Zhang C, Chen X, Wang J, Tan L (2017). Toxic effects of microplastic on marine microalgae Skeletonema costatum: Interactions between microplastic and algae. Environmental Pollution, 220: 1282–1288

[36] Zhang R, Zhang D, Mao H, Song W, Gao G, Liu F (2006). Preparation and characterization of Ag/AgO nanoshells on carboxylated polystyrene latex particles. Journal of Materials Research, 21(2): 349–354

[37] Ziajahromi S, Kumar A, Neale P A, Leusch F D (2017). Impact of microplastic beads and fibers on waterflea (Ceriodaphnia dubia) survival, growth, and reproduction: Implications of single and mixture exposures. Environmental Science & Technology, 51(22), 13397–13406

Acknowledgements

Authors appreciate the facility support from the Center for Research in Energy and Environment (CREE) at Missouri S&T, and the help from Xiaolong He and Shuo Yang from the Chemistry Department at Missouri S&T, for TOC analysis and SEM image.

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-020-1276-3 and is accessible for authorized users.

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