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Cadmium-induced ultrastructural changes and apoptosis in the gill of freshwater mussel Anodonta woodiana

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Abstract

This study investigated the acute toxicity of cadmium (Cd) to the freshwater mussel Anodonta woodiana. The freshwater mussels were exposed to five concentrations of Cd (0 mg/L, 8.43 mg/L, 16.86 mg/L, 33.72 mg/L, and 67.45 mg/L) for up to 96 h. The 24-h, 48-h, 72-h, and 96-h LC50 values for Cd were estimated as 562.3 mg/L, 331.1 mg/L, 182.0 mg/L, and 134.9 mg/L, respectively. Caspase-3, caspase-8, caspase-9, and Ca-ATPase activities; protein and H2O2 levels; DNA fragmentation; and ultrastructure of the gill were also investigated. The activities of caspase-3 and caspase-9 in mussels were increased by Cd in a dose-dependent manner, where higher doses of Cd (33.72 mg/L and 67.45 mg/L) significantly increased the enzyme activities compared to the controls (P < 0.05). The caspase-8 activity was significantly depressed by a low dose of Cd (8.43 mg/L) but was clearly induced by higher doses of Cd (16.86 mg/L, 33.72 mg/L, and 67.45 mg/L) (P < 0.05). The Ca-ATPase activity and H2O2 levels were elevated and reached maximum values under the medium dose of Cd (16.86 mg/L). However, protein levels were decreased by Cd in an inverse dose–dependent manner. In the gills of the mussels, Cd treatment induced DNA fragmentation as demonstrated by DNA ladders observed via agarose gel electrophoresis. Moreover, ultrastructural alterations in gill cells of mussels treated with Cd (16.86 mg/L and 67.45 mg/L) for 96 h were observed by electronic microscopy. The ultrastructure abnormalities were characterized by the following features: (1) a disordered arrangement and breaking off of microvilli of epithelial cells; (2) chromatin condensed near the nuclear membrane and the appearances of extremely irregular nuclei, some with a fingerlike shape and an unclear, swollen, invaginated, or ruptured nuclear membrane and apoptotic bodies; (3) swollen and vacuolating mitochondria, some with disintegrated or missing cristae; (4) a disintegrated rough endoplasmic reticulum containing different sizes of vesicles; and (5) shrinking and deformation of Golgi bodies with decreased vesicle numbers. Our results demonstrated that Cd could activate caspase-3, caspase-8, caspase-9, and Ca-ATPase; cause ultrastructural changes; and produce DNA fragmentation in the mussels investigated. Based on the information obtained through this study, it is reasonable to conclude that Cd can induce apoptosis in the gills of the mussels, eventually leading to tissue damage.

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The data and materials used or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We want to allocate thanks to Chien M. Chen for the guidance in our research.

Funding

This study was sponsored by the National Natural Science Foundation of China (No. 31672293), the Key Research and Development (R&D) Projects of Shanxi Province (201803D221019-4; 201803D31026), and Applied Basic Research Project of Shanxi Province (201801D121194).

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Authors and Affiliations

  1. School of Life Science, Shanxi University, Taiyuan, 030006, Shanxi Province, China

    Yong Quan Li, Na Liu & Lan Wang

  2. Department of Environmental Resources Management, Chia Nan University of Pharmacy & Science, Tainan, Taiwan

    Chien M. Chen

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Yong Quan Li is a major operator for the study design, experimental work, and writing the manuscript. Na Liu is a contributor for the data analysis. Chien Ming Chen and Lan Wang mainly contribute to the revision of the final manuscript. The authors declare they all made contribution for the study design, experimental works, data analysis, and writing of the article.

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Correspondence to Lan Wang.

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Highlights

• The acute toxic effects of Cd on Anodonta woodiana are time-dependent, and this mussel species has higher tolerance to Cd stress than other aquatic species.

• H2O2 is not the main ROS responsible for inducing caspase activation or apoptosis in the gill of Anodonta woodiana.

• After Cd exposure, DNA fragmentation in the gill cells of Anodonta woodiana was induced and was proportional to the Cd concentration.

• The most typical apoptotic characteristics in the gill cells of Anodonta woodiana were the morphological changes of nuclei and mitochondria.

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Li, Y.Q., Chen, C.M., Liu, N. et al. Cadmium-induced ultrastructural changes and apoptosis in the gill of freshwater mussel Anodonta woodiana. Environ Sci Pollut Res 29, 23338–23351 (2022). https://doi.org/10.1007/s11356-021-16877-w

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