Size-dependent effects of polystyrene plastic particles on the nematode Caenorhabditis elegans as related to soil physicochemical properties

doi:10.1016/j.envpol.2019.113740

Environmental Pollution

Volume 258, March 2020, 113740

https://doi.org/10.1016/j.envpol.2019.113740 Get rights and content

Highlights

•
We assessed the nano- and micro-plastic toxicity using nematode species in soil.
•
C. elegans showed more sensitive response in soil than in liquid.
•
The nematodes showed high sensitivity to larger particles than smaller ones.
•
The size-dependent effects were intensified in clay-rich soil samples.
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We concluded that the plastic toxicity is highly linked with soil properties.

Abstract

Plastic polymers are widely used in various applications and are thus prevalent in the environment. Over time, these polymers are slowly degraded into nano- and micro-scale particles. In this study, the free-living nematode, Caenorhabditis elegans, was exposed to polystyrene particles of two different sizes (42 and 530 nm) in both liquid and soil media. The number of offspring significantly (p < 0.05) decreased at polystyrene concentrations of 100 mg/L and 10 mg/kg in liquid and soil media, respectively. In soil media, but not liquid media, C. elegans was more sensitive to the larger particles (530 nm) than the smaller particles (42 nm), and the median effective concentration (EC₅₀) values of the 42 and 530 nm-sized particles were found to be > 100 and 14.23 (8.91–22.72) mg/kg, respectively. We performed the same toxicity bioassay on five different field-soil samples with different physicochemical properties and found that the size-dependent effects were intensified in clay-rich soil samples. A principal component analysis showed that the bulk density, cation exchange capacity, clay content, and sand content were the dominant factors influencing the toxicity of the 530 nm-sized polystyrene particles. Therefore, we conclude that the soil composition has a significant effect on the toxicity induced by these 530 nm-sized polystyrene particles.

Graphical abstract

Introduction

Owing to their versatility and durability, plastic polymers are one of the most widely used materials. They are often released into the natural aquatic and terrestrial environments, thus continuously exposing the inhabitants to their hazardous constituents (Browne, 2010; Rillig, 2012). Plastic polymer fragments slowly convert into nano- (<100 nm) and micro- (<5 mm) particles (Lambert and Wagner, 2018; PlasticsEurope, 2015). Numerous previous studies have reported that these plastic particles have adverse physical and biological effects on marine and freshwater organisms and induce complex toxic effects in combination with other pollutants (Antunes et al., 2013; Guzzetti et al., 2018; Prokić et al., 2019; Rist and Hartmann, 2018; Wright et al., 2013).

Numerous problems associated with plastic particles in soil and terrestrial ecosystems have been highlighted previously (Rillig, 2012) and have started to be addressed recently (Chae and An, 2018). The plastic particles originate from various plastic sources, including domestic sewage (Talvitie et al., 2017; Ziajahromi et al., 2017), fertilizers (Horton et al., 2017; Nizzetto et al., 2016), and vinyl mulch used in agriculture (Farmer et al., 2017; Sintim and Flury, 2017). Monitoring of microplastic particles has shown that they can be found at a concentration of 300–67,500 mg/kg in industrial soils (Fuller and Gautam, 2016) and at 55.5 mg/kg in floodplains at a depth of 0–5 cm (Scheurer and Bigalke, 2018). They can be transported to deeper soil layers and might as well be ingested by soil organisms such as earthworms and insects.

Previous studies have simulated the exposure of collembolans (Maaβ et al., 2017; Zhu et al., 2018a,b), various earthworm species (Gaylor et al., 2013; Hodson et al., 2017; Huerta Lwanga et al., 2016, 2017; Rodriguez-Seijo et al., 2017), isopods (Kokalj et al., 2018), mites (Zhu et al., 2018a), and nematodes to plastic particles (Lei et al., 2018; Zhao et al., 2017). It has been reported that earthworms can ingest microplastic particles and transport them through their burrowing and excretion activities (Huerta Lwanga et al., 2016; Rillig, 2012). Furthermore, several studies have reported that microplastic particles can induce sub-lethal effects on earthworm species at the individual and immune levels (Hodson et al., 2017; Huerta Lwanga et al., 2016, 2017; Rodriguez-Seijo et al., 2017). Although numerous reliable studies have supported the assertion that nano- and micro-plastic exposures can induce adverse biological effects, these studies do not represent real soil environmental conditions because several of them were conducted in non-soil media such as liquids or mixtures of plaster and activated charcoal (Kokalj et al., 2018; Lei et al., 2018; Maaβ et al., 2017; Zhao et al., 2017; Zhu et al., 2018a). In general, these studies have reported that nanoplastics can cause a decrease in the growth and reproduction of various nematode species (Lei et al., 2018; Zhao et al., 2017). For example, Zhu et al. (2018c) found that an exposure to nano-sized polystyrene changes intestinal microbial diversity in soil oligochaetes. Although these studies improve our understanding of the toxicity mechanisms of plastic particles, the exposure media used, including the essential nutrients for each species, were liquid.

