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

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.

The Accumulation of Toxic Elements (Pb, Hg, Cd, As, and Cu) in Red Swamp Crayfish (Procambarus clarkii) in Qianjiang and the Associated Risks to Human Health

“…Methylmercury binding through cysteine can reduce the bioaccessibility of methylmercury in muscle tissue [ 67 ]. The hepatopancreas generates oxidative stress under chronic exposure to Hg, affecting the synthesis of non-enzymatic antioxidants, such as tocopherols, ascorbic acid, and glutathione (GSH) [ 68 ]. Methylmercury can inhibit the rate-limiting enzyme of GSH synthesis, γ-glutamyl-cysteine synthetase [ 69 ].…”

Probiotics, Prebiotics, and Synbiotics Utilization in Crayfish Aquaculture and Factors Affecting Gut Microbiota

“…A possible solution to Cd increased concentration could be the inoculation of probiotic B. subtilis, which was found to mineralize Cd and attenuate Cd accumulation in crayfish [ 105 ]. Except for Cd polystyrene and polyethylene nanoplastic, nitrite, and sulfide, mercury and Hepatotoxin microcystion-LR exposure seem to also have an adverse effect on intestinal microbiota [ 66 , 100 , 101 , 106 , 107 ]. The relative abundance of lactic acid bacteria, Citrobacter , and other probiotics decreased, while the relative abundance of some intestinal pathogens and some other genera such as Shewanella and Acinetobacter increased [ 66 , 106 ].…”

“…Analyzed data obtained from Refs. [ 97 , 98 , 99 , 100 , 101 , 102 , 103 ]. P. clarkii photo, retrieved from [ 104 ].…”

Redox Metabolism in Ecophysiology and Evolution

“…Zhang et al [ 9 ] focused on the effects of mercury (as HgCl 2 ) toxicity on Procambarus clarkii , a type of crayfish commonly found in aquatic environments worldwide. The study examined the acute impact of Hg on various aspects, including biochemical responses, histopathology, hepatopancreatic transcriptome, and intestinal microbiome.…”