Gill Junction Injury and Microbial Disorders Induced by Microcystin-Leucine Arginine in Lithobates catesbeianus Tadpoles

Abstract

Microcystin-LR (MC-LR) is widely present in waters around the world, but its potential toxic effects and mechanisms on amphibian gills remain unknown. In the present study, tadpoles (Lithobates catesbeianus) were exposed to environmentally realistic concentrations of 0.5, 2 μg/L MC-LR, and 0 μg/L MC-LR (Control) for 30 days with the objective to unveil the impairment of gill health. The lysozyme was downregulated, while pattern recognition receptors and complement and adaptive immune processes were upregulated and the ability of gill supernatant to inhibit pathogenic bacteria decreased in the 0.5 and 2 μg/L MC-LR groups. The transcriptions of epithelial barrier components (e.g., CLDN1) were significantly decreased in MC-LR-exposed gills, while the gill content of lipopolysaccharide (LPS) endotoxins and the transcriptions of downstream responsive genes (e.g., TLR4 and NF-κB) were concurrently increased. In addition, the number of eosinophils and the expression of pro-inflammatory cytokines (e.g., IL-1β and TNF-α) were increased. These results imply that exposure of tadpoles to low environmentally concentrations of MC-LR leads to inflammation, increased permeability, and a reduced ability to inhibit pathogenic bacteria. The epithelial cells of inner gill filaments increased and transcriptions of hypoxic stress genes (e.g., HIF-1α, FLT1, and SERPINE1) were upregulated within the exposed group. As a consequence, exposure to MC-LR may lead to hypoxic stress. MC-LR exposure also drove gill microbiota to a dysbiosis. The relative abundance of Elizabethkingia was positively correlated with content of LPS and transcriptions of NF-κB and TNF-α. Overall, this study presents the first evidence about the pronounced impacts of MC-LR exposure on gills of amphibians, highlighting the susceptibility of early developing tadpoles to the environmental risks of MC-LR.

Conventional Anthelmintic Concentration of Deltamethrin Immersion Disorder in the Gill Immune Responses of Crucian Carp

“…The epithelial cells of the gill serve as the first defense mechanism for fish against various environmental stresses, and its structural integrity is essential for preventing the infiltration of toxic substances and potential pathogens [ 1 , 30 , 36 ]. In the current study, microscopic observations of typical gill lesions are severe hyperplasia in the secondary lamella and apoptotic epithelial cells after DEL immersion, which were substantiated via HE and TUNEL assays.…”

“…Like this, exposure to herbicides and microplastics has been found to induce the secretion of mucus in an irregular manner, serving as a defensive mechanism to safeguard the epithelial mucosal surfaces [ 48 , 49 ]. Additionally, gill epithelial barriers rely on the cellular structures called tight junctions to enhance paracellular permeability, which selectively permits the passage of ions and soluble small molecules [ 36 ]. After DEL immersion, the transcription levels of tight junction genes including occludin , claudin12 , zo-1 were downregulated even though not significantly.…”

“…Notably, recent years have witnessed novel revelations regarding the microbiota of fish mucosal surfaces [ 19 , 33 , 34 ]. Furthermore, the gill microbiome plays a role in mitigating host stress in response to external environmental factors, in conjunction with the gills [ 33 , 35 , 36 ]. Lai et al demonstrated that the gill microbiota of marine medaka could respond to osmotic stress, and the dominant microbiota including Vibrio , Pseudomonas , and Cetobacterium were found to change the glycosaminoglycan and chitin metabolisms [ 35 ].…”

Effects of Dietary Changes on the Gut Microbiota of <italic>Cynops orientalis</italic>

“…Studying various factors that affect the host gut microbial assembly and structure, elucidating the dynamic shifts in diversity and composition of microbes, and analyzing the host′s gut microbial adaptive mechanisms in reaction to various external disturbances are important for protecting amphibians. In the past 30 years, research on the association between amphibians and their gut microbial composition has mainly focused on the order Anura, such as Xenopus tropicalis, Rana dybowskii, Bufo gargarizans, Pelophylax nigromaculatus, and Fejervarya limnocharis (Chai et al, 2022;Huang et al, 2021;Huang et al, 2022;Li et al, 2020;Tong et al, 2020a;Xu et al, 2020;Zhang et al, 2023;Zhao et al, 2022;Zheng et al, 2021;Zhu et al, 2023), while only a few studies have focused on the order Caudata (Jiang et al, 2022;Li et al, 2022;Lv et al, 2022;Mu et al, 2018). Although knowledge about environmental factors driving shifts in the gut microbiota of amphibians is constantly being supplemented, the understanding of the external environment on the composition, source, and dynamic shifts of the gut microbiota of Caudata is still limited.…”