ABSTRACT
Microplastics are ubiquitous pollutants in the global marine environment. However, few studies have adequately explored the different toxic mechanisms of microplastics (MPs) and nanoplastics (NPs) in aquatic organisms. The sea cucumber, Apostichopus japonicus, is a key organism in the marine benthic ecosystem due to its crucial roles in biogeochemical cycles and food web. This study investigated the bioaccumulation and adverse effects of polystyrene micro- and nanoplastics (PS-M/NPs) of different sizes (20 µm, 1 µm and 80 nm) in the regenerated intestine of A. japonicus using multi-omics analysis. The results showed that after 30-day exposure at the concentration of 0.1 mg L-1, PS-MPs and PS-NPs accumulated to 155.41-175.04 µg g-1 and 337.95 µg g-1, respectively. This excessive accumulation led to increased levels of antioxidases (SOD, CAT, GPx and T-AOC) and reduced activities of immune enzymes (AKP, ACP and T-NOS), indicating oxidative damage and compromised immunity in the regenerated intestine. PS-NPs had more profound negative impacts on cell proliferation and differentiation compared to PS-MPs. Transcriptomic analysis revealed that PS-NPs primarily affected pathways related to cellular components, e.g., ribosome, and oxidative phosphorylation. In comparison, PS-MPs had greater influences on actin-related organization and organic compound metabolism. In the PS-M/NPs-treated groups, differentially expressed metabolites were mainly amino acids, fatty acids, glycerol phospholipid, and purine nucleosides. Additionally, microbial community reconstruction in the regenerated intestine was severely disrupted by the presence of PS-M/NPs. In the PS-NPs group, Burkholderiaceae abundance significantly increased while Rhodobacteraceae abundance decreased. Correlation analyses demonstrated that intestinal regeneration of A. japonicus was closely linked to its enteric microorganisms. These microbiota-host interactions were notably affected by different PS-M/NPs, with PS-NPs exposure causing the most remarkable disruption of mutual symbiosis. The multi-omic approaches used here provide novel insights into the size-dependent toxicity of PS-M/NPs and highlight their detrimental effects on invertebrates in M/NPs-polluted marine benthic ecosystems.
ABSTRACT
Micro/nano-plastics (M/NPs) are emerging contaminants in aquatic environment, however, little knowledge regarding the adverse effects of functionalized NPs has been documented so far. This study investigated the accumulation of different polystyrene nanoplastics (PS-NPs, i.e., plain PS, carboxyl-functional PS-COOH and amino-functional PS-NH2) at two particle sizes of 100 nm and 200 nm, and evaluated the impacts on oxidative stress, energy metabolism and mitochondrial pathway responses in intestine and respiratory tree of Apostichopus japonicus during the 20-d exposure experiment. The results showed that there were significant interactions of particle size and nanoplastic type on the accumulation of different PS-NPs. Exposure to NPs significantly increased the production of malondialdehyde, glutathione and reactive oxygen species, as well as the activities of antioxidant enzymes including glutathione reductase, superoxide dismutase and catalase, resulting in various degrees of oxidative damage in sea cucumber. The significant decrease in adenosine triphosphate content and increases in alkaline phosphatase and lactate dehydrogenase activities suggested that NPs impaired energy metabolism and modified their energy allocation. After 20-d exposure, the complex I, II and III activities in mitochondrial respiratory chain were significantly inhibited. Meanwhile, the Bax and Caspase-3 gene expression were significantly up-regulated, and Bacl-2 was down-regulated, indicating the toxicity on mitochondrial pathway of A. japonicus. The calculated IBR values elucidated the greater detriment to mitochondrial pathway than oxidative stress and energy metabolism. For 100 nm particle size, plain PS has stronger influence on all the biomarkers compared to PS-COOH/NH2, however, the opposite trends were observed in 200 nm PS-NPs. Furthermore, 100 nm PS-NPs were recognized to be more hazardous to sea cucumber than 200 nm microbeads. These findings provide new insights for understanding the differentiated toxic effects of functionalized NPs in marine invertebrates.