It is well known that the adverse effects of general toxicants (metals and organic pollutants) are strongly linked to soil properties. For example, soil organic carbon and matter can alter toxicant bioavailability in soil receptors, including plants, soil invertebrates, and microbes (Marschner and Kalbitz, 2003; Pinto et al., 2004). In addition, the partitioning between solid and solution phases depends on specific soil factors, such as pH and presence of clay minerals (Lamb et al., 2009; Sauvé et al., 2000). In microplastic research, however, the interactions between plastic toxicity and soil properties have not been fully addressed. In the present study, we conducted bioassays in both liquid and soil media to evaluate the media-dependent effects of nano- and micro-plastic particles, using a variety of field soils. Based on our previous finding, the free-living nematode, Caenorhabditis elegans, was chosen as the test species, and the number of offspring was selected as the primary indicator of the effects of these particles (Kim et al., 2014, 2018). The plastic particles of two different sizes and five soil samples were used to assess whether the effects of these particles were dependent on particle size and soil physicochemical properties.

Section snippets

Materials and target organism

Polystyrene (PS) beads of two different sizes, 42 nm (42 PS; product number FS02F-12719) and 530 nm (530 PS; product number FS03F-9360), were obtained as dispersions from Bangs Laboratories, Inc. (Fishers, IN, USA). These beads exhibited strong fluorescent properties with <480 nm excitation and >520 nm emission wavelengths. To confirm the PS particle type, a Fourier transform infrared (FTIR, 4100typeA, JASCO, Japan) spectral analysis was carried out using dried samples at a wavenumber range of

Size-dependent toxicity of PS in different test media

As shown in Fig. 1A, 100 mg/L of the 42 PS and 530 PS particles in liquid media caused a significant decrease in offspring number (p < 0.05). There was no evidence of a size-dependent effect since both 42 PS and 530 PS particles produced similar effects. In the soil media test, the number of offspring started to decrease significantly (p < 0.05) at 10 mg/kg of the 530 PS particles; however, for the 42 PS particles, significant decreases (p < 0.05) were observed only at 100 mg/kg (Fig. 1B). The

Discussion

Previous studies have reported the toxicity of plastic particles towards C. elegans using liquid media tests. Lei et al. (2018) have reported that an exposure (2 days) to 5.0 mg/m² of microplastics can significantly impact the survival, growth, and reproduction of C. elegans. Zhao et al. (2017) found that a chronic exposure (4.5 days) to nano-polystyrene induces alterations in the behavior, survival, and reproduction of C. elegans at concentrations higher than 10 μg/L, and these effects could

CRediT authorship contribution statement

Shin Woong Kim: Conceptualization, Methodology, Writing - original draft. Dasom Kim: Investigation, Writing - original draft. Seung-Woo Jeong: Writing - review & editing. Youn-Joo An: Supervision, Writing - review & editing, Funding acquisition.

Declaration of competing interest

The authors declare no conflicts of interest.

Acknowledgement

This paper was supported by Konkuk University in 2019. We thank the Korean Basic Science Institute (KBSI) for their assistance with our dynamic light scattering and TEM analyses.

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^☆: This paper has been recommended for acceptance by Eddy Y. Zeng.

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Size-dependent effects of polystyrene plastic particles on the nematode Caenorhabditis elegans as related to soil physicochemical properties☆

Highlights

Abstract

Graphical abstract

Introduction

Section snippets

Materials and target organism

Size-dependent toxicity of PS in different test media

Discussion

CRediT authorship contribution statement

Declaration of competing interest

Acknowledgement

Agric. Ecosyst. Environ.

Estuar. Coast Shelf Sci.

Environ. Pollut.

Ecotoxicol. Environ. Saf.

Soil Tillage Res.

Environ. Toxicol. Pharmacol.

Sci. Total Environ.

Environ. Pollut.

Environ. Pollut.

Ecotoxicol. Environ. Saf.

Environ. Pol.

J. Hazard Mater.

Sci. Total Environ.

Geoderma

Environ. Pollut.

Sci. Total Environ.

Sci. Total Environ.

Environ. Pollut.

Environ. Toxicol. Pharmacol.

Water Res.

Environ. Pollut.

Environ. Pollut.

Pedobiologia

Environ. Pollut.

Soil Biol. Biochem.

Environ. Pollut.

Water Res.

Environ. Pollut.

Standard Guide for Conducting Laboratory Soil Toxicity Tests with the Nematode Caenorhabditis elegans. E2172-01

The genetics of Caenorhabditis elegans

Genetics

Spatial patterns of plastic debris along estuarine shorelines

Environ. Sci. Technol.

Using the Caenorhabditis elegans soil toxicity test to identify factors affecting toxicity of four metal ions in intact soil

Water Air Soil Pollut.

Habitable pore space and microbial trophic interactions

Oikos