Micro/nano-plastics cause neurobehavioral toxicity in discus fish (Symphysodon aequifasciatus): Insight from brain-gut-microbiota axis

Jun-Nan Huang; Bin Wen; Lei Xu; Huan-Chao Ma; Xin-Xin Li; Jian-Zhong Gao; Zai-Zhong Chen

doi:10.1016/j.jhazmat.2021.126830

Micro/nano-plastics cause neurobehavioral toxicity in discus fish (Symphysodon aequifasciatus): Insight from brain-gut-microbiota axis

J Hazard Mater. 2022 Jan 5:421:126830. doi: 10.1016/j.jhazmat.2021.126830. Epub 2021 Aug 5.

Authors

Jun-Nan Huang¹, Bin Wen², Lei Xu¹, Huan-Chao Ma³, Xin-Xin Li³, Jian-Zhong Gao¹, Zai-Zhong Chen⁴

Affiliations

¹ National Demonstration Centre for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai 201306, China; Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture and Rural Affairs, Shanghai Ocean University, Shanghai 201306, China; Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai 201306, China; Shanghai Engineering Research Centre of Aquaculture, Shanghai Ocean University, Shanghai 201306, China.
² National Demonstration Centre for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai 201306, China; Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture and Rural Affairs, Shanghai Ocean University, Shanghai 201306, China; Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai 201306, China; Shanghai Engineering Research Centre of Aquaculture, Shanghai Ocean University, Shanghai 201306, China. Electronic address: bwen@shou.edu.cn.
³ National Demonstration Centre for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai 201306, China.
⁴ National Demonstration Centre for Experimental Fisheries Science Education, Shanghai Ocean University, Shanghai 201306, China; Key Laboratory of Freshwater Aquatic Genetic Resources, Ministry of Agriculture and Rural Affairs, Shanghai Ocean University, Shanghai 201306, China; Shanghai Collaborative Innovation for Aquatic Animal Genetics and Breeding, Shanghai Ocean University, Shanghai 201306, China; Shanghai Engineering Research Centre of Aquaculture, Shanghai Ocean University, Shanghai 201306, China. Electronic address: chenzz@shou.edu.cn.

PMID: 34396975
DOI: 10.1016/j.jhazmat.2021.126830

Abstract

Numerous studies have investigated neurobehavioral toxicity of microplastics, but no studies have illustrated mechanism via brain-gut axis. Here, juvenile discus fish (Symphysodon aequifasciatus) were exposed for 96 h to microfibers (900 µm, fiber, MFs) or nanoplastics (~88 nm, bead, NPs) with three concentrations (0, 20 and 200 µg/L). Accumulation in fish gut was independent of plastics type and concentration. MFs reduced growth performance while NPs weakened swimming and predatory performance of post-exposed discus. For brain cholinesterase activity, acetylcholinesterase was activated by NPs while NPs/MFs exposure inhibited butyrylcholinesterase. Concentrations of neurotransmitters (acetylcholine, dopamine and γ-aminobutyric acid) increased in brain but decreased in gut after NPs or MFs exposure. For gut microbiota, increased richness under MFs exposure was observed. At phylum level, Proteobacteria proportion was lower in NPs but higher in MFs. Abundance of Clostridia and Fusobacteriia (Bacillus), potentially secreting neurotransmitters, increased in NPs but decreased in MFs. Brain transcriptomics revealed seven upregulated and four downregulated genes concerning neural-activities. Pathways of neuroactive ligand-receptor interaction and serotonergic synapse were enriched in both MFs and NPs, but dopaminergic synapse pathway was enriched only in MFs. These results established a novel mechanism by which microplastics might cause behavioral toxicities via brain-gut-microbiota axis.

Keywords: Gut microbiota; Microplastic; Neurotransmitter; Predatory performance.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Acetylcholinesterase
Animals
Brain
Butyrylcholinesterase
Gastrointestinal Microbiome*
Microplastics
Plastics*

Substances

Microplastics
Plastics
Acetylcholinesterase
Butyrylcholinesterase