Multigenerational effects of polyethylene terephthalate microfibers in Caenorhabditis elegans
Introduction
Ubiquitous microfiber (MF) pollution in the environment has long been discussed. Based on the GESAMP (Joint Group of Experts on the Scientific Aspects of Marine Environmental Protection) report involved in UNEP (United Nations Environment Program), MFs are defined as tiny threads which are long (<5 mm) and narrow (<10 μm) (GESAMP, 2019). As emerging anthropogenic contaminants, MFs produced with 60% synthetic MF are dominant in ecosystems and present a greater threat than other microplastic morphotypes (Mishra et al., 2019). The main MF sources are the textile industry and domestic laundering (Hernandez et al., 2017), which may reveal that development of light industries has caused considerable environmental damage.
There is a rapidly increasing volume of research into microplastics that shows that MFs have adverse impacts on ingestive behavior, food consumption, and the energy balance of aquatic organisms (Watts et al., 2015; Welden and Cowie, 2016). Recently, the transfer of small-sized MFs between trophic levels in freshwater and marine food chains has gained attention in environmental toxicology. Some previous studies have revealed that, due to their nonbiodegradability, synthetic MFs are consumed by small fish, are transferred through the food chain, and, as a result, can severely impact larger aquatic animals (Mishra et al., 2019). In real environments, the size of MFs remains in the range of 1–5000 μm (Li et al., 2018; Zhang et al., 2019).
The number of publications on the effects of MFs on aquatic organisms is rapidly increasing, and many studies have warned of the potential ecotoxicity of MFs, with effects such as increased mortality, decreased growth, and reduced body mass (Au et al., 2015; Jemec et al., 2016; Welden and Cowie, 2016; Ziajahromi et al., 2017). Apart from affecting aquatic ecology, MFs can alter the soil physical properties and damage the sustainability of terrestrial ecosystem, which may be reflected in decreased energy reserves (Selonen et al., 2020), food intake disorders, and gastrointestinal tissue damage in some soil organisms (Song et al., 2019). However, although previous studies have shown that MFs have negligible reproductive toxicity on some organisms (Kokalj et al., 2018; Selonen et al., 2020), there appears to be insufficient evidence to verify the multigenerational toxic effects.
In the present study, Caenorhabditis elegans was selected as a model organism to study the underlying multigenerational toxicity of MFs, and polyethylene terephthalate (PET) MFs were chosen as a test material. We measured the survival rate, reproduction rate, body length, locomotion behavior, reactive oxygen species (ROS) production, and used scanning electron microscopy (SEM) to assess test organisms after exposure to MF and MF-free test solutions. ROS production, a classical endpoint, is employed to detect the intracellular oxidative damage and mitochondrial dysfunction (Georgieva et al., 2020; Zhao et al., 2020b; Kim and Park, 2020), effectively reflecting the cytotoxicity of microfibers in C. elegans. As body length indicates growth and development (Qiao et al., 2014; Qiang et al., 2020), we measured this characteristic to investigate the developmental impacts of microfibers. Locomotion behavior is the most sensitive indicator in evaluating the toxicity of environmental pollution (Zhang et al., 2020), indicating the functional state of motor neurons (Cheng et al., 2020). Head thrash and body bend were used to assess the possible neurotoxicity on locomotion behavior (Zhao et al., 2020a). In C. elegans, the epidermal barrier is an extremely flexible and resilient exoskeleton that performs the function of protection against environmental toxicants (Page and Johnstone, 2007). Therefore, in this study, we detected the dermal damage to reveal the epidermal barrier damage by SEM analysis. Finally, we hypothesized that (a) continuous MF exposure can induce adverse effects in each generation of C. elegans and (b) C. elegans may gain an impermanent memory of MF toxicity after continuous MF exposure. This is the first study evaluating the multigenerational toxicity of microfibers in C. elegans.
Section snippets
MF characterization
PET MFs (diameter 17.4 μm) were obtained from the Korea Institute of Industrial Technology (KITECH), and their composition was confirmed by analyzing a Fourier transform infrared (FTIR, 4100typeA, JASCO, Japan) spectrum (Figure S1, Supporting Information). MFs of different dimensions were manually cut under a stereomicroscope, and morphological identification of the test MF was conducted using a high-resolution field emission scanning electron microscope (FE-SEM, SU8010, Hitachi
Comparison of parental toxicity under multidimensional PET MF exposure
Among the groups exposed to PET MFs of all sizes, only 250-μm PET MFs caused decreases in locomotion behavior and significant inductions of intestinal ROS production in P0 generation compared with the control group (Fig. 2). Similar to previous studies of nanotoxicity in C. elegans (Jeong et al., 2016; Kim et al., 2019; Ma et al., 2019), maternal toxicity appeared in response to PET MF exposure in a size-dependent manner, which might correspond to the phenomenon that C. elegans were more
Implications and outlooks
Continuous exposures of P0–F5 generations to MFs, and of F6–F7 generations to MF-free conditions were conducted to confirm our hypothesis, with the following conclusions: (a) continuous 250-μm PET MF exposure can induce multigenerational effects in C. elegans and (b) C. elegans might gain an impermanent memory to MF toxicity after continuous MF exposure. The results of toxicity tests on the P0 generation under multidimensional PET MF exposure implied that the PET MFs caused size-dependent
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
This research was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT and future planning (2020R1A2B5B02001734).
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