Mercury Induced Tissue Damage, Redox Metabolism, Ion Transport, Apoptosis, and Intestinal Microbiota Change in Red Swamp Crayfish (Procambarus clarkii): Application of Multi-Omics Analysis in Risk Assessment of Hg

Lang Zhang; Yuntao Zhou; Ziwei Song; Hongwei Liang; Shan Zhong; Yali Yu; Ting Liu; Hang Sha; Li He; Jinhua Gan

doi:10.3390/antiox11101944

Mercury Induced Tissue Damage, Redox Metabolism, Ion Transport, Apoptosis, and Intestinal Microbiota Change in Red Swamp Crayfish (Procambarus clarkii): Application of Multi-Omics Analysis in Risk Assessment of Hg

Antioxidants (Basel). 2022 Sep 29;11(10):1944. doi: 10.3390/antiox11101944.

Authors

Lang Zhang¹, Yuntao Zhou¹, Ziwei Song², Hongwei Liang¹, Shan Zhong^{2

3}, Yali Yu¹, Ting Liu¹, Hang Sha¹, Li He^{1

4}, Jinhua Gan^{1

4}

Affiliations

¹ Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Wuhan 430223, China.
² Department of Genetics, Wuhan University, Wuhan 430071, China.
³ Hubei Province Key Laboratory of Allergy and Immunology, Wuhan 430071, China.
⁴ Key Laboratory of Control of Quality and Safety for Aquatic Products, Ministry of Agriculture and Rural Affairs, Beijing 100141, China.

Abstract

As one of the most toxic elements, mercury (Hg) is a widespread toxicant in aquatic environments. Crayfish are considered suitable for indicating the impact of heavy metals on aquatic crustaceans. Nevertheless, Hg toxicity on Procambarus clarkii is largely unknown. In this research, the acute Hg-induced alterations of biochemical responses, histopathology, hepatopancreatic transcriptome, and intestinal microbiome of Procambarus clarkii were studied. Firstly, Hg induced significant changes in reactive oxygen species (ROS) and malonaldehyde (MDA) content as well as antioxidant enzyme activity. Secondly, Hg exposure caused structural damage to the hepatopancreas (e.g., vacuolization of the epithelium and dilatation of the lumen) as well as to the intestines (e.g., dysregulation of lamina epithelialises and extension of lamina proprias). Thirdly, after treatment with three different concentrations of Hg, RNA-seq assays of the hepatopancreas revealed a large number of differentially expressed genes (DEGs) linked to a specific function. Among the DEGs, a lot of redox metabolism- (e.g., ACOX3, SMOX, GPX3, GLO1, and P4HA1), ion transport- (e.g., MICU3, MCTP, PYX, STEAP3, and SLC30A2), drug metabolism- (e.g., HSP70, HSP90A, CYP2L1, and CYP9E2), immune response- (e.g., SMAD4, HDAC1, and DUOX), and apoptosis-related genes (e.g., CTSL, CASP7, and BIRC2) were identified, which suggests that Hg exposure may perturb the redox equilibrium, disrupt the ion homeostasis, weaken immune response and ability, and cause apoptosis. Fourthly, bacterial 16S rRNA gene sequencing showed that Hg exposure decreased bacterial diversity and dysregulated intestinal microbiome composition. At the phylum level, there was a marked decrease in Proteobacteria and an increase in Firmicutes after exposure to high levels of Hg. With regards to genus, abundances of Bacteroides, Dysgonomonas, and Arcobacter were markedly dysregulated after Hg exposures. Our findings elucidate the mechanisms involved in Hg-mediated toxicity in aquatic crustaceans at the tissue, cellular, molecular as well as microbial levels.

Keywords: Procambarus clarkii; hepatopancreatic transcriptome; histopathology; intestinal microbiota; mercury.

Abstract

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