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

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...

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Detalles Bibliográficos
Autores principales: Jiang, Huiling, He, Jun, Wang, Hui, Zheng, Lingling, Wang, Xiaoran, Zhang, Huijuan, Wu, Hailong, Shu, Yilin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9322459/
https://www.ncbi.nlm.nih.gov/pubmed/35878217
http://dx.doi.org/10.3390/toxins14070479
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author Jiang, Huiling
He, Jun
Wang, Hui
Zheng, Lingling
Wang, Xiaoran
Zhang, Huijuan
Wu, Hailong
Shu, Yilin
author_facet Jiang, Huiling
He, Jun
Wang, Hui
Zheng, Lingling
Wang, Xiaoran
Zhang, Huijuan
Wu, Hailong
Shu, Yilin
author_sort Jiang, Huiling
collection PubMed
description 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.
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spelling pubmed-93224592022-07-27 Gill Junction Injury and Microbial Disorders Induced by Microcystin-Leucine Arginine in Lithobates catesbeianus Tadpoles Jiang, Huiling He, Jun Wang, Hui Zheng, Lingling Wang, Xiaoran Zhang, Huijuan Wu, Hailong Shu, Yilin Toxins (Basel) Article 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. MDPI 2022-07-13 /pmc/articles/PMC9322459/ /pubmed/35878217 http://dx.doi.org/10.3390/toxins14070479 Text en © 2022 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Jiang, Huiling
He, Jun
Wang, Hui
Zheng, Lingling
Wang, Xiaoran
Zhang, Huijuan
Wu, Hailong
Shu, Yilin
Gill Junction Injury and Microbial Disorders Induced by Microcystin-Leucine Arginine in Lithobates catesbeianus Tadpoles
title Gill Junction Injury and Microbial Disorders Induced by Microcystin-Leucine Arginine in Lithobates catesbeianus Tadpoles
title_full Gill Junction Injury and Microbial Disorders Induced by Microcystin-Leucine Arginine in Lithobates catesbeianus Tadpoles
title_fullStr Gill Junction Injury and Microbial Disorders Induced by Microcystin-Leucine Arginine in Lithobates catesbeianus Tadpoles
title_full_unstemmed Gill Junction Injury and Microbial Disorders Induced by Microcystin-Leucine Arginine in Lithobates catesbeianus Tadpoles
title_short Gill Junction Injury and Microbial Disorders Induced by Microcystin-Leucine Arginine in Lithobates catesbeianus Tadpoles
title_sort gill junction injury and microbial disorders induced by microcystin-leucine arginine in lithobates catesbeianus tadpoles
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9322459/
https://www.ncbi.nlm.nih.gov/pubmed/35878217
http://dx.doi.org/10.3390/toxins14070479
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